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The potential of using blood circular RNA as liquid biopsy biomarker for human diseases

Guoxia Wen, Tong Zhou, Wanjun Gu

Protein & Cell · 2020 · Review · CC BY

Abstract

Circular RNA (circRNA) is a novel class of single-stranded RNAs with a closed loop structure. The majority of circRNAs are formed by a back-splicing process in pre-mRNA splicing. Their expression is dynamically regulated and shows spatiotemporal patterns among cell types, tissues and developmental stages. CircRNAs have important biological functions in many physiological processes, and their aberrant expression is implicated in many human diseases. Due to their high stability, circRNAs are becoming promising biomarkers in many human diseases, such as cardiovascular diseases, autoimmune diseases and human cancers. In this review, we focus on the translational potential of using human blood circRNAs as liquid biopsy biomarkers for human diseases. We highlight their abundant expression, essential biological functions and significant correlations to human diseases in various components of peripheral blood, including whole blood, blood cells and extracellular vesicles. In addition, we summarize the current knowledge of blood circRNA biomarkers for disease diagnosis or prognosis.

Full text

From PubMed Central, U.S. National Library of Medicine, as current on Oct 23, 2026. Paragraph numbers are ours, so an answer can point at one.

INTRODUCTION

1Liquid biopsy is a biopsy that uses body liquids as the sample source to diagnose, predict the outcome of or monitor the development of human diseases (Rubis et al.,; Luo et al., ). Compared to traditional tissue biopsy, liquid biopsy has the advantages of being noninvasive, performed in real-time and accurate (Rubis et al.,; Luo et al., ). It has been proven to be applicable to the management of many human diseases, including cancers (Heitzer et al.,; Mattox et al.,; Rubis et al., ), prenatal genetic disorders (Zhang et al., ), heart diseases (Zemmour et al., ), schizophrenia (Chen et al., ), transplant rejection (Bloom et al., ) and infectious diseases (Burnham et al.,; Hong et al.,; Blauwkamp et al.,; Han et al., ). To date, most liquid biopsy studies have focused on its clinical application in human cancers (reviewed in Siravegna et al.,; Heitzer et al.,; Mattox et al.,; Rubis et al., ). For example, a cell-free DNA (cfDNA)-based liquid biopsy test that determines the mutational status of the epidermal growth factor receptor (EGFR) gene was used to guide the response of EGFR tyrosine kinase inhibitors in non-small cell lung cancer (NSCLC) patients, which was approved by the FDA in clinical practice (Kwapisz, ). Another FDA-approved liquid biopsy test, Epi proColon, assessed the methylation status of the Septin9 gene in whole blood, which was used to screen colorectal cancer patients from healthy controls (Lamb and Dhillon, ). In addition to cfDNA (Wan et al.,; Cescon et al., ), several other analytes within circulating body fluids were investigated as liquid biopsy biomarkers, such as circulating tumor cells (CTCs) (Yu et al., ), extracellular vesicles (EVs) (Torrano et al., ), cell-free RNA (cfRNA) (Zaporozhchenko et al., ), circulating proteins (Surinova et al., ), circulating metabolites (Crutchfield et al., ) and platelets (Joosse and Pantel,; Best et al., ). Among them, RNA-based liquid biopsy biomarkers have gained much more attention in recent years since they have dynamic expressions and are closely related to different disease conditions (Zaporozhchenko et al.,; Sole et al., ). Circulating noncoding RNAs, especially microRNAs (miRNAs), have shown promising potential as stable blood-based biomarkers in liquid biopsy (Mitchell et al.,; Anfossi et al.,; Pardini et al., ).

2Circular RNAs (circRNAs) are a group of endogenous noncoding RNA molecules (Chen,,; Li et al., ). They were first found in plant viroids (Sanger et al., ) and eukaryotic cells (Hsu and Coca-Prados, ) in 1970s, and were recently observed to be functional (Hansen et al.,; Memczak et al., ). They are joined head to tail to generate a covalently closed loop structure through back-splicing (Vicens and Westhof,; Li et al., ). They lack a 5-prime cap and 3-prime poly-A tail, which is quite different from canonical linear RNAs (Vicens and Westhof,; Li et al., ). CircRNAs have been identified in almost all organisms across the eukaryotic tree of life (Wang et al., ). Some circRNAs are the predominant transcript isoform of their host genes expressed in specific tissues or cell types (Salzman et al.,,; Rybak-Wolf et al., ). Furthermore, they are expressed in a tissue- (Zhou et al., ), cell-type- (Salzman et al., ) and developmental stage-specific manner (Zhou et al., ). Accumulating studies have revealed many regulatory roles and versatile cellular functions that circRNAs can perform (Li et al.,; Chen, ). They can act as miRNA decoys (Hansen et al., ), RNA binding protein (RBP) sponges (Ashwal-Fluss et al.,; Huang et al., ) and protein scaffolds (Li et al.,, ). Moreover, a small percentage of circRNAs can be translated into proteins (Legnini et al.,; Pamudurti et al.,; Heesch et al., ). Aberrant expression of circRNAs has been related to many human diseases, including cancers (Shang et al.,; Vo et al., ), neurodegenerative diseases, cardiovascular diseases (Aufiero et al., ) and immune diseases (Chen et al.,; Zhou et al., ). Due to their high stability (Enuka et al., ), abundant expression (Jeck et al., ) and high specificity (Zhou et al., ), circRNAs are becoming promising biomarkers for human diseases (Zhang et al., ).

3Due to the importance of liquid biopsy biomarkers in precision medicine (Vargas and Harris, ) and the superior characteristics of circRNAs as disease biomarkers (Zhang et al., ), recent studies have put great efforts into researching the use of circRNAs as liquid biopsy biomarkers for human diseases. Here, we review current progress that has been made on this topic. We focus on circRNAs in the peripheral blood, although circRNAs are abundantly expressed in other body fluids, such as saliva (Bahn et al.,; Ghods, ) and urine (Kölling et al.,; Lam and Lo,; Vo et al., ). In this review, we first briefly introduce the biogenesis, function, and expression patterns of circRNAs and their close correlations to human diseases. Then, we emphasize the functional roles they may play in different blood components, including blood cells, serum, plasma, platelets and EVs in the blood. We summarize peripheral blood circRNA biomarkers that have been constructed for the management of human diseases. Finally, we discuss future opportunities and challenges of translating blood circRNAs into clinical practice.

THE BIOGENESIS OF CIRCRNAS

4CircRNAs are derived from pre-mRNAs and formed by back-splicing, in which a downstream 5-prime splice site (ss) is covalently joined with an upstream 3-prime ss (Fig. 1) (Li et al., ). There are three major types of circRNAs, exonic circRNAs (ecircRNAs), exon-intron circRNAs (EIcircRNAs) and circular intronic RNAs (ciRNAs) (Fig. 1). EcircRNAs only contain exons, and most ecircRNAs are located in the cytoplasm. Two models have been proposed to explain the production of ecircRNAs (Fig. 1A) (Chen,; Wu et al.,; Kristensen et al.,; Xiao et al., ). The first model suggests that when the pre-mRNA is partially folded during transcription, canonical splicing will cause an “exon jump” and generate a linear RNA containing skipped exons (Starke et al.,; Kelly et al., ). A subsequent back-splicing event will turn the ‘lariat intermediate’ into a closed circular transcript (Barrett et al.,; Li et al., ). The second model proposes that when the 5-prime ss is pulled closer to the 3-prime ss by base pairing of flanking intronic complementary sequences (Ivanov et al.,; Vicens and Westhof,; Zhang et al.,; Wilusz, ) or specific bindings of intronic sequences to RBPs (Conn et al., ), a back-splicing event may occur, and a circRNA may be generated (Jeck et al., ). These models are supported by accumulating evidence showing that cis-acting elements (Jeck et al.,; Zhang et al.,; Yoshimoto et al., ) and trans-acting factors (Ashwal-Fluss et al.,; Conn et al.,; Agirre et al., ) play crucial regulatory roles in circRNA formation. EIcircRNAs are generated when an intron or several introns are alternatively retained in splicing (Li et al., ). Therefore, EIcircRNAs are mainly considered intermediates of ecircRNAs (Li et al., ). CiRNAs, which only contain introns, are produced through escape from debranching of intron lariats (Zhang et al., ). This process depends on a GU-rich motif near the 5-prime ss and a C-rich motif close to the branch-point site (Zhang et al., ). Unlike ecircRNAs, EIcircRNAs and ciRNAs are mainly located in the nucleus.

THE FUNCTION OF CIRCRNAS

5With the rapid application of high-throughput RNA-sequencing (RNA-seq) technology (Stark et al., ) and related bioinformatics tools that identify circRNAs from RNA-seq datasets (Jeck and Sharpless,; Szabo and Salzman,; Li et al.,; Gao and Zhao, ), more than one million circRNAs have been annotated in model organisms (Glažar et al.,; Vo et al.,; Cai et al.,; Wu et al., ). However, the functional characterization of circRNAs is still at its early stage (Chen,,; Li et al., ). Their circular conformation and the large sequence overlap with their linear mRNA counterparts have posed substantial challenges in investigating the functions of circRNAs (Li et al., ). Based on our current knowledge, circRNAs have diverse functions as miRNA decoys, protein regulators and translation templates (Fig. 1B, see (Chen,,; Li et al., ) for excellent reviews).

MiRNA decoys

6The most well-known function of circRNAs is that they can act as a sponge to inhibit the function of miRNAs and indirectly regulate the expression of miRNA target genes at the posttranscriptional level (Fig. 1B) (Hansen et al.,; Memczak et al.,; Weng et al., ). For example, Cdr1as can compete with mRNAs by binding miR-7 through miRNA response elements (MREs) (Hansen et al., ). A follow-up in vivo experiment that knocked down the Cdr1as locus in the mouse genome confirmed the importance of the Cdr1as and miR-7 interaction in normal brain function (Piwecka et al., ). Although it may not be a common phenomenon for most circRNAs (Guo et al., ), several abundant circRNAs also function as miRNA sponges, including circASAP1 (Hu et al., ), circBIRC6 (Yu et al., ), circHIPK2 (Huang et al., ), circHIPK3 (Zheng et al., ) and circSry (Hansen et al., ).

Protein regulators

7In addition to miRNAs, circRNAs can interact with proteins or protein complexes to regulate protein expression and function (Fig. 1B) (Huang et al., ). First, circRNAs can bind to some RBPs and act as RBP sponges. CircMbl, a circRNA originating from the second exon of the splicing factor muscleblind (MBL), is the first circRNA that was discovered to function as an RBP sponge (Ashwal-Fluss et al., ). It was observed that both the circular exon and the flanking introns of circMbl contain many MBL binding sites that can be specifically bound by MBL (Ashwal-Fluss et al., ). Therefore, increased expression of MBL can promote back-splicing of circMbl and lead to decreased expression of canonical linear MBL transcripts. At the same time, circMbl can sequester MBL in the cytoplasm and prevent it from performing splicing functions (Ashwal-Fluss et al., ). Several other circRNAs, such as circAmotl1 (Yang et al., ), circANRIL (Holdt et al., ), circPABPN1 (Abdelmohsen et al., ), circPOLR2A (Li et al., ) and circDHX34 (Li et al., ), can function as protein decoys as well. Second, circRNAs can form a complex with other RNAs and proteins to perform functions. For example, some intron-containing circRNAs, such as circEIF3J and circBPTF, can interact with U1 snRNP to form an RNA-protein complex, which further interacts with RNA polymerase II (Pol II) at the promoter region of their parental genes and enhances their transcription (Zhang et al.,; Li et al., ). Similarly, some ciRNAs, such as ci-ankrd52, can also associate with Pol II as well (Zhang et al.,; Li et al., ). They can also regulate the expression of their parental gene by modulating the elongation of Pol II (Zhang et al.,; Li et al., ). Many circRNAs, rather than a specific circRNA, can interact with NF90/NF110 as a group to form circRNP complexes in the cytoplasm, which may function as a reservoir of NF90/NF110 (Li et al., ). Upon viral invasion, NF90/NF110 could be released from circRNP complexes and bind to viral mRNAs to perform its antiviral functions (Li et al., ). Third, the interaction of circRNAs with proteins can facilitate or block the function of their binding proteins. For instance, increased expression of circFoxo3 in the cytoplasm may arrest the anti-senescent protein ID1, transcription factor E2F1, anti-stress proteins FAK and HIF1α and prevent the nuclear translocation of these transcription factors and their function, thus leading to increased cellular senescence (Du et al., ). CircFoxo3 can also form a tertiary circRNA-protein complex with cyclin-dependent kinase 2 (CDK2) and cyclin-dependent kinase inhibitor 1 (p21), which facilitates the inhibition of CDK2 by p21, thus blocking cell cycle progression (Du et al., ). Moreover, circFoxo3 can bind to Mdm2 and p53 in a breast cancer cell line, which leads to tumor cell apoptosis (Du et al., ).

Translation

8Some circRNAs with an internal ribosome entry site (IRES), such as circMbl (Pamudurti et al., ) and circZNF609 (Legnini et al., ), can share the start codon of their host genes and be translated in a cap-independent manner. The translation initiation of circRNAs may be promoted by N6-methyladenosine (m6A) modification of circRNAs (Yang et al., ). In the human heart, 40 circRNAs were observed to be associated with ribosomes and thus may be translated (Heesch et al., ). Some of them, including circSLC8A1, circMYBPC3 and circRYR2, are heart-specific circRNAs (Heesch et al., ). The translation of these circRNAs may be related to the physiological roles of the human heart. Further functional analysis observed that some circRNA-encoded proteins can exert agonist or antagonist effects on cancer progression. For example, PINT87aa (Zhang et al., ) and AKT3-A74aa (Xia et al., ), two peptides encoded by circRNAs, can interact with signal factors and inhibit glioblastoma tumorigenicity in glioblastoma. However, circGprc5a-secreted peptides can promote bladder oncogenesis and metastasis through its binding to Gprc5a (Gu et al., ).

CIRCRNA EXPRESSION AND ITS IMPLICATION IN DISEASES

9Given the important functions that circRNAs can perform, their expression may provide significant clues in understanding the underlying mechanisms of biological processes and disease states. Previous studies have observed that circRNAs are widely expressed in all tissues (Zhou et al.,; Ji et al.,; Wu et al., ) and cell types (Salzman et al., ) of nearly all species across the eukaryotic tree of life (Wang et al., ). Specifically, circRNAs are enriched in brain samples (Westholm et al.,; Rybak-Wolf et al.,; Szabo et al.,; Venø et al., ) and human blood samples (Memczak et al., ), including peripheral blood mononuclear cells (PBMCs) (Qian et al., ), erythrocytes (Alhasan et al., ), platelets (Alhasan et al., ) and exosomes (Li et al., ). Furthermore, circRNAs are expressed in tissue- (Guo et al.,; Szabo et al.,; Zhou et al., ) or cell-type- (Salzman et al., ) specific and age-dependent manner (Rybak-Wolf et al.,; Szabo et al.,; You et al.,; Zhou et al., ). Using the rat BodyMap dataset, we observed tissue-specific circRNA expression in all 11 rat tissues, which may be closely related to the physiological functions of those tissues (Zhou et al., ). The dynamic expression of circRNAs across time has also been correlated with neuronal differentiation (Rybak-Wolf et al., ), neural development (Szabo et al.,; You et al., ), human terminal B cell differentiation (Agirre et al., ) and spermatogenesis (Zhou et al., ).

10The spatiotemporal expression of circRNAs is mediated by the balance between circRNA generation and circRNA turnover, which can be regulated at both the transcriptional and posttranscriptional levels (Li et al.,; Chen, ). On the one hand, the production of circRNAs can be regulated by intronic complement sequences (ICSs) (Jeck et al.,; Liang and Wilusz,; Zhang et al., ), cis-splicing elements (Ashwal-Fluss et al.,; Starke et al.,; Wang and Wang, ) and trans-acting splicing factors (Ashwal-Fluss et al.,; Conn et al.,; Kramer et al.,; Khan et al.,; Aktaş et al.,; Errichelli et al.,; Fei et al.,; Li et al., ). On the other hand, the degradation of circRNAs can be affiliated by miRNA-initiated AGO2 cleavage (Kleaveland et al., ) and nuclease-mediated cleavage, including RNase L endonuclease (Liu et al., ), RNase P/MRP endonuclease complex (Park et al., ) and G3BP1 endonuclease (Fischer et al., ). Dysregulation of circRNA generation or turnover may lead to aberrant circRNA expression in cells or tissues, which may be related to many human diseases (Chen et al., ). Cdr1as, one of the most studied circRNAs, harbors more than 70 binding sites for miR-7, and its overexpression strongly inhibits the activity of the tumor suppressor miR-7 (Hansen et al., ). Accumulating evidence has demonstrated its significant increase in colorectal cancer samples, which can inhibit miR-7 function and activate EGFR and RAF1 oncogenes (Weng et al., ). Moreover, the dysregulation of the miR-7/Cdr1as axis is involved in some other diseases, such as Alzheimer’s diseases (Lukiw, ), diabetes (Xu et al., ) and cardiometabolic diseases (Geng et al., ). Furthermore, the loss of the Cdr1as locus causes miRNA deregulation and affects synaptic transmission in knockout mice (Piwecka et al., ). In addition to Cdr1as, other circRNAs are also implicated in many different human diseases, including cancers (Zhang et al.,; Chen et al.,; Smid et al.,; Su et al.,; Vo et al., ), cardiovascular diseases (Zhang et al.,; Aufiero et al., ), neurodevelopment and neurodegenerative diseases (Kumar et al.,; Zhang et al.,; Dube et al.,; Chen et al.,; Hanan et al., ) and immune diseases (Chen et al.,; Zhou et al., ).

CIRCRNAS ARE PROMISING BIOMARKERS FOR HUMAN DISEASES

11In general, biomarkers are physiological indexes or biological molecules that can be objectively measured and can indicate either a normal or a pathogenic state (Lesko and Atkinson, ). Technological advances in genomics, transcriptomics, proteomics and metabolomics have led to the discovery and validation of many biomarkers that are pushing personalized medicine forward (Chen et al.,; Karczewski and Snyder,; Ahadi et al., ). A good biomarker with clinical significance must meet the criteria of analytical validity, clinical validity and clinical utility (Byron et al., ). As a novel type of noncoding RNA, circRNA has several distinct advantages over canonical linear RNAs as a disease biomarker (Zhang et al., ). First, circRNA is more stable than linear RNAs because it has a closed loop structure without 5-prime and 3-prime ends (Enuka et al.,; Li et al., ). In the MCF10A human mammary epithelial cell line, Enuka et al. observed at least 2.5 times longer half-lives of circRNAs compared to linear RNAs, including mRNAs and miRNAs (Enuka et al., ). Second, circRNAs are abundantly expressed in many tissue samples. For example, brain samples express more than 10,000 circRNAs in the rat BodyMap dataset (Zhou et al., ). In some cases, the expression values of circRNAs are much higher than their linear counterparts (Westholm et al.,; Rybak-Wolf et al.,; You et al.,; Liang et al., ). Third, circRNAs are expressed in a tissue-specific (Salzman et al.,; Guo et al.,; Szabo et al.,; Zhou et al., ) and developmental stage-specific manner (Rybak-Wolf et al.,; Szabo et al.,; You et al.,; Zhou et al., ). Importantly, the tissue specificity of circRNA is higher than that of mRNA of its host gene (Guo et al.,; Zhou et al., ). These features suggest that circRNAs may have better analytical validity (Zhang et al., ), including analytical specificity, robustness, reproducibility and repeatability (Byron et al., ), when used as biomarker molecules. In a recent study, Maass et al. investigated circRNA expression in 20 clinically relevant tissue samples, which underscored the feasibility of using circRNAs as potential disease biomarkers (Maass et al., ).

12To date, many circRNAs have been identified as biomarkers for human diseases (Zhang et al., ), especially human cancers (Li et al.,; Meng et al.,; Su et al.,; Sheng et al., ). For example, Cdr1as has been revealed as a prognostic biomarker in colorectal cancer patients (Weng et al., ). In a training cohort comprising 153 primary colorectal cancer tissues and 44 matched normal mucosae, significantly increased Cdr1as expression was observed in colorectal cancer tissues, and its overexpression was associated with poor patient survival. The prognostic power of Cdr1as was further validated in an independent validation cohort comprising 165 colorectal cancer patients (Weng et al., ). A four-circRNA signature, consisting of hsa_circ_101308, hsa_circ_104423, hsa_circ_104916 and hsa_circ_100269, has been constructed that can predict the early recurrence of stage III gastric cancer (GC) patients after surgery (Zhang et al., ). Moreover, Vo et al. constructed a comprehensive catalog of circRNAs in human cancer tissues in a systematic analysis of more than 2,000 cancer samples (Vo et al., ). They identified two circRNAs, circ-AURKA and circ-AMACR, as potential diagnostic biomarkers for neuroendocrine prostate cancer (Vo et al., ). Although these circRNA biomarkers are potentially useful in cancer management, most of them are derived from tissue samples (Li et al.,; Meng et al.,; Su et al.,; Sheng et al., ). To improve biomarker accessibility, especially for biomarkers of cancer screening and diagnosis, circRNA biomarkers in body fluids are ideal for clinical application (Anfossi et al., ). Hence, the authors further investigated and validated the reliability of detecting circRNA biomarkers in urine samples of prostate cancer patients (Vo et al., ), which suggests that circRNA in urine samples is a promising strategy for prostate cancer screening.

BLOOD CIRCRNAS AND LIQUID BIPOSY BIOMARKERS

13Liquid biopsy has been a revolutionary tool in disease management, supporting the diagnosis, prognosis and treatment guidance of human diseases (Heitzer et al.,; Mattox et al.,; Rubis et al.,; Luo et al., ). In comparison to urine, saliva or cerebrospinal fluid, peripheral blood has been used as the major body fluid in liquid biopsy (Rubis et al.,; Luo et al., ). In the circulating blood, aberrantly expressed RNAs or fusion transcripts in different blood components have been associated with human cancers (Byron et al.,; Zaporozhchenko et al.,; Sole et al., ) and infectious diseases (Byron et al.,; Correia et al., ). These RNA biomarkers include cfRNAs in plasma or serum (Mitchell et al.,; Fehlmann et al., ), exosome-derived RNAs (Maas et al., ), EV-incorporated cfRNAs (Maas et al., ) and RNA transcripts in tumor-educated platelets (Best et al.,, ). These cell-free or EV-incorporated RNA biomarkers represent the changes in expression that occur in abnormal cells, such as dysregulated genes in cancer cells (Byron et al.,; Rubis et al.,; Luo et al., ). Other than cfRNAs, gene expression profiles of PBMCs or whole blood have been proven to be good indicators of many human diseases (Chaussabel and Baldwin,; Chaussabel, ), since they can assess the immune status (Chaussabel, ). Unlike the expression of cfRNAs in serum, plasma or EVs, RNA expression levels in PBMCs or whole blood are measures of the host response to exogenous pathogens or autoantigens (Schnell et al.,; Shaked, ). Several whole blood or PBMC gene expression signatures have been developed for cancer management, including the early diagnosis of colorectal cancer (Marshall et al.,; Ciarloni et al.,, ) and lung cancer (Showe et al.,; Kossenkov et al., ), the prognosis of adult acute myeloid leukemia (Bullinger et al.,; Valk et al., ) and prostate cancer patients (Ross et al., ), and the monitoring of renal cell carcinoma relapse (Giraldo et al., ). Moreover, whole blood or PBMC RNA signatures have been widely investigated as liquid biopsy diagnostic tools for infectious diseases (Ramilo and Mejias, ), such as discriminating influenza from other respiratory viral infections (Zaas et al., ), differentiating viral and bacterial infections (Tsalik et al., ), diagnosing septic patients (Sweeney et al.,; Gunsolus et al.,; Mayhew et al., ), and discriminating active tuberculosis (TB) patients from patients with latent TB or other lung diseases (Bloom et al.,; Anderson et al.,; Qian et al.,; Zak et al.,; Sambarey et al.,; MacLean et al.,; Warsinske et al.,; Esmail et al.,; Gupta et al., ). In addition, the transcriptome of blood cells has been implicated in assessing the likelihood of developing obstructive coronary artery disease in symptomatic nondiabetic patients (Vargas et al., ) and predicting antibody-mediated kidney allograft rejection in kidney transplant patients (Loon et al., ).

14With regard to RNA molecules, both protein-coding mRNAs (Byron et al.,; Sole et al., ) and several classes of noncoding RNAs (Byron et al.,; Anfossi et al.,; Pardini et al.,; Sole et al., ) have been used as blood disease biomarkers. In comparison to mRNAs or long noncoding RNAs, small noncoding RNAs, such as miRNAs (Mitchell et al.,; Max et al.,; Fehlmann et al., ) and noncanonical small RNAs (Fritz et al.,; Pardini et al., ), have the advantage of high stability in the circulating blood (Mitchell et al.,; Anfossi et al., ). This superiority is especially important when translating RNA biomarkers into clinical practice (Byron et al.,; Anfossi et al., ), since fast mRNA degradation in blood sample processing may affect the performance of mRNA biomarkers (Dvinge et al., ). Given the high stability of circRNAs, great efforts and substantial progress have been made to investigate the possibility of using circRNA biomarkers in liquid biopsy in recent years.

15Next, we summarize circRNAs in the peripheral blood, their correlations with human diseases and their potential application in liquid biopsy as disease biomarkers (Fig. 2). We classified blood circRNAs into blood cell-free circRNAs and circRNAs in blood cells since they have distinct biological meanings in the context of human diseases. Blood cell-free circRNAs, including circulating cell-free circRNAs in plasma, serum and blood EVs, are secreted from different tissue cells into the blood. Therefore, cell-free circRNAs have corresponding tissue origins, and cell-free circRNA biomarkers represent their clinical significance in the original tissue (Li et al.,, ). On the other hand, blood cell circRNAs consist of circRNAs in various blood cells, such as monocytes, erythrocytes, neutrophils and platelets. CircRNAs in mixtures of different blood cells, such as circRNAs in lymphocytes, PBMCs and whole blood, are classified in this group as well. The circRNA expression profiles of peripheral blood cells or a mixture of blood cells are important indicators of the host’s immune status (Chaussabel, ), which may undergo dynamic changes during acute events such as viral infections (Chen et al.,; Rose et al.,; Zhou et al., ). Hence, circRNA biomarkers in blood cells, PBMCs or whole blood represent the specific immune response of an individual to different physiological aspects.

Cell-free circRNAs in peripheral blood

16Mounting evidence has demonstrated abundant circRNA expression in blood plasma (Maass et al.,; Yi et al.,; Smid et al., ) and serum (Gu et al.,; Maass et al.,; Sonnenschein et al.,; Sun et al., ) (Fig. 2A). In the circulating blood, EVs, including exosomes and microvesicles, are important blood components that have great diagnostic and prognostic value (Revenfeld et al., ). Li et al. investigated circRNA expression in MHCC-LM3 liver cancer cells and cell-derived exosomes and found at least 2-fold circRNA enrichment in exosomes compared to producer cells (Li et al., ). They further found that the expression level of exosomal circRNAs is largely the same after serum incubation at room temperature for up to 24 h (Li et al., ). Using the extracellular vesicle long RNA (exLR) sequencing method, the same group explored the expression profiles of circRNAs in 352 plasma EV samples (Li et al., ). They found 137,196 circRNA candidates that were expressed in normal plasma EV samples, and the circular to linear ratio was significantly higher in EVs than in PBMCs (Li et al., ). A recent study also isolated platelet-derived EVs and demonstrated the selective release of platelet-specific circRNAs in exosomes and microvesicles (Preußer et al., ). Based on these data, a database of blood exosomal circRNAs, exoRBase, has been developed to facilitate the development of circRNA signatures in blood exosomes (Li et al., ). In addition, two previous studies have observed that the majority of circulating cell-free miRNAs were associated with AGO2 protein complexes rather than with vesicles in blood plasma (Arroyo et al.,; Turchinovich et al., ). Like cell-free miRNAs, blood cell-free circRNAs may bind to several RNA-binding proteins or protein complexes as well (Huang et al., ). Therefore, some cell-free circRNAs may not be associated with blood EVs. In a pilot study of circRNA expression profiles in 348 primary breast cancer tissue samples, Smid et al. found that circCNOT2 is a prognostic biomarker of aromatase inhibitor therapy in advanced breast cancer patients (Smid et al., ). To investigate the possibility of using circCNOT2 as a noninvasive biomarker, they further amplified circCNOT2 in plasma samples of four breast cancer patients and found variable circCNOT2 expression in all plasma samples (Smid et al., ). All these results suggest that cell-free circRNAs in peripheral blood are stable, enriched and detectable.

17Blood EVs can be secreted from cells of many different biological systems and can be circulated to recipient cells through the bloodstream (Revenfeld et al.,; Lasda and Parker, ). Therefore, blood cell-free circRNAs can perform vital roles in many biological processes, such as cancer cell proliferation, cancer metastasis, drug resistance, hemostasis and inflammation (Fig. 2B) (Wang et al.,; Cui et al.,; Li et al.,; Shang et al.,; Xu et al., ). For example, circ-deubiquitination (circ-DB) in adipose-secreted exosomes was found to regulate deubiquitination via the suppression of miR-34a and the activation of deubiquitination-related USP7 in plasma samples of hepatocellular carcinoma (HCC) patients, which could reduce DNA damage and promote HCC cell growth (Zhang et al., ). Exosomal circSHKBP1 was found to promote the progression of GC by regulating the miR-582-3p/HUR/VEGF pathway and suppressing HSP90 degradation (Xie et al., ). CircUHRF1 in plasma exosomes can inhibit the functions of natural killer cells by upregulating the expression of TIM-3 via miR-449c-5p degradation and drive resistance to anti-PD1 immunotherapy in HCC patients (Zhang et al., ). Moreover, exosomal circHIPK3 can prevent ischemic muscle injury by downregulating miR-421 expression, increasing FOXO3a expression, inhibiting pyroptosis and releasing IL-1β and IL-18 (Yan et al., ).

18Given the biological functions that blood cell-free circRNAs can perform (Wang et al.,; Cui et al.,; Li et al., ) and their implications in many human diseases, cell-free circRNAs in the peripheral blood have great potential as liquid biopsy biomarkers of human diseases (Fig. 2C) (Anfossi et al.,; Zaporozhchenko et al.,; Zhang et al., ). To date, many blood cell-free circRNAs have been introduced for cancer management, including early cancer diagnosis, cancer prognosis and prediction of cancer treatment (Preußer et al.,; Aufiero et al.,; Fraipont et al.,; Lu et al.,; Pardini et al.,; Sole et al.,; Su et al.,; Wang et al.,; Beltrán-García et al.,; Cui et al.,; Li et al., ). In a recent study, Luo et al. measured the expression levels of two circRNAs in plasma samples of 231 lung cancer patients and 41 healthy controls using reverse transcription droplet digital PCR (RT-ddPCR) (Luo et al., ). They identified hsa_circ_0000190 as a circRNA biomarker in human blood plasma that can predict the survival outcomes of lung cancer patients (Luo et al., ). Furthermore, the increased expression of plasma hsa_circ_0000190 was also correlated with poor response to systemic therapy and immunotherapy in lung cancer patients (Luo et al., ). Similarly, Li et al. investigated the clinical relevance of serum exosomal circFLI1 in lung cancer patients in a cohort of 61 small cell lung cancer (SCLC) patients and 55 normal subjects. They found that serum exosomal circFLI1 levels were significantly higher in SCLC patients, especially in SCLC patients with distant metastasis (Li et al., ). Notably, they observed that SCLC patients with lower exosomal circFLI1 expression levels experienced longer disease remissions, indicating its prognostic power in SCLC. The authors also suggested that serum exosomal circFLI1 may be used as a biomarker that can monitor the clinical response to chemotherapy in SCLC patients (Li et al., ). By analyzing blood plasma samples of 62 GC patients and 25 healthy controls, Tang et al. proposed a novel circulating diagnostic biomarker of GC, plasma exosomal circKIAA124, that was correlated with clinical TNM stage, lymphatic metastasis and overall survival time of GC patients (Tang et al., ). In addition to the aberrant expression of blood cell-free circRNAs, the presence of some fusion circRNAs (f-circRNAs) in the peripheral blood has also been used as a liquid biopsy biomarker. Guarnerio et al. found that f-circRNAs could be produced from cancer-associated chromosomal translocations in cancer cells (Fig. 1), and f-circRNAs could promote cellular transformation, cell viability and resistance upon therapy (Guarnerio et al., ). In a systematic analysis of f-circRNAs in localized prostate cancer tissues, Chen et al. observed more f-circRNAs in tumors with worse prognosis (Chen et al., ). Due to the lack of recurrence of these f-circRNAs, the authors suggested that f-circRNAs are good biomarker candidates (Chen et al., ). In NSCLC patients, Tan et al. found that F-circEA, an f-circRNA originating from the EML4-ALK fusion gene, was exclusively expressed in the plasma of patients with the EML4-ALK fusion (Tan et al., ). Therefore, plasma F-circEA may serve as a liquid biopsy biomarker to diagnose NSCLC patients with EML4-ALK translocation and guide targeted therapy for NSCLC patients in this subgroup (Tan et al., ). More cell-free circRNA biomarkers in the blood are summarized in Table 1.

CircRNAs in blood cells and whole blood

19CircRNA expression in blood cells and whole blood, a major source of liquid biopsy samples, has been extensively investigated (Fig. 2A). In a pilot study, Memczak et al. detected thousands of circRNAs in peripheral whole blood samples using RNA-seq (Memczak et al., ). They found that the expression levels of these blood circRNAs were comparable to those in circRNA-rich cerebellar tissue (Memczak et al., ). In separate blood cell populations, circRNAs were observed to be enriched approximately 100-fold in platelets and anucleate erythrocytes relative to nucleated tissues, such as lung, brain and colon (Alhasan et al., ). Gaffo et al. investigated circRNA expression in T cells, B cells and monocytes of healthy subjects and found abundant circRNA expression in these mature blood cells (Gaffo et al., ). We also explored the expression landscape of circRNAs in PBMCs and found that the expression level of circRNAs in PBMCs, together with that in platelets, red blood cells (RBCs) and whole blood, is high enough to be detected (Qian et al., ). All these results suggest that whole blood (Memczak et al.,; Qian et al., ), PBMCs (Qian et al., ), and several blood cells, including neutrophils (Maass et al., ), T cells (Gaffo et al., ), B cells (Gaffo et al., ), monocytes (Gaffo et al., ), RBCs (Alhasan et al.,; Qian et al., ) and platelets (Maass et al.,; Qian et al.,; Gaffo et al., ), are reliable clinical samples for circRNA profiling in liquid biopsy.

20Accumulating evidence has suggested that circRNAs play crucial roles in the immune response and its regulation (Fig. 3) (Chen et al.,,; Xu et al.,,; Yang et al.,; Zhou et al.,; Awan et al., ). First, circRNAs are important regulators of blood cell biogenesis, differentiation and activation (Chen et al.,; Zhou et al.,; Xu et al., ). In a comprehensive study of circRNA expression in hematopoietic progenitors, differentiated lymphoid and myeloid cells, Nicolet et al. observed a cell-type specific pattern of circRNA expression profiles in blood cells, and the type and number of circRNAs increased upon hematopoietic maturation (Nicolet et al., ). Moreover, Holdt et al. found that circANRIL can bind to PES1 to impede the generation of pre-rRNA and ribosomes, resulting in the biogenesis of macrophages by p53 activation (Holdt et al., ). Second, circRNAs are actively involved in antiviral immune responses (Fig. 3B) (Cadena and Hur,; Awan et al., ). For example, Chen et al. showed that exogenous circRNAs released by viruses can be recognized by the pattern recognition receptor RIG-I of host cells, which activates host innate immunity (Chen et al., ). In their subsequent work, the authors showed that m6A RNA modification of human circRNAs inhibits innate immunity, while unmodified circRNAs and K63-polyubiquitin can activate RIG-I and innate immune response (Chen et al., ). Li et al. found that two immune factors, NF90/NF110, not only promote circRNA production in the nucleus but also bind to mature host circRNAs to form circRNP complexes in the cytoplasm. Upon viral infection, circRNP complexes in the cytoplasm can release NF90/NF110, which binds viral mRNAs to inhibit viral replication (Li et al., ). Moreover, Liu et al. presented that circRNAs can form RNA duplexes and act as inhibitors of innate immunity-related protein kinase (PKR) under normal conditions (Liu et al., ). Upon poly(I:C) treatment or viral infection, RNase L is activated to efficiently degrade circRNAs, and PKR is thus released from circRNA inhibition to initiate the early cellular innate immune response (Liu et al., ). Third, circRNAs are closely associated with the antibacterial immune response as well. Ng et al. characterized circRNAs induced by lipopolysaccharide (LPS) and identified circRasGEF1B as a conserved positive regulator of the LPS response (Ng et al., ). Their functional analysis revealed that circRasGEF1B can induce the expression of ICAM-1 in the TLR4/LPS pathway, which activates pathogen recognition and the inflammatory response upon microbial infection (Fig. 3A) (Ng et al., ).

21The important functions of circRNAs in blood cells suggest that the dysregulation of circRNA expression in blood cells is likely to contribute to the occurrence and progression of immune-related diseases, including autoimmune diseases, infectious diseases and cardiovascular diseases (Chen et al.,; Gaffo et al.,; Zhou et al.,; Xie et al.,; Xu et al., ). For instance, we determined that the expression level of PBMC circRNAs is higher in TB patients than healthy controls, and five immune-related pathways were upregulated upon Mycobacterium tuberculosis infection, including “cytokine-cytokine receptor interactions”, “chemokine signaling pathways”, and “neurotrophic signaling pathways” (Qian et al., ). Similarly, Huang et al. identified 13 upregulated and 24 downregulated circRNAs in PBMCs of TB patients (Huang et al., ). Among them, hsa_circRNA_001937 is likely to participate in the inflammatory response by targeting miR-26b and modulating the NF-κB pathway (Huang et al., ). In addition, Zhang et al. investigated the roles that circRNAs play in early human immunodeficiency virus (HIV) infection (EHI), especially in regulating HIV replication (Zhang et al., ). EHI represents a stage where viral replication increases to a peak level and intense antiviral immune response and immune injury occur (Powers et al.,; Richey and Halperin, ). The authors characterized the expression profiles of circRNAs, mRNAs and miRNAs in PBMCs of EHI patients and constructed a circRNA-associated competing endogenous network in EHI patients. They revealed 67 differentially expressed circRNAs, such as CCNK, CDKN1A and IL-15, that are potentially involved in HIV replication by regulating the expression of genes in the immune response, inflammatory response and defense response to the virus (Zhang et al., ). Regarding autoimmune diseases, Liu et al. detected a global reduction in circRNAs and activation of RNase L in PBMCs of systemic lupus erythematosus (SLE) patients (Liu et al., ). They further found that circPOLR2A overexpression can lead to reduced PKR activation, EIF2α phosphorylation and type I IFN-induced gene suppression. This highlights the link between circRNAs and innate immunity regulation and provides the potential for circRNA manipulation in SLE treatment (Liu et al., ). In addition to the above examples, the abnormal expression of blood circRNAs is related to several other diseases, such as the immune response to Ebola virus (Wang et al., ) and hepatitis C virus (Jost et al., ), rheumatoid arthritis (RA) (Yang et al., ), type 2 diabetes mellitus (T2DM) (Fang et al., ), heart failure (Han et al., ) and adenosine deaminase deficiency (Maass et al., ).

22With increasing knowledge of blood cell circRNAs and their function, many circRNAs in blood cells or whole blood have been proposed as liquid biopsy biomarkers for human diseases (Fig. 2C) (Aufiero et al.,; Beltrán-García et al.,; Kumar et al.,; Ravnik-Glavač and Glavač,; Sun et al., ). For instance, we developed a PBMC circRNA-based molecular signature that discriminates active TB patients from healthy controls in our previous study (Qian et al., ). The classification power of this PBMC circRNA signature was further validated in an independent cohort with an area under the receiver operating characteristic curve (AUC) of 0.946 (Qian et al., ). In another study, Huang et al. found that the expression of hsa_circ_001937 in PBMCs was significantly higher in TB patients than in pneumonia, chronic obstructive pulmonary disease (COPD) and lung cancer patients (Huang et al., ). In a cohort consisting of 115 TB, 40 pneumonia, 40 COPD, and 40 lung cancer patients and 90 healthy control subjects, hsa_circ_001937 had good discriminative power with an AUC of 0.873. After anti-TB treatment, the expression level of hsa_circ_001937 was significantly decreased compared to that of healthy controls. These results suggest that PBMC hsa_circ_001937 may be a TB diagnostic biomarker (Huang et al., ). Furthermore, Lei et al. found an upregulation of circ_0000798 expression in PBMCs of HCC patients, which was associated with poor overall survival (Lei et al., ). In a cohort of 72 HCC patients and 30 healthy control subjects, circ_0000798 expression could distinguish HCC patients from healthy controls with an AUC of up to 0.703. The authors suggested that PBMC circ_0000798 has potential as a blood biomarker for HCC diagnosis and prognosis (Lei et al., ). In addition, Li et al. measured circRNA expression changes between children with SLE and healthy children and investigated the significance of blood circRNAs in SLE diagnosis (Li et al., ). They identified and validated the diagnostic power of two circRNAs in whole blood, hsa_circ_0057762 and hsa_circ_0003090, that can differentiate children with SLE from healthy controls (Li et al., ). Zhao et al. also identified and validated hsa_circ_0054633 in peripheral whole blood as a sensitive and specific diagnostic biomarker for prediabetes and T2DM (Zhao et al., ). In addition to the above examples, the potential of using blood circRNAs as disease biomarkers has been explored for many other human diseases, such as coronary artery disease (Zhao et al.,; Wang et al.,; Liang et al., ), community‐acquired pneumonia (Zhao et al., ), and schizophrenia (Yao et al., ). A list of current proposed potential blood circRNA biomarkers is listed in Table 2.

CONCLUSIONS AND FUTURE PERSPECTIVES

23The high stability, abundance and spatiotemporal specific expression of blood circRNAs make them ideal biomarkers for liquid biopsy. In the past several years, many studies have shown that blood circRNAs, both cell-free blood circRNAs and circRNAs in blood cells, have great potential as biomarkers of many human diseases in liquid biopsy. A biomarker with broad clinical application must have demonstrated analytical validity, clinical validity and clinical utility (Byron et al., ). Therefore, several issues need to be considered and investigated before peripheral blood circRNA biomarkers can be translated into clinical practice. First, a blood circRNA-based gene test should prove its analytical validity within clinically relevant conditions. Although substantial advances have been made in the past several years (Szabo and Salzman,; Kristensen et al., ), the methods to discover and profile circRNAs are far from optimal. Future studies need to test the analytical performance of different circRNA profiling methods in clinical blood samples, such as RNA-seq, circRNA microarray, reverse transcription quantitative PCR (RT-qPCR) and RT-ddPCR (Kristensen et al., ). In estimating analytical sensitivity and specificity, reference standards that can be specifically applied in circRNA discovery and profiling are needed (Hardwick et al., ). Furthermore, the procedure to discover and validate blood circRNA biomarkers needs to be standardized, including blood collection and preservation, circRNA extraction, library construction, and computational analysis (Byron et al.,; Anfossi et al., ). With the use of a standardized procedure, future studies need to estimate the technical robustness and reproducibility of the proposed biomarkers within and between laboratories. Second, the blood circRNA biomarkers identified in current studies (Tables 1 and 2) are only preliminary biomarker signatures for human diseases. The designed experiments in most studies are case-control studies of samples with well-defined phenotypes, and the sample size is relatively small. To test their clinical validity, more clinical samples are required to validate their sensitivity and specificity in a larger cohort, especially their performance in discriminating patients with similar clinical phenotypes. Moreover, their performance in diagnosing the disease or predicting the disease outcome also needs to be tested in a prospective cohort in a clinical practice setting. Finally, further studies are needed to test and validate the usefulness of these biomarkers in clinical practice, such as their ability to inform clinical decisions and improve outcomes. Although many challenges and problems need to be solved, the promising potential of translating blood circRNA biomarkers into the clinic brings us new and inspiring options for liquid biopsy.

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49.
Conn SJ, Pillman KA, Toubia J, Conn VM, Salmanidis M, Phillips CA, Roslan S, Schreiber AW, Gregory PA, Goodall GJ. The RNA binding protein quaking regulates formation of circRNAs. Cell. 2015;160:1125-1134.
Not in our library10.1016/j.cell.2015.02.014
50.
Circulating microRNAs as Potential Biomarkers of Infectious Disease · 2017
No notice
51.
Advances in mass spectrometry-based clinical biomarker discovery · 2016
No notice
52.
Functions and mechanisms of circular RNAs in cancer radiotherapy and chemotherapy resistance · 2020
No notice
53.
de Fraipont F, Gazzeri S, Cho, WC, Eymin B. Circular RNAs and RNA splice variants as biomarkers for prognosis and therapeutic response in the liquid biopsies of lung cancer patients. Front Genet. 2019;10:390.
Not in our library10.3389/fgene.2019.00390
54.
Ding C, Yi X, Wu X, Bu X, Wang D, Wu Z, Zhang G, Gu J, Kang D. Exosome-mediated transfer of circRNA CircNFIX enhances temozolomide resistance in glioma. Cancer Lett. 2020;479:1-12.
Not in our library10.1016/j.canlet.2020.03.002
55.
Dolinar A, Koritnik B, Glavac D, Ravnik-Glavac M. Circular RNAs as potential blood biomarkers in amyotrophic lateral sclerosis. Mol Neurobiol. 2019;56:8052-8062.
Not in our library10.1007/s12035-019-1627-x
56.
Du WW, Fang L, Yang W, Wu N, Awan FM, Yang Z, Yang BB. Induction of tumor apoptosis through a circular RNA enhancing Foxo3 activity. Cell Death Differ. 2016;24:357-370.
Not in our library10.1038/cdd.2016.133
57.
Du WW, Yang W, Chen Y, Wu Z-K, Foster FS, Yang Z, Li X, Yang BB. Foxo3 circular RNA promotes cardiac senescence by modulating multiple factors associated with stress and senescence responses. Eur Heart J. 2017;38:1402-1412.
Not in our library10.1093/eurheartj/ehw001
58.
Du WW, Yang W, Liu E, Yang Z, Dhaliwal P, Yang BB. Foxo3 circular RNA retards cell cycle progression via forming ternary complexes with p21 and CDK2. Nucleic Acids Res. 2016;44:2846-2858.
Not in our library10.1093/nar/gkw027
59.
Dube U, Del-Aguila JL, Li Z, Budde JP, Jiang S, Hsu S, Ibanez L, Fernandez M, Farias F, Norton J, et al. An atlas of cortical circular RNA expression in Alzheimer disease brains demonstrates clinical and pathological associations. Nat Neurosci. 2019;22:1-10.
Not in our library10.1038/s41593-019-0501-5
60.
Dvinge H, Ries RE, Ilagan JO, Stirewalt DL, Meshinchi S, Bradley RK. Sample processing obscures cancer-specific alterations in leukemic transcriptomes. Proc Natl Acad Sci USA. 2014;111:16802-16807.
Not in our library10.1073/pnas.1413374111
61.
Enuka Y, Lauriola M, Feldman ME, Sas-Chen A, Ulitsky I, Yarden Y. Circular RNAs are long-lived and display only minimal early alterations in response to a growth factor. Nucleic Acids Res. 2015;44:1370-1383.
Not in our library10.1093/nar/gkv1367
62.
FUS affects circular RNA expression in murine embryonic stem cell-derived motor neurons · 2017
No notice
63.
Esmail H, Cobelens F, Goletti D. Transcriptional biomarkers for predicting development of tuberculosis: progress and clinical considerations. Eur Respir J. 2020;55:1901957.
Not in our library10.1183/13993003.01957-2019
64.
Circular RNA profiling and its potential for esophageal squamous cell cancer diagnosis and prognosis · 2019
Corrected
65.
Fang Y, Wang X, Li W, Han J, Jin J, Su F, Zhang J, Huang W, Xiao F, Pan Q, et al. Screening of circular RNAs and validation of circANKRD36 associated with inflammation in patients with type 2 diabetes mellitus. Int J Mol Med. 2018;42:1865-1874.
Not in our library10.3892/ijmm.2018.3783
66.
Fehlmann T, Kahraman M, Ludwig N, Backes C, Galata V, Keller V, Geffers L, Mercaldo N, Hornung D, Weis T, et al. Evaluating the use of circulating microRNA profiles for lung cancer detection in symptomatic patients. JAMA Oncol. 2020;6(5):714-723.
Not in our library10.1001/jamaoncol.2020.0001
67.
Fei T, Chen Y, Xiao T, Li W, Cato L, Zhang P, Cotter MB, Bowden M, Lis RT, Zhao SG, et al. Genome-wide CRISPR screen identifies HNRNPL as a prostate cancer dependency regulating RNA splicing. Proc Natl Acad Sci USA. 2017;114:E5207-E5215.
Not in our library10.1073/pnas.1617467114
68.
Fischer JW, Busa VF, Shao Y, Leung AKL. Structure-mediated RNA decay by UPF1 and G3BP1. Mol Cell. 2020;78:70-84.e76.
Not in our library10.1016/j.molcel.2020.01.021
69.
Fritz JV, Heintz-Buschart A, Ghosal A, Wampach L, Etheridge A, Galas D, Wilmes P. Sources and functions of extracellular small RNAs in human circulation. Annu Rev Nutr. 2016;36:301-336.
Not in our library10.1146/annurev-nutr-071715-050711
70.
Fu Y, Wang J, Qiao J, Yi Z. Signature of circular RNAs in peripheral blood mononuclear cells from patients with active tuberculosis. J Cell Mol Med. 2019;23:1917-1925.
Not in our library10.1111/jcmm.14093
71.
Gaffo E, Boldrin E, Molin A, Bresolin S, Bonizzato A, Trentin L, Frasson C, Debatin K-M, Meyer LH, te Kronnie G, et al. Circular RNA differential expression in blood cell populations and exploration of circRNA deregulation in pediatric acute lymphoblastic leukemia. Sci Rep. 2019;9:14670.
Not in our library10.1038/s41598-019-50864-z
72.
Gao Y, Zhao F. Computational strategies for exploring circular RNAs. Trends Genet. 2018.
Not in our library10.1016/j.tig.2017.12.016
73.
The Circular RNA Cdr1as Promotes Myocardial Infarction by Mediating the Regulation of miR-7a on Its Target Genes Expression · 2016
No notice
74.
Ghods F. Circular RNA in saliva. Adv Exp Med Biol. 2018;1087:131-139.
Not in our library10.1007/978-981-13-1426-1_11
75.
Giraldo NA, Becht E, Vano Y, Petitprez F, Lacroix L, Validire P, Sanchez-Salas R, Ingels A, Oudard S, Moatti A, et al. Tumor-infiltrating and peripheral blood T-cell immunophenotypes predict early relapse in localized clear cell renal cell carcinoma. Clin Cancer Res. 2017;23:4416-4428.
Not in our library10.1158/1078-0432.ccr-16-2848
76.
Glažar P, Papavasileiou P, Rajewsky N. circBase: a database for circular RNAs. RNA. 2014;20:1666-1670.
Not in our library10.1261/rna.043687.113
77.
Gong Y, Mao J, Wu D, Wang X, Li L, Zhu L, Song R. Circ-ZEB1.33 promotes the proliferation of human HCC by sponging miR-200a-3p and upregulating CDK6. Cancer Cell Int. 2018;18:116.
Not in our library10.1186/s12935-018-0602-3
78.
Gu C, Zhou N, Wang Z, Li G, Kou Y, Yu S, Feng Y, Chen L, Yang J, Tian F. circGprc5a promoted bladder oncogenesis and metastasis through Gprc5a-targeting peptide. Mol Ther Nucleic Acids. 2018;13:633-641.
Not in our library10.1016/j.omtn.2018.10.008
79.
Gu Y, Ke G, Wang L, Zhou E, Zhu K, Wei Y. Altered expression profile of circular RNAs in the serum of patients with diabetic retinopathy revealed by microarray. Ophthalmic Res. 2017;58:176-184.
Not in our library10.1159/000479156
80.
Guarnerio J, Bezzi M, Jeong J, Paffenholz SV, Berry K, Naldini MM, Lo-Coco F, Tay Y, Beck AH, Pandolfi P. Oncogenic role of fusion-circRNAs derived from cancer-associated chromosomal translocations. Cell. 2016;165:289-302.
Not in our library10.1016/j.cell.2016.03.020
81.
Gunsolus IL, Sweeney TE, Liesenfeld O, Ledeboer NA. Diagnosing and managing sepsis by probing the host response to infection: advances, opportunities, and challenges. J Clin Microbiol. 2019;57:e00425-e1419.
Not in our library10.1128/jcm.00425-19
82.
Expanded identification and characterization of mammalian circular RNAs · 2014
No notice
83.
Guo G, Wang H, Ye L, Shi X, Yan K, Lin K, Huang Q, Li B, Lin Q, Zhu L, et al. Hsa_circ_0000479 as a novel diagnostic biomarker of systemic lupus erythematosus. Front Immunol. 2019;10:2281.
Not in our library10.3389/fimmu.2019.02281
84.
Concise whole blood transcriptional signatures for incipient tuberculosis: a systematic review and patient-level pooled meta-analysis · 2020
No notice
85.
Liquid biopsy for infectious diseases: a focus on microbial cell-free DNA sequencing · 2020
No notice
86.
Han J, Zhang L, Hu L, Yu H, Xu F, Yang B, Zhang R, Zhang Y, An Y. Circular RNA-expression profiling reveals a potential role of hsa_circ_0097435 in heart failure via sponging multiple microRNAs. Front Genet. 2020;11:212.
Not in our library10.3389/fgene.2020.00212
87.
A Dual-Circular RNA Signature as a Non-invasive Diagnostic Biomarker for Gastric Cancer · 2020
Not checked
88.
A Parkinson's disease CircRNAs Resource reveals a link between circSLC8A1 and oxidative stress · 2020
Corrected
89.
A novel plasma circular RNA circ FARSA is a potential biomarker for non‐small cell lung cancer · 2018
No notice
90.
Hansen TB, Jensen TI, Clausen BH, Bramsen JB, Finsen B, Damgaard CK, Kjems J. Natural RNA circles function as efficient microRNA sponges. Nature. 2013;495:384-388.
Not in our library10.1038/nature11993
91.
Hardwick SA, Deveson IW, Mercer TR. Reference standards for next-generation sequencing. Nat Rev Genet. 2017;18(8):473-484.
Not in our library10.1038/nrg.2017.44
92.
He F, Zhong X, Lin Z, Lin J, Qiu M, Li X, Hu Z. Plasma exo-hsa_circRNA_0056616: A potential biomarker for lymph node metastasis in lung adenocarcinoma. J Cancer. 2020;11:4037-4046.
Not in our library10.7150/jca.30360
93.
Heitzer E, Haque IS, Roberts CES, Speicher MR. Current and future perspectives of liquid biopsies in genomics-driven oncology. Nat Rev Genet. 2019;20:71-88.
Not in our library10.1038/s41576-018-0071-5
94.
Circular non-coding RNA ANRIL modulates ribosomal RNA maturation and atherosclerosis in humans · 2016
No notice
95.
Hong DK, Blauwkamp TA, Kertesz M, Bercovici S, Truong C, Banaei N. Liquid biopsy for infectious diseases: sequencing of cell-free plasma to detect pathogen DNA in patients with invasive fungal disease. Diagn Microbiol Infect Dis. 2018;92(3):210-213.
Not in our library10.1016/j.diagmicrobio.2018.06.009
96.
Hsu M-T, Coca-Prados M. Electron microscopic evidence for the circular form of RNA in the cytoplasm of eukaryotic cells. Nature. 1979;280:339-340.
Not in our library10.1038/280339a0
97.
circGSK3β promotes metastasis in esophageal squamous cell carcinoma by augmenting β-catenin signaling · 2019
No notice
98.
Hu Y, Zhu Y, Zhang W, Lang J, Ning L. Utility of plasma circBNC2 as a diagnostic biomarker in epithelial ovarian cancer. Onco Targets Ther. 2019;12:9715-9723.
Not in our library10.2147/ott.s211413
99.
Hu ZQ, Zhou SL, Li J, Zhou ZJ, Wang PC, Xin HY, Mao L, Luo CB, Yu SY, Huang XW, et al. Circular RNA sequencing identifies circASAP1 as a key regulator in hepatocellular carcinoma metastasis. Hepatology. 2019.
Not in our library10.1002/hep.31068
100.
Huang M, He YR, Liang LC, Huang Q, Zhu ZQ. Circular RNA hsa_circ_0000745 may serve as a diagnostic marker for gastric cancer. World J Gastroenterol. 2017;23:6330-6338.
Not in our library10.3748/wjg.v23.i34.6330
101.
Huang R, Zhang Y, Han B, Bai Y, Zhou R, Gan G, Chao J, Hu G, Yao H. Circular RNA HIPK2 regulates astrocyte activation via cooperation of autophagy and ER stress by targeting MIR124-2HG. Autophagy. 2017;13:1722-1741.
Not in our library10.1080/15548627.2017.1356975
102.
Huang Z, Su R, Deng Z, Xu J, Peng Y, Luo Q, Li J. Identification of differentially expressed circular RNAs in human monocyte derived macrophages response to Mycobacterium tuberculosis infection. Sci Rep. 2017;7:13673.
Not in our library10.1038/s41598-017-13885-0
103.
Plasma Circular RNAs hsa_circ_0001953 and hsa_circ_0009024 as Diagnostic Biomarkers for Active Tuberculosis · 2018
Not checked
104.
Huang Z, Su R, Yao F, Peng Y, Luo Q, Li J. Circulating circular RNAs hsa_circ_0001204 and hsa_circ_0001747 act as diagnostic biomarkers for active tuberculosis detection. Int J Clin Exp Pathol. 2018;11:586-594.
Not in our library
105.
Huang Z-K, Yao F-Y, Xu J-Q, Deng Z, Su R-G, Peng Y-P, Luo Q, Li J-M. Microarray expression profile of circular RNAs in peripheral blood mononuclear cells from active tuberculosis patients. Cell Physiol Biochem. 2018;45:1230-1240.
Not in our library10.1159/000487454
106.
Circular RNA-protein interactions: functions, mechanisms, and identification · 2020
No notice
107.
Exosomal circRNA-100338 promotes hepatocellular carcinoma metastasis via enhancing invasiveness and angiogenesis · 2020
No notice
108.
Iparraguirre L, Muñoz-Culla M, Prada-Luengo I, Castillo-Triviño T, Olascoaga J, Otaegui D. Circular RNA profiling reveals that circular RNAs from ANXA2 can be used as new biomarkers for multiple sclerosis. Hum Mol Genet. 2017;26:3564-3572.
Not in our library10.1093/hmg/ddx243
109.
Ivanov A, Memczak S, Wyler E, Torti F, Porath HT, Orejuela MR, Piechotta M, Levanon EY, Landthaler M, Dieterich C, et al. Analysis of intron sequences reveals hallmarks of circular RNA biogenesis in animals. Cell Rep. 2014;10:170-177.
Not in our library10.1016/j.celrep.2014.12.019
110.
Jeck WR, Sharpless NE. Detecting and characterizing circular RNAs. Nat Biotechnol. 2014;32:453-461.
Not in our library10.1038/nbt.2890
111.
Jeck WR, Sorrentino JA, Wang K, Slevin MK, Burd CE, Liu J, Marzluff WF, Sharpless NE. Circular RNAs are abundant, conserved, and associated with ALU repeats. RNA. 2013;19:141-157.
Not in our library10.1261/rna.035667.112
112.
Ji P, Wu W, Chen S, Zheng Y, Zhou L, Zhang J, Cheng H, Yan J, Zhang S, Yang P, et al. Expanded expression landscape and prioritization of circular RNAs in mammals. Cell Rep. 2019;26:3444-3460.e3445.
Not in our library10.1016/j.celrep.2019.02.078
113.
Jiang M, Lash GE, Zhao X, Long Y, Guo C, Yang H. CircRNA-0004904, circRNA-0001855, and PAPP-A: potential novel biomarkers for the prediction of preeclampsia. Cell Physiol Biochem. 2018;46:2576-2586.
Not in our library10.1159/000489685
114.
Joosse SA, Pantel K. Tumor-educated platelets as liquid biopsy in cancer patients. Cancer Cell. 2015;28:552-554.
Not in our library10.1016/j.ccell.2015.10.007
115.
Jost I, Shalamova LA, Gerresheim GK, Niepmann M, Bindereif A, Rossbach O. Functional sequestration of microRNA-122 from Hepatitis C Virus by circular RNA sponges. RNA Biol. 2018;15(8):1-8.
Not in our library10.1080/15476286.2018.1435248
116.
Karczewski KJ, Snyder MP. Integrative omics for health and disease. Nat Rev Genet. 2018;19:299-310.
Not in our library10.1038/nrg.2018.4
117.
Kelly S, Greenman C, Cook PR, Papantonis A. Exon skipping is correlated with exon circularization. J Mol Biol. 2015;427:2414-2417.
Not in our library10.1016/j.jmb.2015.02.018
118.
Khan M, Reckman YJ, Aufiero S, van den Hoogenhof M, van der Made I, Beqqali A, Koolbergen DR, Rasmussen TB, van der Velden J, Creemers EE, et al. RBM20 regulates circular RNA production from the Titin gene. Circ Res. 2016;119:996-1003.
Not in our library10.1161/circresaha.116.309568
119.
Kleaveland B, Shi CY, Stefano J, Bartel DP. A network of noncoding regulatory RNAs acts in the mammalian brain. Cell. 2018;174(2):350-362.
Not in our library10.1016/j.cell.2018.05.022
120.
Kölling M, Haddad G, Wegmann U, Kistler A, Bosakova A, Seeger H, Hübel K, Haller H, Mueller T, Wüthrich RP, et al. Circular RNAs in urine of kidney transplant patients with acute T cell-mediated allograft rejection. Clin Chem. 2019;65:1287-1294.
Not in our library10.1373/clinchem.2019.305854
121.
Kong S, Yang Q, Tang C, Wang T, Shen X, Ju S. Identification of hsa_circ_0001821 as a novel diagnostic biomarker in gastric cancer via comprehensive circular RNA profiling. Front Genet. 2019;10:878.
Not in our library10.3389/fgene.2019.00878
122.
Kossenkov AV, Qureshi R, Dawany NB, Wickramasinghe J, Liu Q, Majumdar SR, Chang C, Widura S, Kumar T, Horng W-H, et al. A gene expression classifier from whole blood distinguishes benign from malignant lung nodules detected by low-dose CT. Cancer Res. 2018;79:263-273.
Not in our library10.1158/0008-5472.can-18-2032
123.
Kramer MC, Liang D, Tatomer DC, Gold B, March ZM, Cherry S, Wilusz JE. Combinatorial control of Drosophila circular RNA expression by intronic repeats, hnRNPs, and SR proteins. Genes Dev. 2015;29(20):2168-2182.
Not in our library10.1101/gad.270421.115
124.
Kristensen LS, Andersen MS, Stagsted LVW, Ebbesen KK, Hansen TB, Kjems J. The biogenesis, biology and characterization of circular RNAs. Nat Rev Genet. 2019;20:1-17.
Not in our library10.1038/s41576-019-0158-7
125.
Kumar L, Shamsuzzama HR, Haque R, Baghel T, Nazir A. Circular RNAs: the emerging class of non-coding RNAs and their potential role in human neurodegenerative diseases. Mol Neurobiol. 2017;54:7224-7234.
Not in our library10.1007/s12035-016-0213-8
126.
Kwapisz D. The first liquid biopsy test approved. Is it a new era of mutation testing for non-small cell lung cancer? Ann Transl Med. 2017;5:46.
Not in our library10.21037/atm.2017.01.32
127.
Lam WKJ, Lo YMD. Circular RNAs as urinary biomarkers. Clin Chem. 2019;65:1196-1198.
Not in our library10.1373/clinchem.2019.309773
128.
Lamb YN, Dhillon S. Epi proColon® 2.0 CE: a blood-based screening test for colorectal cancer. Mol Diagn Ther. 2017;21:225-232.
Not in our library10.1007/s40291-017-0259-y
129.
Circular RNAs Co-Precipitate with Extracellular Vesicles: A Possible Mechanism for circRNA Clearance · 2016
No notice
130.
Legnini I, Timoteo GD, Rossi F, Morlando M, Briganti F, Sthandier O, Fatica A, Santini T, Andronache A, Wade M, et al. Circ-ZNF609 is a circular RNA that can be translated and functions in myogenesis. Mol Cell. 2017;66:22-37.
Not in our library10.1016/j.molcel.2017.02.017
131.
Lei B, Zhou J, Xuan X, Tian Z, Zhang M, Gao W, Lin Y, Ni B, Pang H, Fan W. Circular RNA expression profiles of peripheral blood mononuclear cells in hepatocellular carcinoma patients by sequence analysis. Cancer Med. 2019;8:1423-1433.
Not in our library10.1002/cam4.2010
132.
Lesko LJ, Atkinson AJ. Use of biomarkers and surrogate endpoints in drug development and regulatory decision making: criteria, validation, strategies. Annu Rev Pharmacol Toxicol. 2001;41:347-366.
Not in our library10.1146/annurev.pharmtox.41.1.347
133.
Li P, Chen S, Chen H, Mo X, Li T, Shao Y, Xiao B, Guo J. Using circular RNA as a novel type of biomarker in the screening of gastric cancer. Clin Chim Acta. 2015;444:132-136.
Not in our library10.1016/j.cca.2015.02.018
134.
Li Y, Zheng Q, Bao C, Li S, Guo W, Zhao J, Chen D, Gu J, He X, Huang S. Circular RNA is enriched and stable in exosomes: a promising biomarker for cancer diagnosis. Cell Res. 2015;25:981-984.
Not in our library10.1038/cr.2015.82
135.
Li Z, Huang C, Bao C, Chen L, Lin M, Wang X, Zhong G, Yu B, Hu W, Dai L, et al. Exon-intron circular RNAs regulate transcription in the nucleus. Nat Struct Mol Biol. 2015;22:256-264.
Not in our library10.1038/nsmb.2959
136.
Li M, Xie X, Zhou J, Sheng M, Yin X, Ko E-A, Zhou T, Gu W. Quantifying circular RNA expression from RNA-seq data using model-based framework. Bioinformatics. 2017;33(14):2131-2139.
Not in our library10.1093/bioinformatics/btx129
137.
Li S, Li Y, Chen B, Zhao J, Yu S, Tang Y, Zheng Q, Li Y, Wang P, He X, et al. exoRBase: a database of circRNA, lncRNA and mRNA in human blood exosomes. Nucleic Acids Res. 2017;46:D106-D112.
Not in our library10.1093/nar/gkx891
138.
Characterization of hsa_circ_0004277 as a New Biomarker for Acute Myeloid Leukemia via Circular RNA Profile and Bioinformatics Analysis · 2017
No notice
139.
Li WH, Song YC, Zhang H, Zhou ZJ, Xie X, Zeng QN, Guo K, Wang T, Xia P, Chang DM. Decreased expression of hsa_circ_00001649 in gastric cancer and its clinical significance. Dis Markers. 2017;2017:4587698.
Not in our library10.1155/2017/4587698
140.
Li X, Liu C-X, Xue W, Zhang Y, Jiang S, Yin Q-F, Wei J, Yao R-W, Yang L, Chen L-L. Coordinated circRNA biogenesis and function with NF90/NF110 in viral infection. Mol Cell. 2017;67:214-227.e217.
Not in our library10.1016/j.molcel.2017.05.023
141.
Circular RNA IARS (circ-IARS) secreted by pancreatic cancer cells and located within exosomes regulates endothelial monolayer permeability to promote tumor metastasis · 2018
No notice
142.
Li L, Li W, Chen N, Zhao H, Xu G, Zhao Y, Pan X, Zhang X, Zhou L, Yu D, et al. FLI1 exonic circular RNAs as a novel oncogenic driver to promote tumor metastasis in small cell lung cancer. Clin Cancer Res. 2018;25:1302-1317.
Not in our library10.1158/1078-0432.ccr-18-1447
143.
Li T, Shao Y, Fu L, Xie Y, Zhu L, Sun W, Yu R, Xiao B, Guo J. Plasma circular RNA profiling of patients with gastric cancer and their droplet digital RT-PCR detection. J Mol Med (Berl). 2018;96:85-96.
Not in our library10.1007/s00109-017-1600-y
144.
Li X, Yang L, Chen L-L. The biogenesis, functions, and challenges of circular RNAs. Mol Cell. 2018;71:428-442.
Not in our library10.1016/j.molcel.2018.06.034
145.
Li Z, Yanfang W, Li J, Jiang P, Peng T, Chen K, Zhao X, Zhang Y, Zhen P, Zhu J, et al. Tumor-released exosomal circular RNA PDE8A promotes invasive growth via the miR-338/MACC1/MET pathway in pancreatic cancer. Cancer Lett. 2018;432:237-250.
Not in our library10.1016/j.canlet.2018.04.035
146.
Li Q, Wang Y, Wu S, Zhou Z, Ding X, Shi R, Thorne RF, Zhang XD, Hu W, Wu M. CircACC1 regulates assembly and activation of AMPK complex under metabolic stress. Cell Metab. 2019;30:157-173.
Not in our library10.1016/j.cmet.2019.05.009
147.
Li S, Zhang J, Tan X, Deng J, Li Y, Piao Y, Li C, Yang W, Mo W, Sun J, et al. Microarray expression profile of circular RNAs and mRNAs in children with systemic lupus erythematosus. Clin Rheumatol. 2019;38:1339-1350.
Not in our library10.1007/s10067-018-4392-8
148.
Li XN, Wang ZJ, Ye CX, Zhao BC, Huang XX, Yang L. Circular RNA circVAPA is up-regulated and exerts oncogenic properties by sponging miR-101 in colorectal cancer. Biomed Pharmacother. 2019;112:108611.
Not in our library10.1016/j.biopha.2019.108611
149.
Li Y, Zhao J, Yu S, Wang Z, He X, Su Y, Guo T, Sheng H, Chen J, Zheng Q, et al. Extracellular vesicles long RNA sequencing reveals abundant mRNA, circRNA, and lncRNA in human blood as potential biomarkers for cancer diagnosis. Clin Chem. 2019;65:798-808.
Not in our library10.1373/clinchem.2018.301291
150.
Li Z, Zhou Y, Yang G, He S, Qiu X, Zhang L, Deng Q, Zheng F. Using circular RNA SMARCA5 as a potential novel biomarker for hepatocellular carcinoma. Clin Chim Acta. 2019;492:37-44.
Not in our library10.1016/j.cca.2019.02.001
151.
Li Z, Zhu X, Huang S. Extracellular vesicle long non-coding RNAs and circular RNAs: biology, functions and applications in cancer. Cancer Lett. 2020;489:111-120.
Not in our library10.1016/j.canlet.2020.06.006
152.
Liang D, Wilusz JE. Short intronic repeat sequences facilitate circular RNA production. Genes Dev. 2014;28:2233-2247.
Not in our library10.1101/gad.251926.114
153.
Liang D, Tatomer DC, Luo Z, Wu H, Yang L, Chen L-L, Cherry S, Wilusz JE. The output of protein-coding genes shifts to circular RNAs when the pre-mRNA processing machinery is limiting. Mol Cell. 2017;68:940-954.e943.
Not in our library10.1016/j.molcel.2017.10.034
154.
Liang B, Li M, Deng Q, Wang C, Rong J, He S, Xiang Y, Zheng F. CircRNA ZNF609 in peripheral blood leukocytes acts as a protective factor and a potential biomarker for coronary artery disease. Ann Transl Med. 2020;8:741.
Not in our library10.21037/atm-19-4728
155.
Lin J, Cai D, Li W, Yu T, Mao H, Jiang S, Xiao B. Plasma circular RNA panel acts as a novel diagnostic biomarker for colorectal cancer. Clin Biochem. 2019;74:60-68.
Not in our library10.1016/j.clinbiochem.2019.10.012
156.
Liu C-X, Li X, Nan F, Jiang S, Gao X, Guo S-K, Xue W, Cui Y, Dong K, Ding H, et al. Structure and degradation of circular RNAs regulate PKR activation in innate immunity. Cell. 2019;177(4):865-880.
Not in our library10.1016/j.cell.2019.03.046
157.
Liu XX, Yang YE, Liu X, Zhang MY, Li R, Yin YH, Qu YQ. A two-circular RNA signature as a noninvasive diagnostic biomarker for lung adenocarcinoma. J Transl Med. 2019;17:50.
Not in our library10.1186/s12967-019-1800-z
158.
Liu YT, Han XH, Xing PY, Hu XS, Hao XZ, Wang Y, Li JL, Zhang ZS, Yang ZH, Shi YK. Circular RNA profiling identified as a biomarker for predicting the efficacy of Gefitinib therapy for non-small cell lung cancer. J Thorac Dis. 2019;11:1779-1787.
Not in our library10.21037/jtd.2019.05.22
159.
Liu H, Lu G, Wang W, Jiang X, Gu S, Wang J, Yan X, He F, Wang J. A panel of circRNAs in the serum serves as biomarkers for Mycobacterium tuberculosis Infection. Front Microbiol. 2020;11:1215.
Not in our library10.3389/fmicb.2020.01215
160.
Loon EV, Gazut S, Yazdani S, Lerut E, de Loor H, Coemans M, Noël L-H, Thorrez L, Lommel LV, Schuit F, et al. Development and validation of a peripheral blood mRNA assay for the assessment of antibody-mediated kidney allograft rejection: a multicentre, prospective study. EBioMedicine. 2019;46:463-472.
Not in our library10.1016/j.ebiom.2019.07.028
161.
Lu J, Zhang PY, Xie JW, Wang JB, Lin JX, Chen QY, Cao LL, Huang CM, Li P, Zheng CH. hsa_circ_0000467 promotes cancer progression and serves as a diagnostic and prognostic biomarker for gastric cancer. J Clin Lab Anal. 2019;33:e22726.
Not in our library10.1002/jcla.22726
162.
Lu J, Zhang PY, Xie JW, Wang JB, Lin JX, Chen QY, Cao LL, Li P, Zheng CH, Huang CM. Circular RNA hsa_circ_0006848 related to ribosomal protein L6 acts as a novel biomarker for early gastric cancer. Dis Markers. 2019;2019:3863458.
Not in our library10.1155/2019/3863458
163.
Lu X, Song M, Wang F. Circulating circular RNAs as biomarkers of cancer. Non-coding RNA Investig. 2019;3:8.
Not in our library
164.
Circular RNA (circRNA) in Alzheimer's disease (AD) · 2013
No notice
165.
Luo Q, Zhang L, Li X, Fu B, Deng Z, Qing C, Su R, Xu J, Guo Y, Huang Z, et al. Identification of circular RNAs hsa_circ_0044235 in peripheral blood as novel biomarkers for rheumatoid arthritis. Clin Exp Immunol. 2018;194:118-124.
Not in our library10.1111/cei.13181
166.
Luo Q, Zhang L, Li X, Fu B, Guo Y, Huang Z, Li J. Identification of circular RNAs hsa_circ_0044235 and hsa_circ_0068367 as novel biomarkers for systemic lupus erythematosus. Int J Mol Med. 2019;44:1462-1472.
Not in our library10.3892/ijmm.2019.4302
167.
Luo H, Zhao Q, Wei W, Zheng L, Yi S, Li G, Wang W, Sheng H, Pu H, Mo H, et al. Circulating tumor DNA methylation profiles enable early diagnosis, prognosis prediction, and screening for colorectal cancer. Sci Transl Med. 2020;12:eaax7533.
Not in our library10.1126/scitranslmed.aax7533
168.
Luo HL, Peng Y, Luo H, Zhang JA, Liu GB, Xu H, Huang GX, Sun YF, Huang J, Zheng BY, et al. Circular RNA hsa_circ_0001380 in peripheral blood as a potential diagnostic biomarker for active pulmonary tuberculosis. Mol Med Rep. 2020;21:1890-1896.
Not in our library10.3892/mmr.2020.10992
169.
Luo Y-H, Yang Y-P, Chien C-S, Yarmishyn AA, Ishola AA, Chien Y, Chen Y-M, Huang T-W, Lee K-Y, Huang W-C, et al. Plasma level of circular RNA hsa_circ_0000190 correlates with tumor progression and poor treatment response in advanced lung cancers. Cancers. 2020;12:1740.
Not in our library10.3390/cancers12071740
170.
Ma J, Qi G, Li L. A novel serum exosomes-based biomarker hsa_circ_0002130 facilitates osimertinib-resistance in non-small cell lung cancer by sponging miR-498. Onco Targets Ther. 2020;13:5293-5307.
Not in our library10.2147/ott.s243214
171.
Maas SLN, Breakefield XO, Weaver AM. Extracellular vesicles: unique intercellular delivery vehicles. Trends Cell Biol. 2017;27:172-188.
Not in our library10.1016/j.tcb.2016.11.003
172.
A map of human circular RNAs in clinically relevant tissues · 2017
No notice
173.
MacLean E, Broger T, Yerlikaya S, Fernandez-Carballo BL, Pai M, Denkinger CM. A systematic review of biomarkers to detect active tuberculosis. Nat Microbiol. 2019;4:748-758.
Not in our library10.1038/s41564-019-0380-2
174.
Marshall K, Mohr S, Khettabi F, Nossova N, Chao S, Bao W, Ma J, Li XJ, Liew CC. A blood-based biomarker panel for stratifying current risk for colorectal cancer. Int J Cancer. 2010;126:1177-1186.
Not in our library10.1002/ijc.24910
175.
Mattox AK, Bettegowda C, Zhou S, Papadopoulos N, Kinzler KW, Vogelstein B. Applications of liquid biopsies for cancer. Sci Transl Med. 2019;11:eaay1984.
Not in our library10.1126/scitranslmed.aay1984
176.
Max KEA, Bertram K, Akat K, Bogardus KA, Li J, Morozov P, Ben-Dov IZ, Li X, Weiss ZR, Azizian A, et al. Human plasma and serum extracellular small RNA reference profiles and their clinical utility. Proc Natl Acad Sci USA. 2018;115:201714397.
Not in our library10.1073/pnas.1714397115
177.
Mayhew MB, Buturovic L, Luethy R, Midic U, Moore AR, Roque JA, Shaller BD, Asuni T, Rawling D, Remmel M, et al. A generalizable 29-mRNA neural-network classifier for acute bacterial and viral infections. Nat Commun. 2020;11:1177.
Not in our library10.1038/s41467-020-14975-w
178.
Mei M, Wang Y, Wang Q, Liu Y, Song W, Zhang M. CircCDYL serves as a new biomarker in Mantle cell lymphoma and promotes cell proliferation. Cancer Manag Res. 2019;11:10215-10221.
Not in our library10.2147/cmar.s232075
179.
Memczak S, Jens M, Elefsinioti A, Torti F, Krueger J, Rybak A, Maier L, Mackowiak SD, Gregersen LH, Munschauer M, et al. Circular RNAs are a large class of animal RNAs with regulatory potency. Nature. 2013;495:333-338.
Not in our library10.1038/nature11928
180.
Identification and Characterization of Circular RNAs As a New Class of Putative Biomarkers in Human Blood · 2015
No notice
181.
CircRNA: functions and properties of a novel potential biomarker for cancer · 2017
No notice
182.
Miao Q, Zhong Z, Jiang Z, Lin Y, Ni B, Yang W, Tang J. RNA-seq of circular RNAs identified circPTPN22 as a potential new activity indicator in systemic lupus erythematosus. Lupus. 2019;28:520-528.
Not in our library10.1177/0961203319830493
183.
Mitchell PS, Parkin RK, Kroh EM, Fritz BR, Wyman SK, Pogosova-Agadjanyan EL, Peterson A, Noteboom J, O’Briant KC, Allen A, et al. Circulating microRNAs as stable blood-based markers for cancer detection. Proc Natl Acad Sci USA. 2008;105:10513-10518.
Not in our library10.1073/pnas.0804549105
184.
Ng WL, Marinov GK, Liau ES, Lam YL, Lim Y-Y, Ea C-K. Inducible RasGEF1B circular RNA is a positive regulator of ICAM-1 in the TLR4/LPS pathway. RNA Biol. 2016;13:861-871.
Not in our library10.1080/15476286.2016.1207036
185.
Nicolet BP, Engels S, Aglialoro F, van den Akker E, von Lindern M, Wolkers MC. Circular RNA expression in human hematopoietic cells is widespread and cell-type specific. Nucleic Acids Res. 2018;46:8168-8180.
Not in our library10.1093/nar/gky721
186.
Ouyang Q, Huang Q, Jiang Z, Zhao J, Shi GP, Yang M. Using plasma circRNA_002453 as a novel biomarker in the diagnosis of lupus nephritis. Mol Immunol. 2018;101:531-538.
Not in our library10.1016/j.molimm.2018.07.029
187.
Ouyang Q, Wu J, Jiang Z, Zhao J, Wang R, Lou A, Zhu D, Shi GP, Yang M. Microarray expression profile of circular RNAs in peripheral blood mononuclear cells from rheumatoid arthritis patients. Cell Physiol Biochem. 2017;42:651-659.
Not in our library10.1159/000477883
188.
Pamudurti NR, Bartok O, Jens M, Ashwal-Fluss R, Stottmeister C, Ruhe L, Hanan M, Wyler E, Perez-Hernandez D, Ramberger E, et al. Translation of circRNAs. Mol Cell. 2017;66:9-21.
Not in our library10.1016/j.molcel.2017.02.021
189.
Identification of Serum Exosomal hsa-circ-0004771 as a Novel Diagnostic Biomarker of Colorectal Cancer · 2019
No notice
190.
Noncoding RNAs in Extracellular Fluids as Cancer Biomarkers: The New Frontier of Liquid Biopsies · 2019
No notice
191.
Park O, Ha H, Lee Y, Boo S, Kwon D, Song H, Kim Y. Endoribonucleolytic cleavage of m6A-containing RNAs by RNase P/MRP complex. Mol Cell. 2019;74(3):494-507.
Not in our library10.1016/j.molcel.2019.02.034
192.
Peng YK, Pu K, Su HX, Zhang J, Zheng Y, Ji R, Guo QH, Wang YP, Guan QL, Zhou YN. Circular RNA hsa_circ_0010882 promotes the progression of gastric cancer via regulation of the PI3K/Akt/mTOR signaling pathway. Eur Rev Med Pharmacol Sci. 2020;24:1142-1151.
Not in our library10.26355/eurrev_202002_20165
193.
Ping L, Jian-Jun C, Chu-Shu L, Guang-Hua L, Ming Z. High circ_100053 predicts a poor outcome for chronic myeloid leukemia and is involved in imatinib resistance. Oncol Res. 2019.
Not in our library10.3727/096504018x15412701483326
194.
Piwecka M, Glažar P, Hernandez-Miranda LR, Memczak S, Wolf SA, Rybak-Wolf A, Filipchyk A, Klironomos F, Cerda Jara CA, Fenske P, et al. Loss of a mammalian circular RNA locus causes miRNA deregulation and affects brain function. Science. 2017;357:eaam8526.
Not in our library10.1126/science.aam8526
195.
Powers KA, Ghani AC, Miller WC, Hoffman IF, Pettifor AE, Kamanga G, Martinson FE, Cohen MS. The role of acute and early HIV infection in the spread of HIV and implications for transmission prevention strategies in Lilongwe, Malawi: a modelling study. Lancet. 2011;378:256-268.
Not in our library10.1016/s0140-6736(11)60842-8
196.
Selective release of circRNAs in platelet-derived extracellular vesicles · 2018
Not checked
197.
Qian Z, Liu H, Li M, Shi J, Li N, Zhang Y, Zhang X, Lv J, Xie X, Bai Y, et al. Potential diagnostic power of blood circular RNA expression in active pulmonary tuberculosis. EBioMedicine. 2018;27:18-26.
Not in our library10.1016/j.ebiom.2017.12.007
198.
Qian Z, Lv J, Kelly GT, Wang H, Zhang X, Gu W, Yin X, Wang T, Zhou T. Expression of nuclear factor, erythroid 2-like 2-mediated genes differentiates tuberculosis. Tuberculosis. 2016;99:56-62.
Not in our library10.1016/j.tube.2016.04.008
199.
Qiao GL, Chen L, Jiang WH, Yang C, Yang CM, Song LN, Chen Y, Yan HL, Ma LJ. Hsa_circ_0003998 may be used as a new biomarker for the diagnosis and prognosis of hepatocellular carcinoma. Onco Targets Ther. 2019;12:5849-5860.
Not in our library10.2147/ott.s210363
200.
Ramilo O, Mejias A. Host transcriptomics for diagnosis of infectious diseases: one step closer to clinical application. Eur Respir J. 2017;49:1700993.
Not in our library10.1183/13993003.00993-2017
201.
Ravnik-Glavač M, Glavač D. Circulating RNAs as potential biomarkers in amyotrophic lateral sclerosis. Int J Mol Sci. 2020;21:1714.
Not in our library10.3390/ijms21051714
202.
Revenfeld ALS, Bæk R, Nielsen MH, Stensballe A, Varming K, Jørgensen M. Diagnostic and prognostic potential of extracellular vesicles in peripheral blood. Clin Ther. 2014;36:830-846.
Not in our library10.1016/j.clinthera.2014.05.008
203.
Richey LE, Halperin J. Acute human immunodeficiency virus infection. Am J Med Sci. 2013;345:136-142.
Not in our library10.1097/maj.0b013e31825d4b88
204.
CircPSMC3 suppresses the proliferation and metastasis of gastric cancer by acting as a competitive endogenous RNA through sponging miR-296-5p · 2019
Retracted
205.
Rose S, Contrepois K, Moneghetti KJ, Zhou W, Mishra T, Mataraso S, Dagan-Rosenfeld O, Ganz AB, Dunn J, Hornburg D, et al. A longitudinal big data approach for precision health. Nat Med. 2019;25:792-804.
Not in our library10.1038/s41591-019-0414-6
206.
Ross RW, Galsky MD, Scher HI, Magidson J, Wassmann K, Lee G-S, Katz L, Subudhi SK, Anand A, Fleisher M, et al. A whole-blood RNA transcript-based prognostic model in men with castration-resistant prostate cancer: a prospective study. Lancet Oncol. 2012;13:1105-1113.
Not in our library10.1016/s1470-2045(12)70263-2
207.
Rubis G, Krishnan S, Bebawy M. Liquid biopsies in cancer diagnosis, monitoring, and prognosis. Trends Pharmacol Sci. 2019;40:172-186.
Not in our library10.1016/j.tips.2019.01.006
208.
Rybak-Wolf A, Stottmeister C, Glažar P, Jens M, Pino N, Giusti S, Hanan M, Behm M, Bartok O, Ashwal-Fluss R, et al. Circular RNAs in the mammalian brain are highly abundant, conserved, and dynamically expressed. Mol Cell. 2015;58:870-885.
Not in our library10.1016/j.molcel.2015.03.027
209.
Cell-Type Specific Features of Circular RNA Expression · 2013
Corrected
210.
Circular RNAs Are the Predominant Transcript Isoform from Hundreds of Human Genes in Diverse Cell Types · 2012
No notice
211.
Sambarey A, Devaprasad A, Mohan A, Ahmed A, Nayak S, Swaminathan S, D'Souza G, Jesuraj A, Dhar C, Babu S, et al. Unbiased identification of blood-based biomarkers for pulmonary tuberculosis by modeling and mining molecular interaction networks. EBioMedicine. 2017;15:112-126.
Not in our library10.1016/j.ebiom.2016.12.009
212.
Sanger HL, Klotz G, Riesner D, Gross HJ, Kleinschmidt AK. Viroids are single-stranded covalently closed circular RNA molecules existing as highly base-paired rod-like structures. Proc Natl Acad Sci USA. 1976;73:3852-3856.
Not in our library10.1073/pnas.73.11.3852
213.
Schnell A, Schmidl C, Herr W, Siska PJ. The peripheral and intratumoral immune cell landscape in cancer patients: a proxy for tumor biology and a tool for outcome prediction. Biomedicines. 2018;6:25.
Not in our library10.3390/biomedicines6010025
214.
Shaked Y. The pro-tumorigenic host response to cancer therapies. Nat Rev Cancer. 2019;19:667-685.
Not in our library10.1038/s41568-019-0209-6
215.
Exosomal circPACRGL promotes progression of colorectal cancer via the miR-142-3p/miR-506-3p- TGF-β1 axis · 2020
No notice
216.
The novel roles of circRNAs in human cancer · 2019
No notice
217.
Shao Y, Tao X, Lu R, Zhang H, Ge J, Xiao B, Ye G, Guo J. Hsa_circ_0065149 is an indicator for early gastric cancer screening and prognosis prediction. Pathol Oncol Res. 2020;26:1475-1482.
Not in our library10.1007/s12253-019-00716-y
218.
Sheng R, Li X, Wang Z, Wang X. Circular RNAs and their emerging roles as diagnostic and prognostic biomarkers in ovarian cancer. Cancer Lett. 2020;473:139-147.
Not in our library10.1016/j.canlet.2019.12.043
219.
Shi L, Tao C, Tang Y, Xia Y, Li X, Wang X. Hypoxia-induced hsa_circ_0000826 is linked to liver metastasis of colorectal cancer. J Clin Lab Anal. 2020;34(9):e23405.
Not in our library10.1002/jcla.23405
220.
Showe MK, Vachani A, Kossenkov AV, Yousef M, Nichols C, Nikonova EV, Chang C, Kucharczuk J, Tran B, Wakeam E, et al. Gene expression profiles in peripheral blood mononuclear cells can distinguish patients with non-small cell lung cancer from patients with nonmalignant lung disease. Cancer Res. 2009;69:9202-9210.
Not in our library10.1158/0008-5472.can-09-1378
221.
Shuai M, Hong J, Huang D, Zhang X, Tian Y. Upregulation of circRNA_0000285 serves as a prognostic biomarker for nasopharyngeal carcinoma and is involved in radiosensitivity. Oncol Lett. 2018;16:6495-6501.
Not in our library10.3892/ol.2018.9471
222.
Siravegna G, Marsoni S, Siena S, Bardelli A. Integrating liquid biopsies into the management of cancer. Nat Rev Clin Oncol. 2017;14:531-548.
Not in our library10.1038/nrclinonc.2017.14
223.
Smid M, Wilting SM, Uhr K, Rodríguez-González GF, de Weerd V, van der Smissen WJC, van der Vlugt-Daane M, van Galen A, Nik-Zainal S, Butler A, et al. The circular RNome of primary breast cancer. Genome Res. 2019;29:356-366.
Not in our library10.1101/gr.238121.118
224.
Sole C, Arnaiz E, Manterola L, Otaegui D, Lawrie CH. The circulating transcriptome as a source of cancer liquid biopsy biomarkers. Semin Cancer Biol. 2019;58:100-108.
Not in our library10.1016/j.semcancer.2019.01.003
225.
Song R, Bai Y, Li X, Zhu J, Zhang H, Shi Y, Li K, Wang B, Zhang H, Yang Y, et al. Plasma circular RNA DYM related to major depressive disorder and rapid antidepressant effect treated by visual cortical repetitive transcranial magnetic stimulation. J Affect Disord. 2020;274:486-493.
Not in our library10.1016/j.jad.2020.05.109
226.
Sonnenschein K, Wilczek A, de Gonzalo-Calvo D, Pfanne A, Derda A, Zwadlo C, Bavendiek U, Bauersachs J, Fiedler J, Thum T. Serum circular RNAs act as blood-based biomarkers for hypertrophic obstructive cardiomyopathy. Sci Rep. 2019;9:20350.
Not in our library10.1038/s41598-019-56617-2
227.
Stark R, Grzelak M, Hadfield J. RNA sequencing: the teenage years. Nat Rev Genet. 2019;20:1-26.
Not in our library10.1038/s41576-019-0150-2
228.
Exon Circularization Requires Canonical Splice Signals · 2015
Not checked
229.
Circular RNAs in Cancer: emerging functions in hallmarks, stemness, resistance and roles as potential biomarkers · 2019
No notice
230.
Sun J-Y, Shi Y, Cai X-Y, Liu J. Potential diagnostic and therapeutic value of circular RNAs in cardiovascular diseases. Cell Signal. 2020;71:109604.
Not in our library10.1016/j.cellsig.2020.109604
231.
Sun X-H, Wang Y-T, Li G-F, Zhang N, Fan L. Serum-derived three-circRNA signature as a diagnostic biomarker for hepatocellular carcinoma. Cancer Cell Int. 2020;20:226.
Not in our library10.1186/s12935-020-01302-y
232.
Sun Y, Jiang X, Lv Y, Liang X, Zhao B, Bian W, Zhang D, Jiang J, Zhang C. Circular RNA expression profiles in plasma from patients with heart failure related to platelet activity. Biomolecules. 2020;10(2):187.
Not in our library10.3390/biom10020187
233.
Surinova S, Radová L, Choi M, Srovnal J, Brenner H, Vitek O, Hajdúch M, Aebersold R. Non-invasive prognostic protein biomarker signatures associated with colorectal cancer. EMBO Mol Med. 2015;7:1153-1165.
Not in our library10.15252/emmm.201404874
234.
A community approach to mortality prediction in sepsis via gene expression analysis · 2018
No notice
235.
Statistically based splicing detection reveals neural enrichment and tissue-specific induction of circular RNA during human fetal development · 2015
Corrected
236.
Szabo L, Salzman J. Detecting circular RNAs: bioinformatic and experimental challenges. Nat Rev Genet. 2016;17:679-692.
Not in our library10.1038/nrg.2016.114
237.
Tan S, Gou Q, Pu W, Guo C, Yang Y, Wu K, Liu Y, Liu L, Wei Y-Q, Peng Y. Circular RNA F-circEA produced from EML4-ALK fusion gene as a novel liquid biopsy biomarker for non-small cell lung cancer. Cell Res. 2018;28:693-695.
Not in our library10.1038/s41422-018-0033-7
238.
CircRNA microarray profiling identifies a novel circulating biomarker for detection of gastric cancer · 2018
No notice
239.
Tang X, Liu S, Ding Y, Guo C, Guo J, Hua K, Qiu J. Serum circular FoxO3a serves as a novel prognostic biomarker in squamous cervical cancer. Cancer Manag Res. 2020;12:2531-2540.
Not in our library10.2147/cmar.s243329
240.
Tao X, Shao Y, Lu R, Ye Q, Xiao B, Ye G, Guo J. Clinical significance of hsa_circ_0000419 in gastric cancer screening and prognosis estimation. Pathol Res Pract. 2020;216:152763.
Not in our library10.1016/j.prp.2019.152763
241.
Teng L, Chen Y, Chen H, He X, Wang J, Peng Y, Duan H, Li H, Lin D, Shao B. Circular RNA hsa_circ_0021001 in peripheral blood: a potential novel biomarker in the screening of intracranial aneurysm. Oncotarget. 2017;8:107125-107133.
Not in our library10.18632/oncotarget.22349
242.
Torrano V, Royo F, Peinado H, Loizaga-Iriarte A, Unda M, Falcón-Perez JM, Carracedo A. Vesicle-MaNiA: extracellular vesicles in liquid biopsy and cancer. Curr Opin Pharmacol. 2016;29:47-53.
Not in our library10.1016/j.coph.2016.06.003
243.
Tsalik EL, Henao R, Nichols M, Burke T, Ko ER, McClain MT, Hudson LL, Mazur A, Freeman DH, Veldman T, et al. Host gene expression classifiers diagnose acute respiratory illness etiology. Sci Transl Med. 2016;8:322ra311.
Not in our library10.1126/scitranslmed.aad6873
244.
Turchinovich A, Weiz L, Langheinz A, Burwinkel B. Characterization of extracellular circulating microRNA. Nucleic Acids Res. 2011;39:7223-7233.
Not in our library10.1093/nar/gkr254
245.
Valk PJM, Verhaak RGW, Beijen MA, Erpelinck CAJ, van Doorn-Khosrovani SBvW, Boer JM, Beverloo HB, Moorhouse MJ, van der Spek PJ, Löwenberg B, et al. Prognostically useful gene-expression profiles in acute myeloid leukemia. N Engl J Med. 2004;350:1617-1628.
Not in our library10.1056/nejmoa040465
246.
van Heesch S, Witte F, Schneider-Lunitz V, Schulz JF, Adami E, Faber AB, Kirchner M, Maatz H, Blachut S, Sandmann C-L, et al. The translational landscape of the human heart. Cell. 2019;178(1):242-260.
Not in our library10.1016/j.cell.2019.05.010
247.
Vargas AJ, Harris CC. Biomarker development in the precision medicine era: lung cancer as a case study. Nat Rev Cancer. 2016;16:525-537.
Not in our library10.1038/nrc.2016.56
248.
Vargas J, Lima JA, Kraus WE, Douglas PS, Rosenberg S. Use of the Corus® CAD gene expression test for assessment of obstructive coronary artery disease likelihood in symptomatic non-diabetic patients. PLoS Curr. 2013.
Not in our library10.1371/currents.eogt.0f04f6081905998fa92b99593478aeab
249.
Vausort M, Salgado-Somoza A, Zhang L, Leszek P, Scholz M, Teren A, Burkhardt R, Thiery J, Wagner DR, Devaux Y. Myocardial infarction-associated circular RNA predicting left ventricular dysfunction. J Am Coll Cardiol. 2016;68:1247-1248.
Not in our library10.1016/j.jacc.2016.06.040
250.
Spatio-temporal regulation of circular RNA expression during porcine embryonic brain development · 2015
No notice
251.
Vicens Q, Westhof E. Biogenesis of circular RNAs. Cell. 2014;159:13-14.
Not in our library10.1016/j.cell.2014.09.005
252.
Vo JN, Cieslik M, Zhang Y, Shukla S, Xiao L, Zhang Y, Wu Y-M, Dhanasekaran SM, Engelke CG, Cao X, et al. The landscape of circular RNA in cancer. Cell. 2019;176:869-881.e813.
Not in our library10.1016/j.cell.2018.12.021
253.
Wan JCM, Massie C, Garcia-Corbacho J, Mouliere F, Brenton JD, Caldas C, Pacey S, Baird R, Rosenfeld N. Liquid biopsies come of age: towards implementation of circulating tumour DNA. Nat Rev Cancer. 2017;17:223-238.
Not in our library10.1038/nrc.2017.7
254.
Wang Y, Wang Z. Efficient backsplicing produces translatable circular mRNAs. RNA. 2015;21:172-179.
Not in our library10.1261/rna.048272.114
255.
Circular RNA Is Expressed across the Eukaryotic Tree of Life · 2014
Corrected
256.
Wang YM, Huang LM, Li DR, Shao JH, Xiong SL, Wang CM, Lu SM. Hsa_circ_0101996 combined with hsa_circ_0101119 in peripheral whole blood can serve as the potential biomarkers for human cervical squamous cell carcinoma. Int J Clin Exp Pathol. 2017;10:11924-11931.
Not in our library
257.
Wang Z-Y, Guo Z-D, Li J-M, Zhao Z-Z, Fu Y-Y, Zhang C-M, Zhang Y, Liu L-N, Qian J, Liu L-N. Genome-wide search for competing endogenous RNAs responsible for the effects induced by Ebola virus replication and transcription using a trVLP system. Front Cell Infect Microbiol. 2017;7:479.
Not in our library10.3389/fcimb.2017.00479
258.
Wang L, Shen C, Wang Y, Zou T, Zhu H, Lu X, Li L, Yang B, Chen J, Chen S, et al. Identification of circular RNA hsa_circ_0001879 and hsa_circ_0004104 as novel biomarkers for coronary artery disease. Atherosclerosis. 2019;286:88-96.
Not in our library10.1016/j.atherosclerosis.2019.05.006
259.
Wang Q, Zhang Q, Sun H, Tang W, Yang L, Xu Z, Liu Z, Jin H, Cao X. Circ-TTC17 promotes proliferation and migration of esophageal squamous cell carcinoma. Dig Dis Sci. 2019;64:751-758.
Not in our library10.1007/s10620-018-5382-z
260.
Wang W, Dong R, Guo Y, He J, Shao C, Yi P, Yu F, Gu D, Zheng J. CircMTO1 inhibits liver fibrosis via regulation of miR-17-5p and Smad7. J Cell Mol Med. 2019;23:5486-5496.
Not in our library10.1111/jcmm.14432
261.
Wang W, Wang J, Zhang X, Liu G. Serum circSETDB1 is a promising biomarker for predicting response to platinum-taxane-combined chemotherapy and relapse in high-grade serous ovarian cancer. Onco Targets Ther. 2019;12:7451-7457.
Not in our library10.2147/ott.s220700
262.
Exosomal circRNAs: biogenesis, effect and application in human diseases · 2019
No notice
263.
Wang Y, Wu C, Zhang F, Zhang Y, Ren Z, Lammi MJ, Guo X. Screening for differentially expressed circular RNAs in the cartilage of osteoarthritis patients for their diagnostic value. Genet Test Mol Biomark. 2019;23:706-716.
Not in our library10.1089/gtmb.2019.0108
264.
Wang J, Kong J, Nie Z, Chen D, Qiang J, Gao W, Chen X. Circular RNA hsa_circ_0066755 as an oncogene via sponging miR-651 and as a promising diagnostic biomarker for nasopharyngeal carcinoma. Int J Med Sci. 2020;17:1499-1507.
Not in our library10.7150/ijms.47024
265.
circRNA-002178 act as a ceRNA to promote PDL1/PD1 expression in lung adenocarcinoma · 2020
No notice
266.
Wang Q, Liu H, Liu Z, Yang L, Zhou J, Cao X, Sun H. Circ-SLC7A5, a potential prognostic circulating biomarker for detection of ESCC. Cancer Genet. 2020;240:33-39.
Not in our library10.1016/j.cancergen.2019.11.001
267.
Wang W, Li Y, Li X, Liu B, Han S, Li X, Zhang B, Li J, Sun S. Circular RNA circ-FOXP1 induced by SOX9 promotes hepatocellular carcinoma progression via sponging miR-875-3p and miR-421. Biomed Pharmacother. 2020;121:109517.
Not in our library10.1016/j.biopha.2019.109517
268.
Wang Y, Wu C, Zhang Y, Yang Y, Ren Z, Lammi MJ, Guo X. Screening for differentially expressed circRNA between Kashin-Beck disease and osteoarthritis patients based on circRNA chips. Clin Chim Acta. 2020;501:92-101.
Not in our library10.1016/j.cca.2019.10.026
269.
Host-response-based gene signatures for tuberculosis diagnosis: A systematic comparison of 16 signatures · 2019
No notice
270.
Weng W, Wei Q, Toden S, Yoshida K, Nagasaka T, Fujiwara T, Cai S, Qin H, Ma Y, Goel A. Circular RNA ciRS-7—a promising prognostic biomarker and a potential therapeutic target in colorectal cancer. Clin Cancer Res. 2017;23:3918-3928.
Not in our library10.1158/1078-0432.ccr-16-2541
271.
Westholm JO, Miura P, Olson S, Shenker S, Joseph B, Sanfilippo P, Celniker SE, Graveley BR, Lai EC. Genome-wide analysis of Drosophila circular RNAs reveals their structural and sequence properties and age-dependent neural accumulation. Cell Rep. 2014;9:1966-1980.
Not in our library10.1016/j.celrep.2014.10.062
272.
Wilusz JE. Repetitive elements regulate circular RNA biogenesis. Mob Genet Elem. 2015;5:39-45.
Not in our library10.1080/2159256x.2015.1045682
273.
Wu H, Yang L, Chen L-L. The diversity of long noncoding RNAs and their generation. Trends Genet. 2017;33:540-552.
Not in our library10.1016/j.tig.2017.05.004
274.
Wu N, Jin L, Cai J. Profiling and bioinformatics analyses reveal differential circular RNA expression in hypertensive patients. Clin Exp Hypertens. 2017;39:454-459.
Not in our library10.1080/10641963.2016.1273944
275.
Wu J, Li J, Liu H, Yin J, Zhang M, Yu Z, Miao H. Circulating plasma circular RNAs as novel diagnostic biomarkers for congenital heart disease in children. J Clin Lab Anal. 2019;33:e22998.
Not in our library10.1002/jcla.22998
276.
Wu J, Zhou Q, Niu Y, Chen J, Zhu Y, Ye S, Xi Y, Wang F, Qiu H, Bu S. Aberrant expression of serum circANRIL and hsa_circ_0123996 in children with Kawasaki disease. J Clin Lab Anal. 2019;33:e22874.
Not in our library10.1002/jcla.22874
277.
CircAtlas: an integrated resource of one million highly accurate circular RNAs from 1070 vertebrate transcriptomes · 2020
No notice
278.
Wu WP, Pan YH, Cai MY, Cen JM, Chen C, Zheng L, Liu X, Xiong XD. Plasma-derived exosomal circular RNA hsa_circ_0005540 as a novel diagnostic biomarker for coronary artery disease. Dis Markers. 2020;2020:3178642.
Not in our library10.1155/2020/3178642
279.
Wu Z, Sun H, Liu W, Zhu H, Fu J, Yang C, Fan L, Wang L, Liu Y, Xu W, et al. Circ-RPL15: a plasma circular RNA as novel oncogenic driver to promote progression of chronic lymphocytic leukemia. Leukemia. 2020;34:919-923.
Not in our library10.1038/s41375-019-0594-6
280.
A novel tumor suppressor protein encoded by circular AKT3 RNA inhibits glioblastoma tumorigenicity by competing with active phosphoinositide-dependent Kinase-1 · 2019
Corrected
281.
Xiao M-S, Ai Y, Wilusz JE. Biogenesis and functions of circular RNAs come into focus. Trends Cell Biol. 2020;30(3):226-240.
Not in our library10.1016/j.tcb.2019.12.004
282.
Exosomal circSHKBP1 promotes gastric cancer progression via regulating the miR-582-3p/HUR/VEGF axis and suppressing HSP90 degradation · 2020
No notice
283.
Xie R, Zhang Y, Zhang J, Li J, Zhou X. The role of circular RNAs in immune-related diseases. Front Immunol. 2020;11:545.
Not in our library10.3389/fimmu.2020.00545
284.
Xie Y, Li J, Li P, Li N, Zhang Y, Binang H, Zhao Y, Duan W, Chen Y, Wang Y, et al. RNA-Seq profiling of serum exosomal circular RNAs reveals circ-PNN as a potential biomarker for human colorectal cancer. Front Oncol. 2020;10:982.
Not in our library10.3389/fonc.2020.00982
285.
Circular RNA Expression Profiling and the Potential Role of hsa_circ_0089172 in Hashimoto’s Thyroiditis via Sponging miR125a-3p · 2019
Not checked
286.
The circular RNA Cdr1as, via miR-7 and its targets, regulates insulin transcription and secretion in islet cells · 2015
No notice
287.
Xu H, Gong Z, Shen Y, Fang Y, Zhong S. Circular RNA expression in extracellular vesicles isolated from serum of patients with endometrial cancer. Epigenomics. 2018;10:187-197.
Not in our library10.2217/epi-2017-0109
288.
Xu Z, Li P, Fan L, Wu M. The potential role of circRNA in tumor immunity regulation and immunotherapy. Front Immunol. 2018;9:9.
Not in our library10.3389/fimmu.2018.00009
289.
Xu M, Xie F, Tang X, Wang T, Wang S. Insights into the role of circular RNA in macrophage activation and fibrosis disease. Pharmacol Res. 2020;156:104777.
Not in our library10.1016/j.phrs.2020.104777
290.
Xu Y, Leng K, Yao Y, Kang P, Liao G, Han Y, Shi G, Ji D, Huang P, Zheng W, et al. A novel circular RNA, circ-CCAC1, contributes to CCA progression, induces angiogenesis, and disrupts vascular endothelial barriers. Hepatology. 2020.
Not in our library10.1002/hep.31493
291.
Stem cell-derived exosomes prevent pyroptosis and repair ischemic muscle injury through a novel exosome/circHIPK3/ FOXO3a pathway · 2020
No notice
292.
Yang F, Liu DY, Guo JT, Ge N, Zhu P, Liu X, Wang S, Wang GX, Sun SY. Circular RNA circ-LDLRAD3 as a biomarker in diagnosis of pancreatic cancer. World J Gastroenterol. 2017;23:8345-8354.
Not in our library10.3748/wjg.v23.i47.8345
293.
Yang Q, Du WW, Wu N, Yang W, Awan F, Fang L, Ma J, Li X, Zeng Y, Yang Z, et al. A circular RNA promotes tumorigenesis by inducing c-myc nuclear translocation. Cell Death Differ. 2017;24(9):1609-1620.
Not in our library10.1038/cdd.2017.86
294.
Extensive translation of circular RNAs driven by N6-methyladenosine · 2017
No notice
295.
Yang L, Fu J, Zhou Y. Circular RNAs and their emerging roles in immune regulation. Front Immunol. 2018;9:2977.
Not in our library10.3389/fimmu.2018.02977
296.
Yang X, Li J, Wu Y, Ni B, Zhang B. Aberrant dysregulated circular RNAs in the peripheral blood mononuclear cells of patients with rheumatoid arthritis revealed by RNA sequencing: novel diagnostic markers for RA. Scand J Clin Lab Investig. 2019;79:551-559.
Not in our library10.1080/00365513.2019.1674004
297.
Yao G, Niu W, Zhu X, He M, Kong L, Chen S, Zhang L, Cheng Z. hsa_circRNA_104597: a novel potential diagnostic and therapeutic biomarker for schizophrenia. Biomark Med. 2019;13:331-340.
Not in our library10.2217/bmm-2018-0447
298.
Ye DX, Wang SS, Huang Y, Chi P. A 3-circular RNA signature as a noninvasive biomarker for diagnosis of colorectal cancer. Cancer Cell Int. 2019;19:276.
Not in our library10.1186/s12935-019-0995-7
299.
Yi Z, Gao K, Li R, Fu Y. Dysregulated circRNAs in plasma from active tuberculosis patients. J Cell Mol Med. 2018;22:4076-4084.
Not in our library10.1111/jcmm.13684
300.
Yin WB, Yan MG, Fang X, Guo JJ, Xiong W, Zhang RP. Circulating circular RNA hsa_circ_0001785 acts as a diagnostic biomarker for breast cancer detection. Clin Chim Acta. 2018;487:363-368.
Not in our library10.1016/j.cca.2017.10.011
301.
Yoshimoto R, Rahimi K, Hansen T, Kjems J, Mayeda A (2019) Biosynthesis of circular RNA ciRS-7/CDR1as is mediated by mammalian-wide interspersed repeats (MIRs). Biorxiv 411231
Not in our library10.1016/j.isci.2020.101345
302.
You X, Vlatkovic I, Babic A, Will T, Epstein I, Tushev G, Akbalik G, Wang M, Glock C, Quedenau C. Neural circular RNAs are derived from synaptic genes and regulated by development and plasticity. Nat Neurosci. 2015;18:603-610.
Not in our library10.1038/nn.3975
303.
The circular RNA circBIRC6 participates in the molecular circuitry controlling human pluripotency · 2017
No notice
304.
Yu M, Bardia A, Wittner BS, Stott SL, Smas ME, Ting DT, Isakoff SJ, Ciciliano JC, Wells MN, Shah AM, et al. Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition. Science. 2013;339:580-584.
Not in our library10.1126/science.1228522
305.
Zaas AK, Chen M, Varkey J, Veldman T, Hero AO, Lucas J, Huang Y, Turner R, Gilbert A, Lambkin-Williams R, et al. Gene expression signatures diagnose Influenza and other symptomatic respiratory viral infections in humans. Cell Host Microbe. 2009;6:207-217.
Not in our library10.1016/j.chom.2009.07.006
306.
Zak DE, Penn-Nicholson A, Scriba TJ, Thompson E, Suliman S, Amon LM, Mahomed H, Erasmus M, Whatney W, Hussey GD, et al. A blood RNA signature for tuberculosis disease risk: a prospective cohort study. Lancet. 2016;387:2312-2322.
Not in our library10.1016/s0140-6736(15)01316-1
307.
Zaporozhchenko IA, Ponomaryova AA, Rykova EY, Laktionov PP. The potential of circulating cell-free RNA as a cancer biomarker: challenges and opportunities. Expert Rev Mol Diagn. 2018;18:133-145.
Not in our library10.1080/14737159.2018.1425143
308.
Non-invasive detection of human cardiomyocyte death using methylation patterns of circulating DNA · 2018
No notice
309.
Zhang Y, Zhang XO, Chen T, Xiang JF, Yin QF, Xing YH, Zhu S, Yang L, Chen LL. Circular intronic long noncoding RNAs. Mol Cell. 2013;51:792-806.
Not in our library10.1016/j.molcel.2013.08.017
310.
Zhang X-O, Wang H-B, Zhang Y, Lu X, Chen L-L, Yang L. Complementary sequence-mediated exon circularization. Cell. 2014;159:134-147.
Not in our library10.1016/j.cell.2014.09.001
311.
Zhang YG, Yang HL, Long Y, Li WL. Circular RNA in blood corpuscles combined with plasma protein factor for early prediction of pre-eclampsia. BJOG. 2016;123:2113-2118.
Not in our library10.1111/1471-0528.13897
312.
Zhang Y, Li J, Yu J, Liu H, Shen Z, Ye G, Mou T, Qi X, Li G. Circular RNAs signature predicts the early recurrence of stage III gastric cancer after radical surgery. Oncotarget. 2017;8:22936-22943.
Not in our library10.18632/oncotarget.15288
313.
Zhang C, Wang X, Chen Y, Wu Z, Zhang C, Shi W. The down-regulation of hsa_circ_0012919, the sponge for miR-125a-3p, contributes to DNA methylation of CD11a and CD70 in CD4(+) T cells of systemic lupus erythematous. Clin Sci (Lond). 2018;132:2285-2298.
Not in our library10.1042/cs20180403
314.
Exosome circRNA secreted from adipocytes promotes the growth of hepatocellular carcinoma by targeting deubiquitination-related USP7 · 2018
Retracted
315.
Zhang J, Xu Y, Xu S, Liu Y, Yu L, Li Z, Xue X, Wang H. Plasma circular RNAs, hsa_circRNA_025016, predict postoperative atrial fibrillation after isolated off-pump coronary artery bypass grafting. J Am Heart Assoc. 2018;7:e006642.
Not in our library
316.
A peptide encoded by circular form of LINC-PINT suppresses oncogenic transcriptional elongation in glioblastoma · 2018
No notice
317.
Zhang MY, Wang JB, Zhu ZW, Li LJ, Liu RS, Yang XK, Leng RX, Li XM, Pan HF, Ye DQ. Differentially expressed circular RNAs in systemic lupus erythematosus and their clinical significance. Biomed Pharmacother. 2018;107:1720-1727.
Not in our library10.1016/j.biopha.2018.08.161
318.
Zhang W, Yang S, Liu Y, Wang Y, Lin T, Li Y, Zhang R. Hsa_circ_0007534 as a blood-based marker for the diagnosis of colorectal cancer and its prognostic value. Int J Clin Exp Pathol. 2018;11:1399-1406.
Not in our library
319.
circRNA_104075 stimulates YAP-dependent tumorigenesis through the regulation of HNF4a and may serve as a diagnostic marker in hepatocellular carcinoma · 2018
No notice
320.
Zhang X, Zhou H, Jing W, Luo P, Qiu S, Liu X, Zhu M, Liang C, Yu M, Tu J. The circular RNA hsa_circ_0001445 regulates the proliferation and migration of hepatocellular carcinoma and may serve as a diagnostic biomarker. Dis Markers. 2018;2018:3073467.
Not in our library10.1155/2018/3073467
321.
Zhang Y, Zhang H, An M, Zhao B, Ding H, Zhang Z, He Y, Shang H, Han X. Crosstalk in competing endogenous RNA networks reveals new circular RNAs involved in the pathogenesis of early HIV infection. J Transl Med. 2018;16:332.
Not in our library10.1186/s12967-018-1706-1
322.
Zhang Z, Yang T, Xiao J. Circular RNAs: promising biomarkers for human diseases. EBioMedicine. 2018;34:267-274.
Not in our library10.1016/j.ebiom.2018.07.036
323.
Zhang J, Li J, Saucier JB, Feng Y, Jiang Y, Sinson J, McCombs AK, Schmitt ES, Peacock S, Chen S, et al. Non-invasive prenatal sequencing for multiple Mendelian monogenic disorders using circulating cell-free fetal DNA. Nat Med. 2019;25:1-9.
Not in our library10.1038/s41591-018-0334-x
324.
Zhang Y, Chen Y, Yao H, Lie Z, Chen G, Tan H, Zhou Y. Elevated serum circ_0068481 levels as a potential diagnostic and prognostic indicator in idiopathic pulmonary arterial hypertension. Pulm Circ. 2019;9:2045894019888416.
Not in our library10.1177/2045894019888416
325.
Cancer cell-derived exosomal circUHRF1 induces natural killer cell exhaustion and may cause resistance to anti-PD1 therapy in hepatocellular carcinoma · 2020
No notice
326.
Zhang S, Song G, Yuan J, Qiao S, Xu S, Si Z, Yang Y, Xu X, Wang A. Circular RNA circ_0003204 inhibits proliferation, migration and tube formation of endothelial cell in atherosclerosis via miR-370-3p/TGFbetaR2/phosph-SMAD3 axis. J Biomed Sci. 2020;27:11.
Not in our library10.1186/s12929-019-0595-9
327.
Peripheral blood circular RNA hsa_circ_0124644 can be used as a diagnostic biomarker of coronary artery disease · 2017
No notice
328.
Hsa_circ_0054633 in peripheral blood can be used as a diagnostic biomarker of pre-diabetes and type 2 diabetes mellitus · 2016
No notice
329.
Zhao K, Zhao Q, Guo Z, Chen Z, Hu Y, Su J, Chen L, He Z, Cai X, Chen M, et al. Hsa_circ_0001275: a potential novel diagnostic biomarker for postmenopausal osteoporosis. Cell Physiol Biochem. 2018;46:2508-2516.
Not in our library10.1159/000489657
330.
Zhao Q, Chen S, Li T, Xiao B, Zhang X. Clinical values of circular RNA 0000181 in the screening of gastric cancer. J Clin Lab Anal. 2018;32:e22333.
Not in our library10.1002/jcla.22333
331.
Zhao T, Zheng Y, Hao D, Jin X, Luo Q, Guo Y, Li D, Xi W, Xu Y, Chen Y, et al. Blood circRNAs as biomarkers for the diagnosis of community-acquired pneumonia. J Cell Biochem. 2019;120:16483-16494.
Not in our library10.1002/jcb.28863
332.
Circular RNA profiling reveals an abundant circHIPK3 that regulates cell growth by sponging multiple miRNAs · 2016
No notice
333.
Zheng S, Gu T, Bao X, Sun J, Zhao J, Zhang T, Zhang L. Circular RNA hsa_circ_0014243 may serve as a diagnostic biomarker for essential hypertension. Exp Ther Med. 2019;17:1728-1736.
Not in our library10.3892/etm.2018.7107
334.
Zheng S, He X, Sun J, Li Q, Zhang T, Zhang L. The up-regulated hsa-circRNA9102-5 may be a risk factor for essential hypertension. J Clin Lab Anal. 2020.
Not in our library10.1002/jcla.23339
335.
Zhou T, Xie X, Li M, Shi J, Zhou JJ, Knox KS, Wang T, Chen Q, Gu W. Rat BodyMap transcriptomes reveal unique circular RNA features across tissue types and developmental stages. RNA. 2018;24:1443-1456.
Not in our library10.1261/rna.067132.118
336.
Zhou X, Liu HY, Wang WY, Zhao H, Wang T. Hsa_circ_0102533 serves as a blood-based biomarker for non-small-cell lung cancer diagnosis and regulates apoptosis in vitro. Int J Clin Exp Pathol. 2018;11:4395-4404.
Not in our library
337.
Longitudinal multi-omics of host–microbe dynamics in prediabetes · 2019
No notice
338.
Roles of circular RNAs in immune regulation and autoimmune diseases · 2019
No notice
339.
Zhu X, Wang X, Wei S, Chen Y, Chen Y, Fan X, Han S, Wu G. hsa_circ_0013958: a circular RNA and potential novel biomarker for lung adenocarcinoma. FEBS J. 2017;284:2170-2182.
Not in our library10.1111/febs.14132
340.
Zhu K, Niu L, Wang J, Wang Y, Zhou J, Wang F, Cheng Y, Zhang Q, Li H. Circular RNA hsa_circ_0000885 levels are increased in tissue and serum samples from patients with osteosarcoma. Med Sci Monit. 2019;25:1499-1505.
Not in our library10.12659/msm.914899
341.
Zhu X, Ding J, Wang B, Wang J, Xu M. Circular RNA DLGAP4 is down-regulated and negatively correlates with severity, inflammatory cytokine expression and pro-inflammatory gene miR-143 expression in acute ischemic stroke patients. Int J Clin Exp Pathol. 2019;12:941-948.
Not in our library
342.
Zhuang Z-G, Zhang J-A, Luo H-L, Liu G-B, Lu Y-B, Ge N-H, Zheng B-Y, Li RX, Chen C, Wang X, et al. The circular RNA of peripheral blood mononuclear cells: Hsa_circ_0005836 as a new diagnostic biomarker and therapeutic target of active pulmonary tuberculosis. Mol Immunol. 2017;90:264-272.
Not in our library10.1016/j.molimm.2017.08.008
343.
Zuo L, Li C, Zu J, Yao H, Yan F. Circular RNA FUNDC1 improves prediction of stroke associated infection in acute ischemic stroke patients with high risk. Biosci Rep. 2020.
Not in our library10.1042/bsr20200902

Cited by papers we hold 4

Peripheral Blood Circular RNAs as a Biomarker for Major Depressive Disorder and Prediction of Possible Pathways · 2022
Not checked
Crosstalk between circRNAs and the PI3K/AKT signaling pathway in cancer progression · 2021
No notice
Analyses of circRNA and mRNA Profiles in Vogt–Koyanagi–Harada Disease · 2021
Not checked
CircIL4R activates the PI3K/AKT signaling pathway via the miR-761/TRIM29/PHLPP1 axis and promotes proliferation and metastasis in colorectal cancer · 2021
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