A marked reduction in priming of cytotoxic CD8+ T cells mediated by stress-induced glucocorticoids involves multiple deficiencies in cross-presentation by dendritic cells

Journal of Immunology

Volumn 186, Issue 1, 2011, Pages 183-194

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

^a PENN STATE COLLEGE OF MEDICINE   (United States)

^b SUNY UPSTATE MEDICAL UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; BETA 2 MICROGLOBULIN; CORTICOSTERONE; GLUCOCORTICOID; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MIFEPRISTONE; OVALBUMIN; PROTEASOME;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN EXPRESSION; ARTICLE; CD8+ T LYMPHOCYTE; CELL PROLIFERATION; CELLULAR IMMUNITY; CONTROLLED STUDY; CROSS PRESENTATION; CYTOTOXIC T LYMPHOCYTE; DENDRITIC CELL; ENDOCYTOSIS; IN VIVO STUDY; MALE; MENTAL STRESS; MOUSE; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL;

ANIMALS; CELLS, CULTURED; COCULTURE TECHNIQUES; CORTICOSTERONE; CROSS-PRIMING; CYTOTOXICITY, IMMUNOLOGIC; DENDRITIC CELLS; IMMOBILIZATION; IMMUNOSUPPRESSION; LYMPHOCYTE ACTIVATION; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; OVALBUMIN; STRESS, PSYCHOLOGICAL; T-LYMPHOCYTES, CYTOTOXIC;

EID: 79251549773     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1001737     Document Type: Article

References (88)

1. Bevan, M. J. 1977. Priming for a cytotoxic response to minor histocompatibility antigens: antigen specificity and failure to demonstrate a carrier effect. J. Immunol. 118: 1370-1374.
2. Bevan, M. J. 1976. Minor H antigens introduced on H-2 different stimulating cells cross-react at the cytotoxic T cell level during in vivo priming. J. Immunol. 117: 2233-2238.
3. Melief, C. J. 2008. Cancer immunotherapy by dendritic cells. Immunity 29: 372-383.
4. Vyas, J. M., A. G. Van der Veen, and H. L. Ploegh. 2008. The known unknowns of antigen processing and presentation. Nat. Rev. Immunol. 8: 607-618.
5. Lin, M. L., Y. Zhan, J. A. Villadangos, and A. M. Lew. 2008. The cell biology of cross-presentation and the role of dendritic cell subsets. Immunol. Cell Biol. 86: 353-362.
6. Villadangos, J. A., W. R. Heath, and F. R. Carbone. 2007. Outside looking in: the inner workings of the cross-presentation pathway within dendritic cells. Trends Immunol. 28: 45-47.
7. + dendritic cells is attributable to their ability to internalize dead cells. Immunology 107: 183-189.
8. Dudziak, D., A. O. Kamphorst, G. F. Heidkamp, V. R. Buchholz, C. Trumpfheller, S. Yamazaki, C. Cheong, K. Liu, H. W. Lee, C. G. Park, et al. 2007. Differential antigen processing by dendritic cell subsets in vivo. Science 315: 107-111.
9. + dendritic cells. J. Immunol. 166: 5327-5330.
10. - dendritic cells cross-prime cytotoxic T cells in vivo. J. Exp. Med. 192: 1685-1696.
11. + dendritic cells in cross-presentation is not dictated by antigen capture. Proc. Natl. Acad. Sci. USA 103: 10729-10734.
12. + dendritic cells selectively present MHC class I-restricted noncytolytic viral and intracellular bacterial antigens in vivo. J. Immunol. 175: 196-200.
13. Heath, W. R., G. T. Belz, G. M. Behrens, C. M. Smith, S. P. Forehan, I. A. Parish, G. M. Davey, N. S. Wilson, F. R. Carbone, and J. A. Villadangos. 2004. Crosspresentation, dendritic cell subsets, and the generation of immunity to cellular antigens. Immunol. Rev. 199: 9-26.
14. 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.
15. Webster, J. I., L. Tonelli, and E. M. Sternberg. 2002. Neuroendocrine regulation of immunity. Annu. Rev. Immunol. 20: 125-163.
16. Bailey, M., H. Engler, J. Hunzeker, and J. F. Sheridan. 2003. The hypothalamic-pituitary-adrenal axis and viral infection. Viral Immunol. 16: 141-157.
17. Steinman, L. 2004. Elaborate interactions between the immune and nervous systems. Nat. Immunol. 5: 575-581.
18. 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.
19. Dhabhar, F. S. 2003. Stress, leukocyte trafficking, and the augmentation of skin immune function. Ann. N. Y. Acad. Sci. 992: 205-217.
20. 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.
21. Ader, R. 2007. Psychoneuroimmunology, 4th Ed. Academic Press, San Diego.
22. Glaser, R., and J. K. Kiecolt-Glaser. 2005. Stress-induced immune dysfunction: implications for health. Nat. Rev. Immunol. 5: 243-251.
23. 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.
24. 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.
25. Steelman, A. J., D. D. Dean, C. R. Young, R. Smith, III, 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.
26. + T cell response to mucosal HSV-1 infection and allows for increased pathogenicity via a glucocorticoid receptor-mediated mechanism. Psychoneuroendocrinology 33: 951-963.
27. + T cell activation during the development of stress-induced herpes simplex virus type-1 encephalitis. Brain Behav. Immun. 21: 791-806.
28. Hermann, G., F. M. Beck, and J. F. Sheridan. 1995. Stress-induced glucocorticoid response modulates mononuclear cell trafficking during an experimental influenza viral infection. J. Neuroimmunol. 56: 179-186.
29. Cohen, S., W. J. Doyle, and D. P. Skoner. 1999. Psychological stress, cytokine production, and severity of upper respiratory illness. Psychosom. Med. 61: 175-180.
30. Elftman, M. D., J. T. Hunzeker, J. C. Mellinger, R. H. Bonneau, C. C. Norbury, and M. E. Truckenmiller. 2010. Stress-induced glucocorticoids at the earliest stages of herpes simplex virus-1 infection suppress subsequent antiviral immunity, implicating impaired dendritic cell function. J. Immunol. 184: 1867-1875.
31. + T lymphocytes in the development of stress-induced herpes simplex encephalitis. J. Neuroimmunol. 140: 13-27.
32. 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.
33. Capitanio, J. P., S. P. Mendoza, N. W. Lerche, and W. A. Mason. 1998. Social stress results in altered glucocorticoid regulation and shorter survival in simian acquired immune deficiency syndrome. Proc. Natl. Acad. Sci. USA 95: 4714-4719.
34. Banchereau, J., and R. M. Steinman. 1998. Dendritic cells and the control of immunity. Nature 392: 245-252.
35. Heath, W. R., and F. R. Carbone. 2009. Dendritic cell subsets in primary and secondary T cell responses at body surfaces. Nat. Immunol. 10: 1237-1244.
36. 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.
37. 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.
38. 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.
39. 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.
40. 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.
41. 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.
42. 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.
43. + dendritic cells are preferentially involved in CTL priming after footpad infection with herpes simplex virus-1. J. Immunol. 170: 4437-4440.
44. Allan, R. S., J. Waithman, S. Bedoui, C. M. Jones, J. A. Villadangos, Y. Zhan, A. M. Lew, K. Shortman, W. R. Heath, and F. R. Carbone. 2006. Migratory dendritic cells transfer antigen to a lymph node-resident dendritic cell population for efficient CTL priming. Immunity 25: 153-162.
45. + dendritic cells but not by Langerhans cells. Science 301: 1925-1928.
46. + dendritic cells. Nat. Immunol. 10: 488-495.
47. Belz, G. T., C. M. Smith, L. Kleinert, P. Reading, A. Brooks, K. Shortman, F. R. Carbone, and W. R. Heath. 2004. Distinct migrating and nonmigrating dendritic cell populations are involved in MHC class I-restricted antigen presentation after lung infection with virus. Proc. Natl. Acad. Sci. USA 101: 8670-8675.
48. + dendritic cells are generally involved in priming CTL immunity to viruses. J. Immunol. 172: 1996-2000.
49. Mombaerts, P., A. R. Clarke, M. A. Rudnicki, J. Iacomini, S. Itohara, J. J. Lafaille, L. Wang, Y. Ichikawa, R. Jaenisch, M. L. Hooper, et al. 1992. Mutations in T-cell antigen receptor genes α and β block thymocyte development at different stages. Nature 360: 225-231.
50. Hogquist, K. A., S. C. Jameson, W. R. Heath, J. L. Howard, M. J. Bevan, and F. R. Carbone. 1994. T cell receptor antagonist peptides induce positive selection. Cell 76: 17-27.
51. Sheridan, J. F., N. G. Feng, R. H. Bonneau, C. M. Allen, B. S. Huneycutt, and R. Glaser. 1991. Restraint stress differentially affects anti-viral cellular and humoral immune responses in mice. J. Neuroimmunol. 31: 245-255.
52. 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.
53. + T cell cross-priming via transfer of proteasome substrates. Science 304: 1318-1321.
54. Shen, Z., G. Reznikoff, G. Dranoff, and K. L. Rock. 1997. Cloned dendritic cells can present exogenous antigens on both MHC class I and class II molecules. J. Immunol. 158: 2723-2730.
55. Sanderson, S., and N. Shastri. 1994. LacZ inducible, antigen/MHC-specific T cell hybrids. Int. Immunol. 6: 369-376.
56. Restifo, N. P., I. Bacík, K. R. Irvine, J. W. Yewdell, B. J. McCabe, R. W. Anderson, L. C. Eisenlohr, S. A. Rosenberg, and J. R. Bennink. 1995. Antigen processing in vivo and the elicitation of primary CTL responses. J. Immunol. 154: 4414-4422.
57. Donohue, K. B., J. M. Grant, E. F. Tewalt, D. C. Palmer, M. R. Theoret, N. P. Restifo, and C. C. Norbury. 2006. Cross-priming utilizes antigen not available to the direct presentation pathway. Immunology 119: 63-73.
58. + T-cell priming. J. Gen. Virol. 88: 2378-2386.
59. Coles, R. M., S. N. Mueller, W. R. Heath, F. R. Carbone, and A. G. Brooks. 2002. Progression of armed CTL from draining lymph node to spleen shortly after localized infection with herpes simplex virus 1. J. Immunol. 168: 834-838.
60. Tewalt, E. F., J. C. Maynard, J. J. Walters, A. M. Schell, B. L. Berwin, C. V. Nicchitta, and C. C. Norbury. 2008. Redundancy renders the glycoprotein 96 receptor scavenger receptor A dispensable for cross priming in vivo. Immunology 125: 480-491.
61. Princiotta, M. F., U. Schubert, W. Chen, J. R. Bennink, J. Myung, C. M. Crews, and J. W. Yewdell. 2001. Cells adapted to the proteasome inhibitor 4-hydroxy-5-iodo-3-nitrophenylacetyl-Leu-Leu-leucinal-vinyl sulfone require enzymatically active proteasomes for continued survival. Proc. Natl. Acad. Sci. USA 98: 513-518.
62. Burgdorf, S., V. Lukacs-Kornek, and C. Kurts. 2006. The mannose receptor mediates uptake of soluble but not of cell-associated antigen for cross-presentation. J. Immunol. 176: 6770-6776.
63. Racoosin, E. L., and J. A. Swanson. 1989. Macrophage colony-stimulating factor (rM-CSF) stimulates pinocytosis in bone marrow-derived macrophages. J. Exp. Med. 170: 1635-1648.
64. + cytolytic T cells. Nature 344: 742-746.
65. Melief, C. J. 2003. Mini-review: Regulation of cytotoxic T lymphocyte responses by dendritic cells: peaceful coexistence of cross-priming and direct priming? Eur. J. Immunol. 33: 2645-2654.
66. Kovacsovics-Bankowski, M., and K. L. Rock. 1995. A phagosome-to-cytosol pathway for exogenous antigens presented on MHC class I molecules. Science 267: 243-246.
67. Norbury, C. C., B. J. Chambers, A. R. Prescott, H. G. Ljunggren, and C. Watts. 1997. Constitutive macropinocytosis allows TAP-dependent major histocompatibility complex class I presentation of exogenous soluble antigen by bone marrow-derived dendritic cells. Eur. J. Immunol. 27: 280-288.
68. Reits, E. A., J. C. Vos, M. Grommé, and J. Neefjes. 2000. The major substrates for TAP in vivo are derived from newly synthesized proteins. Nature 404: 774-778.
69. + dendritic cells capable of inducing antiviral T cell responses. J. Immunol. 182: 4200-4207.
70. Norbury, C. C., L. J. Hewlett, A. R. Prescott, N. Shastri, and C. Watts. 1995. Class I MHC presentation of exogenous soluble antigen via macropinocytosis in bone marrow macrophages. Immunity 3: 783-791.
71. Burgdorf, S., A. Kautz, V. Böhnert, P. A. Knolle, and C. Kurts. 2007. Distinct pathways of antigen uptake and intracellular routing in CD4 and CD8 T cell activation. Science 316: 612-616. (Pubitemid 46683149)
72. Giodini, A., C. Rahner, and P. Cresswell. 2009. Receptor-mediated phagocytosis elicits cross-presentation in nonprofessional antigen-presenting cells. Proc. Natl. Acad. Sci. USA 106: 3324-3329.
73. Reits, E. A., J. C. Vos, M. Gromme, and J. Neefjes. 2000. The major substrates for TAP in vivo are derived from newly synthesized proteins. Nature 404: 774-778.
74. Princiotta, M. F., D. Finzi, S. B. Qian, J. Gibbs, S. Schuchmann, F. Buttgereit, J. R. Bennink, and J. W. Yewdell. 2003. Quantitating protein synthesis, degradation, and endogenous antigen processing. Immunity 18: 343-354.
75. Cascio, P., C. Hilton, A. F. Kisselev, K. L. Rock, and A. L. Goldberg. 2001. 26S proteasomes and immunoproteasomes produce mainly N-extended versions of an antigenic peptide. EMBO J. 20: 2357-2366.
76. Ackerman, A. L., C. Kyritsis, R. Tampé, and P. Cresswell. 2003. Early phagosomes in dendritic cells form a cellular compartment sufficient for cross presentation of exogenous antigens. Proc. Natl. Acad. Sci. USA 100: 12889-12894.
77. Guermonprez, P., L. Saveanu, M. Kleijmeer, J. Davoust, P. Van Endert, and S. Amigorena. 2003. ER-phagosome fusion defines an MHC class I cross-presentation compartment in dendritic cells. Nature 425: 397-402. (Pubitemid 37187268)
78. Lay, M. D., L. Zhang, R. M. Ribeiro, S. N. Mueller, G. T. Belz, and M. P. Davenport. 2009. Kinetics of major histocompatibility class I antigen presentation in acute infection. J. Immunol. 182: 902-911.
79. + T cells by infected dendritic cells in vivo. Nat. Immunol. 3: 265-271.
80. 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.
81. Shortman, K., and S. H. Naik. 2007. Steady-state and inflammatory dendritic-cell development. Nat. Rev. Immunol. 7: 19-30.
82. Shortman, K., and Y. J. Liu. 2002. Mouse and human dendritic cell subtypes. Nat. Rev. Immunol. 2: 151-161.
83. + T cells: cross-priming in infectious diseases. Curr. Opin. Immunol. 13: 437-441.
84. Sanders, V. M., and R. H. Straub. 2002. Norepinephrine, the β-adrenergic receptor, and immunity. Brain Behav. Immun. 16: 290-332.
85. + T cell responses. Proc. Natl. Acad. Sci. USA 106: 5300-5305.
86. Sternberg, E. M. 2006. Neural regulation of innate immunity: a coordinated nonspecific host response to pathogens. Nat. Rev. Immunol. 6: 318-328.
87. Grebe, K. M., K. Takeda, H. D. Hickman, A. L. Bailey, A. M. Bailey, A. C. Embry, J. R. Bennink, and J. W. Yewdell. 2010. Cutting edge: sympathetic nervous system increases proinflammatory cytokines and exacerbates influenza A virus pathogenesis. J. Immunol. 184: 540-544.
88. Dhabhar, F. S., and B. S. McEwen. 1996. Stress-induced enhancement of antigen-specific cell-mediated immunity. J. Immunol. 156: 2608-2615.