Infection with cytotoxic T-lymphocyte escape mutants results in increased mortality and growth retardation in mice infected with a neurotropic coronavirus

Journal of Virology

Volumn 72, Issue 7, 1998, Pages 5912-5918

  Pewe, Lecia ^a   Xue, Shurong ^b   Perlman, Stanley ^a,b  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD8 ANTIGEN;

ANIMAL MODEL; ARTICLE; CORONAVIRUS; CYTOTOXIC T LYMPHOCYTE; DELETION MUTANT; ENCEPHALOMYELITIS; GENE MUTATION; GROWTH RETARDATION; HEPATITIS VIRUS; MOLECULAR RECOGNITION; MORTALITY; MOUSE; NEUROTROPISM; NONHUMAN; PRIORITY JOURNAL;

EID: 0031775861     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.72.7.5912-5918.1998     Document Type: Article

References (48)

1. Banner, L., J. G. Keck, and M. M. C. Lai. 1990. A clustering of RNA recombination sites adjacent to a hypervariable region of the peplomer gene of murine coronavirus. Virology 175:548-555.
2. b-restricted CTL response. J. Gen. Virol. 77:315-325.
3. Bertoletti, A., A. Costanzo, F. V. Chisari, M. Levero, M. Artini, A. Sette, A. Penna, T. Giuberti, F. Fiaccadori, and C. Ferrari. 1994. Cytotoxic T lymphocyte response to a wild type hepatitis B virus epitope in patients chronically infected by variant viruses carrying substitutions within the epitope. J. Exp. Med. 180:933-943.
4. Bertoletti, A., A. Sette, F. V. Chisari, A. Penna, M. Levrero, M. De Carli, F. Fiaccadori, and C. Ferrari. 1994. Natural variants of cytotoxic epitopes are T-cell receptor antagonists for antiviral cytotoxic T cells. Nature 369:407-410.
5. Borrow, P., H. Lewicki, X. Wei, M. Horwitz, N. Peffer, H. Meyers, J. A. Nelson, J. Gairin, B. Hahn, M. B. A. Oldstone, and G. Shaw. 1997. Antiviral pressure exerted by HIV-1-specific cytotoxic T lymphocytes (CTLs) during primary infection demonstrated by rapid selection of CTL escape mutants. Nat. Med. 3:205-211.
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. + T-cell epitopes within the surface glycoprotein of a neurotropic coronavirus and correlation with pathogenicity. J. Virol. 69:8127-8131.
8. 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 222:247-251.
9. De Campos-Lima, P. O., V. Levitsky, J. Brooks, S. P. Lee, L. Hu, A. B. Rickinson, and M. G. Masucci. 1994. T cell responses and virus evolution: loss of HLA A11-restricted CTL epitopes in Epstein-Barr virus isolates from highly A11-positive populations by selective mutation of anchor residues. J. Exp. Med. 179:1297-1305.
10. Franco, A., C. Ferrari, A. Sette, and F. V. Chisari. 1995. Viral mutations, TCR antagonism and escape from the immune response. Curr. Opin. Immunol. 7:524-531.
11. Gombold, J., R. Sutherland, E. Lavi, Y. Paterson, and S. R. Weiss. 1995. Mouse hepatitis virus A59-induced demyelination can occur in the absence of CD8+ T cells. Microb. Pathog. 18:211-221.
12. Goulder, P., R. Phillips, R. Colbert, S. McAdam, G. Ogg, M. 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.
13. Hall, W., and P. W. Choppin. 1981. Measles-virus proteins in the brain tissue of patients with subacute sclerosing panencephalitis. N. Engl. J. Med. 304: 1152-1155.
14. + cytotoxic T cells against mouse hepatitis virus A59. Immunology 84:521-527.
15. Houtman, J. J., and J. O. Fleming. 1996. Dissociation of demyelination and viral clearance in congenitally immunodeficient mice infected with murine coronavirus JHM. J. Neurovirol. 2:101-110.
16. Houtman, J. J., and J. O. Fleming. 1996. Pathogenesis of mouse hepatitis virus-induced demyelination. J. Neurovirol. 2:361-376.
17. b: application to the design of high-affinity, allele-specific peptides. Mol. Immunol. 32:895-907.
18. Klenerman, P., S. Rowland-Jones, S. McAdam, J. Edwards, S. Daenke, D. Lalloo, B. Koppe, W. Rosenberg, D. Boyd, A. Edwards, P. Glangrande, R. E. Phillips, and A. J. McMichael. 1994. Cytotoxic T-cell activity antagonized by naturally occurring HIV-1 gag variants. Nature 369:403-407.
19. Koup, R. 1994. Virus escape from CTL recognition. J. Exp. Med. 180:779-782.
20. Kyuwa, S., and S. A. Stohlman. 1990. Pathogenesis of a neurotropic murine coronavirus, strain JHM in the central nervous system of mice. Semin. Virol. 1:273-280.
21. Lane, T. E., and M. J. Buchmeier. 1997. Murine coronavirus infection: a paradigm for virus-induced demyelinating disease. Trends Microbiol. 5:9-14.
22. Lehmann, P., T. Forsthuber, A. Miller, and E. E. Sercarz. 1992. Spreading of T-cell autoimmunity to cryptic determinants of an autoantigen. Nature 358: 155-157.
23. Lewicki, H., M. Von Herrath, C. Evans, J. L. Whitton, and M. Oldstone. 1995. CTL escape viral variants. II. Biologic activity in vivo. Virology 211: 443-450.
24. Luytjes, W., L. S. Sturman, P. J. Bredenbeek, J. Charite, B. A. M. van der Zeijst, M. C. Horzinek, and W. J. M. Spaan. 1987. Primary structure of the glycoprotein E2 of coronavirus MHV-A59 and identification of the trypsin cleavage site. Virology 161:479-487.
25. McMichael, A. J., and R. E. Phillips. 1997. Escape of human immunodeficiency virus from immune control. Annu. Rev. Immunol. 15:271-296.
26. Miller, S. D., and W. J. Karpus. 1994. The immunopathogenesis and regulation of T-cell-mediated demyelinating diseases. Immunol. Today 15:356-361.
27. Miller, S. D., C. Vanderlugt, W. Begolka, W. Pao, R. Yauch, K. Neville, Y. Katz-Levy, A. Carrizosa, and B. Kim. 1997. Persistent infection with Theiler's virus leads to CNS autoimmunity via epitope spreading. Nat. Med. 3:1133-1136.
28. + T cell subset that responds to viral glycoproteins. Virology 187:443-452.
29. Moskophidis, D., and R. M. Zinkernagel. 1995. Immunobiology of cytotoxic T-cell escape mutants of lymphocytic choriomeningitis virus. J. Virol. 69: 2187-2193.
30. Nowak, M. A., R. M. May, R. E. Phillips, S. Rowland-Jones, D. G. Lalloo, S. McAdam, P. Klenerman, B. Koppe, K. Sigmund, C. R. M. Bangham, and A. J. McMichael. 1995. Antigenic oscillations and shifting immunodominance in HIV-1 infections. Nature 375:606-611.
31. Parker, S. E., 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: 664-673.
32. Perlman, S., G. Jacobsen, A. L. Olson, and A. Afifi. 1990. Identification of the spinal cord as a major site of persistence during chronic infection with a murine coronavirus. Virology 175:418-426.
33. 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.
34. Pewe, L., G. Wu, E. M. Barnett, R. Castro, and S. Perlman. 1996. Cytotoxic T cell-resistant variants are selected in a virus-induced demyelinating disease. Immunity 5:253-262.
35. 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.
36. Phillips, R. E., S. Rowland-Jones, D. F. Nixon, F. M. Gotch, J. P. Edwards, A. O. Ogunlesi, J. G. Elvin, J. A. Rothbard, C. R. M. Bangham, C. R. Rizza, and A. J. McMichael. 1991. Human immunodeficiency virus genetic variation that can escape cytotoxic T cell recognition. Nature 354:453-459.
37. Pircher, H., D. Moskophidis, U. Rohrer, K. Burki, H. Hengartner, and R. Zinkernagel. 1990. Viral escape by selection of cytotoxic T cell-resistant virus variants in vivo. Nature 346:629-633.
38. Price, D., P. Goulder, P. Klenerman, A. Sewell, P. Easterbrook, M. Troop, C. R. Bangham, and R. E. Phillips. 1997. Positive selection of HIV-1 cytotoxic T lymphocyte escape variants during primary infection. Proc. Natl. Acad. Sci. USA 94:1890-1895.
39. Rehermann, B., C. Pasquinelli, S. Mosier, and F. Chisari. 1995. Hepatitis B virus (HBV) sequence variation in cytotoxic T lymphocyte epitopes is not common in patients with chronic HBV infection. J. Clin. Invest. 96:1527-1534.
40. Rowe, C. L., S. C. Baker, M. J. Nathan, and J. O. Fleming. 1997. Evolution of mouse hepatitis virus: detection and characterization of S1 deletion variants during persistent infection. J. Virol. 71:2959-2967.
41. Sedgwick, J. D., and P. G. Holt. 1983. A solid-phase immunoenzymatic technique for the enumeration of specific antibody-secreting cells. J. Immunol. Methods 57:301-309.
42. Sun, N., D. Grzybicki, R. Castro, S. Murphy, and S. Perlman. 1995. Activation of astrocytes in the spinal cord of mice chronically infected with a neurotropic coronavirus. Virology 213:482-493.
43. Tsunoda, I., and R. S. Fujinami. 1996. Two models of multiple sclerosis: experimental allergic encephalomyelitis and Theiler's murine encephalomyelitis virus. J. Neuropathol. Exp. Neurol. 55:672-686.
44. Wang, F., S. A. Stohlman, and J. O. Fleming. 1990. Demyelination induced by murine hepatitis virus JHM strain (MHV-4) is immunologically mediated. J. Neuroimmunol. 30:31-41.
45. Weiner, A., A. Erickson, J. Kanospon, K. Crawford, E. Muchmore, A. 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.
46. + T cells. J. Virol. 64:4589-4592.
47. Wolinsky, S. M., B. Korber, A. U. Neumann, M. Daniels, K. Kunstman, A. Whetsell, M. Furtado, Y. Cao, D. Ho, J. Safrit, and R. Koup. 1996. Adaptive evolution of human immunodeficiency virus-type 1 during the natural course of infection. Science 272:537-542.
48. Xue, S., and S. Perlman. 1997. Antigen specificity of CD4 T cell response in the central nervous system of mice infected with mouse hepatitis virus. Virology 238:68-78.