Animal model for study of human hepatitis viruses

Journal of Gastroenterology and Hepatology (Australia)

Volumn 26, Issue 1, 2011, Pages 13-18

  Chayama, Kazuaki ^a,b   Hayes, C Nelson ^a,b   Hiraga, Nobuhiko ^a,b   Abe, Hiromi ^a,b   Tsuge, Masataka ^a,b   Imamura, Michio ^a,b  

^a HIROSHIMA UNIVERSITY   (Japan)

^b Liver Research Project Center   (Japan)

Author keywords

Hepatitis B virus; Hepatitis C virus; UPA scid mouse model

Indexed keywords

ALPHA INTERFERON; ALPHA2B INTERFERON; CILUPREVIR; GANCICLOVIR; INTERFERON; LAMIVUDINE; TELAPREVIR; THYMIDINE KINASE 1; UROKINASE;

ANTIVIRAL THERAPY; ARTICLE; BYSTANDER EFFECT; CARDIOTOXICITY; CELL PROLIFERATION; CHIMERA; COMPETITIVE INHIBITION; DRUG METABOLISM; EXPERIMENTAL MODEL; HALF LIFE TIME; HEPATITIS B; HEPATITIS B VIRUS; HEPATITIS C; HEPATITIS C VIRUS; HEPATOCYTE TRANSPLANTATION; HERPES SIMPLEX VIRUS 1; HUMAN; IMMUNOCOMPETENT CELL; NONHUMAN; PRIORITY JOURNAL; SCID MOUSE; TRANSGENIC MOUSE; VIRUS INFECTIVITY; VIRUS REPLICATION; VIRUS STRAIN; VIRUS TRANSMISSION;

EID: 78650409662     PISSN: 08159319     EISSN: 14401746     Source Type: Journal    
DOI: 10.1111/j.1440-1746.2010.06470.x     Document Type: Article

References (72)

1. Shepard CW, Simard EP, Finelli L, Flore AE, Bell BP. Hepatitis B virus infection: epidemiology and vaccination. Epidemiol. Rev. 2006; 28: 112-25.
2. Sy T, Jamal MM. Epidemiology of Hepatitis C Virus (HCV) infection. Int. J. Med. Sci. 2006; 3: 41-6.
3. Yuen MF, Hou JL, Chutaputti A, Prevent APWP. Hepatocellular carcinoma in the Asia pacific region. J. Gastroenterol. Hepatol. 2009; 24: 346-53.
4. Guidotti LG, Matzke B, Schaller H, Chisari FV. High-level Hepatitis-B Virus-replication in transgenic mice. J. Virol. 1995; 69: 6158-69.
5. Weber O, Schlemmer KH, Hartmann E et al. Inhibition of human hepatitis B virus (HBV) by a novel non-nucleosidic compound in a transgenic mouse model. Antiviral Res. 2002; 54: 69-78.
6. Julander JG, Sidwell RW, Morrey JD. Characterizing antiviral activity of adefovir dipivoxil in transgenic mice expressing hepatitis B virus. Antiviral Res. 2002; 55: 27-40.
7. Julander JG, Colonno RJ, Sidwell RW, Morrey JD. Characterization of antiviral activity of entecavir in transgenic mice expressing hepatitis B virus. Antiviral Res. 2003; 59: 155-61.
8. Uprichard SL, Boyd B, Althage A, Chisari FV. Clearance of hepatitis B virus from the liver of transgenic mice by short hairpin RNA. Proc. Natl. Acad. Sci U S A 2005; 102: 773-8.
9. Ilan E, Burakova T, Dagan S et al. The hepatitis B virus-trimera mouse: a model for human HBV infection and evaluation of Anti-HBV therapeutic agents. Hepatology 1999; 29: 553-62.
10. Ilan E, Arazi J, Nussbaum O et al. The hepatitis C virus (HCV)-Trimera mouse: a model for evaluation of agents against HCV. J. Infect. Dis. 2002; 185: 153-61.
11. Heckel JL, Sandgren EP, Degen JL, Palmiter RD, Brinster RL. Neonatal bleeding in transgenic mice expressing urokinase-type plasminogen-activator. Cell 1990; 62: 447-56.
12. Rhim JA, Sandgren EP, Palmiter RD, Brinster RL. Complete reconstitution of mouse-liver with xenogeneic hepatocytes. Proc. Natl. Acad Sci U S A 1995; 92: 4942-6.
13. Tsuge M, Hiraga N, Takaishi H et al. Infection of human hepatocyte chimeric mouse with genetically engineered hepatitis B virus. Hepatology 2005; 42: 1046-54.
14. Hiraga N, Imamura M, Tsuge M et al. Infection of human hepatocyte chimeric mouse with genetically engineered Hepatitis C Virus and its susceptibility to interferon. FEBS Lett. 2007; 581: 1983-7.
15. Kimura T, Imamura M, Hiraga N et al. Establishment of an infectious genotype 1b Hepatitis C Virus clone in human hepatocyte chimeric mice. J.l Gen. Virol. 2008; 89: 2108-13.
16. Dandri M, Burda MR, Torok E et al. Repopulation of mouse liver with human hepatocytes and in vivo infection with hepatitis B virus. Hepatology 2001; 33: 981-8.
17. Mercer DF, Schiller DE, Elliott JF et al. Hepatitis C virus replication in mice with chimeric human livers. Nat. Med. 2001; 7: 927-33.
18. Douglas DN, Kawahara T, Sis B et al. therapeutic efficacy of human hepatocyte transplantation in a SCID/uPA mouse model with inducible liver disease. PLoS ONE 2010; 5: e9209.
19. Tateno C, Yoshizane Y, Saito N et al. Near completely humanized liver in mice shows human-type metabolic responses to drugs. Am. J. Pathol. 2004; 165: 901-12.
20. Bissig KD, Wieland SF, Tran P et al. Human liver chimeric mice provide a model for hepatitis B and C virus infection and treatment. J. Clin. Invest. 2010; 120: 924-30.
21. Yu AM, Idle JR, Gonzalez FJ. Polymorphic cytochrome p450 2D6: humanized mouse model and endogenous substrates. Drug. Metab. Rev. 2004; 36: 243-77.
22. Katoh M, Sawada T, Soeno Y et al. In vivo drug metabolism model for human cytochrome P450 enzyme using chimeric mice with humanized liver. J. Pharm. Sci.-Us. 2007; 96: 428-37.
23. Katoh M, Matsui T, Nakajima M et al. In vivo induction of human cytochrome P450 enzymes expressed in chimeric mice with humanized liver. Drug. Metab. Dispos. 2005; 33: 754-63.
24. Katoh M, Matsui T, Okumura H et al. Expression of human phase II enzymes in chimeric mice with humanized liver. Drug. Metab. Dispos. 2005; 33: 1333-40.
25. Okumura H, Katoh M, Sawada T et al. Humanization of excretory pathway in chimeric mice with humanized liver. Toxicol. Sci. 2007; 97: 533-8.
26. Shoda J, Okada K, Inada Y et al. Bezafibrate induces multidrug-resistance P-Glycoprotein 3 expression in cultured human hepatocytes and humanized livers of chimeric mice. Hepatol. Res. 2007; 37: 548-56.
27. Petersen J, Burda MR, Dandri M, Rogler CE. Transplantation of human hepatocytes in immunodeficient UPA mice: a model for the study of hepatitis B virus. Methods Mol. Med. 2004; 96: 253-60.
28. Yoshizato K, Tateno C. A human hepatocyte-bearing mouse: an animal model to predict drug metabolism and effectiveness in humans. PPAR Res. 2009; 2009: 476217.
29. Yoshizato K, Tateno C, Utoh R. The mechanism of liver size control in mammals: a novel animal study. Int. J. Design & Nature Ecodynamics 2009; 4: 123-42.
30. Utoh R, Tateno C, Yamasaki C et al. Susceptibility of chimeric mice with livers repopulated by serially subcultured human hepatocytes to hepatitis B virus. Hepatology 2008; 47: 435-46.
31. Meuleman P, Leroux-Roels G. The human liver-uPA-SCID mouse: a model for the evaluation of antiviral compounds against HBV and HCV. Antiviral Res. 2008; 80: 231-8.
32. Dandri M, Lutgehetmann M, Volz T, Petersen J. Small animal model systems for studying Hepatitis B Virus replication and pathogenesis. Semin. Liver Dis. 2006; 26: 181-91.
33. Dandri M, Volz TK, Lutgehetmann M, Petersen J. Animal models for the study of HBV replication and its variants. J. Clin. Virol. 2005; 34 (Suppl. 1): S54-62.
34. Barth H, Robinet E, Liang TJ, Baumert TF. Mouse models for the study of HCV infection and virus-host interactions. J. Hepatol. 2008; 49: 134-42.
35. Kneteman NM, Toso C. In vivo study of HCV in mice with chimeric human livers. Methods Mol. Biol. 2009; 510: 383-99.
36. Meuleman P, Libbrecht L, De Vos R et al. Morphological and biochemical characterization of a human liver in a uPA-SCID mouse chimera. Hepatology 2005; 41: 847-56.
37. Sugiyama M, Tanaka Y, Kato T et al. Influence of hepatitis B virus genotypes on the intra- and extracellular expression of viral DNA and antigens. Hepatology 2006; 44: 915-24.
38. Tsuge M, Hiraga N, Akiyama R et al. HBx protein is indispensable for development of viremia in human hepatocyte chimeric mice. J. Gen. Virol. 2010.
39. Meuleman P, Libbrecht L, Wieland S et al. Immune suppression uncovers endogenous cytopathic effects of the hepatitis B virus. J. Virol. 2006; 80: 2797-807.
40. Sugiyama M, Tanaka Y, Kurbanov F et al. Direct cytopathic effects of particular hepatitis B virus genotypes in severe combined immunodeficiency transgenic with urokinase-type plasminogen activator mouse with human hepatocytes. Gastroenterology 2009; 136: 652-62.
41. Tanaka Y, Sanchez LV, Sugiyama M et al. Characteristics of Hepatitis B Virus genotype G coinfected with genotype H in chimeric mice carrying human hepatocytes. Virology 2008; 376: 408-15.
42. Tatematsu K, Tanaka Y, Kurbanov F et al. A genetic variant of Hepatitis B Virus divergent from known human and ape genotypes isolated from a Japanese patient and provisionally assigned to new genotype J. J. Virol. 2009; 83: 10538-47.
43. Tabuchi A, Tanaka J, Katayama K et al. Titration of Hepatitis B Virus infectivity in the sera of pre-acute and late acute phases of HBV infection: transmission experiments to chimeric mice with human liver repopulated hepatocytes. J. Med. Virol. 2008; 80: 2064-8.
44. Noguchi C, Imamura M, Tsuge M et al. G-to-A Hypermutation in Hepatitis B Virus (HBV) and clinical course of patients with chronic HBV infection. J. Infect. Dis. 2009; 199: 1599-607.
45. Dandri M, Murray JM, Lutgehetmann M, Volz T, Lohse AW, Petersen J. Virion half-life in chronic hepatitis B infection is strongly correlated with levels of viremia. Hepatology 2008; 48: 1079-86.
46. Hiraga N, Imamura M, Hatakeyama T et al. Absence of viral interference and different susceptibility to interferon between Hepatitis B Virus and Hepatitis C Virus in human hepatocyte chimeric mice. J. Hepatol. 2009; 51: 1046-54.
47. Dandri M, Burda MR, Zuckerman DM et al. Chronic infection with Hepatitis B Viruses and antiviral drug evaluation in uPA mice after liver repopulation with tupaia hepatocytes. J. Hepatol. 2005; 42: 54-60.
48. Yatsuji H, Noguchi C, Hiraga N et al. Emergence of a novel lamivudine-resistant hepatitis B virus variant with a substitution outside the YMDD motif. Antimicrob. Agents Chemother. 2006; 50: 3867-74.
49. Petersen J, Dandri M, Mier W et al. Prevention of Hepatitis B Virus infection in vivo by entry inhibitors derived from the large envelope protein. Nat. Biotechnol. 2008; 26: 335-41.
50. Turrini P, Sasso R, Germoni S et al. Development of humanized mice for the study of hepatitis C virus infection. Transplant. Proc. 2006; 38: 1181-4.
51. Cagnon L, Wagaman P, Bartenschlager R et al. Application of the trak-C (TM) HCV core assay for monitoring antiviral activity in HCV replication systems. J. Virol. Methods 2004; 118: 23-31.
52. Kurbanov F, Tanaka Y, Chub E et al. Molecular epidemiology and interferon susceptibility of the natural recombinant Hepatitis C Virus Strain RF1-2k/1b. J. Infect. Dis. 2008; 198: 1448-56.
53. Wakita T, Pietschmann T, Kato T et al. Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat. Med. 2005; 11: 791-6.
54. Grove J, Huby T, Stamataki Z et al. Scavenger receptor BI and BII expression levels modulate Hepatitis C Virus infectivity. J. Virol. 2007; 81: 3162-9.
55. Lindenbach BD, Meuleman P, Ploss A et al. Cell culture-grown Hepatitis C Virus is infectious in vivo and can be recultured in vitro. Proc. Natl. Acad. Sci. U S A 2006; 103: 3805-9.
56. Kaul A, Woerz I, Meuleman P, Leroux-Roels G, Bartenschlager R. Cell culture adaptation of Hepatitis C Virus and in vivo viability of an adapted variant. J. Virol. 2007; 81: 13168-79.
57. Vassilaki N, Friebe P, Meuleman P et al. Role of the Hepatitis C Virus Core+1 open reading frame and core cis-acting RNA Elements in Viral RNA translation and replication. J. Virol. 2008; 82: 11503-15.
58. Meuleman P, Hesselgesser J, Paulson M et al. Anti-CD81 antibodies can prevent a Hepatitis C Virus infection in vivo. Hepatology 2008; 48: 1761-8.
59. Vanwolleghem T, Bukh J, Meuleman P et al. Polyclonal immunoglobulins from a chronic Hepatitis C Virus patient protect human liver-chimeric mice from infection with a homologous Hepatitis C Virus strain. Hepatology 2008; 47: 1846-55.
60. Matsumura T, Hu ZY, Kato T et al. Amphipathic DNA polymers inhibit Hepatitis C Virus infection by blocking viral entry. Gastroenterology 2009; 137: 673-81.
61. Law M, Maruyama T, Lewis J et al. Broadly neutralizing antibodies protect against Hepatitis C Virus quasispecies challenge. Nat. Med. 2008; 14: 25-7.
62. Walters KA, Joyce MA, Thompson JC et al. Application of functional genomics to the chimeric mouse model of HCV infection: optimization of microarray protocols and genomics analysis. Virol. J. 2006; 3: 37-44.
63. Walters KA, Joyce MA, Thompson JC et al. Host-specific response to HCV infection in the chimeric SCID-beige/Alb-uPA mouse model: role of the innate antiviral immune response. PLoS Pathog. 2006; 2: 591-602.
64. Joyce MA, Walters KA, Lamb SE et al. HCV Induces Oxidative and ER Stress, and Sensitizes Infected Cells to Apoptosis in SCID/Alb-uPA Mice. PLoS Pathog. 2009; 5: e10000291.
65. Kneteman NM, Weiner AJ, O'Connell J et al. Anti-HCV therapies in chimeric scid-Alb/uPA mice parallel outcomes in human clinical application. Hepatology 2006; 43: 1346-53.
66. Hsu EC, Hsi B, Hirota-Tsuchihara M et al. Modified apoptotic molecule (BID) reduces hepatitis C virus infection in mice with chimeric human livers. Nat. Biotechnol. 2003; 21: 519-25.
67. Umehara T, Sudoh M, Yasui F et al. Serine palmitoyltransferase inhibitor suppresses HCV replication in a mouse model. Biochem. Biophys. Res. Commun. 2006; 346: 67-73.
68. Laporte MG, Jackson RW, Draper TL et al. The discovery of pyrano[3, 4-b]indole-based allosteric inhibitors of HCV NS5B polymerase with in vivo activity. Med. Chem. 2008; 3: 1508-15.
69. Kneteman NM, Howe AYM, Gao TJ et al. HCV796: a selective nonstructural protein 5B polymerase inhibitor with potent Anti-Hepatitis C Virus activity in vitro, in mice with chimeric human livers, and in humans infected with Hepatitis C Virus. Hepatology 2009; 49: 745-52.
70. Ohira M, Ishiyama K, Tanaka Y et al. Adoptive immunotherapy with liver allograft-derived lymphocytes induces anti-HCV activity after liver transplantation in humans and humanized mice. J. Clin. Invest. 2009; 119: 3226-35.
71. Kamiya N, Iwao E, Hiraga N et al. Practical Evaluation of a Mouse with Chimeric Human Liver Model for Hepatitis C Virus Infection Using an NS3-4A Protease Inhibitor. J. Gen. Virol. 2010; 91: 1668-77.
72. Vanwolleghem T, Meuleman P, Libbrecht L et al. Ultra-rapid cardiotoxicity of the hepatitis C virus protease inhibitor BILN 2061 in the urokinase-type plasminogen activator mouse. Gastroenterology 2007; 133: 1144-55.