Mouse models of hepatitis B virus pathogenesis

Cold Spring Harbor Perspectives in Medicine

Volumn 5, Issue 11, 2015, Pages

  Iannacone, Matteo ^a,b   Guidotti, Luca G ^a,c  

^a SAN RAFFAELE HOSPITAL   (Italy)

^b VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACUTE HEPATITIS; ARTICLE; CHRONIC HEPATITIS; HEPATITIS B; HEPATITIS B VIRUS; HUMAN; MOUSE MODEL; NONHUMAN; VIRUS PATHOGENESIS; ANIMAL; DISEASE MODEL; MOUSE; PATHOGENICITY; PHYSIOLOGY; VIROLOGY;

ANIMALS; DISEASE MODELS, ANIMAL; HEPATITIS B; HEPATITIS B VIRUS; HEPATITIS B, CHRONIC; MICE;

EID: 84926290538     PISSN: None     EISSN: 21571422     Source Type: Journal    
DOI: 10.1101/cshperspect.a021477     Document Type: Article

References (56)

1. Ando K, Guidotti LG, Wirth S, Ishikawa T, Missale G, Moriyama T, Schreiber RD, Schlicht HJ, Huang SN, Chisari FV. 1994. Class I-restricted cytotoxic T lymphocytes are directly cytopathic for their target cells in vivo. J Immunol 152: 3245-3253.
2. Azuma H, Paulk N, Ranade A, Dorrell C, Al-Dhalimy M, Ellis E, Strom S, Kay MA, Finegold M, Grompe M. 2007. Robust expansion of human hepatocytes in Fah2/2/ Rag22/2/Il2rg2/2 mice. Nat Biotechnol 25: 903-910.
3. BissigKD, Le TT,Woods NB,Verma IM. 2007.Repopulation of adult and neonatal mice with human hepatocytes: A chimeric animal model. Proc Natl Acad Sci 104: 20507- 20511.
4. Bissig K-D,Wieland SF, Tran P, Isogawa M, Le TT, Chisari FV, Verma IM. 2010. Human liver chimeric mice provide a model for hepatitis B and C virus infection and treatment. J Clin Invest 120: 924-930.
5. Brećhot C. 2004. Pathogenesis of hepatitis B virus-related hepatocellular carcinoma: Old and new paradigms. Gastroenterology 127: S56-S61.
6. Brećhot C, Kremsdorf D, Soussan P, Pineau P, Dejean A, Paterlini-Brećhot P, Tiollais P. 2010. Hepatitis B virus (HBV)-related hepatocellular carcinoma (HCC):Molecular mechanisms and novel paradigms. Pathol Biol 58: 278-287.
7. Chen M, Sällberg M, Thung SN, Hughes J, Jones J, Milich DR. 2001. Modeling the T-helper cell response in acute and chronic hepatitis B virus infection using T-cell receptor transgenic mice. Antiviral Res 52: 99-111.
8. Dandri M. 2001. Repopulation of mouse liver with human hepatocytes and in vivo infection with hepatitis B virus. Hepatology 33: 981-988.
9. Dandri M, Lütgehetmann M. 2014. Mouse models of hepatitis B and delta virus infection. J Immunol Methods 410: 39-49.
10. Dion S, Bourgine M, Godon O, Levillayer F, Michel M-L. 2013. Adeno-associated virus-mediated gene transfer leads to persistent hepatitis B virus replication in mice expressing HLA-A2 and HLA-DR1 molecules. J Virol 87: 5554-5563.
11. Ganem D, Prince A. 2004. Hepatitis B virus infection-Natural history and clinical consequences. N Engl J Med 350: 1118-1129.
12. Grompe M, Strom S. 2013. Mice with human livers. Gastroenterology 145: 1209-1214.
13. Guidotti LG, Chisari FV. 2006. Immunobiology and pathogenesis of viral hepatitis. Annu Rev Pathol 1: 23-61.
14. Guidotti LG, Ando K, Hobbs MV, Ishikawa T, Runkel L, Schreiber RD, Chisari FV. 1994. Cytotoxic T lymphocytes inhibit hepatitis B virus gene expression by a noncytolytic mechanism in transgenic mice. Proc Natl Acad Sci 91: 3764-3768.
15. Guidotti LG, Matzke B, Schaller H, Chisari FV. 1995. Highlevel hepatitis B virus replication in transgenic mice. J Virol 69: 6158-6169.
16. Guidotti LG, Ishikawa T, Hobbs MV, Matzke B, Schreiber R, Chisari FV. 1996. Intracellular inactivation of the hepatitis B virus by cytotoxic T lymphocytes. Immunity 4: 25-36.
17. Guidotti LG, Rochford R, Chung J, Shapiro M, Purcell R, Chisari FV. 1999. Viral clearance without destruction of infected cells during acute HBV infection. Science 284: 825-829.
18. Guidotti LG, McClary H, Loudis JM, Chisari FV. 2000. Nitric oxide inhibits hepatitis B virus replication in the livers of transgenic mice. 191: 1247-1252.
19. Guidotti LG, Inverso D, Sironi L, Di Lucia P, Fioravanti J, Ganzer L, Fiocchi R, Vacca M, Aiolfi R, Sammicheli S, et al. 2015. Immunosurveillance of the liver by intravascular effector CD8þ T cells. Cell doi:10.1016/j.cell.2015. 03.005.
20. Heckel JL, Sandgren EP, Degen JL, Palmiter RD, Brinster RL. 1990. Neonatal bleeding in transgenic mice expressing urokinase-type plasminogen activator. Cell 62: 447-456.
21. Heise T, Guidotti LG, Cavanaugh VJ, Chisari FV. 1999a. Hepatitis B virus RNA-binding proteins associated with cytokine-induced clearance of viral RNA from the liver of transgenic mice. J Virol 73: 474-481.
22. Heise T, Guidotti LG, Chisari FV. 1999b. La autoantigen specifically recognizes a predicted stem-loop in hepatitis B virus RNA. J Virol 73: 5767-5776.
23. Heise T, Guidotti LG, Chisari FV. 2001. Characterization of nuclear RNases that cleave hepatitis B virus RNA near the La protein binding site. J Virol 75: 6874-6883.
24. Huang Y-H, Fang C-C, Tsuneyama K, Chou H-Y, Pan W-Y, Shih Y-M,Wu P-Y, Chen Y, Leung PSC, Gershwin ME, et al. 2011. A murine model of hepatitis B-associated hepatocellular carcinoma generated by adeno-associated virus- mediated gene delivery. Int J Oncol 39: 1511-1519.
25. Iannacone M, Sitia G, Isogawa M, Marchese P, Castro MG, Lowenstein PR, Chisari FV, Ruggeri ZM, Guidotti LG. 2005. Platelets mediate cytotoxic T lymphocyte-induced liver damage. Nat Med 11: 1167-1169.
26. Iannacone M, Sitia G, Narvaiza I, Ruggeri ZM, Guidotti LG. 2007a. Antiplatelet drug therapy moderates immunemediated liver disease and inhibits viral clearance in mice infected with a replication-deficient adenovirus. Clin Vaccine Immunol 14: 1532-1535.
27. Iannacone M, Sitia G, Ruggeri ZM, Guidotti LG. 2007b. HBV pathogenesis in animal models: Recent advances on the role of platelets. J Hepatol 46: 719-726.
28. Ilan E, Burakova T, Dagan S, Nussbaum O, Lubin I, Eren R, Ben-Moshe O, Arazi J, Berr S, Neville L, et al. 1999. The hepatitis B virus-trimera mouse: A model for human HBV infection and evaluation of anti-HBV therapeutic agents. Hepatology 29: 553-562.
29. Isogawa M, Furuichi Y, Chisari FV. 2005. Oscillating CD8þ T cell effector functions after antigen recognition in the liver. Immunity 23: 53-63.
30. Kakimi K, Lane TE, Wieland S, Asensio VC, Campbell IL, Chisari FV, Guidotti LG. 2001. Blocking chemokine responsive to γ-2/interferon (IFN)-γ inducible protein and monokine induced by IFN-γ activity in vivo reduces the pathogenetic but not the antiviral potential of hepatitis B virus-specific cytotoxic T lymphocytes. J Exp Med 194: 1755-1766.
31. Kosaka K, Hiraga N, Imamura M, Yoshimi S, Murakami E, Nakahara T, Honda Y, Ono A, Kawaoka T, Tsuge M, et al. 2013. A novel TK-NOG based humanized mouse model for the study of HBVand HCV infections. Biochem Biophys Res Commun 441: 230-235.
32. Kremsdorf D, Soussan P, Paterlini-Brechot P, Brechot C. 2006. Hepatitis B virus-related hepatocellular carcinoma: Paradigms for viral-related human carcinogenesis. Oncogene 25: 3823-3833.
33. Li H, Zhuang Q, Wang Y, Zhang T, Zhao J, Zhang Y, Zhang J, Lin Y, Yuan Q, Xia N, et al. 2014. HBV life cycle is restricted in mouse hepatocytes expressing human NTCP. Cell Mol Immunol 11: 175-183.
34. Lim WF, Inoue-Yokoo T, Tan KS, Lai MI, Sugiyama D. 2013. Hematopoietic cell differentiation from embryonic and induced pluripotent stem cells. Stem Cell Res Ther 4: 71.
35. Nakamoto Y, Guidotti LG, Kuhlen CV, Fowler P, Chisari FV. 1998. Immune pathogenesis of hepatocellular carcinoma. J Exp Med 188: 341-350.
36. Nakamoto Y, Suda T, Momoi T, Kaneko S. 2004. Different procarcinogenic potentials of lymphocyte subsets in a transgenic mouse model of chronic hepatitis B. Cancer Res 64: 3326-3333.
37. Raney AK, Eggers CM, Kline EF, Guidotti LG, Pontoglio M, Yaniv M, McLachlan A. 2001. Nuclear covalently closed circular viral genomic DNA in the liver of hepatocyte nuclear factor 1 a-null hepatitis B virus transgenic mice. J Virol 75: 2900-2911.
38. Rhim J, Sandgren E, Degen J, Palmiter R, Brinster R. 1994. Replacement of diseased mouse liver by hepatic cell transplantation. Science 263: 1149-1152.
39. RobekMD,Wieland SF, Chisari FV. 2002. Inhibition of hepatitis B virus replication by interferon requires proteasome activity. J Virol 76: 3570-3574.
40. Robek MD, Boyd BS, Wieland SF, Chisari FV. 2004. Signal transduction pathways that inhibit hepatitis B virus replication. Proc Natl Acad Sci 101: 1743-1747.
41. Sette AD, Oseroff C, Sidney J, Alexander J, Chesnut RW, Kakimi K, Guidotti LG, Chisari FV. 2001. Overcoming T cell tolerance to the hepatitis B virus surface antigen in hepatitis B virus-transgenic mice. J Immunol 166: 1389-1397.
42. Shimizu Y, Guidotti LG, Fowler P, Chisari FV. 1998. Dendritic cell immunization breaks cytotoxic T lymphocyte tolerance in hepatitis B virus transgenic mice. J Immunol 161: 4520-4529.
43. Sitia G, Isogawa M, Kakimi K,Wieland SF, Chisari FV, Guidotti LG. 2002. Depletion of neutrophils blocks the recruitment of antigen-nonspecific cells into the liver without affecting the antiviral activity of hepatitis B virusspecific cytotoxic T lymphocytes. Proc Natl Acad Sci 99: 13717-13722.
44. Sitia G, Isogawa M, Iannacone M, Campbell IL, Chisari FV, Guidotti LG. 2004.MMPs are required for recruitment of antigen-nonspecific mononuclear cells into the liver by CTLs. J Clin Invest 113: 1158-1167.
45. Sitia G, Iannacone M, Müller S, Bianchi ME, Guidotti LG. 2007. Treatment with HMGB1 inhibitors diminishes CTL-induced liver disease in HBV transgenic mice. J Leukoc Biol 81: 100-107.
46. Sitia G, Iannacone M, Aiolfi R, Isogawa M, van Rooijen N, Scozzesi C, Bianchi ME, Andrian von UH, Chisari FV, Guidotti LG. 2011. Kupffer cells hasten resolution of liver immunopathology in mouse models of viral hepatitis. PLoS Pathog 7: e1002061.
47. Sitia G, Aiolfi R, Di Lucia P, Mainetti M, Fiocchi A, Mingozzi F, Esposito A, Ruggeri ZM, Chisari FV, Iannacone M, et al. 2012. Antiplatelet therapy prevents hepatocellular carcinoma and improves survival in a mouse model of chronic hepatitis B. Proc Natl Acad Sci 109: E2165-E2172.
48. Sprinzl MF, Oberwinkler H, Schaller H, Protzer U. 2001. Transfer of hepatitis B virus genome by adenovirus vectors into cultured cells and mice: Crossing the species barrier. J Virol 75: 5108-5118.
49. SungW-K, Zheng H, Li S, Chen R, Liu X, Li Y, Lee NP, Lee WH, Ariyaratne PN, Tennakoon C, et al. 2012. Genomewide survey of recurrent HBV integration in hepatocellular carcinoma. Nat Genet 44: 765-769.
50. Tsui LV, Guidotti LG, Ishikawa T, Chisari FV. 1995. Posttranscriptional clearance of hepatitis B virus RNA by cytotoxicT lymphocyte-activated hepatocytes. ProcNatlAcad Sci 92: 12398-12402.
51. Washburn ML, Bility MT, Zhang L, Kovalev GI, Buntzman A, Frelinger JA, BarryW, Ploss A, Rice CM, Su L. 2011. A humanized mouse model to study hepatitis C virus infection, immune response, and liver disease. Gastroenterology 140: 1334-1344.
52. Wieland SF, Guidotti LG, Chisari FV. 2000. Intrahepatic induction of α/β interferon eliminates viral RNA-containing capsids in hepatitis B virus transgenic mice. J Virol 74: 4165-4173.
53. Yan H, Zhong G, Xu G, HeW, Jing Z, Gao Z, Huang Y, Qi Y, Peng B, Wang H, et al. 2012. Sodium taurocholate cotransporting polypeptide is a functional receptor for human hepatitis B and D virus. eLife 1: e00049.
54. Yang PL, Althage A, Chung J, Chisari FV. 2002. Hydrodynamic injection of viral DNA: A mouse model of acute hepatitis B virus infection. Proc Natl Acad Sci 99: 13825- 13830.
55. Yang D, Liu L, Zhu D, Peng H, Su L, Fu Y-X, Zhang L. 2013. A mouse model for HBV immunotolerance and immunotherapy. Cell Mol Immunol 11: 71-78.
56. Zhu S, Rezvani M, Harbell J, Mattis AN, Wolfe AR, Benet LZ, Willenbring H, Ding S. 2014. Mouse liver repopulation with hepatocytes generated from human fibroblasts. Nature 508: 93-97