Neuropathogenesis of theiler's murine encephalomyelitis virus infection, an animal model for multiple sclerosis

Journal of Neuroimmune Pharmacology

Volumn 5, Issue 3, 2010, Pages 355-369

  Tsunoda, Ikuo ^a,b   Fujinami, Robert S ^a  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^b LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

Author keywords

adhesion molecules; apoptosis; axonal damage; central nervous system; experimental autoimmune encephalomyelitis; inside out model

Indexed keywords

APOPTOSIS; AUTOIMMUNE DISEASE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; DEMYELINATION; DISEASE MODEL; ENCEPHALOMYELITIS; GRAY MATTER; MOUSE STRAIN; MULTIPLE SCLEROSIS; MURINE ENCEPHALOMYELITIS VIRUS; NERVE CELL; NERVE FIBER DEGENERATION; NEUROPATHOLOGY; NONHUMAN; PRIORITY JOURNAL; PROGRESSIVE MULTIFOCAL LEUKOENCEPHALOPATHY; REVIEW; SPINAL CORD;

ANIMALS; ANTIBODIES, VIRAL; APOPTOSIS; AXONS; BRAIN; CARDIOVIRUS INFECTIONS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CENTRAL NERVOUS SYSTEM VIRAL DISEASES; DEMYELINATING DISEASES; DISEASE MODELS, ANIMAL; MICE; MULTIPLE SCLEROSIS; NEUROIMMUNOMODULATION; THEILOVIRUS; TOLL-LIKE RECEPTORS;

EID: 77955984560     PISSN: 15571890     EISSN: 15571904     Source Type: Journal    
DOI: 10.1007/s11481-009-9179-x     Document Type: Review

References (159)

1. Agol VI (2002) Picornavirus genome: an overview. In: Semler BL, Wimmer E (eds) Molecular biology of picornaviruses. ASM, Washington, D.C., pp 127-148
2. S Akira S Uematsu O Takeuchi 2006 Pathogen recognition and innate immunity Cell 124 783 801 1:CAS:528:DC%2BD28Xit1Kltb8%3D
3. ML Albert B Sauter N Bhardwaj 1998 Dendritic cells acquire antigen from apoptotic cells and induce class I-restricted CTLs Nature 392 86 89 1:CAS:528:DyaK1cXhvVOntrw%3D
4. 2 m gene J Virol 75 7723 7726 1:CAS:528:DC%2BD3MXlsFKrs70%3D
5. b gene become resistant to persistent infection by Theiler's virus J Virol 68 4049 4052 1:CAS:528:DyaK2cXjt1Snurk%3D
6. YY Bahk CA Kappel G Rasmussen BS Kim 1997 Association between susceptibility to Theiler's virus-induced demyelination and T-cell receptor Jβ1-Cβ1 polymorphism rather than Vβ deletion J Virol 71 4181 4185 1:CAS:528:DyaK2sXisFWksr4%3D
7. RL Barbano MC Dal Canto 1984 Serum and cells from Theiler's virus-infected mice fail to injure myelinating cultures or to produce in vivo transfer of disease. The pathogenesis of Theiler's virus-induced demyelination appears to differ from that of EAE J Neurol Sci 66 283 293 1:STN:280: DyaL2M7lvFOjtw%3D%3D
8. WS Begolka LM Haynes JK Olson J Padilla KL Neville MC Dal Canto J Palma BS Kim SD Miller 2001 CD8-deficient SJL mice display enhanced susceptibility to Theiler's virus infection and increased demyelinating pathology J NeuroVirol 7 409 420 1:STN:280:DC%2BD3MrjsVaqtg%3D%3D
9. A Bitsch J Schuchardt S Bunkowski T Kuhlmann W Brück 2000 Acute axonal injury in multiple sclerosis. Correlation with demyelination and inflammation Brain 123 1174 1183
10. C Bjartmar RP Kinkel G Kidd RA Rudick BD Trapp 2001 Axonal loss in normal-appearing white matter in a patient with acute MS Neurology 57 1248 1252 1:STN:280:DC%2BD3MrksVyhtw%3D%3D
11. b molecules complexed with a viral VP2 peptide lacking a consensus anchor residue J Virol 71 5244 5250 1:CAS:528:DyaK2sXjvVKms7o%3D
12. EJ Buenz BM Sauer RG Lafrance-Corey C Deb A Denic CL German CL Howe 2009 Apoptosis of hippocampal pyramidal neurons is virus independent in a mouse model of acute neurovirulent picornavirus infection Am J Pathol 175 668 684 1:CAS:528:DC%2BD1MXhtVGqtrfM
13. FR Burns XB Li N Shen H Offner YK Chou AA Vandenbark E Heber-Katz 1989 Both rat and mouse T cell receptors specific for the encephalitogenic determinant of myelin basic protein use similar V alpha and V beta chain genes even though the major histocompatibility complex and encephalitogenic determinants being recognized are different J Exp Med 169 27 39 1:CAS:528:DyaL1MXhsFagsbY%3D
14. RK Burt J Padilla MC Dal Canto SD Miller 1999 Viral hyperinfection of the central nervous system and high mortality after hematopoietic stem cell transplantation for treatment of Theiler's murine encephalomyelitis virus-induced demyelinating disease Blood 94 2915 2922 1:CAS:528: DyaK1MXmslanu7g%3D
15. NG Carlson KE Hill I Tsunoda RS Fujinami JW Rose 2006 The pathologic role for COX-2 in apoptotic oligodendrocytes in virus induced demyelinating disease: implications for multiple sclerosis J Neuroimmunol 174 21 31 1:CAS:528:DC%2BD28XjvVajsLo%3D
16. PA Carpentier MT Getts SD Miller 2008 Pro-inflammatory functions of astrocytes correlate with viral clearance and strain-dependent protection from TMEV-induced demyelinating disease Virology 375 24 36 1:CAS:528: DC%2BD1cXlslWhuro%3D
17. E Cash M Chamorro M Brahic 1988 Minus-strand RNA synthesis in the spinal cords of mice persistently infected with Theiler's virus J Virol 62 1824 1826 1:CAS:528:DyaL1cXitF2ktLw%3D
18. D Chen DE Texada C Duggan Y Deng TB Redens MP Langford 2006 Caspase-3 and -7 mediate apoptosis of human Chang's conjunctival cells induced by enterovirus 70 Virology 347 307 322 1:CAS:528:DC%2BD28XjvVais7o%3D
19. RJ Clatch RW Melvold SD Miller HL 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 Neuroimmunol 135 1408 1414 1:STN:280:DyaL2M3jsFGrtw%3D%3D
20. H2 model: a personal perspective Nat Immunol 7 539 541 1:CAS:528:DC%2BD28Xksleks7k%3D
21. RL Coffman J Ohara MW Bond J Carty A Zlotnik WE Paul 1986 B cell stimulatory factor-1 enhances the IgE response of lipopolysaccharide-activated B cells J Immunol 136 4538 4541 1:CAS:528:DyaL28XksVSrur0%3D
22. K Crozat B Beutler 2004 TLR7: a new sensor of viral infection Proc Natl Acad Sci USA 101 6835 6836 1:CAS:528:DC%2BD2cXktFertbc%3D
23. MC Dal Canto HL Lipton 1975 Primary demyelination in Theiler's virus infection. An ultrastructural study Lab Invest 33 626 637 1:STN:280: DyaE28%2FntlKgtA%3D%3D
24. MC Dal Canto HL Lipton 1980 Schwann cell remyelination and recurrent demyelination in the central nervous system of mice infected with attenuated Theiler's virus Am J Pathol 98 101 122 1:STN:280:DyaL3c%2FosFGqug%3D%3D
25. MC Dal Canto RL Barbano 1984 Remyelination during remission in Theiler's virus infection Am J Pathol 116 30 45 1:STN:280:DyaL2c3lsVSisQ%3D%3D
26. MC Dal Canto MA Calenoff SD Miller CL Vanderlugt 2000 Lymphocytes from mice chronically infected with Theiler's murine encephalomyelitis virus produce demyelination of organotypic cultures after stimulation with the major encephalitogenic epitope of myelin proteolipid protein. Epitope spreading in TMEV infection has functional activity J Neuroimmunol 104 79 84 1:CAS:528:DC%2BD3cXht1Ojs70%3D
27. JB Daniels AM Pappenheimer S Richardson 1952 Observations on encephalomyelitis of mice (DA strain) J Exp Med 96 517 535 1:STN:280: DyaG3s%2FkslGjtw%3D%3D
28. S Dethlefs N Escriou M Brahic S van der Werf 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 1:CAS:528:DyaK2sXjvVKkt7o%3D
29. RA Du Pasquier MC Stein MA Lima X Dang J Jean-Jacques Y Zheng NL Letvin IJ Koralnik 2006 JC virus induces a vigorous CD8+ cytotoxic T cell response in multiple sclerosis patients J Neuroimmunol 176 181 186
30. 2-microglobulin-deficient mice J Virol 67 589 592 1:STN:280:DyaK3s7gtVynug%3D%3D
31. Finkelstein SD (1997) Polyomaviruses and progressive multifocal leukoencephalopathy. In: Connor DH, Chandler FW, Schwartz DA, Manz HJ, Lack EE (eds) Pathology of infectious disease. Appleton & Lange, Stamford, pp 265-272
32. RB Fritz X Wang M-L Zhao 2000 Alterations in the spinal cord T cell repertoire during relapsing experimental autoimmune encephalomyelitis J Immunol 164 6662 6668 1:CAS:528:DC%2BD3cXktFWlu7o%3D
33. RS Fujinami A Zurbriggen HC Powell 1988 Monoclonal antibody defines determinant between Theiler's virus and lipid-like structures J Neuroimmunol 20 25 32 1:STN:280:DyaL1M%2FjsVyisA%3D%3D
34. RS Fujinami A Rosenthal PW Lampert A Zurbriggen M Yamada 1989 Survival of athymic (nu/nu) mice after Theiler's murine encephalomyelitis virus infection by passive administration of neutralizing monoclonal antibody J Virol 63 2081 2087 1:CAS:528:DyaL1MXitFSmtr8%3D
35. SJ Gerety WJ Karpus AR Cubbon RG Goswami MK Rundell JD Peterson SD Miller 1994 Class II-restricted T cell responses in Theiler's murine encephalomyelitis virus-induced demyelinating disease. V. Mapping of a dominant immunopathologic VP2 T cell epitope in susceptible SJL/J mice J Immunol 152 908 918 1:CAS:528:DyaK2cXhtlWlur4%3D
36. + T cell line specific for an immunodominant VP2 epitope J Immunol 152 919 929 1:CAS:528:DyaK2cXhtlaisLo%3D
37. JJG Geurts PK Stys A Minagar S Amor R Zivadinov 2009 Gray matter pathology in (chronic) MS: modern views on an early observation J Neurol Sci 282 12 20
38. S Ghosh E Goldin FH Gordon HA Malchow J Rask-Madsen P Rutgeerts P Vyhnálek Z Zádorová B Chir T Palmer S Donoghue 2003 Natalizumab for active Crohn's disease. (The Natalizumab Pan-European Study Group) N Engl J Med 348 24 32 1:CAS:528:DC%2BD3sXhsVSltg%3D%3D
39. S Girard AS Gosselin I Pelletier F Colbere-Garapin T Couderc B Blondel 2002 Restriction of poliovirus RNA replication in persistently infected nerve cells J Gen Virol 83 1087 1093 1:CAS:528:DC%2BD38XjsFWmsL0%3D
40. A Inoue YK Choe BS Kim 1994 Analysis of antibody responses to predominant linear epitopes of Theiler's murine encephalomyelitis virus J Virol 68 3324 3333 1:CAS:528:DyaK2cXjt1Sqsr0%3D
41. A Inoue C-S Koh M Yamazaki M Ichikawa M Isobe Y Ishihara H Yagita BS Kim 1997 Anti-adhesion molecule therapy in Theiler's murine encephalomyelitis virus-induced demyelinating disease Int Immunol 9 1837 1847 1:CAS:528: DyaK1cXktVSmtg%3D%3D
42. Jelachich ML, Lipton HL (2005) Theiler's murine encephalomyelitis virus (TMEV)-induced demyelination: apoptosis in TMEV infection. In: Lavi E, Constantinescu CS (eds) Experimental models of multiple sclerosis. Springer, New York, pp 697-708
43. AJ Johnson MK Njenga MJ Hansen ST Kuhns L Chen M Rodriguez LR Pease 1999 Prevalent class I-restricted T-cell response to the Theiler's virus epitope Db:VP2121-130 in the absence of endogenous CD4 help, tumor necrosis factor alpha, gamma interferon, perforin, or costimulation through CD28 J Virol 73 3702 3708 1:CAS:528:DyaK1MXis1ens7o%3D
44. + virus peptide-specific T cells in Theiler's virus infection FASEB J 15 2760 2762 1:CAS:528:DC%2BD3MXptFagtbw%3D
45. J-A Kang M Mohindru B-S Kang SH Park BS Kim 2000 Clonal expansion of infiltrating T cells in the spinal cords of SJL/J mice infected with Theiler's virus J Immunol 165 583 590 1:CAS:528:DC%2BD3cXksVKltb8%3D
46. + T cells infiltrating the central nervous systems of SJL/J mice infected with BeAn and DA strains of Theiler's murine encephalomyelitis virus J Virol 76 11780 11784 1:CAS:528:DC%2BD38XoslKjtb8%3D
47. + 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 1:CAS:528:DC%2BD38XkvVGht7c%3D
48. + T cells from virus-infected C57BL/6 mice Virus Res 108 57 61 1:CAS:528:DC%2BD2MXosVKmsA%3D%3D
49. CA Kappel MC Dal Canto RW Melvold BS Kim 1991 Hierarchy of effects of the MHC and T cell receptor beta-chain genes in susceptibility to Theiler's murine encephalomyelitis virus-induced demyelinating disease J Immunol 147 4322 4326 1:STN:280:DyaK38%2FptFOnsQ%3D%3D
50. JFR Kerr AH Wyllie AR Currie 1972 Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics Br J Cancer 26 239 257 1:STN:280:DyaE3s%2FgsFSksw%3D%3D
51. T Kielian 2006 Toll-like receptors in central nervous system glial inflammation and homeostasis J Neurosci Res 83 711 730 1:CAS:528: DC%2BD28XjsFGju7o%3D
52. BS Kim YY Bahk HK Kang RL Yauch J-A Kang MJ Park NM Ponzio 1999 Diverse fine specificity and receptor repertoire of T cells reactive to the major VP1 epitope (VP1230-250) of Theiler's virus: Vβ restriction correlates with T cell recognition of the c-terminal residue J Immunol 162 7049 7057 1:CAS:528:DyaK1MXktF2itb8%3D
53. BS Kim JP Palma A Inoue C-S Koh 2000 Pathogenic immunity in Theiler's virus-induced demyelinating disease: a viral model for multiple sclerosis Arch Immunol Ther Exp (Warsz ) 48 373 379 1:STN:280:DC%2BD3M7jslOqtw%3D%3D
54. S-K Kim M Cornberg XZ Wang HD Chen LK Selin RM Welsh 2005 Private specificities of CD8 T cell responses control patterns of heterologous immunity J Exp Med 201 523 533 1:CAS:528:DC%2BD2MXhs1KmsLg%3D
55. BK Kleinschmidt-DeMasters KL Tyler 2005 Progressive multifocal leukoencephalopathy complicating treatment with natalizumab and interferon beta-1a for multiple sclerosis N Engl J Med 353 369 374 1:CAS:528: DC%2BD2MXms1KntrY%3D
56. IJ Koralnik 2004 New insights into progressive multifocal leukoencephalopathy Curr Opin Neurol 17 365 370
57. T Kuhlmann G Lingfeld A Bitsch J Schuchardt W Brück 2002 Acute axonal damage in multiple sclerosis is most extensive in early disease stages and decreases over time Brain 125 2202 2212
58. A Langer-Gould SW Atlas AJ Green AW Bollen D Pelletier 2005 Progressive multifocal leukoencephalopathy in a patient treated with natalizumab N Engl J Med 353 375 381 1:CAS:528:DC%2BD2MXms1Kntrc%3D
59. OJP Léger TA Yednock L Tanner HC Horner DK Hines S Keen J Saldanha ST Jones LC Fritz MM Bendig 1997 Humanization of a mouse antibody against human alpha-4 integrin: a potential therapeutic for the treatment of multiple sclerosis Hum Antibodies 8 3 16
60. Q Li AG Yafal YM Lee J Hogle M Chow 1994 Poliovirus neutralization by antibodies to internal epitopes of VP4 and VP1 results from reversible exposure of these sequences at physiological temperature J Virol 68 3965 3970 1:STN:280:DyaK2c3ks1OnsA%3D%3D
61. Libbey JE, Fujinami RS (2003) Viral demyelinating disease in experimental animals. In: Herndon RM (ed) Multiple sclerosis: immunology, pathology and pathophysiology. Demos, New York, pp 125-133
62. MY Lin RM Welsh 1998 Stability and diversity of T cell receptor repertoire usage during lymphocytic choriomeningitis virus infection of mice J Exp Med 188 1993 2005 1:CAS:528:DyaK1cXnvFOhurs%3D
63. HL Lipton 1975 Theiler's virus infection in mice: an unusual biphasic disease process leading to demyelination Infect Immun 11 1147 1155 1:STN:280:DyaE2M7jt1GrsA%3D%3D
64. C Liu J Collins E Sharp 1967 The pathogenesis of Theiler's GDVII encephalomyelitis virus infection in mice as studied by immunofluorescent technique and infectivity titrations J Immunol 98 46 55 1:STN:280: DyaF2s%2Fptl2htg%3D%3D
65. G Lovas N Szilágyi K Majtényi M Palkovits S Komoly 2000 Axonal changes in chronic demyelinated cervical spinal cord plaques Brain 123 308 317
66. b-restricted regions of the BeAn strain of Theiler's virus and exhibit different cytokine profiles J Virol 76 3125 3134 1:CAS:528:DC%2BD38Xit1Gqtbc%3D
67. MF Lyon BW Ogunkolade MC Brown DJ Atherton VH Perry 1993 A gene affecting Wallerian nerve degeneration maps distally on mouse chromosome 4 Proc Natl Acad Sci USA 90 9717 9720 1:CAS:528:DyaK3sXms1eru7s%3D
68. Y Matsumoto 2000 Characterization of T cell receptor (TCR) of organ-specific autoimmune disease-inducing T cells and TCR-based immunotherapy with DNA vaccines J Neuroimmunol 110 1 12 1:CAS:528:DC%2BD3cXntF2hsLo%3D
69. Y Matsumoto 2005 New approach to immunotherapy against organ-specific autoimmune diseases with T cell receptor and chemokine receptor DNA vaccines Curr Drug Targets Immune Endocr Metabol Disord 5 73 77 1:CAS:528: DC%2BD2MXisVKktLg%3D
70. Y Matsumoto Y Jee M Sugisaki 2000 Successful TCR-based immunotherapy for autoimmune myocarditis with DNA vaccines after rapid identification of pathogenic TCR J Immunol 164 2248 2254 1:CAS:528:DC%2BD3cXhtlylsrk%3D
71. Y Matsumoto WK Yoon Y Jee K Fujihara T Misu S Sato I Nakashima Y Itoyama 2003 Complementarity-determining region 3 spectratyping analysis of the TCR repertoire in multiple sclerosis J Immunol 170 4846 4853 1:CAS:528: DC%2BD3sXjtVKnu7g%3D
72. PM Matthews N De Stefano S Narayanan GS Francis JS Wolinsky JP Antel DL Arnold 1998 Putting magnetic resonance spectroscopy studies in context: axonal damage and disability in multiple sclerosis Semin Neurol 18 327 336 1:STN:280:DyaK1M%2Fjt1Cktw%3D%3D
73. IJ McCright RS Fujinami 1997 Lack of correlation of Theiler's virus binding to cells with infection J NeuroVirol 3 Suppl 1 S68 S70
74. RW Melvold DM Jokinen RL Knobler HL Lipton 1987 Variations in genetic control of susceptibility to Theiler's murine encephalomyelitis virus (TMEV)-induced demyelinating disease. I. Differences between susceptible SJL/J and resistant BALB/c strains map near the T cell β-chain constant gene on chromosome 6 J Immunol 138 1429 1433 1:STN:280:DyaL2s7htVOjsA%3D%3D
75. L Mestre F Docagne F Correa F Loría M Hernangómez J Borrell C Guaza 2009 A cannabinoid agonist interferes with the progression of a chronic model of multiple sclerosis by downregulating adhesion molecules Mol Cell Neurosci 40 258 266 1:CAS:528:DC%2BD1MXhs1aku70%3D
76. SD Miller SJ Gerety MK Kennedy JD Peterson JL Trotter VK Tuohy C Waltenbaugh MC Dal Canto HL Lipton 1990 Class II-restricted T cell responses in Theiler's murine encephalomyelitis virus (TMEV)-induced demyelinating disease. III. Failure of neuroantigen-specific immune tolerance to affect the clinical course of demyelination J Neuroimmunol 26 9 23 1:STN:280:DyaK3c%2FpsVKrtg%3D%3D
77. SD Miller CL Vanderlugt WS Begolka W Pao RL Yauch KL Neville Y Katz-Levy A Carrizosa BS Kim 1997 Persistent infection with Theiler's virus leads to CNS autoimmunity via epitope spreading Nat Med 3 1133 1136 1:CAS:528: DyaK2sXmsF2is7Y%3D
78. DH Miller OA Khan WA Sheremata LD Blumhardt GPA Rice MA Libonati AJ Willmer-Hulme CM Dalton KA Miszkiel PW O'Connor 2003 A controlled trial of Natalizumab for relapsing multiple sclerosis. (International Natalizumab Multiple Sclerosis Trial Group.) N Engl J Med 348 15 23 1:CAS:528: DC%2BD3sXhtlCntg%3D%3D
79. + T cells make discrete contributions to demyelination and neurologic disease in a viral model of multiple sclerosis J Virol 72 7320 7329 1:CAS:528:DyaK1cXlsVSnu7s%3D
80. P Musette J-F Bureau G Gachelin P Kourilsky 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 1593 1:CAS:528: DyaK2MXms1Kmu7c%3D
81. + T cell epitope region of Theiler's virus in resistant C57BL/6 mice is critical for anti-viral immune responses, viral persistence, and binding to the host cells Virology 360 159 171 1:CAS:528:DC%2BD2sXisVWjtrw%3D
82. MK Njenga C Marques M Rodriguez 2004 The role of cellular immune response in Theiler's virus-induced central nervous system demyelination J Neuroimmunol 147 73 77 1:CAS:528:DC%2BD2cXltVOnug%3D%3D
83. LA O'Neill 2004 Immunology. After the toll rush Science 303 1481 1482
84. Y Ohara A Senkowski JL Fu L Klaman J Goodall M Toth RP Roos 1988 Trypsin-sensitive neutralization site on VP1 of Theiler's murine encephalomyelitis viruses J Virol 62 3527 3529 1:CAS:528:DyaL1cXlsVKhsLo%3D
85. PK Olitsky 1939 Viral effect produced by intestinal contents of normal mice and of those having spontaneous encephalomyelitis Proc Soc Exp Biol Med 41 434 437
86. JK Olson SD Miller 2004 Microglia initiate central nervous system innate and adaptive immune responses through multiple TLRs J Immunol 173 3916 3924 1:CAS:528:DC%2BD2cXnsVWksb4%3D
87. JK Olson AM Girvin SD Miller 2001 Direct activation of innate and antigen-presenting functions of microglia following infection with Theiler's virus J Virol 75 9780 9789 1:CAS:528:DC%2BD3MXnt1Ggs7o%3D
88. T Owens 2006 Animal models for multiple sclerosis Adv Neurol 98 77 89
89. + T cell-mediated apoptosis of activated astrocytes in Theiler's virus-induced demyelination J Immunol 162 6543 6551 1:CAS:528:DyaK1MXjtlKitrc%3D
90. WT Penberthy I Tsunoda 2009 The importance of NAD in multiple sclerosis Curr Pharm Des 15 64 99 1:CAS:528:DC%2BD1MXjvVOms7k%3D
91. GF Rall L Mucke MBA Oldstone 1995 Consequences of cytotoxic T lymphocyte interaction with major histocompatibility complex class I-expressing neurons in vivo J Exp Med 182 1201 1212 1:CAS:528:DyaK2MXovFWrurk%3D
92. L Ramió-Torrentà J Sastre-Garriga GT Ingle GR Davies V Ameen DH Miller AJ Thompson 2006 Abnormalities in normal appearing tissues in early primary progressive multiple sclerosis and their relation to disability: a tissue specific magnetisation transfer study J Neurol Neurosurg Psychiatry 77 40 45
93. + T cell-mediated immunopathology in the brain J Exp Med 170 1045 1050 1:STN:280: DyaL1MzmtFagtw%3D%3D
94. C Rivera-Quiñones D McGavern JD Schmelzer SF Hunter PA Low M Rodriguez 1998 Absence of neurological deficits following extensive demyelination in a class I-deficient murine model of multiple sclerosis Nat Med 4 187 193
95. d transgene suppresses Theiler's virus-induced demyelination in susceptible strains of mice J NeuroVirol 1 111 117 1:STN:280:DyaK2szmsFGhsg%3D%3D
96. M Rodriguez J Leibowitz CS David 1986 Susceptibility to Theiler's virus-induced demyelination. Mapping of the gene within the H-2D region J Exp Med 163 620 631 1:STN:280:DyaL287kt1Gjuw%3D%3D
97. M Rodriguez AK Patick LR Pease CS David 1992 Role of T cell receptor Vβ genes in Theiler's virus-induced demyelination of mice J Immunol 148 921 927 1:CAS:528:DyaK38Xht1Kksrs%3D
98. M Rodriguez N Prayoonwiwat P Zhou C David 1993 Expression of T cell receptor Vβ transcripts in central nervous system of mice susceptible and resistant to Theiler's virus-induced demyelination J Neuroimmunol 47 95 100 1:CAS:528:DyaK2cXhtVCktbw%3D
99. LI Romanova PV Lidsky MS Kolesnikova KV Fominykh AP Gmyl EV Sheval SV Hato FJM van Kuppeveld VI Agol 2009 Antiapoptotic activity of the cardiovirus leader protein, a viral "security" protein J Virol 83 7273 7284 1:CAS:528:DC%2BD1MXosFKlur8%3D
100. RP Roos R Wollmann 1984 DA strain of Theiler's murine encephalomyelitis virus induces demyelination in nude mice Ann Neurol 15 494 499 1:STN:280:DyaL2c3ivF2iuw%3D%3D
101. JW Rose KE Hill Y Wada CIB Kurtz I Tsunoda RS Fujinami AH Cross 1998 Nitric oxide synthase inhibitor, aminoguanidine, reduces inflammation and demyelination produced by Theiler's virus infection J Neuroimmunol 81 82 89 1:CAS:528:DyaK1cXhtVWls7Y%3D
102. JW Rose CT Welsh KE Hill MK Houtchens RS Fujinami JJ Townsend 1999 Contrasting effects of anti-adhesion molecule therapy in experimental allergic encephalomyelitis and Theiler's murine encephalomyelitis J Neuroimmunol 97 110 118 1:CAS:528:DyaK1MXksVygsbo%3D
103. A Rosenthal RS Fujinami PW Lampert 1986 Mechanism of Theiler's virus-induced demyelination in nude mice Lab Invest 54 515 522 1:STN:280:DyaL283gtFGrug%3D%3D
104. JD Rothstein L Jin M Dykes-Hoberg RW Kuncl 1993 Chronic inhibition of glutamate uptake produces a model of slow neurotoxicity Proc Natl Acad Sci USA 90 6591 6595 1:CAS:528:DyaK3sXlsFOms78%3D
105. J Satoh M Nakanishi F Koike S Miyake T Yamamoto M Kawai S Kikuchi K Nomura K Yokoyama K Ota T Kanda T Fukazawa T Yamamura 2005 Microarray analysis identifies an aberrant expression of apoptosis and DNA damage-regulatory genes in multiple sclerosis Neurobiol Dis 18 537 550 1:CAS:528:DC%2BD2MXhvFynsLw%3D
106. BP Schlitt M Felrice ML Jelachich HL Lipton 2003 Apoptotic cells, including macrophages, are prominent in Theiler's virus-induced inflammatory, demyelinating lesions J Virol 77 4383 4388 1:CAS:528:DC%2BD3sXisVKrsLk%3D
107. A Shahar G Frankel Y David A Friedmann 1986 In vitro cytotoxicity and demyelination induced by Theiler viruses in cultures of spinal cord slices J Neurosci Res 16 671 681 1:STN:280:DyaL2s%2Fos1ygsg%3D%3D
108. R Sharma PA Narayana JS Wolinsky 2001 Grey matter abnormalities in multiple sclerosis: proton magnetic resonance spectroscopic imaging Mult Scler 7 221 226 1:STN:280:DC%2BD3MvpvFequw%3D%3D
109. LP Shriver BN Dittel 2006 T-cell-mediated disruption of the neuronal microtubule network: correlation with early reversible axonal dysfunction in acute experimental autoimmune encephalomyelitis Am J Pathol 169 999 1011 1:CAS:528:DC%2BD28XpvFWqs78%3D
110. BV Siegel 1961 Identification of virus isolated from Hodgkin's disease lymph nodes serially passaged in mouse brain Virology 14 378 379
111. JP Smith M Morris-Downes FR Brennan GJ Wallace S Amor 2000 A role for α4-integrin in the pathology following Semliki Forest virus infection J Neuroimmunol 106 60 68 1:CAS:528:DC%2BD3cXjt1aqsbk%3D
112. EY So MH Kang BS Kim 2006 Induction of chemokine and cytokine genes in astrocytes following infection with Theiler's murine encephalomyelitis virus is mediated by the Toll-like receptor 3 Glia 53 858 867
113. K-N Son S Pugazhenthi HL Lipton 2009 Activation of tumor suppressor protein p53 is required for Theiler's murine encephalomyelitis virus-induced apoptosis in M1-D macrophages J Virol 83 10770 10777 1:CAS:528: DC%2BD1MXhtlCltr7K
114. S Steurbaut B Rombaut R Vrijsen 2006 Persistent infection of RAW264.7 macrophages with the DA strain of Theiler's murine encephalomyelitis virus: an in vitro model to study viral persistence J NeuroVirol 12 108 115
115. WG Stroop JR Baringer M Brahic 1981 Detection of Theiler's virus RNA in mouse central nervous system by in situ hybridization Lab Invest 45 504 509 1:STN:280:DyaL387gt1antA%3D%3D
116. WG Stroop M Brahic JR Baringer 1982 Detection of tissue culture-adapted Theiler's virus RNA in spinal cord white matter cells throughout infection Infect Immun 37 763 770 1:STN:280:DyaL3s%2FgsFyhuw%3D%3D
117. M Theiler 1934 Spontaneous encephalomyelitis of mice-a new virus disease Science 80 122 1:STN:280:DC%2BC3cvmvFChtA%3D%3D
118. M Theiler 1937 Spontaneous encephalomyelitis of mice, a new virus disease J Exp Med 65 705 719 1:STN:280:DC%2BC3crjs1elsw%3D%3D
119. ND Tolley I Tsunoda RS Fujinami 1999 DNA vaccination against Theiler's murine encephalomyelitis virus leads to alterations in demyelinating disease J Virol 73 993 1000 1:CAS:528:DyaK1MXmtlWrsw%3D%3D
120. S Tracy NM Chapman KM Drescher K Kono W Tapprich 2006 Evolution of virulence in picornaviruses Curr Top Microbiol Immunol 299 193 209 1:CAS:528:DC%2BD28XivFequ78%3D
121. M Trottier P Kallio W Wang HL 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 7420 7428 1:CAS:528:DC%2BD3MXlsFKkur0%3D
122. I Tsunoda 2008 Axonal degeneration as a self-destructive defense mechanism against neurotropic virus infection Future Virol 3 579 593 1:CAS:528:DC%2BD1cXht12isbrL
123. I Tsunoda RS Fujinami 1996 Two models for multiple sclerosis: experimental allergic encephalomyelitis and Theiler's murine encephalomyelitis virus J Neuropathol Exp Neurol 55 673 686 1:STN:280:DyaK283jvFGlsQ%3D%3D
124. Tsunoda I, Fujinami RS (1999) Theiler's murine encephalomyelitis virus. In: Ahmed R, Chen ISY (eds) Persistent viral infections. Wiley, Chichester, pp 517-536
125. I Tsunoda RS Fujinami 2002 Inside-out versus outside-in models for virus induced demyelination: axonal damage triggering demyelination Springer Semin Immunopathol 24 105 125 1:CAS:528:DC%2BD38Xot12ltrc%3D
126. Tsunoda I, Fujinami RS (2005) TMEV and neuroantigens: Myelin genes and proteins, molecular mimicry, epitope spreading, and autoantibody-mediated remyelination. In: Lavi E, Constantinescu CS (eds) Experimental models of multiple sclerosis. Springer, New York, pp 593-616
127. I Tsunoda Y Iwasaki H Terunuma K Sako Y Ohara 1996 A comparative study of acute and chronic diseases induced by two subgroups of Theiler's murine encephalomyelitis virus Acta Neuropathol (Berl) 91 595 602 1:STN:280: DyaK28znsFehtw%3D%3D
128. I Tsunoda CIB Kurtz RS Fujinami 1997 Apoptosis in acute and chronic central nervous system disease induced by Theiler's murine encephalomyelitis virus Virology 228 388 393 1:CAS:528:DyaK2sXhsFehsb8%3D
129. I Tsunoda ND Tolley DJ Theil JL Whitton H Kobayashi RS Fujinami 1999 Exacerbation of viral and autoimmune animal models for multiple sclerosis by bacterial DNA Brain Pathol 9 481 493 1:CAS:528:DyaK1MXkvFGjtL8%3D
130. S mouse strains Brain Pathol 10 402 418 1:CAS:528:DC%2BD3cXltFSjtLY%3D
131. + cytotoxic cells during Theiler's murine encephalomyelitis virus infection: implications for autoimmunity J Virol 76 12834 12844 1:CAS:528:DC%2BD38XptVynsr8%3D
132. I Tsunoda L-Q Kuang JE Libbey RS Fujinami 2003 Axonal injury heralds virus-induced demyelination Am J Pathol 162 1259 1269
133. I Tsunoda TE Lane J Blackett RS Fujinami 2004 Distinct roles for IP-10/CXCL10 in three animal models, Theiler's virus infection, EAE, and MHV infection, for multiple sclerosis: implication of differing roles for IP-10 Mult Scler 10 26 34 1:CAS:528:DC%2BD2cXht1Kqs7o%3D
134. + T cell clones following virus infection J Virol 79 14640 14646 1:CAS:528:DC%2BD2MXht1Cgsb%2FJ
135. I Tsunoda JE Libbey L-Q Kuang EJ Terry RS Fujinami 2005 Massive apoptosis in lymphoid organs in animal models for primary and secondary progressive multiple sclerosis Am J Pathol 167 1631 1646 1:CAS:528:DC%2BD28Xkt1arsQ%3D%3D
136. I Tsunoda JE Libbey M Kobayashi-Warren RS Fujinami 2006 IFN-γ production and astrocyte recognition by autoreactive T cells induced by Theiler's virus infection: role of viral strains and capsid proteins J Neuroimmunol 172 85 93 1:CAS:528:DC%2BD28XhvVWgsrc%3D
137. I Tsunoda JE Libbey RS Fujinami 2007 TGF-β1 suppresses T cell infiltration and VP2 puff B mutation enhances apoptosis in acute polioencephalitis induced by Theiler's virus J Neuroimmunol 190 80 89 1:CAS:528:DC%2BD2sXht1agsb3O
138. I Tsunoda T Tanaka Y Saijoh RS Fujinami 2007 Targeting inflammatory demyelinating lesions to sites of Wallerian degeneration Am J Pathol 171 1563 1575 1:CAS:528:DC%2BD2sXhtlKqsLjF
139. I Tsunoda T Tanaka EJ Terry RS Fujinami 2007 Contrasting roles for axonal degeneration in an autoimmune versus viral model for multiple sclerosis: when can axonal injury be beneficial? Am J Pathol 170 214 226 1:CAS:528: DC%2BD2sXhsV2gu74%3D
140. I Tsunoda EJ Terry BJ Marble E Lazarides CM Woods RS Fujinami 2007 Modulation of experimental autoimmune encephalomyelitis by VLA-2 blockade Brain Pathol 17 45 55 1:CAS:528:DC%2BD2sXkvFSiu7Y%3D
141. + T cell clones and hybridomas. In: Binder MD, Hirokawa N, Windhorst U (eds) Encyclopedia of neuroscience. Springer, New York, pp 619-625
142. NP Turrin 2008 Central nervous system Toll-like receptor expression in response to Theiler's murine encephalomyelitis virus-induced demyelination disease in resistant and susceptible mouse strains Virol J 5 154
143. Ulrich R, Kalkuhl A, Deschl U, Baumgärtner W (2009) Machine learning approach identifies new pathways associated with demyelination in a viral model of multiple sclerosis. J Cell Mol Med doi: 10.1111/j.1582-4934.2008.00646.x
144. DR Ure M Rodriguez 2002 Preservation of neurologic function during inflammatory demyelination correlates with axon sparing in a mouse model of multiple sclerosis Neuroscience 111 399 411 1:CAS:528:DC%2BD38Xjt1WjsLo%3D
145. Ure DR, Rodriguez M (2005) Histopathology in the Theiler's virus model of demyelination. In: Lavi E, Constantinescu CS (eds) Experimental models of multiple sclerosis. Springer, New York, pp 579-591
146. Ure DR, McGavern DB, Sathornsumetee S, Rodriguez M (2001) The contribution of axonal injury to neurologic dysfunction in Theiler's virus-induced inflammatory demyelinating disease. In: Hommes OR, Clanet M, Wekerle H (eds) Genes and viruses in multiple sclerosis. Elsevier, Amsterdam, pp 79-88
147. EJ Usherwood IC Johnston LJ Lovelidge P Tonks AA Nash 1995 Lymphocyte recognition elements on the VP1 protein of Theiler's virus Immunology 85 190 197 1:CAS:528:DyaK2MXmsl2rs70%3D
148. G Van Assche M Van Ranst R Sciot B Dubois S Vermeire M Noman J Verbeeck K Geboes W Robberecht P Rutgeerts 2005 Progressive multifocal leukoencephalopathy after natalizumab therapy for Crohn's disease N Engl J Med 353 362 368
149. E Verdun G Isoardo A Oggero B Ferrero A Ghezzi E Montanari M Zaffaroni L Durelli 2002 Autoantibodies in multiple sclerosis patients before and during IFN-beta 1b treatment: are they correlated with the occurrence of autoimmune diseases? J Interferon Cytokine Res 22 245 255 1:CAS:528:DC%2BD38Xjt12iuro%3D
150. RM Welsh LK Selin 2002 No one is naive: the significance of heterologous T-cell immunity Nat Rev Immunol 2 417 426 1:CAS:528:DC%2BD38Xksl2murY%3D
151. Z Wroblewska DH Gilden M Wellish LB Rorke KG Warren JS Wolinsky 1977 Virus-specific intracytoplasmic inclusions in mouse brain produced by a newly isolated strain of Theiler virus. I. Virologic and morphologic studies Lab Invest 37 595 602 1:STN:280:DyaE1c%2FptVGqsg%3D%3D
152. Z Wroblewska SU Kim WD Sheffield DH Gilden 1979 Growth of the WW strain of Theiler virus in mouse central nervous system organotypic culture Acta Neuropathol (Berl) 47 13 19 1:STN:280:DyaE1M3ivVWmsA%3D%3D
153. M Yamada A Zurbriggen RS Fujinami 1990 Monoclonal antibody to Theiler's murine encephalomyelitis virus defines a determinant on myelin and oligodendrocytes, and augments demyelination in experimental allergic encephalomyelitis J Exp Med 171 1893 1907 1:STN:280:DyaK3c3nvVentA%3D%3D
154. RL Yauch BS Kim 1994 A predominant viral epitope recognized by T cells from the periphery and demyelinating lesions of SJL/J mice infected with Theiler's virus is located within VP1233-244 J Immunol 153 4508 4519 1:CAS:528:DyaK2MXit1eqsL4%3D
155. RL Yauch K Kerekes K Saujani BS Kim 1995 Identification of a major T-cell epitope within VP3 amino acid residues 24 to 37 of Theiler's virus in demyelination-susceptible SJL/J mice J Virol 69 7315 7318 1:CAS:528: DyaK2MXoslWrsb8%3D
156. RL Yauch JP Palma H Yahikozawa C-S Koh BS Kim 1998 Role of individual T-cell epitopes of Theiler's virus in the pathogenesis of demyelination correlates with the ability to induce a Th1 response J Virol 72 6169 6174 1:CAS:528:DyaK1cXjvFGltbc%3D
157. B Zhu L Luo GRW Moore DW Paty MS Cynader 2003 Dendritic and synaptic pathology in experimental autoimmune encephalomyelitis Am J Pathol 162 1639 1650
158. LJ Zoecklein KD Pavelko J Gamez L Papke DB McGavern DR Ure MK Njenga AJ Johnson S Nakane M Rodriguez 2003 Direct comparison of demyelinating disease induced by the Daniels strain and BeAn strain of Theiler's murine encephalomyelitis virus Brain Pathol 13 291 308
159. A Zurbriggen JM Hogle RS Fujinami 1989 Alteration of amino acid 101 within capsid protein VP-1 changes the pathogenicity of Theiler's murine encephalomyelitis virus J Exp Med 170 2037 2049 1:CAS:528:DyaK3cXltlektA%3D%3D