Antiviral antibodies are necessary to prevent cytotoxic T-lymphocyte escape in mice infected with a coronavirus

Journal of Virology

Volumn 81, Issue 24, 2007, Pages 13291-13298

  Butler, Noah S ^a   Dandekar, Ajai A ^a,b   Perlman, Stanley ^a  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

VIRUS ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ARTICLE; CLEARANCE; COMPARATIVE STUDY; CONTROLLED STUDY; CORONAVIRUS; CYTOTOXIC T LYMPHOCYTE; LYMPHOCYTE DEPLETION; MOUSE; NONHUMAN; PRIORITY JOURNAL; VIRUS INFECTION; VIRUS REPLICATION;

ANIMALS; ANIMALS, SUCKLING; ANTIBODIES, VIRAL; CORONAVIRUS INFECTIONS; ENCEPHALOMYELITIS; EPITOPES, T-LYMPHOCYTE; FEMALE; HUMANS; IMMUNODOMINANT EPITOPES; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MURINE HEPATITIS VIRUS; MUTATION; T-LYMPHOCYTES, CYTOTOXIC;

CORONAVIRUS; MUS;

EID: 37048999985     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01580-07     Document Type: Article

References (45)

1. AbuAttieh, M., M. Rebrovich, P. J. Wettstein, Z. Vuk-Pavlovic, A. H. Limper, J. L. Platt, and M. Cascalho. 2007. Fitness of cell-mediated immunity independent of repertoire diversity. J. Immunol. 178:2950-2960.
2. Barouch, D. H., J. Kunstman, M. J. Kuroda, J. E. Schmitz, S. Santra, F. W. Peyerl, G. R. Krivulka, K. Beaudry, M. A. Lifton, D. A. Gorgone, D. C. Monteflori, M. G. Lewis, S. M. Wolinsky, and N. L. Letvin. 2002. Eventual AIDS vaccine failure in a rhesus monkey by viral escape from cytotoxic T lymphocytes. Nature 415:335-339.
3. Bergmann, C. C., C. Ramakrishna, M. Kornacki, and S. A. Stohlman. 2001. Impaired T cell immunity in B cell-deficient mice following viral central nervous system infection. J. Immunol. 167:1575-1583.
4. Betts, M. R., J. M. Brenchley, D. A. Price, S. C. De Rosa, D. C. Douek, M. Roederer, and R. A. Roup. 2003. Sensitive and viable identification of anti-gen-specific CD8+ T cells by a flow cytometric assay for degranulation. J. Immunol. Methods 281:65-78.
5. Bowen, D. G., and C. M. Walker. 2005. Mutational escape from CD8+ T cell immunity: HCV evolution, from chimpanzees to man. J. Exp. Med. 201: 1709-1714.
6. Castro, R. F., G. D. Evans, A. Jaszewski, and S. Perlman. 1994. Coronavirus-induced demyelination occurs in the presence of virus-specific cytotoxic T cells. Virology 200:733-743.
7. Chen, M., M. Sallberg, A. Sonnerborg, O. Weiland, L. Mattsson, L. Jin, A. Birkett, D. Peterson, and D. R. Milich. 1999. Limited humoral immunity in hepatitis C virus infection. Gastroenterology 116:135-143.
8. Cheng-Mayer, C., and J. A. Levy. 1988. Distinct biological and serological properties of human immunodeficiency viruses from the brain. Ann. Neurol. 23(Suppl.):S58-S61.
9. Cox, A. L., T. Mosbruger, Q. Mao, Z. Liu, X. H. Wang, H. C. Yang, J. Sidney, A. Sette, D. Pardoll, D. L. Thomas, and S. C. Ray. 2005. Cellular immune selection with hepatitis C virus persistence in humans. J. Exp. Med. 201: 1741-1752.
10. Dandekar, A. A., G. Jacobsen, T. J. Waldschmidt, and S. Perlman. 2003. Antibody-mediated protection against cytotoxic T-cell escape in coronavirus-induced demyelination. J. Virol. 77:11867-11874.
11. Draenert, R., S. Le Gall, K. J. Pfafferott, A. J. Leslie, P. Chetty, C. Brander, E. C. Holmes, S. C. Chang, M. E. Feeney, M. M. Addo, L. Ruiz, D. Ramduth, P. Jeena, M. Altfeld, S. Thomas, Y. Tang, C. L. Verrill, C. Dixon, J. G. Prado, P. Kiepiela, J. Martinez-Picado, B. D. Walker, and P. J. Goulder. 2004. Immune selection for altered antigen processing leads to cytotoxic T lymphocyte escape in chronic HIV-1 infection. J. Exp. Med. 199:905-915.
12. Erickson, A. L., Y. Kimura, S. Igarashi, J. Eichelberger, M. Houghton, J. Sidney, D. McKinney, A. Sette, A. L. Hughes, and C. M. Walker. 2001. The outcome of hepatitis C virus infection is predicted by escape mutations in epitopes targeted by cytotoxic T lymphocytes. Immunity 15:883-895.
13. Friedrich, T. C., E. J. Dodds, L. J. Yant, L. Vojnov, R. Rudersdorf, C. Cullen, D. T. Evans, R. C. Desrosiers, B. R. Mothe, J. Sidney, A. Sette, K. Kunstman, S. Wolinsky, M. Piatak, J. Lifson, A. L. Hughes, N. Wilson, D. H. O'Connor, and D. I. Watkins. 2004. Reversion of CTL escape-variant immunodeficiency viruses in vivo. Nat. Med. 10:275-281.
14. Goulder, P. J., R. E. Phillips, R. A. Colbert, S. McAdam, G. Ogg, M. A. Nowak, P. Giangrande, G. Luzzi, B. Morgan, A. Edwards, A. J. McMichael, and S. Rowland-Jones. 1997. Late escape from an immunodominant cytotoxic T-lymphocyte response associated with progression to AIDS. Nat. Med. 3:212-217.
15. Goulder, P. J., and D. I. Watkins. 2004. HIV and SIV CTL escape: implications for vaccine design. Nat. Rev. Immunol. 4:630-640.
16. Homsy, J., M. Meyer, and J. A. Levy. 1990. Serum enhancement of human immunodeficiency virus (HIV) infection correlates with disease in HIV-infected individuals. J. Virol. 64:1437-1440.
17. Joao, C., B. M. Ogle, C. Gay-Rabinstein, J. L. Platt, and M. Cascalho. 2004. B cell-dependent TCR diversification. J. Immunol. 172:4709-4716.
18. Johnston, M. I., and A. S. Fauci. 2007. An HIV vaccine - evolving concepts. N. Engl. J. Med. 356:2073-2081.
19. Jonjic, S., I. Pavic, B. Polic, I. Crnkovic, P. Lucin, and U. H. Koszinowski. 1994. Antibodies are not essential for the resolution of primary cytomegalovirus infection but limit dissemination of recurrent virus. J. Exp. Med. 179:1713-1717.
20. Kim, I. J., E. Flano, D. L. Woodland, and M. A. Blackman. 2002. Antibody-mediated control of persistent gamma-herpesvirus infection. J. Immunol. 168:3958-3964.
21. Kim, T. S., and S. Perlman. 2003. Protection against CTL escape and clinical disease in a murine model of virus persistence. J. Immunol. 171:2006-2013.
22. Lee, B. O., J. Rangel-Moreno, J. E. Moyron-Quiroz, L. Hartson, M. Makris, F. Sprague, F. E. Lund, and T. D. Randall. 2005. CD4 T cell-independent antibody response promotes resolution of primary influenza infection and helps to prevent reinfection. J. Immunol. 175:5827-5838.
23. McMichael, A. J., and R. E. Phillips. 1997. Escape of human immunodeficiency virus from immune control. Annu. Rev. Immunol. 15:271-296.
24. O'Connor, D., T. Friedrich, A. Hughes, T. M. Allen, and D. Watkins. 2001. Understanding cytotoxic T-lymphocyte escape during simian immunodeficiency virus infection. Immunol. Rev. 183:115-126.
25. O'Connor, D. H., T. M. Allen, T. U. Vogel, P. Jing, I. P. DeSouza, E. Dodds, E. J. Dunphy, C. Melsaether, B. Mothe, H. Yamamoto, H. Horton, N. Wilson, A. L. Hughes, and D. I. Watkins. 2002. Acute phase cytotoxic T lymphocyte escape is a hallmark of simian immunodeficiency virus infection. Nat. Med. 8:493-499.
26. +-T-lymphocyte selection in simian immunodeficiency virus sequence variation. J. Virol. 78:14012-14022.
27. Ontiveros, E., T. S. Kim, T. M. Gallagher, and S. Perlman. 2003. Enhanced virulence mediated by the murine coronavirus, mouse hepatitis virus strain JHM, is associated with a glycine at residue 310 of the spike glycoprotein. J. Virol. 77:10260-10269.
28. Ontiveros, E., L. Kuo, P. S. Masters, and S. Perlman. 2001. Inactivation of expression of gene 4 of mouse hepatitis virus strain JHM does not affect virulence in the murine CNS. Virology 289:230-238.
29. Perlman, S., R. Schelper, E. Bolger, and D. Ries. 1987. Late onset, symptomatic, demyelinating encephalomyelitis in mice infected with MHV-JHM in the presence of maternal antibody. Microb. Pathog. 2:185-194.
30. Pewe, L., and S. Perlman. 1999. Immune response to the immunodominant epitope of mouse hepatitis virus is polyclonal, but functionally monospecific in C57B1/6 mice. Virology 255:106-116.
31. Pewe, L., G. F. Wu, E. M. Barnett, R. F. Castro, and S. Perlman. 1996. Cytotoxic T cell-resistant variants are selected in a virus-induced demyelinating disease. Immunity 5:253-262.
32. Pewe, L., S. Xue, and S. Perlman. 1997. Cytotoxic T-cell-resistant variants arise at early times after infection in C57BL/6 but not in SCID mice infected with a neurotropic Coronavirus. J. Virol. 71:7640-7647.
33. Peyerl, F. W., D. H. Barouch, W. W. Yeh, H. S. Bazick, J. Kunstman, K. J. Kunstman, S. M. Wolinsky, and N. L. Letvin. 2003. Simian-human immunodeficiency virus escape from cytotoxic T-lymphocyte recognition at a structurally constrained epitope. J. Virol. 77:12572-12578.
34. Pircher, H., D. Moskophidis, U. Rohrer, K. Burki, H. Hengartner, and R. M. Zinkernagel. 1990. Viral escape by selection of cytotoxic T cell-resistant virus variants in vivo. Nature 346:629-633.
35. Price, G. E., R. Ou, H. Jiang, L. Huang, and D. Moskophidis. 2000. Viral escape by selection of cytotoxic T cell-resistant variants in influenza A virus pneumonia. J. Exp. Med. 191:1853-1867.
36. Ramakrishna, C., S. A. Stohlman, R. D. Atkinson, M. J. Shlomchik, and C. C. Bergmann. 2002. Mechanisms of central nervous system viral persistence: the critical role of antibody and B cells. J. Immunol. 168:1204-1211.
37. Ray, S. C., L. Fanning, X. H. Wang, D. M. Netski, E. Kenny-Walsh, and D. L. Thomas. 2005. Divergent and convergent evolution after a common-source outbreak of hepatitis C virus. J. Exp. Med. 201:1753-1759.
38. Richman, D. D., T. Wrin, S. J. Little, and C. J. Petropoulos. 2003. Rapid evolution of the neutralizing antibody response to HIV type 1 infection. Proc. Natl. Acad. Sci. USA 100:4144-4149.
39. Seifert, U., H. Liermann, V. Racanelli, A. Halenius, M. Wiese, H. Wedemeyer, T. Ruppert, K. Rispeter, P. Henklein, A. Sijts, H. Hengel, P. M. Kloetzel, and B. Rehermann. 2004. Hepatitis C virus mutation affects proteasomal epitope processing. J. Clin. Investig. 114:250-259.
40. Street, N. E., and T. R. Mosmann. 1991. Functional diversity of T lymphocytes due to secretion of different cytokine patterns. FASEB J. 5:171-177.
41. Takaki, A., M. Wiese, G. Maertens, E. Depla, U. Seifert, A. Liebetrau, J. L. Miller, M. P. Manns, and B. Rehermann. 2000. Cellular immune responses persist and humoral responses decrease two decades after recovery from a single-source outbreak of hepatitis C. Nat. Med. 6:578-582.
42. Tester, I., S. Smyk-Pearson, P. Wang, A. Wertheimer, E. Yao, D. M. Lewinsohn, J. E. Tavis, and H. R. Rosen. 2005. Immune evasion versus recovery after acute hepatitis C virus infection from a shared source. J. Exp. Med. 201:1725-1731.
43. Thomsen, A. R., J. Johansen, O. Marker, and J. P. Christensen. 1996. Exhaustion of CTL memory and recrudescence of viremia in lymphocytic choriomeningitis virus-infected MHC class II-deficient mice and B cell-deficient mice. J. Immunol. 157:3074-3080.
44. Timm, J., G. M. Lauer, D. G. Kavanagh, I. Sheridan, A. Y. Kim, M. Lucas, T. Pillay, K. Ouchi, L. L. Reyor, J. Schulze zur Wiesch, R. T. Gandhi, R. T. Chung, N. Bhardwaj, P. Klenerman, B. D. Walker, and T. M. Allen. 2004. CD8 epitope escape and reversion in acute HCV infection. J. Exp. Med. 200:1593-1604.
45. Weiner, A., A. L. Erickson, J. Kansopon, K. Crawford, E. Muchmore, A. L. Hughes, M. Houghton, and C. M. Walker. 1995. Persistent hepatitis C virus infection in a chimpanzee is associated with emergence of a cytotoxic T lymphocyte escape variant. Proc. Natl. Acad. Sci. USA 92:2755-2759.