Stress-induced glucocorticoids at the earliest stages of herpes simplex virus-1 infection suppress subsequent antiviral immunity, implicating impaired dendritic cell function

Journal of Immunology

Volumn 184, Issue 4, 2010, Pages 1867-1875

  Elftman, Michael D ^a   Hunzeker, John T ^a   Mellinger, Jennifer C ^a   Bonneau, Robert H ^a   Norbury, Christopher C ^a   Truckenmiller, Mary E ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD8 ANTIGEN; CORTICOSTERONE; GAMMA INTERFERON; GLUCOCORTICOID; GLUCOCORTICOID RECEPTOR; GRANZYME B; MIFEPRISTONE; GLYCOPROTEIN B, SIMPLEXVIRUS; IMMUNOSUPPRESSIVE AGENT; VIRUS ENVELOPE PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD8+ T LYMPHOCYTE; CELL STRESS; CONTROLLED STUDY; CYTOKINE PRODUCTION; DEGRANULATION; DENDRITIC CELL; HERPES SIMPLEX; HERPES SIMPLEX VIRUS 1; HERPES SIMPLEX VIRUS 1 INFECTION; IMMUNE RESPONSE; IMMUNOMODULATION; IN VIVO STUDY; KNOCKOUT MOUSE; LYMPH NODE; LYMPHOCYTE FUNCTION; MALE; MOUSE; NEUROENDOCRINE SYSTEM; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE; VIRUS IMMUNITY; ANIMAL; C57BL MOUSE; IMMOBILIZATION; IMMUNOLOGY; MENTAL STRESS; METABOLISM; PATHOLOGY; TRANSGENIC MOUSE; VIROLOGY;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CORTICOSTERONE; DENDRITIC CELLS; HERPES SIMPLEX; HERPESVIRUS 1, HUMAN; IMMOBILIZATION; IMMUNOSUPPRESSIVE AGENTS; LYMPH NODES; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; STRESS, PSYCHOLOGICAL; VIRAL ENVELOPE PROTEINS;

EID: 77949881218     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0902469     Document Type: Article

References (63)

1. McEwen, B. S., C. A. Biron, K. W. Brunson, K. Bulloch, W. H. Chambers, F. S. Dhabhar, R. H. Goldfarb, R. P. Kitson, A. H. Miller, R. L. Spencer, and J. M. Weiss. 1997. The role of adrenocorticoids as modulators of immune function in health and disease: neural, endocrine and immune interactions. Brain Res. Brain Res. Rev. 23: 79-133.
2. Webster, J. I., L. Tonelli, and E. M. Sternberg. 2002. Neuroendocrine regulation of immunity. Annu. Rev. Immunol. 20: 125-163.
3. Bailey, M., H. Engler, J. Hunzeker, and J. F. Sheridan. 2003. The hypothalamic-pituitary-adrenal axis and viral infection. Viral Immunol. 16: 141-157.
4. Segerstrom, S. C., and G. E. Miller. 2004. Psychological stress and the human immune system: a meta-analytic study of 30 years of inquiry. Psychol. Bull. 130: 601-630.
5. Dhabhar, F. S. 2003. Stress, leukocyte trafficking, and the augmentation of skin immune function. Ann. N. Y. Acad. Sci. 992: 205-217.
6. Dhabhar, F. S., and B. S. McEwen. 1996. Stress-induced enhancement of antigen-specific cell-mediated immunity. J. Immunol. 156: 2608-2615.
7. Dopp, J. M., G. E. Miller, H. F. Myers, and J. L. Fahey. 2000. Increased natural killer-cell mobilization and cytotoxicity during marital conflict. Brain Behav. Immun. 14: 10-26.
8. Glaser, R., and J. K. Kiecolt-Glaser. 2005. Stress-induced immune dysfunction: implications for health. Nat. Rev. Immunol. 5: 243-251.
9. Ader, R. 2007. Psychoneuroimmunology, 4th Ed.. Academic Press, San Diego.
10. Kelso, A., and A. Munck. 1984. Glucocorticoid inhibition of lymphokine secretion by alloreactive T lymphocyte clones. J. Immunol. 133: 784-791. (Pubitemid 14093469)
11. Braun, C.M., S. K. Huang, G. G. Bashian, A. Kagey-Sobotka, L. M. Lichtenstein, and D. M. Essayan. 1997. Corticosteroid modulation of human, antigen-specific Th1 and Th2 responses. J. Allergy Clin. Immunol. 100: 400-407.
12. Padgett, D. A., R. C. MacCallum, and J. F. Sheridan. 1998. Stress exacerbates age-related decrements in the immune response to an experimental influenza viral infection. J. Gerontol. A Biol. Sci. Med. Sci. 53: B347-B353.
13. Ashcraft, K. A., J. Hunzeker, and R. H. Bonneau. 2008. Psychological stress impairs the local CD8+ T cell response to mucosal HSV-1 infection and allows for increased pathogenicity via a glucocorticoid receptor-mediated mechanism. Psychoneuroendocrinology 33: 951-963.
14. Steelman,A. J.,D.D.Dean,C.R.Young,R.Smith, 3rd,T.W.Prentice,M.W.Meagher, and C. J. Welsh. 2009. Restraint stress modulates virus specific adaptive immunity during acute Theiler's virus infection. Brain Behav. Immun. 23: 830-843.
15. Bonneau, R. H., J. F. Sheridan, N. G. Feng, and R. Glaser. 1991. 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: 170-192.
16. Dobbs, C. M., M. Vasquez, R. Glaser, and J. F. Sheridan. 1993. Mechanisms of stress-induced modulation of viral pathogenesis and immunity. J. Neuroimmunol. 48: 151-160.
17. Anglen, C. S., M. E. Truckenmiller, T. D. Schell, and R. H. Bonneau. 2003. The dual role of CD8+ T lymphocytes in the development of stress-induced herpes simplex encephalitis. J. Neuroimmunol. 140: 13-27.
18. Young, E. E., T. W. Prentice, D. Satterlee, H. McCullough, A. N. Sieve, R. R. Johnson, T. H. Welsh, C. J. Welsh, and M. W. Meagher. 2008. Glucocorticoid exposure alters the pathogenesis of Theiler's murine encephalomyelitis virus during acute infection. Physiol. Behav. 95: 63-71.
19. Banchereau, J., F. Briere, C. Caux, J. Davoust, S. Lebecque, Y. J. Liu, B. Pulendran, and K. Palucka. 2000. Immunobiology of dendritic cells. Annu. Rev. Immunol. 18: 767-811.
20. Mellman, I., and R. M. Steinman. 2001. Dendritic cells: specialized and regulated antigen processing machines. Cell 106: 255-258.
21. Jung, S., D. Unutmaz, P. Wong, G. Sano, K. De los Santos, T. Sparwasser, S. Wu, S. Vuthoori, K. Ko, F. Zavala, et al. 2002. In vivo depletion of CD11c(+) dendritic cells abrogates priming of CD8(+) T cells by exogenous cell-associated antigens. Immunity 17: 211-220.
22. Kassim, S. H., N. K. Rajasagi, X. Zhao, R. Chervenak, and S. R. Jennings. 2006. In vivo ablation of CD11c-positive dendritic cells increases susceptibility to herpes simplex virus type 1 infection and diminishes NK and T-cell responses. J. Virol. 80: 3985-3993.
23. Moser, M., T. De Smedt, T. Sornasse, F. Tielemans, A. A. Chentoufi, E. Muraille, M. Van Mechelen, J. Urbain, and O. Leo. 1995. Glucocorticoids down-regulate dendritic cell function in vitro and in vivo. Eur. J. Immunol. 25: 2818-2824.
24. Piemonti, L., P. Monti, P. Allavena, M. Sironi, L. Soldini, B. E. Leone, C. Socci, and V. Di Carlo. 1999. Glucocorticoids affect human dendritic cell differentiation and maturation. J. Immunol. 162: 6473-6481.
25. Woltman, A. M., J. W. de Fijter, S. W. Kamerling, L. C. Paul, M. R. Daha, and C. van Kooten. 2000. The effect of calcineurin inhibitors and corticosteroids on the differentiation of human dendritic cells. Eur. J. Immunol. 30: 1807-1812.
26. Matyszak, M. K., S. Citterio, M. Rescigno, and P. Ricciardi-Castagnoli. 2000. Differential effects of corticosteroids during different stages of dendritic cell maturation. Eur. J. Immunol. 30: 1233-1242.
27. Elftman, M. D., C. C. Norbury, R. H. Bonneau, and M. E. Truckenmiller. 2007. Corticosterone impairs dendritic cell maturation and function. Immunology 122: 279-290.
28. Truckenmiller, M. E., M. F. Princiotta, C. C. Norbury, and R. H. Bonneau. 2005. Corticosterone impairs MHC class I antigen presentation by dendritic cells via reduction of peptide generation. J. Neuroimmunol. 160: 48-60.
29. Truckenmiller, M. E., R. H. Bonneau, and C. C. Norbury. 2006. Stress presents a problem for dendritic cells: corticosterone and the fate of MHC class I antigen processing and presentation. Brain Behav. Immun. 20: 210-218.
30. Brewer, J. A., B. Khor, S. K. Vogt, L. M. Muglia, H. Fujiwara, K. E. Haegele, B. P. Sleckman, and L. J. Muglia. 2003. T-cell glucocorticoid receptor is required to suppress COX-2-mediated lethal immune activation. Nat. Med. 9: 1318-1322.
31. Mueller, S. N., W. Heath, J. D. McLain, F. R. Carbone, and C. M. Jones. 2002. Characterization of two TCR transgenic mouse lines specific for herpes simplex virus. Immunol. Cell Biol. 80: 156-163.
32. Paré, W. P., and G. B. Glavin. 1986. Restraint stress in biomedical research: a review. Neurosci. Biobehav. Rev. 10: 339-370.
33. Hermann, G., C. A. Tovar, F. M. Beck, and J. F. Sheridan. 1994. Kinetics of glucocorticoid response to restraint stress and/or experimental influenza viral infection in two inbred strains of mice. J. Neuroimmunol. 49: 25-33.
34. Nair, A., and R. H. Bonneau. 2006. Stress-induced elevation of glucocorticoids increases microglia proliferation through NMDA receptor activation. J. Neuroimmunol. 171: 72-85.
35. Bonneau, R. H., and S. R. Jennings. 1989. Modulation of acute and latent herpes simplex virus infection in C57BL/6 mice by adoptive transfer of immune lymphocytes with cytolytic activity. J. Virol. 63: 1480-1484.
36. Leo, N. A., and R. H. Bonneau. 2000. Mechanisms underlying chemical sympathectomy-induced suppression of herpes simplex virus-specific cytotoxic T lymphocyte activation and function. J. Neuroimmunol. 110: 45-56.
37. Nyström, K., M. Biller, A. Grahn, M. Lindh, G. Larson, and S. Olofsson. 2004. Real time PCR for monitoring regulation of host gene expression in herpes simplex virus type 1-infected human diploid cells. J. Virol. Methods 118: 83-94.
38. Kastrukoff, L. F., A. S. Lau, and M. L. Puterman. 1986. Genetics of natural resistance to herpes simplex virus type 1 latent infection of the peripheral nervous system in mice. J. Gen. Virol. 67: 613-621.
39. Jones, C. M., S. C. Cose, R. M. Coles, A. C. Winterhalter, A. G. Brooks, W. R. Heath, and F. R. Carbone. 2000. Herpes simplex virus type 1-specific cytotoxic T-lymphocyte arming occurs within lymph nodes draining the site of cutaneous infection. J. Virol. 74: 2414-2419.
40. Smith, P. M., R. M. Wolcott, R. Chervenak, and S. R. Jennings. 1994. Control of acute cutaneous herpes simplex virus infection: T cell-mediated viral clearance is dependent upon interferon-γ (IFN-γ). Virology 202: 76-88.
41. Nair, A., J. Hunzeker, and R. H. Bonneau. 2007. Modulation of microglia and CD8(+) T cell activation during the development of stress-induced herpes simplex virus type-1 encephalitis. Brain Behav. Immun. 21: 791-806.
42. McNally, J. M., D. Dempsey, R. M. Wolcott, R. Chervenak, and S. R. Jennings. 1999. Phenotypic identification of antigen-dependent and antigen-independent CD8 CTL precursors in the draining lymph node during acute cutaneous herpes simplex virus type 1 infection. J. Immunol. 163: 675-681.
43. Yorty, J. L., S. A. Schultz, and R. H. Bonneau. 2004. Postpartum maternal corticosterone decreases maternal and neonatal antibody levels and increases the susceptibility of newborn mice to herpes simplex virus-associated mortality. J. Neuroimmunol. 150: 48-58.
44. Norbury, C. C., D. Malide, J. S. Gibbs, J. R. Bennink, and J. W. Yewdell. 2002. Visualizing priming of virus-specific CD8+ T cells by infected dendritic cells in vivo. Nat. Immunol. 3: 265-271.
45. Allan, R. S., C. M. Smith, G. T. Belz, A. L. van Lint, L. M. Wakim, W. R. Heath, and F. R. Carbone. 2003. Epidermal viral immunity induced by CD8alpha+ dendritic cells but not by Langerhans cells. Science 301: 1925-1928.
46. Smith, C. M., G. T. Belz, N. S. Wilson, J. A. Villadangos, K. Shortman, F. R. Carbone, and W. R. Heath. 2003. Cutting edge: conventional CD8 alpha+ dendritic cells are preferentially involved in CTL priming after footpad infection with herpes simplex virus-1. J. Immunol. 170: 4437-4440.
47. Montano, M. M., M. H. Wang, M. D. Even, and F. S. vom Saal. 1991. Serum corticosterone in fetal mice: sex differences, circadian changes, and effect of maternal stress. Physiol. Behav. 50: 323-329.
48. Vizzardelli, C., N. Pavelka, A. Luchini, I. Zanoni, L. Bendickson, M. Pelizzola, O. Beretta, M. Foti, F. Granucci, M. Nilsen-Hamilton, and P. Ricciardi-Castagnoli. 2006. Effects of dexamethazone on LPS-induced activationand migration of mouse dendritic cells revealed by a genome-wide transcriptional analysis. Eur. J. Immunol. 36: 1504-1515.
49. Reis e Sousa, C., S. Hieny, T. Scharton-Kersten, D. Jankovic, H. Charest, R. N. Germain, and A. Sher. 1997. In vivo microbial stimulation induces rapid CD40 ligand-independent production of interleukin 12 by dendritic cells and their redistribution to T cell areas. J. Exp. Med. 186: 1819-1829.
50. Mueller, S. N., C. M. Jones, C. M. Smith, W. R. Heath, and F. R. Carbone. 2002. Rapid cytotoxic T lymphocyte activation occurs in the draining lymph nodes after cutaneous herpes simplex virus infection as a result of early antigen presentation and not the presence of virus. J. Exp. Med. 195: 651-656.
51. Shortman, K., and Y. J. Liu. 2002. Mouse and human dendritic cell subtypes. Nat. Rev. Immunol. 2: 151-161.
52. Shortman, K., and S. H. Naik. 2007. Steady-state and inflammatory dendritic-cell development. Nat. Rev. Immunol. 7: 19-30.
53. den Haan, J. M., S. M. Lehar, and M. J. Bevan. 2000. CD8(+) but not CD8(-) dendritic cells cross-prime cytotoxic T cells in vivo. J. Exp. Med. 192: 1685-1696.
54. Pooley, J. L., W. R. Heath, and K. Shortman. 2001. Cutting edge: intravenous soluble antigen is presented to CD4 T cells by CD8- dendritic cells, but cross-presented to CD8 T cells by CD8+ dendritic cells. J. Immunol. 166: 5327-5330.
55. Lee, H. K., M. Zamora, M. M. Linehan, N. Iijima, D. Gonzalez, A. Haberman, and A. Iwasaki. 2009. Differential roles of migratory and resident DCs in T cell priming after mucosal or skin HSV-1 infection. J. Exp. Med. 206: 359-370.
56. Lund, J. M., M. M. Linehan, N. Iijima, and A. Iwasaki. 2006. Cutting Edge: Plasmacytoid dendritic cells provide innate immune protection against mucosal viral infection in situ. J. Immunol. 177: 7510-7514.
57. Yoneyama, H., K. Matsuno, E. Toda, T. Nishiwaki, N. Matsuo, A. Nakano, S. Narumi, B. Lu, C. Gerard, S. Ishikawa, and K. Matsushima. 2005. Plasmacytoid DCs help lymph node DCs to induce anti-HSV CTLs. J. Exp. Med. 202: 425-435.
58. Steinman, L. 2004. Elaborate interactions between the immune and nervous systems. Nat. Immunol. 5: 575-581.
59. Sanders, V. M., and R. H. Straub. 2002. Norepinephrine, the β-adrenergic receptor, and immunity. Brain Behav. Immun. 16: 290-332.
60. Yin, D., D. Tuthill, R. A. Mufson, and Y. Shi. 2000. Chronic restraint stress promotes lymphocyte apoptosis by modulating CD95 expression. J. Exp. Med. 191: 1423-1428.
61. Sternberg, E. M. 2006. Neural regulation of innate immunity: a coordinated nonspecific host response to pathogens. Nat. Rev. Immunol. 6: 318-328.
62. Grebe, K. M., H. D. Hickman, K. R. Irvine, K. Takeda, J. R. Bennink, and J.W.Yewdell. 2009. Sympathetic nervous system control of anti-influenza CD8+ T cell responses. Proc. Natl. Acad. Sci. USA 106: 5300-5305.
63. Schwartzman, R. A., and J. A. Cidlowski. 1994. Glucocorticoid-induced apoptosis of lymphoid cells. Int. Arch. Allergy Immunol. 105: 347-354.