Ineffective CD8 + T-cell immunity to adeno-associated virus can result in prolonged liver injury and fibrogenesis

American Journal of Pathology

Volumn 179, Issue 5, 2011, Pages 2370-2381

  Spahn, Jessica ^a,b   Pierce, Robert H ^c   Crispe, Ian N ^a,b  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b SEATTLE BIOMEDICAL RESEARCH INSTITUTE   (United States)

^c Merck Research Laboratory   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CXCL9 CHEMOKINE; ENHANCED GREEN FLUORESCENT PROTEIN; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 7 RECEPTOR ALPHA; PROGRAMMED DEATH 1 RECEPTOR;

ADENO ASSOCIATED VIRUS; ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD8+ T LYMPHOCYTE; CELL ACTIVATION; CELL COMPARTMENTALIZATION; CELL DIVISION; CELL EXPANSION; CELL KINETICS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DNA VECTOR; FIBROGENESIS; FIBROSIS; FLOW CYTOMETRY; HEPATITIS; IMMUNITY; IMMUNOPATHOLOGY; INFLAMMATION; LEUKOCYTE; LIVER INJURY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA VECTOR; STELLATE CELL; UPREGULATION; VIRUS REPLICATION;

ADENOVIRIDAE INFECTIONS; ADOPTIVE TRANSFER; ALANINE TRANSAMINASE; ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; CHEMOKINE CXCL10; CHEMOKINE CXCL9; GENETIC VECTORS; HEPATITIS, CHRONIC; HEPATITIS, VIRAL, ANIMAL; INTERCELLULAR ADHESION MOLECULE-1; INTERFERON-GAMMA; KUPFFER CELLS; LIVER; LIVER CIRRHOSIS; LYMPHOCYTE ACTIVATION; LYMPHOCYTE TRANSFUSION; MALE; MICE; MICE, INBRED C57BL; PROGRAMMED CELL DEATH 1 RECEPTOR; RNA; TRANSGENES; VASCULAR CELL ADHESION MOLECULE-1;

EID: 80055007453     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2011.08.004     Document Type: Article

References (56)

1. P. Bertolino, D.G. Bowen, G.W. McCaughan, and B. Fazekas de St Groth Antigen-specific primary activation of CD8+ T cells within the liver J Immunol 166 2001 5430 5438
2. Y.C. Lee, L. Lu, F. Fu, W. Li, A.W. Thomson, J.J. Fung, and S. Qian Hepatocytes and liver nonparenchymal cells induce apoptosis in activated T cells Transplant Proc 31 1999 784
3. P. Bertolino, M.C. Trescol-Biemont, and C. Rabourdin-Combe Hepatocytes induce functional activation of naive CD8+ T lymphocytes but fail to promote survival Eur J Immunol 28 1998 221 236
4. S.A. Wuensch, J. Spahn, and I.N. Crispe Direct, help-independent priming of CD8+ T cells by adeno-associated virus-transduced hepatocytes Hepatology 52 2010 1068 1077
5. G. Sass, S. Heinlein, A. Agli, R. Bang, J. Schumann, and G. Tiegs Cytokine expression in three mouse models of experimental hepatitis Cytokine 19 2002 115 120
6. G. Tiegs, J. Hentschel, and A. Wendel A T cell-dependent experimental liver injury in mice inducible by concanavalin A J Clin Invest 90 1992 196 203
7. L.G. G Guidotti, T. Ishikawa, M.V. Hobbs, B. Matzke, R. Schreiber, and F.V. Chisari Intracellular inactivation of the hepatitis B virus by cytotoxic T lymphocytes Immunity 4 1996 25 36
8. R.M. Zinkernagel, E. Haenseler, T. Leist, A. Cerny, H. Hengartner, and A. Althage T cell-mediated hepatitis in mice infected with lymphocytic choriomeningitis virus Liver cell destruction by H-2 class I-restricted virus-specific cytotoxic T cells as a physiological correlate of the 51Cr-release assay? J Exp Med 164 1986 1075 1092
9. S.A. Wuensch, R.H. Pierce, and I.N. Crispe Local intrahepatic CD8+ T cell activation by a non-self-antigen results in full functional differentiation J Immunol 177 2006 1689 1697
10. R.O. Snyder, C.H. Miao, G.A. Patijn, S.K. Spratt, O. Danos, D. Nagy, A.M. Gown, B. Winther, L. Meuse, L.K. Cohen, A.R. Thompson, and M.A. Kay Persistent and therapeutic concentrations of human factor IX in mice after hepatic gene transfer of recombinant AAV vectors Nat Genet 16 1997 270 276
11. J. Gosálvez, E. Rodríguez-Iigo, J.L. Ramiro-Díaz, J. Bartolomé, J.F. Tomás, H. Oliva, and V. Carreo Relative quantification and mapping of hepatitis C virus by in situ hybridization and digital image analysis Hepatology 27 1998 1428 1434
12. M. Giannandrea, R.H. Pierce, and I.N. Crispe Indirect action of tumor necrosis factor-alpha in liver injury during the CD8+ T cell response to an adeno-associated virus vector in mice Hepatology 49 2009 2010 2020
13. K.A. Hogquist, S.C. Jameson, W.R. Heath, J.L. Howard, M.J. Bevan, and F.R. Carbone T cell receptor antagonist peptides induce positive selection Cell 76 1994 17 27
14. V.P. Badovinac, J.S. Haring, and J.T. Harty Initial T cell receptor transgenic cell precursor frequency dictates critical aspects of the CD8(+) T cell response to infection Immunity 26 2007 827 841
15. M. Azadniv, K. Dugger, W.J. Bowers, C. Weaver, and I.N. Crispe Imaging CD8+ T cell dynamics in vivo using a transgenic luciferase reporter Int Immunol 19 2007 1165 1173
16. J.T. Harty, A.R. Tvinnereim, and D.W. White CD8+ T cell effector mechanisms in resistance to infection Annu Rev Immunol 18 2000 275 308
17. H.C. Spangenberg, S. Viazov, N. Kersting, C. Neumann-Haefelin, D. McKinney, M. Roggendorf, F. von Weizscker, H.E. Blum, and R. Thimme Intrahepatic CD8+ T-cell failure during chronic hepatitis C virus infection Hepatology 42 2005 828 837
18. N.H. Gruener, F. Lechner, M.C. Jung, H. Diepolder, T. Gerlach, G. Lauer, B. Walker, J. Sullivan, R. Phillips, G.R. Pape, and P. Klenerman Sustained dysfunction of antiviral CD8+ T lymphocytes after infection with hepatitis C virus J Virol 75 2001 5550 5558
19. P.D. Hodgkin, J.H. Lee, and A.B. Lyons B cell differentiation and isotype switching is related to division cycle number J Exp Med 184 1996 277 281
20. S. Urbani, B. Amadei, D. Tola, M. Massari, S. Schivazappa, G. Missale, and C. Ferrari PD-1 expression in acute hepatitis C (HCV) invection is associated with HCV-specific CD8+ exhaustion J Virol 80 2006 11398 11403
21. B. Bengsch, H.C. Spangenberg, N. Kersting, C. Neumann-Haefelin, E. Panther, F. von Weizscker, H.E. Blum, H. Pircher, and R. Thimme Analysis of CD127 and KLRG1 expression on hepatitis C virus-specific CD8+ T cells reveals the existence of different memory T-cell subsets in the peripheral blood and liver J Virol 81 2007 945 953
22. H. Radziewicz, C.C. Ibegbu, M.L. Fernandez, K.A. Workowski, K. Obideen, M. Wehbi, H.L. Hanson, J.P. Steinberg, D. Masopust, E.J. Wherry, J.D. Altman, B.T. Rouse, G.J. Freeman, R. Ahmed, and A. Grakoui Liver-infiltrating lymphocytes in chronic human hepatitis C virus infection display an exhausted phenotype with high levels of PD-1 and low levels of CD127 expression J Virol 81 2007 2545 2553
23. J.M. Roberts, J.W. Searle, and W.G. Cooksley Histological patterns of prolonged hepatitis C infection Gastroenterol Jpn 28 Suppl 5 1993 37 41
24. N. Bach, S.N. Thung, and F. Schaffner The histological features of chronic hepatitis C and autoimmune chronic hepatitis: a comparative analysis Hepatology 15 1992 572 577
25. F. Liao, R.L. Rabin, J.R. Yannelli, L.G. Koniaris, P. Vanguri, and J.M. Farber Human Mig chemokine: biochemical and functional characterization J Exp Med 182 1995 1301 1314
26. A.D. Luster, J.C. Unkeless, and J.V. Ravetch Gamma-interferon transcriptionally regulates an early-response gene containing homology to platelet proteins Nature 315 1985 672 676
27. D.D. Taub, A.R. Lloyd, K. Conlon, J.M. Wang, J.R. Ortaldo, A. Harada, K. Matsushima, D.J. Kelvin, and J.J. Oppenheim Recombinant human interferon-inducible protein 10 is a chemoattractant for human monocytes and T lymphocytes and promotes T cell adhesion to endothelial cells J Exp Med 177 1993 1809 1814
28. P.L. Shields, C.M. Morland, M. Salmon, S. Qin, S.G. Hubscher, and D.H. Adams Chemokine and chemokine receptor interactions provide a mechanism for selective T cell recruitment to specific liver compartments within hepatitis C-infected liver J Immunol 163 1999 6236 6243
29. C. Hughes, D.K. Male, and P.L. Lantos Adhesion of lymphocytes to cerebral microvascular cells: effects of interferon-gamma, tumour necrosis factor and interleukin-1 Immunology 64 1988 677 681
30. D.C. Look, M.R. Pelletier, and M.J. Holtzman Selective interaction of a subset of interferon-gamma response element-binding proteins with the intercellular adhesion molecule-1 (ICAM-1) gene promoter controls the pattern of expression on epithelial cells J Biol Chem 269 1994 8952 8958
31. P. Dillon, D. Belchis, T. Tracy, R. Cilley, L. Hafer, and T. Krummel Increased expression of intercellular adhesion molecules in biliary atresia Am J Pathol 145 1994 263 267
32. W.Y. Lee, and P. Kubes Leukocyte adhesion in the liver: distinct adhesion paradigm from other organs J Hepatol 48 2008 504 512
33. B. John, and I.N. Crispe Passive and active mechanisms trap activated CD8+ T cells in the liver J Immunol 172 2004 5222 5229
34. D.A. Brenner Molecular pathogenesis of liver fibrosis Trans Am Clin Climatol Assoc 120 2009 361 368
35. E.J. Wherry, J.N. Blattman, K. Murali-Krishna, R. van der Most, and R. Ahmed Viral persistence alters CD8 T-cell immunodominance and tissue distribution and results in distinct stages of functional impairment J Virol 77 2003 4911 4927
36. B. Rehermann Hepatitis C virus versus innate and adaptive immune responses: a tale of coevolution and coexistence J Clin Invest 119 2009 1745 1754
37. W.Z. Mehal, F. Azzaroli, and I.N. Crispe Antigen presentation by liver cells controls intrahepatic T cell trapping, whereas bone marrow-derived cells preferentially promote intrahepatic T cell apoptosis J Immunol 167 2001 667 673
38. D.G. Bowen, A. Warren, T. Davis, M.W. Hoffmann, G.W. McCaughan, B. Fazekas de St Groth, and P. Bertolino Cytokine-dependent bystander hepatitis due to intrahepatic murine CD8 T-cell activation by bone marrow-derived cells Gastroenterology 123 2002 1252 1264
39. B. Perussia, E.T. Dayton, V. Fanning, P. Thiagarajan, J. Hoxie, and G. Trinchieri Immune interferon and leukocyte-conditioned medium induce normal and leukemic myeloid cells to differentiate along the monocytic pathway J Exp Med 158 1983 2058 2080
40. K.L. Hokeness, E.S. Deweerd, M.W. Munks, C.A. Lewis, R.P. Gladue, and T.P. Salazar-Mather CXCR3-dependent recruitment of antigen-specific T lymphocytes to the liver during murine cytomegalovirus infection J Virol 81 2007 1241 1250
41. P. Bertolino, Schrage Arnhild, G. David, Bowen, Kl Katja, P. Bertolino, A. Schrage, D.G. Bowen, K. Klugewitz, S. Ghani, K. Eulenburg, L. Holz, N. Hogg, G.W. McCaughan, and A. Hamann Early intrahepatic antigen-specific retention of naive CD8+ T cells is predominantly ICAM-1/LFA-1 dependent in mice Hepatology 42 2005 1063 1071
42. N.K. Polakos, J.C. Cornejo, D.A. Murray, K.O. Wright, J.J. Treanor, I.N. Crispe, D.J. Topham, and R.H. Pierce Kupffer cell-dependent hepatitis occurs during influenza infection Am J Pathol 168 2006 1169 1178
43. R. Higashiyama, Y. Inagaki, Y.Y. Hong, M. Kushida, S. Nakao, M. Niioka, T. Watanabe, H. Okano, Y. Matsuzaki, G. Shiota, and I. Okazaki Bone marrow-derived cells express matrix metalloproteinases and contribute to regression of liver fibrosis in mice Hepatology 45 2007 213 222
44. Y.O. Kweon, Z.D. Goodman, J.L. Dienstag, E.R. Schiff, N.A. Brown, E. Burchardt, R. Schoonhoven, D.A. Brenner, and M.W. Fried Decreasing fibrogenesis: an immunohistochemical study of paired liver biopsies following lamivudine therapy for chronic hepatitis B J Hepatol 35 2001 749 755
45. J.L. Dienstag, R.D. Goldin, E.J. Heathcote, H.W. Hann, M. Woessner, S.L. Stephenson, S. Gardner, D.F. Gray, and E.R. Schiff Histological outcome during long-term lamivudine therapy Gastroenterology 124 2003 105 117
46. Y. Shiratori, F. Imazeki, M. Moriyama, M. Yano, Y. Arakawa, O. Yokosuka, T. Kuroki, S. Nishiguchi, M. Sata, G. Yamada, S. Fujiyama, H. Yoshida, and M. Omata Histologic improvement of fibrosis in patients with hepatitis C who have sustained response to interferon therapy Ann Intern Med 132 2000 517 524
47. T. Poynard, J. McHutchison, M. Manns, C. Trepo, K. Lindsay, Z. Goodman, M.H. Ling, and J. Albrecht Impact of pegylated interferon alfa-2b and ribavirin on liver fibrosis in patients with chronic hepatitis C Gastroenterology 122 2002 1303 1313
48. P. Farci, T. Roskams, L. Chessa, G. Peddis, A.P. Mazzoleni, R. Scioscia, G. Serra, M.E. Lai, M. Loy, L. Caruso, V. Desmet, R.H. Purcell, and A. Balestrieri Long-term benefit of interferon alpha therapy of chronic hepatitis D: regression of advanced hepatic fibrosis Gastroenterology 126 2004 1740 1749
49. J.P. Iredale, R.C. Benyon, J. Pickering, M. McCullen, M. Northrop, S. Pawley, C. Hovell, and M.J. Arthur Mechanisms of spontaneous resolution of rat liver fibrosis Hepatic stellate cell apoptosis and reduced hepatic expression of metalloproteinase inhibitors J Clin Invest 102 1998 538 549
50. J.R. Larrubia, S. Benito-Martínez, J. Miquel, M. Calvino, E. Sanz-de-Villalobos, and T. Parra-Cid Costimulatory molecule programmed death-1 in the cytotoxic response during chronic hepatitis C World J Gastroenterol 15 2009 5129 5140
51. X.S. Liang, Y. Zhou, C.Z. Li, and M.B. Wan Natural course of chronic hepatitis B is characterized by changing patterns of programmed death type-1 of CD8-positive T cells World J Gastroenterol 16 2010 618 624
52. A. Dolganiuc, O. Norkina, K. Kodys, D. Catalano, G. Bakis, C. Marshall, P. Mandrekar, and G. Szabo Viral and host factors induce macrophage activation and loss of toll-like receptor tolerance in chronic HCV infection Gastroenterology 133 2007 1627 1636
53. K.J. Helbig, A. Ruszkiewicz, R.E. Lanford, M.D. Berzsenyi, H.A. Harley, S.R. McColl, and M.R. Beard Differential expression of the CXCR3 ligands in chronic hepatitis C virus (HCV) infection and their modulation by HCV in vitro J Virol 83 2009 836 846
54. A. Boonstra, L.J. van der Laan, T. Vanwolleghem, and H.L. Janssen Experimental models for hepatitis C viral infection Hepatology 50 2009 1646 1655
55. C. Neumann-Haefelin, Hans Christian Spangenberg, Hubert E. Blum, and Robert Thimme Host and viral factors contributing to CD8+ T cell failure in hepatitis C virus infection World J Gastroenterol 13 2007 4839 4847
56. N.H. Gruner, T.J. Gerlach, M.C. Jung, H.M. Diepolder, C.A. Schirren, W.W. Schraut, R. Hoffmann, R. Zachoval, T. Santantonio, M. Cucchiarini, A. Cerny, and G.R. Pape Association of hepatitis C virus-specific CD8+ T cells with viral clearance in acute hepatitis C J Infect Dis 181 2000 1528 1536