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Long noncoding RNAs: a potential novel class of cancer biomarkers

Aliaksandr A. Yarmishyn, Igor V. Kurochkin

Frontiers in Genetics · 2015 · Review

doi:10.3389/fgene.2015.00145

Abstract

Long noncoding RNAs (lncRNAs) are a novel class of RNA molecules defined as transcripts longer than 200 nucleotides that lack protein coding potential. They constitute a major, but still poorly characterized part of human transcriptome, however, evidence is growing that they are important regulatory molecules involved in various cellular processes. It is becoming increasingly clear that many lncRNAs are deregulated in cancer and some of them can be important drivers of malignant transformation. On the one hand, some lncRNAs can have highly specific expression in particular types of cancer making them a promising tool for diagnosis. The expression of other lncRNAs can correlate with different pathophysiological features of tumor growth and with patient survival, thus making them convenient biomarkers for prognosis. In this review we outline the current state of knowledge about the fast growing field of application of lncRNAs as tumor biomarkers.

Full text

From PubMed Central, U.S. National Library of Medicine, as current on Oct 19, 2026. Paragraph numbers are ours, so an answer can point at one.

Introduction

The development of high resolution microarray and genome wide sequencing technologies allowed comprehensive characterization of mammalian transcriptomes. The main conclusion from the pioneering in-depth transcriptome studies performed by FANTOM (Functional Annotation Of Mouse genome) and ENCODE (Encyclopedia of DNA Elements) consortia was discovery of the pervasive transcription of the mouse and human genomes with protein coding mRNAs constituting only a minor fraction of the transcribed sequences. The most recent data from ENCODE consortium indicates that around 70% of human genome is transcribed, generating a vast range of noncoding RNAs. Based on transcript size noncoding RNAs are classified into small noncoding RNAs (<200 nt) and long noncoding RNAs (lncRNAs; >200 nt). Small noncoding RNAs, particularly miRNAs are well characterized as post-transcriptional regulators of mRNAs and have well established roles in cancer.

On the other hand, lncRNAs still remain poorly characterized, however, evidence for their importance and functionality is mounting. The number of known lncRNA genes is still rising as the process of their annotation is ongoing. The current version of GENCODE (encyclopedia of genes and gene variants) includes 15,877 human lncRNA genes encoding 26,414 transcripts based on manual curation, computational analysis, and experimental validation (Version 21, June 2014 freeze, GRCh38 – Ensembl 77;; www.gencodegenes.org).

Long noncoding RNAs share common features with mRNAs, such as many of them are transcribed by RNA polymerase II, undergo splicing, polyadenylation, and 5′-capping (Table 1). Similarly, to protein coding genes, lncRNA genes have histone marks of active promoters (H3K4me2/3, H2K9ac, H3K27ac) and actively transcribed gene bodies (H3K36me3;; ). On the other hand, lncRNAs have several distinct features that distinguish them from protein coding mRNAs (Table 1). LncRNAs generally lack or have very little open reading frames (ORFs). Commonly, lncRNA transcripts are shorter and have fewer exons. Unlike mRNAs, which are mostly transported to the cytoplasm, the majority of lncRNAs are localized to the nucleus. LncRNAs demonstrate relatively lower expression levels than protein coding genes, however, they exhibit more specific tissue expression patterns.

Contrary to the initial view that lncRNAs might be a mere transcriptional noise, several lines of evidence indicate to their functionality. Firstly, many lncRNAs demonstrate clear signs of evolutionary conservation and selection. Secondly, expression of many lncRNAs is developmentally and temporally regulated and restricted to certain tissues. It is becoming increasingly clear that lncRNAs are important regulatory molecules acting at different levels of gene expression, such as chromatin remodeling, transcription, stability, posttranscriptional modifications, and translation. For example, lncRNAs Xist and HOTAIR (HOX transcript antisense RNA) recruit chromatin remodeling complexes, such as Polycomb repressive complex 2 (PRC2) to induce heterochromatin state, thus repressing gene expression at target loci (;; Figure 1). Indeed, a considerable proportion of lncRNAs has been shown to associate with PRC2 complex, implying that it might be one of the prevalent mechanisms for their functionality. LncRNAs directly regulate transcription by different mechanisms, such as via interaction with RNA binding proteins, repression of promoters, acting as co-activators of transcription factors, or negatively regulating transcription factors by sequestration. At the level of pre-mRNA processing, lncRNA MALAT1 can regulate alternative splicing by interacting with several serine/arginine (SR) splicing factors.

Long noncoding RNAs can interact with mRNAs and modulate their translation both positively and negatively. For example, lincRNA-p21 interacts with JUNB and CTNNB1 mRNAs and selectively lowers their translation through a mechanism that includes reduced polysome sizes or ribosome ‘drop-off’. In contrast, lncRNA antisense to Uchl1 gene increases translation of UCHL1 protein in a mechanism dependent on a 5′ overlapping sequence and an embedded inverted SINEB2 element in lncRNA. LncRNA can also regulate stability of target mRNAs through imperfect base pairing between an Alu element in the 3′ UTR of a Staufen 1 (STAU1)-mediated mRNA decay target and another Alu element in a cytoplasmic lncRNA. This imperfect base-pairing creates a lncRNA–mRNA duplex that binds STAU1 resulting in degradation of mRNA.

With the growing evidence of lncRNA functionality it is of no surprise that they are implicated in diverse pathologic conditions, including cancer. Various lncRNAs have been found to be differentially expressed in cancer and their enforced expression or knock down could result in altered phenotypical responses related to malignant transformation, such as changes in proliferation, invasive potential, or apoptosis. Similarly, to protein coding genes, lncRNAs can be classified into oncogenes and tumor suppressors. This opens opportunities for application of lncRNAs as biomarkers for cancer diagnosis and prognosis. Indeed, the functions of lncRNAs are more likely to correlate with their abundance as they do not encode proteins, making them highly suitable as biomarkers. In this review, we summarize the current knowledge about lncRNAs as potential diagnostic and prognostic biomarkers of cancer.

Diagnostic Cancer Biomarkers

The tissue specific nature of expression of lncRNAs, which is generally higher than that of protein coding mRNAs, makes them potentially advantageous for identification of highly specific diagnostic biomarkers. Whereas some well known lncRNAs, such as HOTAIR are known to be deregulated in a wide spectrum of cancers, several lncRNAs have been described to be highly specific for a particular cancer type.

For example, expression of lncRNA PCA3 (Prostate Cancer Antigen 3) is highly restricted to prostate tissue. In the same study it was shown by differential display analysis that PCA3 is highly overexpressed in prostatic tumors in comparison with non-neoplastic prostatic tissue of the same patients. Moreover, its expression was not detected in other tumor types or cell lines. PCGEM1 is another lncRNA gene with highly prostate tissue-specific expression. Interestingly, its elevated expression was associated with high risk groups, such as the African–American population, which is more susceptible to prostate cancer as compared to Caucasian–American or those individuals with family history of prostate cancer as compared to those without family history. Another lncRNA, encoded in 8q24 locus reported to be associated with prostate cancer susceptibility in European and African–American populations, termed PRNCR1 (prostate cancer noncoding RNA 1), was shown to be up-regulated in some of the prostate cancer cells as well as precursor lesion prostatic intraepithelial neoplasia.

HULC (highly up-regulated in liver cancer) has been identified as highly up-regulated in hepatocellular carcinoma and colorectal carcinomas that produce liver metastases but not in the primary colon tumors or their non-liver metastases. Interestingly, the specific genetic variant rs7763881 in HULC was found to be associated with decreased risk of HCC in persistent carriers of HBV.

Detection of cancer at the early stages significantly gnosis is the screening for biomarkers by non-invasive methods, such as sampling of extracellular fluids. A fraction of DNA and RNA molecules referred to as circulating nucleic acids (CNAs) are found in blood serum and other extracellular fluids. Changes in the levels of CNAs are associated with tumor burden and malignant progression, thus pointing to their potential as tumor biomarkers easily detected by PCR assays. Several lncRNAs have been characterized as potential biomarkers in human body fluids. The most prominent example of such biomarkers is PCA3, a lncRNA highly expressed is prostate cancer. The detection of PCA3 in the urine has been demonstrated to be a more specific marker to diagnose prostate cancer than the commonly used prostate-specific antigen (PSA) and already found wide application in clinics. Similarly, UCA1 (urothelial carcinoma associated 1) transcript detected in urine was shown to be a highly sensitive and specific biomarker of bladder carcinoma. HULC was detected with high frequency in plasma of patients with hepatocellular carcinoma, making it a promising diagnostic biomarker for this type of cancer. Several other studies identify promising biomarkers for different types of cancer, such as MALAT1 derived fragment detected in plasma as a biomarker for prostate cancer, AA174084 found in gastric juice as indicator of gastric cancer, a set of salivary lncRNAs as potential markers for oral squamous cell carcinoma diagnosis.

Exosomes are nanovesicles secreted into the extracellular environment from the cells upon fusion of intracellular vesicles with the plasma membrane. The molecular content of exosomes replicates that of the releasing cell and reflects its status. The abundance of exosomes in body fluids and possibility to detect tumor specific material of their parental cancer cells makes exosomes a promising tool for non-invasive diagnostics. The content of exosomes comprises different kinds of RNA, including lncRNAs. Indeed, lncRNAs are highly enriched in exosomes compared to donor cells. For example, lncRNA TUC339 was found to be highly enriched in extracellular vesicles secreted from hepatocellular carcinoma cells where it modulated tumor cell growth and adhesion. LincRNA–ROR, another lncRNA from hepatocellular carcinoma derived extracellular vesicles was shown to modulate chemotherapeutic response in this type of cancer. Given the fact that most transcriptome studies aimed to identify biomarkers were focused on miRNAs, shifting the focus to more unbiased characterization that would include other types of transcripts present in cancer derived exosomes would potentially lead to discovery of more lncRNA based biomarkers.

Prognostic Cancer Biomarkers

Different lncRNAs were shown to be aberrantly expressed in cancer and correlate with tumorigenesis, tumor progression, and metastatic properties in various cancer conditions. Such lncRNA can be involved in both oncogenic and tumor suppressor pathways and their expression can correlate with good or bad prognosis, making them promising prognostic biomarkers (Table 2).

HOTAIR is one of the most well studied examples of lncRNA implicated in cancer. Initially it was identified by to be highly overexpressed in primary and metastatic breast cancer tissues as compared to normal breast epithelium. High HOTAIR expression level in primary tumors was shown to be a significant predictor of eventual metastasis and death. Enforced expression of HOTAIR in breast carcinoma cells induced genome wide retargeting of PRC2 and, as a result, altered H3K27 methylation and gene expression patterns, increased invasiveness, and metastasis. Interestingly, BRCA1, an important suppressor of breast cancer inhibits HOTAIR dependent PRC2 activity by competitive binding to its catalytic subunit EZH2. In another breast cancer study it was shown that HOTAIR is regulated by oestradiol in estrogen receptor dependent manner.

HOTAIR was also shown to be involved in hepatocellular carcinoma. Overexpression of HOTAIR in tumor tissues was reported to be associated with increased risk of recurrence after hepatectomy, as well as positively correlate with lymph node metastasis. Similarly, increased HOTAIR was shown to be prognostic factor of tumor recurrence following liver transplantation. In the same study, knock down of HOTAIR in HCC cell line reduced cell viability and invasion, as well as increased sensitivity to cisplatin and doxorubicin. Patients with overexpressed HOTAIR had poorer prognoses and larger tumor sizes, more rapid proliferation of tumor cells.

In colorectal carcinoma high expression of HOTAIR was also shown to correlate with poor prognosis and liver metastasis. Positive correlation between expression levels of HOTAIR, the members of PRC2 complex, Suz12, and Ezh2, and H3K27me3 chromatin marks suggests the role of HOTAIR in PRC2 mediated chromatin reprogramming in metastasis. Apart from the primary tumors, HOTAIR was also shown to be a negative prognostic factor in the blood of colorectal patients suggesting that measuring the HOTAIR blood levels may provide a minimally invasive test to identify patients with unfavorable prognosis. High expression of HOTAIR associated with advanced stage, lymphatic node metastasis and poor survival was also reported in gastric cancer. The increased expression level of HOTAIR positively correlates with Suz12, implying PRC2 dependent mechanism of epigenetic reprogramming in oncogenicity of gastric carcinoma. Also HOTAIR was shown to act as an endogenous sponge of miR-331-3p miRNA, thus abolishing repression of its target HER2, implicated in development of gastric cancer. In addition to the above described, HOTAIR was reported to be a negative prognosis biomarker for a number of other malignancies, such as pancreatic cancer, lung cancer, esophageal carcinoma, cervical cancer, and colon cancer. A meta-analysis study of prognostic capability of HOTAIR in different types of cancer revealed that it is a more reliable predictor of overall survival in patients with digestive system malignancies.

Another paradigmal case of lncRNA based cancer biomarkers is MALAT1 (Metastasis-associated Lung Adenocarcinoma Transcript 1). As its name implies, it was discovered as a predictive marker of metastasis development in early stage lung adenocarcinoma. In a MALAT1 knockout model of human lung cancer cells it was shown that MALAT1 regulates metastatic signature of genes. In such model metastatic capacities of lung adenocarcinoma mouse xenografts were significantly compromised. In the same study, targeting MALAT1 with antisense nucleotides significantly reduced metastasis making it an interesting target for therapy.

In hepatocellular carcinoma (HCC) MALAT1 overexpression is a predictive factor for tumor recurrence following liver transplantation. The depletion of MALAT1 by siRNA in HepG2 cell line resulted in reduction of cell viability, mobility and invasiveness, as well as increase of sensitivity to apoptosis. High expression of MALAT1 was shown to be a marker of poor postoperative prognosis in colorectal carcinoma. Moreover, the obvious oncogenic role of MALAT1 was demonstrated in a number of other cancer models, including bladder cancer, cervical cancer, uterine sarcoma, and osteosarcoma.

H19 is lncRNA expressed from the maternal allele that plays an important role in genomic imprinting during growth and development. Loss of imprinting at the H19 locus in paternal allele results in biallelic expression and, therefore, elevated H19 levels in a wide range of cancers. High expression of H19 was shown to be associated with a range of risk factors, such as smoking, exposure to carcinogens and hypoxia. Indeed, hypoxia causes up-regulation of H19 in cell lines with mutated p53. H19 is also directly induced by MYC oncogene in different cell lines. Further adding to the host of oncogenic pathways with the involvement of H19, it serves as a precursor of miR-675, miRNA that down-regulates RB1 tumor suppressor transcript in colorectal cancer.

NcRAN (noncoding RNA expressed in aggressive neuroblastoma) is encoded by a gene mapped to chromosome arm 17q, whose amplification is one of the most common genetic abnormalities associated with poor prognosis in neuroblastoma. Indeed, the high expression levels of ncRAN were significantly associated with poor prognosis of the neuroblastoma patients. In addition, ncRAN was found to be upregulated in bladder cancer as compared to normal tissues and confer a set of oncogenic properties, such as increased cell proliferation, migration, and invasion. In contrast, down-regulation of ncRAN was shown to be associated with metastatic properties and predict poor overall survival in colorectal carcinoma.

In addition to lncRNAs with pronounced oncogenic effects, which positively correlate with poor prognosis, a few lncRNAs have been characterized to act as tumor suppressors. One such example is GAS5 (growth arrest-specific 5), a tumor suppressor lncRNA which reduces growth, metabolism, and sensitizes cells to apoptosis by inhibiting glucocorticoid receptor. GAS5 is down-regulated in a number of cancers, such as breast cancer, renal cell carcinoma, pancreatic cancer, bladder cancer, non-small-cell lung cancer, gastric cancer, malignant pleural mesothelioma, hepatocellular carcinoma. Low level of GAS5 indicates a poor prognosis in cancer patients.

Another example of a tumor suppressor lncRNA is lincRNA-p21. This lncRNA was shown to be directly induced by p53 and play a crucial role in p53 mediated transcriptional response. Maternally expressed gene 3 (MEG3) is another prominent tumor suppressor lncRNA that acts by increasing p53 activity on specific transcription targets. Besides, MEG3 is able to inhibit cell proliferation in the absence of p53 suggesting that this lncRNA may act also via p53-independent pathway. Consistently, MEG3 is down-regulated in a number of cancers, including myeloid leukemia, pituitary adenoma, meningioma, and glioma.

In conclusion, lncRNAs may act both as oncogenes and tumor suppressors without obvious prevalence of one class over another. In this respect lncRNAs behave similarly, to protein-coding transcripts.

Prognostic Expression Signatures Based on lncRNAs

Characterizing tumor transcriptomes at the system’s level allows identification of molecular subtypes of cancer and development of predictive and prognostic gene expression signatures. Microarrays have been widely used for the past two decades in preclinical research to characterize tumor gene expression profiles on a genome-wide scale. Most of these signatures were based on protein coding genes as little was known about lncRNAs and their important roles in cancer. However, the widely used commercial microarray platforms in addition to protein coding mRNAs were designed to detect numerous ESTs and non-annotated RNAs. Many of these transcripts are now annotated as bona fide lncRNAs, therefore the vast collection of microarray datasets accumulated during the past two decades provides a valuable resource for identification of novel gene expression signatures and biomarkers based on lncRNAs. In our recent study we annotated probe sets detecting lncRNAs on widely used Affymetrix U133 series of microarray platforms by using two approaches: firstly by matching probe sets to Gencode database of lncRNAs and secondly by developing a stringent in silico protein coding potential prediction filter. Affymetrix U133 microarrays have been found to contain probe sets for the measurement of 1581 lncRNAs. Using this resource and previously deposited microarray-based data on expression profiling of neuroblastic tumors we identified 159 lncRNA signature that discriminates between localized and metastatic stages of neuroblastoma, as well as between relapsing and non-relapsing primary tumors. The data mining of Affymetrix U133 Plus datasets was also applied to identify lncRNA signatures associated with different histological subtypes and malignancy grades of glioma. In the follow up study, the six-lncRNA prognostic signature of glioma significantly associated with overall survival was identified. In another study the classification of glioma into three molecular subtypes based on lncRNA expression profiles was proposed. Similarly, using lncRNA mining approach, identified six lncRNA prognostic signature significantly associated with disease free survival in colorectal carcinoma. LncRNA-based expression profiles were also utilized to classify colorectal cancer samples into five distinct molecular subtypes, each characterized by distinct biological pathways and clinical outcome.

As high throughput sequencing technology becomes cheaper and more accessible we might expect the influx of de novo data from transcriptome sequencing and identification of new biomarkers and diagnostic signatures. For example, utilized RNA-Seq approach to identify 121 lncRNAs associated with prostate cancer progression in a cohort of 102 patients. One of these lncRNAs PCAT-1 was further characterized as a regulator of proliferation in prostate cancer cells. In a similar study the sequencing of transcriptomes of high and low risk neuroblastoma identified a set of differentially expressed lncRNAs. One of them NBAT-1 was characterized as a tumor suppressor, whose loss contributes to aggressive neuroblastoma by increasing proliferation and impairing differentiation. RNA-Seq analysis was also employed by to detect lncRNAs associated with lung cancer. In this study the transcriptome sequencing data from a cohort of 567 patients were used to identify 111 novel lncRNAs differentially regulated between tumor and adjacent normal tissue samples. Further meta-analysis revealed that a subset of these lncRNAs was deregulated in a broad range of tumors and another subset was highly deregulated specifically in lung cancers, making the latter a promising source of biomarkers.

Concluding Remarks

The last decade witnessed a vast expansion of knowledge regarding lncRNAs and their important roles in regulation of various biological processes and development of disease. A number of lncRNAs, such as HOTAIR, MALAT and H19 were found to be aberrantly expressed in a number of cancers and extensively characterized as important players affecting the hallmark events of carcinogenesis, such as proliferation, apoptosis, and metastasis. These examples demonstrate that lncRNAs, on par with protein coding genes and miRNAs, have a great potential to be used as cancer biomarkers. Indeed, since lncRNAs are implicated in cancer biology at the level of RNA unlike mRNAs, which represent an intermediate on the way to functioning protein, their levels of expression are more likely to correlate with cancer phenotypes. Also, since proteins and lncRNAs represent different regulatory realms, their combination might increase each other’s power as diagnostic and prognostic tools. It should be noted that the few examples described in this review are just a tip of the iceberg, as the field of lncRNAs is currently evolving and the work of annotation and characterization of lncRNAs is ongoing. With the deep sequencing technology becoming cheaper and more accessible one might expect an explosive growth of newly identified lncRNAs differentially expressed in cancers and associated with various clinical parameters.

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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    Khalil A. M. Guttman M. Huarte M. Garber M. Raj A. Rivea Morales D. (2009 ). Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression. Proc. Natl. Acad. Sci. U.S.A. 106 11667–11672

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    Kim H. T. Choi B. H. Niikawa N. Lee T. S. Chang S. I. (1998 ). Frequent loss of imprinting of the H19 and IGF-II genes in ovarian tumors. Am. J. Med. Genet. 80 391–395

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  46. 46.

    Kim K. Jutooru I. Chadalapaka G. Johnson G. Frank J. Burghardt R. (2013 ). HOTAIR is a negative prognostic factor and exhibits pro-oncogenic activity in pancreatic cancer. Oncogene 32 1616–1625

    Not in our library10.1038/onc.2012.193

  47. 47.

    Kim S. J. Park S. E. Lee C. Lee S. Y. Jo J. H. Kim J. M. (2002 ). Alterations in promoter usage and expression levels of insulin-like growth factor-II and H19 genes in cervical carcinoma exhibiting biallelic expression of IGF-II. Biochim. Biophys. Acta 1586 307–315

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  48. 48.

    Kino T. Hurt D. E. Ichijo T. Nader N. Chrousos G. P. (2010 ). Noncoding RNA gas5 is a growth arrest- and starvation-associated repressor of the glucocorticoid receptor. Sci. Signal. 3:ra8

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  49. 49.

    Kogo R. Shimamura T. Mimori K. Kawahara K. Imoto S. Sudo T. (2011 ). Long noncoding RNA HOTAIR regulates polycomb-dependent chromatin modification and is associated with poor prognosis in colorectal cancers. Cancer Res. 71 6320–6326

    Not in our library10.1158/0008-5472.can-11-1021

  50. 50.

    Kogure T. Yan I. K. Lin W. L. Patel T. (2013 ). Extracellular vesicle-mediated transfer of a novel long noncoding RNA TUC339: a mechanism of intercellular signaling in human hepatocellular cancer. Genes Cancer 4 261–272

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  51. 51.

    Kondo M. Suzuki H. Ueda R. Osada H. Takagi K. Takahashi T. (1995 ). Frequent loss of imprinting of the H19 gene is often associated with its overexpression in human lung cancers. Oncogene 10 1193–1198.

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  52. 52.

    Kong Y. W. Ferland-McCollough D. Jackson T. J. Bushell M. (2012 ). microRNAs in cancer management. Lancet Oncol. 13:e249–e258

    Not in our library10.1016/s1470-2045(12)70073-6

  53. 53.

    Lai M. C. Yang Z. Zhou L. Zhu Q. Q. Xie H. Y. Zhang F. (2012 ). Long noncoding RNA MALAT-1 overexpression predicts tumor recurrence of hepatocellular carcinoma after liver transplantation. Med. Oncol. 29 1810–1816

    Not in our library10.1007/s12032-011-0004-z

  54. 54.

    Lee G. L. Dobi A. Srivastava S. (2011 ). Prostate cancer: diagnostic performance of the PCA3 urine test. Nat. Rev. Urol. 8 123–124

    Not in our library10.1038/nrurol.2011.10

  55. 55.

    Li R. Qian J. Wang Y. Y. Zhang J. X. You Y. P. (2014 ). Long noncoding RNA profiles reveal three molecular subtypes in glioma. CNS Neurosci. Ther. 20 339–343

    Not in our library10.1111/cns.12220

  56. 56.
    The long non-coding RNA HOTAIR indicates a poor prognosis and promotes metastasis in non-small cell lung cancer · 2013
    No notice
  57. 57.
    Downregulation of GAS5 Promotes Bladder Cancer Cell Proliferation, Partly by Regulating CDK6 · 2013
    No notice
  58. 58.
    Lnc RNA HOTAIR functions as a competing endogenous RNA to regulate HER2 expression by sponging miR-331-3p in gastric cancer · 2014
    No notice
  59. 59.
    A Genetic Variant in Long Non-Coding RNA HULC Contributes to Risk of HBV-Related Hepatocellular Carcinoma in a Chinese Population · 2012
    No notice
  60. 60.

    Lottin S. Adriaenssens E. Dupressoir T. Berteaux N. Montpellier C. Coll J. (2002 ). Overexpression of an ectopic H19 gene enhances the tumorigenic properties of breast cancer cells. Carcinogenesis 23 1885–1895

    Not in our library10.1093/carcin/23.11.1885

  61. 61.

    Lu X. Fang Y. Wang Z. Xie J. Zhan Q. Deng X. (2013 ). Downregulation of gas5 increases pancreatic cancer cell proliferation by regulating CDK6. Cell Tissue Res. 354 891–896

    Not in our library10.1007/s00441-013-1711-x

  62. 62.
    Long Noncoding RNA HOTAIR Is a Prognostic Marker for Esophageal Squamous Cell Carcinoma Progression and Survival · 2013
    No notice
  63. 63.

    Martianov I. Ramadass A. Serra Barros A. Chow N. Akoulitchev A. (2007 ). Repression of the human dihydrofolate reductase gene by a noncoding interfering transcript. Nature 445 666–670

    Not in our library10.1038/nature05519

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    Matouk I. J. Abbasi I. Hochberg A. Galun E. Dweik H. Akkawi M. (2009 ). Highly upregulated in liver cancer noncoding RNA is overexpressed in hepatic colorectal metastasis. Eur. J. Gastroenterol. Hepatol. 21 688–692

    Not in our library10.1097/meg.0b013e328306a3a2

  65. 65.
    The H19 Non-Coding RNA Is Essential for Human Tumor Growth · 2007
    No notice
  66. 66.

    Matouk I. J. Mezan S. Mizrahi A. Ohana P. Abu-Lail R. Fellig Y. (2010 ). The oncofetal H19 RNA connection: hypoxia, p53 and cancer. Biochim. Biophys. Acta 1803 443–451

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    Mercer T. R. Dinger M. E. Sunkin S. M. Mehler M. F. Mattick J. S. (2008 ). Specific expression of long noncoding RNAs in the mouse brain. Proc. Natl. Acad. Sci. U.S.A. 105 716–721

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    Mourtada-Maarabouni M. Pickard M. R. Hedge V. L. Farzaneh F. Williams G. T. (2009 ). GAS5 a non-protein-coding RNA, controls apoptosis and is downregulated in breast cancer. Oncogene 28 195–208

    Not in our library10.1038/onc.2008.373

  69. 69.

    Müller S. Zirkel D. Westphal M. Zumkeller W. (2000 ). Genomic imprinting of IGF2 and H19 in human meningiomas. Eur. J. Cancer 36 651–655

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  70. 70.

    Nakagawa T. Endo H. Yokoyama M. Abe J. Tamai K. Tanaka N. (2013 ). Large noncoding RNA HOTAIR enhances aggressive biological behavior and is associated with short disease-free survival in human non-small cell lung cancer. Biochem. Biophys. Res. Commun. 436 319–324

    Not in our library10.1016/j.bbrc.2013.05.101

  71. 71.

    Okazaki Y. Furuno M. Kasukawa T. Adachi J. Bono H. Kondo S. (2002 ). Analysis of the mouse transcriptome based on functional annotation of 60770 full-length cDNAs. Nature 420 563–573

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  72. 72.

    Pandey G. K. Mitra S. Subhash S. Hertwig F. Kanduri M. Mishra K. (2014 ). The risk-associated long noncoding RNA NBAT-1 controls neuroblastoma progression by regulating cell proliferation and neuronal differentiation. Cancer Cell 26 722–737

    Not in our library10.1016/j.ccell.2014.09.014

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    Panzitt K. Tschernatsch M. M. Guelly C. Moustafa T. Stradner M. Strohmaier H. M. (2007 ). Characterization of HULC, a novel gene with striking up-regulation in hepatocellular carcinoma, as noncoding RNA. Gastroenterology 132 330–342

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  74. 74.

    Petrovics G. Zhang W. Makarem M. Street J. P. Connelly R. Sun L. (2004 ). Elevated expression of PCGEM1 a prostate-specific gene with cell growth-promoting function, is associated with high-risk prostate cancer patients. Oncogene 23 605–611

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  75. 75.

    Ponjavic J. Ponting C. P. Lunter G. (2007 ). Functionality or transcriptional noise? Evidence for selection within long noncoding RNAs. Genome Res. 17 556–565

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  76. 76.

    Ponting C. P. Belgard T. G. (2010 ). Transcribed dark matter: meaning or myth? Hum. Mol. Genet. 19 R162–R168

    Not in our library10.1093/hmg/ddq362

  77. 77.

    Prensner J. R. Iyer M. K. Balbin O. A. Dhanasekaran S. M. Cao Q. Brenner J. C. (2011 ). Transcriptome sequencing across a prostate cancer cohort identifies PCAT-1 an unannotated lincRNA implicated in disease progression. Nat. Biotechnol. 29 742–749

    Not in our library10.1038/nbt.1914

  78. 78.

    Properzi F. Logozzi M. Fais S. (2013 ). Exosomes: the future of biomarkers in medicine. Biomark. Med. 7 769–778

    Not in our library10.2217/bmm.13.63

  79. 79.

    Qi P. Xu M. D. Ni S. J. Shen X. H. Wei P. Huang D. (2014 ). Down-regulation of ncRAN, a long noncoding RNA, contributes to colorectal cancer cell migration and invasion and predicts poor overall survival for colorectal cancer patients. Mol. Carcinog. 9 1039–1045

    Not in our library10.1002/mc.22137

  80. 80.

    Qiao H. P. Gao W. S. Huo J. X. Yang Z. S. (2013 ). Long noncoding RNA GAS5 functions as a tumor suppressor in renal cell carcinoma. Asian Pac. J. Cancer Prev. 14 1077–1082

    Not in our library10.7314/apjcp.2013.14.2.1077

  81. 81.

    Raposo G. Stoorvogel W. (2013 ). Extracellular vesicles: exosomes, microvesicles, and friends. J. Cell Biol. 200 373–383

    Not in our library10.1083/jcb.201211138

  82. 82.

    Ravasi T. Suzuki H. Pang K. C. Katayama S. Furuno M. Okunishi R. (2006 ). Experimental validation of the regulated expression of large numbers of noncoding RNAs from the mouse genome. Genome Res. 16 11–19

    Not in our library10.1101/gr.4200206

  83. 83.

    Ren S. Wang F. Shen J. Sun Y. Xu W. Lu J. (2013 ). Long noncoding RNA metastasis associated in lung adenocarcinoma transcript 1 derived miniRNA as a novel plasma-based biomarker for diagnosing prostate cancer. Eur. J. Cancer 49 2949–2959

    Not in our library10.1016/j.ejca.2013.04.026

  84. 84.

    Renganathan A. Kresoja-Rakic J. Echeverry N. Ziltener G. Vrugt B. Opitz I. (2014 ). GAS5 long noncoding RNA in malignant pleural mesothelioma. Mol. Cancer 13:119

    Not in our library10.1186/1476-4598-13-119

  85. 85.

    Rinn J. L. Kertesz M. Wang J. K. Squazzo S. L. Xu X. Brugmann S. A. (2007 ). Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 129 1311–1323

    Not in our library10.1016/j.cell.2007.05.022

  86. 86.

    Schwarzenbach H. Hoon D. S. Pantel K. (2011 ). Cell-free nucleic acids as biomarkers in cancer patients. Nat. Rev. Cancer 11 426–437

    Not in our library10.1038/nrc3066

  87. 87.

    Shao Y. Ye M. Jiang X. Sun W. Ding X. Liu Z. (2014 ). Gastric juice long noncoding RNA used as a tumor marker for screening gastric cancer. Cancer 120 3320–3328

    Not in our library10.1002/cncr.28882

  88. 88.

    Shi X. Sun M. Liu H. Yao Y. Kong R. Chen F. (2013 ). A critical role for the long noncoding RNA GAS5 in proliferation and apoptosis in non-small-cell lung cancer. Mol. Carcinog. [Epub ahead of print].

    Not in our library10.1002/mc.22120

  89. 89.
    Decreased expression of long noncoding RNA GAS5 indicates a poor prognosis and promotes cell proliferation in gastric cancer · 2014
    No notice
  90. 90.

    Svoboda M. Slyskova J. Schneiderova M. Makovicky P. Bielik L. Levy M. (2014 ). HOTAIR long noncoding RNA is a negative prognostic factor not only in primary tumors, but also in the blood of colorectal cancer patients. Carcinogenesis 35 1510–1515

    Not in our library10.1093/carcin/bgu055

  91. 91.

    Takahashi K. Yan I. K. Kogure T. Haga H. Patel T. (2014 ). Extracellular vesicle-mediated transfer of long noncoding RNA ROR modulates chemosensitivity in human hepatocellular cancer. FEBS Open Bio. 4 458–467

    Not in our library10.1016/j.fob.2014.04.007

  92. 92.

    Tang H. Wu Z. Zhang J. Su B. (2013 ). Salivary lncRNA as a potential marker for oral squamous cell carcinoma diagnosis. Mol. Med. Rep. 7 761–766

    Not in our library10.3892/mmr.2012.1254

  93. 93.

    Tinzl M. Marberger M. Horvath S. Chypre C. (2004 ). DD3PCA3 RNA analysis in urine—a new perspective for detecting prostate cancer. Eur. Urol. 46 182–186

    Not in our library10.1016/j.eururo.2004.06.004

  94. 94.

    Tripathi V. Ellis J. D. Shen Z. Song D. Y. Pan Q. Watt A. T. (2010 ). The nuclear-retained noncoding RNA MALAT1 regulates alternative splicing by modulating SR splicing factor phosphorylation. Mol. Cell 39 925–938

    Not in our library10.1016/j.molcel.2010.08.011

  95. 95.

    Tsang W. P. Ng E. K. Ng S. S. Jin H. Yu J. Sung J. J. (2010 ). Oncofetal H19-derived miR-675 regulates tumor suppressor RB in human colorectal cancer. Carcinogenesis 31 350–358

    Not in our library10.1093/carcin/bgp181

  96. 96.

    Tu Z. Q. Li R. J. Mei J. Z. Li X. H. (2014 ). Down-regulation of long noncoding RNA GAS5 is associated with the prognosis of hepatocellular carcinoma. Int. J. Clin. Exp. Pathol. 7 4303–4309.

    Not in our library

  97. 97.

    Ulaner G. A. Vu T. H. Li T. Hu J. F. Yao X. M. Yang Y. (2003 ). Loss of imprinting of IGF2 and H19 in osteosarcoma is accompanied by reciprocal methylation changes of a CTCF-binding site. Hum. Mol. Genet. 12 535–549

    Not in our library10.1093/hmg/ddg034

  98. 98.

    Wang L. Zeng X. Chen S. Ding L. Zhong J. Zhao J. C. (2013 ). BRCA1 is a negative modulator of the PRC2 complex. EMBO J. 32 1584–1597

    Not in our library10.1038/emboj.2013.95

  99. 99.

    Wang P. Ren Z. Sun P. (2012 ). Overexpression of the long noncoding RNA MEG3 impairs in vitro glioma cell proliferation. J. Cell Biochem. 113 1868–1874

    Not in our library10.1002/jcb.24055

  100. 100.

    Wang X. Arai S. Song X. Reichart D. Du K. Pascual G. (2008 ). Induced ncRNAs allosterically modify RNA-binding proteins in cis to inhibit transcription. Nature 454 126–130

    Not in our library10.1038/nature06992

  101. 101.

    Wang X. S. Zhang Z. Wang H. C. Cai J. L. Xu Q. W. Li M. Q. (2006 ). Rapid identification of UCA1 as a very sensitive and specific unique marker for human bladder carcinoma. Clin. Cancer Res. 12 4851–4858

    Not in our library10.1158/1078-0432.ccr-06-0134

  102. 102.
    Transcriptome sequencing reveals altered long intergenic non-coding RNAs in lung cancer · 2014
    No notice
  103. 103.

    Wu Y. Zhang L. Wang Y. Li H. Ren X. Wei F. (2014a ). Long noncoding RNA HOTAIR involvement in cancer. Tumour Biol. 35 9531–9538

    Not in our library10.1007/s13277-014-2523-7

  104. 104.

    Wu Z. H. Wang X. L. Tang H. M. Jiang T. Chen J. Lu S. (2014b ). Long noncoding RNA HOTAIR is a powerful predictor of metastasis and poor prognosis and is associated with epithelial-mesenchymal transition in colon cancer. Oncol. Rep. 32 395–402

    Not in our library10.3892/or.2014.3186

  105. 105.
    Plasma HULC as a Promising Novel Biomarker for the Detection of Hepatocellular Carcinoma · 2013
    No notice
  106. 106.

    Xu Z. Y. Yu Q. M. Du Y. A. Yang L. T. Dong R. Z. Huang L. (2013 ). Knockdown of long noncoding RNA HOTAIR suppresses tumor invasion and reverses epithelial-mesenchymal transition in gastric cancer. Int. J. Biol. Sci. 9 587–597

    Not in our library10.7150/ijbs.6339

  107. 107.

    Yamada K. Kano J. Tsunoda H. Yoshikawa H. Okubo C. Ishiyama T. (2006 ). Phenotypic characterization of endometrial stromal sarcoma of the uterus. Cancer Sci. 97 106–112

    Not in our library10.1111/j.1349-7006.2006.00147.x

  108. 108.

    Yang Z. Zhou L. Wu L. M. Lai M. C. Xie H. Y. Zhang F. (2011 ). Overexpression of long noncoding RNA HOTAIR predicts tumor recurrence in hepatocellular carcinoma patients following liver transplantation. Ann. Surg. Oncol. 18 1243–1250

    Not in our library10.1245/s10434-011-1581-y

  109. 109.

    Yarmishyn A. A. Batagov A. O. Tan J. Z. Sundaram G. M. Sampath P. Kuznetsov V. A. (2014 ). HOXD-AS1 is a novel lncRNA encoded in HOXD cluster and a marker of neuroblastoma progression revealed via integrative analysis of noncoding transcriptome. BMC Genomics 15(Suppl. 9):S7

    Not in our library10.1186/1471-2164-15-s9-s7

  110. 110.

    Ying L. Chen Q. Wang Y. Zhou Z. Huang Y. Qiu F. (2012 ). Upregulated MALAT-1 contributes to bladder cancer cell migration by inducing epithelial-to-mesenchymal transition. Mol. Biosyst. 8 2289–2294

    Not in our library10.1039/c2mb25070e

  111. 111.

    Yoon J. H. Abdelmohsen K. Srikantan S. Yang X. Martindale J. L. De S. (2012 ). LincRNA-p21 suppresses target mRNA translation. Mol. Cell 47 648–655

    Not in our library10.1016/j.molcel.2012.06.027

  112. 112.

    Yu M. Ohira M. Li Y. Niizuma H. Oo M. L. Zhu Y. (2009 ). High expression of ncRAN, a novel noncoding RNA mapped to chromosome 17q25.1, is associated with poor prognosis in neuroblastoma. Int. J. Oncol. 34 931–938.

    Not in our library10.3892/ijo_00000219

  113. 113.

    Zhang S. Chen S. Yang G. Gu F. Li M. Zhong B. (2014 ). Long noncoding RNA HOTAIR as an independent prognostic marker in cancer: a meta-analysis. PLoS ONE 9:e105538

    Not in our library10.1371/journal.pone.0105538

  114. 114.

    Zhang X. Gejman R. Mahta A. Zhong Y. Rice K. A. Zhou Y. (2010 ). Maternally expressed gene 3 an imprinted noncoding RNA gene, is associated with meningioma pathogenesis and progression. Cancer Res. 70 2350–2358

    Not in our library10.1158/0008-5472.can-09-3885

  115. 115.

    Zhang X. Q. Sun S. Lam K. F. Kiang K. M. Pu J. K. Ho A. S. (2013 ). A long noncoding RNA signature in glioblastoma multiforme predicts survival. Neurobiol. Dis. 58 123–131

    Not in our library10.1016/j.nbd.2013.05.011

  116. 116.

    Zhang X. Sun S. Pu J. K. Tsang A. C. Lee D. Man V. O. (2012 ). Long noncoding RNA expression profiles predict clinical phenotypes in glioma. Neurobiol. Dis. 48 1–8

    Not in our library10.1016/j.nbd.2012.06.004

  117. 117.

    Zhao J. Sun B. K. Erwin J. A. Song J. J. Lee J. T. (2008 ). Polycomb proteins targeted by a short repeat RNA to the mouse X chromosome. Science 322 750–756

    Not in our library10.1126/science.1163045

  118. 118.

    Zheng H. T. Shi D. B. Wang Y. W. Li X. X. Xu Y. Tripathi P. (2014 ). High expression of lncRNA MALAT1 suggests a biomarker of poor prognosis in colorectal cancer. Int. J. Clin. Exp. Pathol. 7 3174–3181.

    Not in our library

  119. 119.

    Zhou Y. Zhong Y. Wang Y. Zhang X. Batista D. L. Gejman R. (2007 ). Activation of p53 by MEG3 noncoding RNA. J. Biol. Chem. 282 24731–24742

    Not in our library10.1074/jbc.m702029200

  120. 120.

    Zhu Y. Yu M. Li Z. Kong C. Bi J. Li J. (2011 ). ncRAN, a newly identified long noncoding RNA, enhances human bladder tumor growth, invasion, and survival. Urology 77:e1–e5

    Not in our library10.1016/j.urology.2010.09.022

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