The LncRNA H19 promotes epithelial to mesenchymal transition by functioning as MiRNA sponges in colorectal cancer

Oncotarget

Volumn 6, Issue 26, 2015, Pages 22513-22525

  Liang, Wei Cheng ^a   Fu, Wei Ming ^b   Wong, Cheuk Wa ^a   Wang, Yan ^a   Wang, Wei Mao ^a   Hu, Guo Xin ^c   Zhang, Li ^a   Xiao, Li Jia ^d   Wan, David Chi Cheong ^a   Zhang, Jin Fang ^a,e   Waye, Mary Miu Yee ^a  

^a CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^b INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^c PEKING UNIVERSITY SHENZHEN HOSPITAL   (China)

^d GUANGDONG MEDICAL UNIVERSITY   (China)

^e CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

CeRNA; LncRNA; miRNA sponges

Indexed keywords

LONG UNTRANSLATED RNA; LONG UNTRANSLATED RNA H19; MICRORNA; MICRORNA 138; MICRORNA 200A; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ZEB1; TRANSCRIPTION FACTOR ZEB2; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG; VIMENTIN; H19 LONG NON-CODING RNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CARCINOGENESIS; CELL CULTURE; CELL MIGRATION; COLON; COLORECTAL CANCER; CONTROLLED STUDY; DISEASE ASSOCIATION; EPITHELIAL MESENCHYMAL TRANSITION; GENE REPRESSION; HT 29 CELL LINE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOPRECIPITATION; IN VITRO STUDY; IN VIVO STUDY; LUCIFERASE ASSAY; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN INTERACTION; TUMOR XENOGRAFT; UPREGULATION; ANIMAL; COLORECTAL TUMOR; GENETICS; HCT 116 CELL LINE; HEK293 CELL LINE; HT-29 CELL LINE; METABOLISM; NUDE MOUSE; PATHOLOGY; XENOGRAFT;

ANIMALS; COLORECTAL NEOPLASMS; EPITHELIAL-MESENCHYMAL TRANSITION; HCT116 CELLS; HEK293 CELLS; HETEROGRAFTS; HT29 CELLS; HUMANS; MICE; MICE, NUDE; MICRORNAS; RNA, LONG NONCODING; UP-REGULATION;

EID: 84941242709     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.4154     Document Type: Article

References (50)

1. Parkin DM, Bray F, Ferlay J, Pisani P. Global cancer statistics, 2002. CA: a cancer journal for clinicians. 2005; 55:74-108.
2. Bates RC, Mercurio AM. The epithelial-mesenchymal transition (EMT) and colorectal cancer progression. Cancer biology & therapy. 2005; 4:365-370.
3. Thiery JP, Sleeman JP. Complex networks orchestrate epithelial-mesenchymal transitions. Nature reviews Molecular cell biology. 2006; 7:131-142.
4. Yang J, Weinberg RA. Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Developmental cell. 2008; 14:818-829.
5. Brabletz T, Jung A, Spaderna S, Hlubek F, Kirchner T. Opinion: migrating cancer stem cells-an integrated concept of malignant tumour progression. Nature reviews Cancer. 2005; 5:744-749.
6. Peinado H, Olmeda D, Cano A. Snail, Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype?. Nature reviews Cancer. 2007; 7:415-428.
7. Thiery JP, Acloque H, Huang RY, Nieto MA. Epithelial-mesenchymal transitions in development and disease. Cell. 2009; 139:871-890.
8. Yap AS. The morphogenetic role of cadherin cell adhesion molecules in human cancer: a thematic review. Cancer investigation. 1998; 16:252-261.
9. Thoreson MA, Reynolds AB. Altered expression of the catenin p120 in human cancer: implications for tumor progression. Differentiation; research in biological diversity. 2002; 70:583-589.
10. Mendez MG, Kojima S, Goldman RD. Vimentin induces changes in cell shape, motility, and adhesion during the epithelial to mesenchymal transition. FASEB journal: official publication of the Federation of American Societies for Experimental Biology. 2010; 24:1838-1851.
11. Keniry A, Oxley D, Monnier P, Kyba M, Dandolo L, Smits G, Reik W. The H19 lincRNA is a developmental reservoir of miR-675 that suppresses growth and Igf1r. Nature cell biology. 2012; 14:659-665.
12. Cui H, Onyango P, Brandenburg S, Wu Y, Hsieh CL, Feinberg AP. Loss of imprinting in colorectal cancer linked to hypomethylation of H19 and IGF2. Cancer research. 2002; 62:6442-6446.
13. Tsang WP, Ng EK, Ng SS, Jin H, Yu J, Sung JJ, Kwok TT. Oncofetal H19-derived miR-675 regulates tumor suppressor RB in human colorectal cancer. Carcinogenesis. 2010; 31:350-358.
14. Hibi K, Nakamura H, Hirai A, Fujikake Y, Kasai Y, Akiyama S, Ito K, Takagi H. Loss of H19 imprinting in esophageal cancer. Cancer research. 1996; 56:480-482.
15. Byun HM, Wong HL, Birnstein EA, Wolff EM, Liang G, Yang AS. Examination of IGF2 and H19 loss of imprinting in bladder cancer. Cancer research. 2007; 67:10753-10758.
16. Luo M, Li Z, Wang W, Zeng Y, Liu Z, Qiu J. Long non-coding RNA H19 increases bladder cancer metastasis by associating with EZH2 and inhibiting E-cadherin expression. Cancer letters. 2013; 333:213-221.
17. Berteaux N, Lottin S, Monte D, Pinte S, Quatannens B, Coll J, Hondermarck H, Curgy JJ, Dugimont T, Adriaenssens E. H19 mRNA-like noncoding RNA promotes breast cancer cell proliferation through positive control by E2F1. The Journal of biological chemistry. 2005; 280:29625-29636.
18. Lottin S, Adriaenssens E, Dupressoir T, Berteaux N, Montpellier C, Coll J, Dugimont T, Curgy JJ. Overexpression of an ectopic H19 gene enhances the tumorigenic properties of breast cancer cells. Carcinogenesis. 2002; 23:1885-1895.
19. Matouk IJ, DeGroot N, Mezan S, Ayesh S, Abu-lail R, Hochberg A, Galun E. The H19 non-coding RNA is essential for human tumor growth. PloS one. 2007; 2:e845.
20. Ariel I, Miao HQ, Ji XR, Schneider T, Roll D, de Groot N, Hochberg A, Ayesh S. Imprinted H19 oncofetal RNA is a candidate tumour marker for hepatocellular carcinoma. Molecular pathology: MP. 1998; 51:21-25.
21. Petrocca F, Lieberman J. Micromanipulating cancer: microRNA-based therapeutics? RNA biology. 2009; 6:335-340.
22. Liang WC, Wang Y, Wan DC, Yeung VS, Waye MM. Characterization of miR-210 in 3T3-L1 adipogenesis. Journal of cellular biochemistry. 2013; 114:2699-2707.
23. Liang WC, Wang Y, Xiao LJ, Wang YB, Fu WM, Wang WM, Jiang HQ, Qi W, Wan DC, Zhang JF, Waye MM. Identification of miRNAs that specifically target tumor suppressive KLF6-FL rather than oncogenic KLF6-SV1 isoform. RNA Biol. 2014;11:845-54.
24. Qi W, Liang W, Jiang H, Miuyee Waye M. The function of miRNA in hepatic cancer stem cell. BioMed research international. 2013; 2013:358902.
25. Ceppi P, Peter ME. MicroRNAs regulate both epithelial-to-mesenchymal transition and cancer stem cells. Oncogene. 2014; 33:269-278.
26. Salmena L, Poliseno L, Tay Y, Kats L, Pandolfi PP. A ceRNA hypothesis: the Rosetta Stone of a hidden RNA language? 1 Cell. 2011; 146:353-358.
27. Poliseno L, Salmena L, Zhang JW, Carver B, Haveman WJ, Pandolfi PP. A coding-independent function of gene and pseudogene mRNAs regulates tumour biology. Nature. 2010; 465:1033-U1090.
28. Jeyapalan Z, Deng Z, Shatseva T, Fang L, He C, Yang BB. Expression of CD44 3'-untranslated region regulates endogenous microRNA functions in tumorigenesis and angiogenesis. Nucleic acids research. 2011; 39:3026-3041.
29. Cesana M, Cacchiarelli D, Legnini I, Santini T, Sthandier O, Chinappi M, Tramontano A, Bozzoni I. A long noncoding RNA controls muscle differentiation by functioning as a competing endogenous RNA. Cell. 2011; 147:358-369.
30. Kumar MS, Armenteros-Monterroso E, East P, Chakravorty P, Matthews N, Winslow MM, Downward J. HMGA2 functions as a competing endogenous RNA to promote lung cancer progression. Nature. 2014; 505:212-217.
31. Hollier BG, Evans K, Mani SA. The epithelial-to-mesenchymal transition and cancer stem cells: a coalition against cancer therapies. Journal of mammary gland biology and neoplasia. 2009; 14:29-43.
32. Ahmed N, Abubaker K, Findlay J, Quinn M. Epithelial mesenchymal transition and cancer stem cell-like phenotypes facilitate chemoresistance in recurrent ovarian cancer. Current cancer drug targets. 2010; 10:268-278.
33. Latifi A, Abubaker K, Castrechini N, Ward AC, Liongue C, Dobill F, Kumar J, Thompson EW, Quinn MA, Findlay JK, Ahmed N. Cisplatin treatment of primary and metastatic epithelial ovarian carcinomas generates residual cells with mesenchymal stem cell-like profile. Journal of cellular biochemistry. 2011; 112:2850-2864.
34. Wang Z, Li Y, Kong D, Banerjee S, Ahmad A, Azmi AS, Ali S, Abbruzzese JL, Gallick GE, Sarkar FH. Acquisition of epithelial-mesenchymal transition phenotype of gemcitabine-resistant pancreatic cancer cells is linked with activation of the notch signaling pathway. Cancer research. 2009; 69:2400-2407.
35. Kajiyama H, Shibata K, Terauchi M, Yamashita M, Ino K, Nawa A, Kikkawa F. Chemoresistance to paclitaxel induces epithelial-mesenchymal transition and enhances metastatic potential for epithelial ovarian carcinoma cells. International journal of oncology. 2007; 31:277-283.
36. Li QQ, Chen ZQ, Cao XX, Xu JD, Xu JW, Chen YY, Wang WJ, Chen Q, Tang F, Liu XP, Xu ZD. Involvement of NF-kappaB/miR-448 regulatory feedback loop in chemotherapy-induced epithelial-mesenchymal transition of breast cancer cells. Cell death and differentiation. 2011; 18:16-25.
37. Selga E, Morales C, Noe V, Peinado MA, Ciudad CJ. Role of caveolin 1, E-cadherin, Enolase 2 and PKCalpha on resistance to methotrexate in human HT29 colon cancer cells. BMC medical genomics. 2008; 1:35.
38. Selga E, Noe V, Ciudad CJ. Transcriptional regulation of aldo-keto reductase 1C1 in HT29 human colon cancer cells resistant to methotrexate: role in the cell cycle and apoptosis. Biochemical pharmacology. 2008; 75:414-426.
39. Huarte M, Rinn JL. Large non-coding RNAs: missing links in cancer? Human molecular genetics. 2010; 19:R152-161.
40. Matouk IJ, Raveh E, Abu-lail R, Mezan S, Gilon M, Gershtain E, Birman T, Gallula J, Schneider T, Barkali M, Richler C, Fellig Y, Sorin V, Hubert A, Hochberg A, Czerniak A. Oncofetal H19 RNA promotes tumor metastasis. Biochimica et biophysica acta. 2014; 1843:1414-1426.
41. Kallen AN, Zhou XB, Xu J, Qiao C, Ma J, Yan L, Lu L, Liu C, Yi JS, Zhang H, Min W, Bennett AM, Gregory RI, Ding Y, Huang Y. The imprinted H19 lncRNA antagonizes let-7 microRNAs. Molecular cell. 2013; 52:101-112.
42. Ma C, Nong K, Zhu H, Wang W, Huang X, Yuan Z, Ai K. H19 promotes pancreatic cancer metastasis by derepressing let-7's suppression on its target HMGA2-mediated EMT. Tumour Biol. 2014;35:9163-9.
43. Park SM, Gaur AB, Lengyel E, Peter ME. The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2. Genes & development. 2008; 22:894-907.
44. Gregory PA, Bert AG, Paterson EL, Barry SC, Tsykin A, Farshid G, Vadas MA, Khew-Goodall Y, Goodall GJ. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nature cell biology. 2008; 10:593-601.
45. Liu X, Wang C, Chen Z, Jin Y, Wang Y, Kolokythas A, Dai Y, Zhou X. MicroRNA-138 suppresses epithelial-mesenchymal transition in squamous cell carcinoma cell lines. The Biochemical journal. 2011; 440:23-31.
46. Rhodes DR, Kalyana-Sundaram S, Mahavisno V, Varambally R, Yu J, Briggs BB, Barrette TR, Anstet MJ, Kincead-Beal C, Kulkarni P, Varambally S, Ghosh D, Chinnaiyan AM. Oncomine 3.0: genes, pathways, and networks in a collection of 18, 000 cancer gene expression profiles. Neoplasia. 2007; 9:166-180.
47. Wilhelm BT, Marguerat S, Watt S, Schubert F, Wood V, Goodhead I, Penkett CJ, Rogers J, Bahler J. Dynamic repertoire of a eukaryotic transcriptome surveyed at single-nucleotide resolution. Nature. 2008; 453:1239-U1239.
48. Chi SW, Zang JB, Mele A, Darnell RB. Argonaute HITS-CLIP decodes microRNA-mRNA interaction maps. Nature. 2009; 460:479-486.
49. Helwak A, Kudla G, Dudnakova T, Tollervey D. Mapping the Human miRNA Interactome by CLASH Reveals Frequent Noncanonical Binding. Cell. 2013; 153:654-665.
50. Geisler S, Coller J. RNA in unexpected places: long non-coding RNA functions in diverse cellular contexts. Nature reviews Molecular cell biology. 2013; 14:699-712.