The C-terminal region of the hepatitis B virus X protein is required for its stimulation of HBV replication in primary mouse hepatocytes

Virus Research

Volumn 165, Issue 2, 2012, Pages 170-178

  Luo, Na ^a   Cai, Yuan ^a   Zhang, Jun ^b   Tang, Weixue ^c   Slagle, Betty L ^d   Wu, Xiaoling ^a   He, Song ^a  

^a THE SECOND AFFILIATED HOSPITAL OF CHONGQING MEDICAL UNIVERSITY   (China)

^b CHONGQING MEDICAL UNIVERSITY   (China)

^c THE FIRST AFFILIATED HOSPITAL OF CHONGQING MEDICAL UNIVERSITY   (China)

^d BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Cell cycle; HBx truncation mutants; Hepatitis B virus; Hepatitis B virus X (HBx); Primary hepatocytes; Viral replication

Indexed keywords

HEPATITIS B VIRUS X PROTEIN;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; HEPATITIS B VIRUS; LIVER CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; VIRUS REPLICATION;

ANIMALS; HEPATITIS B VIRUS; HEPATOCYTES; MICE; MICE, INBRED C57BL; TRANS-ACTIVATORS; VIRUS REPLICATION;

HEPATITIS B VIRUS; RATTUS;

EID: 84862824257     PISSN: 01681702     EISSN: 18727492     Source Type: Journal    
DOI: 10.1016/j.virusres.2012.02.013     Document Type: Article

References (54)

1. Beasley R.P., Hwang L.Y., Lin C.C., Chien C.S. Hepatocellular carcinoma and hepatitis B virus. A prospective study of 22707 men in Taiwan. Lancet 1981, 2(8256):1129-1133.
2. Besson A., Dowdy S.F., Roberts J.M. CDK inhibitors: cell cycle regulators and beyond. Dev. Cell 2008, 14(2):159-169.
3. Bonilla Guerrero R., Roberts L.R. The role of hepatitis B virus integrations in the pathogenesis of human hepatocellular carcinoma. J. Hepatol. 2005, 42(5):760-777.
4. Bouchard M.J., Wang L.H., Schneider R.J. Calcium signaling by HBx protein in hepatitis B virus DNA replication. Science 2002, 294(5550):2376-2378.
5. Cánepa E.T., Scassa M.E., Ceruti J.M., Marazita M.C., Carcagno A.L., Sirkin P.F., Ogara M.F. INK4 proteins, a family of mammalian CDK inhibitors with novel biological functions. IUBMB Life 2007, 59(7):419-426.
6. Chen H.S., Kaneko S., Girones R., Anderson R.W., Hornbuckle W.E., Tennant B.C., Cote P.J., Gerin J.L., Purcell R.H., Miller R.H. The woodchuck hepatitis virus X gene is important for establishment of virus infection in woodchucks. J. Virol. 1993, 67(3):1218-1226.
7. Clippinger A.J., Bouchard M.J. Hepatitis B virus HBx protein localizes to mitochondria in primary rat hepatocytes and modulates mitochondrial membrane potential. J. Virol. 2008, 82(14):6798-6811.
8. Clippinger A.J., Gearhart T.L., Bouchard M.J. Hepatitis B virus X protein modulates apoptosis in primary rat hepatocytes by regulating both NF-kB and the mitochondrial permeability transition pore. J. Virol. 2009, 83(10):4718-4731.
9. Cooper S. Reappraisal of serum starvation, the restriction point, G0, and G1 phase arrest points. FASEB J. 2003, 17(3):333-340.
10. Diao J., Garces R., Richardson C.D. X protein of hepatitis B virus modulates cytokine and growth factor related signal transduction pathways during the course of viral infections and hepatocarcinogenesis. Cytokine Growth Factor Rev. 2001, 12(2-3):189-205.
11. Donehower L.A., Harvey M., Slagle B.L., McArthur M.J., Montgomery C.A., Butel J.S., Bradley A. Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours. Nature 1992, 356(6366):215-221.
12. el-Deiry W.S., Tokino T., Velculescu V.E., Levy D.B., Parsons R., Trent J.M., Lin D., Mercer W.E., Kinzler K.W., Vogelstein B. WAF1, a potential mediator of p53 tumor suppression. Cell 1993, 75(4):817-825.
13. Feitelson M.A. Hepatocellular injury in hepatitis B and C virus infections. Clin. Lab. Med. 1996, 16(2):307-324.
14. Friedrich B., Wollersheim M., Brandenburg B., Foerste R., Will H., Hildt E. Induction of anti-proliferative mechanisms in hepatitis B virus producing cells. J. Hepatol. 2005, 43:696-703.
15. Gearhart T.L., Bouchard M.J. The hepatitis B virus X protein modulates hepatocyte proliferation pathways to stimulate viral replication. J. Virol. 2010, 84(6):2675-2686.
16. Gearhart T.L., Bouchard M.J. Replication of the hepatitis B virus requires a calcium-dependent HBx-induced G1 phase arrest of hepatocytes. Virology 2010, 407(1):14-25.
17. Harper J.V., Brooks G. The mammalian cell cycle: an overview. Methods Mol. Biol. 2005, 296:113-153.
18. Hodgson A.J., Hyser J.M., Keasler V.V., Cang Y., Slagle B.L. Hepatitis B virus regulatory HBx protein binding to DDB1 is required but is not sufficient for maximal HBV replication. Virology 2012, (Epub ahead of print).
19. Huang Y.Q., Wang L.W., Yan S.N., Gong Z.J. Effects of cell cycle on telomerase activity and on hepatitis B virus replication in HepG2 2.2.15 cells. Hepatobiliary Pancreat. Dis. Int. 2004, 3(4):543-547.
20. Keasler V.V., Hodgson A.J., Madden C.R., Slagle B.L. Enhancement of hepatitis B virus replication by the regulatory X protein in vitro and in vivo. J. Virol. 2007, 81(6):2656-2662.
21. Keasler V.V., Hodgson A.J., Madden C.R., Slagle B.L. Hepatitis B virus HBx protein localized to the nucleus restores HBx-deficient virus replication in HepG2 cells and in vivo in hydrodynamically-injected mice. Virology 2009, 390(1):122-129.
22. Krishna M., Lloyd R.V., Batts K.P. Detection of albumin messenger RNA in hepatic and extrahepatic neoplasms. A marker of hepatocellular differentiation. Am. J. Surg. Pathol. 1997, 21(2):147-152.
23. Lee T.H., Elledge S.J., Butel J.S. Hepatitis B virus X protein interacts with a probable cellular DNA repair protein. J. Virol. 1995, 69(2):1107-1114.
24. Leupin O., Bontron S., Schaeffer C., Strubin M. Hepatitis B virus X protein stimulates viral genome replication via a DDB1-dependent pathway distinct from that leading to cell death. J. Virol. 2005, 79(7):4238-4245.
25. Lizzano R.A., Yang B., Clippinger A.J., Bouchard M.J. The C-terminal region of the hepatitis B virus X protein is essential for its stability and function. Virus Res. 2011, 155(1):231-239.
26. Li W.-C., Ralphs K.L., Tosh D. Isolation and culture of adult mouse hepatocytes. Methods Mol. Biol. 2010, 633:185-196.
27. Madden C.R., Slagle B.L. Stimulation of cellular proliferation by hepatitis B virus X protein. Dis. Markers 2001, 17:153-157.
28. Melegari M., Scaglioni P.P., Wands J.R. Cloning and characterization of a novel hepatitis B virus X binding protein that inhibits viral replication. J. Virol. 1998, 72(3):1737-1743.
29. Minami M., Daimon Y., Mori K., Takashima H., Nakajima T., Itoh Y., Okanoue T. Hepatitis B virus-related insertional mutagenesis in chronic hepatitis B patients as an early drastic genetic change leading to hepatocarcinogenesis. Oncogene 2005, 24(27):4340-4348.
30. Murakami Y., Saigo K., Takashima H., Minami M., Okanoue T., Bréchot C., Paterlini-Bréchot P. Large scaled analysis of hepatitis B virus (HBV) DNA integration in HBV related hepatocellular carcinomas. Gut 2005, 54(8):1162-1168.
31. Murray A.W. Recycling the cell cycle: cyclins revisited. Cell 2004, 116(2):221-234.
32. Nakatake H., Chisaka O., Yamamoto S., Matsubara K., Koshy R. Effect of X protein on transactivation of hepatitis B virus promoters and on viral replication. Virology 1993, 195(2):305-314.
33. Ozer A., Khaoustov V.I., Mearns M., Lewis D.E., Genta R.M., Darlington G.J., Yoffe B. Effect of hepatocyte proliferation and cellular DNA synthesis on hepatitis B virus replication. Gastroenterology 1996, 110(5):1519-1528.
34. Pan J., Duan L.X., Sun B.S., Feitelson M.A. Hepatitis B virus X protein protects against anti-Fas-mediated apoptosis in human liver cells by inducing NF-kappa B. J. Gen. Virol. 2001, 82(Pt 1):171-182.
35. Park U.S., Park S.K., Lee Y.I., Park J.G., Lee Y.I. Hepatitis B virus-X protein upregulates the expression of p21waf1/cip1 and prolongs G1/S transition via a p53-independent pathway in human hepatoma cells. Oncogene 2000, 19(30):3384-3394.
36. Pezzella F., Micklem K., Turley H., Pulford K., Jones M., Kocialkowski S., Delia D., Aiello A., Bicknell R., Smith K., Harris A.L., Gatter K.C., Mason D.Y. Antibody for detecting p53 protein by immunohistochemistry in normal tissues. J. Clin. Pathol. 1994, 47(7):592-596.
37. Poussin K., Dienes H., Sirma H., Urban S., Beaugrand M., Franco D., Schirmacher P., Bréchot C., Paterlini-Bréchot P. Expression of mutated hepatitis B virus X genes in human hepatocellular carcinomas. Int. J. Cancer 1999, 80(4):497-505.
38. Qiao L., Leach K., McKinstry R., Gilfor D., Yacoub A., Park J.S., Grant S., Hylemon P.B., Fisher P.B., Dent P. Hepatitis B virus X protein increases expression of p21Cip-1/WAF1/MDA6 and p27Kip-1 in primary mouse hepatocytes, leading to a reduced cell cycle progression. Hepatology 2001, 34(5):906-917.
39. Ross J.S., Linette G.P., Stec J., Ross M.S., Anwar S., Boguniewicz A. DNA ploidy and cell cycle analysis in breast cancer. Am. J. Clin. Pathol. 2003, 120(Suppl. 1):S72-S84.
40. Scaglioni P.P., Melegari M., Wands J.R. Posttranscriptional regulation of hepatitis B virus replication by the precore protein. J. Virol. 1997, 71(1):345-353.
41. Schafer K.A. The cell cycle: a review. Vet. Pathol. 1998, 35(6):461-478.
42. Sherr C.J., Roberts J.M. CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev. 1999, 13(12):1501-1512.
43. Sirma H., Giannini C., Poussin K., Paterlini P., Kremsdorf D., Bréchot C. Hepatitis B virus X mutants, present in hepatocellular carcinoma tissue abrogate both the antiproliferative and transactivation effects of HBx. Oncogene 1999, 18(34):4848-4859.
44. Tang H., Delgermaa L., Huang F., Oishi N., Liu L., He F., Zhao L., Murakami S. The transcriptional transactivation function of HBx protein is important for its augmentation role in hepatitis B virus replication. J. Virol. 2005, 79(9):5548-5556.
45. Thorgeirsson S.S. Hepatic stem cells in liver regeneration. FASEB J. 1996, 10:1249-1256.
46. Tsuge M., Hiraga N., Akiyama R., Tanaka S., Matsushita M., Mitsui F., Abe H., Kitamura S., Hatakeyama T., Kimura T., Miki D., Mori N., Imamura M., Takahashi S., Hayes C.N., Chayama K. HBx protein is indispensable for development of viremia in human hepatocyte chimeric mice. J. Gen. Virol. 2010, 91(Pt 7):1854-1864.
47. Tu H., Bonura C., Giannini C., Mouly H., Soussan P., Kew M., Paterlini-Bréchot P., Bréchot C., Kremsdorf D. Biological impact of natural COOH-terminal deletions of hepatitis B virus X protein in hepatocellular carcinoma tissues. Cancer Res. 2001, 61(21):7803-7810.
48. van Gijssel H.E., Maassen C.B., Mulder G.J., Meerman J.H. p53 protein expression by hepatocarcinogens in the rat liver and its potential role in mitoinhibition of normal hepatocytes as a mechanism of hepatic tumour promotion. Carcinogenesis 1997, 18(5):1027-1033.
49. Vermeulen K., Van Bockstaele D.R., Berneman Z.N. The cell cycle: a review of regulation, deregulation and therapeutic targets in cancer. Cell Prolif. 2003, 36(3):131-149.
50. Wang J., Chenivesse X., Henglein B., Brechot C. Hepatitis B virus integration in a cyclin A gene in a hepatocellular carcinoma. Nature 1990, 343(6258):555-557.
51. Wang X.W., Forrester K., Yeh H., Feitelson M.A., Gu J.R., Harris C.C. Hepatitis B virus X protein inhibits p53 sequence-specific DNA binding, transcriptional activity, and association with transcription factor ERCC3. Proc. Natl. Acad. Sci. U.S.A. 1994, 91(6):2230-2234.
52. Zhang H., Shan C.L., Li N., Zhang X., Zhang X.Z., Xu F.Q., Zhang S., Qiu L.Y., Ye L.H., Zhang X.D. Identification of a natural mutant of HBV X protein truncated 27 amino acids at the COOH terminal and its effect on liver cell proliferation. Acta Pharmacol. Sin. 2008, 29(4):473-480.
53. Zhang Z., Protzer U., Hu Z., Jacob J., Liang T.J. Inhibition of cellular proteasome activities enhances hepadnavirus replication in an HBX-dependent Manner. J. Virol. 2004, 78(9):4566-4572.
54. Zoulim F., Saputelli J., Seeger C. Woodchuck hepatitis virus X protein is required for viral infection in vivo. J. Virol. 1994, 68(3):2026-2030.