Involvement of miRNA-29a in epigenetic regulation of transforming growth factor-β-induced epithelial-mesenchymal transition in hepatocellular carcinoma

Hepatology Research

Volumn 44, Issue 8, 2014, Pages 907-919

  Kogure, Takayuki ^a   Kondo, Yasuteru ^a   Kakazu, Eiji ^a   Ninomiya, Masashi ^a   Kimura, Osamu ^a   Shimosegawa, Tooru ^a  

^a TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

E cadherin; Epithelial mesenchymal transition; Hepatocellular carcinoma; miR 29a

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; DNA; DNA METHYLTRANSFERASE 1; DNA METHYLTRANSFERASE 3B; MICRORNA 29A; TRANSFORMING GROWTH FACTOR BETA; UVOMORULIN;

ARTICLE; CELL TRANSFORMATION; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; ELECTROPORATION; EPIGENETICS; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION; HEPATOCELLULAR CARCINOMA CELL LINE; HEPG2 CELL LINE; HUMAN; HUMAN CELL; LIVER CARCINOGENESIS; LIVER CELL CARCINOMA; PRIORITY JOURNAL; PROMOTER REGION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

EID: 84904747598     PISSN: 13866346     EISSN: 1872034X     Source Type: Journal    
DOI: 10.1111/hepr.12188     Document Type: Article

References (49)

1. Parkin DM, Bray F, Ferlay J, Pisani P. Estimating the world cancer burden: Globocan 2000. Int J Cancer 2001; 94: 153-156.
2. Lo CM, Ngan H, Tso WK etal. Randomized controlled trial of transarterial lipiodol chemoembolization for unresectable hepatocellular carcinoma. Hepatology 2002; 35: 1164-1171.
3. N'Kontchou G, Mahamoudi A, Aout M etal. Radiofrequency ablation of hepatocellular carcinoma: long-term results and prognostic factors in 235 Western patients with cirrhosis. Hepatology 2009; 50: 1475-1483.
4. Gao D, Vahdat LT, Wong S, Chang JC, Mittal V. Microenvironmental regulation of epithelial-mesenchymal transitions in cancer. Cancer Res 2012; 72: 4883-4889.
5. Giannelli G, Bergamini C, Fransvea E, Sgarra C, Antonaci S. Laminin-5 with transforming growth factor-beta1 induces epithelial to mesenchymal transition in hepatocellular carcinoma. Gastroenterology 2005; 129: 1375-1383.
6. Lee TK, Poon RT, Yuen AP etal. Twist overexpression correlates with hepatocellular carcinoma metastasis through induction of epithelial-mesenchymal transition. Clin Cancer Res 2006; 12: 5369-5376.
7. Xu Z, Shen MX, Ma DZ, Wang LY, Zha XL. TGF-beta1-promoted epithelial-to-mesenchymal transformation and cell adhesion contribute to TGF-beta1-enhanced cell migration in SMMC-7721 cells. Cell Res 2003; 13: 343-350.
8. Yoshiura K, Kanai Y, Ochiai A, Shimoyama Y, Sugimura T, Hirohashi S. Silencing of the E-cadherin invasion-suppressor gene by CpG methylation in human carcinomas. Proc Natl Acad Sci U S A 1995; 92: 7416-7419.
9. Kanai Y. Genome-wide DNA methylation profiles in precancerous conditions and cancers. Cancer Sci 2010; 101: 36-45.
10. Yang B, Guo M, Herman JG, Clark DP. Aberrant promoter methylation profiles of tumor suppressor genes in hepatocellular carcinoma. Am J Pathol 2003; 163: 1101-1107.
11. Oh BK, Kim H, Park HJ etal. DNA methyltransferase expression and DNA methylation in human hepatocellular carcinoma and their clinicopathological correlation. Int J Mol Med 2007; 20: 65-73.
12. Saito Y, Kanai Y, Nakagawa T etal. Increased protein expression of DNA methyltransferase (DNMT) 1 is significantly correlated with the malignant potential and poor prognosis of human hepatocellular carcinomas. Int J Cancer 2003; 105: 527-532.
13. Saito Y, Kanai Y, Sakamoto M, Saito H, Ishii H, Hirohashi S. Overexpression of a splice variant of DNA methyltransferase 3b, DNMT3b4, associated with DNA hypomethylation on pericentromeric satellite regions during human hepatocarcinogenesis. Proc Natl Acad Sci U S A 2002; 99: 10060-10065.
14. Fabbri M, Garzon R, Cimmino A etal. MicroRNA-29 family reverts aberrant methylation in lung cancer by targeting DNA methyltransferases 3A and 3B. Proc Natl Acad Sci U S A 2007; 104: 15805-15810.
15. Meunier L, Siddeek B, Vega A etal. Perinatal programming of adult rat germ cell death after exposure to xenoestrogens: role of microRNA miR-29 family in the down-regulation of DNA methyltransferases and Mcl-1. Endocrinology 2012; 153: 1936-1947.
16. Su H, Yang JR, Xu T etal. MicroRNA-101, down-regulated in hepatocellular carcinoma, promotes apoptosis and suppresses tumorigenicity. Cancer Res 2009; 69: 1135-1142.
17. Xiong Y, Fang JH, Yun JP etal. Effects of microRNA-29 on apoptosis, tumorigenicity, and prognosis of hepatocellular carcinoma. Hepatology 2009; 51: 836-845.
18. Braconi C, Kogure T, Valeri N etal. microRNA-29 can regulate expression of the long non-coding RNA gene MEG3 in hepatocellular cancer. Oncogene 2011; 30: 4750-4756.
19. Lim SO, Gu JM, Kim MS etal. Epigenetic changes induced by reactive oxygen species in hepatocellular carcinoma: methylation of the E-cadherin promoter. Gastroenterology 2008; 135: 2128-2140, 40 e1-8.
20. Fujii S, Ochiai A. Enhancer of zeste homolog 2 downregulates E-cadherin by mediating histone H3 methylation in gastric cancer cells. Cancer Sci 2008; 99: 738-746.
21. Cao Q, Yu J, Dhanasekaran SM etal. Repression of E-cadherin by the polycomb group protein EZH2 in cancer. Oncogene 2008; 27: 7274-7284.
22. French SW. Molecular events in hepatic preneoplasia: a review. Exp Mol Pathol 2010; 88: 219-224.
23. Fabregat I, Roncero C, Fernandez M. Survival and apoptosis: a dysregulated balance in liver cancer. Liver Int 2007; 27: 155-162.
24. Park SS, Eom YW, Kim EH etal. Involvement of c-Src kinase in the regulation of TGF-beta1-induced apoptosis. Oncogene 2004; 23: 6272-6281.
25. Fransvea E, Angelotti U, Antonaci S, Giannelli G. Blocking transforming growth factor-beta up-regulates E-cadherin and reduces migration and invasion of hepatocellular carcinoma cells. Hepatology 2008; 47: 1557-1566.
26. Yang MH, Chen CL, Chau GY etal. Comprehensive analysis of the independent effect of twist and snail in promoting metastasis of hepatocellular carcinoma. Hepatology 2009; 50: 1464-1474.
27. Siegel PM, Massague J. Cytostatic and apoptotic actions of TGF-beta in homeostasis and cancer. Nat Rev Cancer 2003; 3: 807-821.
28. Zavadil J, Bottinger EP. TGF-beta and epithelial-to-mesenchymal transitions. Oncogene 2005; 24: 5764-5774.
29. Shirai Y, Kawata S, Tamura S etal. Plasma transforming growth factor-beta 1 in patients with hepatocellular carcinoma. Comparison with chronic liver diseases. Cancer 1994; 73: 2275-2279.
30. Shirai Y, Kawata S, Ito N etal. Elevated levels of plasma transforming growth factor-beta in patients with hepatocellular carcinoma. Jpn J Cancer Res 1992; 83: 676-679.
31. Ikeguchi M, Iwamoto A, Taniguchi K, Katano K, Hirooka Y. The gene expression level of transforming growth factor-beta (TGF-beta) as a biological prognostic marker of hepatocellular carcinoma. J Exp Clin Cancer Res 2005; 24: 415-421.
32. Cano A, Perez-Moreno MA, Rodrigo I etal. The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat Cell Biol 2000; 2: 76-83.
33. Onder TT, Gupta PB, Mani SA, Yang J, Lander ES, Weinberg RA. Loss of E-cadherin promotes metastasis via multiple downstream transcriptional pathways. Cancer Res 2008; 68: 3645-3654.
34. Comijn J, Berx G, Vermassen P etal. The two-handed E box binding zinc finger protein SIP1 downregulates E-cadherin and induces invasion. Mol Cell 2001; 7: 1267-1278.
35. Batlle E, Sancho E, Franci C etal. The transcription factor snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nat Cell Biol 2000; 2: 84-89.
36. Bolos V, Peinado H, Perez-Moreno MA, Fraga MF, Esteller M, Cano A. The transcription factor Slug represses E-cadherin expression and induces epithelial to mesenchymal transitions: a comparison with Snail and E47 repressors. J Cell Sci 2003; 116: 499-511.
37. Baylin SB. DNA methylation and gene silencing in cancer. Nat Clin Pract Oncol 2005; 2 (Suppl 1): S4-11.
38. Clark SJ, Melki J. DNA methylation and gene silencing in cancer: which is the guilty party? Oncogene 2002; 21: 5380-5387.
39. Zhang Q, Chen L, Helfand BT etal. TGF-beta regulates DNA methyltransferase expression in prostate cancer, correlates with aggressive capabilities, and predicts disease recurrence. PLoS ONE 2011; 6: e25168.
40. Lee C, Zhang Q, Zi X etal. TGF-β mediated DNA methylation in prostate cancer. Transl Androl Urol 2012; 1: 78-88.
41. Garzon R, Liu S, Fabbri M etal. MicroRNA-29b induces global DNA hypomethylation and tumor suppressor gene reexpression in acute myeloid leukemia by targeting directly DNMT3A and 3B and indirectly DNMT1. Blood 2009; 113: 6411-6418.
42. Kwiecinski M, Noetel A, Elfimova N etal. Hepatocyte growth factor (HGF) inhibits collagen I and IV synthesis in hepatic stellate cells by miRNA-29 induction. PLoS ONE 2011; 6: e24568.
43. Wang B, Komers R, Carew R etal. Suppression of microRNA-29 expression by TGF-beta1 promotes collagen expression and renal fibrosis. J Am Soc Nephrol 2012; 23: 252-265.
44. Xiong Y, Fang JH, Yun JP etal. Effects of microRNA-29 on apoptosis, tumorigenicity, and prognosis of hepatocellular carcinoma. Hepatology 2010; 51: 836-845.
45. Cummins JM, He Y, Leary RJ etal. The colorectal microRNAome. Proc Natl Acad Sci U S A 2006; 103: 3687-3692.
46. Calin GA, Ferracin M, Cimmino A etal. A MicroRNA signature associated with prognosis and progression in chronic lymphocytic leukemia. N Engl J Med 2005; 353: 1793-1801.
47. Pekarsky Y, Croce CM. Is miR-29 an oncogene or tumor suppressor in CLL? Oncotarget 2010; 1: 224-227.
48. Garzon R, Calin GA, Croce CM. MicroRNAs in cancer. Annu Rev Med 2009; 60: 167-179.
49. Eades G, Yao Y, Yang M, Zhang Y, Chumsri S, Zhou Q. miR-200a regulates SIRT1 expression and epithelial to mesenchymal transition (EMT)-like transformation in mammary epithelial cells. J Biol Chem 2011; 286: 25992-26002.