β-Adrenergic receptor mediated increases in activation and function of natural killer cells following repeated social disruption

Brain, Behavior, and Immunity

Volumn 26, Issue 8, 2012, Pages 1226-1238

  Tarr, Andrew J ^a   Powell, Nicole D ^a   Reader, Brenda F ^a   Bhave, Neela S ^b   Roloson, Amanda L ^a   Carson, William E ^b   Sheridan, John F ^a,b  

^a OHIO STATE UNIVERSITY   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

Activation; Degranulation; Inhibitory; Interferon gamma; NK cells; Social disruption; Stress

Indexed keywords

BETA ADRENERGIC RECEPTOR; CD16 ANTIGEN; CD69 ANTIGEN; GAMMA INTERFERON; IMMUNOGLOBULIN G; INTERLEUKIN 2; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; NATURAL KILLER CELL RECEPTOR NKG2A;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN EXPRESSION; ARTICLE; CELL ACTIVATION; CELL FUNCTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; MALE; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR INTRINSIC ACTIVITY; SIGNAL TRANSDUCTION; SOCIAL STRESS;

ANIMALS; BEHAVIOR, ANIMAL; DISEASE MODELS, ANIMAL; KILLER CELLS, NATURAL; LUNG; MALE; MICE; MICE, INBRED C57BL; RECEPTORS, ADRENERGIC, BETA; SIGNAL TRANSDUCTION; SOCIAL BEHAVIOR; SPLEEN;

EID: 84867226089     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2012.07.002     Document Type: Article

References (64)

1. Alter G., Malenfant J.M., Altfeld M. CD107a as a functional marker for the identification of natural killer cell activity. J. Immunol. Methods 2004, 294:15-22.
2. Andoniou C.E., van Dommelen S.L., Voigt V., Andrews D.M., Brizard G., sselin-Paturel C., Delale T., Stacey K.J., Trinchieri G., gli-Esposti M.A. Interaction between conventional dendritic cells and natural killer cells is integral to the activation of effective antiviral immunity. Nat. Immunol. 2005, 6:1011-1019.
3. Avitsur R., Kavelaars A., Heijnen C., Sheridan J.F. Social stress and the regulation of tumor necrosis factor-alpha secretion. Brain Behav. Immun. 2005, 19:311-317.
4. Avitsur R., Padgett D.A., Dhabhar F.S., Stark J.L., Kramer K.A., Engler H., Sheridan J.F. Expression of glucocorticoid resistance following social stress requires a second signal. J. Leukoc. Biol. 2003, 74:507-513.
5. Avitsur R., Stark J.L., Dhabhar F.S., Sheridan J.F. Social stress alters splenocyte phenotype and function. J. Neuroimmunol. 2002, 132:66-71.
6. Avitsur R., Stark J.L., Sheridan J.F. Social stress induces glucocorticoid resistance in subordinate animals. Horm. Behav. 2001, 39:247-257.
7. Bailey M.T., Avitsur R., Engler H., Padgett D.A., Sheridan J.F. Physical defeat reduces the sensitivity of murine splenocytes to the suppressive effects of corticosterone. Brain Behav. Immun. 2004, 18:416-424.
8. Bailey M.T., Engler H., Powell N.D., Padgett D.A., Sheridan J.F. Repeated social defeat increases the bactericidal activity of splenic macrophages through a Toll-like receptor-dependent pathway. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2007, 293:R1180-R1190.
9. Benschop R.J., Jacobs R., Sommer B., Schurmeyer T.H., Raab J.R., Schmidt R.E., Schedlowski M. Modulation of the immunologic response to acute stress in humans by beta-blockade or benzodiazepines. FASEB J. 1996, 10:517-524.
10. Benschop R.J., Oostveen F.G., Heijnen C.J., Ballieux R.E. Beta 2-adrenergic stimulation causes detachment of natural killer cells from cultured endothelium. Eur. J. Immunol. 1993, 23:3242-3247.
11. Betts M.R., Brenchley J.M., Price D.A., De Rosa S.C., Douek D.C., Roederer M., Koup R.A. Sensitive and viable identification of antigen-specific CD8+ T cells by a flow cytometric assay for degranulation. J. Immunol. Methods 2003, 281:65-78.
12. Boehm U., Klamp T., Groot M., Howard J.C. Cellular responses to interferon-gamma. Annu. Rev. Immunol. 1997, 15:749-795.
13. Borrego F., Robertson M.J., Ritz J., Pena J., Solana R. CD69 is a stimulatory receptor for natural killer cell and its cytotoxic effect is blocked by CD94 inhibitory receptor. Immunology 1999, 97:159-165.
14. Brooks A.G., Posch P.E., Scorzelli C.J., Borrego F., Coligan J.E. NKG2A complexed with CD94 defines a novel inhibitory natural killer cell receptor. J. Exp. Med. 1997, 185:795-800.
15. Carson W.E., Giri J.G., Lindemann M.J., Linett M.L., Ahdieh M., Paxton R., Anderson D., Eisenmann J., Grabstein K., Caligiuri M.A. Interleukin (IL) 15 is a novel cytokine that activates human natural killer cells via components of the IL-2 receptor. J. Exp. Med. 1994, 180:1395-1403.
16. Carson W.E., Parihar R., Lindemann M.J., Personeni N., Dierksheide J., Meropol N.J., Baselga J., Caligiuri M.A. Interleukin-2 enhances the natural killer cell response to Herceptin-coated Her2/neu-positive breast cancer cells. Eur. J. Immunol. 2001, 31:3016-3025.
17. Curry J.M., Hanke M.L., Piper M.G., Bailey M.T., Bringardner B.D., Sheridan J.F., Marsh C.B. Social disruption induces lung inflammation. Brain Behav. Immun. 2010, 24:394-402.
18. Dhabhar F.S. Acute stress enhances while chronic stress suppresses skin immunity. The role of stress hormones and leukocyte trafficking. Ann. N. Y. Acad. Sci. 2000, 917:876-893.
19. Dhabhar F.S., McEwen B.S. Acute stress enhances while chronic stress suppresses cell-mediated immunity in vivo: a potential role for leukocyte trafficking. Brain Behav. Immun. 1997, 11:286-306.
20. Dhabhar F.S., Miller A.H., McEwen B.S., Spencer R.L. Stress-induced changes in blood leukocyte distribution. Role of adrenal steroid hormones. J. Immunol. 1996, 157:1638-1644.
21. Dhabhar F.S., Miller A.H., McEwen B.S., Spencer R.L. Effects of stress on immune cell distribution. Dynamics and hormonal mechanisms. J. Immunol. 1995, 154:5511-5527.
22. Dokur M., Boyadjieva N., Sarkar D.K. Catecholaminergic control of NK cell cytolytic activity regulatory factors in the spleen. J. Neuroimmunol. 2004, 151:148-157.
23. Dong-Newsom P., Powell N.D., Bailey M.T., Padgett D.A., Sheridan J.F. Repeated social stress enhances the innate immune response to a primary HSV-1 infection in the cornea and trigeminal ganglia of Balb/c mice. Brain Behav. Immun. 2010, 24:273-280.
24. Engler H., Bailey M.T., Engler A., Sheridan J.F. Effects of repeated social stress on leukocyte distribution in bone marrow, peripheral blood and spleen. J. Neuroimmunol. 2004, 148:106-115.
25. Engler H., Dawils L., Hoves S., Kurth S., Stevenson J.R., Schauenstein K., Stefanski V. Effects of social stress on blood leukocyte distribution: the role of alpha- and beta-adrenergic mechanisms. J. Neuroimmunol. 2004, 156:153-162.
26. Engler H., Engler A., Bailey M.T., Sheridan J.F. Tissue-specific alterations in the glucocorticoid sensitivity of immune cells following repeated social defeat in mice. J. Neuroimmunol. 2005, 163:110-119.
27. Feau S., Facchinetti V., Granucci F., Citterio S., Jarrossay D., Seresini S., Protti M.P., Lanzavecchia A., Ricciardi-Castagnoli P. Dendritic cell-derived IL-2 production is regulated by IL-15 in humans and in mice. Blood 2005, 105:697-702.
28. Fehniger T.A., Carson W.E., Caligiuri M.A. Costimulation of human natural killer cells is required for interferon gamma production. Transpl. Proc. 1999, 31:1476-1478.
29. Fehniger T.A., Shah M.H., Turner M.J., VanDeusen J.B., Whitman S.P., Cooper M.A., Suzuki K., Wechser M., Goodsaid F., Caligiuri M.A. Differential cytokine and chemokine gene expression by human NK cells following activation with IL-18 or IL-15 in combination with IL-12: implications for the innate immune response. J. Immunol. 1999, 162:4511-4520.
30. Gerosa F., Tommasi M., Benati C., Gandini G., Libonati M., Tridente G., Carra G., Trinchieri G. Differential effects of tyrosine kinase inhibition in CD69 antigen expression and lytic activity induced by rIL-2, rIL-12, and rIFN-alpha in human NK cells. Cell. Immunol. 1993, 150:382-390.
31. Granucci F., Zanoni I., Pavelka N., van Dommelen S.L., Andoniou C.E., Belardelli F., gli Esposti M.A., Ricciardi-Castagnoli P. A contribution of mouse dendritic cell-derived IL-2 for NK cell activation. J. Exp. Med. 2004, 200:287-295.
32. Hanke, M.L., Powell, N.D., Stiner, L.M., Bailey, M.T., Sheridan, J.F., in press. Beta adrenergic blockade decreases the immunomodulatory effects of social disruption stress. Brain Behav. Immun.
33. Held W., Cado D., Raulet D.H. Transgenic expression of the Ly49A natural killer cell receptor confers class I major histocompatibility complex (MHC)-specific inhibition and prevents bone marrow allograft rejection. J. Exp. Med. 1996, 184:2037-2041.
34. Henney C.S., Kuribayashi K., Kern D.E., Gillis S. Interleukin-2 augments natural killer cell activity. Nature 1981, 291:335-338.
35. Houchins J.P., Lanier L.L., Niemi E.C., Phillips J.H., Ryan J.C. Natural killer cell cytolytic activity is inhibited by NKG2-A and activated by NKG2-C. J. Immunol. 1997, 158:3603-3609.
36. Irwin M., Patterson T., Smith T.L., Caldwell C., Brown S.A., Gillin J.C., Grant I. Reduction of immune function in life stress and depression. Biol. Psychiatry 1990, 27:22-30.
37. Karlhofer F.M., Ribaudo R.K., Yokoyama W.M. The interaction of Ly-49 with H-2Dd globally inactivates natural killer cell cytolytic activity. Trans. Assoc. Am. Physicians 1992, 105:72-85.
38. Kimura K., Isowa T., Matsunaga M., Murashima S., Ohira H. The temporal redistribution pattern of NK cells under acute stress based on CD62L adhesion molecule expression. Int. J. Psychophysiol. 2008, 70:63-69.
39. Kinsey S.G., Bailey M.T., Sheridan J.F., Padgett D.A., Avitsur R. Repeated social defeat causes increased anxiety-like behavior and alters splenocyte function in C57BL/6 and CD-1 mice. Brain Behav. Immun. 2007, 21:458-466.
40. Krug A., French A.R., Barchet W., Fischer J.A., Dzionek A., Pingel J.T., Orihuela M.M., Akira S., Yokoyama W.M., Colonna M. TLR9-dependent recognition of MCMV by IPC and DC generates coordinated cytokine responses that activate antiviral NK cell function. Immunity 2004, 21:107-119.
41. Liu T., Tang Q., Hendricks R.L. Inflammatory infiltration of the trigeminal ganglion after herpes simplex virus type 1 corneal infection. J. Virol. 1996, 70:264-271.
42. Long E.O. Negative signaling by inhibitory receptors: the NK cell paradigm. Immunol. Rev. 2008, 224:70-84.
43. Mach B., Steimle V., Martinez-Soria E., Reith W. Regulation of MHC class II genes: lessons from a disease. Annu. Rev. Immunol. 1996, 14:301-331.
44. Marquez M.E., Millet C., Stekman H., Conesa A., Deglesne P.A., Toro F., Sanctis J.D., Blanca I. CD16 cross-linking induces increased expression of CD56 and production of IL-12 in peripheral NK cells. Cell. Immunol. 2010, 264:86-92.
45. Mays J.W., Bailey M.T., Hunzeker J.T., Powell N.D., Papenfuss T., Karlsson E.A., Padgett D.A., Sheridan J.F. Influenza virus-specific immunological memory is enhanced by repeated social defeat. J. Immunol. 2010, 184:2014-2025.
46. Moretta A., Poggi A., Pende D., Tripodi G., Orengo A.M., Pella N., Augugliaro R., Bottino C., Ciccone E., Moretta L. CD69-mediated pathway of lymphocyte activation: anti-CD69 monoclonal antibodies trigger the cytolytic activity of different lymphoid effector cells with the exception of cytolytic T lymphocytes expressing T cell receptor alpha/beta. J. Exp. Med. 1991, 174:1393-1398.
47. Orange J.S., Biron C.A. Characterization of early IL-12, IFN-alphabeta, and TNF effects on antiviral state and NK cell responses during murine cytomegalovirus infection. J. Immunol. 1996, 156:4746-4756.
48. Perussia B. Fc receptors on natural killer cells. Curr. Top. Microbiol. Immunol. 1998, 230:63-88.
49. Powell N.D., Bailey M.T., Mays J.W., Stiner-Jones L.M., Hanke M.L., Padgett D.A., Sheridan J.F. Repeated social defeat activates dendritic cells and enhances Toll-like receptor dependent cytokine secretion. Brain Behav. Immun. 2009, 23:225-231.
50. Powell N.D., Mays J.W., Bailey M.T., Hanke M.L., Sheridan J.F. Immunogenic dendritic cells primed by social defeat enhance adaptive immunity to influenza A virus. Brain Behav. Immun. 2011, 25:46-52.
51. Rehman J., Mills P.J., Carter S.M., Chou J., Thomas J., Maisel A.S. Dynamic exercise leads to an increase in circulating ICAM-1: further evidence for adrenergic modulation of cell adhesion. Brain Behav. Immun. 1997, 11:343-351.
52. Sanders V.M., Straub R.H. Norepinephrine, the beta-adrenergic receptor, and immunity. Brain Behav. Immun. 2002, 16:290-332.
53. Schedlowski M., Jacobs R., Alker J., Prohl F., Stratmann G., Richter S., Hadicke A., Wagner T.O., Schmidt R.E., Tewes U. Psychophysiological, neuroendocrine and cellular immune reactions under psychological stress. Neuropsychobiology 1993, 28:87-90.
54. Schedlowski M., Jacobs R., Stratmann G., Richter S., Hadicke A., Tewes U., Wagner T.O., Schmidt R.E. Changes of natural killer cells during acute psychological stress. J. Clin. Immunol. 1993, 13:119-126.
55. Shakhar G., Ben-Eliyahu S. In vivo beta-adrenergic stimulation suppresses natural killer activity and compromises resistance to tumor metastasis in rats. J. Immunol. 1998, 160:3251-3258.
56. Stark J.L., Avitsur R., Hunzeker J., Padgett D.A., Sheridan J.F. Interleukin-6 and the development of social disruption-induced glucocorticoid resistance. J. Neuroimmunol. 2002, 124:9-15.
57. Stark J.L., Avitsur R., Padgett D.A., Campbell K.A., Beck F.M., Sheridan J.F. Social stress induces glucocorticoid resistance in macrophages. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2001, 280:R1799-R1805.
58. Takamoto T., Hori Y., Koga Y., Toshima H., Hara A., Yokoyama M.M. Norepinephrine inhibits human natural killer cell activity in vitro. Int. J. Neurosci. 1991, 58:127-131.
59. Trapani J.A., Jans D.A., Jans P.J., Smyth M.J., Browne K.A., Sutton V.R. Efficient nuclear targeting of granzyme B and the nuclear consequences of apoptosis induced by granzyme B and perforin are caspase-dependent, but cell death is caspase-independent. J. Biol. Chem. 1998, 273:27934-27938.
60. Trapani J.A., Smyth M.J. Functional significance of the perforin/granzyme cell death pathway. Nat. Rev. Immunol. 2002, 2:735-747.
61. Trinchieri G. Biology of natural killer cells. Adv. Immunol. 1989, 47:187-376.
62. Tseng R.J., Padgett D.A., Dhabhar F.S., Engler H., Sheridan J.F. Stress-induced modulation of NK activity during influenza viral infection: role of glucocorticoids and opioids. Brain Behav. Immun. 2005, 19:153-164.
63. Wohleb E.S., Hanke M.L., Corona A.W., Powell N.D., Stiner L.M., Bailey M.T., Nelson R.J., Godbout J.P., Sheridan J.F. {beta}-Adrenergic receptor antagonism prevents anxiety-like behavior and microglial reactivity induced by repeated social defeat. J. Neurosci. 2011, 31:6277-6288.
64. Zingoni A., Palmieri G., Morrone S., Carretero M., Lopez-Botel M., Piccoli M., Frati L., Santoni A. CD69-triggered ERK activation and functions are negatively regulated by CD94/NKG2-A inhibitory receptor. Eur. J. Immunol. 2000, 30:644-651.