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The functional role of long non-coding RNA in human carcinomas

Ewan A Gibb, Carolyn J Brown, Wan L Lam

Molecular Cancer · 2011 · Review

Abstract

Long non-coding RNAs (lncRNAs) are emerging as new players in the cancer paradigm demonstrating potential roles in both oncogenic and tumor suppressive pathways. These novel genes are frequently aberrantly expressed in a variety of human cancers, however the biological functions of the vast majority remain unknown. Recently, evidence has begun to accumulate describing the molecular mechanisms by which these RNA species function, providing insight into the functional roles they may play in tumorigenesis. In this review, we highlight the emerging functional role of lncRNAs in human cancer.

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From PubMed Central, U.S. National Library of Medicine, as current on Oct 17, 2026. Paragraph numbers are ours, so an answer can point at one.

Introduction

1One of modern biology's great surprises was the discovery that the human genome encodes only ~20,000 protein-coding genes, representing <2% of the total genome sequence. However, with the advent of tiling resolution genomic microarrays and whole genome and transcriptome sequencing technologies it was determined that at least 90% of the genome is actively transcribed. The human transcriptome was found to be more complex than a collection of protein-coding genes and their splice variants; showing extensive antisense, overlapping and non-coding RNA (ncRNA) expression. Although initially argued to be spurious transcriptional noise, recent evidence suggests that the proverbial "dark matter" of the genome may play a major biological role in cellular development and metabolism. One such player, the newly discovered long non-coding RNA (lncRNA) genes, demonstrate developmental and tissue specific expression patterns, and aberrant regulation in a variety of diseases, including cancer.

2NcRNAs are loosely grouped into two major classes based on transcript size; small ncRNAs and lncRNAs (Table 1). Small ncRNAs are represented by a broad range of known and newly discovered RNA species, with many being associated with 5' or 3' regions of genes. This class includes the well-documented miRNAs, RNAs ~22 nucleotides (nt) long involved in the specific regulation of both protein-coding, and putatively non-coding genes, by post-transcriptional silencing or infrequently by activation. miRNAs serve as major regulators of gene expression and as intricate components of the cellular gene expression network. Another newly described subclass are the transcription initiation RNAs (tiRNAs), which are the smallest functional RNAs at only 18 nt in length. While a number of small ncRNAs classes, including miRNAs, have established roles in tumorigenesis, an intriguing association between the aberrant expression of ncRNA satellite repeats and cancer has been recently demonstrated.

3In contrast to miRNAs, lncRNAs, the focus of this article, are mRNA-like transcripts ranging in length from 200 nt to ~100 kilobases (kb) lacking significant open reading frames. Many identified lncRNAs are transcribed by RNA polymerase II (RNA pol II) and are polyadenylated, but this is not a fast rule. There are examples of lncRNAs, such as the antisense asOct4-pg5 or the brain-associated BC200, which are functional, but not polyadenylated. Generally, lncRNA expression levels appear to be lower than protein-coding genes, and some lncRNAs are preferentially expressed in specific tissues. However, recent findings have suggested novel lncRNAs may contribute a significant portion of the aforementioned 'dark matter' of the human transcriptome. In an exciting report by Kapranov et.al., it was revealed the bulk of the relative mass of RNA in a human cell, exclusive of the ribosomal and mitochondrial RNA, is represented by non-coding transcripts with no known function.

4Like miRNAs and protein-coding genes, some transcriptionally active lncRNA genes display histone H3K4 trimethylation at their 5'-end and histone H3K36 trimethylation in the body of the gene. The small number of characterized human lncRNAs have been associated with a spectrum of biological processes, for example, epigenetics, alternative splicing, nuclear import, as structural components, as precursors to small RNAs and even as regulators of mRNA decay. Furthermore, accumulating reports of misregulated lncRNA expression across numerous cancer types suggest that aberrant lncRNA expression may be a major contributor to tumorigenesis. This surge in publications reflects the increasing attention to this subject (Figure 1) and a number of useful lncRNA databases have been created (Table 2). In this review we highlight the emerging functional role of aberrant lncRNA expression, including transcribed ultraconserved regions (T-UCRs), within human carcinomas.

Nomenclature and Classification of LncRNA

5The definition 'non-coding RNA' is typically used to describe transcripts where sequence analysis has failed to identify an open reading frame. However, one should exercise caution when exploring putative non-coding transcripts, as there are cases where 'non-coding' transcripts were found to encode short, functional peptides. Currently, a universal classification scheme to define lncRNAs does not exist and therefore there are numerous synonyms describing the same type of transcripts. Terms such as large non-coding RNA, mRNA-like long RNA, and intergenic RNA all define cellular RNAs, exclusive of rRNAs, greater than 200 nt in length and having no obvious protein-coding capacity. Consequently, this has led to confusion in the literature as to exactly which transcripts should constitute a lncRNA. For example, one subclass of lncRNAs is called large or long intergenic ncRNAs (lincRNAs). These lncRNAs are exclusively intergenic and are marked by a chromatin signature indicative of transcription. To further compound classification confusion, RNA species that are bifunctional preclude categorization into either group of protein-coding or ncRNAs as their transcripts function both at the RNA and protein levels. In these rare cases, they are classified on a case-by-case basis, reserving the term 'lncRNA' to describe transcripts with no protein-coding capacity. In the meantime, and for the purposes of this review, we will consider lncRNAs as a blanket term to encompass mRNA-like ncRNAs, lincRNAs, as well as antisense and intron-encoded transcripts, T-UCRs and transcribed pseudogenes.

Discovery of LncRNAs

6The earliest reports describing lncRNA predated the discovery of miRNAs, although the term 'lncRNA' had not been coined at the time (Figure 2). One of the first lncRNA genes reported was the imprinted H19 gene, which was quickly followed by the discovery of the silencing X-inactive-specific transcript (XIST) lncRNA gene, which plays a critical function in X-chromosome inactivation. However, the discovery of the first miRNA lin-14 dramatically redirected the focus of ncRNA research from long ncRNAs to miRNAs. Moreover, during this time the discovery of miRNAs revealed RNA could regulate gene expression and later that entire gene networks could be affected by ncRNA expression and within the last decade miRNAs were discovered to be associated with cancer (Figure 2). At the time of this writing there are approximately 1049 human miRNAs described in miRBase V16 with the potential of affecting the expression of approximately 60% of protein -coding genes. Conversely, the variety and dynamics of lncRNA expression was not to be fully appreciated until the introduction of whole transcriptome sequencing. With the advent of the FANTOM and ENCODE transcript mapping projects, it was revealed that the mammalian genome is extensively transcribed, although a large portion of this represented non-coding sequences. Coupled with the novel functional annotation of a few lncRNAs, this discovery promoted research focusing on lncRNA discovery and characterization. Recent reports have described new lncRNA classes such as lincRNAs and T-UCRs. Current estimates of the lncRNA gene content in the human genome ranges from ~7000 - 23,000 unique lncRNAs, implying this class of ncRNA will represent an enormous, yet undiscovered, component of normal cellular networks that may be disrupted in cancer biology.

Emerging Role of Long Non-Coding RNA in Tumorigenesis

7A role for differential lncRNA expression in cancer had been suspected for many years, however, lacked strong supporting evidence. With advancements in cancer transcriptome profiling and accumulating evidence supporting lncRNA function, a number of differentially expressed lncRNAs have been associated with cancer (Table 3). LncRNAs have been implicated to regulate a range of biological functions and the disruption of some of these functions, such as genomic imprinting and transcriptional regulation, plays a critical role in cancer development. Here we describe some of the better characterized lncRNAs that have been associated with cancer biology.

Imprinted lncRNA genes

8Imprinting is a process whereby the copy of a gene inherited from one parent is epigenetically silenced. Intriguingly, imprinted regions often include multiple maternal and paternally expressed genes with a high frequency of ncRNA genes. The imprinted ncRNA genes are implicated in the imprinting of the region by a variety of mechanisms including enhancer competition and chromatin remodeling. A key feature of cancer is the loss of this imprinting resulting in altered gene expression. Two of the best known imprinted genes are in fact lncRNAs.

H19

9The H19 gene encodes a 2.3 kb lncRNA that is expressed exclusively from the maternal allele. H19 and its reciprocally imprinted protein-coding neighbor the Insulin-Like Growth Factor 2 or IGF2 gene at 11p15.5 were among the first genes, non-coding or otherwise, found to demonstrate genomic imprinting. The expression of H19 is high during vertebrate embryo development, but is downregulated in most tissues shortly after birth with the exception of skeletal tissue and cartilage. Loss of imprinting and subsequent strong gene expression has been well-documented in human cancers. Likewise, loss of imprinting at the H19 locus resulted in high H19 expression in cancers of the esophagus, colon, liver, bladder and with hepatic metastases.

10H19 has been implicated as having both oncogenic and tumor suppression properties in cancer. H19 is upregulated in a number of human cancers, including hepatocellular, bladder and breast carcinomas, suggesting an oncogenic function for this lncRNA. In colon cancer H19 was shown to be directly activated by the oncogenic transcription factor c-Myc, suggesting H19 may be an intermediate functionary between c-Myc and downstream gene expression. Conversely, the tumor suppressor gene and transcriptional activator p53 has been shown to down-regulate H19 expression. H19 transcripts also serve as a precursor for miR-675, a miRNA involved in the regulation of developmental genes. miR-675 is processed from the first exon of H19 and functionally downregulates the tumor suppressor gene retinoblastoma (RB1) in human colorectal cancer, further implying an oncogenic role for H19.

11There is evidence suggesting H19 may also play a role in tumor suppression. Using a mouse model for colorectal cancer, it was shown that mice lacking H19 manifested an increased polyp count compared to wild-type. Secondly, a mouse teratocarcinoma model demonstrated larger tumor growth when the embryo lacked H19, and finally in a hepatocarcinoma model, mice developed cancer much earlier when H19 was absent. The discrepancy as to whether H19 has oncogenic or tumor suppressive potential may be due in part to the bifunctional nature of the lncRNA or may be context dependent. In either case, the precise functional and biological role of H19 remains to be determined.

XIST - X-inactive-specific transcript

12The 17 kb lncRNA XIST is arguably an archetype for the study of functional lncRNAs in mammalian cells, having been studied for nearly two decades. In female cells, the XIST transcript plays a critical role in X-chromosome inactivation by physically coating one of the two X-chromosomes, and is necessary for the cis-inactivation of the over one thousand X-linked genes. Like the lncRNAs HOTAIR and ANRIL, XIST associates with polycomb-repressor proteins, suggesting a common pathway of inducing silencing utilized by diverse lncRNAs. In mice, X inactivation in the extraembryonic tissues is non-random, and the initial expression of Xist is always paternal in origin, followed later by random X inactivation in the epiblast associated with random mono-allelic expression. Intriguingly, regulation of Xist in mouse has been shown to be controlled by interactions amongst additional ncRNAs, including an antisense transcript, Tsix, enhancer-associated ncRNAs (Xite) and the upstream Jpx and Ftx lncRNAs. Intriguingly, murine Xist and Tsix duplexes are processed into small RNAs by an apparently Dicer-dependent manner, suggesting a significant overlap between the regulatory networks of both lncRNAs and sRNAs. It is unclear, however, how much of this regulation is conserved in humans, who do not show imprinted X inactivation. While XIST expression levels are correlated with outcome in some cancers, such as the therapeutic response in ovarian cancer, the actual role that XIST may play in human carcinomas, if any, is not entirely clear.

13There is generally believed to be only a limited developmental window in which X inactivation can occur, and loss of XIST from an inactive X chromosome does not result in reactivation of the X chromosome. Thus, tumors with additional X chromosomes generally keep the inactivation status of the duplicated X. For tumors in which two active X chromosomes are observed, as has been frequently observed in breast cancer, the most common mechanism involves loss of the inactive X and duplication of the active X, often resulting in heterogeneous XIST expression in these tumors. Loss of the inactive X and abnormalities of XIST expression may be indicative of more general heterochromatin defects. Analogously, failure to properly reset XIST and X inactivation may serve as a marker of proper resetting of epigenetic marks in stem cells or induced pluripotent stem cells. Correlations between XIST expression and cancer state can also occur spuriously. Notably, in cytogenetically normal cells, XIST is found only in females as males do not have an inactive X. Therefore in cancers correlations can be observed with XIST expression due to differential presence of male or female samples, and many cancers do show different onsets and progressions in males and females. Furthermore, XIST expression will increase with the number of inactive X chromosomes. While it might be anticipated that there would be little advantage to a tumor acquiring inactive chromosomes, it has been shown that approximately 15% of human X-linked genes continue to be expressed from the inactive X chromosome.

HOTAIR - HOX antisense intergenic RNA

14Several lncRNAs have been implicated in metastasis. One of the first lncRNAs described to have a fundamental role in cancer was the metastasis-associated HOX Antisense Intergenic RNA (HOTAIR), a 2.2 kb gene located in the mammalian HOXC locus on chromosome 12q13.13. This lncRNA was found to be highly upregulated in both primary and metastatic breast tumors, demonstrating up to 2000-fold increased transcription over normal breast tissue. High levels of HOTAIR expression were found to be correlated with both metastasis and poor survival rate, linking a ncRNA with cancer invasiveness and patient prognosis. Furthermore, it was demonstrated that if cells expressing HOTAIR were grafted into mouse mammary fat pads, a modest increase in the rate of primary tumor growth was observed. Interestingly, there are reports indicating that numerous lncRNAs are transcribed from the HOX locus, suggesting that HOTAIR may be only one example of a global regulatory phenomena.

15The spliced and polyadenylated HOTAIR RNA does not encode any proteins but has been demonstrated to be intimately associated with the mammalian polycomb repressive complex 2 (PRC2) which is comprised of the H3K27 methylase EZH2, SUZ12 and EED (Figure 3). Polycomb group proteins mediate repression of transcription of thousands of genes controlling differentiation pathways during development, and have roles in stem cell pluripotency and human cancer.

16HOTAIR binding results in a genome-wide re-targeting of the PRC2 complex. The HOXD locus on chromosome 2 is a PRC2 target (Figure 3). The consequence of PRC2/HOTAIR localization is the transcriptional silencing of a 40 kb region of the HOXD locus which remodels the gene expression pattern of breast epithelial cells to more closely resemble that of embryonic fibroblasts. The HOTAIR RNA appears to act as a molecular scaffold, binding at least two distinct histone modification complexes. The 5' region of the RNA binds the PRC2 complex responsible for H3K27 methylation, while the 3' region of HOTAIR binds LSD1, a histone lysine demethylase that mediates enzymatic demethylation of H3K4Me2. Although, the precise mechanism of HOTAIR activities remains to be elucidated, it is clear that HOTAIR reprograms chromatin state to promote cancer metastasis.

MALAT1 - Metastasis-associated lung adenocarcinoma transcript 1

17The MALAT1 gene, or metastasis-associated lung adenocarcinoma transcript 1, was first associated with high metastatic potential and poor patient prognosis during a comparative screen of non-small cell lung cancer patients with and without metastatic tumors. This lncRNA is widely expressed in normal human tissues and is found to be upregulated in a variety of human cancers of the breast, prostate, colon, liver and uterus. Notably, the MALAT1 locus at 11q13.1 has been identified to harbor chromosomal translocation breakpoints associated with cancer.

18Intriguingly, cellular MALAT1 transcripts are subject to post-transcriptional processing to yield a short, tRNA-like molecule mascRNA and a long MALAT1 transcript with a poly(A) tail-like moiety (Figure 4). Using the mouse homologue to the human MALAT1 gene, it was revealed that ribonuclease (RNase) P processing generates the 3' end of the long MALAT1 transcript and the 5' end of the mascRNA. The shorter mascRNA adopts a tRNA clover-leaf structure and is subject to RNaseZ processing and the addition of a CCA to its 3' end before being exported to the cytoplasm. The generation of putatively functional sRNAs by post-transcriptional processing of lncRNAs, such mascRNA from MALAT1, may be reflective of a central, unexplored theme in ncRNA biology. Recent evidence suggests regulated post-transcriptional processing events, such as splicing and post-cleavage capping, may increase the functional diversity of the metazoan transcriptome. In contrast, the long MALAT1 transcript is not polyadenylated, but has a poly(A) tail-like sequence that is genome encoded and is putatively present to protect the MALAT1 transcript from degradation. Moreover, MALAT1 localizes to nuclear speckles in a transcription dependent manner.

19Following the correlation between high levels of MALAT1 expression and metastasis, a number of studies have implicated MALAT1 in the regulation of cell mobility. For example, RNA interference (RNAi)-mediated silencing of MALAT1 impaired the in vitro migration of lung adenocarcinoma cells through concomitant regulation of motility regulated genes via transcriptional and/or post-transcriptional means. Similarly, short hairpin RNA inhibition of MALAT1 reduced cell proliferation and invasive potential of a cervical cancer cell line. Collectively, these studies suggest that MALAT1 regulates the invasive potential of metastatic tumor cells. Other examples of cancer-associated lncRNAs subject to post-transcriptional processing include the miR-155 host gene BIC and the miR-17-92 cluster in B-cell lymphoma and neuroblastoma, respectively.

20Recent efforts have focused on elucidating the molecular role of nuclear speckle localized MALAT1 transcripts, while the function for the mascRNA has yet to be determined. Nuclear speckles are thought to be involved in the assembly, modification and/or storage of pre-mRNA processing machinery. A recent publication revealed MALAT1 RNA strongly associates with serine-arginine rich splicing factor (SR) proteins which are involved in both constitutive and alternative splicing and the levels of MALAT1 regulated the cellular levels of phosphorylated SR proteins. These findings imply that the lncRNA MALAT1 may serve a function in the regulation of alternate splicing by modulating the activity of SR proteins, although precisely how this may contribute to tumorigenesis remains unknown.

MEG3 - Maternally expressed gene 3

21The maternally expressed gene 3 (MEG3) was the first lncRNA proposed to function as a tumor suppressor. The MEG3 gene is expressed in many normal human tissues, with the highest expression in the brain and pituitary gland. MEG3 expression was not detectable in various brain cancers, nor in a range of human cancer cell lines implicating a potential role of this lncRNA in suppression of cell growth. Moreover, ectopic expression of MEG3 RNA was found to suppress the growth of several human cancer cell lines, further supporting the role of MEG3 as a tumor suppressor. In clinically nonfunctioning pituitary tumors, it was demonstrated that hypermethylation of the MEG3 regulatory region was associated with the loss of MEG3 expression, providing evidence for a mechanism of MEG3 inactivation.

22MEG3 is a paternally imprinted, single copy gene comprised of 10 exons. To date, 12 MEG3 isoforms have been detected (MEG3; a-3k) due to alternative splicing. Each isoform contains the common exons 1-3 and 8-10, but varies in the combination of exons 4-7 in the middle of the transcript. Notably, the last intron of MEG3 encodes the evolutionarily conserved miR-770, a miRNA with a number of putative mRNA targets. This arrangement mirrors the presence of miR-675 in H19, except in that instance the miRNA was exon encoded. The originally identified isoform of MEG3 is expressed as a 1.6 kb polyadenylated transcript that is localized to the nucleus where it is associated with chromatin although some cytoplasmic MEG3 transcripts have been detected. All 12 MEG3 isoforms demonstrate three distinct secondary folding motifs designated M1, M2 and M3.

23Functionally, MEG3 has been implicated as a top-level regulatory RNA due to its ability to stimulate both p53-dependent and p53-independent pathways. Critically, the MEG3-mediated functional activation of p53 is dependent on the secondary structure of the MEG3 RNA rather than on primary sequence conservation. In an elegant series of experiments, Zhang et al. demonstrated that replacing particular regions of the MEG3 with unrelated sequence had no effect on the activation of p53 provided the original secondary structure was preserved. This observation strengthens the argument that the rapid evolution and relative lack of sequence conservation does not limit the potential functionality of these unique RNA species. Conversely, the novel lincRNA-p21 has been described as a downstream repressor in the p53 transcriptional response, suggesting the complex p53 transcriptional network includes numerous regulatory lncRNAs.

Depletion of miRNAs by a lncRNA 'molecular decoy' or 'miRNA sponge'

24Expression of miRNAs in cancer can be deregulated by a range of mechanisms, including copy number alterations and epigenetic silencing. Two recent examples have demonstrated that lncRNAs can act as natural 'miRNA sponges' to reduce miRNA levels.

HULC - Highly Upregulated in Liver Cancer

25The most highly upregulated transcript found in a microarray-based study of gene expression in hepatocellular carcinoma was determined to be the ncRNA HULC, or Highly Upregulated in Liver Cancer. Transcribed from chromosome 6p24.3, this lncRNA demonstrates the hallmarks of a typical mRNA molecule, including a single spliced GT-AG intron, canonical polyadenylation signals upstream of the poly(A) tail and nuclear export demonstrating strong localization to the cytoplasm. Although HULC was found to co-purify with ribosomes, no translation product for this lncRNA has been detected, supporting its classification as a non-coding transcript. In addition to liver cancer, HULC was found to be highly upregulated in hepatic colorectal cancer metastasis and in hepatocellular carcinoma cell lines (HCC) producing hepatitis B virus (HBV).

26A recent paper began to elucidate the mechanism of upregulation of HULC in liver cancer cells, and to provide a potential mechanism of HULC function. HULC exists as part of an intricate auto-regulatory network, which when perturbed, resulted in increased HULC expression (Figure 5). The HULC RNA appeared to function as a 'molecular decoy' or 'miRNA sponge' sequestering miR-372, of which one function is the translational repression of PRKACB, a kinase targeting cAMP response element binding protein (CREB). Once activated, the CREB protein was able to promote HULC transcription by maintaining an open chromatin structure at the HULC promoter resulting in increased HULC transcription.

Pseudogene pairs: PTEN and PTENP1

27The discovery that HULC can act as a molecular decoy or 'miRNA sponge' mirrors a recent report describing an intricate relationship between the tumor suppressor phosphatase and tensin homolog (PTEN) and the matching lncRNA phosphatase and tensin homolog pseudogene 1 (PTENP1). The RNA transcripts of the PTEN/PTENP1 pair share similar 3' untranslated regions (3'UTRs) which both bind the same miRNAs. By binding miRNAs, PTENP1 transcripts reduce the effects of translational repression on PTEN therefore allowing expression of this tumor suppressor. In cancer, specific mutations inactivate these miRNA binding sites in PTENP1, therefore reducing the translation of PTEN and promoting tumor growth. This is especially pertinent as subtle changes in PTEN levels can influence cancer susceptibility.

ANRIL - Antisense Non-coding RNA in the INK4 Locus

28Located as part of the 42kb INK4b-ARF-INK4a locus on chromosome 9p21.3, the Antisense Non-coding RNA in the INK4 Locus (ANRIL) is transcribed by RNA pol II and processed into alternatively spliced isoforms, including an unspliced transcript of 34.8 kb termed p15AS. The INK4b-ARF-INKa locus has an important role in cell cycle control, cell senescence, stem cell renewal and apoptosis through P14ARF-MDM2-P53 and P16Ink4a/p15Ink4b-Cdk4/6-pRb pathways. A mouse model suggests that the well-characterized tumor suppressor genes encoded within this locus are regulated by Polycomb proteins.

29Aberrant expression and single nucleotide polymorphisms (SNPs) within ANRIL have been associated with susceptibility to a range of human diseases, including cancer. Moreover, the INK4b-ARF-INK4a locus is subject to frequent deletion or hypermethylation in cancers, including leukemia, melanoma, lung and bladder cancers. ANRIL has been associated with epigenetic silencing of the tumor suppressor gene p15, although the molecular events leading to this silencing were unclear.

30Evidence has suggested an intriguing mechanisms for ANRIL-mediated silencing of the INK4b-ARF-INK4a locus. Recently an interaction between chromatin modifying PRC complexes and ANRIL has been described, further elucidating the regulatory mechanism of this lncRNA. Like the lncRNA HOTAIR which binds both the polycomb repressor complex PRC2 and the LSD1 complex, ANRIL binds and recruits two polycomb repressor complexes modifying complexes, PRC1 and PRC2. This resulted in ANRIL/PRC mediated silencing of the genes in the INK4b-ARF-INK4a locus. While the distinct regions of the HOTAIR lncRNA required for interactions with each protein complex were determined, future studies will be necessary to elucidate the structural requirements of lncRNAs such as ANRIL with chromatin regulators such as PRC1/PRC2.

31The molecular details of ANRIL-mediated tumor suppression are becoming more clear. However, other mechanisms of lncRNA-mediated suppression of tumor suppressor genes have been reported. For example, a change in the expression ratio of bidirectional genes has been shown to mediate the expression of the tumor suppressor p21. Collectively, these observations suggest that lncRNA-mediated silencing of tumor suppressor genes may be a major mechanism driving tumorigenesis.

Cancer type specific lncRNA expression

32Many of the described lncRNAs are expressed in a variety of cancers, however a select few thus far have been associated with a single cancer type. HOTAIR, for example, has only been described in breast cancer, while three lncRNAs PCGEM1, DD3 and PCNCR1 have been associated solely with prostate cancer. The most recently described of these, Prostate Cancer Non-Coding RNA 1 (PCNCR1) lncRNA, was identified in a 'gene desert' on chromosome 8q24.2 and is associated with susceptibility to prostate cancer. PCNCR1 is expressed as an intronless, ~13 kb transcript with a potential role in trans-activation of androgen receptor (AR), a key player in prostate cancer progression. Likewise, PCGEM1 (Prostate Specific Gene 1) was found to have properties supporting tumorigenesis, as ectopic overexpression of PCGEM1 RNA resulted in increased cell growth and colony formation in cell lines. The lncRNA Differential Display Code 3 (DD3) is also highly over expressed in prostate cancer, yet little is known about the role DD3 may play in prostate cancer progression. Finally, the liver associated lncRNA HULC is highly expressed in primary liver tumors, and in colorectal carcinomas that metastasized to the liver, but not in the primary colon tumors or in non-liver metastases.

RNA polymerase III transcription of lncRNA

33The lncRNAs described thus far are products of RNA pol II transcription, yet many ncRNAs are transcribed by RNA polymerase III (RNA pol III). Importantly, RNA pol III is frequently deregulated in cancer cells resulting in increased activity. The molecular mechanisms driving increased RNA pol III activity in tumor cells include overexpression of RNA pol III transcription factors, escape from RNA pol III repressors and direct oncogene-mediated activation. Aberrant RNA pol III function may have consequences to the expression of lncRNAs transcribed by this polymerase.

34For example, the lncRNA BC200 is a small cytoplasmic lncRNA in the neurons of primate nervous systems and human cancers, but not in non-neuronal organs. Unlike the majority of lncRNAs described thus far, BC200 is transcribed by RNA pol III and shares unique homology with human Alu elements. Similarly, the lncRNA HULC also shares homology with mobile DNA, in this case with a long terminal repeat (LTR) retroelement. The BC200 RNA has been characterized as a negative regulator of eIF4A-dependent translation initiation.

35Due to the fact that many whole transcriptome sequencing methods were developed to enrich for poly(A) purified transcripts, RNA pol III transcripts may have been excluded from analysis. This suggests that other, yet unidentified RNA pol III lncRNAs over-expressed in cancer may be participating in tumorigenesis.

Aberrant T-UCR expression in human carcinoma

36Transcribed ultraconserved Regions (T-UCRs) are evolutionary conserved sequences found in both intergenic and intragenic regions of the human genome. These unique sequences are defined as 481 segments of DNA that are absolutely conserved between orthologous regions of the human, rat and mouse genomes. The transcription products of T-UCRs are 200-779 nt in length and were originally classed into three categories, non-exonic, exonic and possibly exonic, according to their overlap with known protein-coding genes. More recently, T-UCRs have been re-annotated into a more descriptive set of five categories: intergenic (38.7%), intronic (42.6%), exonic (4.2%), partly exonic (5%) or exonic containing (5.6%) (Figure 6).

37The high degree of conservation of T-UCRs, combined with their tissue-specific expression, suggests these ncRNAs may play a critical role in cellular metabolism and development. The expression of many T-UCRs is significantly altered in cancer, notably in adult chronic lymphocytic leukemias, colorectal and hepatocellular carcinomas and neuroblastomas. Their aberrant transcription profiles can be used to differentiate types of human cancers and have been linked to patient outcome. Some of the T-UCRs reside in genomic regions associated with specific types of cancer. For example, in colon cancer, the T-UCR uc.73A is one of the most highly upregulated T-UCRs, and this lncRNA has been found to show oncogenic properties by proliferation assays. Similarly, T-UCR uc.338 is significantly upregulated in human hepatocarcinoma tumor and cell lines, and uc.338 was found to be part of a larger transcriptional unit coined TUC338 which is involved in cell growth.

38The mechanism by which T-UCRs are differentially expressed is unclear. A study profiling T-UCRs in neuroblastomas did not find a consistent association between genomic alterations and T-UCR expression, suggesting aberrant T-UCR expression may be a consequence of epigenetic mechanisms. Like miRNAs and coding genes, T-UCR expression has been shown to be repressed by CpG island hypermethylation. Similarly, miRNAs have been shown to bind to, and downregulate T-UCRs, suggesting a complex regulatory mechanism may exist between ncRNAs in human cancers. Collectively, these reports have suggested that aberrant T-UCR expression may have a yet undetermined biological role in tumorigenesis.

Utility of LncRNAs in Cancer Diagnostics and Therapies

39Like their smaller non-coding miRNA counterparts, lncRNAs represent a significant untapped resource in terms of developing diagnostics and therapies. Differential or high level expression of certain cancer type-specific lncRNAs can be exploited for the development of novel biomarkers as lncRNA expression or may potentially correlate with patient response to chemotherapy. Understanding the mechanism(s) by which lncRNAs act will continue to provide novel approaches to regulating genes including the development of mimetics to compete with binding sites for miRNAs, chromatin remodelers, or DNA. It has been suggested that mediating transcriptional gene silencing (TGS) pathways, especially those of tumor suppressors or oncogenes, could be of high therapeutic benefit.

40It has been widely reported that cancer-specific miRNAs are detectable in the blood, sputum and urine of cancer patients. Likewise, lncRNAs have demonstrated utility as fluid-based markers of specific cancers. For example, the prostate specific lncRNA DD3 has been developed into highly specific, nucleic acid amplification-based marker of prostate cancer, which demonstrated higher specificity than serum prostate-specific antigen (PSA). Similarly, the highly expressed hepatocarcinoma-associated lncRNA HULC is detectable in the blood of hepatocarcinoma patients by conventional PCR methods.

41The use of lncRNAs as therapeutic agents is only beginning to be explored. Although our understanding of the molecular mechanisms of lncRNA function is limited, some features of lncRNAs make them ideal candidates for therapeutic intervention. Many lncRNAs appear to have protein-binding or functional potential that is dependent on secondary structure, this may provide a means of intervention. Preventing the interactions of HOTAIR with the PRC2 or LSD1 complexes, for example, may limit the metastatic potential of breast cancer cells.

42The tumor expression of certain lncRNAs provides a source of regulatory regions that can be used to reduce the risk of affecting normal tissues during transgene-mediated treatment. For example, H19 is strongly expressed in embryonic cells and in a wide-range of human cancers. As such, a plasmid-based system has been developed to exploit the tumor-specific expression of H19, primarily tested in treating bladder cancer. A plasmid construct, harboring a diptheria toxin gene driven by H19 specific regulatory sequences, is either administered via intratumoral injection as naked DNA, or complexed to the cationic polymer polyethylenimine (PEI) to form a polyplex vector. PEI-complexed plasmid is thought to increase the efficiency of DNA uptake via clathrin-dependent and -independent (cholesterol-dependent) pathways. Upon uptake, high levels of diptheria toxin are expressed in the tumor, resulting in a reduction in tumor size in human trials. Collectively, these advances indicate the potential in developing lncRNA mediated diagnostics and therapies.

Conclusions

43Differential expression of lncRNAs is becoming recognized as a hallmark feature in cancer, however the functional role for the vast majority of these unique genes is still in question. In this review, we highlight characterized lncRNAs described to play a functional role in cancer-associated processes, such as metastasis and loss of imprinting. Aberrant lncRNA expression participates in carcinogenesis by disrupting major biological processes, such as redirecting chromatin remodeling complexes or inactivating major tumor suppressor genes. We also describe the potential role of dysregulated T-UCRs in cancer, and place these unique RNAs in the lncRNA category. Finally, we note the potential utility of lncRNAs in cancer as diagnostic and prognostic markers, as well as the potential of developing lncRNA mediated therapy.

Abbreviations

44ANRIL: Antisense Non-coding RNA in the INK4 Locus; AR: androgen receptor; CREB: cAMP response element binding protein; DD3: Differential Display Code 3; HBV: hepatitis B virus; HCC: hepatocellular carcinoma cell lines; HOTAIR: HOX Antisense Intergenic RNA; HULC: Highly Upregulated in Liver Cancer; IGF2: Insulin-Like Growth Factor 2; kb: kilobase; lincRNA: long or large intergenic non-coding RNA; lncRNA: long non-coding RNA; LTR: long terminal repeat; MALAT1: Metastatis-Associated Lung Adenocarcinoma Transcript 1; MEG3: Maternally Expressed Gene 3; miRNA: microRNA; ncRNA: non-coding RNA; nt: nucleotide; PCNCR1: Prostate Cancer Non-Coding RNA 1; PEI: polyethylenimine; PRC: polycomb repressive complex; PTEN: phosphatase and tensin homolog; PTENP1: phosphatase and tensin homolog pseudogene 1; RNase: ribonuclease; RNA pol II: RNA polymerase II; RNA pol III: RNA polymerase III; RNAi: RNA interference; SR: serine-arginine rich splicing proteins; TGS: transcriptional gene silencing; tiRNA: transcription initiation RNAs; T-UCR: transcribed ultraconserved region; UTR: untranslated region; XIST: X-Inactive-Specific Transcript.

Competing interests

45The authors declare that they have no competing interests.

Authors' contributions

46EAG wrote the first draft of the article, CJB and WLL finalized the manuscript. All authors read and approved the final manuscript.

Authors' information

47EAG is a research fellow at the BC Cancer Agency Research Centre, specializing in non-coding RNA gene structure and function. CJB is a professor of Medical Genetics at the University of British Columbia. Her research focuses on human X chromosome inactivation, in particular the role of XIST, a gene she first described during postdoctoral studies in the Willard lab. WLL is a professor of Pathology and Laboratory Medicine at the University of British Columbia. His team invented tiling path array technologies for whole genome and methylome analyses.

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Not in our library10.1016/j.mrfmmm.2008.07.010
134.
Hayami S Kelly JD Cho HS Yoshimatsu M Unoki M Tsunoda T Field HI Neal DE Yamaue H Ponder BA Overexpression of LSD1 contributes to human carcinogenesis through chromatin regulation in various cancersInt J Cancer2011 1283574586
Not in our library10.1002/ijc.25349
135.
Ji P Diederichs S Wang W Boing S Metzger R Schneider PM Tidow N Brandt B Buerger H Bulk E MALAT-1, a novel noncoding RNA, and thymosin beta4 predict metastasis and survival in early-stage non-small cell lung cancerOncogene2003 223980318041
Not in our library10.1038/sj.onc.1206928
136.
A screen for nuclear transcripts identifies two linked noncoding RNAs associated with SC35 splicing domains · 2007
No notice
137.
Yamada K Kano J Tsunoda H Yoshikawa H Okubo C Ishiyama T Noguchi M Phenotypic characterization of endometrial stromal sarcoma of the uterusCancer Sci2006 972106112
Not in our library10.1111/j.1349-7006.2006.00147.x
138.
Lin R Maeda S Liu C Karin M Edgington TS A large noncoding RNA is a marker for murine hepatocellular carcinomas and a spectrum of human carcinomasOncogene2007 266851858
Not in our library10.1038/sj.onc.1209846
139.
Luo JH Ren B Keryanov S Tseng GC Rao UN Monga SP Strom S Demetris AJ Nalesnik M Yu YP Transcriptomic and genomic analysis of human hepatocellular carcinomas and hepatoblastomasHepatology2006 44410121024
Not in our library10.1002/hep.21328
140.
Davis IJ Hsi BL Arroyo JD Vargas SO Yeh YA Motyckova G Valencia P Perez-Atayde AR Argani P Ladanyi M Cloning of an Alpha-TFEB fusion in renal tumors harboring the t(6;11)(p21;q13) chromosome translocationProc Natl Acad Sci USA2003 1001060516056
Not in our library10.1073/pnas.0931430100
141.
Kuiper RP Schepens M Thijssen J van Asseldonk M van den Berg E Bridge J Schuuring E Schoenmakers EF van Kessel AG Upregulation of the transcription factor TFEB in t(6;11)(p21;q13)-positive renal cell carcinomas due to promoter substitutionHum Mol Genet2003 121416611669
Not in our library10.1093/hmg/ddg178
142.
Rajaram V Knezevich S Bove KE Perry A Pfeifer JD DNA sequence of the translocation breakpoints in undifferentiated embryonal sarcoma arising in mesenchymal hamartoma of the liver harboring the t(11;19)(q11;q13.4) translocationGenes Chromosomes Cancer2007 465508513
Not in our library10.1002/gcc.20437
143.
Wilusz JE Freier SM Spector DL 3' end processing of a long nuclear-retained noncoding RNA yields a tRNA-like cytoplasmic RNACell2008 1355919932
Not in our library10.1016/j.cell.2008.10.012
144.
Kapranov P Cheng J Dike S Nix DA Duttagupta R Willingham AT Stadler PF Hertel J Hackermuller J Hofacker IL RNA maps reveal new RNA classes and a possible function for pervasive transcriptionScience2007 316583014841488
Not in our library10.1126/science.1138341
145.
Mercer TR Wilhelm D Dinger ME Solda G Korbie DJ Glazov EA Truong V Schwenke M Simons C Matthaei KI Expression of distinct RNAs from 3' untranslated regionsNucleic Acids Res2010
Not in our library10.1093/nar/gkq1158
146.
Mercer TR Dinger ME Bracken CP Kolle G Szubert JM Korbie DJ Askarian-Amiri ME Gardiner BB Goodall GJ Grimmond SM Regulated post-transcriptional RNA cleavage diversifies the eukaryotic transcriptomeGenome Res2010 201216391650
Not in our library10.1101/gr.112128.110
147.
Ni T Corcoran DL Rach EA Song S Spana EP Gao Y Ohler U Zhu J A paired-end sequencing strategy to map the complex landscape of transcription initiationNat Methods2010 77521527
Not in our library10.1038/nmeth.1464
148.
Otsuka Y Kedersha NL Schoenberg DR Identification of a cytoplasmic complex that adds a cap onto 5'-monophosphate RNAMol Cell Biol2009 29821552167
Not in our library10.1128/mcb.01325-08
149.
Post-transcriptional processing generates a diversity of 5'-modified long and short RNAsNature2009 457723210281032
Not in our library10.1038/nature07759
150.
Bernard D Prasanth KV Tripathi V Colasse S Nakamura T Xuan Z Zhang MQ Sedel F Jourdren L Coulpier F A long nuclear-retained non-coding RNA regulates synaptogenesis by modulating gene expressionEMBO J2010 291830823093
Not in our library10.1038/emboj.2010.199
151.
Tano K Mizuno R Okada T Rakwal R Shibato J Masuo Y Ijiri K Akimitsu N MALAT-1 enhances cell motility of lung adenocarcinoma cells by influencing the expression of motility-related genesFEBS Lett2010 5842245754580
Not in our library10.1016/j.febslet.2010.10.008
152.
Guo F Li Y Liu Y Wang J Li G Inhibition of metastasis-associated lung adenocarcinoma transcript 1 in CaSki human cervical cancer cells suppresses cell proliferation and invasionActa Biochim Biophys Sin (Shanghai)2010 423224229
Not in our library10.1093/abbs/gmq008
153.
Eis PS Tam W Sun L Chadburn A Li Z Gomez MF Lund E Dahlberg JE Accumulation of miR-155 and BIC RNA in human B cell lymphomasProc Natl Acad Sci USA2005 1021036273632
Not in our library10.1073/pnas.0500613102
154.
Mestdagh P Bostrom AK Impens F Fredlund E Van Peer G De Antonellis P von Stedingk K Ghesquiere B Schulte S Dews M The miR-17-92 microRNA cluster regulates multiple components of the TGF-beta pathway in neuroblastomaMol Cell2010 405762773
Not in our library10.1016/j.molcel.2010.11.038
155.
Zhao R Bodnar MS Spector DL Nuclear neighborhoods and gene expressionCurr Opin Genet Dev2009 192172179
Not in our library10.1016/j.gde.2009.02.007
156.
Miyoshi N Wagatsuma H Wakana S Shiroishi T Nomura M Aisaka K Kohda T Surani MA Kaneko-Ishino T Ishino F Identification of an imprinted gene, Meg3/Gtl2 and its human homologue MEG3, first mapped on mouse distal chromosome 12 and human chromosome 14qGenes Cells2000 53211220
Not in our library10.1046/j.1365-2443.2000.00320.x
157.
Zhang X Zhou Y Mehta KR Danila DC Scolavino S Johnson SR Klibanski A A pituitary-derived MEG3 isoform functions as a growth suppressor in tumor cellsJ Clin Endocrinol Metab2003 881151195126
Not in our library10.1210/jc.2003-030222
158.
Zhang X Rice K Wang Y Chen W Zhong Y Nakayama Y Zhou Y Klibanski A Maternally expressed gene 3 (MEG3) noncoding ribonucleic acid: isoform structure, expression, and functionsEndocrinology2010 1513939947
Not in our library10.1210/en.2009-0657
159.
At Least Ten Genes Define the Imprinted Dlk1-Dio3 Cluster on Mouse Chromosome 12qF1 · 2009
No notice
160.
Schuster-Gossler K Bilinski P Sado T Ferguson-Smith A Gossler A The mouse Gtl2 gene is differentially expressed during embryonic development, encodes multiple alternatively spliced transcripts, and may act as an RNADev Dyn1998 2122214228
Not in our library10.1002/(sici)1097-0177(199806)212:2<214::aid-aja6>3.0.co;2-k
161.
Mondal T Rasmussen M Pandey GK Isaksson A Kanduri C Characterization of the RNA content of chromatinGenome Res2010 207899907
Not in our library10.1101/gr.103473.109
162.
Zhou Y Zhong Y Wang Y Zhang X Batista DL Gejman R Ansell PJ Zhao J Weng C Klibanski A Activation of p53 by MEG3 non-coding RNAJ Biol Chem2007 282342473124742
Not in our library10.1074/jbc.m702029200
163.
Pang KC Frith MC Mattick JS Rapid evolution of noncoding RNAs: lack of conservation does not mean lack of functionTrends Genet2006 22115
Not in our library10.1016/j.tig.2005.10.003
164.
Huarte M Guttman M Feldser D Garber M Koziol MJ Kenzelmann-Broz D Khalil AM Zuk O Amit I Rabani M A large intergenic noncoding RNA induced by p53 mediates global gene repression in the p53 responseCell2010 1423409419
Not in our library10.1016/j.cell.2010.06.040
165.
Zhang L Huang J Yang N Greshock J Megraw MS Giannakakis A Liang S Naylor TL Barchetti A Ward MR microRNAs exhibit high frequency genomic alterations in human cancerProc Natl Acad Sci USA2006 1032491369141
Not in our library10.1073/pnas.0508889103
166.
Calin GA Sevignani C Dumitru CD Hyslop T Noch E Yendamuri S Shimizu M Rattan S Bullrich F Negrini M Human microRNA genes are frequently located at fragile sites and genomic regions involved in cancersProc Natl Acad Sci USA2004 101929993004
Not in our library10.1073/pnas.0307323101
167.
Weber B Stresemann C Brueckner B Lyko F Methylation of human microRNA genes in normal and neoplastic cellsCell Cycle2007 6910011005
Not in our library10.4161/cc.6.9.4209
168.
Lehmann U Hasemeier B Christgen M Muller M Romermann D Langer F Kreipe H Epigenetic inactivation of microRNA gene hsa-mir-9-1 in human breast cancerJ Pathol2008 21411724
Not in our library10.1002/path.2251
169.
Ebert MS Neilson JR Sharp PA MicroRNA sponges: competitive inhibitors of small RNAs in mammalian cellsNat Methods2007 49721726
Not in our library10.1038/nmeth1079
170.
Panzitt K Tschernatsch MM Guelly C Moustafa T Stradner M Strohmaier HM Buck CR Denk H Schroeder R Trauner M Characterization of HULC, a novel gene with striking up-regulation in hepatocellular carcinoma, as noncoding RNAGastroenterology2007 1321330342
Not in our library10.1053/j.gastro.2006.08.026
171.
Matouk IJ Abbasi I Hochberg A Galun E Dweik H Akkawi M Highly upregulated in liver cancer noncoding RNA is overexpressed in hepatic colorectal metastasisEur J Gastroenterol Hepatol2009 216688692
Not in our library10.1097/meg.0b013e328306a3a2
172.
Wang J Liu X Wu H Ni P Gu Z Qiao Y Chen N Sun F Fan Q CREB up-regulates long non-coding RNA, HULC expression through interaction with microRNA-372 in liver cancerNucleic Acids Res2010 381653665383
Not in our library10.1093/nar/gkq285
173.
Poliseno L Salmena L Zhang J Carver B Haveman WJ Pandolfi PP A coding-independent function of gene and pseudogene mRNAs regulates tumour biologyNature2010 465730110331038
Not in our library10.1038/nature09144
174.
Alimonti A Carracedo A Clohessy JG Trotman LC Nardella C Egia A Salmena L Sampieri K Haveman WJ Brogi E Subtle variations in Pten dose determine cancer susceptibilityNat Genet2010 425454458
Not in our library10.1038/ng.556
175.
Yu W Gius D Onyango P Muldoon-Jacobs K Karp J Feinberg AP Cui H Epigenetic silencing of tumour suppressor gene p15 by its antisense RNANature2008 4517175202206
Not in our library10.1038/nature06468
176.
Relationship between CAD Risk Genotype in the Chromosome 9p21 Locus and Gene Expression. Identification of Eight New ANRIL Splice Variants · 2009
No notice
177.
Serrano M Hannon GJ Beach D A new regulatory motif in cell-cycle control causing specific inhibition of cyclin D/CDK4Nature1993 3666456704707
Not in our library10.1038/366704a0
178.
Kamb A Gruis NA Weaver-Feldhaus J Liu Q Harshman K Tavtigian SV Stockert E Day RS Johnson BE Skolnick MH A cell cycle regulator potentially involved in genesis of many tumor typesScience1994 2645157436440
Not in our library10.1126/science.8153634
179.
Kamijo T Zindy F Roussel MF Quelle DE Downing JR Ashmun RA Grosveld G Sherr CJ Tumor suppression at the mouse INK4a locus mediated by the alternative reading frame product p19ARFCell1997 915649659
Not in our library10.1016/s0092-8674(00)80452-3
180.
Jacobs JJ Kieboom K Marino S DePinho RA van Lohuizen M The oncogene and Polycomb-group gene bmi-1 regulates cell proliferation and senescence through the ink4a locusNature1999 3976715164168
Not in our library10.1038/16476
181.
Popov N Gil J Epigenetic regulation of the INK4b-ARF-INK4a locus: in sickness and in healthEpigenetics2010 58685690
Not in our library10.4161/epi.5.8.12996
182.
Chromosome 9p21 SNPs Associated with Multiple Disease Phenotypes Correlate with ANRIL Expression · 2010
No notice
183.
Yap KL Li S Munoz-Cabello AM Raguz S Zeng L Mujtaba S Gil J Walsh MJ Zhou MM Molecular interplay of the noncoding RNA ANRIL and methylated histone H3 lysine 27 by polycomb CBX7 in transcriptional silencing of INK4aMol Cell2010 385662674
Not in our library10.1016/j.molcel.2010.03.021
184.
Kotake Y Nakagawa T Kitagawa K Suzuki S Liu N Kitagawa M Xiong Y Long non-coding RNA ANRIL is required for the PRC2 recruitment to and silencing of p15(INK4B) tumor suppressor geneOncogene2010
Not in our library10.1038/onc.2010.568
185.
Bidirectional Transcription Directs Both Transcriptional Gene Activation and Suppression in Human Cells · 2008
No notice
186.
Szell M Bata-Csorgo Z Kemeny L The enigmatic world of mRNA-like ncRNAs: their role in human evolution and in human diseasesSemin Cancer Biol2008 182141148
Not in our library10.1016/j.semcancer.2008.01.007
187.
Chung S Nakagawa H Uemura M Piao L Ashikawa K Hosono N Takata R Akamatsu S Kawaguchi T Morizono T Association of a novel long non-coding RNA in 8q24 with prostate cancer susceptibilityCancer Sci2011 1021245252
Not in our library10.1111/j.1349-7006.2010.01737.x
188.
Petrovics G Zhang W Makarem M Street JP Connelly R Sun L Sesterhenn IA Srikantan V Moul JW Srivastava S Elevated expression of PCGEM1, a prostate-specific gene with cell growth-promoting function, is associated with high-risk prostate cancer patientsOncogene2004 232605611
Not in our library10.1038/sj.onc.1207069
189.
Bussemakers MJ van Bokhoven A Verhaegh GW Smit FP Karthaus HF Schalken JA Debruyne FM Ru N Isaacs WB DD3: a new prostate-specific gene, highly overexpressed in prostate cancerCancer Res1999 592359755979
Not in our library
190.
de Kok JB Verhaegh GW Roelofs RW Hessels D Kiemeney LA Aalders TW Swinkels DW Schalken JA DD3(PCA3), a very sensitive and specific marker to detect prostate tumorsCancer Res2002 62926952698
Not in our library
191.
Dieci G Fiorino G Castelnuovo M Teichmann M Pagano A The expanding RNA polymerase III transcriptomeTrends Genet2007 2312614622
Not in our library10.1016/j.tig.2007.09.001
192.
White RJ RNA polymerases I and III, non-coding RNAs and cancerTrends Genet2008 2412622629
Not in our library10.1016/j.tig.2008.10.003
193.
White RJ RNA polymerase III transcription and cancerOncogene2004 231832083216
Not in our library10.1038/sj.onc.1207547
194.
Integrative genomic analyses identify BRF2 as a novel lineage-specific oncogene in lung squamous cell carcinoma. · 2010
Not checked
195.
Marshall L White RJ Non-coding RNA production by RNA polymerase III is implicated in cancerNat Rev Cancer2008 812911914
Not in our library10.1038/nrc2539
196.
Watson JB Sutcliffe JG Primate brain-specific cytoplasmic transcript of the Alu repeat familyMol Cell Biol1987 7933243327
Not in our library10.1128/mcb.7.9.3324-3327.1987
197.
Tiedge H Chen W Brosius J Primary structure, neural-specific expression, and dendritic location of human BC200 RNAJ Neurosci1993 13623822390
Not in our library10.1523/jneurosci.13-06-02382.1993
198.
Martignetti JA Brosius J BC200 RNA: a neural RNA polymerase III product encoded by a monomeric Alu elementProc Natl Acad Sci USA1993 90241156311567
Not in our library10.1073/pnas.90.24.11563
199.
Lin D Pestova TV Hellen CU Tiedge H Translational control by a small RNA: dendritic BC1 RNA targets the eukaryotic initiation factor 4A helicase mechanismMol Cell Biol2008 28930083019
Not in our library10.1128/mcb.01800-07
200.
Calin GA Liu CG Ferracin M Hyslop T Spizzo R Sevignani C Fabbri M Cimmino A Lee EJ Wojcik SE Ultraconserved regions encoding ncRNAs are altered in human leukemias and carcinomasCancer Cell2007 123215229
Not in our library10.1016/j.ccr.2007.07.027
201.
Katzman S Kern AD Bejerano G Fewell G Fulton L Wilson RK Salama SR Haussler D Human genome ultraconserved elements are ultraselectedScience2007 3175840915
Not in our library10.1126/science.1142430
202.
Bejerano G Pheasant M Makunin I Stephen S Kent WJ Mattick JS Haussler D Ultraconserved elements in the human genomeScience2004 304567513211325
Not in our library10.1126/science.1098119
203.
Braconi C Valeri N Kogure T Gasparini P Huang N Nuovo GJ Terracciano L Croce CM Patel T Expression and functional role of a transcribed noncoding RNA with an ultraconserved element in hepatocellular carcinomaProc Natl Acad Sci USA2010
Not in our library10.1073/pnas.1011098108
204.
Lujambio A Portela A Liz J Melo SA Rossi S Spizzo R Croce CM Calin GA Esteller M CpG island hypermethylation-associated silencing of non-coding RNAs transcribed from ultraconserved regions in human cancerOncogene2010 294863906401
Not in our library10.1038/onc.2010.361
205.
Morris KV RNA-directed transcriptional gene silencing and activation in human cellsOligonucleotides2009 194299306
Not in our library10.1089/oli.2009.0212
206.
Scholer N Langer C Dohner H Buske C Kuchenbauer F Serum microRNAs as a novel class of biomarkers: a comprehensive review of the literatureExp Hematol2010 381211261130
Not in our library10.1016/j.exphem.2010.10.004
207.
Xie Y Todd NW Liu Z Zhan M Fang H Peng H Alattar M Deepak J Stass SA Jiang F Altered miRNA expression in sputum for diagnosis of non-small cell lung cancerLung Cancer2010 672170176
Not in our library10.1016/j.lungcan.2009.04.004
208.
Xing L Todd NW Yu L Fang H Jiang F Early detection of squamous cell lung cancer in sputum by a panel of microRNA markersMod Pathol2010 23811571164
Not in our library10.1038/modpathol.2010.111
209.
Kosaka N Iguchi H Ochiya T Circulating microRNA in body fluid: a new potential biomarker for cancer diagnosis and prognosisCancer Sci2010 1011020872092
Not in our library10.1111/j.1349-7006.2010.01650.x
210.
Hanke M Hoefig K Merz H Feller AC Kausch I Jocham D Warnecke JM Sczakiel G A robust methodology to study urine microRNA as tumor marker: microRNA-126 and microRNA-182 are related to urinary bladder cancerUrol Oncol2010 286655661
Not in our library10.1016/j.urolonc.2009.01.027
211.
Tinzl M Marberger M Horvath S Chypre C DD3PCA3 RNA analysis in urine--a new perspective for detecting prostate cancerEur Urol2004 462182186discussion 187
Not in our library10.1016/j.eururo.2004.06.004
212.
Hessels D Klein Gunnewiek JM van Oort I Karthaus HF van Leenders GJ van Balken B Kiemeney LA Witjes JA Schalken JA DD3(PCA3)-based molecular urine analysis for the diagnosis of prostate cancerEur Urol2003 441815discussion 15-16
Not in our library10.1016/s0302-2838(03)00201-x
213.
Costa FF Non-coding RNAs and new opportunities for the private sectorDrug Discov Today2009 149-10446452
Not in our library10.1016/j.drudis.2009.01.008
214.
Hung T Chang HY Long noncoding RNA in genome regulation: Prospects and mechanismsRNA Biol2010 75
Not in our library10.4161/rna.7.5.13216
215.
Tsai MC Spitale RC Chang HY Long Intergenic Noncoding RNAs: New Links in Cancer ProgressionCancer Res2011 71137
Not in our library10.1158/0008-5472.can-10-2483
216.
Smaldone MC Davies BJ BC-819, a plasmid comprising the H19 gene regulatory sequences and diphtheria toxin A, for the potential targeted therapy of cancersCurr Opin Mol Ther2010 125607616
Not in our library
217.
Midoux P Breuzard G Gomez JP Pichon C Polymer-based gene delivery: a current review on the uptake and intracellular trafficking of polyplexesCurr Gene Ther2008 85335352
Not in our library10.2174/156652308786071014
218.
Amit D Hochberg A Development of targeted therapy for bladder cancer mediated by a double promoter plasmid expressing diphtheria toxin under the control of H19 and IGF2-P4 regulatory sequencesJ Transl Med2010 81134
Not in our library10.1186/1479-5876-8-134
219.
Ohana P Gofrit O Ayesh S Al-Sharef W Mizrahi A Birman T Schneider T Matouk I de Groot N Tavdy E Regulatory sequences of the H19 gene in DNA based therapy of bladder cancerGene Therapy and Molecular Biology2004 8181192
Not in our library
220.
Scaiewicz V Sorin V Fellig Y Birman T Mizrahi A Galula J Abu-Lail R Shneider T Ohana P Buscail L Use of H19 Gene Regulatory Sequences in DNA-Based Therapy for Pancreatic CancerJ Oncol2010 2010178174
Not in our library10.1155/2010/178174
221.
Development of targeted therapy for ovarian cancer mediated by a plasmid expressing diphtheria toxin under the control of H19 regulatory sequences · 2009
No notice
222.
Phizicky EM Hopper AK tRNA biology charges to the frontGenes Dev2010 241718321860
Not in our library10.1101/gad.1956510
223.
Hannan KM Hannan RD Rothblum LI Transcription by RNA polymerase IFront Biosci1998 3d376398
Not in our library10.2741/a282
224.
Stults DM Killen MW Pierce HH Pierce AJ Genomic architecture and inheritance of human ribosomal RNA gene clustersGenome Res2008 1811318
Not in our library10.1101/gr.6858507
225.
Lin H piRNAs in the germ lineScience2007 3165823397
Not in our library10.1126/science.1137543
226.
Kapranov P Ozsolak F Kim SW Foissac S Lipson D Hart C Roels S Borel C Antonarakis SE Monaghan AP New class of gene-termini-associated human RNAs suggests a novel RNA copying mechanismNature2010 4667306642646
Not in our library10.1038/nature09190
227.
Kiss T Small nucleolar RNA-guided post-transcriptional modification of cellular RNAsEMBO J2001 201436173622
Not in our library10.1093/emboj/20.14.3617
228.
Filipowicz W Pogacic V Biogenesis of small nucleolar ribonucleoproteinsCurr Opin Cell Biol2002 143319327
Not in our library10.1016/s0955-0674(02)00334-4
229.
Seila AC Calabrese JM Levine SS Yeo GW Rahl PB Flynn RA Young RA Sharp PA Divergent transcription from active promotersScience2008 322590918491851
Not in our library10.1126/science.1162253
230.
Valadkhan S snRNAs as the catalysts of pre-mRNA splicingCurr Opin Chem Biol2005 96603608
Not in our library10.1016/j.cbpa.2005.10.008
231.
Faulkner GJ Carninci P Altruistic functions for selfish DNACell Cycle2009 81828952900
Not in our library10.4161/cc.8.18.9536
232.
Faulkner GJ Kimura Y Daub CO Wani S Plessy C Irvine KM Schroder K Cloonan N Steptoe AL Lassmann T The regulated retrotransposon transcriptome of mammalian cellsNat Genet2009 415563571
Not in our library10.1038/ng.368
233.
Kandhavelu M Lammi C Buccioni M Dal Ben D Volpini R Marucci G Existence of snoRNA, microRNA, piRNA characteristics in a novel non-coding RNA: x-ncRNA and its biological implication in Homo sapiensJournal of Bioinformatics and Sequence Analysis2009 123140
Not in our library
234.
Christov CP Gardiner TJ Szuts D Krude T Functional requirement of noncoding Y RNAs for human chromosomal DNA replicationMol Cell Biol2006 261869937004
Not in our library10.1128/mcb.01060-06
235.
Li Z Kim SW Lin Y Moore PS Chang Y John B Characterization of viral and human RNAs smaller than canonical MicroRNAsJ Virol2009 83241275112758
Not in our library10.1128/jvi.01325-09
236.
Parrott AM Mathews MB snaR genes: recent descendants of Alu involved in the evolution of chorionic gonadotropinsCold Spring Harb Symp Quant Biol2009 74363373
Not in our library10.1101/sqb.2009.74.038
237.
Parrott AM Tsai M Batchu P Ryan K Ozer HL Tian B Mathews MB The evolution and expression of the snaR family of small non-coding RNAsNucleic Acids Res2011 39414851500
Not in our library10.1093/nar/gkq856
238.
Stadler PF Chen JJ Hackermuller J Hoffmann S Horn F Khaitovich P Kretzschmar AK Mosig A Prohaska SJ Qi X Evolution of vault RNAsMol Biol Evol2009 26919751991
Not in our library10.1093/molbev/msp112
239.
Zheng D Frankish A Baertsch R Kapranov P Reymond A Choo SW Lu Y Denoeud F Antonarakis SE Snyder M Pseudogenes in the ENCODE regions: consensus annotation, analysis of transcription, and evolutionGenome Res2007 176839851
Not in our library10.1101/gr.5586307
240.
Identification and analysis of unitary pseudogenes: historic and contemporary gene losses in humans and other primates · 2010
No notice
241.
Zheng R Shen Z Tripathi V Xuan Z Freier SM Bennett CF Prasanth SG Prasanth KV Polypurine-repeat-containing RNAs: a novel class of long non-coding RNA in mammalian cellsJ Cell Sci2010 123Pt 2137343744
Not in our library10.1242/jcs.070466
242.
Louro R Smirnova AS Verjovski-Almeida S Long intronic noncoding RNA transcription: expression noise or expression choice?Genomics2009 934291298
Not in our library10.1016/j.ygeno.2008.11.009
243.
Rearick D Prakash A McSweeny A Shepard SS Fedorova L Fedorov A Critical association of ncRNA with intronsNucleic Acids Res2010
Not in our library10.1093/nar/gkq1080
244.
Katayama S Tomaru Y Kasukawa T Waki K Nakanishi M Nakamura M Nishida H Yap CC Suzuki M Kawai J Antisense transcription in the mammalian transcriptomeScience2005 309574015641566
Not in our library10.1126/science.1112009
245.
Preker P Nielsen J Kammler S Lykke-Andersen S Christensen MS Mapendano CK Schierup MH Jensen TH RNA exosome depletion reveals transcription upstream of active human promotersScience2008 322590918511854
Not in our library10.1126/science.1164096
246.
Zhang Y Guan DG Yang JH Shao P Zhou H Qu LH ncRNAimprint: a comprehensive database of mammalian imprinted noncoding RNAsRNA2010 161018891901
Not in our library10.1261/rna.2226910
247.
Szymanski M Erdmann VA Barciszewski J Noncoding RNAs database (ncRNAdb)Nucleic Acids Res2007 35Database issueD162164
Not in our library10.1093/nar/gkl994
248.
Mituyama T Yamada K Hattori E Okida H Ono Y Terai G Yoshizawa A Komori T Asai K The Functional RNA Database 3.0: databases to support mining and annotation of functional RNAsNucleic Acids Res2009 37Database issueD8992
Not in our library10.1093/nar/gkn805
249.
Liu C Bai B Skogerbo G Cai L Deng W Zhang Y Bu D Zhao Y Chen R NONCODE: an integrated knowledge database of non-coding RNAsNucleic Acids Res2005 33Database issueD112115
Not in our library10.1093/nar/gki041
250.
Amaral PP Clark MB Gascoigne DK Dinger ME Mattick JS lncRNAdb: a reference database for long noncoding RNAsNucleic Acids Res2011 39Database issueD146151
Not in our library10.1093/nar/gkq1138
251.
Gardner PP Daub J Tate JG Nawrocki EP Kolbe DL Lindgreen S Wilkinson AC Finn RD Griffiths-Jones S Eddy SR Rfam: updates to the RNA families databaseNucleic Acids Res2009 37Database issueD136140
Not in our library10.1093/nar/gkn766
252.
Dinger ME Pang KC Mercer TR Crowe ML Grimmond SM Mattick JS NRED: a database of long noncoding RNA expressionNucleic Acids Res2009 37Database issueD122126
Not in our library10.1093/nar/gkn617
253.
Erdmann VA Szymanski M Hochberg A Groot N Barciszewski J Non-coding, mRNA-like RNAs database Y2KNucleic Acids Res2000 281197200
Not in our library10.1093/nar/28.1.197
254.
Wu T Wang J Liu C Zhang Y Shi B Zhu X Zhang Z Skogerbo G Chen L Lu H NPInter: the noncoding RNAs and protein related biomacromolecules interaction databaseNucleic Acids Res2006 34Database issueD150152
Not in our library10.1093/nar/gkj025
255.
Fellenberg J Bernd L Delling G Witte D Zahlten-Hinguranage A Prognostic significance of drug-regulated genes in high-grade osteosarcomaMod Pathol2007 201010851094
Not in our library10.1038/modpathol.3800937
256.
Koshimizu TA Fujiwara Y Sakai N Shibata K Tsuchiya H Oxytocin stimulates expression of a noncoding RNA tumor marker in a human neuroblastoma cell lineLife Sci2010 8611-12455460
Not in our library10.1016/j.lfs.2010.02.001
257.
Ariel I Sughayer M Fellig Y Pizov G Ayesh S Podeh D Libdeh BA Levy C Birman T Tykocinski ML The imprinted H19 gene is a marker of early recurrence in human bladder carcinomaMol Pathol2000 536320323
Not in our library10.1136/mp.53.6.320
258.
Yballe CM Vu TH Hoffman AR Imprinting and expression of insulin-like growth factor-II and H19 in normal breast tissue and breast tumorJ Clin Endocrinol Metab1996 81416071612
Not in our library10.1210/jc.81.4.1607
259.
Tanos V Ariel I Prus D De-Groot N Hochberg A H19 and IGF2 gene expression in human normal, hyperplastic, and malignant endometriumInt J Gynecol Cancer2004 143521525
Not in our library10.1111/j.1048-891x.2004.014314.x
260.
Douc-Rasy S Barrois M Fogel S Ahomadegbe JC Stehelin D Coll J Riou G High incidence of loss of heterozygosity and abnormal imprinting of H19 and IGF2 genes in invasive cervical carcinomas. Uncoupling of H19 and IGF2 expression and biallelic hypomethylation of H19Oncogene1996 122423430
Not in our library
261.
Arima T Matsuda T Takagi N Wake N Association of IGF2 and H19 imprinting with choriocarcinoma developmentCancer Genet Cytogenet1997 9313947
Not in our library10.1016/s0165-4608(96)00221-x
262.
Tanos V Prus D Ayesh S Weinstein D Tykocinski ML De-Groot N Hochberg A Ariel I Expression of the imprinted H19 oncofetal RNA in epithelial ovarian cancerEur J Obstet Gynecol Reprod Biol1999 851711
Not in our library10.1016/s0301-2115(98)00275-9
263.
Berteaux N Lottin S Adriaenssens E Van Coppenolle F Leroy X Coll J Dugimont T Curgy JJ Hormonal regulation of H19 gene expression in prostate epithelial cellsJ Endocrinol2004 18316978
Not in our library10.1677/joe.1.05696
264.
Kondo M Takahashi T [Altered genomic imprinting in the IGF2 and H19 genes in human lung cancer]Nippon Rinsho1996 542492496
Not in our library
265.
Pasic I Shlien A Durbin AD Stavropoulos DJ Baskin B Ray PN Novokmet A Malkin D Recurrent focal copy-number changes and loss of heterozygosity implicate two noncoding RNAs and one tumor suppressor gene at chromosome 3q13.31 in osteosarcomaCancer Res2010 701160171
Not in our library10.1158/0008-5472.can-09-1902
266.
PCGEM1, a prostate-specific gene, is overexpressed in prostate cancer · 2000
Not checked
267.
Fu X Ravindranath L Tran N Petrovics G Srivastava S Regulation of apoptosis by a prostate-specific and prostate cancer-associated noncoding gene, PCGEM1DNA Cell Biol2006 253135141
Not in our library10.1089/dna.2006.25.135
268.
Wang XS Zhang Z Wang HC Cai JL Xu QW Li MQ Chen YC Qian XP Lu TJ Yu LZ Rapid identification of UCA1 as a very sensitive and specific unique marker for human bladder carcinomaClin Cancer Res2006 121648514858
Not in our library10.1158/1078-0432.ccr-06-0134
269.
Wang F Li X Xie X Zhao L Chen W UCA1, a non-protein-coding RNA up-regulated in bladder carcinoma and embryo, influencing cell growth and promoting invasionFEBS Lett2008 5821319191927
Not in our library10.1016/j.febslet.2008.05.012
270.
Tsang WP Wong TW Cheung AH Co CN Kwok TT Induction of drug resistance and transformation in human cancer cells by the noncoding RNA CUDRRNA2007 136890898
Not in our library10.1261/rna.359007
271.
Korneev SA Korneeva EI Lagarkova MA Kiselev SL Critchley G O'Shea M Novel noncoding antisense RNA transcribed from human anti-NOS2A locus is differentially regulated during neuronal differentiation of embryonic stem cellsRNA2008 141020302037
Not in our library10.1261/rna.1084308
272.
Pasmant E Laurendeau I Heron D Vidaud M Vidaud D Bieche I Characterization of a germ-line deletion, including the entire INK4/ARF locus, in a melanoma-neural system tumor family: identification of ANRIL, an antisense noncoding RNA whose expression coclusters with ARFCancer Res2007 67839633969
Not in our library10.1158/0008-5472.can-06-2004
273.
Mourtada-Maarabouni M Pickard MR Hedge VL Farzaneh F Williams GT GAS5, a non-protein-coding RNA, controls apoptosis and is downregulated in breast cancerOncogene2009 282195208
Not in our library10.1038/onc.2008.373
274.
Leygue E Steroid receptor RNA activator (SRA1): unusual bifaceted gene products with suspected relevance to breast cancerNucl Recept Signal2007 5e006
Not in our library10.1621/nrs.05006
275.
Chooniedass-Kothari S Hamedani MK Troup S Hube F Leygue E The steroid receptor RNA activator protein is expressed in breast tumor tissuesInt J Cancer2006 118410541059
Not in our library10.1002/ijc.21425
276.
Zhu Y Yu M Li Z Kong C Bi J Li J Gao Z ncRAN, a Newly Identified Long Noncoding RNA, Enhances Human Bladder Tumor Growth, Invasion, and SurvivalUrology2010 772510 e511515
Not in our library10.1016/j.urology.2010.09.022
277.
Yu M Ohira M Li Y Niizuma H Oo ML Zhu Y Ozaki T Isogai E Nakamura Y Koda T High expression of ncRAN, a novel non-coding RNA mapped to chromosome 17q25.1, is associated with poor prognosis in neuroblastomaInt J Oncol2009 344931938
Not in our library10.3892/ijo_00000219

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Long non-coding RNAs affecting cell metabolism in cancer · 2022
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The Epithelial–Mesenchymal Transition at the Crossroads between Metabolism and Tumor Progression · 2022
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ALS-linked FUS mutations confer loss and gain of function in the nucleus by promoting excessive formation of dysfunctional paraspeckles · 2019
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lncRNA SNHG6 regulates EZH2 expression by sponging miR-26a/b and miR-214 in colorectal cancer · 2019
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The long noncoding RNA SNHG1 regulates colorectal cancer cell growth through interactions with EZH2 and miR-154-5p · 2018
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Long noncoding RNA CRNDE promotes colorectal cancer cell proliferation via epigenetically silencing DUSP5/CDKN1A expression · 2017
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LncRNA UCA1 in anti-cancer drug resistance · 2017
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LncRNA AK023391 promotes tumorigenesis and invasion of gastric cancer through activation of the PI3K/Akt signaling pathway · 2017
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Colorectal Carcinoma: A General Overview and Future Perspectives in Colorectal Cancer · 2017
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Long noncoding RNA MRCCAT1 promotes metastasis of clear cell renal cell carcinoma via inhibiting NPR3 and activating p38-MAPK signaling · 2017
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Discovery and validation of immune-associated long non-coding RNA biomarkers associated with clinically molecular subtype and prognosis in diffuse large B cell lymphoma · 2017
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Long non-coding RNA in glioma: signaling pathways · 2017
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