Restraint stress modulates virus specific adaptive immunity during acute Theiler's virus infection

Brain, Behavior, and Immunity

Volumn 23, Issue 6, 2009, Pages 830-843

  Steelman, Andrew J ^a   Dean, Dana D ^a   Young, Colin R ^a   Smith III, Roger ^a   Prentice, Thomas W ^b   Meagher, Mary W ^b   Welsh, C Jane R ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

^b TEXAS A AND M UNIVERSITY   (United States)

Author keywords

Multiple sclerosis; Restraint stress; T cell; Theiler's virus

Indexed keywords

DEXAMETHASONE; GAMMA INTERFERON; GLUCOCORTICOID; MESSENGER RNA; MIFEPRISTONE; VIRUS PROTEIN;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; IMMOBILIZATION STRESS; IMMUNE DEFICIENCY; IMMUNOMODULATION; LYMPHOCYTE ACTIVATION; LYMPHOCYTE COUNT; LYMPHOCYTE FUNCTION; MOUSE; MULTIPLE SCLEROSIS; MURINE ENCEPHALOMYELITIS VIRUS; NONHUMAN; PERSISTENT VIRUS INFECTION; PRIORITY JOURNAL; RNA VIRUS INFECTION; SPLEEN;

ACUTE DISEASE; ANIMALS; BLOTTING, WESTERN; BODY WEIGHT; CARDIOVIRUS INFECTIONS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CYTOKINES; FEMALE; FLOW CYTOMETRY; GATA3 TRANSCRIPTION FACTOR; IMMUNE TOLERANCE; IMMUNITY, CELLULAR; MICE; PLAQUE ASSAY; RESTRAINT, PHYSICAL; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STRESS, PSYCHOLOGICAL; TH1 CELLS; TH2 CELLS; THEILOVIRUS;

EID: 67649875612     PISSN: 08891591     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbi.2009.03.010     Document Type: Article

References (100)

1. Ackerman K.D., Heyman R., Rabin B.S., Anderson B.P., Houck P.R., Frank E., and Baum A. Stressful life events precede exacerbations of multiple sclerosis. Psychosom. Med. 64 (2003) 916-920
2. Afkarian M., Sedy J.R., Yang J., Jacobson N.G., Cereb N., Yang S.Y., Murphy T.L., and Murphy T.M. T-bet is a STAT1-induced regulator of IL-12R expression in naïve CD4+ T cells. Nat. Immunol. 3 (2002) 549-557
3. Anglen C.S., Truckenmiller M.E., Schell T.D., and Bonneau R.H. The dual role of CD8+ T lymphocytes in the development of stress-induced herpes simplex encephalitis. J. Neuroimmunol. 140 (2003) 13-27
4. Annunziato F., Cosmi L., Santarlasci V., Maggi L., Liotta F., Mazzinghi B., Parente E., Filì L., Ferri S., Frosali F., Giudici F., Romagnani P., Parronchi P., Tonelli F., Maggi E., and Romagnani S. Phenotypic and functional features of human Th17 cells. J. Exp. Med. 204 (2007) 1849-1861
5. Begolka W.S., Haynes L.M., Olson J.K., Padilla J., Neville K.L., Dal Canto M., Palma J., Kim B.S., and Miller S.D. CD8-deficient SJL mice display enhanced susceptibility to Theiler's virus infection and increased demyelinating pathology. J. Neurovirol. 7 (2001) 409-420
6. Bonneau R.H., Sheridan J.F., Feng N.G., and Glaser R. Stress induced suppression of herpes simplex virus (HSV)-specific cytotoxic T lymphocyte and natural killer cell activity and enhancement of acute pathogenesis following local HSV infection. Brain Behav. Immun. 5 (1991) 170-192
7. Borrow P., Tonks P., Welsh C.J., and Nash A.A. The role of CD8+ T cells in the acute and chronic phases of Theiler's murine encephalomyelitis virus-induced disease in mice. J. Gen. Virol. 73 (1992) 1861-1865
8. Brahic M., Bureau J.F., and Michiels T. The genetics of the persistent infection and demyelinating disease caused by Theiler's virus. Annu. Rev. Microbiol. 59 (2005) 279-298
9. Buljevac D., Flach H.Z., Hop W.C., Hijdra D., Laman J.D., Savelkoul H.F., van Der Meché F.G., van Doorn P.A., and Hintzen R.Q. Prospective study on the relationship between infections and multiple sclerosis exacerbations. Brain 125 (2002) 952-960
10. Campbell T., Meagher M.W., Sieve A., Scott B., Storts R., Welsh T.H., and Welsh C.J.R. The effects of restraint stress on the neuropathogenesis of Theiler's virus infection: I. Acute disease. Brain Behav. Immun. 15 (2001) 235-254
11. Clatch R.J., Miller S.D., Metzner R., Dal Canto M.C., and Lipton H.L. Monocytes/macrophages isolated from the mouse central nervous system contain infectious Theiler's murine encephalomyelitis virus (TMEV). Virology 176 (1990) 244-254
12. Cohen S., Tyrrell D.A., and Smith A.P. Psychological stress and susceptibility to the common cold. N. Engl. J. Med. 325 (1991) 606-612
13. Correa S.G., Rodriguez-Galán M.C., Rivero V.E., and Riera C.M. Chronic varied stress modulates experimental autoimmune encephalomyelitis in Wistar rats. Brain Behav. Immun. 12 (1998) 134-148
14. DeLano R.M., and Mallery S.R. Stress-related modulation of central nervous system immunity in a murine model of herpes simplex encephalitis. J. Neuroimmunol. 89 (1998) 51-58
15. Dhabhar F.S., and McEwen B.S. Acute stress enhances while chronic stress suppresses immune function in vivo: a potential role for leukocyte trafficking. Brain Behav. Immun. 11 (1997) 286-306
16. Dobbs C.M., Feng N., Beck F.M., and Sheridan J.F. Neuroendocrine regulation of cytokine production during experimental influenza viral infection: Effects of restraint stress-induced elevation in endogenous corticosterone. J. Immunol. 157 (1996) 1870-1877
17. Elenkov I.J. Glucocorticoids and the Th1/Th2 balance. Ann. NY Acad. Sci. 1024 (2004) 138-146
18. Elftman M.D., Norbury C.C., Bonneau R.H., and Truckenmiller M.E. Corticosterone impairs dendritic cell maturation and function. Immunology 122 (2007) 279-290
19. Fazakerley J.K., and Walker R. Virus demyelination. J. Neurovirol. 9 (2003) 148-164
20. Feng N., Pagniano R., Tovar C.A., Bonneau R.H., Sheridan J.F., Glaser R., and Moynihan J.A. The effect of restraint stress on the kinetics, magnitude, and isotype of the humora immune response to influenza virus infection. Brain Behav. Immun. 38 (1991) 129-137
21. Ferber I.A., Brocke S., Taylor-Edwards C., Ridgway W., Dinisco C., Steinman L., Dalton D., and Fathman C.G. Mice with a disrupted IFN-gamma gene are susceptible to the induction of experimental autoimmune encephalomyelitis (EAE). J. Immunol. 156 (1996) 5-7
22. Fiette L., Aubert C., Brahic M., and Rossi C.P. Theiler's virus infection of β-2 microglobulin-deficient mice. J. Virol. 67 (1993) 589-592
23. Franchimont D., Galon J., Gadina M., Visconti R., Zhou Y., Aringer M., Frucht D.M., Chrousos G.P., and O'Shea J.J. Inhibition of Th1 immune response by glucocorticoids: dexamethasone selectively inhibits IL-12-induced Stat4 phosphorylation in T lymphocytes. J. Immunol. 164 (2000) 1768-1774
24. Freeman M.L., Sheridan B.S., Bonneau R.H., and Hendricks R.L. Psychological stress compromises CD8+ T cell control of latent herpes simplex virus type 1 infections. J. Immunol. 179 (2007) 322-328
25. Gale C., and Martyn C.N. Migrant studies in multiple sclerosis. Prog. Neurobiol. 47 (1995) 425-448
26. Gerety S.J., Clatch R.J., Lipton H.L., Goswami R.G., Rundell M.K., and Miller S.D. Class II-restricted T cell responses in Theiler's murine encephalomyelitis virus-induced demyelinating disease IV. Identification of an immunodominant T cell determinant on the N-terminal end of the VP2 capsid protein in susceptible SJL/J mice. J. Immunol. 146 (1991) 2401-2408
27. Gerety S., Karpus W., Cubbon A.R., Goswami R., Randell M.K., Peterson J., and Miller S.D. Class II-restricted T cell responses in Theieler's murine encephalomyelitis virus-induced demyelinating disease V. Mapping of a dominant immunopathological VP2 T cell epitope in susceptible mice. J. Immunol. 152 (1994) 908-918
28. Griffin A.C., Lo W.D., Wolny A.C., and Whitacre C.C. Suppression of experimental autoimmune encephalomyelitis by restraint stress: Sex differences. J. Neuroimmunol. 44 (1993) 103-116
29. Hu X., Li W.P., Meng C., and Ivashkiv L.B. Inhibition of IFN-γ signaling by glucocorticoids. J. Immunol. 170 (2003) 4833-4839
30. Ifergan I., Kébir H., Bernard M., Wosik K., Dodelet-Devillers A., Cayrol R., Arbour N., and Prat A. The blood-brain barrier induces differentiation of migrating monocytes into Th17-polarizing dendritic cells. Brain 131 (2008) 785-799
31. Inoue A., Koh C.S., Yamazaki M., Yahikozawa H., Ichikawa M., Yagita H., and Kim B.S. Suppressive effects on Theiler's murine encephalomyelitis virus-induced demyelinating disease by the administration of anti-IL-12 antibody. J. Immunol. 161 (1998) 5586-5593
32. Jee Y.K., Gilmour J., Kelly A., Bowen H., Richards D., Soh C., Smith P., Hawrylowiez C., Cousins D., Lee T., and Lavender P. Repression of interleukin-5 transcription by glucocorticoid receptor targets GATA3 signaling and involves histone deacetylase recruitment. J. Biol. Chem. 280 (2005) 23243-23250
33. Jeffery D.R. Failure of allogeneic bone marrow transplantation to arrest disease activity in multiple sclerosis. Mult. Scler. 13 (2007) 1071-1075
34. Johnson A.J., Upshaw J., Pavelko K.D., Rodriguez M., and Pease L.R. Preservation of motor function by inhibition of CD8+ virus peptide-specific T cells in Theiler's virus infection. FASEB J. 15 (2001) 2760-2762
35. Kang B.S., Lyman M.A., and Kim B.S. The majority of infiltrating CD8 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 (2002) 6577-6585
36. Kang B.S., Palma J.P., Lyman M.A., Dal Canto M., and Kim B.S. Antibody response is required for protection from Theiler's virus induced encephalitis in C57BL/6 mice in the absence of CD8+ cells. Virology 340 (2005) 84-94
37. Kebir H., Kreymborg K., Ifergan I., Dodelet-Devillers A., Cayrol R., Bernard M., Giuliani F., Arbour N., Becher B., and Prat A. Human TH17 lymphocytes promote blood-brain barrier disruption and central nervous system inflammation. Nat. Med. 10 (2007) 1173-1175
38. Krakowski M., and Owens T. Interferon-gamma confers resistance to experimental allergic encephalomyelitis. Eur. J. Immunol. 26 (1996) 1641-1646
39. Kurtzke J.F., and Heltberg A. Multiple sclerosis in the Faroe Islands: an epitome. J. Clin. Epidemiol. 54 (2001) 1-22
40. Levillayer E., Mas M., Levi-Acobas F., Brahic M., and Bureau J.E. Interleukin 22 is a candidate gene for Tmevp3, a locus controlling Theiler's virus-induced neurological disease. Genetics 176 (2007) 1835-1844
41. Levine S., Strebel R., Wenk E.J., and Harman P.J. Suppression of experimental allergic encephalomyelitis by stress. Proc. Soc. Exp. Biol. Med. 109 (1962) 294-298
42. Liang S.C., Tan X.Y., Luxenberg D.P., Karim R., Dunussi-Joannopoulos K., Collins M., and Fouser L.A. Interleukin (IL)-22 and IL-17 are coexpressed by Th17 cells and cooperatively enhance expression of antimicrobial peptides. J. Exp. Med. 203 (2006) 2271-2279
43. Liberman A.C., Refojo D., Jimena D., Toscano M., Rein T., Holsboer F., and Arzt E. The activated glucocorticoid receptor inhibits the transcription factor T-bet by direct protein-protein interaction. FASEB J. 21 (2007) 1177-1188
44. Liberman, A.C., Druker, J., Refojo, D., Holsboer, F., Arzt, E., 2009. Glucocorticoids inhibit GATA-3 phosphorylation and activity in T cells. FASEB J. doi:10.1096/fj.08-121236 [Epub ahead of print].
45. Lin X., Ma X., Rodriguez M., and Roos R.P. CD4+ T cells are important for clearance of DA strain of TMEV from the central nervous system of SJL/J mice. Int. Immunol. 16 (2004) 1237-1240
46. Lipton H.L. Theiler's virus infection in mice: an unusual biphasic disease process leading to demyelination. Infect. Immun. 11 (1975) 1147-1155
47. Lipton H.L., and Melvold R. Genetic analysis of susceptibility to Theiler's virus induced demyelinating disease in mice. J. Immunol. 132 (1984) 1821-1825
48. Lord G.M., Rao R.M., Choe H., Sullivan B.M., Lichtman A.H., Luscinskas F.W., and Glimcher L.H. T-bet is required for optimal proinflammatory CD4+ T-cell trafficking. Blood 106 (2005) 3432-3439
49. Lucchinetti C., Bruck W., Parisi J., Scheithauer B., Rodriguez M., and Lassmann H. Heterogeneity of multiple sclerosis lesions: Implications for the pathogenesis of demyelination. Ann. Neurol. 47 (2000) 707-717
50. Lugo-Villarino G., Maldonado-Lopez R., Possemato R., Penaranda C., and Glimcher L.H. T-bet is required for optimal production of IFN-γ and antigen-specific T cell activation by dendritic cells. Proc. Natl. Acad. Sci. USA 100 (2003) 7749-7754
51. Matsui M., Moriya O., Yoshimoto T., and Akatsuka T. T-bet is required for protection against vaccinia virus infection. J. Virol. 79 (2005) 12798-12806
52. Mayer K.D., Mohrs K., Reiley W., Wittmer S., Kohlmeier J.E., Pearl J.E., Cooper A.M., Johnson L.L., Woodland D.L., and Mohrs M. Cutting edge: T-bet and IL-27R are critical for in vivo IFN-gamma production by CD8 T cells during infection. J. Immunol. 180 (2008) 693-697
53. Mi W., Belyavskyi M., Johnson R.R., Sieve A.N., Storts R., Meagher M.W., and Welsh C.J.R. Alterations in chemokine expression following Theiler's virus infection and restraint stress. J. Neuroimmunol. 151 (2004) 103-115
54. Mi W., Prentice T.W., Young C.R., Johnson R.R., Sieve A.N., Meagher M.W., and Welsh C.J.R. Restraint stress decreases virus-induced pro-inflammatory cytokine expression during acute Theiler's virus infection. J. Neuroimmunol. 178 (2006) 49-61
55. Mi W., Young C.R., Storts R., Steelman A., Meagher M.W., and Welsh C.J.R. Stress alters pathogenecity and facilitates systemic dissemination of Theiler's virus. Microb. Pathog. 41 (2006) 133-143
56. Miller D.J., Rivera-Quiñones C., Njenga M.K., Leibowitz J., and Rodriguez M. Spontaneous CNS remyelination in beta 2 microglobulin-deficient mice following virus-induced demyelination. J. Neurosci. 15 (1995) 8345-8352
57. Mizobe K., Kishihara K., Ezz-Din El-Naggar R., Madkour G.A., Kubo C., and Nomoto K. Restraint stress-induced elevation of endogenous glucocorticoid suppresses migration of granulocytes and macrophages to an inflammatory locus. J. Neuroimmunol. 73 (1997) 81-89
58. Mohindru M., Kang B., and Kim B.S. Initial capsid-specific CD4+ T cell responses protect against Theiler's murine encephalomyelitis virus-induced demyelinating disease. Eur. J. Immunol. 36 (2006) 1-10
59. Mohr D.C., Hart S.L., Julian L., Cox D., and Pelletier D. Association between stressful life events and exacerbation in multiple sclerosis: a meta-analysis. BMJ 328 (2004) 731-735
60. Murray P.D., McGavern D.B., Lin X., Njenga M.K., Leibowitz J., Pease L.R., and Rodriguez M. Perforin-dependent neurologic injury in a viral model of multiple sclerosis. J. Neurosci. 18 (1998) 7306-7314
61. Murray P.D., McGavern D.B., Pease L.R., and Rodriguez M. Cellular sources and targets of IFN-γ-mediated protection against viral demyelination and neurological deficits. Eur. J. Immunol. 32 (2002) 606-615
62. Noseworthy J.H., Lucchinetti C., Rodriguez M., and Weinshenker B.G. Multiple sclerosis. N. Eng. J. Med. 343 (2000) 938-952
63. Oleszak E.L., Chang J.R., Friedman H., Katsetos C.D., and Platsoucas C.D. Theiler's virus infection: a model for multiple sclerosis. Clin. Microbiol. Rev. 17 (2004) 174-207
64. Ottaway C.A., and Husband A.J. The influence of neuroendocrine pathways on lymphocyte migration. Immunol. Today 15 (1994) 511-517
65. Palma J.P., Lee H.G., Mohindru M., Kang B.S., Dal Canto M., Miller S.D., and Kim B.S. Enhanced susceptibility to Theiler's virus-induced demyelinating disease in perforin-deficient mice. J. Neuroimmunol. 116 (2001) 125-135
66. Panitch H.S., Hirsch R.L., Haley A.S., and Johnson K.P. Exacerbations of multiple sclerosis in patients treated with gamma interferon. Lancet. 1 (1987) 893-895
67. Peng S.L., Szabo S.J., and Glimcher L.H. T-bet regulates IgG2a class switching and pathogenic autoantibody production. Proc. Natl. Acad. Sci. USA 99 (2002) 5545-5550
68. Pullen L.C., Miller S.D., Dal Canto M.C., and Kim B.S. Class I-deficient resistant mice intracerebrally inoculated with Theiler's virus show an increased T cell response to viral antigens and susceptibility to demyelination. Eur. J. Immunol. 23 (1993) 2287-2293
69. Rodriguez M., and David C.S. Demyelination induced by Theiler's virus: influence of the H-2 haplotype. J. Immunol. 135 (1985) 2145-2148
70. Rodriguez M., Pavelko K., and Coffman R.L. Gamma interferon is critical for resistance to Theiler's virus-induced demyelination. J. Virol. 69 (1995) 7286-7290
71. Rodriguez M., Zoecklein L.J., Howe C.L., Pavelko K.D., Gamez J., Nakane S., and Papke L.M. Gamma interferon is critical for neuronal viral clearance and protection in a susceptible mouse strain following early intracranial Theiler's murine encephalomyelitis virus infection. J. Virol. 77 (2003) 12252-12265
72. Rodriguez M., Zoecklein L., Gamez J.D., Pavelko K.D., Papke L.M., Nakane S., Howe C., Radhakrishnan S., Hansen M.J., David C.S., Warrington A.E., and Pease L.R. STAT4- and STAT6-signaling molecules in a murine model of multiple sclerosis. FASEB J. 20 (2006) 343-345
73. Rossi C.P., McAllister A., Tanguy M., Kagi D., and Brahic M. Theiler's virus infection of perforin-deficient mice. J. Virol. 72 (1998) 4515-4519
74. Rueckert R.R., and Pallansch M.A. Preparation and characterization of encephalomyocarditis (EMC) virus. Methods Enzymol. 78 (1981) 315-325
75. Sheridan J.F., Feng N., Bonneau R.H., Allen C.M., Huneycutt B.S., and Glaser R. Restraint stress differentially affects anti-viral cellular and humoral immune responses in mice. J. Neuroimmunol. 3 (1991) 245-255
76. Sieve A.N., Steelman A.J., Young C.R., Storts R., Welsh T.H., Welsh C.J.R., and Meagher M.W. Chronic restraint stress during early Theiler's virus infection exacerbates the subsequent demyelinating disease in SJL mice. J. Neuroimmunol. 155 (2004) 103-118
77. Sullivan B.M., Juedes A., Szabo S.J., von Herranth M., and Glimcher L.H. Antigen driven effector CD8 T cell function regulated by T-bet. Proc. Natl. Acad. Sci. USA 100 (2003) 15818-15823
78. Svensson A., Nordstrom I., Sun J.-B., and Eriksson K. Protective immunity to genital herpes simplex virus type 2 infection is mediated by T-bet. J. Immunol. 174 (2005) 6266-6273
79. Szabo S.J., Kim S.T., Costa G.L., Zhang X., Fathman C.G., and Glimcher L.H. A novel transcription factor, T-bet, directs Th1 lineage commitment. Cell 100 (2000) 655-669
80. Szabo S.J., Sullivan B.M., Stemmann C., Satoskar A.R., Sleckman B.P., and Glimcher L.H. Distinct effects of T-bet in Th1 lineage commitment and IFN-γ production in CD4 and CD8 T cells. Science 295 (2002) 338-342
81. Theiler M. Spontaneous encephalomyelitis of mice, a new virus disease. J. Exp. Med. 65 (1937) 705-719
82. Townsend M.J., Weinmann A.S., Matsuda J.L., Salomon R., Farnham P.J., Biron C.A., Gapin L., and Glimcher L.M. T-bet regulates the terminal maturation and homeostasis of NK and Valpha14i NKT cells. Immunity 20 (2004) 477-494
83. Truckenmiller M.E., Princiotta M.F., Norbury C.C., and Bonneau R.H. Corticosterone impairs MHC class I antigen presentation by dendritic cells via reduction of peptide generation. J. Neuroimmunol. 160 (2005) 48-60
84. Tseng R.J., Padgett D.A., Dhabhar F.S., Engler H., and Sheridan J.F. Stress induced modulation of NK activity during influenza viral infection: role of glucocorticoids and opioids. Brain Behav. Immun. 19 (2005) 153-164
85. Usui T., Preiss J.C., Kanno Y., Yao Z.J., Bream J.H., O'Shea J.J., and Strober W. T-bet regulates Th1 responses through essential effects on GATA-3 function rather than on IFNG gene acetylation and transcription. J. Exp. Med. 203 (2006) 755-766
86. Vaknin-Dembinsky A., Balashov K., and Weiner H.L. IL-23 is increased in dendritic cells in multiple sclerosis and down-regulation of IL-23 by antisense oligos increases dendritic cell IL-10 production. J. Immunol. 176 (2006) 7768-7774
87. Webster J.I., Tonelli L., and Sternberg E.M. Neuroendocrine regulation of immunity. Annu. Rev. Immunol. 20 (2002) 125-163
88. Wei H., Zheng X., Lou D., Zhang L., Zhang R., Sun R., and Tian Z. Tumor induced suppression of interferon-γ production and enhancement of Interleukin-10 production by natural killer (NK) cells: Paralleled to CD4+ T cells. Mol. Immunol. 42 (2005) 1023-1031
89. Welsh C.J., Tonks P., Nash A.A., and Blakemore W.F. The effect of L3T4 T cell depletion on the pathogenesis of Theiler's murine encephalomyelitis virus infection in CBA mice. J. Gen. Virol. 68 (1987) 1659-1667
90. Welsh C.J.R., Blakemore W.F., Tonks P., Borrow P., and Nash A.A. Theiler's murine encephalomyelitis virus infection in mice: a persistent viral infection of the central nervous system which induces demyelination. In: Dimmock N. (Ed). Immune Responses, Virus Infections and Disease (1989), Oxford University Press, Oxford 125-147
91. Welsh C.J.R., Sapatino B., Rosenbaum B., Smith R., and Linthicum D.S. Correlation between susceptibility to demyelination and interferon gamma induction of major histocompatibility complex class II antigens on murine cerebrovascular endothelial cells. J. Neuroimmunol. 48 (1993) 91-98
92. Welsh C.J.R., Bustamante L., Nayak M., Welsh T.H., Dean D.D., and Meagher M.W. The effects of restraint stress on the neuropathogenesis of Theiler's virus infection II: NK cell function and cytokine levels in acute disease. Brain Behav. Immun. 18 (2004) 166-174
93. Willenborg D.O., Fordham S., Bernard C.C., Cowden W.B., and Ramshaw I.A. IFN-gamma plays a critical down-regulatory role in the induction and effector phase of myelin oligodendrocyte glycoprotein-induced autoimmune encephalomyelitis. J. Immunol. 157 (1996) 3223-3327
94. Witowski J., Ksiazek A., and Jorres A. Interleukin-17: a mediator of inflammatory responses. Cell. Mol. Life Sci. 61 (2004) 567-579
95. Wurster A.L., Tanaka T., and Grusby M.J. The biology of Stat4 and Stat6. Oncogene 19 (2000) 2577-2584
96. Xu W., and Zhang J.J. Stat1-dependent synergistic activation of T bet for IgG2a production during early stage of B cell activation. J. Immunol. 175 (2005) 7419-7424
97. Yamamoto K., Kawamura I., Tominaga T., Nomura T., Kohda C., Ito J., and Mitsuyama M. Listeriolysin O, acytolysin derived from Listeria monocytogenes, inhibits generation of ovalbumin-specific Th2 immuno response by skewing maturation of antigen-specific T cells into Th1 cells. Clin. Exp. Immunol. 142 (2005) 268-274
98. Young E.E., Prentice T.W., Satterlee D., McCullough H., Sieve A.N., Johnson R.R., Welsh T.H., Welsh C.J.R., and Meagher M.W. Glucocorticoid exposure alters the pathogenesis of Theiler's murine encephalomyelitis virus during acute infection. Physiol. Behav. 95 (2008) 63-71
99. Zhang D., Kishihara K., Wang B., Mizobe K., Kubo C., and Nomoto K. Restraint stress-induced immunosuppression by inhibiting leukocyte migration and Th1 cytokine expression during the intraperitoneal infection of Listeria monocytogenes. J. Neuroimmunol. 92 (1998) 139-151
100. Zheng L., Calenoff M.A., and Dal Canto M.C. Astrocytes not microglia are the main cells responsible for viral persistence in Theiler's murine encephalomyelitis virus infection leading to demyelination. J. Neuroimmunol. 118 (2001) 256-267