Transition from acute to persistent Theiler's virus infection requires active viral replication that drives proinflammatory cytokine expression and chronic demyelinating disease

Journal of Virology

Volumn 78, Issue 22, 2004, Pages 12480-12488

  Trottier, Mark ^a,c,e   Schlitt, Brian P ^a   Kung, Aisha Y ^a   Lipton, Howard L ^a,b,c,d  

^a EVANSTON HOSPITAL   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c NORTHWESTERN UNIVERSITY   (United States)

^d New York University ^*  (United States)

^e NEW YORK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; CYTOKINE; GAMMA INTERFERON; MESSENGER RNA; TUMOR NECROSIS FACTOR ALPHA; VIRUS RNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ANTIBODY TITER; ARTICLE; BRAIN; BRAIN STEM; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; CORRELATION ANALYSIS; DEMYELINATING DISEASE; DISEASE SEVERITY; ENCEPHALOMYELITIS; FEMALE; IMMUNE RESPONSE; INFECTION SENSITIVITY; MOUSE; MURINE ENCEPHALOMYELITIS VIRUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA REPLICATION; SPINAL CORD; VIRUS EXPRESSION; VIRUS GENOME; VIRUS RESISTANCE;

ANIMALS; ANTIBODIES, VIRAL; BRAIN; CARDIOVIRUS INFECTIONS; CD40 LIGAND; CHRONIC DISEASE; CYTOKINES; DEMYELINATING DISEASES; FEMALE; MICE; RNA, MESSENGER; RNA, VIRAL; SPINAL CORD; THEILOVIRUS; VIRUS REPLICATION;

EID: 7644231753     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.78.22.12480-12488.2004     Document Type: Article

References (51)

1. Aubagnac, S., M. Brahic, and J.-F. Bureau. 2001. Viral load increases in SJL/J mice persistentiy infected by Theiler's virus after inactivation of the β2m gene. J. Virol. 75:7723-7726.
2. Aubert, C., and M. Brahic. 1995. Early infection of the central nervous system by the GDVII and DA strains of Theiler's virus. J. Virol. 69:3197-3200.
3. Aubert, C., M. Chamorro, and M. Brahic. 1987. Identification of Theiler's virus infected cells in the central nervous system of the mouse during demyelinating disease. Microb. Pathog. 3:319-326.
4. Begolka, W. S., L. M. Haynes, J. K. Olson, J. Padilla, K. L. Neville, M. C. Dal Canto, J. P. Palma, B. S. Kim, and S. D. Miller. 2001. CD8-deficient SJL mice display enhanced susceptibility to Theiler's virus infection and increased demyelinating pathology. J. Neurovirol. 7:409-420.
5. Begolka, W. S., C. L. Vanderlugt, S. M. Rahbe, and S. D. Miller. 1999. Differential expression of inflammatory cytokines parallels progression of central nervous system pathology in two clinically distinct models of multiple sclerosis. J. Immunol. 161:4437-4446.
6. Blakemore, W. F., C. J. Welsh, P. Tonks, and A. A. Nash. 1988. Observations on demyelinating lesions induced by Theiler's virus in CBA mice. Acta Neuropathol. 76:581-589.
7. b molecules complexed with a viral VP2 peptide lacking a consensus anchor residue. J. Virol. 71:5244-5250.
8. Brahic, M., and J.-F. Bureau. 1998. Genetics of susceptibility to Theiler's virus infection. BioEssays 20:627-633.
9. Brahic, M., W. G. Stroop, and J. R. Baringer. 1981. Theiler's virus persists in glial cells during demyelinating disease. Cell 126:123-128.
10. Bureau, J.-F., X. Montagutelli, S. Lefebvre, J. L. Guenet, M. Pla, and M. Brahic. 1992. The interaction of two groups of murine genes determines the persistence of Theiler's virus in the central nervous system. J. Virol. 66:4698-4704.
11. Chamorro, M., C. Aubert, and M. Brahic. 1986. Demyelinating lesions due to Theiler's virus are associated with ongoing central nervous system infection. J. Virol. 57:992-997.
12. Chang, J. R., E. Zaczynska, C. D. Katsetos, C. D. Platsoucas, and E. L. Oleszak. 2000. Differential expression of transforming growth factor beta, interleukin-2, and other cytokines in the central nervous system of Theiler's murine encephalitis virus-infected susceptible and resistant strains of mice. J. Virol. 278:346-360.
13. Clatch, R. J., H. L. Lipton, and S. D. Miller. 1986. Characterization of Theiler's murine encephalomyelitis virus (TMEV)-specific delayed-type hypersensitivity responses in TMEV-induced demyelinating disease: correlation with clinical signs. J. Immunol. 136:920-926.
14. Clatch, R. J., R. W. Melvold, S. D. Miller, and H. L. Lipton. 1985. Theiler's murine encephalomyelitis virus (TMEV)-induced demyelinating disease in mice is influenced by the H-2D region: correlation with TMEV-specific delayed-type hypersensitivity. J. Immunol. 135:1408-1414.
15. Dal Canto, M. C., and H. L. Lipton. 1976. Primary demyelination in Theiler's virus infection. An ultrastructural study. Lab. Investig. 33:626-637.
16. Dal Canto, M. C., and H. L. Lipton. 1982. Ultrastructural immunohistochemical localization of virus in acute and chronic demyelinating Theiler's virus infection. Am. J. Pathol. 106:20-29.
17. Dethlefs, S., M. Brahic, and E.-L. Larsson-Sciard. 1997. An early, abundant cytotoxic T-lymphocyte response against Theiler's virus is critical for preventing viral persistence. J. Virol. 71:8875-8878.
18. Dethlefs, S., N. Escriou, M. Brahic, S. van der Werf, and E.-L. Larsson-Sciard. 1997. Theiler's virus and Mengo virus induce cross-reactive cytotoxic T lymphocytes restricted to the same immunodominant VP2 epitope in C57BL/6 mice. J. Virol. 71:5361-5365.
19. + T cell line specific for an immunodominant VP2 epitope. J. Immunol. 152:919-929.
20. Hirano, T. 1998. Interleukin-6 and its receptor: 10 years later. Int. Rev. Immunol. 16:249-284.
21. Hoffman, L. M., B. T. Fife, W. S. Begolka, S. D. Miller, and W. J. Karpus. 1999. Central nervous system chemokine expression during Theiler's virus-induced demyelinating disease. J. Neurovirol. 5:635-642.
22. Howard, L. M., K. L. Neville, L. M. Haynes, M. C. Dal Canto, and S. D. Miller. 2003. CD154 blockade results in transient reduction in Theiler's murine encephalomyelitis virus-induced demyelinating disease. J. Virol. 77: 2247-2250.
23. Jelachich, M. L., and H. L. Lipton. 1999. Restricted Theiler's murine encephalomyelitis virus infection in murine macrophages induces apoptosis. J. Gen. Virol. 80:1701-1705.
24. + T cells infiltrating the central nervous system of SJL/J mice infected with BeAn and DA strains of Theiler's murine encephalomyelitis virus. J. Virol. 76:11780-11784.
25. + T cells in the central nervous system of susceptible SJL/J mice infected with Theiler's virus are virus specific and fully functional. J. Virol. 76:6577-6585.
26. + subset. Multiple Sclerosis 8:469-474.
27. Katz-Levy, V., K. L. Neville, J. Padilla, S. Rahbe, W. S. Begolka, A. M. Girvin, J. K. Olson, C. L. Vanderlugt, and S. D. Miller. 2000. Temporal development of autoreactive Th1 responses and endogenous presentation of self myelin epitopes by central nervous system-resident APCs in Theiler's virus-infected mice. J. Immunol. 165:5304-5314.
28. Lipton, H. L., A. Friedmann, P. Sethi, and J. R. Crowther. 1998. Characterization of Vilyuisk virus, a cause of human encephalitis in Russia. J. Med. Virol. 12:195-204.
29. Lipton, H. L., and R. Melvold. 1984. Genetic analysis of susceptibility to Theiler's virus-induced demyelinating disease in mice. J. Immunol. 132: 1821-1825.
30. Lipton, H. L., G. Twaddle, and M. L. Jelachich. 1995. The predominant virus antigen burden is present in macrophages in Theiler's murine encephalomyelitis virus (TMEV)-induced demyelinating disease. J. Virol. 69:2525-2533.
31. Markovic-Plese, S., and H. F. McFarland. 2001. Immunopathogenesis of the multiple sclerosis lesion. Curr. Neurol. Neurosci. Rep. 1:257-262.
32. + T cell response against a single immunodominant viral peptide. Eur. J. Immunol. 33:2501-2510.
33. Miller, S. D., C. VanderLugt, W. S. Begolka, W. Pao, R. L. Yauch, K. L. Neville, Y. Katz-Levy, A. Carrizosa, and B. S. Kim. 1997. Persistent infection with Theiler's virus leads to CNS autoimmunity via epitope spreading. Nat. Med. 3:1113-1136.
34. Murray, P. D., K. Krivacic, A. Chernosky, T. Wei, R. M. Ransohoff, and M. Rodriguez. 2000. Biphasic and regionally-restricted chemokine expression in the central nervous system in the Theiler's virus model of multiple sclerosis. J. Neurovirol. 6:S44-S52.
35. Neville, K. L., J. Padilla, and S. D. Miller. 2002. Myelin-specific tolerance attenuates the progression of a virus-induced demyelinating disease: implications for the treatment of MS. J. Neuroimmunol. 123:18-29.
36. + T lymphocytes provide protection against TMEV-induced demyelinating disease in BALB/c mice. J. Immunol. 156: 1276-1283.
37. Nicholson, S. M., J. D. Peterson, S. D. Miller, K. Wang, M. C. Dal Canto, and R. W. Melvold. 1994. BALB/c substrain differences in susceptibility to Theiler's murine encephalomyelitis virus-induced demyelinating disease. J. Neuroimmunol. 52:19-24.
38. Njenga, M. K., K. Asakura, S. F. Hunter, P. Wettstein, L. R. Pease, and M. Rodriguez. 1997. The immune system preferentially clears Theiler's virus from the gray matter of the central nervous system. J. Virol. 71:8592-8601.
39. Ohara, Y., S. Stein, J. Fu, L. Stillman L. Klaman, and R. P. Roos. 1988. Molecular cloning and sequence determination of DA strain of Theiler's murine encephalomyelitis virus. Virology 164:245-255.
40. Peterson, J. D., C. Waltenbaugh, and S. D. Miller. 1992. IgG subclass responses to Theiler's murine encephalomyelitis virus infection and immunization suggest a dominant role for Th1 cells in susceptible mouse strains. Immunology 75:652-658.
41. Pevear, D. C., M. Calenoff, E. Rozhon, and H. L. Lipton. 1987. Analysis of the complete nucleotide sequence of the picornavirus Theiler's murine encephalomyelitis virus indicates that it is closely related to cardioviruses. J. Virol. 61:1507-1516.
42. + T cells and viral persistence. J. Virol. 76:2217-2224.
43. Rodriguez, M., J. Leibowitz, and C. S. David. 1986. Susceptibility to Theiler's virus-induced demyelination. Mapping of the gene within the H-2D region. J. Exp. Med. 163:620-631.
44. Rodriguez, M., J. L. Leibowitz, and P. W. Lampert. 1983. Persistent infection of oligodendrocytes in Theiler's virus-induced encephalomyelitis. Ann. Neurol. 13:426-433.
45. Rozhon, E. J., J. D. Kratochvil, and H. L. Lipton. 1983. Analysis of genetic variation in Theiler's virus during persistent infection in the mouse central nervous system. Virology 128:16-32.
46. Sato, S., S. L. Reiner, M. A. Jensen, and R. P. Roos. 1997. Central nervous system cytokine mRNA expression following Theiler's murine encephalomyelitis virus infection. J. Neuroimmunol. 76:213-223.
47. Simas, J. P., and J. K. Fazakerley. 1996. The course of disease and persistence of virus in the central nervous system varies between individual CBA mice infected with the BeAn strain of Theiler's murine encephalomyelitis virus. J. Gen. Virol. 77:2701-2711.
48. Steinman, L., R. Martin, C. Bernard, P. Conlon, and J. R. Oksenberg. 2002. Multiple sclerosis: deeper understanding of its pathogenesis reveals new targets for therapy. Annu. Rev. Neurosci. 25:491-505.
49. Trottier, M., P. Kallio, W. Wang, and H. L. Lipton. 2001. High numbers of viral RNA copies in the central nervous system of mice during persistent infection with Theiler's virus. J. Virol. 75:7428.
50. Trottier, M., B. P. Schlitt, and H. L. Lipton. 2002. Enhanced detection of Theiler's virus RNA copy equivalents in the mouse central nervous system by real-time RT-PCR. J. Virol. Methods 103:89-99.
51. Zheng, L., M. A. Calenoff, and M. C. Dal Canto. 2001. Astrocytes, not microglia, are the main cells responsible for viral persistence in Theiler's murine encephalomyelitis virus infection leading to demyelination. J. Neurovirol. 118:256-267.