An Inducible Transgenic Mouse Model for Immune Mediated Hepatitis Showing Clearance of Antigen Expressing Hepatocytes by CD8+ T Cells

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Cebula, Marcin ^a   Ochel, Aaron ^a   Hillebrand, Upneet ^a   Pils, Marina C ^a   Schirmbeck, Reinhold ^b   Hauser, Hansjörg ^a   Wirth, Dagmar ^a  

^a HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

^b UNIVERSITY HOSPITAL ULM   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

OVALBUMIN; TAMOXIFEN;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; CD8+ T LYMPHOCYTE; CELL INTERACTION; CONTROLLED STUDY; DISEASE COURSE; HEPATITIS; IMMUNE RESPONSE; IMMUNOREGULATION; LIVER CELL; LIVER INJURY; MORTALITY; MOUSE; NONHUMAN; RELAPSE; TISSUE SPECIFICITY; TRANSGENIC MOUSE;

ANIMALS; ANTIGENS; CD8-POSITIVE T-LYMPHOCYTES; DISEASE MODELS, ANIMAL; FEMALE; HEPATITIS; HEPATOCYTES; LYMPHOCYTE ACTIVATION; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MODELS, IMMUNOLOGICAL; OVALBUMIN; TAMOXIFEN;

EID: 84880263137     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0068720     Document Type: Article

References (32)

1. Crispe IN, (2003) Hepatic T cells and liver tolerance. Nat Rev Immunol 3: 51-62. doi:10.1038/nri981. PubMed: 12511875.
2. Thomson AW, Knolle PA, (2010) Antigen-presenting cell function in the tolerogenic liver environment. Nat Rev Immunol 10: 753-766. doi:10.1038/nri2858. PubMed: 20972472.
3. Bertolino P, Bowen DG, McCaughan GW, Fazekas de St Groth B, (2001) Antigen-specific primary activation of CD8+ T cells within the liver. J Immunol 166: 5430-5438. PubMed: 11313380.
4. Rehermann B, Nascimbeni M, (2005) Immunology of hepatitis B virus and hepatitis C virus infection. Nat Rev Immunol 5: 215-229. doi:10.1038/nri1573. PubMed: 15738952.
5. Wirth S, Guidotti LG, Ando K, Schlicht HJ, Chisari FV, (1995) Breaking tolerance leads to autoantibody production but not autoimmune liver disease in hepatitis B virus envelope transgenic mice. J Immunol 154: 2504-2515. PubMed: 7868916.
6. Voehringer D, Blaser C, Grawitz AB, Chisari FV, Buerki K, et al. (2000) Break of T cell ignorance to a viral antigen in the liver induces hepatitis. J Immunol 165: 2415-2422. PubMed: 10946266.
7. Derkow K, Loddenkemper C, Mintern J, Kruse N, Klugewitz K, et al. (2007) Differential priming of CD8 and CD4 T-cells in animal models of autoimmune hepatitis and cholangitis. Hepatology 46: 1155-1165. doi:10.1002/hep.21796. PubMed: 17657820.
8. Zierden M, Kühnen E, Odenthal M, Dienes HP, (2010) Effects and regulation of autoreactive CD8+ T cells in a transgenic mouse model of autoimmune hepatitis. Gastroenterology 139: 975-986, e971-973. doi:10.1053/j.gastro.2010.05.075. PubMed: 20639127.
9. Ernst E, Schönig K, Bugert JJ, Bläker H, Pfaff E, et al. (2007) Generation of inducible hepatitis C virus transgenic mouse lines. J Med Virol 79: 1103-1112. doi:10.1002/jmv.20911. PubMed: 17596832.
10. Wakita T, Katsume A, Kato J, Taya C, Yonekawa H, et al. (2000) Possible role of cytotoxic T cells in acute liver injury in hepatitis C virus cDNA transgenic mice mediated by Cre/loxP system. J Med Virol 62: 308-317. doi:10.1002/1096-9071(200011)62:3. PubMed: 11055240.
11. Stabenow D, Frings M, Trück C, Gärtner K, Förster I, et al. (2010) Bioluminescence imaging allows measuring CD8 T cell function in the liver. Hepatology 51: 1430-1437. doi:10.1002/hep.23575. PubMed: 20373369.
12. 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 U S A 99: 13825-13830. doi:10.1073/pnas.202398599. PubMed: 12374864.
13. Stiffler JD, Nguyen M, Sohn JA, Liu C, Kaplan D, et al. (2009) Focal distribution of hepatitis C virus RNA in infected livers. PLOS ONE 4: e6661. doi:10.1371/journal.pone.0006661. PubMed: 19688046.
14. Hartman ZC, Kiang A, Everett RS, Serra D, Yang XY, et al. (2007) Adenovirus infection triggers a rapid, MyD88-regulated transcriptome response critical to acute-phase and adaptive immune responses in vivo. J Virol 81: 1796-1812. doi:10.1128/JVI.01936-06. PubMed: 17121790.
15. Rácz Z, Godó M, Révész C, Hamar P, (2011) Immune activation and target organ damage are consequences of hydrodynamic treatment but not delivery of naked siRNAs in mice. Nucleic Acid Ther 21: 215-224. PubMed: 21749298.
16. Sandhu U, Cebula M, Behme S, Riemer P, Wodarczyk C, et al. (2011) Strict control of transgene expression in a mouse model for sensitive biological applications based on RMCE compatible ES cells. Nucleic Acids Res 39: e1. doi:10.1093/nar/gkq742. PubMed: 20935052.
17. Schuler M, Dierich A, Chambon P, Metzger D, (2004) Efficient temporally controlled targeted somatic mutagenesis in hepatocytes of the mouse. Genesis 39: 167-172. doi:10.1002/gene.20039. PubMed: 15282742.
18. Imayoshi I, Ohtsuka T, Metzger D, Chambon P, Kageyama R, (2006) Temporal regulation of Cre recombinase activity in neural stem cells. Genesis 44: 233-238. doi:10.1002/dvg.20212. PubMed: 16652364.
19. Valitutti S, Müller S, Salio M, Lanzavecchia A, (1997) Degradation of T cell receptor (TCR)-CD3-zeta complexes after antigenic stimulation. J Exp Med 185: 1859-1864. doi:10.1084/jem.185.10.1859. PubMed: 9151711.
20. Boni C, Fisicaro P, Valdatta C, Amadei B, Di Vincenzo P, et al. (2007) Characterization of hepatitis B virus (HBV)-specific T-cell dysfunction in chronic HBV infection. J Virol 81: 4215-4225. doi:10.1128/JVI.02844-06. PubMed: 17287266.
21. Golden-Mason L, Palmer B, Klarquist J, Mengshol JA, Castelblanco N, et al. (2007) Upregulation of PD-1 expression on circulating and intrahepatic hepatitis C virus-specific CD8+ T cells associated with reversible immune dysfunction. J Virol 81: 9249-9258. doi:10.1128/JVI.00409-07. PubMed: 17567698.
22. Thimme R, Bukh J, Spangenberg HC, Wieland S, Pemberton J, et al. (2002) Viral and immunological determinants of hepatitis C virus clearance, persistence, and disease. Proc Natl Acad Sci U S A 99: 15661-15668. doi:10.1073/pnas.202608299. PubMed: 12441397.
23. Chisari FV, Isogawa M, Wieland SF, (2010) Pathogenesis of hepatitis B virus infection. Pathol Biol (Paris) 58: 258-266. doi:10.1016/j.patbio.2009.11.001.
24. Thimme R, Wieland S, Steiger C, Ghrayeb J, Reimann KA, et al. (2003) CD8(+) T cells mediate viral clearance and disease pathogenesis during acute hepatitis B virus infection. J Virol 77: 68-76. doi:10.1128/JVI.77.1.68-76.2003. PubMed: 12477811.
25. Holz LE, Benseler V, Bowen DG, Bouillet P, Strasser A, et al. (2008) Intrahepatic murine CD8 T-cell activation associates with a distinct phenotype leading to Bim-dependent death. Gastroenterology 135: 989-997. doi:10.1053/j.gastro.2008.05.078. PubMed: 18619445.
26. Wuensch SA, Pierce RH, Crispe IN, (2006) Local intrahepatic CD8+ T cell activation by a non-self-antigen results in full functional differentiation. J Immunol 177: 1689-1697. PubMed: 16849478.
27. Lopes AR, Kellam P, Das A, Dunn C, Kwan A, et al. (2008) Bim-mediated deletion of antigen-specific CD8 T cells in patients unable to control HBV infection. J Clin Invest 118: 1835-1845. doi:10.1172/JCI33402. PubMed: 18398508.
28. Maier H, Isogawa M, Freeman GJ, Chisari FV, (2007) PD-1:PD-L1 interactions contribute to the functional suppression of virus-specific CD8+ T lymphocytes in the liver. J Immunol 178: 2714-2720. PubMed: 17312113.
29. Wieland SF, Chisari FV, (2005) Stealth and cunning: hepatitis B and hepatitis C viruses. J Virol 79: 9369-9380. doi:10.1128/JVI.79.15.9369-9380.2005. PubMed: 16014900.
30. Postic C, Shiota M, Niswender KD, Jetton TL, Chen Y, et al. (1999) Dual roles for glucokinase in glucose homeostasis as determined by liver and pancreatic beta cell-specific gene knockouts using Cre recombinase. J Biol Chem 274: 305-315. doi:10.1074/jbc.274.1.305. PubMed: 9867845.
31. Hogquist KA, Jameson SC, Heath WR, Howard JL, Bevan MJ, et al. (1994) T cell receptor antagonist peptides induce positive selection. Cell 76: 17-27. doi:10.1016/0092-8674(94)90169-4. PubMed: 8287475.
32. Wahl C, Bochtler P, Schirmbeck R, Reimann J, (2007) Type I IFN-producing CD4 Valpha14i NKT cells facilitate priming of IL-10-producing CD8 T cells by hepatocytes. J Immunol 178: 2083-2093. PubMed: 17277112.