Adrenergic and glucocorticoid modulation of the sterile inflammatory response

Brain, Behavior, and Immunity

Volumn 36, Issue , 2014, Pages 183-192

  Cox, Stewart S ^a   Speaker, Kristin J ^a   Beninson, Lida A ^a   Craig, Wendy C ^a   Paton, Madeline M ^a   Fleshner, Monika ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

Acute stress; Catecholamines; Cytokine; Glucocorticoids; Heat shock protein; Monocyte chemotactic protein 1; Sterile inflammation

Indexed keywords

ADRENERGIC RECEPTOR; ALPHA 1 ADRENERGIC RECEPTOR; BETA 1 ADRENERGIC RECEPTOR; BETA 2 ADRENERGIC RECEPTOR; BETA 3 ADRENERGIC RECEPTOR; GLUCOCORTICOID; HEAT SHOCK PROTEIN 72; MIFEPRISTONE; MONOCYTE CHEMOTACTIC PROTEIN 1; PRAZOSIN; PROPRANOLOL;

ARTICLE; CIRCULATION; CONTROLLED STUDY; INFLAMMATION; LEUKOCYTE MIGRATION; LIVER; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; SPLEEN; SUBCUTANEOUS FAT;

ACUTE STRESS; CATECHOLAMINES; CYTOKINE; GLUCOCORTICOIDS; HEAT SHOCK PROTEIN; MONOCYTE CHEMOTACTIC PROTEIN-1; STERILE INFLAMMATION;

ADIPOSE TISSUE; ANIMALS; ELECTRIC STIMULATION; HSP70 HEAT-SHOCK PROTEINS; INFLAMMATION; INFLAMMATION MEDIATORS; MALE; RATS; RATS, INBRED F344; RECEPTORS, ADRENERGIC; RECEPTORS, GLUCOCORTICOID; SPLEEN; STRESS, PSYCHOLOGICAL;

EID: 84891826730     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2013.11.018     Document Type: Article

References (62)

1. Ando T., Rivier J., Yanaihara H., Arimura A. Peripheral corticotropin-releasing factor mediates the elevation of plasma IL-6 by immobilization stress in rats. Am. J. Physiol. 1998, 275:R1461-R1467.
2. Asea A. Mechanisms of HSP72 release. J. Biosci. 2007, 32:579-584.
3. Berg T., Piercey B.W., Jensen J. Role of beta1-3-adrenoceptors in blood pressure control at rest and during tyramine-induced norepinephrine release in spontaneously hypertensive rats. Hypertension 2010, 55:1224-1230.
4. Brattsand R., Linden M. Cytokine modulation by glucocorticoids: mechanisms and actions in cellular studies. Aliment. Pharmacol. Ther. 1996, 81-92.
5. Campisi J., Fleshner M. Role of extracellular HSP72 in acute stress-induced potentiation of innate immunity in active rats. J. Appl. Physiol. 2003, 94:43-52.
6. Cavero I., Roach A.G. The pharmacology of prazosin, a novel antihypertensive agent. Life Sci. 1980, 27:1525-1540.
7. Coppack S.W. Pro-inflammatory cytokines and adipose tissue. Proc. Nutr. Soc. 2001, 60:349-356.
8. Dessy C., Saliez J., Ghisdal P., Daneau G., Lobysheva I.I., Frérart F., Belge C., Jnaoui K., Noirhomme P., Feron O., Balligand J.L. Endothelial beta3-adrenoreceptors mediate nitric oxide-dependent vasorelaxation of coronary microvessels in response to the third-generation beta-blocker nebivolol. Circulation 2005, 112:1198-1205.
9. Dhabhar F.S. Stress-induced enhancement of cell-mediated immunity. Ann. N.Y. Acad. Sci. 1998, 840:359-372.
10. Dhabhar F.S. Enhancing versus suppressive effects of stress on immune function: implications for immunoprotection and immunopathology. NeuroImmunoModulation 2009, 16:300-317.
11. 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.
12. Elliott J. Alpha-adrenoceptors in equine digital veins: evidence for the presence of both alpha1 and alpha2-receptors mediating vasoconstriction. J. Vet. Pharmacol. Ther. 1997, 20:308-317.
13. Engler A., Roy S., Sen C.K., Padgett D.A., Sheridan J.F. Restraint stress alters lung gene expression in an experimental influenza A viral infection. J. Neuroimmunol. 2005, 162:103-111.
14. Fleshner M. Stress-evoked sterile inflammation, danger associated molecular patterns (DAMPs), microbial associated molecular patterns (MAMPs) and the inflammasome. Brain Behav. Immun. 2013, 27:1-7.
15. Fleshner M., Brennan F.X., Nguyen K., Watkins L.R., Maier S.F. RU-486 blocks differentially suppressive effect of stress on in vivo anti-KLH immunoglobulin response. Am. J. Physiol. 1996, 271:R1344-R1352.
16. Fleshner M., Campisi J., Deak T., Greenwood B.N., Kintzel J.A., Leem T.H., Smith T.P., Sorensen B. Acute stressor exposure facilitates innate immunity more in physically active than in sedentary rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2002, 282:R1680-R1686.
17. Fleshner M., Sharkey C.M., Nickerson M., Johnson J.D. Endogenous extracellular Hsp72 release is an adaptive feature of the acute stress response. Psychoneuroimmunology 2006, 1013-1034. Elsevier/Academic Press, San Diego.
18. Fleshner M., Johnson J.D., Friedman J. Extracellular Hsp72: a double-edged sword for host defense. Heat Shock Proteins: Potent Mediators of Inflammation and Immunity 2007, 235-263. Springer, Dordrecht, The Netherlands.
19. Griffiths R.J., Stam E.J., Downs J.T., Otterness I.G. ATP induces the release of IL-1 from LPS-primed cells in vivo. J. Immunol. 1995, 154:2821-2828.
20. Grubbs F.E. Procedures for detecting outlying observations in samples. Technometrics 1969, 11:1-21.
21. Hartl F.U. Molecular chaperones in cellular protein folding. Nature 1996, 381:571-579.
22. Haskó G., Elenkov I.J., Kvetan V., Vizi E.S. Differential effect of selective block of alpha 2-adrenoreceptors on plasma levels of tumour necrosis factor-alpha, interleukin-6 and corticosterone induced by bacterial lipopolysaccharide in mice. J. Endocrinol. 1995, 144:457-462.
23. Heikinheimo O., Kekkonen R. Dose-response relationships of RU 486. Ann. Med. 1993, 25:71-76.
24. Johnson J.D., Campisi J., Sharkey C.M., Kennedy S.L., Nickerson M., Fleshner M. Adrenergic receptors mediate stress-induced elevations in extracellular Hsp72. J. Appl. Physiol. (Bethesda, Md.: 1985) 2005, 99:1789-1795.
25. Johnson J.D., Campisi J., Sharkey C.M., Kennedy S.L., Nickerson M., Greenwood B.N., Fleshner M. Catecholamines mediate stress-induced increases in peripheral and central inflammatory cytokines. Neuroscience 2005, 135:1295-1307.
26. Kennedy S.L., Nickerson M., Campisi J., Johnson J.D., Smith T.P., Sharkey C., Fleshner M. Splenic norepinephrine depletion following acute stress suppresses in vivo antibody response. J. Neuroimmunol. 2005, 165:150-160.
27. Kong Y., Zhang Y., Li N., Zhang L., Gao Y., Xue H., Li Y., Li W.M. Association between beta3-adrenergic receptor and oxidative stress in chronic heart failure rats. Zhonghua Xinxueguanbing Zazhi 2010, 38:435-439.
28. Krief S., Lönnqvist F., Raimbault S., Baude B., Van Spronsen A., Arner P., Strosberg A.D., Ricquier D., Emorine L.J. Tissue distribution of beta 3-adrenergic receptor mRNA in man. J. Clin. Invest. 1993, 91:344-349.
29. Kubes P., Mehal W.Z. Sterile inflammation in the liver. Gastroenterology 2012, 143:1158-1172.
30. Kunicka J.E., Talle M.A., Denhardt G.H., Brown M., Prince L.A., Goldstein G. Immunosuppression by glucocorticoids: inhibition of production of multiple lymphokines by in vivo administration of dexamethasone. Cell. Immunol. 1993, 149:39-49.
31. Lancaster G.I., Febbraio M.A. Mechanisms of stress-induced cellular HSP72 release: implications for exercise-induced increases in extracellular HSP72. Exerc. Immunol. Rev. 2005, 11:46-52.
32. Maslanik T., Bernstein-Hanley I., Helwig B., Fleshner M. The impact of acute-stressor exposure on splenic innate immunity: a gene expression analysis. Brain Behav. Immun. 2012, 26:142-149.
33. Maslanik T., Tannura K., Mahaffey L., Loughridge A.B., Benninson L., Ursell L., Greenwood B.N., Fleshner M. Commensal bacteria and MAMPs are necessary for stress-induced increases in IL-1β and IL-18 but not IL-6, IL-10 or MCP-1. PLoS ONE 2012, 7:e50636.
34. Maslanik T., Mahaffey L., Tannura K., Beninson L., Greenwood B.N., Fleshner M. The inflammasome and danger associated molecular patterns (DAMPs) are implicated in cytokine and chemokine responses following stressor exposure. Brain Behav. Immun. 2013, 28:54-62.
35. Menkes D.B., Baraban J.M., Aghajanian G.K. Prazosin selectively antagonizes neuronal responses mediated by alpha1-adrenoceptors in brain. Naunyn Schmiedebergs. Arch. Pharmacol. 1981, 317:273-275.
36. Michel M.C., Harding S.E., Bond R.A. Are there functional β3-adrenoceptors in the human heart?. Br. J. Pharmacol. 2011, 162:817-822.
37. Mohamed-Ali V., Pinkney J.H., Coppack S.W. Adipose tissue as an endocrine and paracrine organ. Int. J. Obes. Relat. Metab. Disord. 1998, 22:1145-1158.
38. Mottillo E.P., Shen X.J., Granneman J.G. Beta3-adrenergic receptor induction of adipocyte inflammation requires lipolytic activation of stress kinases p38 and JNK. Biochim. Biophys. Acta 2010, 1801:1048-1055.
39. Nadeau S., Rivest S. Glucocorticoids play a fundamental role in protecting the brain during innate immune response. J. Neurosci. 2003, 23:5536-5544.
40. Netea M.G., Simon A., Van de Veerdonk F., Kullberg B.J., Van der Meer J.W.M., Joosten L.A.B. IL-1beta processing in host defense: beyond the inflammasomes. PLoS Pathog. 2010, 6:e1000661.
41. Nguyen K.T., Deak T., Will M.J., Hansen M.K., Hunsaker B.N., Fleshner M., Watkins L.R., Maier S.F. Timecourse and corticosterone sensitivity of the brain, pituitary, and serum interleukin-1beta protein response to acute stress. Brain Res. 2000, 859:193-201.
42. Nickerson M., Kennedy S.L., Johnson J.D., Fleshner M. Sexual dimorphism of the intracellular heat shock protein 72 response. J. Appl. Physiol. (Bethesda, Md.: 1985) 2006, 101:566-575.
43. O'Connor K.A., Johnson J.D., Hansen M.K., Wieseler Frank J.L., Maksimova E., Watkins L.R., Maier S.F. Peripheral and central proinflammatory cytokine response to a severe acute stressor. Brain Res. 2003, 991:123-132.
44. Ott L. An Introduction to Statistical Methods and Data Analysis 1984, Duxbury Press, Boston, (pp. 365-370).
45. Pardridge W.M., Sakiyama R., Fierer G. Transport of propranolol and lidocaine through the rat blood-brain barrier: primary role of globulin-bound drug. J. Clin. Invest. 1983, 71:900-908.
46. Pastores S.M., Hasko G., Vizi E.S., Kvetan V. Cytokine production and its manipulation by vasoactive drugs. New Horiz. 1996, 4:252-264.
47. Persoons J.H., Schornagel K., Brevé J., Berkenbosch F., Kraal G. Acute stress affects cytokines and nitric oxide production by alveolar macrophages differently. Am. J. Respir. Crit. Care Med. 1995, 152:619-624.
48. Pertsov S.S., Koplik E.V., Stepanyuk V.L., Simbirtsev A.S. Blood cytokines in rats with various behavioral characteristics during emotional stress and treatment with interleukin-1beta. Bull. Exp. Biol. Med. 2009, 148:196-199.
49. Petersen R.G. Design and Analysis of Experiments 1985, Marcel Dekker, Inc., New York and Basel, (pp. 77-84).
50. Pittman K., Kubes P. Damage-associated molecular patterns control neutrophil recruitment. J Innate Immun. 2013, 5:315-323.
51. Pond C.M. Adipose tissue: quartermaster to the lymph node garrisons. Biologist 2000, 47:147-150. (London, UK).
52. Rang H.P. Pharmacology 2003, Churchill Livingstone, Edinburgh, (pp. 163-270).
53. Rath G., Balligand J.L., Dessy C., Chantal D. Vasodilatory mechanisms of beta receptor blockade. Curr. Hypertens. Rep. 2012, 14:310-317.
54. Rollins B.J., Yoshimura T., Leonard E.J., Pober J.S. Cytokine-activated human endothelial cells synthesize and secrete a monocyte chemoattractant, MCP-1/JE. Am. J. Pathol. 1990, 136:1229-1233.
55. Speaker, K.J., Cox, S.S., Paton, M.M., Serebrakian, A., Maslanik, T., Greenwood, B.N., Fleshner, M., 2013. Habitual exercise exerts a depot specific, anti-inflammatory effect on stress-evoked cytokines in the white adipose tissue of lean rats. Brain Behav. Immun., 2013. http://dx.doi.org/10.1016/j.bbi.2013.10.028.
56. Steer J.H., Kroeger K.M., Abraham L.J., Joyce D.A. Glucocorticoids suppress tumor necrosis factor-alpha expression by human monocytic THP-1 cells by suppressing transactivation through adjacent NF-kappa B and c-Jun-activating transcription factor-2 binding sites in the promoter. J. Biol. Chem. 2000, 275:18432-18440.
57. Tan K.S., Nackley A.G., Satterfield K., Maixner W., Diatchenko L., Flood P.M. Beta2 adrenergic receptor activation stimulates pro-inflammatory cytokine production in macrophages via PKA- and NF-kappaB-independent mechanisms. Cell. Signal. 2007, 19:251-260.
58. Thompson R.S., Strong P.V., Fleshner M. Physiological consequences of repeated exposures to conditioned fear. Behav. Sci. 2012, 2:57-78.
59. Uchida Y., Takeshita K., Yamamoto K., Kikuchi R., Nakayama T., Nomura M., Cheng X.W., Egashira K., Matsushita T., Nakamura H., Murohara T. Stress augments insulin resistance and prothrombotic state: role of visceral adipose-derived monocyte chemoattractant protein-1. Diabetes 2012, 61:1552-1561.
60. You Z., Luo C., Zhang W., Chen Y., He J., Zhao Q., Zuo R., Wu Y. Pro- and anti-inflammatory cytokines expression in rat's brain and spleen exposed to chronic mild stress: involvement in depression. Behav. Brain Res. 2011, 225:135-141.
61. Zhou D., Kusnecov A.W., Shurin M.R., DePaoli M., Rabin B.S. Exposure to physical and psychological stressors elevates plasma interleukin 6: relationship to the activation of hypothalamic-pituitary-adrenal axis. Endocrinology 1993, 133:2523-2530.
62. Zuckerman S.H., Shellhaas J., 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. 1989, 19:301-305.