Long noncoding RNAs: novel players in colorectal cancer.

Colorectal cancer (CRC) is the most common type of cancer in the world. Despite its commonness, the underlying mechanism of CRC is not completely understood. Long noncoding RNAs (lncRNAs) have received increased attention with the development of whole genome and transcriptome sequencing technologies. Recent findings reveal that lncRNAs are implicated in serial steps of cancer development. These lncRNAs interact with DNA, RNA, protein molecules and/or their combinations, acting as an essential regulator in chromatin organization, and transcriptional and post-transcriptional regulation. In this review, we highlight recent findings of emerging roles for lncRNAs in CRC and discuss rapid translational lncRNA research for clinical application in diagnosis, prognosis and potential treatment.

[1]  S. Miyano,et al.  Long noncoding RNA HOTAIR regulates polycomb-dependent chromatin modification and is associated with poor prognosis in colorectal cancers. , 2011, Cancer research.

[2]  C. Plass,et al.  Loss of imprinting of the insulin-like growth factor II gene occurs by biallelic methylation in a core region of H19-associated CTCF-binding sites in colorectal cancer. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[3]  Y. Mo,et al.  The human long non-coding RNA-RoR is a p53 repressor in response to DNA damage , 2012, Cell Research.

[4]  Jianlin Ren,et al.  Resveratrol Inhibits Invasion and Metastasis of Colorectal Cancer Cells via MALAT1 Mediated Wnt/β-Catenin Signal Pathway , 2013, PloS one.

[5]  A. Hochberg,et al.  Regulatory sequences of H19 and IGF2 genes in DNA‐based therapy of colorectal rat liver metastases , 2005 .

[6]  Lawrence C. LaPointe,et al.  Colorectal Neoplasia Differentially Expressed (CRNDE), a Novel Gene with Elevated Expression in Colorectal Adenomas and Adenocarcinomas. , 2011, Genes & cancer.

[7]  K Sugimachi,et al.  Amplification of PVT-1 is involved in poor prognosis via apoptosis inhibition in colorectal cancers , 2013, British Journal of Cancer.

[8]  Qin Chen,et al.  lncRNA H19/miR‐675 axis represses prostate cancer metastasis by targeting TGFBI , 2014, The FEBS journal.

[9]  Cole Trapnell,et al.  Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses. , 2011, Genes & development.

[10]  Wei Wu,et al.  Understanding the Role of Long Noncoding RNAs in the Cancer Genome , 2013 .

[11]  N. Caplen,et al.  p53-dependent Induction of PVT1 and miR-1204* , 2011, The Journal of Biological Chemistry.

[12]  A. Feinberg,et al.  Loss of imprinting in colorectal cancer linked to hypomethylation of H19 and IGF2. , 2002, Cancer research.

[13]  P. Molloy,et al.  CRNDE, a long non-coding RNA responsive to insulin/IGF signaling, regulates genes involved in central metabolism. , 2014, Biochimica et biophysica acta.

[14]  M. Mourtada-Maarabouni,et al.  Growth arrest in human T-cells is controlled by the non-coding RNA growth-arrest-specific transcript 5 (GAS5) , 2008, Journal of Cell Science.

[15]  J. Bishop,et al.  The PVT gene frequently amplifies with MYC in tumor cells , 1989, Molecular and cellular biology.

[16]  Wen-Lin Kuo,et al.  Amplification of PVT1 Contributes to the Pathophysiology of Ovarian and Breast Cancer , 2007, Clinical Cancer Research.

[17]  J. Rinn,et al.  Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression , 2009, Proceedings of the National Academy of Sciences.

[18]  Stephen P. Jackson,et al.  hnRNP K: An HDM2 Target and Transcriptional Coactivator of p53 in Response to DNA Damage , 2005, Cell.

[19]  Shuhan Sun,et al.  Epigenetic activation of the MiR-200 family contributes to H19-mediated metastasis suppression in hepatocellular carcinoma. , 2013, Carcinogenesis.

[20]  F. Hou,et al.  Long non-coding RNA MALAT1 promotes tumour growth and metastasis in colorectal cancer through binding to SFPQ and releasing oncogene PTBP2 from SFPQ/PTBP2 complex , 2014, British Journal of Cancer.

[21]  F. Saad,et al.  uPM3, a new molecular urine test for the detection of prostate cancer. , 2004, Urology.

[22]  Hongtu Zheng,et al.  High expression of lncRNA MALAT1 suggests a biomarker of poor prognosis in colorectal cancer. , 2014, International journal of clinical and experimental pathology.

[23]  P. Molloy,et al.  CRNDE: A Long Non-Coding RNA Involved in CanceR, Neurobiology, and DEvelopment , 2012, Front. Gene..

[24]  Ke Liu,et al.  Linc2GO: a human LincRNA function annotation resource based on ceRNA hypothesis , 2013, Bioinform..

[25]  Anna L. Walsh,et al.  Long noncoding RNAs and prostate carcinogenesis: the missing 'linc'? , 2014, Trends in molecular medicine.

[26]  Gordon G Carmichael,et al.  Long noncoding RNAs in mammalian cells: what, where, and why? , 2010, Wiley interdisciplinary reviews. RNA.

[27]  B. Davies,et al.  BC-819, a plasmid comprising the H19 gene regulatory sequences and diphtheria toxin A, for the potential targeted therapy of cancers. , 2010, Current opinion in molecular therapeutics.

[28]  Hui Zhou,et al.  starBase: a database for exploring microRNA–mRNA interaction maps from Argonaute CLIP-Seq and Degradome-Seq data , 2010, Nucleic Acids Res..

[29]  Michael Thomas,et al.  MALAT-1, a novel noncoding RNA, and thymosin β4 predict metastasis and survival in early-stage non-small cell lung cancer , 2003, Oncogene.

[30]  Junhui Ge,et al.  Human colorectal cancer-specific CCAT1-L lncRNA regulates long-range chromatin interactions at the MYC locus , 2014, Cell Research.

[31]  Hongtu Zheng,et al.  Low expression of novel lncRNA RP11-462C24.1 suggests a biomarker of poor prognosis in colorectal cancer , 2014, Medical Oncology.

[32]  M. Mourtada-Maarabouni,et al.  GAS5, a non-protein-coding RNA, controls apoptosis and is downregulated in breast cancer , 2009, Oncogene.

[33]  R. Reinhardt,et al.  Sequence and functional comparison in the Beckwith-Wiedemann region: implications for a novel imprinting centre and extended imprinting. , 2000, Human molecular genetics.

[34]  Martin Vingron,et al.  Expression profile and transcription factor binding site exploration of imprinted genes in human and mouse , 2009, BMC Genomics.

[35]  L. You,et al.  Genome-wide screen identifies PVT1 as a regulator of Gemcitabine sensitivity in human pancreatic cancer cells. , 2011, Biochemical and biophysical research communications.

[36]  Fang Wang,et al.  Oncofetal long noncoding RNA PVT1 promotes proliferation and stem cell‐like property of hepatocellular carcinoma cells by stabilizing NOP2 , 2014, Hepatology.

[37]  Thomas Thum,et al.  Exosomes: new players in cell-cell communication. , 2012, The international journal of biochemistry & cell biology.

[38]  A. Feinberg,et al.  Loss of imprinting of IGF2: a common epigenetic modifier of intestinal tumor risk. , 2005, Cancer research.

[39]  K. Zatloukal,et al.  Characterization of HULC, a novel gene with striking up-regulation in hepatocellular carcinoma, as noncoding RNA. , 2007, Gastroenterology.

[40]  David G. Knowles,et al.  The GENCODE v7 catalog of human long noncoding RNAs: Analysis of their gene structure, evolution, and expression , 2012, Genome research.

[41]  Tim R. Mercer,et al.  NRED: a database of long noncoding RNA expression , 2008, Nucleic Acids Res..

[42]  Franck Court,et al.  Long-range chromatin interactions at the mouse Igf2/H19 locus reveal a novel paternally expressed long non-coding RNA , 2011, Nucleic acids research.

[43]  Esko Ukkonen,et al.  The common colorectal cancer predisposition SNP rs6983267 at chromosome 8q24 confers potential to enhanced Wnt signaling , 2009, Nature Genetics.

[44]  J. Ferlay,et al.  Global Cancer Statistics, 2002 , 2005, CA: a cancer journal for clinicians.

[45]  Hui Xiao,et al.  NONCODE v3.0: integrative annotation of long noncoding RNAs , 2011, Nucleic Acids Res..

[46]  Xu Gao,et al.  Intragenic microRNA and long non‐coding RNA: novel potential regulator of IGF2‐H19 imprinting region , 2014, Evolution & development.

[47]  M. Rosenfeld,et al.  LncRNA-Dependent Mechanisms of Androgen Receptor-regulated Gene Activation Programs , 2013, Nature.

[48]  Gerd Ritter,et al.  Colon cancer associated transcript‐1: A novel RNA expressed in malignant and pre‐malignant human tissues , 2012, International journal of cancer.

[49]  A. Chinnaiyan,et al.  The emergence of lncRNAs in cancer biology. , 2011, Cancer discovery.

[50]  Debora S. Marks,et al.  miRcode: a map of putative microRNA target sites in the long non-coding transcriptome , 2012, Bioinform..

[51]  Ning Liu,et al.  Long Non-Coding RNA H19 Promotes Glioma Cell Invasion by Deriving miR-675 , 2014, PloS one.

[52]  Gajendra P. S. Raghava,et al.  lncRNome: a comprehensive knowledgebase of human long noncoding RNAs , 2013, Database J. Biol. Databases Curation.

[53]  Letizia Carramusa,et al.  The PVT‐1 oncogene is a Myc protein target that is overexpressed in transformed cells , 2007, Journal of cellular physiology.

[54]  David Reich,et al.  A common genetic risk factor for colorectal and prostate cancer , 2007, Nature Genetics.

[55]  A. Stojadinovic,et al.  Detection of a long non-coding RNA (CCAT1) in living cells and human adenocarcinoma of colon tissues using FIT-PNA molecular beacons. , 2014, Cancer letters.

[56]  Leonard Lipovich,et al.  Genome-wide computational identification and manual annotation of human long noncoding RNA genes. , 2010, RNA.

[57]  O. Fodstad,et al.  Clinical significance of long intergenic noncoding RNA-p21 in colorectal cancer. , 2013, Clinical colorectal cancer.

[58]  M. Mourtada-Maarabouni,et al.  Long non-coding RNA GAS5 regulates apoptosis in prostate cancer cell lines. , 2013, Biochimica et biophysica acta.

[59]  J. Terdiman,et al.  Colorectal cancer screening: scientific review. , 2003, JAMA.

[60]  Howard Y. Chang,et al.  Detection of Long Non-Coding RNA in Archival Tissue: Correlation with Polycomb Protein Expression in Primary and Metastatic Breast Carcinoma , 2012, PloS one.

[61]  W. Gu,et al.  Downregulation of a long noncoding RNA-ncRuPAR contributes to tumor inhibition in colorectal cancer , 2014, Tumor Biology.

[62]  Kotb Abdelmohsen,et al.  LincRNA-p21 suppresses target mRNA translation. , 2012, Molecular cell.

[63]  Hui Zhou,et al.  starBase v2.0: decoding miRNA-ceRNA, miRNA-ncRNA and protein–RNA interaction networks from large-scale CLIP-Seq data , 2013, Nucleic Acids Res..

[64]  John L Hopper,et al.  Multiple loci with different cancer specificities within the 8q24 gene desert. , 2008, Journal of the National Cancer Institute.

[65]  Y Kopelman,et al.  Phase 1/2a, dose-escalation, safety, pharmacokinetic and preliminary efficacy study of intratumoral administration of BC-819 in patients with unresectable pancreatic cancer , 2012, Cancer Gene Therapy.

[66]  S. Diederichs,et al.  Gutschner T , Diederichs S . The hallmarks of cancer : a long non-coding RNA point of view . RNA Biol 9 : 703-719 , 2012 .

[67]  Yu-qin Pan,et al.  Up-Regulation of 91H Promotes Tumor Metastasis and Predicts Poor Prognosis for Patients with Colorectal Cancer , 2014, PloS one.

[68]  Yu-qin Pan,et al.  Loss of imprinting of IGF2 correlates with hypomethylation of the H19 differentially methylated region in the tumor tissue of colorectal cancer patients. , 2012, Molecular medicine reports.

[69]  Daniel Birnbaum,et al.  8q24 Cancer Risk Allele Associated with Major Metastatic Risk in Inflammatory Breast Cancer , 2012, PloS one.

[70]  Pavel Vodicka,et al.  HOTAIR long non-coding RNA is a negative prognostic factor not only in primary tumors, but also in the blood of colorectal cancer patients. , 2014, Carcinogenesis.

[71]  B. Cullen,et al.  The imprinted H19 noncoding RNA is a primary microRNA precursor. , 2007, RNA.

[72]  Jun Yu,et al.  Oncofetal H19-derived miR-675 regulates tumor suppressor RB in human colorectal cancer. , 2010, Carcinogenesis.

[73]  Yunli Zhou,et al.  MEG3 noncoding RNA: a tumor suppressor. , 2012, Journal of molecular endocrinology.

[74]  Yusuke Nakamura,et al.  Association of a novel long non‐coding RNA in 8q24 with prostate cancer susceptibility , 2011, Cancer science.

[75]  Shaoli Das,et al.  lnCeDB: Database of Human Long Noncoding RNA Acting as Competing Endogenous RNA , 2014, PloS one.

[76]  Jianfeng Jin,et al.  Coexpression of an intronic microRNA and its host gene reveals a potential role for miR-483-5p as an IGF2 partner , 2011, Molecular and Cellular Endocrinology.

[77]  U. Gezer,et al.  Long non‐coding RNAs with low expression levels in cells are enriched in secreted exosomes , 2014, Cell biology international.

[78]  Howard Y. Chang,et al.  Molecular mechanisms of long noncoding RNAs. , 2011, Molecular cell.

[79]  A. Hochberg,et al.  Regional therapy with DTA-H19 vector suppresses growth of colon adenocarcinoma metastases in the rat liver. , 2011, International journal of oncology.

[80]  Ming Liu,et al.  Long intergenic noncoding RNA HOTAIR is overexpressed and regulates PTEN methylation in laryngeal squamous cell carcinoma. , 2013, The American journal of pathology.

[81]  Peter Beighton,et al.  de la Chapelle, A. , 1997 .

[82]  Alexander Stojadinovic,et al.  Differential expression of colon cancer associated transcript1 (CCAT1) along the colonic adenoma-carcinoma sequence , 2013, BMC Cancer.

[83]  Kiyoshi Asai,et al.  The Functional RNA Database 3.0: databases to support mining and annotation of functional RNAs , 2008, Nucleic Acids Res..

[84]  Hui Zhou,et al.  ChIPBase: a database for decoding the transcriptional regulation of long non-coding RNA and microRNA genes from ChIP-Seq data , 2012, Nucleic Acids Res..

[85]  G. Chrousos,et al.  Noncoding RNA Gas5 Is a Growth Arrest– and Starvation-Associated Repressor of the Glucocorticoid Receptor , 2010, Science Signaling.

[86]  R. Kong,et al.  Long noncoding RNA GAS5 affects cell proliferation and predicts a poor prognosis in patients with colorectal cancer , 2014, Medical Oncology.

[87]  Michael Weber,et al.  H19 Antisense RNA Can Up-Regulate Igf2 Transcription by Activation of a Novel Promoter in Mouse Myoblasts , 2012, PloS one.

[88]  William R. Jeck,et al.  Expression of Linear and Novel Circular Forms of an INK4/ARF-Associated Non-Coding RNA Correlates with Atherosclerosis Risk , 2010, PLoS genetics.

[89]  J. Foekens,et al.  CCAT2, a novel noncoding RNA mapping to 8q24, underlies metastatic progression and chromosomal instability in colon cancer , 2013, Genome research.

[90]  Lennart Martens,et al.  LNCipedia: a database for annotated human lncRNA transcript sequences and structures , 2012, Nucleic Acids Res..

[91]  Xing Chen,et al.  LncRNADisease: a database for long-non-coding RNA-associated diseases , 2012, Nucleic Acids Res..

[92]  Lin Zhang,et al.  Association between polymorphisms in long non-coding RNA PRNCR1 in 8q24 and risk of colorectal cancer , 2013, Journal of experimental & clinical cancer research : CR.

[93]  M. Washington,et al.  Malignant transformation of colonic epithelial cells by a colon-derived long noncoding RNA. , 2013, Biochemical and biophysical research communications.

[94]  B. Blencowe,et al.  The nuclear-retained noncoding RNA MALAT1 regulates alternative splicing by modulating SR splicing factor phosphorylation. , 2010, Molecular cell.

[95]  Christopher A. Haiman,et al.  The 8q24 cancer risk variant rs6983267 demonstrates long-range interaction with MYC in colorectal cancer , 2009, Nature Genetics.

[96]  M. Fernö,et al.  c‐myc amplification is an independent prognostic factor in postmenopausal breast cancer , 1992, International journal of cancer.

[97]  M. Kitagawa,et al.  Long non-coding RNA ANRIL is required for the PRC2 recruitment to and silencing of p15INK4B tumor suppressor gene , 2011, Oncogene.

[98]  R. Kurokawa Long noncoding RNA as a regulator for transcription. , 2011, Progress in molecular and subcellular biology.

[99]  Weihua Jia,et al.  Overexpression of long noncoding RNA PCAT-1 is a novel biomarker of poor prognosis in patients with colorectal cancer , 2013, Medical Oncology.

[100]  Marcel E. Dinger,et al.  lncRNAdb v2.0: expanding the reference database for functional long noncoding RNAs , 2014, Nucleic Acids Res..

[101]  C. Ponting,et al.  Evolution and Functions of Long Noncoding RNAs , 2009, Cell.

[102]  Jun Yu,et al.  Oncofetal H 19-derived miR-675 regulates tumor suppressor RB in human colorectal cancer , 2010 .

[103]  Haojie Huang,et al.  Phosphorylation of EZH2 by CDK1 and CDK2 , 2011, Cell cycle.

[104]  Martin Reczko,et al.  DIANA-LncBase: experimentally verified and computationally predicted microRNA targets on long non-coding RNAs , 2012, Nucleic Acids Res..

[105]  Yumei Du,et al.  Elevation of Highly Up-regulated in Liver Cancer (HULC) by Hepatitis B Virus X Protein Promotes Hepatoma Cell Proliferation via Down-regulating p18* , 2012, The Journal of Biological Chemistry.

[106]  Wei Wang,et al.  Long non-coding RNA H19 increases bladder cancer metastasis by associating with EZH2 and inhibiting E-cadherin expression. , 2013, Cancer letters.

[107]  C. Croce,et al.  Non-codingRNA sequence variations in human chronic lymphocytic leukemia and colorectal cancer. , 2010, Carcinogenesis.

[108]  Wei Gao,et al.  Long non-coding RNA GAS5 functions as a tumor suppressor in renal cell carcinoma. , 2013, Asian Pacific journal of cancer prevention : APJCP.

[109]  Min-hui Yang,et al.  MALAT-1: a long non-coding RNA and its important 3' end functional motif in colorectal cancer metastasis. , 2011, International journal of oncology.

[110]  Howard Y. Chang,et al.  Long noncoding RNA HOTAIR reprograms chromatin state to promote cancer metastasis , 2010, Nature.

[111]  Kazuhiro Murakami,et al.  Expression profile of LIT1/KCNQ1OT1 and epigenetic status at the KvDMR1 in colorectal cancers , 2006, Cancer science.