Inverted immunodominance and impaired cytolytic function of CD8+ T cells during viral persistence in the central nervous system

Journal of Immunology

Volumn 163, Issue 6, 1999, Pages 3379-3387

  Bergmann, Cornelia C ^a   Altman, John D ^b   Hinton, David ^a   Stohlman, Stephen A ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD69 ANTIGEN; CD8 ANTIGEN; GAMMA INTERFERON;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN SPECIFICITY; ANTIVIRAL ACTIVITY; ARTICLE; CONTROLLED STUDY; CYTOLYSIS; DEMYELINATION; IMMUNOMODULATION; MALE; MOUSE; MURINE HEPATITIS CORONAVIRUS; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE SUBPOPULATION; VIRUS ENCEPHALITIS; VIRUS RESISTANCE;

ACUTE DISEASE; ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CENTRAL NERVOUS SYSTEM; CORONAVIRUS INFECTIONS; CROSSES, GENETIC; CYTOTOXICITY, IMMUNOLOGIC; IMMUNODOMINANT EPITOPES; LYMPHOCYTE COUNT; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MURINE HEPATITIS VIRUS; T-LYMPHOCYTE SUBSETS; VIRAL LOAD; VIRUS REPLICATION;

EID: 0033568030     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (66)

1. Ahmed, R., and D. Gray. 1996. Immunological memory and protective immunity: understanding their relation. Science 272:54.
2. + T-cell memory to viruses. Curr. Opin. Immunol. 6:545.
3. + T cells in primary and secondary influenza pneumonia. Immunity 8:683.
4. Murali-Krishna, K., J. D. Altman, M. Suresh, D. J. D. Sourdive, A. J. Zajac, J. S. Miller, J. Slansky, and R. Ahmed. 1998. Counting antigen-specific CD8 T cells: a reevaluation of bystander activation during viral infection. Immunity 8:177.
5. Gallimore, A., A. Glithero, A. Godkin, A. C. Tissot, A. Pluckthun, T. Elliott, H. Hengartner, and R. Zinkernagel. 1998. Induction and exhaustion of lymphocytic choriotneningitis virus-specific cytotoxic T lymphocytes visualized using soluble tetrameric major histocompatibility complex class I-peptide complexes. J. Exp. Med. 187:1383.
6. Zajac, A. J., J. N. Blattman, K. Murali-Krishna, D. J. D. Sourdive, M. Suresh, J. D. Altman, and R. Ahmed. 1998. Viral immune evasion due to persistence of activated cells without effector function. J. Exp. Med. 188:2205.
7. Akbar, A. N., and M. Salmon. 1997. Cellular environments and apoptosis: tissue microenvironments control activated T-cell death. Immunol. Today 18:72.
8. + T cells during the primary immune response to Epstein-Barr virus in vivo. J. Exp. Med 187:1395.
9. Chisari, F. V., and C. Ferrari. 1995. Hepatitis B virus immunopathogenesis. Annu. Rev. Immunol. 13:29.
10. Gordon, L. B., S. C. Nolan, H. F. Cserr, P. M. Knopf, and C. J. Harling-Berg. 1997. Growth of P511 mastocytoma cells in BALB/c mouse brain elicits CTL response without tumor elimination. J. Immunol. 159:2399.
11. Hawke, S., P. G. Stevenson, S. Freeman, and C. R. M. Bangham. 1998. Longterm persistence of activated cytotoxic T lymphocytes after viral infection of the central nervous system. J. Exp. Med. 187:1575.
12. Steven, N. M., A. M. Leese, N. E. Annels, S. P. Lee, and A. B. Rickinson. 1996. Epitope focusing in the primary cytotoxic T cell response to Epstein-Barr virus and its relationship to memory. J. Exp. Med. 184:1801.
13. Stevenson, P. G., G. T. Belz, J. D. Altman, and P. C. Doherty. 1999 Changing patterns of dominance in the CD8 T cell response during acute and persistent murine γ-herpesvirus infection. Eur. J. Immunol. 29:1059.
14. Kristensson, K., and E. Norrby. 1986. Persistence of RNA viruses in the central nervous system. Annu. Rev. Microbiol. 40:159.
15. Lipton, H. L., and D. H. Gilden. 1997. Viral diseases of the nervous system: persistent infections. In Viral Pathogenesis, N. Nathanson, R. Ahmed, F. Gonzalez-Scarano, D. E. Griffin, K. V. Holmes, F. A. Murphy, and H. L. Robinson, et al., eds. Lippencott-Raven Publishers, Philadelphia, p. 855.
16. Fabry, Z., C. S. Raine, and M. N. Hart. 1994. Nervous tissue as an immune compartment: the dialect of the immune response in the CNS. Immunol. Today 15:218.
17. Bonetti, B., J. Pohl, Y.-L. Gao, and C. S. Raine. 1997. Cell death during autoimmune demyelination: effector but not target cells are eliminated by apoptosis. J. Immunol. 159:5733.
18. Kyuwa, S., and S. A. Stohlman. 1990. Pathogenesis of a neurotropic murine coronavirus, strain JHM in the central nervous system of mice. Semin. Virol. 1:273.
19. Lane, T. E., and M. J. Buchmeier. 1997. Murine coronavirus infection: a paradigm for virus-induced demyelinating disease. Trends Microbiol. 1:9.
20. Stohlman, S. A., C. Bergmann, R. van der Veen, and D. Hinton. 1995. Mouse hepatitis virus nucleocapsid-specific cytotoxic T cells protect from lethal infection without eliminating virus from oligodendroglia. J. Virol. 69:684.
21. + T cells. J. Immunol. 160:2896.
22. Fleming, J. O., M. Trousdale, F. E. Zactarim, S. A. Stohlman, and L. P. Weiner. 1986. Pathogenicity of antigenic variants of murine coronavirus JHM selected with mAb. J. Virol. 58:869.
23. Fleming, J. O., C. Adami, S. E. Pooley, J. Glomb, E. Stecker, F. Fazal, and S. Baker. 1995. Mutations associated with viral sequences isolated from mice persistently infected with MHV-JHM. Adv. Exp. Med. Biol. 380:591.
24. Stohlman, S. A., and L. P. Weiner. 1981. Chronic central nervous system demyelination in mice after JHM virus infection. Neurology 31:38.
25. Parra, B., D. R. Hinton, N. W. Marten, C. C. Bergmann, M. T. Lin, C. S. Yang, and S. A. Stohlman. 1999. IFN-γ is required for viral clearance from central nervous system oligodendroglia. J. Immunol. 162: 1641.
26. Bergmann, C., E. Dimacali, S. Stohl, W. Wei, M. M. C. Lai, S. Tahara, and N. Marten. 1998. Variability of persisting MHV RNA sequences comprising immune and replication relevant domains. Virology 244:563.
27. 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.
28. Rowe, C. L., S. C. Baker, M. J. Nathan, and J. Fleming. 1997. Evolution of mouse hepatitis virus: deletion and characterization of spike detection variants during persistent infection. J. Virol. 71:2959.
29. Lin, M. T., S. A. Stohlman, and D. R. Hinton. 1997. Mouse hepatitis virus is cleared from the central nervous system of mice lacking perforin-mediated cytolysis. J. Virol. 71:383.
30. Perlman, S., and D. Ries. 1987. The astrocyte is a target cell in mice persistently infected with mouse hepatitis virus, strain JHM. Microb. Pathog. 3:309.
31. Williamson, J., S. P. K. Sykes, and S. Stohlman. 1991. Characterization of brain infiltrating mononuclear cells during infection with mouse hepatitis virus strain JHM. J. Neuroimmunol. 32:199.
32. + cells with highly focused specificity during viral persistence in the central nervous system. J. Immunol. 162:3905.
33. Stohlman, S. A., S. Kyuwa, J. M. Polo, D. Brady, M. C. Lai, and C. C. Bergmann. 1993. Characterization of mouse hepatitis virus-specific cytotoxic T cells derived from the central nervous system of mice infected with the JHM strain. J. Virol. 67:7050.
34. d-restricted cytotoxic T lymphocyte epitope in the mouse hepatitis virus nucleocapsid protein. J. Virol. 67:7041.
35. b-restricted cytotoxic T cell response. J. Gen. Virol. 77:315.
36. + T-cell epitopes within the surface glycoprotein of a neurotropic coronavirus and correlation with pathogenicity. J. Virol. 59:8127.
37. + T cells using an ELISPOT assay. J. Immunol. Methods 181:45.
38. Parra, B., D. R. Hinton, M. T. Lin, D. J. Cua, and S. A. Stohlman. 1997. Kinetics of cytokine mRNA expressin in the central nervous system following lethal and nonlethal coronavirus-induced acute encephalomyelitis. Virology 233:260.
39. Wang, F. I., S. A. Slohlman, and J. O. Fleming. 1990. Demyelination induced by murine hepatitis virus, JHM strain (MHV-4) is immunologically mediated. J. Neuroimmunol. 30:31.
40. Lai, M., and D. Cavanagh. 1997. Molecular biology of coronaviruses. Adv. Virus Res. 48:1.
41. Parker, S., T. M. Gallagher, and M. J. Buchmeier. 1989. Sequence analysis reveals extensive polymorphism and evidence of deletions within the E2 glycoprotein gene of several strains of murine hepatitis virus. Virology 173:664.
42. Castro, R. F., and S. Perlman. 1996. Differential antigen recognition by T cells from the spleen and central nervous system of coronavirus-infected mice. Virology 222:247.
43. Altman, J. D., P. A. H. Moss, P. J. R. Goulder, D. H. Barouch, M. G. McHeyzer-Williams, J. I. Bell, A. J. McMichael, and M. M. Davis. 1996. Phenotypic analysis of antigen-specific T lymphocytes. Science 274:94.
44. Irani, D. N., K.-I. Lin, and D. E. Griffin. 1997. Regulation of brain-derived T cells during acute central nervous inflammation. J. Immunol. 158:2318.
45. + T lymphocytes from the central nervous system of rats with coronavirus JHM induced demyelinating encephalomyelitis. J. Neurovirol. 1:340.
46. Salmon, M., D. Pilling, N. J. Borthwick, N. Viner, G. Janossy, P. A. Bacon, and A. N. Akbar. 1994. The progressive differentiation of primed T cells is associated with an increasing susceptibility to apoptosis. Eur. J. Immunol. 24:892.
47. Hudson, S. J., and J. W. Streilein. 1994. Functional cytotoxic T cells are associated with focal lesions in the brains of SJL mice with experimental herpes simplex encephalitis. J. Immunol. 152:5540.
48. Lindsley, M., D. R. Thiemann, and M. Rodriquez. 1991. Cytotoxic T cells isolated from the central nervous systems of mice infected with Theiler's virus. J. Virol. 65:6612.
49. Liu, Y., R. V. Blanden, and A. Mullbacher. 1989. Identification of cytolytic lymphocytes in West Nile virus-infected murine central nervous system. J. Gen. Virol. 70:565.
50. Lampson, L. 1987. Molecular basis of the immune response to neural antigens. Trends Neurosci. 10:211.
51. Hickey, W. F., B. L. Hsu, and H. Kimura. 1991. T-lymphocyte entry into the central nervous system. J. Neurosci. Res. 28:254.
52. Irani, D. N., and D. E. Griffin. 1996. Regulation of lymphocyte homing into the brain during viral encephalitis at various stages of infection. J. Immunol. 156: 3850.
53. Williams, K. C., and W. F. Hickey. 1995. Traffic of hematogenous cells through the central nervous system. Curr. Top. Microbiol. Immunol. 202:221.
54. Karin, N., F. Szafer, D. Mitchell, D. P. Gold, and L. Steinman. 1993. Selective and nonselective stages in homing of T lymphocytes to the central nervous system during experimental allergic encephalomyelitis. J. Immunol. 150:4116.
55. Musette, P., J.-F. Bureau, G. Gachelin, P. Kourilsky, and M. Brahic. 1995. T lymphocyte repertoire in Theiler's virus encephalomyelitis: the nonspecific infiltration of the central nervous system of infected SJL/J mice is associated with a selective local T cell expansion. Eur. J. Immunol. 25:1589.
56. Lin, X., L. R. Pease, P. D. Murray, and M. Rodriguez. 1998. Theiler's virus infection of genetically susceptible mice induces central nervous system-infiltrating CTLs with no apparent viral or major myelin antigenic specificity. J. Immunol. 160:5661.
57. Stevenson, P. G., S. Freeman, C. R. M. Bangham, and S. Hawke. 1997. Virus dissemination through the brain parenchyma without immunologic control. J. Immunol. 159:1876.
58. Craston, R., M. Koh, A. Mc Dermott, N. Ray, H. G. Prentice, and M. W. Lowdell. 1997. Temporal dynamics of CD69 expression on lymphoid cells. J. Immunol. Methods 209:37.
59. Ziegler, S. F., R. Ramsdell, and M. R. Alderson. 1994. The activation antigen CD69. Stem Cells 12:456.
60. Pope, J. G., W. J. Karpus, C. Van der Lugt, and S. D. Miller. 1996. Flow cytometric and functional analyses of central nervous system-infiltrating cells in SJL/J mice with Theiler' svirus-induced demeylinating disease. J. Immunol. 156:4050.
61. + T cells expressing early activation antigen CD69 in murine lupus: possible abnormal regulatory role for cytokine imbalance. J. Immunol. 161:1267.
62. Stalder, A. K., M. J. Carson, A. Pagenstecher, V. C. Asensio, C. Kincaid, M. Benedict, H. C. Powell, E. Masliah, and I. Campbell. 1998. Late-onset chronic inflammatory encephalopathy in immune-competent and severe combined immune-deficient (SCID) mice with astrocyte-targeted expression of tumor necrosis factor. Am. J. Pathol. 153:767.
63. van der Most, R. G., A. Sette, C. Oseroff, J. Alexander, K. Murali-Krishna, L. L. Lau, S. Southwood, J. Sidney, R. W. Chestnut, M. Matloubian, and R. Ahmed. 1996. Analysis of cytotoxic T cell responses to dominant and subdominant epitopes during acute and chronic lymphocytic choriomeningitis virus infection. J. Immunol. 157:5543.
64. Butz, E. A., and M. J. Bevan. 1998. Differential presentation of the same MHC class I epitopes by fibroblasts and dendritic cells. J. Immunol. 161:2139.
65. Reali, E., R. Guerrini, M. Marastoni, R. Tomatis, M. G. Masucci, S. Traniello, and R. Gavioli. 1999. A single specific amino acid residue in peptide antigens is sufficient to activate memory CTL: potential role of cross-reactive peptides in memory T cell maintenance. J. Immunol. 162:106.
66. Engelhardt, B., M. T. Martin-Simonet, L. S. Rott, E. C. Butcher, E. C., and S. A. Michie. 1998. Adhesion molecule phenotype of T lymphocytes in inflamed CNS. J. Neuroimmunol. 84:92.