Long non-coding RNAs in cancer invasion and metastasis

Modern Pathology

Volumn 28, Issue 1, 2015, Pages 4-13

  Shen, Xiao Han ^a,b,c   Qi, Peng ^a,b,c   Du, Xiang ^a,b,c  

^a FUDAN UNIVERSITY SHANGHAI CANCER CENTER   (China)

^b FUDAN UNIVERSITY   (China)

^c Dongjiang Pathology Institue   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; BIOCHEMICAL MARKER; HEPATOCYTE NUCLEAR FACTOR; LONG UNTRANSLATED RNA; MITOGEN ACTIVATED PROTEIN KINASE; WNT PROTEIN;

CANCER PROGNOSIS; HUMAN; METASTASIS; NONHUMAN; REVIEW; RNA TRANSCRIPTION; SIGNAL TRANSDUCTION; TUMOR INVASION; ANIMAL; GENETICS; NEOPLASM;

ANIMALS; HUMANS; NEOPLASM INVASIVENESS; NEOPLASMS; RNA, LONG NONCODING;

EID: 84920697843     PISSN: 08933952     EISSN: 15300285     Source Type: Journal    
DOI: 10.1038/modpathol.2014.75     Document Type: Review

References (100)

1. Kapranov P, Willingham AT, Gingeras TR. Genomewide transcription and the implications for genomic organization. Nat Rev Genet 2007;8:413-423.
2. Khachane AN, Harrison PM. Mining mammalian transcript data for functional long non-coding RNAs. PLoS One 2010;5:e10316.
3. Guttman M, Amit I, Garber M, et al. Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature 2009; 458:223-227.
4. Ponting CP, Oliver PL, Reik W. Evolution and functions of long noncoding RNAs. Cell 2009;136:629-641.
5. Kapranov P, St. Laurent G, Raz T, et al. The majority of total nuclear-encoded non-ribosomal RNA in a human cell is "dark matter" un-annotated RNA. BMC Biol 2010;8:149.
6. Mercer TR, Dinger ME, Mattick JS. Long non-coding RNAs: insights into functions. Nat Rev Genet 2009; 10:155-159.
7. Birney E, Stamatoyannopoulos JA, Dutta A, et al. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 2007;447:799-816.
8. Carninci P, Kasukawa T, Katayama S, et al. The transcriptional landscape of the mammalian genome. Science 2005;309:1559-1563.
9. Gutschner T, Diederichs S. The hallmarks of cancer: a long non-coding RNA point of view. RNA Biol 2012; 9:703-719.
10. Talmadge JE, Fidler IJ. AACR centennial series: the biology of cancer metastasis: historical perspective. Cancer Res 2010;70:5649-5669.
11. Eccles SA, Welch DR. Metastasis: recent discoveries and novel treatment strategies. Lancet 2007;369: 742-757.
12. Liu Q, Liu L, Zhao Y, et al. Hypoxia induces genomic DNA demethylation through the activation of HIF-1a and transcriptional upregulation of MAT2A in hepatoma cells. Mol Cancer Ther 2011;10:1113-1123.
13. Ohm JE, McGarvey KM, Yu X, et al. A stem cell-like chromatin pattern may predispose tumor suppressor genes to DNA hypermethylation and heritable silencing. Nat Genet 2007;39:237-242.
14. Sparmann A, van Lohuizen M. Polycomb silencers control cell fate, development and cancer. Nat Rev Cancer 2006;6:846-856.
15. Rinn JL, Kertesz M, Wang JK, et al. Functional demarcation of active and silent chromatin domains in human HOX loci by non-coding RNAs. Cell 2007;129:1311-1323.
16. Khalil AM, Guttman M, Huarte M, et al. Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression. Proc Natl Acad Sci USA 2009;106: 11667-11672.
17. Zhao J, Sun BK, Erwin JA, et al. Polycomb proteins targeted by a short repeat RNA to the mouse X-chromosome. Science 2008;322:750-756.
18. Kogo R, Shimamura T, Mimori K, et al. Long noncoding RNA HOTAIR regulates polycomb-dependent chromatin modification and is associated with poor prognosis in colorectal cancers. Cancer Res 2011;71:6320-6326.
19. Gupta RA, Shah N, Wang KC, et al. Long noncoding RNA HOTAIR reprograms chromatin state to promote cancer metastasis. Nature 2010;464:1071-1076.
20. Chisholm KM, Wan Y, Li R, et al. Detection of long non-coding RNA in archival tissue: correlation with polycomb protein expression in primary and metastatic breast carcinoma. PLoS One 2012;7:e47998.
21. Wan Y, Chang HY. HOTAIR: flight of noncoding RNAs in cancer metastasis. Cell Cycle 2010;9:3391-3392.
22. Kleer CG, Cao Q, Varambally S, et al. EZH2 is a marker of aggressive breast cancer and promotes neoplastic transformation of breast epithelial cells. Proc Natl Acad Sci USA 2003;100:11606-11611.
23. Shi X, Sun M, Liu H, et al. Long non-coding RNAs: a new frontier in the study of human diseases. Cancer Lett. 2013;339:159-166.
24. Prensner JR, Iyer MK, Balbin OA, et al. Transcriptome sequencing across a prostate cancer cohort identifies PCAT-1, an unannotated lincRNA implicated in disease progression. Nat Biotechnol 2011;29:742-749.
25. Ge XS, Chen YB, Liao XY, et al. Overexpression of long noncoding RNA PCAT-1 is a novel biomarker of poor prognosis in patients with colorectal cancer. Med Oncol 2013;30:588.
26. Prensner JR, Rubin MA, Wei JT, et al. Beyond PSA: the next generation of prostate cancer biomarkers. Sci Transl Med 2012;4127rv3.
27. Ji P, Diederichs S, Wang W, et al. MALAT-1, a novel noncoding RNA, and thymosin beta4 predict metastasis and survival in early-stage non-small cell lung cancer. Oncogene 2003;22:8031-8041.
28. Xie L, Hu Z, Wang X, et al. Expression of long noncoding RNA MALAT1 gene in human nasopharyngeal carcinoma cell lines and its biological significance. Nan Fang Yi Ke Da Xue Xue Bao 2013;33: 692-697.
29. Guffanti A, Iacono M, Pelucchi P, et al. A transcriptional sketch of a primary human breast cancer by 454 deep sequencing. BMC Genomics 2009;10:163.
30. Lin R, Maeda S, Liu C, et al. A large noncoding RNA is a marker for murine hepatocellular carcinomas and a spectrum of human carcinomas. Oncogene 2007;26:851-858.
31. Tripathi V, Ellis JD, Shen Z, et al. The nuclearretained noncoding RNA MALAT1 regulates alternative splicing by modulating SR splicing factor phosphorylation. Mol Cell 2010;39:925-938.
32. Yang L, Lin C, Liu W, et al. NcRNA-and Pc2 methylation-dependent gene relocation between nuclear structures mediates gene activation programs. Cell 2011;147:773-788.
33. Schmidt LH, Spieker T, Koschmieder S, et al. The long noncoding MALAT-1 RNA indicates a poor prognosis in non-small cell lung cancer and induces migration and tumor growth. J Thorac Oncol 2011;6: 1984-1992.
34. Gutschner T, Hämmerle M, Eissmann M, et al. The noncoding RNA MALAT1 is a critical regulator of the metastasis phenotype of lung cancer cells. Cancer Res 2013;73:1180-1189.
35. Hellerbrand C, Amann T, Schlegel J, et al. The novel gene MIA2 acts as a tumour suppressor in hepatocellular carcinoma. Gut 2008;57:243-251.
36. Xu Y, Li WL, Fu L, et al. Slit2/Robo1 signaling in glioma migration and invasion. Neurosci Bull 2010; 26:474-478.
37. Sekine Y, Demosky SJ, Stonik JA, et al. High-density lipoprotein induces proliferation and migration of human prostate androgen-independent cancer cells by an ABCA1-dependent mechanism. Mol Cancer Res 2010;8:1284-1294.
38. Jeremy SL, Deborah KM. Complexity in the signaling network: insights from the use of targeted inhibitors in cancer therapy. Genes Dev 2012;26:641-650.
39. Vogelstein B, Kinzler KW. Cancer genes and the pathways they control. Nat Med 2004;10:789-799.
40. Huarte M, Guttman M, Feldser D, et al. A large intergenic noncoding RNA induced by p53 mediates global gene repression in the p53 response. Cell 2010;142:409-419.
41. Antonella B, Andrea M. Long non-coding RNAs and p53 regulation. Int J Mol Sci 2012;13:16708-16717.
42. Yang F, Huo XS, Yuan SX, et al. Repression of the long noncoding RNA-LET by histone deacetylase 3 contributes to hypoxia-mediated metastasis. Mol Cell 2013;49:1083-1096.
43. Cayre A, Rossignol F, Clottes E, et al. aHIF but not HIF-1 alpha transcript is a poor prognostic marker in human breast cancer. Breast Cancer Res 2003;5: R223-R230.
44. Kuwano Y, Pullmann R Jr., Marasa BS, et al. NF90 selectively represses the translation of target mRNAs bearing an AU-rich signature motif. Nucleic Acids Res 2010;38:225-238.
45. Jackson AL, Zhou B, Kim WY. HIF, hypoxia and the role of angiogenesis in non-small cell lung cancer. Expert Opin Ther Targets 2010;14:1047-1057.
46. Chua HL, Bhat-Nakshatri P, Clare SE, et al. NF-kappaB represses E-cadherin expression and enhances epithelial to mesenchymal transition of mammary epithelial cells: potential involvement of ZEB-1 and ZEB-2. Oncogene 2007;26:711-724.
47. Jiang YG, Luo Y, He DL, et al. Role of Wnt/betacatenin signaling pathway in epithelial-mesenchymal transition of human prostate cancer induced by hypoxia-inducible factor-1alpha. Int J Urol 2007;14: 1034-1039.
48. Li Y, Hively WP, Varmus HE. Use of MMTV-Wnt-1 transgenic mice for studying the genetic basis of breast cancer. Oncogene 2000;19:1002-1009.
49. Ying L, Chen Q, Wang Y, et al. Upregulated MALAT-1 contributes to bladder cancer cell migration by inducing epithelial-to-mesenchymal transition. Mol Biosyst 2012;82289-82294.
50. Ayesh S, Matouk I, Schneider T, et al. Possible physiological role of H19 RNA. Mol Carcinog 2002; 35:63-74.
51. Adriaenssens E, Lottin S, Berteaux N, et al. Cross talk between mesenchyme and epithelium increases H19 gene expression during scattering and morphogenesis of epithelial cells. Exp Cell Res 2002;275: 215-229.
52. Fellig Y, Ariel I, Ohana P, et al. H19 expression in hepatic metastases from a range of human carcinomas. J Clin Pathol. 2005;58:1064-1068.
53. Luo M, Li Z, Wang W, et al. Long non-coding RNA H19 increases bladder cancer metastasis by associating with EZH2 and inhibiting E-cadherin expression. Cancer Lett 2013;333:213-221.
54. Ling H, Spizzo R, Atlasi Y, et al. CCAT2, a novel noncoding RNA mapping to 8q24, underlies metastatic progression and chromosomal instability in colon cancer. Genome Res 2013;23:1446-1461.
55. Mulholland DJ, Kobayashi N, Ruscetti M, et al. Ptenloss and RAS/MAPK activation cooperate to promote EMT and metastasis initiated from prostate cancer stem/progenitor cells. Cancer Res 2012;72: 1878-1889.
56. Caldas C, Kern SE. K-ras mutation and pancreatic adenocarcinoma. Int J Pancreatol 1995;18:1-6.
57. Kanda M, Matthaei H, Wu J, et al. Presence of somatic mutations in most early-stage pancreatic intraepithelial neoplasia. Gastroenterology 2012;142: 730-733.
58. Schubbert S, Shannon K, Bollag G. Hyperactive Ras in developmental disorders and cancer. Nat Rev Cancer 2007;7:295-308.
59. Calhoun ES, Jones JB, Ashfaq R, et al. BRAF and FBXW7 (CDC4, FBW7, AGO, SEL10) mutations in distinct subsets of pancreatic cancer: potential therapeutic targets. Am J Pathol 2003;163:1255-1260.
60. Macgregor-Das AM, Iacobuzio-Donahue CA. Molecular pathways in pancreatic carcinogenesis. J Surg Oncol 2013;107:8-14.
61. Nakaya HI, Amaral PP, Louro R, et al. Genome mapping and expression analyses of human intronic noncoding RNAs reveal tissue-specific patterns and enrichment in genes related to regulation of transcription. Genome Biol 2007;8:R43.
62. Reis EM, Ojopi EP, Alberto FL, et al. Large-scale transcriptome analyses reveal new genetic marker candidates of head, neck, and thyroid cancer. Cancer Res 2005;65:1693-1699.
63. Brito GC, Fachel AA, Vettore AL, et al. Identification of protein-coding and intronic noncoding RNAs down-regulated in clear cell renal carcinoma. Mol Carcinog 2008;47:757-767.
64. Tahira AC, Kubrusly MS, Faria MF, et al. Long noncoding intronic RNAs are differentially expressed in primary and metastatic pancreatic cancer. Mol Cancer 2011;10:141.
65. Zhao Y, Shen S, Guo J, et al. Mitogen-activated protein kinases and chemoresistance in pancreatic cancer cells. J Surg Res 2006;136:325-335.
66. Wu X, Weng L, Li X, et al. Identification of a 4-microRNA Signature for clear cell renal cell carcinoma metastasis and prognosis. PLoS One 2012;7: e35661.
67. Weinberg RA. Leaving home early: reexamination of the canonical models of tumor progression. Cancer Cell 2008;14:283-284.
68. Caroline C, Murray GI. Current and emerging concepts in tumour metastasis. J Pathol 2010;222:1-15.
69. Qi P, Xu MD, Ni SJ, et al. Low expression of LOC285194 is associated with poor prognosis in colorectal cancer. J Transl Med 2013;11:122.
70. Chen FJ, Sun M, Li SQ, et al. Upregulation of the long non-coding RNA HOTAIR promotes esophageal squamous cell carcinoma metastasis and poor prognosis. Mol Carcinog. 2013;52:908-915.
71. Nie Y, Liu X, Qu S, et al. Long non-coding RNA HOTAIR is an independent prognostic marker for nasopharyngeal carcinoma progression and survival. Cancer Sci 2013;104:458-464.
72. Endo H, Shiroki T, Nakagawa T, et al. Enhanced expression of long non-coding RNA HOTAIR is associated with the development of gastric cancer. PLoS One 2013;8:e77070.
73. Tang L, Zhang W, Su B, et al. Long non-coding RNA HOTAIR is associated with motility, invasion, and metastatic potential of metastatic melanoma. Biomed Res Int 2013;2013:251098.
74. Wheeler TM, Leger AJ, Pandey SK, et al. Targeting nuclear RNA for in vivo correction of myotonic dystrophy. Nature 2012;488111-488115.
75. Ren S, Liu Y, Xu W, et al. Long noncoding RNA MALAT-1 is a new potential therapeutic target for castration resistant prostate cancer. J Urol 2013;190: 2278-2287.
76. Xu C, Yang M, Tian J, et al. MALAT-1: a long noncoding RNA and its important 3' end functional motif in colorectal cancer metastasis. Int J Oncol 2011;39: 169-175.
77. Park SM, Park SJ, Kim HJ, et al. A known expressed sequence tag, BM742401, is a potent lincRNA inhibiting cancer metastasis. Exp Mol Med 2013; 45:e31.
78. Qi P, Xu MD, Ni SJ, et al. Down-regulation of ncRAN, a long non-coding RNA, contributes to colorectal cancer cell migration and invasion and predicts poor overall survival for colorectal cancer patients. Mol Carcinog 2014 (e-pub ahead of print).
79. Bonnomet A, Brysse A, Tachsidis A, et al. Epithelialto-mesenchymal transitions and circulating tumor cells. J Mammary Gland Biol Neoplasia 2010;15: 261-273.
80. Xu ZY, Yu QM, Du YA, et al. Knockdown of long non-coding RNA HOTAIR suppresses tumor invasion and reverses epithelial-mesenchymal transition in gastric cancer. Int J Biol Sci 2013;9:587-597.
81. Kotake Y, Nakagawa T, Kitagawa K, et al. Long noncoding RNA ANRIL is required for the PRC2 recruitment to and silencing of p15(INK4B) tumor suppressor gene. Oncogene 2011;30:1956-1962.
82. Yap KL, Li S, Muñ oz-Cabello AM, et al. Molecular interplay of the noncoding RNA ANRIL and methylated histone H3 lysine 27 by polycomb CBX7 in transcriptional silencing of INK4a. Mol Cell 2010;38: 662-674.
83. Nguyen VT, Kiss T, Michels AA, et al. 7SK small nuclear RNA binds to and inhibits the activity of CDK9/cyclin T complexes. Nature 2001;414: 322-325.
84. Eilebrecht S, Brysbaert G, Wegert T, et al. 7SK small nuclear RNA directly affects HMGA1 function in transcription regulation. Nucleic Acids Res 2011;39: 2057-2072.
85. Mourtada-Maarabouni M, Pickard MR, Hedge VL, et al. GAS5, a non-protein-coding RNA, controls apoptosis and is downregulated in breast cancer. Oncogene 2009;28:195-208.
86. Azzalin CM, Reichenbach P, Khoriauli L, et al. Telomeric repeat containing RNA and RNA surveillance factors at mammalian chromosome ends. Science 2007;318:798-801.
87. Ng LJ, Cropley JE, Pickett HA, et al. Telomerase activity is associated with an increase in DNA methylation at the proximal subtelomere and a reduction in telomeric transcription. Nucleic Acids Res 2009;37:1152-1159.
88. Uchida T, Rossignol F, Matthay MA, et al. Prolonged hypoxia differentially regulates hypoxia-inducible factor (HIF)-1alpha and HIF-2alpha expression in lung epithelial cells: implication of natural antisense HIF-1alpha. J Biol Chem 2004;279:14871-14878.
89. Madamanchi NR, Hu ZY, Li F, et al. A noncoding RNA regulates human protease-activated receptor-1 gene during embryogenesis. Biochim Biophys Acta 2002;1576:237-245.
90. Fu X, Ravindranath L, Tran N, et al. Regulation of apoptosis by a prostate-specific and prostate cancerassociated noncoding gene, PCGEM1. DNA Cell Biol 2006;25:135-141.
91. Petrovics G, Zhang W, Makarem M, et al. Elevated expression of PCGEM1, a prostate-specific gene with cell growth-promoting function, is associated with high-risk prostate cancer patients. Oncogene 2004;23:605-611.
92. Tsang WP, Wong TW, Cheung AH, et al. Induction of drug resistance and transformation in human cancer cells by the noncoding RNA CUDR. RNA 2007;13: 890-898.
93. Qiu M, Xu Y, Yang X, et al. CCAT2 is a lung adenocarcinoma-specific long non-coding RNA and promotes invasion of non-small cell lung cancer. Tumour Biol 2014 (e-pub ahead of print).
94. Han L, Kong R, Yin DD, et al. Low expression of long noncoding RNA GAS6-AS1 predicts a poor prognosis in patients with NSCLC. Med Oncol 2013;30:694.
95. Zhao Y, Guo Q, Chen J, et al. Role of long non-coding RNA HULC in cell proliferation, apoptosis and tumor metastasis of gastric cancer: a clinical and in vitro investigation. Oncol Rep 2014;31:358-364.
96. Sun W, Wu Y, Yu X, et al. Decreased expression of long noncoding RNA AC096655.1-002 in gastric cancer and its clinical significance. Tumour Biol. 2013;34:2697-2701.
97. Matouk IJ, Abbasi I, Hochberg A, et al. Highly upregulated in liver cancer noncoding RNA is overexpressed in hepatic colorectal metastasis. Eur J Gastroenterol Hepatol 2009;21:688-692.
98. Huang JF, Guo YJ, Zhao CX, et al. Hepatitis B virus X protein (HBx)-related long noncoding RNA (lncRNA) downregulated expression by HBx (Dreh) inhibits hepatocellular carcinoma metastasis by targeting the intermediate filament protein vimentin. Hepatology 2013;57:1882-1892.
99. Wang CM, Wu QQ, Li SQ, et al. Upregulation of the long non-coding RNA PlncRNA-1 promotes esophageal squamous carcinoma cell proliferation and correlates with advanced clinical stage. Dig Dis Sci. 2014;59:591-597.
100. He W, Cai Q, Sun F, et al. linc-UBC1 physically associates with polycomb repressive complex 2 (PRC2) and acts as a negative prognostic factor for lymph node metastasis and survival in bladder cancer. Biochim Biophys Acta 2013;1832:1528-1537.