Journal of Neuroimmunology
Volume 178, Issue 1 , Pages 49-61 , September 2006

Restraint stress decreases virus-induced pro-inflammatory cytokine mRNA expression during acute Theiler's virus infection

  • W. Mi

      Affiliations

    • Department of Veterinary Integrative Biosciences, College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, TX 77843, USA
    • Genetics Program, Texas A&M University, College Station, TX 77843, USA
    • ,
  • T.W. Prentice

      Affiliations

    • Department of Psychology, College of Liberal Arts, Texas A&M University, College Station, TX 77843, USA
    • ,
  • C.R. Young

      Affiliations

    • Department of Veterinary Integrative Biosciences, College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, TX 77843, USA
    • Department of Psychology, College of Liberal Arts, Texas A&M University, College Station, TX 77843, USA
    • ,
  • R.R. Johnson

      Affiliations

    • Department of Psychology, College of Liberal Arts, Texas A&M University, College Station, TX 77843, USA
    • ,
  • A.N. Sieve

      Affiliations

    • Department of Psychology, College of Liberal Arts, Texas A&M University, College Station, TX 77843, USA
    • ,
  • M.W. Meagher

      Affiliations

    • Department of Psychology, College of Liberal Arts, Texas A&M University, College Station, TX 77843, USA
    • ,
  • C.J.R. Welsh

      Affiliations

    • Department of Veterinary Integrative Biosciences, College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, TX 77843, USA
    • Genetics Program, Texas A&M University, College Station, TX 77843, USA
    • Department of Veterinary Pathobiology, College of Veterinary Medicine, Texas A&M University, College Station, TX 77843, USA
    • Corresponding Author InformationCorresponding author. Department of Veterinary Integrative Biosciences, College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, TX 77843-4458, USA. Tel.: +1 979 862 4974; fax: +1 979 847 8981.

Received 2 December 2005 ,Revised 13 May 2006 ,Accepted 17 May 2006.

References 

  1. Aubagnac S, Brahic M, Bureau JF. Viral load and a locus on chromosome 11 affect the late clinical disease caused by Theiler's virus. J. Virol. 1999;73:7965–7971
  2. Begolka WS, Vanderlugt CL, Rahbe SM, Miller SD. Differential expression of inflammatory cytokines parallels progression of central nervous system pathology in two clinically distinct models of multiple sclerosis. J. Immunol. 1998;161:4437–4446
  3. Benedict CA, Banks TA, Senderowicz L, Ko M, Britt WJ, Angulo A, et al. Lymphotoxins and cytomegalovirus cooperatively induce interferon-beta, establishing host-virus detente. Immunity. 2001;15:617–626
  4. Biron CA. Role of early cytokines, including alpha and beta interferons (IFNalpha/ beta), in innate and adaptive immune responses to viral infections. Semin. Immunol. 1998;10:383–390
  5. Bonneau RH, Sheridan JF, Feng NG, 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. 1991;5:170–192
  6. Borrow P, Welsh CJ, Nash AA. Study of the mechanisms by which CD4+T cells contribute to protection in Theiler's murine encephalomyelitis. Immunology. 1993;80:502–506
  7. Borrow P, Welsh CJ, Dean D, Tonks P, Blakemore WF, Nash AA. Investigation of the role of autoimmune responses to myelin in the pathogenesis of TMEV-induced demyelinating disease. Immunology. 1998;93:478–484
  8. Brahic M, Bureau JF. Genetics of susceptibility to Theiler's virus infection. BioEssays. 1998;20:627–633
  9. Campbell T, Meagher MW, Sieve A, Scott B, Storts R, Welsh TH, et al. The effects of restraint stress on the neuropathogenesis of Theiler's virus infection: I. Acute disease. Brain Behav. Immun. 2001;15:235–254
  10. Chang JR, Zaczynska E, Katsetos CD, Platsoucas CD, Oleszak EL. Differential expression of TGF-beta, IL-2, and other cytokines in the CNS of Theiler's murine encephalomyelitis virus-infected susceptible and resistant strains of mice. Virology. 2000;278:346–360
  11. Chesler DA, Reiss CS. The role of IFN-gamma in immune responses to viral infections of the central nervous system. Cytokine Growth Factor Rev. 2002;13:441–454
  12. Dal Canto MC, Calenoff MA, Miller SD, Vanderlugt CL. Lymphocytes from mice chronically infected with Theiler's murine encephalomyelitis virus produce demyelination of organotypic cultures after stimulation with the major encephalitic epitope of myelin proteolipid protein. Epitope spreading in TMEV infection has functional activity. J. Neuroimmunol. 2000;104:79–84
  13. Dinarello CA. Interleukin-18 and the treatment of rheumatoid arthritis. Rheum. Dis. Clin. North Am. 2004;30:417–434
  14. Dhabhar FS, Miller AH, McEwen BS, Spencer RL. Effects of stress on immune cell distribution. Dynamics and hormonal mechanisms. J. Immunol. 1995;154:5511–5527
  15. Dobbs CM, Vasquez M, Glaser R, Sheridan JF. Mechanisms of stress-induced modulation of viral pathogenesis and immunity. J. Neuroimmunol. 1993;48:151–160
  16. Drescher KM, Murray PD, Lin X, Carlino JA, Rodriguez M. TGF-beta 2 reduces demyelination, virus antigen expression, and macrophage recruitment in a viral model of multiple sclerosis. J. Immunol. 2000;164:3207–3213
  17. Ehlers S, Holscher C, Scheu S, Tertilt C, Hehlgans T, Suwinski J, et al. The lymphotoxin beta receptor is critically involved in controlling infections with the intracellular pathogens Mycobacterium tuberculosis and Listeria monocytogenes. J. Immunol. 2003;170:5210–5218
  18. Elenkov IJ, Chrousos GP. Stress hormones, proinflammatory and antiinflammatory cytokines, and autoimmunity. Ann. N.Y. Acad. Sci. 2002;966:290–303
  19. Elenkov IJ, Wilder RL, Chrousos GP, Vizi ES. The sympathetic nerve-an integrative interface between two supersystems: the brain and the immune system. Pharmacol. Rev. 2000;52:595–638
  20. Fleshner M, Hermann J, Lockwood LL, Laudenslager ML, Watkins LR, Maier SF. Stressed rats fail to expand the CD45RC+CD4+ (Th1-like) T cell subset in response to KLH: possible involvement of IFN-gamma. Brain Behav. Immun. 1995;9:101–112
  21. Franchimont D. Overview of the actions of glucocorticoids on the immune response: a good model to characterize new pathways of immunosuppression for new treatment strategies. Ann. N. Y. Acad. Sci. 2004;1024:124–137
  22. Gerety SJ, Karpus WJ, Cubbon AR, Goswami RG, Rundell MK, Peterson JD, et al. 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. 1994;152:908–918
  23. Gilden DH, Lipton HL. Infectious causes of multiple sclerosis. Lancet Neurol. 2005;4:195–202
  24. Haddad JJ, Saade NE, Safieh-Garabedian B. Cytokines and neuro-immune-endocrine interactions: a role for the hypothalamic-pituitary-adrenal revolving axis. J. Neuroimmunol. 2002;133(1-2):1–19(Dec, Review)
  25. Hunzeker J, Padgett DA, Sheridan PA, Dhabhar FS, Sheridan JF. Modulation of natural killer cell activity by restraint stress during an influenza A/PR8 infection in mice. Brain Behav. Immun. 2004;18:526–535
  26. Ito M, O'Malley JA. Anti-viral effects of recombinant human tumor necrosis factor. Lymphokine Res. 1987;6:309–318
  27. Karagiannidis C, Akdis M, Holopainen P, Woolley NJ, Hense G, Ruckert B, et al. Glucocorticoids up-regulate FOXP3 expression and regulatory T cells in asthma. J. Allergy Clin. Immunol. 2004;114:1425–1433
  28. Klimstra WB, Nguyen KB, Biron CA, Johnston RE, Karp CL. Interferon beta in multiple sclerosis: is IL-12 suppression the key?. J. Virol. 2000;74:3366–3378
  29. Lin X, Ma X, Rodriguez M, Feng X, Zoecklein L, Fu YX, et al. Membrane lymphotoxin is required for resistance to Theiler's virus infection. Int. Immunol. 2003;15:955–962
  30. Lipton HL. Theiler's virus infection in mice: an unusual biphasic disease process leading to demyelination. Infect. Immun. 1975;11:1147–1155
  31. Lipton HL, Kratochvil J, Sethi P, Dal Canto MC. Theiler's virus antigen detected in mouse spinal cord 2 1/2 years after infection. Neurology. 1984;34:1117–1119
  32. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 2001;25:402–408
  33. Lyman MA, Myoung J, Mohindru M, Kim BS. Quantitative, not qualitative, differences in CD8(+) T cell responses to Theiler's murine encephalomyelitis virus between resistant C57BL/6 and susceptible SJL/J mice. Eur. J. Immunol. 2004;34:2730–2739
  34. Mabbott NA, Young J, McConnell I, Bruce ME. Follicular dendritic cell dedifferentiation by treatment with an inhibitor of the lymphotoxin pathway dramatically reduces scrapie susceptibility. J. Virol. 2003;77:6845–6854
  35. Marshall WL, Brinkman BM, Ambrose CM, Pesavento PA, Uglialoro AM, Teng E, et al. Signaling through the lymphotoxin-beta receptor stimulates HIV-1 replication alone and in cooperation with soluble or membrane-bound TNF-alpha. J. Immunol. 1999;162:6016–6023
  36. Mi W, Belyavskyi M, Johnson RR, Sieve AN, Storts R, Meagher MW, et al. Alterations in chemokine expression following Theiler's virus infection and restraint stress. J. Neuroimmunol. 2004;151:103–115
  37. Mi, W., Young, C.R., Storts, R., Steelman, A., Meagher, M.W., Welsh, C.J., in press. Stress alters pathogenecity and facilitates systemic dissemination of Theiler's virus. Microb. Pathog.
  38. Miller SD, VanDerlugt CL, Begolka WS, Pao W, Yauch RL, Neville KL, et al. Persistent infection with Theiler's virus leads to CNS autoimmunity via epitope spreading. Nat. Med. 1997;3:1133–1136
  39. Mohr DC, Hart SL, Julian L, Cox D, Pelletier D. Association between stressful life events and exacerbation in Multiple Sclerosis: a meta analysis. BMJ. 2004;328(7442):731–735
  40. Murray PD, McGavern DB, Pease LR, Rodriguez M. Cellular sources and targets of IFN-gamma-mediated protection against viral demyelination and neurological deficits. Eur. J. Immunol. 2002;32:606–615
  41. Oldstone MB, Race R, Thomas D, Lewicki H, Homann D, Smelt S, et al. Lymphotoxin-alpha-and lymphotoxin-beta-deficient mice differ in susceptibility to scrapie: evidence against dendritic cell involvement in neuroinvasion. J. Virol. 2002;76:4357–4363
  42. Oleszak EL, Chang JR, Friedman H, Katsetos CD, Platsoucas CD. Theiler's virus infection: a model for multiple sclerosis. Clin. Microbiol. Rev. 2004;17:174–207
  43. Olson JK, Girvin AM, Miller SD. Direct activation of innate and antigen presenting functions of microglia following infection with Theiler's virus. J. Virol. 2001;75:9780–9789
  44. Paya CV, Patick AK, Leibson PJ, Rodriguez M. Role of natural killer cells as immune effectors in encephalitis and demyelination induced by Theiler's virus. J. Immunol. 1989;143:95–102
  45. Peng ZC, Kristensson K, Bentivoglio M. Distribution and temporal regulation of the immune response in the rat brain to intracerebroventricular injection of interferon-gamma. Exp. Neurol. 1998;154:403–417
  46. Pruett S. Stress and the immune system. Pathophysiology. 2003;9:133–153
  47. Ramierz F, Fowell DJ, Puklavec M, Simmonds S, Mason D. Glucocorticoids promote a TH2 cytokine response by CD4+ T cells in vitro. J. Immunol. 1996;156:2406–2412
  48. Rempel JD, Quina LA, Blakely-Gonzales PK, Buchmeier MJ, Gruol DL. Viral induction of central nervous system innate immune responses. J. Virol. 2005;79:4369–4381
  49. Rodriguez M, Leibowitz JL, Lampert PW. Persistent infection of oligodendrocytes in Theiler's virus-induced encephalomyelitis. Ann. Neurol. 1983;13:426–433
  50. Rodriguez M, Pavelko K, Coffman RL. Gamma interferon is critical for resistance to Theiler's virus-induced demyelination. J. Virol. 1995;69:7286–7290
  51. Rodriguez M, Pavelko KD, Njenga MK, Logan WC, Wettstein PJ. The balance between persistent virus infection and immune cells determines demyelination. J. Immunol. 1996;157:5699–5709
  52. Rodriguez A, Angel SO, Pinto DC, Vila I, Acosta A, Amendoeira RR, et al. Interferon-gamma independent oxidation of melatonin by macrophages. Vaccine. 2003;21:1327–1335
  53. Sato S, Reiner SL, Jensen MA, Roos RP. Central nervous system cytokine mRNA expression following Theiler's murine encephalomyelitis virus infection. J. Neuroimmunol. 1997;76:213–223
  54. Selmaj KW, Raine CS. Tumor necrosis factor mediates myelin and oligodendrocyte damage in vitro. Ann. Neurol. 1988;23:339–346
  55. Shaw-Jackson C, Michiels T. Infection of macrophages by Theiler's murine encephalomyelitis virus is highly dependent on their activation or differentiation state. J. Virol. 1997;71:8864–8867
  56. Sheridan JF, Feng NG, Bonneau RH, Allen CM, Huneycutt BS, Glaser R. Restraint stress differentially affects anti-viral cellular and humoral immune responses in mice. J. Neuroimmunol. 1991;31:245–255
  57. Sieve AN, Steelman AJ, Young CR, Storts R, Welsh TH, Welsh CJ, et al. Chronic restraint stress during early Theiler's virus infection exacerbates the subsequent demyelinating disease in SJL mice. J. Neuroimmunol. 2004;155:103–118
  58. Soderberg KA, Linehan MM, Ruddle NH, Iwasaki A. MAdCAM-1 expressing sacral lymph node in the lymphotoxin beta-deficient mouse provides a site for immune generation following vaginal herpes simplex virus-2 infection. J. Immunol. 2004;173:1908–1913
  59. Stefanski V, Peschel A, Reber S. Social stress affects migration of blood T cells into lymphoid organs. J. Neuroimmunol. 2003;138:17–24
  60. Theil DJ, Tsunoda I, Libbey JE, Derfuss TJ, Fujinami RS. Alterations in cytokine but not chemokine mRNA expression during three distinct Theiler's virus infections. J. Neuroimmunol. 2000;104:22–30
  61. Trottier M, Schlitt BP, Kung AY, Lipton HL. Transition from acute to persistent Theiler's virus infection requires active viral replication that drives proinflammatory cytokine expression and chronic demyelinating disease. J. Virol. 2004;78:12480–12488
  62. Tseng RJ, Padgett DA, Dhabhar FS, Engler H, Sheridan JF. Stress induced modulation of NK activity during influenza viral infection: role of glucocorticoids and opioids. Brain Behav. Immun. 2005;19:153–164
  63. Watford WT, Moriguchi M, Morinobu A, O'Shea JJ. The biology of IL-12: coordinating innate and adaptive immune responses. Cytokine Growth Factor Rev. 2003;14:361–368
  64. Welsh CJ, Tonks P, Nash AA, Blakemore WF. The effect of L3T4 T cell depletion on the pathogenesis of Theiler's murine encephalomyelitis virus infection in CBA mice. J. Gen. Virol. 1987;68:1659–1667
  65. Welsh CJ, Sapatino BV, Rosenbaum BA, Smith R. Characteristics of cloned cerebrovascular endothelial cells following infection with Theiler's virus: I. Acute infection. J. Neuroimmunol. 1995;62:119–125
  66. Welsh CJ, Bustamante L, Nayak M, Welsh TH, Dean DD, Meagher MW. 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. 2004;18:166–174
  67. Wong GH, Goeddel DV. Tumor necrosis factors alpha and beta inhibit virus replication and synergize with interferons. Nature. 1986;323:819–822

PII: S0165-5728(06)00196-2

doi: 10.1016/j.jneuroim.2006.05.010

Journal of Neuroimmunology
Volume 178, Issue 1 , Pages 49-61 , September 2006

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