Hepatitis C virus core protein induces epithelial-mesenchymal transition in human hepatocytes by upregulating E12/E47 levels

Cancer Letters

Volumn 362, Issue 1, 2015, Pages 131-138

  Tiwari, Indira ^a   Yoon, Min Ho ^a   Park, Bum Joon ^a   Jang, Kyung Lib ^a  

^a Pusan National University   (South Korea)

Author keywords

E cadherin; E12 E47; Epithelial mesenchymal transition; Hepatitis C virus core protein; Hepatocellular carcinoma

Indexed keywords

CORE PROTEIN; FIBRONECTIN; PLAKOGLOBIN; PROTEASOME; PROTEIN E12; PROTEIN E47; TRANSCRIPTION FACTOR; UBIQUITIN; UNCLASSIFIED DRUG; UVOMORULIN; CADHERIN; TRANSCRIPTION FACTOR 3;

ARTICLE; CELL MIGRATION; DISEASE ASSOCIATION; E BOX ELEMENT; EPITHELIAL MESENCHYMAL TRANSITION; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; LIVER CELL CARCINOMA; LIVER CELL CULTURE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; UPREGULATION; DOWN REGULATION; GENETICS; HEPACIVIRUS; LIVER CELL; LIVER TUMOR; METABOLISM; PATHOLOGY; VIROLOGY;

HEPATITIS C VIRUS;

CADHERINS; CARCINOMA, HEPATOCELLULAR; DOWN-REGULATION; EPITHELIAL-MESENCHYMAL TRANSITION; HEPACIVIRUS; HEPATOCYTES; HUMANS; LIVER NEOPLASMS; TRANSCRIPTION FACTOR 3; UP-REGULATION; VIRAL CORE PROTEINS;

EID: 84931070961     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2015.03.032     Document Type: Article

References (52)

1. Caselmann W.H., Alt M. Hepatitis C virus infection as a major risk factor for hepatocellular carcinoma. J. Hepatol 1996, 24:61-66.
2. Suzuki T., Aizaki H., Murakami K., Shoji I., Wakita T. Molecular biology of hepatitis C virus. J. Gastroenterol 2007, 42:411-423.
3. Liang T.J., Heller T. Pathogenesis of hepatitis C-associated hepatocellular carcinoma. Gastroenterology 2004, 127:S62-S71.
4. Koike K. Hepatitis C virus contributes to hepatocarcinogenesis by modulating metabolic and intracellular signaling pathways. J. Gastroenterol. Hepatol 2007, 22(Suppl. 1):S108-S111.
5. Ray R.B., Lagging L.M., Meyer K., Ray R. Hepatitis C virus core protein cooperates with ras and transforms primary rat embryo fibroblasts to tumorigenic phenotype. J. Virol 1996, 70:4438-4443.
6. Moriya K., Fujie H., Shintani Y., Yotsuyanagi H., Tsutsumi T., Ishibashi K., et al. The core protein of hepatitis C virus induces hepatocellular carcinoma in transgenic mice. Nat. Med 1998, 4:1065-1067.
7. Takeichi M. Morphogenetic roles of classic cadherins. Curr. Opin. Cell Biol 1995, 7:619-627.
8. van Roy F., Berx G. The cell-cell adhesion molecule E-cadherin. Cell. Mol. Life Sci 2008, 65:3756-3788.
9. Hirohashi S., Kanai Y. Cell adhesion system and human cancer morphogenesis. Cancer Sci 2003, 94:575-581.
10. Yang B., Guo M., Herman J.G., Clark D.P. Aberrant promoter methylation profiles of tumor suppressor genes in hepatocellular carcinoma. Am. J. Pathol 2003, 163:1101-1107.
11. Kanai Y., Ushijima S., Hui A.M., Ochiai A., Tsuda H., Sakamoto M., et al. The E-cadherin gene is silenced by CpG methylation in human hepatocellular carcinomas. Int. J. Cancer 1997, 71:355-359.
12. Watabe M., Nagafuchi A., Tsukita S., Takeichi M. Induction of polarized cell-cell association and retardation of growth by activation of the E-cadherin-catenin adhesion system in a dispersed carcinoma line. J. Cell Biol 1994, 127:247-256.
13. Le Bras G.F., Taubenslag K.J., Andl C.D. The regulation of cell-cell adhesion during epithelial-mesenchymal transition, motility and tumor progression. Cell Adh. Migr 2012, 6:365-373.
14. Wells A., Yates C., Shepard C.R. E-cadherin as an indicator of mesenchymal to epithelial reverting transitions during the metastatic seeding of disseminated carcinomas. Clin. Exp. Metastasis 2008, 25:621-628.
15. Kalluri R., Weinberg R.A. The basics of epithelial-mesenchymal transition. J. Clin. Invest 2009, 119:1420-1428.
16. Bose S.K., Meyer K., Di Bisceglie A.M., Ray R.B., Ray R. Hepatitis C virus induces epithelial-mesenchymal transition in primary human hepatocytes. J. Virol 2012, 86:13621-13628.
17. Akkari L., Gregoire D., Floc'h N., Moreau M., Hernandez C., Simonin Y., et al. Hepatitis C viral protein NS5A induces EMT and participates in oncogenic transformation of primary hepatocyte precursors. J. Hepatol 2012, 57:1021-1028.
18. Conti B., Minutolo A., Arciello M., Balsano C. Are Hedgehog and Wnt/beta-catenin pathways involved in hepatitis C virus-mediated EMT?. J. Hepatol 2013, 58:636-637.
19. Iqbal J., McRae S., Mai T., Banaudha K., Sarkar-Dutta M., Waris G. Role of hepatitis C virus induced osteopontin in epithelial to mesenchymal transition, migration and invasion of hepatocytes. PLoS ONE 2014, 9:e87464.
20. Park J., Jang K.L. Hepatitis C virus represses E-cadherin expression via DNA methylation to induce epithelial to mesenchymal transition in human hepatocytes. Biochem. Biophys. Res. Commun 2014, 446:561-567.
21. Quan H., Zhou F., Nie D., Chen Q., Cai X., Shan X., et al. Hepatitis C virus core protein epigenetically silences SFRP1 and enhances HCC aggressiveness by inducing epithelial-mesenchymal transition. Oncogene 2014, 33:2826-2835.
22. Arora P., Kim E.O., Jung J.K., Jang K.L. Hepatitis C virus core protein downregulates E-cadherin expression via activation of DNA methyltransferase 1 and 3b. Cancer Lett 2008, 261:244-252.
23. Battaglia S., Benzoubir N., Nobilet S., Charneau P., Samuel D., Zignego A.L., et al. Liver cancer-derived hepatitis C virus core proteins shift TGF-beta responses from tumor suppression to epithelial-mesenchymal transition. PLoS ONE 2009, 4:e4355.
24. Murre C., McCaw P.S., Baltimore D. A new DNA binding and dimerization motif in immunoglobulin enhancer binding, daughterless, MyoD, and myc proteins. Cell 1989, 56:777-783.
25. Murre C., McCaw P.S., Vaessin H., Caudy M., Jan L.Y., Jan Y.N., et al. Interactions between heterologous helix-loop-helix proteins generate complexes that bind specifically to a common DNA sequence. Cell 1989, 58:537-544.
26. Shen C.P., Kadesch T. B-cell-specific DNA binding by an E47 homodimer. Mol. Cell. Biol 1995, 15:4518-4524.
27. Quong M.W., Romanow W.J., Murre C. E protein function in lymphocyte development. Annu. Rev. Immunol 2002, 20:301-322.
28. Henthorn P., Kiledjian M., Kadesch T. Two distinct transcription factors that bind the immunoglobulin enhancer microE5/kappa 2 motif. Science 1990, 247:467-470.
29. Perez-Moreno M.A., Locascio A., Rodrigo I., Dhondt G., Portillo F., Nieto M.A., et al. A new role for E12/E47 in the repression of E-cadherin expression and epithelial-mesenchymal transitions. J. Biol. Chem 2001, 276:27424-27431.
30. Murre C., Bain G., van Dijk M.A., Engel I., Furnari B.A., Massari M.E., et al. Structure and function of helix-loop-helix proteins. Biochim. Biophys. Acta 1994, 1218:129-135.
31. von Burstin J., Eser S., Paul M.C., Seidler B., Brandl M., Messer M., et al. E-cadherin regulates metastasis of pancreatic cancer in vivo and is suppressed by a SNAIL/HDAC1/HDAC2 repressor complex. Gastroenterology 2009, 137:361-371. 371 e361-365.
32. Peinado H., Ballestar E., Esteller M., Cano A. Snail mediates E-cadherin repression by the recruitment of the Sin3A/histone deacetylase 1 (HDAC1)/HDAC2 complex. Mol. Cell. Biol 2004, 24:306-319.
33. Teng Y., Li X. The roles of HLH transcription factors in epithelial mesenchymal transition and multiple molecular mechanisms. Clin. Exp. Metastasis 2014, 31:367-377.
34. Tania M., Khan M.A., Fu J. Epithelial to mesenchymal transition inducing transcription factors and metastatic cancer. Tumour Biol 2014, 35:7335-7342.
35. Chang J., Yang S.H., Cho Y.G., Hwang S.B., Hahn Y.S., Sung Y.C. Hepatitis C virus core from two different genotypes has an oncogenic potential but is not sufficient for transforming primary rat embryo fibroblasts in cooperation with the H-ras oncogene. J. Virol 1998, 72:3060-3065.
36. Lee J.O., Kwun H.J., Jung J.K., Choi K.H., Min D.S., Jang K.L. Hepatitis B virus X protein represses E-cadherin expression via activation of DNA methyltransferase 1. Oncogene 2005, 24:6617-6625.
37. Batlle E., Sancho E., Franci C., Dominguez D., Monfar M., Baulida J., et al. The transcription factor snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nat. Cell Biol 2000, 2:84-89.
38. Kato T., Date T., Miyamoto M., Furusaka A., Tokushige K., Mizokami M., et al. Efficient replication of the genotype 2a hepatitis C virus subgenomic replicon. Gastroenterology 2003, 125:1808-1817.
39. Zhong J., Gastaminza P., Cheng G., Kapadia S., Kato T., Burton D.R., et al. Robust hepatitis C virus infection in vitro. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:9294-9299.
40. Takeuchi T., Katsume A., Tanaka T., Abe A., Inoue K., Tsukiyama-Kohara K., et al. Real-time detection system for quantification of hepatitis C virus genome. Gastroenterology 1999, 116:636-642.
41. Lin Y., Wu Y., Li J., Dong C., Ye X., Chi Y.I., et al. The SNAG domain of Snail1 functions as a molecular hook for recruiting lysine-specific demethylase 1. EMBO J. 2010, 29:1803-1816.
42. Kawanishi J., Kato J., Sasaki K., Fujii S., Watanabe N., Niitsu Y. Loss of E-cadherin-dependent cell-cell adhesion due to mutation of the beta-catenin gene in a human cancer cell line, HSC-39. Mol. Cell. Biol 1995, 15:1175-1181.
43. Rodriguez L.G., Wu X., Guan J.L. Wound-healing assay. Methods Mol. Biol 2005, 294:23-29.
44. Birchmeier W., Behrens J. Cadherin expression in carcinomas: role in the formation of cell junctions and the prevention of invasiveness. Biochim. Biophys. Acta 1994, 1198:11-26.
45. Llovet J.M., Chen Y., Wurmbach E., Roayaie S., Fiel M.I., Schwartz M., et al. A molecular signature to discriminate dysplastic nodules from early hepatocellular carcinoma in HCV cirrhosis. Gastroenterology 2006, 131:1758-1767.
46. Ripoli M., Barbano R., Balsamo T., Piccoli C., Brunetti V., Coco M., et al. Hypermethylated levels of E-cadherin promoter in Huh-7 cells expressing the HCV core protein. Virus Res 2011, 160:74-81.
47. Lee S., Lee H.J., Kim J.H., Lee H.S., Jang J.J., Kang G.H. Aberrant CpG island hypermethylation along multistep hepatocarcinogenesis. Am. J. Pathol 2003, 163:1371-1378.
48. Blattler A., Farnham P.J. Cross-talk between site-specific transcription factors and DNA methylation states. J. Biol. Chem 2013, 288:34287-34294.
49. Roberts V.J., Steenbergen R., Murre C. Localization of E2A mRNA expression in developing and adult rat tissues. Proc. Natl. Acad. Sci. U.S.A. 1993, 90:7583-7587.
50. Kho C.J., Huggins G.S., Endege W.O., Hsieh C.M., Lee M.E., Haber E. Degradation of E2A proteins through a ubiquitin-conjugating enzyme, UbcE2A. J. Biol. Chem 1997, 272:3845-3851.
51. Huggins G.S., Chin M.T., Sibinga N.E., Lee S.L., Haber E., Lee M.E. Characterization of the mUBC9-binding sites required for E2A protein degradation. J. Biol. Chem 1999, 274:28690-28696.
52. Sun L., Trausch-Azar J.S., Ciechanover A., Schwartz A.L. E2A protein degradation by the ubiquitin-proteasome system is stage-dependent during muscle differentiation. Oncogene 2007, 26:441-448.