Repeated stressor exposure regionally enhances beta-adrenergic receptor-mediated brain IL-1β production

Brain, Behavior, and Immunity

Volumn 26, Issue 8, 2012, Pages 1249-1255

  Porterfield, Veronica M ^a   Gabella, Kristin M ^a   Simmons, Mark A ^b   Johnson, John D ^a  

^a KENT STATE UNIVERSITY   (United States)

^b NORTHEAST OHIO MEDICAL UNIVERSITY   (United States)

Author keywords

Anhedonia; Chronic mild stress; Cytokine; Depression; Norepinephrine; Rat; Receptor binding; Sensitization

Indexed keywords

BETA ADRENERGIC RECEPTOR; BETA ADRENERGIC RECEPTOR STIMULATING AGENT; INTERLEUKIN 1; INTERLEUKIN 1BETA; ISOPRENALINE; NORADRENALIN;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN STEM; CHRONIC STRESS; FISCHER 344 RAT; HIPPOCAMPUS; HYPOTHALAMUS; MALE; NEUROPATHOLOGY; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT;

ANIMALS; BRAIN; DEPRESSION; INTERLEUKIN-1BETA; MALE; NOREPINEPHRINE; RATS; RATS, INBRED F344; RECEPTORS, ADRENERGIC, BETA; STRESS, PHYSIOLOGICAL;

EID: 84867203989     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2012.08.001     Document Type: Article

References (55)

1. Asanuma M., Ogawa N., Mizukawa K., Haba K., Hirata H., Mori A. Distribution of the beta-2 adrenergic receptor messenger RNA in the rat brain by in situ hybridization histochemistry: effects of chronic reserpine treatment. Neurochem. Res. 1991, 16:1253-1256.
2. Bekris S., Antoniou K., Daskas S., Papadopoulou-Daifoti Z. Behavioural and neurochemical effects induced by chronic mild stress applied to two different rat strains. Behav. Brain Res. 2005, 161:45-59.
3. Ben Menachem-Zidon O., Goshen I., Kreisel T., Ben Menahem Y., Reinhartz E., Ben Hur T., Yirmiya R. Intrahippocampal transplantation of transgenic neural precursor cells overexpressing interleukin-1 receptor antagonist blocks chronic isolation-induced impairment in memory and neurogenesis. Neuropsychopharmacology 2008, 33:2251-2262.
4. Bhatnagar S., Dallman M. Neuroanatomical basis for facilitation of hypothalamic-pituitary-adrenal responses to a novel stressor after chronic stress. Neuroscience 1998, 84:1025-1039.
5. Blandino P., Barnum C.J., Deak T. The involvement of norepinephrine and microglia in hypothalamic and splenic IL-1beta responses to stress. J. Neuroimmunol. 2006, 173:87-95.
6. Blandino P., Barnum C.J., Solomon L.G., Larish Y., Lankow B.S., Deak T. Gene expression changes in the hypothalamus provide evidence for regionally-selective changes in IL-1 and microglial markers after acute stress. Brain Behav. Immun. 2009, 23:958-968.
7. Bondi C.O., Jett J.D., Morilak D.A. Beneficial effects of desipramine on cognitive function of chronically stressed rats are mediated by alpha1-adrenergic receptors in medial prefrontal cortex. Prog. Neuropsychopharmacol. Biol. Psychiatry 2010, 34:913-923.
8. Camp R.M., Remus J.L., Kalburgi S.N., Porterfield V.M., Johnson J.D. Fear conditioning can contribute to behavioral changes observed in a repeated stress model. Behav. Brain Res. 2012, 233:536-544.
9. Collins S., Caron M.G., Lefkowitz R.J. From ligand binding to gene expression: new insights into the regulation of G-protein-coupled receptors. Trends Biochem. Sci. 1992, 17:37-39.
10. Craft T.K., DeVries A.C. Role of IL-1 in poststroke depressive-like behavior in mice. Biol. Psychiatry 2006, 60:812-818.
11. Dalla C., Antoniou K., Drossopoulou G., Xagoraris M., Kokras N., Sfikakis A., Papadopoulou-Daifoti Z. Chronic mild stress impact: are females more vulnerable?. Neuroscience 2005, 135:703-714.
12. Fillenz M. Noradrenergic Neurons 1990, Cambridge University Press, Cambridge.
13. Flak J.N., Ostrander M.M., Tasker J.G., Herman J.P. Chronic stress-induced neurotransmitter plasticity in the PVN. J. Comp. Neurol. 2009, 517:156-165.
14. Flugge G. Alterations in the central nervous alpha 2-adrenoceptor system under chronic psychosocial stress. Neuroscience 1996, 75:187-196.
15. 125I]iodocyanopindolol bindings sites. Cell Mol. Neurobiol. 1997, 17:417-432.
16. Flugge G., Van Kampen M., Mijnster M.J. Perturbations in brain monoamine systems during stress. Cell Tissue Res. 2004, 315:1-14.
17. Frank M.G., Baratta M.V., Sprunger D.B., Watkins L.R., Maier S.F. Microglia serve as a neuroimmune substrate for stress-induced potentiation of CNS pro-inflammatory cytokine responses. Brain Behav. Immun. 2007, 21:47-59.
18. Frank, M.G., Miguel, Z.D., Watkins, L.R., Maier, S.F., 2009. Prior exposure to glucocorticoids sensitizes the neuroinflammatory and peripheral inflammatory responses to E. coli lipopolysaccharide. Brain Behav. Immun.
19. Goshen I., Kreisel T., Ben-Menachem-Zidon O., Licht T., Weidenfeld J., Ben-Hur T., Yirmiya R. Brain interleukin-1 mediates chronic stress-induced depression in mice via adrenocortical activation and hippocampal neurogenesis suppression. Mol. Psychiatry 2008, 13:717-728.
20. Grippo A.J., Francis J., Beltz T.G., Felder R.B., Johnson A.K. Neuroendocrine and cytokine profile of chronic mild stress-induced anhedonia. Physiol. Behav. 2005, 84:697-706.
21. Herman J.P., Flak J., Jankord R. Chronic stress plasticity in the hypothalamic paraventricular nucleus. Prog. Brain Res. 2008, 170:353-364.
22. Hinwood M., Morandini J., Day T.A., Walker F.R. Evidence that microglia mediate the neurobiological effects of chronic psychological stress on the medial prefrontal cortex 2011, Cereb. Cortex.
23. Hosoda K., Duman R.S. Regulation of beta 1-adrenergic receptor mRNA and ligand binding by antidepressant treatments and norepinephrine depletion in rat frontal cortex. J. Neurochem. 1993, 60:1335-1343.
24. Jedema H.P., Sved A.F., Zigmond M.J., Finlay J.M. Sensitization of norepinephrine release in medial prefrontal cortex: effect of different chronic stress protocols. Brain Res. 1999, 830:211-217.
25. Johnson E.W., Wolfe B.B., Molinoff P.B. Regulation of subtypes of beta-adrenergic receptors in rat brain following treatment with 6-hydroxydopamine. J. Neurosci. 1989, 9:2297-2305.
26. 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.
27. Johnson J.D., Cortez V., Kennedy S.L., Foley T.E., Hanson H., Fleshner M. Role of central beta-adrenergic receptors in regulating proinflammatory cytokine responses to a peripheral bacterial challenge. Brain Behav. Immun. 2008, 22:1078-1086.
28. Johnson J.D., O'Connor K.A., Deak T., Stark M., Watkins L.R., Maier S.F. Prior stressor exposure sensitizes LPS-induced cytokine production. Brain Behav. Immun. 2002, 16:461-476.
29. Klimek V., Papp M. The effect of MK-801 and imipramine on beta-adrenergic and 5-HT2 receptors in the chronic mild stress model of depression in rats. Polish J. Pharmacol. 1994, 46:67-69.
30. Koo J.W., Duman R.S. IL-1beta is an essential mediator of the antineurogenic and anhedonic effects of stress. Proc. Natl. Acad. Sci. USA 2008, 105:751-756.
31. Koo J.W., Duman R.S. Evidence for IL-1 receptor blockade as a therapeutic strategy for the treatment of depression. Curr. Opin. Invest. Drugs 2009, 10:664-671.
32. Ma S., Morilak D.A. Chronic intermittent cold stress sensitises the hypothalamic-pituitary-adrenal response to a novel acute stress by enhancing noradrenergic influence in the rat paraventricular nucleus. J. Neuroendocrinol. 2005, 17:761-769.
33. McNamee E.N., Griffin E.W., Ryan K.M., Ryan K.J., Heffernan S., Harkin A., Connor T.J. Noradrenaline acting at beta-adrenoceptors induces expression of IL-1beta and its negative regulators IL-1ra and IL-1RII, and drives an overall anti-inflammatory phenotype in rat cortex. Neuropharmacology 2010, 59:37-48.
34. Miller A.H., Maletic V., Raison C.L. Inflammation and its discontents: the role of cytokines in the pathophysiology of major depression. Biol. Psychiatry 2009, 65:732-741.
35. Morilak D.A., Barrera G., Echevarria D.J., Garcia A.S., Hernandez A., Ma S., Petre C.O. Role of brain norepinephrine in the behavioral response to stress. Prog. Neuropsychopharmacol. Biol. Psychiatry 2005, 29:1214-1224.
36. Papp M., Klimek V., Willner P. Effects of imipramine on serotonergic and beta-adrenergic receptor binding in a realistic animal model of depression. Psychopharmacology (Berl.) 1994, 114:309-314.
37. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates 1998, Academic Press, San Diego.
38. Porterfield V.M., Zimomra Z.R., Caldwell E.A., Camp R.M., Gabella K.M., Johnson J.D. Rat strain differences in restraint stress-induced brain cytokines. Neuroscience 2011, 188:48-54.
39. 14C]inulin in rat. Neuroscience 2000, 95:577-592.
40. Pugh C.R., Nguyen K.T., Gonyea J.L., Fleshner M., Wakins L.R., Maier S.F., Rudy J.W. Role of interleukin-1 beta in impairment of contextual fear conditioning caused by social isolation. Behav. Brain Res. 1999, 106:109-118.
41. Raison C.L., Dantzer R., Kelley K.W., Lawson M.A., Woolwine B.J., Vogt G., Spivey J.R., Saito K., Miller A.H. CSF concentrations of brain tryptophan and kynurenines during immune stimulation with IFN-alpha: relationship to CNS immune responses and depression. Mol. Psychiatry 2010, 15:393-403.
42. Schmidt H.D., Duman R.S. The role of neurotrophic factors in adult hippocampal neurogenesis, antidepressant treatments and animal models of depressive-like behavior. Behav. Pharmacol. 2007, 18:391-418.
43. Seo D.O., Shin C.Y., Seung C.H., Han S.Y., Ko K.H. Effects of chronic electroconvulsive shock on the expression of beta-adrenergic receptors in rat brain: immunological study. Biochem. Mol. Biol. Int. 1999, 47:195-203.
44. Staehelin M., Muller P., Portenier M., Harris A.W. Beta-Adrenergic receptors and adenylate cyclase activity in murine lymphoid cell lines. J. Cyclic Nucleotide Protein Phosphorylat. Res. 1985, 10:55-64.
45. Suarez E.C., Shiller A.D., Kuhn C.M., Schanberg S., Williams R.B., Zimmermann E.A. The relationship between hostility and beta-adrenergic receptor physiology in health young males. Psychosom. Med. 1997, 59:481-487.
46. Sugama S., Takenouchi T., Fujita M., Kitani H., Hashimoto M. Cold stress induced morphological microglial activation and increased IL-1beta expression in astroglial cells in rat brain. J. Neuroimmunol. 2011, 233:29-36.
47. Sugama S., Takenouchi T., Sekiyama K., Kitani H., Hashimoto M. Immunological responses of astroglia in the rat brain under acute stress: interleukin 1 beta co-localized in astroglia. Neuroscience 2011, 192:429-437.
48. 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.
49. Tomozawa Y., Yabuuchi K., Inoue T., Satoh M. Participation of cAMP and cAMP-dependent protein kinase in beta- adrenoceptor-mediated interleukin-1 beta mRNA induction in cultured microglia. Neurosci. Res. 1995, 22:399-409.
50. Tynan R.J., Naicker S., Hinwood M., Nalivaiko E., Buller K.M., Pow D.V., Day T.A., Walker F.R. Chronic stress alters the density and morphology of microglia in a subset of stress-responsive brain regions. Brain Behav. Immun. 2010, 24:1058-1068.
51. Wang J., Li J., Sheng X., Zhao H., Cao X.D., Wang Y.Q., Wu G.C. Beta-adrenoceptor mediated surgery-induced production of pro-inflammatory cytokines in rat microglia cells. J. Neuroimmunol. 2010, 223:77-83.
52. 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.
53. Woo C.C., Wilson D.A., Sullivan R.M., Leon M. Early locus coeruleus lesions increase the density of beta-adrenergic receptors in the main olfactory bulb of rats. Int. J. Dev. Neurosci. 1996, 14:913-919.
54. Yirmiya R., Goshen I. Immune modulation of learning, memory, neural plasticity and neurogenesis. Brain Behav. Immun. 2011, 25:181-213.
55. 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.