Hepatitis C virus replication in stably transfected HepG2 cells promotes hepatocellular growth and tumorigenesis

Journal of Cellular Physiology

Volumn 201, Issue 3, 2004, Pages 447-458

  Sun, Bill S ^a   Pan, Jingbo ^a   Clayton, Marcy M ^a   Liu, Jie ^a,c   Yan, Xiaoping ^a,d   Matskevich, Alexey A ^a   Strayer, David S ^a   Gerber, Michael ^b   Feitelson, Mark A ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b TULANE UNIVERSITY   (United States)

^c FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^d First Hospital   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; COMPLEMENTARY DNA; CORE PROTEIN; PROTEIN NS5B; RIBONUCLEASE; UNCLASSIFIED DRUG; VIRUS RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL GROWTH; CELL STRAIN HEPG2; CONTROLLED STUDY; GENETIC TRANSFECTION; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; LIVER CARCINOGENESIS; LIVER CELL CARCINOMA; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; NUDE MOUSE; PRIORITY JOURNAL; RNA EXTRACTION; RNA SYNTHESIS; SCID MOUSE; VIRUS CARCINOGENESIS; VIRUS CONCENTRATION; VIRUS REPLICATION;

ANIMALS; CELL LINE, TUMOR; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; GENE EXPRESSION REGULATION, VIRAL; HEPACIVIRUS; HEPATOCYTES; HUMANS; INTERFERON-ALPHA; MICE; MICE, SCID; RNA VIRUSES; TRANSFECTION; VIRAL CORE PROTEINS; VIRAL NONSTRUCTURAL PROTEINS; VIRUS REPLICATION;

HEPATITIS C VIRUS;

EID: 7544250771     PISSN: 00219541     EISSN: None     Source Type: Journal    
DOI: 10.1002/jcp.20083     Document Type: Article

References (71)

1. Aizaki H, Nagamori S, Matsuda M, Kawakami H, Hashimoto O, Ishiko H, Kawada M, Matsuura T, Hasumura S, Matsuura Y, Suzuki T, Miyamura T. 2003. Production and release of infectious hepatitis C virus from human liver cell cultures in the three-dimensional radial-flow bioreactor. Virology 314:16-25.
2. Alter HJ, Purcell RH, Shih JW, Melpolder JC, Houghton M, Choo QL, Kuo G. 1989. Detection of antibody to hepatitis C virus in prospectively followed transfusion recipients with acute and chronic non-A, non-B hepatitis. N Engl J Med 321:1495-1500.
3. Bertolini L, Lacovacci C, Carloni G. 1993. The human bone marrow derived B cell line CE, susceptible to hepatitis C virus infection. Res Virol 144:281-285.
4. Blight KJ, Kolykhalov AA, Rice CM. 2000. Efficient initiation of HCV RNA replication in cell culture. Science 290:1972-1974.
5. Blight KJ, McKeating JA, Rice CM. 2002. Highly permissive cell lines for subgenomic and genomic hepatitis C virus RNA replication. J Virol 76:13001-13014.
6. Blight KJ, McKeating JA, Marcotrigiano J, Rice CM. 2003. Efficient replication of hepatitis C virus genotype 1a RNAs in cell culture. J Virol 77:3181-3190.
7. Carloni G, Iacovacci S, Sargiacomo M, Pavagnan G, Ponsetto A, Peschle C, Battaglia M. 1993. Susceptibility of human liver cell cultures to hepatitis C virus infection. Arch Virol 8:31-39.
8. Castet V, Fournier C, Soulier A, Brillet R, Coste J, Larrey D, Dhumeaux D, Maurel P, Pawlotsky JM. 2002. Alpha interferon inhibits hepatitis C virus replication in primary human hepatocytes infected in vitro. J Virol 76:8189-8199.
9. Chambers TJ, Hahn CS, Galler R, Rice CM. 1990. Flavivirus genome organization, expression, and replication. Ann Rev Microbiol 44:649-688.
10. Chang J, Yang SH, Cho YG, Hwang SB, Hahn YS, Sung YC. 1998. 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 72:3060-3065.
11. Chang M, Williams O, Mittler J, Quintanilla A, Carithers RL, Jr., Perkins J, Corey L, Gretch DR. 2003. Dynamics of hepatitis C virus replication in human liver. Am J Pathol 163:433-444.
12. Chien DY, Xhoo QL, Tabrizi A, Kuo C, McFarland J, Berger K, Lee C, Shuster JR, Nguyen T, Moyer DL. 1992. Diagnosis of hepatitis C virus (HCV) infection using an immunodominant chronic polypeptide to capture circulating antibodies. Revaluation of the role of HCV in liver disease. Proc Natl Acad Sci USA 89:10011-10015.
13. Choo QL, Kuo G, Weiner AJ, Overby LR, Bradley DW, Houghton M. 1989. Isolation of a cDNA clone derived from a blood-borne non-A, non-B viral hepatitis genome. Science 244:359-362.
14. Chung RT, He W, Saquib A, Contreras AM, Xavier RJ, Chawla A, Wang TC, Schmidt EV. 2001. Hepatitis C virus replication is directly inhibited by IFN-alpha in a full-length binary expression system. Proc Natl Acad Sci USA 98:9847-9852.
15. Contreras AM, Hiasa Y, He W, Terella A, Schmidt EV, Chung RT. 2002. Viral RNA mutations are region specific and increased by ribavirin in a full-length hepatitis c virus replication system. J Virol 76:8505-8517.
16. Dash S, Halim AB, Tsuji H, Hiramatsu N, Gerber MA. 1997. Transfection of HepG2 cells with infectious hepatitis C virus genome. Am J Pathol 151:363-373.
17. Dash S, Kalkeri G, McClure HM, Garry RF, Clejan S, Thung SN, Murthy KK. 2001. Transmission of HCV to a chimpanzee using virus particles produced in an RNA-transfected HepG2 cell culture. J Med Virol 65:276-281.
18. Davis GL. 2000. Current therapy for chronic hepatitis C. Gastroenterology 118:S104-S114.
19. Di Bisceglie AM. 1995. Hepatitis C and hepatocellular carcinoma. Sem Liver Dis 15:64-69.
20. Feitelson MA. 2002. Hepatitis C virus: From bench to bedside. Cambridge: Cambridge University Press. pp 113-117.
21. Fournier C, Sureau C, Coste J, Ducos J, Pageaux G, Larrey D, Domergue J, Maurel P. 1998. In vitro infection of adult normal human hepatocytes in primary culture by hepatitis C virus. J Gen Virol 79:2367-2374.
22. Fujita T, Ishido S, Muramatsu S, Itoh M, Hotta H. 1996. Suppression of actinomycin D-induced apoptosis by the NS3 protein of hepatitis C virus. Biochem Biophys Res Commun 229:825-831.
23. Gale M, Jr., Kwieciszewski B, Dossett M, Nakao H, Katze MG. 1999. Antiapoptotic and oncogenic potentials of hepatitis C virus are linked to interferon resistance by viral repression of the PKR protein kinase. J Virol 73:6506-6516.
24. Gerber MA, Shieh YSC, Shim KS, Thung SN, Demetris AJ, Schwartz M, Akyol G, Dash S. 1992. Detection of replicative hepatitis C virus sequences in hepatocellular carcinoma. Am J Pathol 141:1271-1277.
25. Ghosh AK, Stelle R, Meyer K, Fay R, Ray RB. 1999. Hepatitis C virus NS5A protein modulates cell cycle regulatory genes and promotes cell growth. J Gen Virol 80:1179-1183.
26. Hijikata M, Shimizu YK, Kato H, Iwamoto A, Shih JW, Alter HJ, Purcell RH, Yoshikura H. 1993. Equilibrium centrifugation studies of hepatitis C virus: Evidence for circulating immune complexes. J Virol 67:1953-1958.
27. Hiramatsu N, Dash S, Gerber MA. 1997. HCV cDNA transfection to HepG2 cells. J Viral Hepat 4:S61-S67.
28. Horiike N, Nonaka T, Kumamoto J, Kajino K, Onji M, Ohta Y. 1993. Hepatitis C virus plus and minus strand RNA in hepatocellular carcinoma and adjoining nontumourous liver. J Med Virol 41:312-315.
29. Houghton MC. 1996. Hepatitis C viruses. In: Fields BN, Knipe DM, Howley PM, editors. Fields virology, 3rd edn. Philadelphia: Lippincott-Raven. pp 1035-1058.
30. Iacovacci S, Sargiacomo M, Parolini I, Ponzetto A, Peschle C, Carloni G. 1993. Replication and multiplication of hepatitis C virus genome in human fetal liver cells. Res Virol 144:275-279.
31. Ikeda M, Sugiyama K, Mizutani T, Tanaka T, Tanaka K, Sekihara H, Shimotohno K, Kato N. 1998. Human hepatocyte clonal cell lines that support persistent replication of hepatitis C virus. Virus Res 56:157-167.
32. Ikeda M, Yi M, Li K, Lemon SM. 2002. Selectable subgenomic and genomic length dicistronic RNAs derived from an infectious molecular clone of the HCV-N strain of hepatitis C virus replicate efficiently in cultured Huh7 cells. J Virol 76:2997-3006.
33. Ito T, Yasui K, Mukaigawa J, Katsume A, Kohara M, Mitamura K. 2001. Acquisition of susceptibility to hepatitis C virus replication in HepG2 cells by fusion with primary human hepatocytes: Establishment of a quantitative assay for hepatitis C virus infectivity in a cull culture system. Hepatology 34:566-572.
34. Jin DY, Wang HL, Zhou Y, Chun AC, Kibler KV, Hou YD, Kung H, Jeang KT. 2000. Hepatitis C virus core protein-induced loss of LZIP function correlates with cellular transformation. EMBO J 19:729-740.
35. Kato N, Nakazawa T, Mizutani T, Shimotohno K. 1995. Susceptibility of human T-lymphotropic virus type 1 infected cell line MT-2 to hepatitis C virus infection. Biochem Biophys Res Commun 206:863-869.
36. Kato N, Ikeda M, Mizutani T, Sugiyama K, Noguchi M, Hirohashi S, Shimotohno K. 1996. Replication of hepatitis C virus in cultured non-neoplastic human hepatocytes. Jpn J Cancer Res 87:787-792.
37. Lai MY, Kao JH, Yang PM, Wang JT, Chen PJ, Chan KW, Chu JS, Chen DS. 1996. Long-term efficacy of ribavirin plus interferon alfa in the treatment of chronic hepatitis C. Gastroenterology 111:1307-1312.
38. Lanford RE, Sureau C, Jacob JR, White R, Fuerst TR. 1994. Demonstration of in vitro infection of chimpanzee hepatocytes with hepatitis C virus using strand-specific RT/PCR. Virology 202:606-614.
39. Lian Z, Pan J, Liu J, Zhu M, Arbuthnot P, Kew MC, Feitelson MA. 1999. The translation initiation factor, SUI1, may be a target of hepatitis B x antigen in hepatocarcinogenesis. Oncogene 18:1677-1687.
40. Lohmann V, Korner F, Koch JO, Herian U, Theilmann L, Bartenschlager R. 1999. Replication of subgenomic hepatitis C virus RNA in a hepatoma cell line. Science 285:110-113.
41. Marusawa H, Hijikata M, Chiba T, Shimotohno K. 1999. Hepatitis C virus core protein inhibits Fas- and tumor necrosis factor alpha-mediated apoptosis via NF-κB activation. J Virol 73:4713-4720.
42. Matsuura Y, Kimura S, Miyamura T, Koike K. 1998. The core protein of hepatitis C virus induces hepatocellular carcinoma in transgenic mice. Nat Med 4:1065-1067.
43. Miyamoto H, Okamoto H, Sato K, Tanaka T, Mishiro S. 1992. Extraordinarily low density of hepatitis C virus estimated by sucrose density gradient centrifugation and the polymerase chain reaction. J Gen Virol 73:715-718.
44. Mizutani T, Kato N, Ikeda M, Sugiyama K, Shimotohno K. 1996. Long term human T cell culture system supporting hepatitis C virus replication. Biochem Biophys Res Commun 227:822-826.
45. Novak JE, Kirkegaard K. 1991. Improved method for detecting negative strands used to demonstrate specificity of plus strand encapsidation and the ratio of positive to negative strands in infected cells. J Virol 65:3384-3387.
46. Pietschmann T, Lohmann V, Kaul A, Krieger N, Rinck G, Rutter G, Strand D, Bartenschlager R. 2002. Persistent and transient replication of full-length hepatitis C virus genomes in cell culture. J Virol 76:4008-4021.
47. Poynard T, Leroy V, Cohard M, Thevenot Th, Mathurin Ph, Opolon P, Zarski JP. 1996. Meta-analysis of interferon randomized trials in the treatment of viral hepatitis C: Effects of dose and duration. Hepatology 24:778-789.
48. Ray RB, Lagging LM, Meyer K, Steele R, Ray R. 1995. Transcriptional regulation of cellular and viral promoters by the hepatitis C virus core protein. Virus Res 37:209-220.
49. WAF1/CIP1/SDI1 promoter activity. Gene 208:331-336.
50. Ray RB, Meyer K, Steele R, Shrivastava A, Aggarwal BB, Ray R. 1998b. Inhibition of tumor necrosis factor (TNF-alpha)-mediated apoptosis by hepatitis C virus core protein. J Biol Chem 273:2256-2259.
51. Reichard O, Norkrans G, Fryden A, Braconier JH, Sonnerborg A, Weiland O. 1998. Alfa-interferon and ribavirin versus alfa-interferon alone as therapy for chronic hepatitis C: A randomized, double-blind, placebo-controlled study. Lancet 351:83-87.
52. Ruggieri A, Harada T, Matsuura Y, Miyamura T. 1997. Sensitization to Fas-mediated apoptosis by hepatitis C virus core protein. Virology 229:68-76.
53. Rumin S, Berthillon P, Tanaka E, Kiyosawa K, Trabaud MA, Bizollon T, Gouillat C, Gripon P, Guguen-Guillouzo C, Inchauspe G, Trepo C. 1999. Dynamic analysis of hepatitis C virus replication and quasispecies selection in long-term cultures of adult human hepatocytes infected in vitro. J Gen Virol 80:3007-3018.
54. Sakamuro D, Furukawa T, Takegami T. 1995. Hepatitis C virus nonstructural protein NS3 transforms NIH3T3 cells. J Virol 69:3893-3896.
55. Schinazi RF, Ilan E, Black PL, Yao X, Dagan S. 1999. Cell-based and animal models for hepatitis B and C viruses. Antiviral Chem Chemother 10:99-114.
56. Seipp S, Mueller HM, Pfaff E, Stremmel W, Theilmann L, Goeser T. 1997. Establishment of persistent hepatitis C virus infection and replication in vitro. J Gen Virol 78:2467-2476.
57. Shimizu YK, Iwamoto A, Hijikata M, Purcell RH, Yoshikura H. 1992. Evidence for in vitro replication of hepatitis C virus genome in a human T-cell line. Proc Natl Acad Sci USA 89:5477-5781.
58. Shimizu YK, Purcell RH, Yoshikura H. 1993. Correlation between the infectivity of hepatitis C virus in vivo and its infectivity in vitro. Proc Natl Acad Sci USA 90:6037-6041.
59. Sun B, Pan J, Gerber M, Feitelson MA. 1999. Evidence for consistent HCV replication in HepG2 cells. Antiviral Ther 4(Suppl 4):A94.
60. Sung VMH, Shimodaira S, Doughty AL, Picchio GR, Can H, Yen TSB, Lindsay KL, Levine AM, Lai MMC. 2003. Establishment of B-cell lymphoma cell lines persistently infected with hepatitis C virus in vivo and in vitro: The apoptotic effects of virus infection. J Virol 77:2134-2146.
61. Takamizawa A, Mori C, Fuke I, Manabe S, Murakami S, Fujita J, Onishi E, Andoh T, Yoshida I, Okayama H. 1991. Structure and organization of the hepatitis C virus genome isolated from human carriers. J Virol 65:1105-1113.
62. Takehara T, Hayashi N, Miyamoto Y, Yamamoto M, Mita E, Fusamoto H, Kamada T. 1995. Expression of the hepatitis C virus genome in rat liver after cationic liposome-mediated in vivo gene transfer. Hepatology 21:746-751.
63. Tan SL, Nakao H, He YP, Vijaysri S, Neddermann P, Jacobs BL, Mayer BJ, Katze MG. 1999. NS5A, a nonstructural protein of hepatitis C virus, binds growth factor receptor-bound protein 2 adaptor protein in a Src homology 3 domain/ligand-dependent manner and perturbs mitogenic signaling. Proc Natl Acad Sci USA 96:5533-5538.
64. Tanaka T, Kato N, Cho MJ, Shimotohno K. 1995. A novel sequence found at the 3′ terminus of hepatitis C virus genome. Biochem Biophys Res Commun 215:744-749.
65. Tang L, Tanaka Y, Enomoto N, Marumo F, Sato C. 1995. Detection of hepatitis C virus RNA in hepatocellular carcinoma by in situ hybridization. Cancer 76:2211-2216.
66. Tine F, Magrin S, Craxi A, Pagliaro L. 1991. Interferon for non-A, non-B chronic hepatitis: A meta-analysis of randomized clinical trials. J Hepatol 13:192-199.
67. Tsuchihara K, Hijikata M, Fukuda K, Kuroki T, Yamamoto N, Shimotohno K. 1999. Hepatitis C virus core protein regulates cell growth and signal transduction pathway transmitting growth stimuli. Virology 258:100-107.
68. Valli MB, Bertolini L, Lucovacci S, Ponzetto A, Carloni G. 1995. Detection of a 5′ UTR variation in the HCV genome after long term in vitro infection. Res Virol 146:285-288.
69. Yoo BJ, Selby M, Cho J, Suh BS, Choi SH, Job JS, Nuovo GJ, Lee HS, Houghton M, Han JH. 1995. Transfection of a differentiated human hepatoma cell line Huh7 with in vitro transcribed hepatitis C virus HCV RNA and establishment of a long term culture persistently infected with HCV. J Virol 69:32-38.
70. Zhao X, Tang ZY, Klumpp B, Wolff-Vorbeck G, Barth H, Levy S, von Weizsacker F, Blum HE, Baumert TF. 2002. Primary hepatocytes of Tupaia belangeri as a potential model for hepatitis C virus infection. J Clin Invest 109:221-232.
71. Zhu N, Khoshnam A, Schneider R, Matsumoto M, Dennert G, Ware C, Lai MM. 1998. Hepatitis C virus core protein binds to the cytoplasmic domain of tumor necrosis factor (TNF) receptor 1 and enhances TNF-induced apoptosis. J Virol 72:3691-3697.