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Brain microRNAs and insights into biological functions and therapeutic potential of brain enriched miRNA-128

Yogita K Adlakha, Neeru Saini

Molecular Cancer · 2014 · Review

Abstract

MicroRNAs, the non-coding single-stranded RNA of 19-25 nucleotides are emerging as robust players of gene regulation. Plethora of evidences support that the ability of microRNAs to regulate several genes of a pathway or even multiple cross talking pathways have significant impact on a complex regulatory network and ultimately the physiological processes and diseases. Brain being a complex organ with several cell types, expresses more distinct miRNAs than any other tissues. This review aims to discuss about the microRNAs in brain development, function and their dysfunction in brain tumors. We also provide a comprehensive summary of targets of brain specific and brain enriched miRNAs that contribute to the diversity and plasticity of the brain. In particular, we uncover recent findings on miRNA-128, a brain-enriched microRNA that is induced during neuronal differentiation and whose aberrant expression has been reported in several cancers. This review describes the wide spectrum of targets of miRNA-128 that have been identified till date with potential roles in apoptosis, angiogenesis, proliferation, cholesterol metabolism, self renewal, invasion and cancer progression and how this knowledge might be exploited for the development of future miRNA-128 based therapies for the treatment of cancer as well as metabolic diseases.

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From PubMed Central, U.S. National Library of Medicine, as current on Oct 21, 2026. Paragraph numbers are ours, so an answer can point at one.

Introduction

1MicroRNAs are small non-coding RNAs of 19–25 nucleotides in length and are known to regulate several protein-coding genes both in plants and animals. The first miRNA, lin-4 that controlled developmental timing in Caenorhabditis elegans was identified by two different groups in 1993. Later, let-7 miRNAs were found to control the timing of fate specification of neuronal and hypodermal cells during larval development. Subsequently, numerous miRNAs have been implicated in a variety of cellular processes including differentiation, apoptosis, cell proliferation, embryonic development, stem cell renewal, stress response and metabolism. Their profound impact on the regulation of numerous cellular processes clearly suggests that any aberration in miRNA biogenesis pathway or its regulation contributes to several human diseases such as cancer, cardiovascular diseases, schizophrenia, psoriasis, diabetes, chronic hepatitis, AIDS, and obesity.

2MicroRNAs (miRNAs) interfere with target gene expression by binding to the 3′ UTRs of their target mRNAs and act primarily at the level of translation. Complete complementarity between miRNA and 3′UTR of its target leads to the degradation of mRNA targets as shown in plants whereas partial complementarity leads to inhibition of translation as seen in mammals. Literature reveals that a single miRNA can target several mRNAs together, and a single mRNA can be targeted by different miRNAs in a concerted manner. Large number of microRNAs and the capacity of each miRNA to target several transcripts suggest a complex regulatory network to fine tune the gene expression and a mechanism by which they are thought to regulate various processes during health and disease.

3The advancement of high-throughput sequencing techniques has led to the rapid growth in the number of annotated miRNA. The most recent miRBase Sequence Database, Release 20 ( http://www.mirbase.org/), harbours 24521 entries representing hairpin precursor miRNAs and expressing 30424 mature miRNA products in 193 species. The sequences of most miRNAs are conserved across large evolutionary distances, suggesting a conserved role in regulation of various physiological processes.

4The diversity and gene-regulatory capacity of miRNAs is particularly valuable in the brain, where persistent flow of information and functional specialization of neurons requires constant neuronal adaptation to environmental cues. The brain expresses more distinct and largest number of miRNAs than any other tissue in vertebrates as it has wide variety of cell types, neuronal and nonneuronal (for e.g. astrocytes). In this review, we summarize present knowledge on the microRNA expression and functions in the brain and their potential involvement in relation to brain tumors. Herein, we also give an overview of the functions and targets of brain-enriched and brain-specific miRNAs before delving into specific example of miRNA-128, the most abundant brain-enriched miRNA. We believe that the understanding of the impact of microRNA-128 on regulation of proliferation, apoptosis and metabolic processes is still at its dawn and needs further research for the development of future miRNA-based therapies for the treatment of metabolic diseases and cancer.

MiRNA biogenesis and mechanism of action

5Approximately, 50% of the mammalian miRNAs have found their location in introns or exons of protein-coding genes or introns of long non-coding RNAs. Their expression is either derived by independent transcriptional units or by protein-coding gene transcriptional units. As shown in Figure 1, miRNAs are transcribed from genomic DNA by RNA polymerase II or III into long, primary transcripts (pri-miRNAs) just like other protein coding genes. These pri-miRNAs are several kilobases in length and usually possess a 5′ CAP and a 3′ poly (A) tail. These pri-miRNAs are processed by a microprocessor complex which consists of a ribonuclease III (RNase III) named Drosha, a RNA-binding protein DiGeorge syndrome critical region 8 (DGCR8/Pasha) and a variety of co-factors [DEAD box helicases p68 and p72 and the heterogeneous nuclear ribonucleoproteins (hnRNPs)] which are thought to promote the specificity and/or activity of Drosha cleavage. Drosha processing occurs co-transcriptionally in most mammalian miRNAs i.e. before splicing of host RNA (canonical pathway). However, Drosha pathway can be evaded by miRtrons (a subset of intronic miRNAs) and are made by splicing and debranching of short hairpin introns. The product of Drosha cleavage is a 70–100 nucleotide hairpin-shaped precursor referred to as pre-miRNA. These pre-miRNAs are exported to the cytoplasm by Ran-GTP and Exportin-5 dependent mechanisms. In cytoplasm, these pre-miRNAs are excised by the RNase III enzyme Dicer into a double-stranded RNA of ~22 nucleotides in length, referred to as the miRNA:miRNA* duplex or by Ago2, an Argonaute protein that is part of the RISC complex and aligns the miRNA and messenger RNA. The criteria for binding and cleavage by Ago2 after the 30th nucleotide are short stem and spanning of the loop by miRNA sequence. The duplex produced by either Dicer or Ago2 is loaded onto an Argonaute protein where one strand, i.e. guide strand, complementary to the target mRNA, is selected and subsequently forms the miRNA effector as part of a miRISC (miRNA-induced silencing complex), while the remaining strand (the "passenger strand") is released and degraded. Similar to Drosha and Dicer assisting proteins, the formation of the miRISC and the execution of its activity involve many additional factors. The two key factors involved in the assembly and function of miRISCs are Argonaute (AGO) proteins, which directly interact with miRNAs, and glycine-tryptophan protein of 182 kDa (GW182), which act as downstream effectors in the repression. miRNA then guides the miRISC to recognize the partially complementary binding sites located in the 3′UTR of their target mRNAs.

6The perfect binding between seed region (5′ 2–8 nucleotides 3′) of mature miRNA and 3′UTR of their target by Watson-Crick base-pairing is considered to be the major determinant in blocking the target mRNA either by translational repression or mRNA degradation. However other 3′- supplementary and 3′- compensatory binding sites in miRNA sequence also play a significant role during interactions. Although miRNA binding sites are most common in 3′UTRs of mRNAs, yet there are some reports of miRNA interaction within the 5′UTR, mRNA coding region and intron-exon junctions. The detailed mechanisms underlying the inhibition of protein synthesis by miRNAs are not well understood, but literature suggests sequestration of mRNA into P bodies from ribosomes, blockage of translational initiation, translational repression or target deadenylation coupled to transcript degradation. However, it is now believed that miRNA regulate gene expression in majority of cases by mRNA decay rather than translational repression. Epigenetic modifications and transcription factors also play a decent role in the regulation of miRNA function. Recent reports also depict the role of pseudogenes as miRNA sequestering sponges or decoys in the regulation of miRNA function.

MicroRNAs in brain development and function

7The brain is a complex organ, with various types of cells (neurons and non-neurons) that form an intricate communication network. Literature reveals that 70% of known miRNAs are expressed in the brain. Surprisingly, only a handful of microRNAs are expressed in a brain specific or brain-enriched manner. Since these miRNAs are dynamically regulated during brain development, have different targets and perform different functions in brain, herein we provide a comprehensive list of the recent validated roles of brain-enriched and brain-specific microRNAs along with their targets in brain in Tables 1 and 2.

8The increasing variety of miRNAs being identified in the brain suggests a sheer connection between the biogenesis, dynamics of action and regulatory potential of miRNAs and the complexity of the brain. Numerous studies on depletion of the Dicer gene in the nervous system of animal models further demonstrate that microRNAs play essential roles in controlling neuronal proliferation, migration and precursor fates and serve important roles in development and function in the brain. Stark et al. in their study, have illustrated the contribution of defects in miRNA biogenesis to brain abnormalities in Dicer deficient mice and mouse model of schizophrenia.

9An expression profiling study by Sempere et al. showed a group of 17 miRNAs were expressed in mouse and human brain (miR-7, -9, -9*, -124a, -124b, -125a, -125b, -128, -132, -135, -137, -139, -153, -149, -183, -190, -219). All these miRNAs have been found to regulate neuronal differentiation, maturation, and/or survival in mouse and human. Conservation of these miRNAs between mouse and human suggests that they may play a conserved role in the establishment and/or maintenance of a cell or tissue type of brain. Specific expression of miR-9 and miR-132 is restricted to hippocampus and medal frontal gyrus whereas miR-124 and miR-128 are unique for neurons and miR-23, miR-26 and miR-29 are specifically expressed in astrocytes. In addition miR-195 displays a moderate to low expression level in the mammalian embryonic brain, with the highest level at the preadult brain developmental stage.

10Studies have further shown that miR-9 expression is necessary for neurogenesis in cultured stem cells and miR-132 plays a role in neurite extension and neurogenesis. MiR-132 has also been linked to BDNF (a member of the nerve growth factor family that is necessary for survival of striatal neurons in the brain) and MeCP2 (methyl-CpG DNA binding protein that plays an essential role in mammalian development) by a negative feedback loop. Interestingly, miR-124 when overexpressed in non-neuronal HeLa cells shifts the gene expression profile from an immature cervix cell into a neuronal phenotype, suggesting that miR-124 downregulates mRNAs directing cells into a non-neuronal phenotype. Recently, it has been observed that MiR-124 targets REST, BTBP and Sox9, all proteins have been known to antagonize the formation of neuronal cells during development. Similar to miR-124, miRNA-128 is induced during brain development and in differentiating neuronal cells; leading to repressed NMD (Nonsense-mediated decay) and the consequent upregulation of batteries of mRNAs encoding proteins important for neuron differentiation and function. MiR-23 is implicated in neural specification while miR-26 is required during neuronal cell differentiation. Report by Kole et al. showed that miR-29b is markedly induced during neuronal maturation and functions as a inhibitor of neuronal apoptosis. Apart from development, aberrant microRNA expression has been discovered in human CNS (central nervous system) diseases including brain tumors in the past decade.

Dysfunction of microRNAs in brain tumors

11Gliomas are the primary brain tumors that are made up of glial cells which provide important structural support for the nerve cells in the brain. Malignant gliomas are the most common and lethal tumors arising in the central nervous system and are classified by the World Health Organization (WHO) into four different grades based on malignancy (I, II, III, IV). Grade IV glioblastoma multiforme (GBM) is the most common lethal primary brain tumor in adults that is characterized by aggressive vascular proliferation, invasiveness, stem cell-like behaviour and chemoresistance to new and traditional therapies. Accumulating evidences indicate the presence of different miRNAs with pro-oncogenic and anti-oncogenic properties in glioblastomas. Koshkin et al. recently observed gradual increase in miR-21 and miR-23a levels in all tumor grades and significant decrease of miR-7 and miR-137 depending on the glioma grade. Further, miR-210 has been found to be highly expressed in human gliomas and confers a poor prognosis in glioma patients. MicroRNA-206 has been found to be a tumor suppressor in human malignant cancers. Low miR-206 expression is associated with poor overall survival in patients with malignant astrocytomas, hence it could become a valuable marker of astrocytoma progression. Apart from these, several independent studies observed that the expressions of miR-16, miR-503, miR-203, miR-34c-3p, miR-34c-5p, miR-106a, Let-7a, miR-218, miR-223, miR-34a, miR-329, miR-145, miR-124, miR-137, miR-138, miR-219-5p, miR-495, miR-383, miR-200b, miR-134, miR-153, miR-195, miR-143, miR-107, miR-326, miR-204 and miR-214 were significantly reduced in high WHO grade glioma tissues relative to low WHO grade glioma tissues and normal brain tissues. The expression of most of these miRNAs decreases with increasing degrees of malignancy. The low expression of Let-7a was correlated with poor prognosis of primary glioblastoma patients. Further, miR-708 and miR-17 ~ 92 cluster were downregulated in GBM tumor cell lines whereas three miR-17 ~ 92 cluster miRNAs (miR-2, -19a and -20) were upregulated in human medulloblastoma with aberrantly activated sonic hedgehog (SHH) signaling pathway. Another group by Skalsky and Ciafre et al. in their cluster analysis further revealed that miR-139, miR-95 and miR-873 were down-regulated specifically in glioblastomas and miR-137 and miR-181a/b were down-regulated in gliomas whereas miR-7, miR-124 and miRNA-128 were down-regulated in both. Interestingly, miRNA-128 and miR-124 are not only down regulated in gliomas but also other brain cancers including medulloblastomas and neuroblastomas. Li et al. reported that decreased miR-146b-5p expression was strongly correlated with chromosome 10q loss in gliomas, especially glioblastomas. The significance of the sequence of miRNA can be illustrated by the example of miR-23 in brain. The expression of miRNA-23b was gradually downregulated with the malignancy of glioma whereas miR-23a was upregulated in malignant glioma tissues. Further, miR-328, miR-106b-5p, miR-155, miR-650, miR-92b, miR-30a-5p, miR-10b, miR-372, miR-183, miR-486 and miR-17 were found to be upregulated in invading glioma cells in vivo and glioma tissues respectively as revealed by miRNA expression profiling of microdissected human tumor biopsy specimens. MiR-650 expression can be used as a significant prognostic indicator in glioma. MiR-19a, -19b and miR-9 have been found to be overexpressed in glioma cell lines and astrocytic glioma tissues, and their expression level is positively correlated with tumor grades. Several studies showed that miR-21 and miR-10b are upregulated in glioblastomas and has recently been shown to be a significant contributor for tumor growth in vivo. Wu et al. have recently documented that overall patient survival for those with low miR-21 expression was significantly longer than those patients with high miR-21 expression. Further, miRNA-21, 221, 222, 181b, 181c, and 128a were found to be significantly deregulated in GBM tissues by Slaby et al. and Zhou et al. It was also observed that miRNA-181b and 181c were the most down regulated miRNAs in patients who responded to radiation therapy (RT) and temozolomide (TMZ) and hence could serve as predictors for RT/TMZ response. Several differentially expressed miRNAs such as miR-124, miR-21, -128, -181, -221 and -222 could serve as potential biomarkers in GBM in general since they play common role in the etiology of malignant brain tumors.

Role of pro-neural miRNA-128 in brain related disorders

12MiRNA-128 is transcribed by two distinct genes, miRNA-128-1 and miRNA-128-2 in two primary transcripts, which are processed into an identical mature miRNA sequence. MiRNA-128-1 and miRNA-128-2 are both present in the intronic regions of two genes on two different chromosomes. MiRNA-128-1 is embedded in the R3HDM1 (R3H domain containing 1) gene on chromosome 2q21.3 and miRNA-128-2 is in the ARPP21 (cyclic AMP-regulated phosphoprotein, 21 kDa) on chromosome 3p22.3. Evidences in the literature reveal that miRNA-128 has tissue specific and developmental specific expression patterns. Apart from brain, miRNA-128 has also been found in the skeletal muscle and thymus and is highly expressed during neuronal differentiation. Down regulation of miRNA-128 has been reported in several brain cancers for example- glioblastoma and medulloblastoma. Allelic loss in chromosome 3p, where miRNA-128-2 is present, has also been associated with the most aggressive forms of neuroblastoma.

13Cui et al. demonstrated that the down-regulation of miRNA-128 inversely correlates with tumor grade. They also observed that the decrease of miRNA-128 is coupled with significant increase in the expression of Bmi-1, the transcription factor E2F-3a and angiopoietin-related growth factor protein 5 (ARP5; ANGPTL6). Increased expression of these factors may explain the undifferentiated, self-renewing state of brain cells and de-regulated cell-cycle signaling pathways that support cellular proliferation in glioma and GBM. Zhang et al. in his study showed that brain-enriched miRNA-128 was also down regulated in glioma tissues and cell-lines and overexpression of miRNA-128 inhibited cellular proliferation through negatively regulating E2F3a, which is highly expressed in glioma and important for cell cycle progression (Figure 2). Papagiannakopoulos et al. recently showed that miRNA-128 represses growth and enhances neuronal differentiation of glioma-initiating neural stem cells (giNSCs) by downregulating oncogenic receptor tyrosine kinases (RTKs), epithelial growth factor receptor (EGFR) and platelet-derived growth factor receptor-α (PDGFRα) (Figure 2). In an independent study, Godlewski et al., reported that overexpression of miRNA-128 reduces glioma cell proliferation by downregulating Bmi-1 (B lymphoma mouse Moloney leukemia virus insertion region 1), decrease in histone methylation (H3K27me3) and Akt phosphorylation and up-regulation of p21CIP1 levels. As Bmi-1 is also known to promote the stem cell renewal, a process that is important in glioma, hence miRNA-128 may be used against the "stem cell-like" characteristics of glioma cells. These data suggest that miRNA-128 may suppress cancer pathogenesis by inducing differentiation out of a stem cell-like state. Roth et al. recently reported upregulation of miRNA-128 in the blood samples of glioblastoma patients compared to healthy controls and speculated that this miRNA fingerprint may be used as suitable biomarker for glioblastoma.

14Besides these, levels of miRNA-128 have been reported to be deregulated in autism, prion-induced neurodegeneration, Huntington disease, Parkinson disease and Alzheimer disease. Several evidences in the literature show that under different biological conditions, expression patterns of miRNA-128 varies i.e. in some instances, it is up regulated whereas in some, it is down regulated (Table 3). Furthermore, Eletto et al. in his study showed that miRNA-128a inhibits expression of the pre-synaptic protein SNAP25 by binding to its 3′UTR (Figure 2). They observed Tat mediated deregulation of miRNA-128, in primary cortical neurons during the infection of neurons by HIV-1. However, the role of miRNA-128a in regulating synaptic activity in normal and in neurodegenerative disorders including HIV-1 Encephalopathy (HIVE) needs to be determined.

Expression of pro-neural miRNA-128 in cancers other than brain

15Cancer occurs due to accumulation of several genomic alterations and is characterized by unrestricted proliferation, invasion, and metastasis. miRNAs normally negatively regulate their transcript targets and recent evidence indicates that miRNAs may function as tumor suppressors (by binding to oncogenes and suppressing them) or oncogenes (by binding to tumor suppressor genes and suppressing them) and alterations in miRNA expression may play a critical role in the cancer initiation and progression. Within the past few years, profiling of the miRNome (global miRNA expression levels) is common and abundant miRNome data are currently available for various cancers. MiRNA expression can be correlated with cancer type, stage, and other clinical variables which may be useful for the classification, diagnosis, or prognosis of some human malignancies. With respect to miRNA-128, it is known that miRNA-128 may act as a tumor-suppressor. Kotani et al. in his study reported down regulation of miRNA-128 in MLL-AF4 Acute Lymphocytic Leukemia and Khan et al. revealed down regulation of miRNA-128 in invasive prostate cancer cells as compared to benign prostate epithelial cell lines, where its levels are elevated. In addition, miRNA-128 was significantly reduced in chemoresistant breast tumor-initiating cells (BT-ICs) enriched from breast cancer cell lines and primary breast tumors (P < 0.01), accompanied by an overexpression of Bmi-1 and ABCC5, which were identified as targets of miRNA-128. In contrast to these studies, strong induction of miRNA-128 has been observed in endometrial cancer as well as in acute lymphoblastic leukemia (ALL). Up regulation of miRNA-128 not only suppressed the colony formation ability and invasiveness of pituitary tumor cells but also suppressed pituitary GH3 tumor growth in xenografts via, Bmi-1. MiRNA-128 found to regulate its direct target Bmi-1 and PTEN-AKT pathway in pituitary tumors. Allelic loss in chromosome 3p (where miRNA-128-2 is present) has been shown to be associated with the most aggressive form of lung carcinogenesis. Furthermore, it was observed that loss of heterozygosity (LOH) of MicroRNA-128b in tumor samples correlated significantly with clinical response and survival following Gefitinib via EGFR. Although the increase/decrease of miRNA-128 has been reported in a number of the studies related to cancer but it is not known whether it is a cause or effect of the disease.

Pro-neural miRNA-128 as regulator of apoptosis

16Alterations in susceptibility to apoptosis is a key factor for the survival of a malignant cell and it enhances resistance to conventional anticancer therapies. As the altered expression of pro-neural miRNA-128 was found in several cancers, numerous studies were undertaken to delineate the mechanism for the inhibition of cell proliferation and induction of apoptosis by miRNA-128. Sean Lawler’s laboratory demonstrated that ectopic expression of miRNA-128 in human glioma neurosphere cultures (having stem-like properties) led to reduction in glioma neurosphere number and volume by down regulating Bmi-1 (Figure 2). In addition to this, several independent studies have illustrated the anti-proliferative role of miRNA-128 in glioma cells and glioblastoma cell lines. Infact, ginsenoside Rh2, a triterpene saponin has also been found to inhibit glioma cell proliferation by upregulating microRNA-128. Further, over expression of miRNA-128 leads to an alteration in the expression of genes implicated in cytoskeletal organization (via truncated isoform of NTRK3) as well as genes involved in apoptosis, cell survival and proliferation, including the anti-apoptotic factor BCL2 in SH-SY5Y neuroblastoma cells. In our laboratory also, we recently observed that miRNA-128 overexpression induced apoptosis by down regulation of Bax and up regulation of p53 and Bak. Furthermore, transcriptome analysis of miRNA-128 overexpressed cells revealed that miRNA-128 inhibits SIRT1 expression directly through a miRNA-128 binding site within the 3′UTR of SIRT1 (Figure 2). Finally, we found that miRNA-128 induces apoptosis in wild type (WT) p53 as well as in mutant p53-expressing cells in a p53-dependent and -independent manner via induction of PUMA in MCF7, MDA-MB-231, HCT116 p53 +/+ and HCT116 p53 -/- cells respectively. In our study, we also demonstrated that miRNA-128 augments the antitumor effects of compounds (Etoposide and Cisplatin). Contrary to our findings, Yolanda’s group has shown that ectopic expression of miRNA-128 downregulated genes that induce apoptosis and upregulated genes implicated in cell survival. In an another recent study, miRNA-128 was found to target Bax in breast cancer cell line MDA-MB-231 and downregulation of miRNA-128 sensitised MDA-MB-231 cells to chemodrugs. Furthermore, Donzelli et al. observed that miRNA-128-2 expression in lung cancer cells inhibits apoptosis and confers increased resistance to cisplatin, doxorubicin and 5-Fluorouracyl treatment via E2F5 (Figure 2). Based on the above information, we can say that depending upon the cell type; miRNA-128 can have anti-apoptotic as well as pro-apoptotic functions. It seems that miRNA-128 can be targeted to facilitate cancer cell death and/or inhibit cancer cell growth; however, this aspect warrants further investigation.

Role of miRNA-128 in cell motility, angiogenesis and senescence

17Ability to migrate and eventually disseminate to distal sites is one of the key characteristic of tumor cells, which is also responsible for the relative aggressiveness of the tumor. Data from several independent studies showed that overexpression of miRNA-128 inhibits cell motility and invasiveness. Evangelisti et al. proved that overexpression of miRNA-128 reduces neuroblastoma cell motility and invasiveness by targeting Reelin and DCX (Figure 2). DCX is a microtubule-associated protein required for neuroblastic migration during cerebral cortex development while Reelin is a high-molecular-weight secreted glycoprotein, which is thought to play its role as a guide for migratory neurons. Messi et al. described DCX as a marker of SK-N-SH neuroblastoma cells that show high motility and invasiveness. DCX expression is also detectable in some tumors of the nervous system, such as GBM and neuroblastoma. Reelin has been shown to be a positive marker for prostate carcinoma aggressiveness and is overexpressed in retinoblastoma and esophageal carcinoma and its expression is directly correlated with tumor aggressiveness. Khan et al. investigated the proteomic alterations in a cohort of 15 prostate-derived tissues from adjacent benign prostate (Benign), clinically localized prostate cancer (PCA) and metastatic disease from distant sites (Mets). By coupling multidimensional protein fractionation and quantitative mass spectrometry with bioinformatics-based enrichment analysis, they demonstrated the involvement of miRNA-128 in the stages of prostate cancer progression. They have shown using qRT-PCR that miRNA-128 levels were reduced in invasive prostate cancer cells as compared to benign prostate epithelial cell lines. Further, over expression of miRNA-128 attenuated invasion in prostate cancer cells while its knockdown induced invasion in benign prostate epithelial cells as revealed by matrigel invasion assay. These findings suggest that miRNA-128 reduces cell motility and invasiveness of tumor cells and thus prevents angiogenesis. In an independent study, Shi et al. observed that miRNA-128 overexpression inhibited tumorigenesis and angiogenesis through targeting p70S6K1 and suppressing downstream molecules of p70S6K1 such as HIF-1 and VEGF. Their study identified a link between miRNA-128 and p70S6K1 axis, which plays a vital role in glioma angiogenesis (Figure 2).

18Over expression of Bmi-1 oncogene has been found to promote NSC self-renewal by repressing the p16Ink4a and p19Arf senescence pathways. As miRNA-128 directly targets Bmi-1 oncogene, the role of miRNA-128 in senescence is also evident. Observation by Venkatraman’s group of increased methylation of histone 3 lysine 9 (H3K9me2) (a mark of repressed gene expression mediated by the Bmi-1 polycomb repressor complex) after overexpression of miRNA-128 further confirms the role of miRNA-128 in promoting cellular senescence. They also observed that overexpression of miRNA-128a in medulloblastoma alters the intracellular redox state of the tumor cells. In our study also, over expression of miRNA-128 in HEK293T cells led to an increase in reactive oxygen species. This is quite interesting for therapeutic scenario where miRNA-128 can be used as therapeutic modality for treating cancer, as cancer stem cells are more resistant to therapy due to a lower overall redox state, where it can induce ROS.

Insights into regulation of cholesterol metabolism by miRNA-128: a new key player in cholesterol related disorders

19Aberrant regulation of cholesterol homeostasis is associated with obesity as well as multiple types of cancer. The regulation of cholesterol homeostasis pathways is complex with transcriptional regulation by sterol-regulatory element-binding protein (SREBP) and liver X receptor/retinoid X receptor (RXR) transcription factors but poorly understood at the post-transcriptional levels. While investigating the mechanism of miRNA-128 induced apoptosis, we observed that besides regulating the genes of apoptosis, miRNA-128 also regulates cholesterol metabolism and fatty acid biosynthesis pathways. In our study, we discovered that miRNA-128 up-regulated cholesterol synthesis genes and down regulated fatty acid biosynthesis genes. miRNA-128 further affected cholesterol efflux pathway by direct targeting ABCA1, ABCG1 and RXRα (Figure 2). We provided the first evidence of miRNA-128-2 to be a new regulator of cholesterol homeostasis. Our invitro results present a novel opportunity to investigate microRNA related interactions invivo and their role in cholesterol regulation. We believe validation using invivo model should not only provide novel insights into understanding of cholesterol regulation by miRNAs but should also help us to combat a variety of cholesterol related pathologies.

Biological relevance of miRNA-128 as revealed by bioinformatic analysis

20The overall cellular functions and pathways affected by this miRNA remains still undiscovered due to lack of high throughput target validation methods. To reveal biological significance of miRNA-128, a list of predicted targets of miRNA-128 was made using the miRNA target prediction software, TargetScan 5 program (Table 4). From this list, we discovered that 90 targets of miRNA-128 were conserved among 9 species (Human, Mouse, Chimpanzee, Rhesus, Cow, Chicken, Frog, Rat, Opossum); thereby indicating possible mechanistically conserved functions of this miRNA (Figure 3). To evaluate the specific pathways or processes that are targeted by miRNA-128, we used the list of these ninety conserved targets to find enriched pathways by the PANTHER and GeneCodis analysis. Insulin/IGF pathway-mitogen activated protein kinase kinase/MAP kinase cascade, TGF-beta signaling pathway, Angiogenesis, Insulin/IGF pathway-protein kinase B signaling cascade, PI3 kinase pathway, Wnt signaling pathway were found to be the most enriched biological pathways as revealed by the PANTHER analysis (Figure 4). Interestingly, we observed that the Insulin signaling pathway and chemokine signaling pathway were the enriched categories (p-value < 0.05) in both PANTHER and GeneCodis analysis. Till now, only one study by Motohashi et al. describes about the regulation of Insulin signaling pathways by miRNA-128a via the regulation of INSR (insulin receptor), IRS1 (insulin receptor substrate 1) and PIK3R1 (phosphatidylinositol 3-kinases regulatory 1). There are a few reports which have talked about the involvement of miRNA-128 in TGF-β signaling and PI3 kinase pathway. The reports which have revealed the association between miRNA-128 and angiogenesis, have been described by us in the above section. However, regulation of Wnt signaling and chemokine signaling pathways by miRNA-128 needs further validation. Surprisingly, metabolic process came out to be the highest rated biological process with maximum number of genes during PANTHER Analysis (Figure 5). Our recent work on the regulation of cholesterol metabolism by miRNA-128 point towards a possible link between miRNA-128 and metabolic processes which is just beginning to be revealed and certainly merits further studies. Such discoveries not only provide new insights into mode of action of miRNA-128, but also raise hopes for translating miRNA-128 for therapy.

Future directions/conclusions

21MiRNA-128 is encoded by two distinct genes, viz., R3HDM1 and ARPP21. Interestingly, insilico analysis of transcription factor binding sites of these two genes reveals almost similar pattern of transcription factors (unpublised data). This suggests that these two genes may presumably resulted from a gene duplication event. Until now, neither transcription factors binding proteins of hsa-miRNA-128 gene nor epigenetic factors, have been identified that interact with the regulatory region of this miRNA. However, Monteys et al. have recently suggested dual regulation of miRNA-128-2 by both intronic (pol III) and host gene (Pol II) promoters in acute lymphoblastic leukemia. The fact that miRNA-128 plays multiple roles - a pro-apoptotic molecule, a anti-apoptotic molecule as well as a regulator of cholesterol homeostasis, raise the possibility of exploiting miRNA-128 for therapeutic intervention and development of novel therapies. Further, therapeutic modalities either using replacement strategy by miRNA-128 mimetics (for upregulation of miRNA-128) or using antisense miRNA oligonucleotides (AMOs or antagomirs), LNAs (Locked nucleic Acid) (for downregulation) may now be pursued in an effort to target a particular disease. We believe that there are several fundamental questions that still need to be answered and are open for investigation which will help in the development of miRNA-128 as therapeutics.

Competing interests

22The authors declare that they have no competing interests.

Authors’ contributions

23YKA and NS conceived the study. The survey of the literature and the inferences were made by YKA and NS. The bioinformatics analysis was carried out by YKA. The manuscript was drafted by YKA and NS. Both authors have read and approved the final manuscript.

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Not in our library10.1111/j.1469-185x.2008.00061.x
13.
Croce CM Calin GA miRNAs, cancer, and stem cell divisionCell2005 12267
Not in our library10.1016/j.cell.2005.06.036
14.
Li C Vagin VV Lee S Xu J Ma S Xi H Seitz H Horwich MD Syrzycka M Honda BM Kittler EL Zapp ML Klattenhoff C Schulz N Theurkauf WE Weng Z Zamore PD Collapse of germline piRNAs in the absence of Argonaute3 reveals somatic piRNAs in fliesCell2009 137509521
Not in our library10.1016/j.cell.2009.04.027
15.
Latronico MV Catalucci D Condorelli G Emerging role of microRNAs in cardiovascular biologyCirc Res2007 10112251236
Not in our library10.1161/circresaha.107.163147
16.
Brain Expressed microRNAs Implicated in Schizophrenia Etiology · 2007
No notice
17.
MicroRNAs: Novel Regulators Involved in the Pathogenesis of Psoriasis? · 2007
No notice
18.
Williams MD Mitchell GM MicroRNAs in insulin resistance and obesityExp Diabetes Res2012 2012484696
Not in our library10.1155/2012/484696
19.
Murakami Y Yasuda T Saigo K Urashima T Toyoda H Okanoue T Shimotohno K Comprehensive analysis of microRNA expression patterns in hepatocellular carcinoma and non-tumorous tissuesOncogene2006 2525372545
Not in our library10.1038/sj.onc.1209283
20.
Hariharan M Scaria V Pillai B Brahmachari SK Targets for human encoded microRNAs in HIV genesBiochem Biophys Res Commun2005 33712141218
Not in our library10.1016/j.bbrc.2005.09.183
21.
Weiler J Hunziker J Hall J Anti-miRNA oligonucleotides (AMOs): ammunition to target miRNAs implicated in human disease?Gene Ther2006 13496502
Not in our library10.1038/sj.gt.3302654
22.
Rogers K Chen X Biogenesis, turnover, and mode of action of plant MicroRNAsPlant Cell2013 2523832399
Not in our library10.1105/tpc.113.113159
23.
Pillai RS Bhattacharyya SN Filipowicz W Repression of protein synthesis by miRNAs: how many mechanisms?Trends Cell Biol2007 17118126
Not in our library10.1016/j.tcb.2006.12.007
24.
Bartel DP MicroRNAs: target recognition and regulatory functionsCell2009 136215233
Not in our library10.1016/j.cell.2009.01.002
25.
Wu W Sun M Zou GM Chen J MicroRNA and cancer: current status and prospectiveInt J Cancer2007 120953960
Not in our library10.1002/ijc.22454
26.
Kozomara A Griffiths-Jones S miRBase: integrating microRNA annotation and deep-sequencing dataNucleic Acids Res2011 39D152D157
Not in our library10.1093/nar/gkq1027
27.
Peterson KJ Dietrich MR McPeek MA MicroRNAs and metazoan macroevolution: insights into canalization, complexity, and the Cambrian explosionBioessays2009 31736747
Not in our library10.1002/bies.200900033
28.
O’Carroll D Schaefer A General principals of miRNA biogenesis and regulation in the brainNeuropsychopharmacology2013 383954
Not in our library10.1038/npp.2012.87
29.
Motti D Bixby JL Lemmon VP MicroRNAs and neuronal developmentSemin Fetal Neonatal Med2012 17347352
Not in our library10.1016/j.siny.2012.07.008
30.
Rodriguez A Griffiths-Jones S Ashurst JL Bradley A Identification of mammalian microRNA host genes and transcription unitsGenome Res2004 1419021910
Not in our library10.1101/gr.2722704
31.
Griffiths-Jones S Annotating noncoding RNA genesAnnu Rev Genomics Hum Genet2007 8279298
Not in our library10.1146/annurev.genom.8.080706.092419
32.
Ul Hussain M Micro-RNAs (miRNAs): genomic organisation, biogenesis and mode of actionCell Tissue Res2012 349405413
Not in our library10.1007/s00441-012-1438-0
33.
Lee Y Ahn C Han J Choi H Kim J Yim J Lee J Provost P Radmark O Kim S Kim VN The nuclear RNase III Drosha initiates microRNA processingNature2003 425415419
Not in our library10.1038/nature01957
34.
Han J Lee Y Yeom KH Kim YK Jin H Kim VN The Drosha-DGCR8 complex in primary microRNA processingGenes Dev2004 1830163027
Not in our library10.1101/gad.1262504
35.
Gregory RI Yan KP Amuthan G Chendrimada T Doratotaj B Cooch N Shiekhattar R The Microprocessor complex mediates the genesis of microRNAsNature2004 432235240
Not in our library10.1038/nature03120
36.
Kim YK Kim VN Processing of intronic microRNAsEMBO J2007 26775783
Not in our library10.1038/sj.emboj.7601512
37.
Okamura K Hagen JW Duan H Tyler DM Lai EC The mirtron pathway generates microRNA-class regulatory RNAs in DrosophilaCell2007 13089100
Not in our library10.1016/j.cell.2007.06.028
38.
Lund E Guttinger S Calado A Dahlberg JE Kutay U Nuclear export of microRNA precursorsScience2004 3039598
Not in our library10.1126/science.1090599
39.
Cheloufi S Dos Santos CO Chong MM Hannon GJ A dicer-independent miRNA biogenesis pathway that requires Ago catalysisNature2010 465584589
Not in our library10.1038/nature09092
40.
Cifuentes D Xue H Taylor DW Patnode H Mishima Y Cheloufi S Ma E Mane S Hannon GJ Lawson ND Wolfe SA Giraldez AJ A novel miRNA processing pathway independent of Dicer requires Argonaute2 catalytic activityScience2010 32816941698
Not in our library10.1126/science.1190809
41.
Yates LA Norbury CJ Gilbert RJ The long and short of microRNACell2013 153516519
Not in our library10.1016/j.cell.2013.04.003
42.
Krol J Loedige I Filipowicz W The widespread regulation of microRNA biogenesis, function and decayNat Rev Genet2010 11597610
Not in our library10.1038/nrg2843
43.
Meister G Tuschl T Mechanisms of gene silencing by double-stranded RNANature2004 431343349
Not in our library10.1038/nature02873
44.
Orom UA Nielsen FC Lund AH MicroRNA-10a binds the 5′UTR of ribosomal protein mRNAs and enhances their translationMol Cell2008 30460471
Not in our library10.1016/j.molcel.2008.05.001
45.
Tay Y Zhang J Thomson AM Lim B Rigoutsos I MicroRNAs to Nanog, Oct4 and Sox2 coding regions modulate embryonic stem cell differentiationNature2008 45511241128
Not in our library10.1038/nature07299
46.
Liu J Control of protein synthesis and mRNA degradation by microRNAsCurr Opin Cell Biol2008 20214221
Not in our library10.1016/j.ceb.2008.01.006
47.
Guo H Ingolia NT Weissman JS Bartel DP Mammalian microRNAs predominantly act to decrease target mRNA levelsNature2010 466835840
Not in our library10.1038/nature09267
48.
Salmena L Poliseno L Tay Y Kats L Pandolfi PP A ceRNA hypothesis: the rosetta stone of a hidden RNA language?Cell2011 146353358
Not in our library10.1016/j.cell.2011.07.014
49.
Tay Y Kats L Salmena L Weiss D Tan SM Ala U Karreth F Poliseno L Provero P Di Cunto F Lieberman J Rigoutsos I Pandolfi PP Coding-independent regulation of the tumor suppressor PTEN by competing endogenous mRNAsCell2011 147344357
Not in our library10.1016/j.cell.2011.09.029
50.
Fineberg SK Kosik KS Davidson BL MicroRNAs potentiate neural developmentNeuron2009 64303309
Not in our library10.1016/j.neuron.2009.10.020
51.
Nowak JS Michlewski G miRNAs in development and pathogenesis of the nervous systemBiochem Soc Trans2013 41815820
Not in our library10.1042/bst20130044
52.
Sempere LF Freemantle S Pitha-Rowe I Moss E Dmitrovsky E Ambros V Expression profiling of mammalian microRNAs uncovers a subset of brain-expressed microRNAs with possible roles in murine and human neuronal differentiationGenome Biol2004 5R13
Not in our library10.1186/gb-2004-5-3-r13
53.
Roese-Koerner B Stappert L Koch P Brustle O Borghese L Pluripotent stem cell-derived somatic stem cells as tool to study the role of microRNAs in early human neural developmentCurr Mol Med2013 13707722
Not in our library10.2174/1566524011313050003
54.
Jeon HM Sohn YW Oh SY Kim SH Beck S Kim S Kim H ID4 imparts chemoresistance and cancer stemness to glioma cells by derepressing miR-9*-mediated suppression of SOX2Cancer Res2011 7134103421
Not in our library10.1158/0008-5472.can-10-3340
55.
Evangelisti C Florian MC Massimi I Dominici C Giannini G Galardi S Bue MC Massalini S McDowell HP Messi E Gulino A Farace MG Ciafrè SA MiR-128 up-regulation inhibits Reelin and DCX expression and reduces neuroblastoma cell motility and invasivenessFASEB J2009 2342764287
Not in our library10.1096/fj.09-134965
56.
Bruno IG Karam R Huang L Bhardwaj A Lou CH Shum EY Song HW Corbett MA Gifford WD Gecz J Pfaff SL Wilkinson MF Identification of a microRNA that activates gene expression by repressing nonsense-mediated RNA decayMol Cell2011 42500510
Not in our library10.1016/j.molcel.2011.04.018
57.
Adlakha YK Saini N MicroRNA-128 downregulates Bax and induces apoptosis in human embryonic kidney cellsCell Mol Life Sci2011 6814151428
Not in our library10.1007/s00018-010-0528-y
58.
Zhang Y Chao T Li R Liu W Chen Y Yan X Gong Y Yin B Qiang B Zhao J Yuan J Peng X MicroRNA-128 inhibits glioma cells proliferation by targeting transcription factor E2F3aJ Mol Med (Berl)2009 874351
Not in our library10.1007/s00109-008-0403-6
59.
Papagiannakopoulos T Friedmann-Morvinski D Neveu P Dugas JC Gill RM Huillard E Liu C Zong H Rowitch DH Barres BA Verma IM Kosik KS Pro-neural miR-128 is a glioma tumor suppressor that targets mitogenic kinasesOncogene2012 3118841895
Not in our library10.1038/onc.2011.380
60.
Godlewski J Nowicki MO Bronisz A Williams S Otsuki A Nuovo G Raychaudhury A Newton HB Chiocca EA Lawler S Targeting of the Bmi-1 oncogene/stem cell renewal factor by microRNA-128 inhibits glioma proliferation and self-renewalCancer Res2008 6891259130
Not in our library10.1158/0008-5472.can-08-2629
61.
Eletto D Russo G Passiatore G Del Valle L Giordano A Khalili K Gualco E Peruzzi F Inhibition of SNAP25 expression by HIV-1 Tat involves the activity of mir-128aJ Cell Physiol2008 216764770
Not in our library10.1002/jcp.21452
62.
Palumbo T Faucz FR Azevedo M Xekouki P Iliopoulos D Stratakis CA Functional screen analysis reveals miR-26b and miR-128 as central regulators of pituitary somatomammotrophic tumor growth through activation of the PTEN-AKT pathwayOncogene2013 3216511659
Not in our library10.1038/onc.2012.190
63.
Guidi M Muinos-Gimeno M Kagerbauer B Marti E Estivill X Espinosa-Parrilla Y Overexpression of miR-128 specifically inhibits the truncated isoform of NTRK3 and upregulates BCL2 in SH-SY5Y neuroblastoma cellsBMC Mol Biol2010 1195
Not in our library10.1186/1471-2199-11-95
64.
Smirnova L Grafe A Seiler A Schumacher S Nitsch R Wulczyn FG Regulation of miRNA expression during neural cell specificationEur J Neurosci2005 2114691477
Not in our library10.1111/j.1460-9568.2005.03978.x
65.
Landgraf P Rusu M Sheridan R Sewer A Iovino N Aravin A Pfeffer S Rice A Kamphorst AO Landthaler M Lin C Socci ND Hermida L Fulci V Chiaretti S Foà R Schliwka J Fuchs U Novosel A Müller RU Schermer B Bissels U Inman J Phan Q Chien M Weir DB Choksi R De Vita G Frezzetti D Trompeter HI A mammalian microRNA expression atlas based on small RNA library sequencingCell2007 12914011414
Not in our library10.1016/j.cell.2007.04.040
66.
Peruzzi P Bronisz A Nowicki MO Wang Y Ogawa D Price R Nakano I Kwon CH Hayes J Lawler SE Ostrowski MC Chiocca EA Godlewski J MicroRNA-128 coordinately targets polycomb repressor complexes in glioma stem cellsNeuro Oncol2013 1512121224
Not in our library10.1093/neuonc/not055
67.
Neurofibromin 1 is a miRNA target in neurons. · 2012
Not checked
68.
Wuchty S Arjona D Li A Kotliarov Y Walling J Ahn S Zhang A Maric D Anolik R Zenklusen JC Fine HA Prediction of Associations between microRNAs and Gene Expression in Glioma BiologyPLoS One2011 6e14681
Not in our library10.1371/journal.pone.0014681
69.
Choudhury NR de Lima AF de Andres-Aguayo L Graf T Caceres JF Rappsilber J Michlewski G Tissue-specific control of brain-enriched miR-7 biogenesisGenes Dev2013 272438
Not in our library10.1101/gad.199190.112
70.
Okuda H Xing F Pandey PR Sharma S Watabe M Pai SK Mo YY Iiizumi-Gairani M Hirota S Liu Y Wu K Pochampally R Watabe K miR-7 suppresses brain metastasis of breast cancer stem-like cells by modulating KLF4Cancer Res2013 7314341444
Not in our library10.1158/0008-5472.can-12-2037
71.
Junn E Lee KW Jeong BS Chan TW Im JY Mouradian MM Repression of alpha-synuclein expression and toxicity by microRNA-7Proc Natl Acad Sci U S A2009 1061305213057
Not in our library10.1073/pnas.0906277106
72.
Dewing AS Rueli RH Robles MJ Nguyen-Wu ED Zeyda T Berry MJ Bellinger FP Expression and regulation of mouse selenoprotein P transcript variants differing in non-coding RNARNA Biol2012 913611369
Not in our library10.4161/rna.22290
73.
Chen H Shalom-Feuerstein R Riley J Zhang SD Tucci P Agostini M Aberdam D Knight RA Genchi G Nicotera P Melino G Vasa-Nicotera M miR-7 and miR-214 are specifically expressed during neuroblastoma differentiation, cortical development and embryonic stem cells differentiation, and control neurite outgrowth in vitroBiochem Biophys Res Commun2010 394921927
Not in our library10.1016/j.bbrc.2010.03.076
74.
Kefas B Godlewski J Comeau L Li Y Abounader R Hawkinson M Lee J Fine H Chiocca EA Lawler S Purow B microRNA-7 inhibits the epidermal growth factor receptor and the Akt pathway and is down-regulated in glioblastomaCancer Res2008 6835663572
Not in our library10.1158/0008-5472.can-07-6639
75.
Edbauer D Neilson JR Foster KA Wang CF Seeburg DP Batterton MN Tada T Dolan BM Sharp PA Sheng M Regulation of synaptic structure and function by FMRP-associated microRNAs miR-125b and miR-132Neuron2010 65373384
Not in our library10.1016/j.neuron.2010.01.005
76.
Wang G Mao W Zheng S Ye J Epidermal growth factor receptor-regulated miR-125a-5p–a metastatic inhibitor of lung cancerFEBS J2009 27655715578
Not in our library10.1111/j.1742-4658.2009.07238.x
77.
Boissart C Nissan X Giraud-Triboult K Peschanski M Benchoua A miR-125 potentiates early neural specification of human embryonic stem cellsDevelopment2012 13912471257
Not in our library10.1242/dev.073627
78.
Lin ST Fu YH miR-23 regulation of lamin B1 is crucial for oligodendrocyte development and myelinationDis Model Mech2009 2178188
Not in our library10.1242/dmm.001065
79.
Siegel C Li J Liu F Benashski SE McCullough LD miR-23a regulation of X-linked inhibitor of apoptosis (XIAP) contributes to sex differences in the response to cerebral ischemiaProc Natl Acad Sci U S A2011 1081166211667
Not in our library10.1073/pnas.1102635108
80.
Wanet A Tacheny A Arnould T Renard P miR-212/132 expression and functions: within and beyond the neuronal compartmentNucleic Acids Res2012 4047424753
Not in our library10.1093/nar/gks151
81.
Klein ME Lioy DT Ma L Impey S Mandel G Goodman RH Homeostatic regulation of MeCP2 expression by a CREB-induced microRNANat Neurosci2007 1015131514
Not in our library10.1038/nn2010
82.
Smith PY Delay C Girard J Papon MA Planel E Sergeant N Buee L Hebert SS MicroRNA-132 loss is associated with tau exon 10 inclusion in progressive supranuclear palsyHum Mol Genet2011 2040164024
Not in our library10.1093/hmg/ddr330
83.
Shaked I Meerson A Wolf Y Avni R Greenberg D Gilboa-Geffen A Soreq H MicroRNA-132 potentiates cholinergic anti-inflammatory signaling by targeting acetylcholinesteraseImmunity2009 31965973
Not in our library10.1016/j.immuni.2009.09.019
84.
Miller BH Zeier Z Xi L Lanz TA Deng S Strathmann J Willoughby D Kenny PJ Elsworth JD Lawrence MS Roth RH Edbauer D Kleiman RJ Wahlestedt C MicroRNA-132 dysregulation in schizophrenia has implications for both neurodevelopment and adult brain functionProc Natl Acad Sci U S A2012 10931253130
Not in our library10.1073/pnas.1113793109
85.
Tognini P Pizzorusso T MicroRNA212/132 family: molecular transducer of neuronal function and plasticityInt J Biochem Cell Biol2012 44610
Not in our library10.1016/j.biocel.2011.10.015
86.
Wayman GA Davare M Ando H Fortin D Varlamova O Cheng HY Marks D Obrietan K Soderling TR Goodman RH Impey S An activity-regulated microRNA controls dendritic plasticity by down-regulating p250GAPProc Natl Acad Sci U S A2008 10590939098
Not in our library10.1073/pnas.0803072105
87.
Clovis YM Enard W Marinaro F Huttner WB De Pietri Tonelli D Convergent repression of Foxp2 3′UTR by miR-9 and miR-132 in embryonic mouse neocortex: implications for radial migration of neuronsDevelopment2012 13933323342
Not in our library10.1242/dev.078063
88.
MicroRNA and Target Protein Patterns Reveal Physiopathological Features of Glioma Subtypes · 2011
No notice
89.
MicroRNA‐132 regulates recognition memory and synaptic plasticity in the perirhinal cortex · 2012
No notice
90.
Strum JC Johnson JH Ward J Xie H Feild J Hester A Alford A Waters KM MicroRNA 132 regulates nutritional stress-induced chemokine production through repression of SirT1Mol Endocrinol2009 2318761884
Not in our library10.1210/me.2009-0117
91.
Huang Y Lei Y Zhang H Hou L Zhang M Dayton AI MicroRNA regulation of STAT4 protein expression: rapid and sensitive modulation of IL-12 signaling in human natural killer cellsBlood2011 11867936802
Not in our library10.1182/blood-2011-05-356162
92.
Godoy J Nishimura M Webster NJ Gonadotropin-releasing hormone induces miR-132 and miR-212 to regulate cellular morphology and migration in immortalized LbetaT2 pituitary gonadotrope cellsMol Endocrinol2011 25810820
Not in our library10.1210/me.2010-0352
93.
Alvarez-Saavedra M Antoun G Yanagiya A Oliva-Hernandez R Cornejo-Palma D Perez-Iratxeta C Sonenberg N Cheng HY miRNA-132 orchestrates chromatin remodeling and translational control of the circadian clockHum Mol Genet2011 20731751
Not in our library10.1093/hmg/ddq519
94.
Potential impact of miR-137 and its targets in schizophrenia · 2013
Not checked
95.
miR-124 and miR-137 inhibit proliferation of glioblastoma multiforme cells and induce differentiation of brain tumor stem cells · 2008
No notice
96.
Smrt RD Szulwach KE Pfeiffer RL Li X Guo W Pathania M Teng ZQ Luo Y Peng J Bordey A Jin P Zhao X MicroRNA miR-137 regulates neuronal maturation by targeting ubiquitin ligase mind bomb-1Stem Cells2010 2810601070
Not in our library10.1002/stem.431
97.
Kwon E Wang W Tsai LH Validation of schizophrenia-associated genes CSMD1, C10orf26, CACNA1C and TCF4 as miR-137 targetsMol Psychiatry2013 181112
Not in our library10.1038/mp.2011.170
98.
Li KK Yang L Pang JC Chan AK Zhou L Mao Y Wang Y Lau KM Poon WS Shi Z Ng HK MIR-137 suppresses growth and invasion, is downregulated in oligodendroglial tumors and targets CSE1LBrain Pathol2013 23426439
Not in our library10.1111/bpa.12015
99.
Chen L Wang X Wang H Li Y Yan W Han L Zhang K Zhang J Wang Y Feng Y Pu P Jiang T Kang C Jiang C miR-137 is frequently down-regulated in glioblastoma and is a negative regulator of Cox-2Eur J Cancer2012 4831043111
Not in our library10.1016/j.ejca.2012.02.007
100.
Sun G Ye P Murai K Lang MF Li S Zhang H Li W Fu C Yin J Wang A Ma X Shi Y miR-137 forms a regulatory loop with nuclear receptor TLX and LSD1 in neural stem cellsNat Commun2011 2529
Not in our library10.1038/ncomms1532
101.
Willemsen MH Valles A Kirkels LA Mastebroek M Olde Loohuis N Kos A Wissink-Lindhout WM de Brouwer AP Nillesen WM Pfundt R Holder-Espinasse M Vallée L Andrieux J Coppens-Hofman MC Rensen H Hamel BC van Bokhoven H Aschrafi A Kleefstra T Chromosome 1p21.3 microdeletions comprising DPYD and MIR137 are associated with intellectual disabilityJ Med Genet2011 48810818
Not in our library10.1136/jmedgenet-2011-100294
102.
Geekiyanage H Chan C MicroRNA-137/181c regulates serine palmitoyltransferase and in turn amyloid beta, novel targets in sporadic Alzheimer’s diseaseJ Neurosci2011 311482014830
Not in our library10.1523/jneurosci.3883-11.2011
103.
Li RY Chen LC Zhang HY Du WZ Feng Y Wang HB Wen JQ Liu X Li XF Sun Y Yang DB Jiang T Li YL Jiang CL MiR-139 inhibits Mcl-1 expression and potentiates TMZ-induced apoptosis in gliomaCNS Neurosci Ther2013 19477483
Not in our library10.1111/cns.12089
104.
Bao W Fu HJ Xie QS Wang L Zhang R Guo ZY Zhao J Meng YL Ren XL Wang T Li Q Jin BQ Yao LB Wang RA Fan DM Chen SY Jia LT Yang AG HER2 interacts with CD44 to up-regulate CXCR4 via epigenetic silencing of microRNA-139 in gastric cancer cellsGastroenterology2011 14120762087
Not in our library10.1053/j.gastro.2011.08.050
105.
Hasseine LK Hinault C Lebrun P Gautier N Paul-Bellon R Van Obberghen E miR-139 impacts FoxO1 action by decreasing FoxO1 protein in mouse hepatocytesBiochem Biophys Res Commun2009 39012781282
Not in our library10.1016/j.bbrc.2009.10.135
106.
Conaco C Otto S Han JJ Mandel G Reciprocal actions of REST and a microRNA promote neuronal identityProc Natl Acad Sci U S A2006 10324222427
Not in our library10.1073/pnas.0511041103
107.
Tan X Wang S Yang B Zhu L Yin B Chao T Zhao J Yuan J Qiang B Peng X The CREB-miR-9 negative feedback minicircuitry coordinates the migration and proliferation of glioma cellsPLoS One2012 7e49570
Not in our library10.1371/journal.pone.0049570
108.
Microarray analysis of microRNA expression in the developing mammalian brain · 2004
No notice
109.
Zhao C Sun G Li S Shi Y A feedback regulatory loop involving microRNA-9 and nuclear receptor TLX in neural stem cell fate determinationNat Struct Mol Biol2009 16365371
Not in our library10.1038/nsmb.1576
110.
Tatro ET Hefler S Shumaker-Armstrong S Soontornniyomkij B Yang M Yermanos A Wren N Moore DJ Achim CL Modulation of BK Channel by MicroRNA-9 in Neurons After Exposure to HIV and MethamphetamineJ Neuroimmune Pharmacol2013 8512101223
Not in our library10.1007/s11481-013-9446-8
111.
Tan SL Ohtsuka T Gonzalez A Kageyama R MicroRNA9 regulates neural stem cell differentiation by controlling Hes1 expression dynamics in the developing brainGenes Cells2012 17952961
Not in our library10.1111/gtc.12009
112.
Jung HJ Coffinier C Choe Y Beigneux AP Davies BS Yang SH Barnes RH 2nd Hong J Sun T Pleasure SJ Young SG Fong LG Regulation of prelamin A but not lamin C by miR-9, a brain-specific microRNAProc Natl Acad Sci U S A2012 109E423E431
Not in our library10.1073/pnas.1111780109
113.
Makeyev EV Zhang J Carrasco MA Maniatis T The MicroRNA miR-124 promotes neuronal differentiation by triggering brain-specific alternative pre-mRNA splicingMol Cell2007 27435448
Not in our library10.1016/j.molcel.2007.07.015
114.
Cheng LC Pastrana E Tavazoie M Doetsch F miR-124 regulates adult neurogenesis in the subventricular zone stem cell nicheNat Neurosci2009 12399408
Not in our library10.1038/nn.2294
115.
Lv Z Yang L MiR-124 inhibits the growth of glioblastoma through the downregulation of SOS1Mol Med Rep2013 8345349
Not in our library10.3892/mmr.2013.1561
116.
Yoo AS Sun AX Li L Shcheglovitov A Portmann T Li Y Lee-Messer C Dolmetsch RE Tsien RW Crabtree GR MicroRNA-mediated conversion of human fibroblasts to neuronsNature2011 476228231
Not in our library10.1038/nature10323
117.
Xia H Cheung WK Ng SS Jiang X Jiang S Sze J Leung GK Lu G Chan DT Bian XW Kung HF Poon WS Lin MC Loss of brain-enriched miR-124 microRNA enhances stem-like traits and invasiveness of glioma cellsJ Biol Chem2012 28799629971
Not in our library10.1074/jbc.m111.332627
118.
Sober S Laan M Annilo T MicroRNAs miR-124 and miR-135a are potential regulators of the mineralocorticoid receptor gene (NR3C2) expressionBiochem Biophys Res Commun2010 391727732
Not in our library10.1016/j.bbrc.2009.11.128
119.
Deng X Ma L Wu M Zhang G Jin C Guo Y Liu R miR-124 radiosensitizes human glioma cells by targeting CDK4J Neurooncol2013 114263274
Not in our library10.1007/s11060-013-1179-2
120.
Doeppner TR Doehring M Bretschneider E Zechariah A Kaltwasser B Muller B Koch JC Bahr M Hermann DM Michel U MicroRNA-124 protects against focal cerebral ischemia via mechanisms involving Usp14-dependent REST degradationActa Neuropathol2013 126251265
Not in our library10.1007/s00401-013-1142-5
121.
Liu X Li F Zhao S Luo Y Kang J Zhao H Yan F Li S Ji X MicroRNA-124-mediated regulation of inhibitory member of apoptosis-stimulating protein of p53 family in experimental strokeStroke2013 4419731980
Not in our library10.1161/strokeaha.111.000613
122.
Dutta R Chomyk AM Chang A Ribaudo MV Deckard SA Doud MK Edberg DD Bai B Li M Baranzini SE Fox RJ Staugaitis SM Macklin WB Trapp BD Hippocampal demyelination and memory dysfunction are associated with increased levels of the neuronal microRNA miR-124 and reduced AMPA receptorsAnn Neurol2013 73637645
Not in our library10.1002/ana.23860
123.
Yoo AS Staahl BT Chen L Crabtree GR MicroRNA-mediated switching of chromatin-remodelling complexes in neural developmentNature2009 460642646
Not in our library10.1038/nature08139
124.
Arvanitis DN Jungas T Behar A Davy A Ephrin-B1 reverse signaling controls a posttranscriptional feedback mechanism via miR-124Mol Cell Biol2010 3025082517
Not in our library10.1128/mcb.01620-09
125.
Visvanathan J Lee S Lee B Lee JW Lee SK The microRNA miR-124 antagonizes the anti-neural REST/SCP1 pathway during embryonic CNS developmentGenes Dev2007 21744749
Not in our library10.1101/gad.1519107
126.
Ponomarev ED Veremeyko T Barteneva NS Visualization and quantitation of the expression of microRNAs and their target genes in neuroblastoma single cells using imaging cytomeBMC Res Notes2011 4517
Not in our library10.1186/1756-0500-4-517
127.
Silber J Hashizume R Felix T Hariono S Yu M Berger MS Huse JT VandenBerg SR James CD Hodgson JG Gupta N Expression of miR-124 inhibits growth of medulloblastoma cellsNeuro Oncol2013 158390
Not in our library10.1093/neuonc/nos281
128.
Lawson SK Dobrikova EY Shveygert M Gromeier M p38alpha mitogen-activated protein kinase depletion and repression of signal transduction to translation machinery by miR-124 and -128 in neuronsMol Cell Biol2013 33127135
Not in our library10.1128/mcb.00695-12
129.
Ponomarev ED Veremeyko T Barteneva N Krichevsky AM Weiner HL MicroRNA-124 promotes microglia quiescence and suppresses EAE by deactivating macrophages via the C/EBP-alpha-PU.1 pathwayNat Med2011 176470
Not in our library10.1038/nm.2266
130.
Franke K Otto W Johannes S Baumgart J Nitsch R Schumacher S miR-124-regulated RhoG reduces neuronal process complexity via ELMO/Dock180/Rac1 and Cdc42 signallingEMBO J2012 3129082921
Not in our library10.1038/emboj.2012.130
131.
Weng R Cohen SM Drosophila miR-124 regulates neuroblast proliferation through its target anachronismDevelopment2012 13914271434
Not in our library10.1242/dev.075143
132.
Sanuki R Onishi A Koike C Muramatsu R Watanabe S Muranishi Y Irie S Uneo S Koyasu T Matsui R Chérasse Y Urade Y Watanabe D Kondo M Yamashita T Furukawa T miR-124a is required for hippocampal axogenesis and retinal cone survival through Lhx2 suppressionNat Neurosci2011 1411251134
Not in our library10.1038/nn.2897
133.
Fang M Wang J Zhang X Geng Y Hu Z Rudd JA Ling S Chen W Han S The miR-124 regulates the expression of BACE1/beta-secretase correlated with cell death in Alzheimer’s diseaseToxicol Lett2012 20994105
Not in our library10.1016/j.toxlet.2011.11.032
134.
Liu K Liu Y Mo W Qiu R Wang X Wu JY He R MiR-124 regulates early neurogenesis in the optic vesicle and forebrain, targeting NeuroD1Nucleic Acids Res2011 3928692879
Not in our library10.1093/nar/gkq904
135.
Niu CS Yang Y Cheng CD MiR-134 regulates the proliferation and invasion of glioblastoma cells by reducing Nanog expressionInt J Oncol2013 4215331540
Not in our library10.3892/ijo.2013.1844
136.
Schratt GM Tuebing F Nigh EA Kane CG Sabatini ME Kiebler M Greenberg ME A brain-specific microRNA regulates dendritic spine developmentNature2006 439283289
Not in our library10.1038/nature04367
137.
Bicker S Khudayberdiev S Weiss K Zocher K Baumeister S Schratt G The DEAH-box helicase DHX36 mediates dendritic localization of the neuronal precursor-microRNA-134Genes Dev2013 27991996
Not in our library10.1101/gad.211243.112
138.
Tay YM Tam WL Ang YS Gaughwin PM Yang H Wang W Liu R George J Ng HH Perera RJ Lufkin T Rigoutsos I Thomson AM Lim B MicroRNA-134 modulates the differentiation of mouse embryonic stem cells, where it causes post-transcriptional attenuation of Nanog and LRH1Stem Cells2008 261729
Not in our library10.1634/stemcells.2007-0295
139.
Li J Wang Y Luo J Fu Z Ying J Yu Y Yu W miR-134 inhibits epithelial to mesenchymal transition by targeting FOXM1 in non-small cell lung cancer cellsFEBS Lett2012 58637613765
Not in our library10.1016/j.febslet.2012.09.016
140.
Ni J Gao Y Gong S Guo S Hisamitsu T Jiang X Regulation of mu-opioid type 1 receptors by microRNA134 in dorsal root ganglion neurons following peripheral inflammationEur J Pain2013 17313323
Not in our library10.1002/j.1532-2149.2012.00197.x
141.
Hirota T Date Y Nishibatake Y Takane H Fukuoka Y Taniguchi Y Burioka N Shimizu E Nakamura H Otsubo K Ieiri I Dihydropyrimidine dehydrogenase (DPD) expression is negatively regulated by certain microRNAs in human lung tissuesLung Cancer2012 771623
Not in our library10.1016/j.lungcan.2011.12.018
142.
Han L Wen Z Lynn RC Baudet ML Holt CE Sasaki Y Bassell GJ Zheng JQ Regulation of chemotropic guidance of nerve growth cones by microRNAMol Brain2011 440
Not in our library10.1186/1756-6606-4-40
143.
Thayanithy V Sarver AL Kartha RV Li L Angstadt AY Breen M Steer CJ Modiano JF Subramanian S Perturbation of 14q32 miRNAs-cMYC gene network in osteosarcomaBone2012 50171181
Not in our library10.1016/j.bone.2011.10.012
144.
Fiore R Khudayberdiev S Christensen M Siegel G Flavell SW Kim TK Greenberg ME Schratt G Mef2-mediated transcription of the miR379-410 cluster regulates activity-dependent dendritogenesis by fine-tuning Pumilio2 protein levelsEMBO J2009 28697710
Not in our library10.1038/emboj.2009.10
145.
Gaughwin P Ciesla M Yang H Lim B Brundin P Stage-specific modulation of cortical neuronal development by Mmu-miR-134Cereb Cortex2011 2118571869
Not in our library10.1093/cercor/bhq262
146.
Gao J Wang WY Mao YW Graff J Guan JS Pan L Mak G Kim D Su SC Tsai LH A novel pathway regulates memory and plasticity via SIRT1 and miR-134Nature2010 46611051109
Not in our library10.1038/nature09271
147.
Meerson A Cacheaux L Goosens KA Sapolsky RM Soreq H Kaufer D Changes in brain MicroRNAs contribute to cholinergic stress reactionsJ Mol Neurosci2010 404755
Not in our library10.1007/s12031-009-9252-1
148.
Golubovskaya VM Sumbler B Ho B Yemma M Cance WG miR-138 and MiR-135 directly target focal adhesion kinase, inhibit cell invasion, and increase sensitivity to chemotherapy in cancer cellsAnticancer Agents Med Chem2014 1411828
Not in our library10.2174/187152061401140108113435
149.
Xu XM Qian JC Deng ZL Cai Z Tang T Wang P Zhang KH Cai JP Expression of miR-21, miR-31, miR-96 and miR-135b is correlated with the clinical parameters of colorectal cancerOncol Lett2012 4339345
Not in our library10.3892/ol.2012.714
150.
Li Z Hassan MQ Volinia S van Wijnen AJ Stein JL Croce CM Lian JB Stein GS A microRNA signature for a BMP2-induced osteoblast lineage commitment programProc Natl Acad Sci U S A2008 1051390613911
Not in our library10.1073/pnas.0804438105
151.
Nagel R le Sage C Diosdado B van der Waal M Oude Vrielink JA Bolijn A Meijer GA Agami R Regulation of the adenomatous polyposis coli gene by the miR-135 family in colorectal cancerCancer Res2008 6857955802
Not in our library10.1158/0008-5472.can-08-0951
152.
Zhao S Deng Y Liu Y Chen X Yang G Mu Y Zhang D Kang J Wu Z MicroRNA-153 is tumor suppressive in glioblastoma stem cellsMol Biol Rep2013 4027892798
Not in our library10.1007/s11033-012-2278-4
153.
Stappert L Borghese L Roese-Koerner B Weinhold S Koch P Terstegge S Uhrberg M Wernet P Brustle O MicroRNA-based promotion of human neuronal differentiation and subtype specificationPLoS One2013 8e59011
Not in our library10.1371/journal.pone.0059011
154.
Mandemakers W Abuhatzira L Xu H Caromile LA Hebert SS Snellinx A Morais VA Matta S Cai T Notkins AL De Strooper B Co-regulation of intragenic microRNA miR-153 and its host gene Ia-2 beta: identification of miR-153 target genes with functions related to IA-2beta in pancreas and brainDiabetologia2013 5615471556
Not in our library10.1007/s00125-013-2901-5
155.
Long JM Ray B Lahiri DK MicroRNA-153 physiologically inhibits expression of amyloid-beta precursor protein in cultured human fetal brain cells and is dysregulated in a subset of Alzheimer disease patientsJ Biol Chem2012 2873129831310
Not in our library10.1074/jbc.m112.366336
156.
Liang C Zhu H Xu Y Huang L Ma C Deng W Liu Y Qin C MicroRNA-153 negatively regulates the expression of amyloid precursor protein and amyloid precursor-like protein 2Brain Res2012 1455103113
Not in our library10.1016/j.brainres.2011.10.051
157.
Doxakis E Post-transcriptional regulation of alpha-synuclein expression by mir-7 and mir-153J Biol Chem2010 2851272612734
Not in our library10.1074/jbc.m109.086827
158.
Xu J Liao X Wong C Downregulations of B-cell lymphoma 2 and myeloid cell leukemia sequence 1 by microRNA 153 induce apoptosis in a glioblastoma cell line DBTRG-05MGInt J Cancer2010 12610291035
Not in our library10.1002/ijc.24823
159.
Xu Q Sun Q Zhang J Yu J Chen W Zhang Z Downregulation of miR-153 contributes to epithelial-mesenchymal transition and tumor metastasis in human epithelial cancerCarcinogenesis2013 34539549
Not in our library10.1093/carcin/bgs374
160.
Rao SA Arimappamagan A Pandey P Santosh V Hegde AS Chandramouli BA Somasundaram K miR-219-5p inhibits receptor tyrosine kinase pathway by targeting EGFR in glioblastomaPLoS One2013 8e63164
Not in our library10.1371/journal.pone.0063164
161.
Investigation of post-transcriptional gene regulatory networks associated with autism spectrum disorders by microRNA expression profiling of lymphoblastoid cell lines · 2010
No notice
162.
Zhao X He X Han X Yu Y Ye F Chen Y Hoang T Xu X Mi QS Xin M Wang F Appel B Lu QR MicroRNA-mediated control of oligodendrocyte differentiationNeuron2010 65612626
Not in our library10.1016/j.neuron.2010.02.018
163.
Dugas JC Cuellar TL Scholze A Ason B Ibrahim A Emery B Zamanian JL Foo LC McManus MT Barres BA Dicer1 and miR-219 Are required for normal oligodendrocyte differentiation and myelinationNeuron2010 65597611
Not in our library10.1016/j.neuron.2010.01.027
164.
Shin D Shin JY McManus MT Ptacek LJ Fu YH Dicer ablation in oligodendrocytes provokes neuronal impairment in miceAnn Neurol2009 66843857
Not in our library10.1002/ana.21927
165.
Kocerha J Faghihi MA Lopez-Toledano MA Huang J Ramsey AJ Caron MG Sales N Willoughby D Elmen J Hansen HF Orum H Kauppinen S Kenny PJ Wahlestedt C MicroRNA-219 modulates NMDA receptor-mediated neurobehavioral dysfunctionProc Natl Acad Sci U S A2009 10635073512
Not in our library10.1073/pnas.0805854106
166.
Cheng HY Papp JW Varlamova O Dziema H Russell B Curfman JP Nakazawa T Shimizu K Okamura H Impey S Obrietan K microRNA modulation of circadian-clock period and entrainmentNeuron2007 54813829
Not in our library10.1016/j.neuron.2007.05.017
167.
Giraldez AJ Cinalli RM Glasner ME Enright AJ Thomson JM Baskerville S Hammond SM Bartel DP Schier AF MicroRNAs regulate brain morphogenesis in zebrafishScience2005 308833838
Not in our library10.1126/science.1109020
168.
De Pietri TD Pulvers JN Haffner C Murchison EP Hannon GJ Huttner WB miRNAs are essential for survival and differentiation of newborn neurons but not for expansion of neural progenitors during early neurogenesis in the mouse embryonic neocortexDevelopment2008 13539113921
Not in our library10.1242/dev.025080
169.
Huang T Liu Y Huang M Zhao X Cheng L Wnt1-cre-mediated conditional loss of Dicer results in malformation of the midbrain and cerebellum and failure of neural crest and dopaminergic differentiation in miceJ Mol Cell Biol2010 2152163
Not in our library10.1093/jmcb/mjq008
170.
Schaefer A O’Carroll D Tan CL Hillman D Sugimori M Llinas R Greengard P Cerebellar neurodegeneration in the absence of microRNAsJ Exp Med2007 20415531558
Not in our library10.1084/jem.20070823
171.
Kawase-Koga Y Low R Otaegi G Pollock A Deng H Eisenhaber F Maurer-Stroh S Sun T RNAase-III enzyme Dicer maintains signaling pathways for differentiation and survival in mouse cortical neural stem cellsJ Cell Sci2010 123586594
Not in our library10.1242/jcs.059659
172.
Bicker S Schratt G microRNAs: tiny regulators of synapse function in development and diseaseJ Cell Mol Med2008 1214661476
Not in our library10.1111/j.1582-4934.2008.00400.x
173.
Fiore R Siegel G Schratt G MicroRNA function in neuronal development, plasticity and diseaseBiochim Biophys Acta2008 1779471478
Not in our library10.1016/j.bbagrm.2007.12.006
174.
Stark KL Xu B Bagchi A Lai WS Liu H Hsu R Wan X Pavlidis P Mills AA Karayiorgou M Gogos JA Altered brain microRNA biogenesis contributes to phenotypic deficits in a 22q11-deletion mouse modelNat Genet2008 40751760
Not in our library10.1038/ng.138
175.
Godlewski J Newton HB Chiocca EA Lawler SE MicroRNAs and glioblastoma; the stem cell connectionCell Death Differ2010 17221228
Not in our library10.1038/cdd.2009.71
176.
Cogswell JP Ward J Taylor IA Waters M Shi Y Cannon B Kelnar K Kemppainen J Brown D Chen C Prinjha RK Richardson JC Saunders AM Roses AD Richards CA Identification of miRNA changes in Alzheimer’s disease brain and CSF yields putative biomarkers and insights into disease pathwaysJ Alzheimers Dis2008 142741
Not in our library10.3233/jad-2008-14103
177.
Zeng Y Regulation of the mammalian nervous system by microRNAsMol Pharmacol2009 75259264
Not in our library10.1124/mol.108.052118
178.
Finnerty JR Wang WX Hebert SS Wilfred BR Mao G Nelson PT The miR-15/107 group of microRNA genes: evolutionary biology, cellular functions, and roles in human diseasesJ Mol Biol2010 402491509
Not in our library10.1016/j.jmb.2010.07.051
179.
Vo N Klein ME Varlamova O Keller DM Yamamoto T Goodman RH Impey S A cAMP-response element binding protein-induced microRNA regulates neuronal morphogenesisProc Natl Acad Sci U S A2005 1021642616431
Not in our library10.1073/pnas.0508448102
180.
Lim LP Lau NC Garrett-Engele P Grimson A Schelter JM Castle J Bartel DP Linsley PS Johnson JM Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAsNature2005 433769773
Not in our library10.1038/nature03315
181.
Kole AJ Swahari V Hammond SM Deshmukh M miR-29b is activated during neuronal maturation and targets BH3-only genes to restrict apoptosisGenes Dev2011 25125130
Not in our library10.1101/gad.1975411
182.
Louis DN Ohgaki H Wiestler OD Cavenee WK Burger PC Jouvet A Scheithauer BW Kleihues P The 2007 WHO classification of tumours of the central nervous systemActa Neuropathol2007 11497109
Not in our library10.1007/s00401-007-0243-4
183.
Ohgaki H Kleihues P Population-based studies on incidence, survival rates, and genetic alterations in astrocytic and oligodendroglial gliomasJ Neuropathol Exp Neurol2005 64479489
Not in our library10.1093/jnen/64.6.479
184.
Koshkin PA Chistiakov DA Nikitin AG Konovalov AN Potapov AA Usachev DY Pitskhelauri DI Kobyakov GL Shishkina LV Chekhonin VP Analysis of expression of microRNAs and genes involved in the control of key signaling mechanisms that support or inhibit development of brain tumors of different gradesClin Chim Acta2014 9430C5562
Not in our library10.1016/j.cca.2014.01.001
185.
Lai NS Dong QS Ding H Miao ZL Lin YC MicroRNA-210 overexpression predicts poorer prognosis in glioma patientsJ Clin Neurosci2013 Sep 11, doi:10.1016/j.jocn.2013.06.024
Not in our library10.1016/j.jocn.2013.06.024
186.
Wang S Lu S Geng S Ma S Liang Z Jiao B Decreased expression of microRNA-206 correlates with poor clinical outcome in patients with malignant astrocytomasPathol Oncol Res2014 doi: 10.1007/s12253-013-9701-6
Not in our library10.1007/s12253-013-9701-6
187.
Yang TQ Luo XJ Wu TF Ding DD Zhao ZH Chen GL Xie XS Li B Wei YX Guo LC Zhang Y Huang YL Zhou YX Du ZW miR-16 inhibits glioma cell growth and invasion through the suppression of BCL2 and NF-kappaB1/MMP-9 signaling pathwayCancer Sci2014 doi:10.1007/s12253-013-9701-6
Not in our library10.1111/cas.12351
188.
Zhang Y Chen X Lian H Liu J Zhou B Han S Peng B Yin J Liu W He X MicroRNA-503 acts as a tumor suppressor in glioblastoma for multiple antitumor effects by targeting IGF-1ROncol Rep2013
Not in our library10.3892/or.2013.2951
189.
Chen Z Li D Cheng Q Ma Z Jiang B Peng R Chen R Cao Y Wan X MicroRNA-203 inhibits the proliferation and invasion of U251 glioblastoma cells by directly targeting PLD2Mol Med Rep2014 9503508
Not in our library10.3892/mmr.2013.1814
190.
Wu Z Wu Y Tian Y Sun X Liu J Ren H Liang C Song L Hu H Wang L Jiao B Differential effects of miR-34c-3p and miR-34c-5p on the proliferation, apoptosis and invasion of glioma cellsOncol Lett2013 614471452
Not in our library10.3892/ol.2013.1579
191.
Dai DW Lu Q Wang LX Zhao WY Cao YQ Li YN Han GS Liu JM Yue ZJ Decreased miR-106a inhibits glioma cell glucose uptake and proliferation by targeting SLC2A3 in GBMBMC Cancer2013 13478
Not in our library10.1186/1471-2407-13-478
192.
Wang XR Luo H Li HL Cao L Wang XF Yan W Wang YY Zhang JX Jiang T Kang CS Liu N You YP Chinese Glioma Cooperative Group (CGCG)Overexpressed let-7a inhibits glioma cell malignancy by directly targeting K-ras, independently of PTENNeuro Oncol2013 1514911501
Not in our library10.1093/neuonc/not107
193.
Song L Huang Q Chen K Liu L Lin C Dai T Yu C Wu Z Li J miR-218 inhibits the invasive ability of glioma cells by direct downregulation of IKK-betaBiochem Biophys Res Commun2010 402135140
Not in our library10.1016/j.bbrc.2010.10.003
194.
Glasgow SM Laug D Brawley VS Zhang Z Corder A Yin Z Wong ST Li XN Foster AE Ahmed N Deneen B The miR-223/nuclear factor I-A axis regulates glial precursor proliferation and tumorigenesis in the CNSJ Neurosci2013 331356013568
Not in our library10.1523/jneurosci.0321-13.2013
195.
Li SZ Hu YY Zhao J Zhao YB Sun JD Yang YF Ji CC Liu ZB Cao WD Qu Y Liu WP Cheng G Fei Z MicroRNA-34a induces apoptosis in the human glioma cell line, A172, through enhanced ROS production and NOX2 expressionBiochem Biophys Res Commun2014
Not in our library10.1016/j.bbrc.2013.12.136
196.
Rani SB Rathod SS Karthik S Kaur N Muzumdar D Shiras AS MiR-145 functions as a tumor-suppressive RNA by targeting Sox9 and adducin 3 in human glioma cellsNeuro Oncol2013 1513021316
Not in our library10.1093/neuonc/not090
197.
Li A Lin X Tan X Yin B Han W Zhao J Yuan J Qiang B Peng X Circadian gene Clock contributes to cell proliferation and migration of glioma and is directly regulated by tumor-suppressive miR-124FEBS Lett2013 58724552460
Not in our library10.1016/j.febslet.2013.06.018
198.
MicroRNA-137 is downregulated in glioblastoma and inhibits the stemness of glioma stem cells by targeting RTVP-1 · 2013
No notice
199.
Qiu S Huang D Yin D Li F Li X Kung HF Peng Y Suppression of tumorigenicity by microRNA-138 through inhibition of EZH2-CDK4/6-pRb-E2F1 signal loop in glioblastoma multiformeBiochim Biophys Acta1832 201316971707
Not in our library10.1016/j.bbadis.2013.05.015
200.
Chen SM Chen HC Chen SJ Huang CY Chen PY Wu TW Feng LY Tsai HC Lui TN Hsueh C Wei KC MicroRNA-495 inhibits proliferation of glioblastoma multiforme cells by downregulating cyclin-dependent kinase 6World J Surg Oncol2013 1187
Not in our library10.1186/1477-7819-11-87
201.
He Z Cen D Luo X Li D Li P Liang L Meng Z Downregulation of miR-383 promotes glioma cell invasion by targeting insulin-like growth factor 1 receptorMed Oncol2013 30557
Not in our library10.1007/s12032-013-0557-0
202.
Peng B Hu S Jun Q Luo D Zhang X Zhao H Li D MicroRNA-200b targets CREB1 and suppresses cell growth in human malignant gliomaMol Cell Biochem2013 3795158
Not in our library10.1007/s11010-013-1626-6
203.
MicroRNA-195 inhibits the proliferation of human glioma cells by directly targeting cyclin D1 and cyclin E1. · 2013
Not checked
204.
Zhao S Liu H Liu Y Wu J Wang C Hou X Chen X Yang G Zhao L Che H Bi Y Wang H Peng F Ai J miR-143 inhibits glycolysis and depletes stemness of glioblastoma stem-like cellsCancer Lett2013 333253260
Not in our library10.1016/j.canlet.2013.01.039
205.
Chen L Chen XR Zhang R Li P Liu Y Yan K Jiang XD MicroRNA-107 inhibits glioma cell migration and invasion by modulating Notch2 expressionJ Neurooncol2013 1125966
Not in our library10.1007/s11060-012-1037-7
206.
Wang S Lu S Geng S Ma S Liang Z Jiao B Expression and clinical significance of microRNA-326 in human glioma miR-326 expression in gliomaMed Oncol2013 30373
Not in our library10.1007/s12032-012-0373-y
207.
Ying Z Li Y Wu J Zhu X Yang Y Tian H Li W Hu B Cheng SY Li M Loss of miR-204 expression enhances glioma migration and stem cell-like phenotypeCancer Res2013 73990999
Not in our library10.1158/0008-5472.can-12-2895
208.
Zhao Z Tan X Zhao A Zhu L Yin B Yuan J Qiang B Peng X microRNA-214-mediated UBC9 expression in gliomaBMB Rep2012 45641646
Not in our library10.5483/bmbrep.2012.45.11.097
209.
Guo P Lan J Ge J Nie Q Mao Q Qiu Y miR-708 acts as a tumor suppressor in human glioblastoma cellsOncol Rep2013 30870876
Not in our library10.3892/or.2013.2526
210.
Fox JL Dews M Minn AJ Thomas-Tikhonenko A Targeting of TGFbeta signature and its essential component CTGF by miR-18 correlates with improved survival in glioblastomaRNA2013 19177190
Not in our library10.1261/rna.036467.112
211.
Uziel T Karginov FV Xie S Parker JS Wang YD Gajjar A He L Ellison D Gilbertson RJ Hannon G Roussel MF The miR-17 92 cluster collaborates with the Sonic Hedgehog pathway in medulloblastomaProc Natl Acad Sci U S A2009 10628122817
Not in our library10.1073/pnas.0809579106
212.
Reduced Expression of Brain-Enriched microRNAs in Glioblastomas Permits Targeted Regulation of a Cell Death Gene · 2011
No notice
213.
Ciafre SA Galardi S Mangiola A Ferracin M Liu CG Sabatino G Negrini M Maira G Croce CM Farace MG Extensive modulation of a set of microRNAs in primary glioblastomaBiochem Biophys Res Commun2005 33413511358
Not in our library10.1016/j.bbrc.2005.07.030
214.
Li KK Pang JC Ching AK Wong CK Kong X Wang Y Zhou L Chen Z Ng HK miR-124 is frequently down-regulated in medulloblastoma and is a negative regulator of SLC16A1Hum Pathol2009 4012341243
Not in our library10.1016/j.humpath.2009.02.003
215.
Li Y Wang Y Yu L Sun C Cheng D Yu S Wang Q Yan Y Kang C Jin S An T Shi C Xu J Wei C Liu J Sun J Wen Y Zhao S Kong Y miR-146b-5p inhibits glioma migration and invasion by targeting MMP16Cancer Lett2013 339260269
Not in our library10.1016/j.canlet.2013.06.018
216.
Jiang J Yang J Wang Z Wu G Liu F TFAM is directly regulated by miR-23b in gliomaOncol Rep2013 3021052110
Not in our library10.3892/or.2013.2712
217.
Hu X Chen D Cui Y Li Z Huang J Targeting microRNA-23a to inhibit glioma cell invasion via HOXD10Sci Rep2013 33423
Not in our library10.1038/srep03423
218.
Delic S Lottmann N Stelzl A Liesenberg F Wolter M Gotze S Zapatka M Shiio Y Sabel MC Felsberg J Reifenberger G Riemenschneider MJ MiR-328 promotes glioma cell invasion via SFRP1-dependent Wnt-signaling activationNeuro Oncol2014 16179190
Not in our library10.1093/neuonc/not164
219.
Liu F Gong J Huang W Wang Z Wang M Yang J Wu C Wu Z Han B MicroRNA-106b-5p boosts glioma tumorigensis by targeting multiple tumor suppressor genesOncogene2013
Not in our library10.1038/onc.2013.428
220.
Ling N Gu J Lei Z Li M Zhao J Zhang HT Li X microRNA-155 regulates cell proliferation and invasion by targeting FOXO3a in gliomaOncol Rep2013 3021112118
Not in our library10.3892/or.2013.2685
221.
Sun B Pu B Chu D Chu X Li W Wei D MicroRNA-650 expression in glioma is associated with prognosis of patientsJ Neurooncol2013 115375380
Not in our library10.1007/s11060-013-1243-y
222.
Wang K Wang X Zou J Zhang A Wan Y Pu P Song Z Qian C Chen Y Yang S Wang Y miR-92b controls glioma proliferation and invasion through regulating Wnt/beta-catenin signaling via Nemo-like kinaseNeuro Oncol2013 15578588
Not in our library10.1093/neuonc/not004
223.
Jia Z Wang K Wang G Zhang A Pu P MiR-30a-5p antisense oligonucleotide suppresses glioma cell growth by targeting SEPT7PLoS One2013 8e55008
Not in our library10.1371/journal.pone.0055008
224.
Guessous F Alvarado-Velez M Marcinkiewicz L Zhang Y Kim J Heister S Kefas B Godlewski J Schiff D Purow B Abounader R Oncogenic effects of miR-10b in glioblastoma stem cellsJ Neurooncol2013 112153163
Not in our library10.1007/s11060-013-1047-0
225.
Li G Zhang Z Tu Y Jin T Liang H Cui G He S Gao G Correlation of microRNA-372 upregulation with poor prognosis in human gliomaDiagn Pathol2013 81
Not in our library10.1186/1746-1596-8-1
226.
Tanaka H Sasayama T Tanaka K Nakamizo S Nishihara M Mizukawa K Kohta M Koyama J Miyake S Taniguchi M Hosoda K Kohmura E MicroRNA-183 upregulates HIF-1alpha by targeting isocitrate dehydrogenase 2 (IDH2) in glioma cellsJ Neurooncol2013 111273283
Not in our library10.1007/s11060-012-1027-9
227.
Song L Lin C Gong H Wang C Liu L Wu J Tao S Hu B Cheng SY Li M Li J miR-486 sustains NF-kappaB activity by disrupting multiple NF-kappaB-negative feedback loopsCell Res2013 23274289
Not in our library10.1038/cr.2012.174
228.
Lu S Wang S Geng S Ma S Liang Z Jiao B Increased expression of microRNA-17 predicts poor prognosis in human gliomaJ Biomed Biotechnol2012 2012970761
Not in our library10.1155/2012/970761
229.
Jia Z Wang K Zhang A Wang G Kang C Han L Pu P miR-19a and miR-19b overexpression in gliomasPathol Oncol Res2013 19847853
Not in our library10.1007/s12253-013-9653-x
230.
Chan JA Krichevsky AM Kosik KS MicroRNA-21 is an antiapoptotic factor in human glioblastoma cellsCancer Res2005 6560296033
Not in our library10.1158/0008-5472.can-05-0137
231.
Gabriely G Yi M Narayan RS Niers JM Wurdinger T Imitola J Ligon KL Kesari S Esau C Stephens RM Tannous BA Krichevsky AM Human glioma growth is controlled by microRNA-10bCancer Res2011 7135633572
Not in our library10.1158/0008-5472.can-10-3568
232.
Wu L Li G Feng D Qin H Gong L Zhang J Zhang Z MicroRNA-21 expression is associated with overall survival in patients with gliomaDiagn Pathol2013 8200
Not in our library10.1186/1746-1596-8-200
233.
Slaby O Lakomy R Fadrus P Hrstka R Kren L Lzicarova E Smrcka M Svoboda M Dolezalova H Novakova J Valik D Vyzula R Michalek J MicroRNA-181 family predicts response to concomitant chemoradiotherapy with temozolomide in glioblastoma patientsNeoplasma2010 57264269
Not in our library10.4149/neo_2010_03_264
234.
Zhou X Ren Y Moore L Mei M You Y Xu P Wang B Wang G Jia Z Pu P Zhang W Kang C Downregulation of miR-21 inhibits EGFR pathway and suppresses the growth of human glioblastoma cells independent of PTEN statusLab Invest2010 90144155
Not in our library10.1038/labinvest.2009.126
235.
MicroRNA 128a Increases Intracellular ROS Level by Targeting Bmi-1 and Inhibits Medulloblastoma Cancer Cell Growth by Promoting Senescence · 2010
No notice
236.
Cui JG Zhao Y Sethi P Li YY Mahta A Culicchia F Lukiw WJ Micro-RNA-128 (miRNA-128) down-regulation in glioblastoma targets ARP5 (ANGPTL6), Bmi-1 and E2F-3a, key regulators of brain cell proliferationJ Neurooncol2010 98297304
Not in our library10.1007/s11060-009-0077-0
237.
Fasano CA Dimos JT Ivanova NB Lowry N Lemischka IR Temple S shRNA knockdown of Bmi-1 reveals a critical role for p21-Rb pathway in NSC self-renewal during developmentCell Stem Cell2007 18799
Not in our library10.1016/j.stem.2007.04.001
238.
Roth P Wischhusen J Happold C Chandran PA Hofer S Eisele G Weller M Keller A A specific miRNA signature in the peripheral blood of glioblastoma patientsJ Neurochem2011 118449457
Not in our library10.1111/j.1471-4159.2011.07307.x
239.
Abu-Elneel K Liu T Gazzaniga FS Nishimura Y Wall DP Geschwind DH Lao K Kosik KS Heterogeneous dysregulation of microRNAs across the autism spectrumNeurogenetics2008 9153161
Not in our library10.1007/s10048-008-0133-5
240.
A miRNA Signature of Prion Induced Neurodegeneration · 2008
No notice
241.
Lee ST Chu K Im WS Yoon HJ Im JY Park JE Park KH Jung KH Lee SK Kim M Roh JK Altered microRNA regulation in Huntington’s disease modelsExp Neurol2011 227172179
Not in our library10.1016/j.expneurol.2010.10.012
242.
Lukiw WJ Micro-RNA speciation in fetal, adult and Alzheimer’s disease hippocampusNeuroreport2007 18297300
Not in our library10.1097/wnr.0b013e3280148e8b
243.
Jiang Q Wang Y Hao Y Juan L Teng M Zhang X Li M Wang G Liu Y miR2Disease: a manually curated database for microRNA deregulation in human diseaseNucleic Acids Res2009 37D98104
Not in our library10.1093/nar/gkn714
244.
Mi S Lu J Sun M Li Z Zhang H Neilly MB Wang Y Qian Z Jin J Zhang Y Bohlander SK Le Beau MM Larson RA Golub TR Rowley JD Chen J MicroRNA expression signatures accurately discriminate acute lymphoblastic leukemia from acute myeloid leukemiaProc Natl Acad Sci U S A2007 1041997119976
Not in our library10.1073/pnas.0709313104
245.
Schultz J Lorenz P Gross G Ibrahim S Kunz M MicroRNA let-7b targets important cell cycle molecules in malignant melanoma cells and interferes with anchorage-independent growthCell Res2008 18549557
Not in our library10.1038/cr.2008.45
246.
Kozaki K Imoto I Mogi S Omura K Inazawa J Exploration of tumor-suppressive microRNAs silenced by DNA hypermethylation in oral cancerCancer Res2008 6820942105
Not in our library10.1158/0008-5472.can-07-5194
247.
Bottoni A Zatelli MC Ferracin M Tagliati F Piccin D Vignali C Calin GA Negrini M Croce CM Degli Uberti EC Identification of differentially expressed microRNAs by microarray: a possible role for microRNA genes in pituitary adenomasJ Cell Physiol2007 210370377
Not in our library10.1002/jcp.20832
248.
Foekens JA Sieuwerts AM Smid M Look MP de Weerd V Boersma AW Klijn JG Wiemer EA Martens JW Four miRNAs associated with aggressiveness of lymph node-negative, estrogen receptor-positive human breast cancerProc Natl Acad Sci U S A2008 1051302113026
Not in our library10.1073/pnas.0803304105
249.
Weiss GJ Bemis LT Nakajima E Sugita M Birks DK Robinson WA Varella-Garcia M Bunn PA Jr Haney J Helfrich BA Kato H Hirsch FR Franklin WA EGFR regulation by microRNA in lung cancer: correlation with clinical response and survival to gefitinib and EGFR expression in cell linesAnn Oncol2008 1910531059
Not in our library10.1093/annonc/mdn006
250.
Iorio MV Ferracin M Liu CG Veronese A Spizzo R Sabbioni S Magri E Pedriali M Fabbri M Campiglio M Ménard S Palazzo JP Rosenberg A Musiani P Volinia S Nenci I Calin GA Querzoli P Negrini M Croce CM MicroRNA gene expression deregulation in human breast cancerCancer Res2005 6570657070
Not in our library10.1158/0008-5472.can-05-1783
251.
Bloomston M Frankel WL Petrocca F Volinia S Alder H Hagan JP Liu CG Bhatt D Taccioli C Croce CM MicroRNA expression patterns to differentiate pancreatic adenocarcinoma from normal pancreas and chronic pancreatitisJAMA2007 29719011908
Not in our library10.1001/jama.297.17.1901
252.
Volinia S Calin GA Liu CG Ambs S Cimmino A Petrocca F Visone R Iorio M Roldo C Ferracin M Prueitt RL Yanaihara N Lanza G Scarpa A Vecchione A Negrini M Harris CC Croce CM A microRNA expression signature of human solid tumors defines cancer gene targetsProc Natl Acad Sci U S A2006 10322572261
Not in our library10.1073/pnas.0510565103
253.
Huang XH Wang Q Chen JS Fu XH Chen XL Chen LZ Li W Bi J Zhang LJ Fu Q Zeng WT Cao LQ Tan HX Su Q Bead-based microarray analysis of microRNA expression in hepatocellular carcinoma: miR-338 is downregulatedHepatol Res2009 39786794
Not in our library10.1111/j.1872-034x.2009.00502.x
254.
Kotani A Ha D Hsieh J Rao PK Schotte D den Boer ML Armstrong SA Lodish HF miR-128b is a potent glucocorticoid sensitizer in MLL-AF4 acute lymphocytic leukemia cells and exerts cooperative effects with miR-221Blood2009 11441694178
Not in our library10.1182/blood-2008-12-191619
255.
Esquela-Kerscher A Slack FJ Oncomirs - microRNAs with a role in cancerNat Rev Cancer2006 6259269
Not in our library10.1038/nrc1840
256.
Sevignani C Calin GA Siracusa LD Croce CM Mammalian microRNAs: a small world for fine-tuning gene expressionMamm Genome2006 17189202
Not in our library10.1007/s00335-005-0066-3
257.
Calin GA Croce CM MicroRNA-cancer connection: the beginning of a new taleCancer Res2006 6673907394
Not in our library10.1158/0008-5472.can-06-0800
258.
Khan AP Poisson LM Bhat VB Fermin D Zhao R Kalyana-Sundaram S Michailidis G Nesvizhskii AI Omenn GS Chinnaiyan AM Sreekumar A Quantitative proteomic profiling of prostate cancer reveals a role for miR-128 in prostate cancerMol Cell Proteomics2010 9298312
Not in our library10.1074/mcp.m900159-mcp200
259.
Zhu Y Yu F Jiao Y Feng J Tang W Yao H Gong C Chen J Su F Zhang Y Song E Reduced miR-128 in breast tumor-initiating cells induces chemotherapeutic resistance via Bmi-1 and ABCC5Clin Cancer Res2011 1771057115
Not in our library10.1158/1078-0432.ccr-11-0071
260.
Myatt SS Wang J Monteiro LJ Christian M Ho KK Fusi L Dina RE Brosens JJ Ghaem-Maghami S Lam EW Definition of microRNAs that repress expression of the tumor suppressor gene FOXO1 in endometrial cancerCancer Res2010 70367377
Not in our library10.1158/0008-5472.can-09-1891
261.
Strasser A Harris AW Bath ML Cory S Novel primitive lymphoid tumours induced in transgenic mice by cooperation between myc and bcl-2Nature1990 348331333
Not in our library10.1038/348331a0
262.
Green DR Reed JC Mitochondria and apoptosisScience1998 28113091312
Not in our library10.1126/science.281.5381.1309
263.
Wu N Wu GC Hu R Li M Feng H Ginsenoside Rh2 inhibits glioma cell proliferation by targeting microRNA-128Acta Pharmacol Sin2011 32345353
Not in our library10.1038/aps.2010.220
264.
Adlakha YK Saini N miR-128 exerts pro-apoptotic effect in a p53 transcription-dependent and -independent manner via PUMA-Bak axisCell Death Dis2013 4e542
Not in our library10.1038/cddis.2013.46
265.
Ji S Shao G Lv X Liu Y Fan Y Wu A Hu H Downregulation of miRNA-128 sensitises breast cancer cell to chemodrugs by targeting BaxCell Biol Int2013 37653658
Not in our library10.1002/cbin.10100
266.
Donzelli S Fontemaggi G Fazi F Di Agostino S Padula F Biagioni F Muti P Strano S Blandino G MicroRNA-128-2 targets the transcriptional repressor E2F5 enhancing mutant p53 gain of functionCell Death Differ2012 1910381048
Not in our library10.1038/cdd.2011.190
267.
Des Portes V Pinard JM Billuart P Vinet MC Koulakoff A Carrie A Gelot A Dupuis E Motte J Berwald-Netter Y Catala M Kahn A Beldjord C Chelly J A novel CNS gene required for neuronal migration and involved in X-linked subcortical laminar heterotopia and lissencephaly syndromeCell1998 925161
Not in our library10.1016/s0092-8674(00)80898-3
268.
Tissir F Goffinet AM Reelin and brain developmentNat Rev Neurosci2003 4496505
Not in our library10.1038/nrn1113
269.
Messi E Florian MC Caccia C Zanisi M Maggi R Retinoic acid reduces human neuroblastoma cell migration and invasiveness: effects on DCX, LIS1, neurofilaments-68 and vimentin expressionBMC Cancer2008 830
Not in our library10.1186/1471-2407-8-30
270.
Perrone G Vincenzi B Zagami M Santini D Panteri R Flammia G Verzi A Lepanto D Morini S Russo A Bazan V Tomasino RM Morello V Tonini G Rabitti C Reelin expression in human prostate cancer: a marker of tumor aggressiveness based on correlation with gradeMod Pathol2007 20344351
Not in our library10.1038/modpathol.3800743
271.
Human embryonic and neuronal stem cell markers in retinoblastoma. · 2007
No notice
272.
Wang Q Lu J Yang C Wang X Cheng L Hu G Sun Y Zhang X Wu M Liu Z CASK and its target gene Reelin were co-upregulated in human esophageal carcinomaCancer Lett2002 1797177
Not in our library10.1016/s0304-3835(01)00846-1
273.
MiR-128 Inhibits Tumor Growth and Angiogenesis by Targeting p70S6K1 · 2012
No notice
274.
Molofsky AV He S Bydon M Morrison SJ Pardal R Bmi-1 promotes neural stem cell self-renewal and neural development but not mouse growth and survival by repressing the p16Ink4a and p19Arf senescence pathwaysGenes Dev2005 1914321437
Not in our library10.1101/gad.1299505
275.
Horton JD Goldstein JL Brown MS SREBPs: activators of the complete program of cholesterol and fatty acid synthesis in the liverJ Clin Invest2002 10911251131
Not in our library10.1172/jci0215593
276.
Beaven SW Tontonoz P Nuclear receptors in lipid metabolism: targeting the heart of dyslipidemiaAnnu Rev Med2006 57313329
Not in our library10.1146/annurev.med.57.121304.131428
277.
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Not in our library10.1038/cddis.2013.301
278.
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Not in our library10.1016/j.molcel.2007.06.017
279.
Thomas PD Campbell MJ Kejariwal A Mi H Karlak B Daverman R Diemer K Muruganujan A Narechania A PANTHER: a library of protein families and subfamilies indexed by functionGenome Res2003 1321292141
Not in our library10.1101/gr.772403
280.
Nogales-Cadenas R Carmona-Saez P Vazquez M Vicente C Yang X Tirado F Carazo JM Pascual-Montano A GeneCodis: interpreting gene lists through enrichment analysis and integration of diverse biological informationNucleic Acids Res2009 37W317322
Not in our library10.1093/nar/gkp416
281.
Motohashi N Alexander MS Shimizu-Motohashi Y Myers JA Kawahara G Kunkel LM Regulation of IRS1/Akt insulin signaling by microRNA-128a during myogenesisJ Cell Sci2013 12626782691
Not in our library10.1242/jcs.119966
282.
Masri S Liu Z Phung S Wang E Yuan YC Chen S The role of microRNA-128a in regulating TGFbeta signaling in letrozole-resistant breast cancer cellsBreast Cancer Res Treat2010 1248999
Not in our library10.1007/s10549-009-0716-3
283.
Monteys AM Spengler RM Wan J Tecedor L Lennox KA Xing Y Davidson BL Structure and activity of putative intronic miRNA promotersRNA2010 16495505
Not in our library10.1261/rna.1731910

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Elevation of brain-enriched miRNAs in cerebrospinal fluid of patients with acute ischemic stroke · 2017
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Resveratrol as a Natural Autophagy Regulator for Prevention and Treatment of Alzheimer’s Disease · 2017
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