Glucocorticoid exposure alters the pathogenesis of Theiler's murine encephalomyelitis virus during acute infection

Physiology and Behavior

Volumn 95, Issue 1-2, 2008, Pages 63-71

  Young, Erin E ^a   Prentice, Thomas W ^a   Satterlee, Danielle ^a   McCullough, Heath ^a   Sieve, Amy N ^a   Johnson, Robin R ^a   Welsh, Thomas H ^a   Welsh, C Jane R ^b   Meagher, Mary W ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

^b TEXAS A AND M UNIVERSITY   (United States)

Author keywords

Corticosterone (CORT); Inflammation; Multiple sclerosis; Restraint stress; Theiler's murine encephalomyelitis virus (TMEV)

Indexed keywords

CORTICOSTERONE; GLUCOCORTICOID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CENTRAL NERVOUS SYSTEM DISEASE; CONTROLLED STUDY; DISEASE EXACERBATION; ENCEPHALOMYELITIS; IMMOBILIZATION STRESS; INFLAMMATION; MALE; MOUSE; MULTIPLE SCLEROSIS; MURINE ENCEPHALOMYELITIS VIRUS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; VIRUS LOAD; WEIGHT REDUCTION;

EID: 49349091736     PISSN: 00319384     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.physbeh.2008.04.024     Document Type: Article

References (71)

1. Ader R., Cohen N., and Felton D. Psychoneuroimmunology. 2nd ed. (1991), Academic Press, Boston
2. Kiecolt-Glaser J.K., and Glaser R. Psychoneuroimmunology and health consequences: data and shared mechanisms. Psychosom Med 57 3 (1995) 269-274
3. Besedovsky H.O., and Del Rey A. Immune-neuro-endocrine interactions: facts and hypotheses. Endocr Rev 17 1 (1996) 64-102
4. McEwen B.S., Biron C.A., Brunson K.W., Bulloch K., chambers W.H., Dhabhar F.S., et al. The role of adrenocorticoids as modulators of immune function in health and disease: neural, endocrine, and immune interactions. Brain Res Brain Res Rev 23 1-2 (1997) 79-133
5. Rhen T., and Cidlowski J.A. Antiinflammatory action of glucocorticoids - new mechanisms for old drugs. N Engl J Med 353 16 (2005) 1711-1723
6. Parant M., Le Contel C., Parant F., and Chedid L. Influence of endogenous glucocorticoid on endotoxin-induced production of circulating TNF-a. Lymphotoxine Cytokine Res 10 4 (1991) 265-271
7. Almawi W.Y., Beyhum H.N., Rahme A.A., and Rieder M.J. Regulation of cytokine and cytokine receptor expression by glucocorticoids. J Leukoc Biol 60 5 (1996) 563-572
8. Bertini R., Bianchi M., and Ghezzi P. Adrenalectomy sensitizes mice to the lethal effects of interleukin 1 and tumor necrosis factor. J Exp Med 167 5 (1988) 1708-1712
9. Goujon E., Parnet P., Laye S., Combe C., and Dantzer R. Adrenalectomy enhances pro-inflammatory cytokines gene expression, in the spleen, pituitary and brain of mice in response to lipopolysaccharide. Brain Res Mol Brain Res 36 1 (1996) 53-62
10. Ozmen L., Pericin M., Hakimi J., Chizzonite R.A., Wysocka M., Trinchieri G., et al. Interleukin 12, interferon g and tumor necrosis factor a are the key cytokines of the generalized Schwartzman reaction. J Exp Med 180 (1994) 907-915
11. Ruzek M.C., Pearce B.D., Miller A.H., and Biron C.A. Endogenous glucocorticoids protect against cytokine-mediated lethality during viral infection. J Immunol 162 6 (1999) 3527-3533
12. Zuckerman S.H., Shellhaas J., and Butler L.D. Differential regulation of lipopolysaccharide-induced interleukin-1 and tumor necrosis factor synthesis: effects of endogenous and exogenous glucocorticoids and the role of the pituitary-adrenal axis. Eur J Immunol 19 2 (1989) 301-305
13. Golde S., Coles A., Lindquist J.A., and Compston A. Decreased iNOS synthesis mediates dexamethasone-induced protection of neurons from inflammatory injury in vitro. Eur J Neurosci 18 9 (2003) 2527-2537
14. Rivest S. Molecular insights on the cerebral innate immune system. Brain Behav Immun 17 1 (2003) 13-19
15. Nadeau S., and Rivest S. Glucocorticoids play a fundamental role in protecting the brain during innate immune response. J Neurosci 23 13 (2003) 5536-5564
16. Benveniste E.N., Sparacio S.M., Norris J.G., Grenett H.E., and Fuller G.M. Induction and regulation of interleukin-6 gene expression in rat astrocytes. J Neuroimmunol 30 2-3 (1990) 201-212
17. Colton C.A., and Chernyshev O.N. Inhibition of microglial anion production by isoproterenol and dexamethasone. Neurochem Int 29 1 (1996) 43-53
18. Drew P.D., and Chavis J.A. Inhibition of microglial cell activation by cortisol. Brain Res Bull 52 5 (2000) 77-85
19. Tanaka J., Fujita H., Matsuda S., Toku K., Sakanaka M., and Maeda N. Glucocorticoid- and mineralocorticoid receptors in microglial cells: the two receptors mediate differential effects of corticosteroids. Glia 20 1 (1997) 23-37
20. Blandino Jr. P., Barnum C.J., and Deak T. The involvement of norepinephrine and microglia in hypothalamic and splenic IL-1 beta responses to stress. J Neuroimmunol 173 1-2 (2006) 87-95
21. Deak T., Bordner K.A., McElderry N.K., Barnum C.J., Blandino Jr. P., Deak M.M., et al. Stress-induced increases in hypothalamic IL-1: a systematic analysis of multiple stressor paradigm. Brain Res Bull 64 6 (2005) 541-546
22. Nguyen K.T., Deak T., Owens S.M., Kohno T., Fleshner M., Watkins L.R., et al. Exposure to acute stress induces brain interleukin-1 beta protein in the rat. J Neurosci 18 6 (1998) 2239-2246
23. O'Connor K.A., Johnson J.D., Hansen M.K., Wieseler-Frank J.L., Maksimova E., Watkins L.R., et al. Peripheral and central proinflammatory cytokine response to a severe acute stressor. Brain Res 991 1-2 (2003) 123-132
24. Pugh C.R., Nguyen K.T., Gonyea J.L., Fleshner M., Watkins L.R., Maier S.F., et al. Role of interleukin-1 beta in impairment of contextual fear conditioning caused by social isolation. Behav Brain Res 106 1-2 (1999) 109-118
25. de Pablos R.M., Villaran R.F., Arguelles S., Herrera A.J., Venero J.L., Ayala A., et al. Stress increases vulnerability to inflammation in the rat prefrontal cortex. J Neurosci 26 21 (2006) 5709-5719
26. Simmons C.P., Thwaites G.E., Quyen N.T., Chau T.T., Mai P.P., Dung N.T., et al. The clinical benefit of adjunctive dexamethasone in tuberculosis meningitis is not associated with measurable attenuation of peripheral or local immune responses. J Immunol 175 1 (2005) 579-590
27. 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 2 (1991) 170-192
28. Bonneau R.H., Sheridan J.F., Feng N., and Glaser R. Stress-induced modulation of the primary cellular immune response to herpes simplex virus infection is mediated by both adrenal-dependent and independent mechanisms. J Neuroimmunol 42 2 (1993) 167-176
29. Dhabhar F.S., and McEwen B.S. Acute stress enhances while chronic stress suppresses cell-mediated immunity in vivo: a potential role for leukocyte trafficking. Brain Behav Immun 11 4 (1997) 286-306
30. Dobbs C.M., Vasquez M., Glaser R., and Sheridan J.F. Mechanisms of stress-induced modulation of viral pathogenesis and immunity. J Neuroimmunol 48 2 (1993) 151-160
31. Feng W.Y., Pagniano R., Tovar C.A., Bonneau R.H., Glaser R., and Sheridan J.F. The effect of restraint stress on kinetics, magnitude, and isotype of the humoral immune response to influenza virus infection. Brain Behav Immun 5 4 (1991) 370-382
32. Padgett D.A., Sheridan J.F., Dorne J., Bernston G.G., Candelora J., and Glaser R. Social stress and the reactivation of latent herpes simplex virus type 1. Proc Natl Acad Sci 95 12 (1998) 7231-7235
33. Sheridan J.F., Dobbs C., Jung J., Chu X., Konstantinos A., Padgett D., et al. Stress-induced neuroendocrine modulation of viral pathogenesis and immunity. Ann N Y Acad Sci 840 (1998) 803-808
34. A.J. Steelman, T.W. Prentice, C.R. Young, D.D. Dean, A.E. Hammons, M.W. Meagher, et al. (in preparation). The effects of restraint stress on adaptive immune responses in SJL mice infected with Theiler's virus.
35. 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
36. Mi W., Belyavskyi M., Johnson R.R., Sieve A.N., Storts R., Meagher M.W., et al. Alterations in chemokine expression following Theiler's virus infection and restraint stress. J Neuroimmunol 151 (2004) 103-115
37. Mi W., Prentice T.W., Young C.R., Johnson R.R., Sieve A.N., Meagher M.W., et al. Restraint stress decreases virus-induced pro-inflammatory cytokine mRNA expression during acute Theiler's virus infection. J Neuroimmunol 178 (2006) 49-61
38. 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
39. Munhoz C.D., Lepsch L.B., Kawamoto E.M., Malta M.B., Lima Lde S., Avellar M.C., et al. Chronic unpredictable stress exacerbates lipopolysaccharide-induced activation of nuclear factor-kappaB in the frontal cortex and hippocampus via glucocorticoid secretion. J Neurosci 26 14 (2006) 3813-3820
40. Nair A., and Bonneau R.H. Stress-induced elevation of glucocorticoids increases microglia proliferation through NMDA receptor activation. J Neuroimmunol 171 1-2 (2006) 72-85
41. Sorrells S.F., and Sapolsky R.M. An inflammatory review of glucocorticoid actions in the CNS. Brain Behav Immun 21 3 (2007) 259-272
42. Dinkel K., MacPherson A., and Sapolsky R.M. Novel glucocorticoid effects on acute inflammation in the CNS. J Neurochem 84 4 (2003) 705-716
43. Quan N., Avitsur R., Stark J.L., He L., Shah M., Caligiuri M., et al. Social stress increases the susceptibility to endotoxic shock. J Neuroimmunol 115 1-2 (2001) 36-45
44. Meagher M.W., Johnson R.R., Young E.E., Vichaya E.G., Lunt S., Harden E., et al. IL-6 as a mechanism for the adverse effects of social stress on acute Theiler's virus infection. Brain Behav Immun 21 8 (2007) 1083-1095
45. Sapolsky R.M., and Pulsinelli W.A. Glucocorticoids potentiate ischemic injury to neurons: therapeutic implications. Science 229 4720 (1985) 1397-1400
46. Campbell T., Meagher M.W., Sieve A., Scott B., Storts R., Welsh T.H., et al. The effects of restraint on the neuropathogenesis of Theiler's virus infection: I. Acute disease. Brain Behav Immun 15 (2001) 235-254
47. Sieve A.N., Steelman A.J., Young C.R., Storts R., Welsh T.H., Welsh C.J.R., et al. Chronic restraint stress during early Theiler's virus infection exacerbates the subsequent demyelinating disease in SJL mice. J Neuroimmunol 155 (2004) 103-118
48. Johnson R.R., Storts R., Welsh T.H., Welsh C.J.R., and Meagher M.W. Social stress alters the severity of acute Theiler's virus infection. J Neuroimmunol 148 (2004) 74-85
49. Johnson R.R., Prentice T., Bridegam P., Young C.R., Steelman A.J., Welsh T.H., et al. Social stress alters the severity and onset of the chronic phase of Theiler's virus infection. J Neuroimmunol 175 (2006) 39-51
50. Njenga M.K., Asakura K., Hunter S.F., Wettstein P., Pease L.R., and Rodriguez M. The immune system preferentially clears Theiler's virus from the gray matter of the central nervous system. J Virol 71 (1997) 8592-8601
51. Theiler M. Spontaneous encephalomyelitis of mice: a new viral disease. J Exp Med 65 (1934) 705-719
52. Welsh C.J.R., Tonks P., Borrow P., and Nash A.A. Theiler's virus: an experimental model of virus-induced demyelination. Autoimmunity 6 (1990) 105-112
53. Sieve A.N., Steelman A.J., Young C.R., Storts R., Welsh T.H., Welsh C.J.R., et al. Sex dependent effects of chronic restraint stress during early Theiler's virus infection on the subsequent demyelinating disease in CBA mice. J Neuroimmunol 177 (2006) 46-62
54. Jellinck P.H., Dhabhar F.S., Sakai R.R., and McEwen B.S. Long term corticosteroid treatment but not chronic stress affect 11beta-hydroxysteroid dehydrogenase type I activity in rat brain and peripheral tissues. J Steroid Biochem Mol Biol 60 5-6 (1997) 319-323
55. Welsh C.J.R., Tonks P., Nash A.A., and Blakemore W.F. The effect of L3T4 cell depletion on the pathogenesis of Theiler's murine encephalomyelitis virus infection in CBA mice. J Gen Virol 68 6 (1987) 1659-1667
56. Keith L.D., Winslow J.R., and Reynolds R.W. A general procedure for estimation of corticosteroid response in individual rats. Steroids 31 (1978) 523-531
57. Satterlee D.M., Sieve A.N., Welsh T.H., Welsh C.J.R., and Meagher M.W. Corticosterone mediates the effects of chronic restraint stress on Theiler's virus infection in mice. Soc Neurosci Abstr 27 (2001) 2238
58. Bowman R.E., Zrull M.C., and Luine V.N. Chronic restraint stress enhances radial arm maze performance in female rats. Brain Res 904 2 (2001) 279-289
59. Clatch R.J., Lipton H.L., and Miller S.D. Class II-restricted T cell responses in Theiler's murine encephalomyelitis virus (TMEV)-induced demyelinating disease. II. Survey of host immune responses and central nervous system virus titers in inbred mouse strains. Microb Pathog 3 5 (1987) 327-337
60. Miller S.D., Vanderlugt C.L., Begolka W.S., Pao W., Neville K.L., Yauch R.L., et al. Epitope spreading leads to myelin-specific autoimmune responses in SJL mice chronically infected with Theiler's virus. J. Neurovirology Suppl 1 S62-S5 (1997)
61. Rodriguez M., and Sriram S. Successful therapy of Theiler's virus-induced demyelination (DA strain) with monoclonal anti-Lyt-2 antibody. J Immunol 140 9 (1988) 2950-2955
62. Roos R.P., and Woolmann R. DA strain of Theiler's murine encephalomyelitis virus induces demyelination in nude mice. Ann Neurol 15 5 (1984) 494-499
63. Lipton H.L., and Dal Canto M.C. Contrasting effects of immunosuppression on Theiler's virus infection in mice. Infect Immun 15 (1977) 903-909
64. Faulkner R.H., Prentice T.W., Johnson R.R., McCullough H.K., Welsh T.H., Storts R., et al. Corticosterone is both necessary and sufficient to observe the adverse effects of restraint stress on acute Theiler's virus infection. Soc for Neurosci Abstracts, New Orleans, LA (2003)
65. Acheson E.D. Epidemiology of multiple sclerosis. Br Med Bull 33 (1977) 9-14
66. Gilden D.H. Infectious causes of multiple sclerosis. Lancet Neurol 4 (2005) 195-202
67. Gottlieb S. Epstein-Barr virus may increase risk of multiple sclerosis. BMJ 326 7392 (2003) 731
68. Kurtzke J.F., and Hyllested K. MS epidemiology in the Faroe Islands. Rev Neurol 57 (1987) 77-87
69. Sospedra M., and Martin R. Immunology of multiple sclerosis. Annu Rev Immunol 23 (2005) 683-747
70. Grant D.H., Brown G.W., Harris T., McDonald W.I., Patteron T., and Trimble M.R. Severely threatening events and marked life difficulties preceding onset or exacerbation of multiple sclerosis. J Neurol Neurosurg Psychiatry 52 (1989) 8-13
71. Warren S., Greehhill S., and Warren K.G. Emotional stress and the development of multiple sclerosis: case-control evidence of a relationship. J Chronic Dis 35 (1982) 821-831