The inflamed axis: The interaction between stress, hormones, and the expression of inflammatory-related genes within key structures comprising the hypothalamic-pituitary-adrenal axis

Physiology and Behavior

Volumn 124, Issue , 2014, Pages 77-91

  Hueston, Cara M ^a   Deak, Terrence ^a  

^a BINGHAMTON UNIVERSITY   (United States)

Author keywords

ACTH; Corticosterone; CRH; Interleukin 1; Neuroinflammation; Stress

Indexed keywords

BETA ACTIN; CORTICOSTERONE; CORTICOTROPIN; CYCLOOXYGENASE 2; DEXAMETHASONE; INTERLEUKIN 1; INTERLEUKIN 1 RECEPTOR TYPE II; INTERLEUKIN 1BETA; INTERLEUKIN 6; PROTEIN C FOS; STRESS HORMONE; TUMOR NECROSIS FACTOR ALPHA; AUTACOID; CORTICOTROPIN RELEASING FACTOR;

ADRENAL GLAND; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; FOOTSHOCK; GENE EXPRESSION; HYPOPHYSIS; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; MALE; NERVOUS SYSTEM INFLAMMATION; NEUROIMMUNOLOGY; NONHUMAN; PRIORITY JOURNAL; RAT; STRESS; ANIMAL; BIOSYNTHESIS; BLOOD; DRUG EFFECTS; ELECTROSTIMULATION; GENE EXPRESSION REGULATION; HYPOPHYSIS ADRENAL SYSTEM; HYPOTHALAMIC PARAVENTRICULAR NUCLEUS; HYPOTHALAMUS HYPOPHYSIS SYSTEM; METABOLISM; PHYSIOLOGICAL STRESS;

ADRENAL GLANDS; ADRENOCORTICOTROPIC HORMONE; ANIMALS; CORTICOSTERONE; CORTICOTROPIN-RELEASING HORMONE; CYCLOOXYGENASE 2; DEXAMETHASONE; ELECTRIC STIMULATION; GENE EXPRESSION REGULATION; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; INFLAMMATION MEDIATORS; INTERLEUKIN-1; INTERLEUKIN-6; MALE; PARAVENTRICULAR HYPOTHALAMIC NUCLEUS; PITUITARY-ADRENAL SYSTEM; RATS; RECEPTORS, INTERLEUKIN-1 TYPE II; STRESS, PHYSIOLOGICAL;

EID: 84888025750     PISSN: 00319384     EISSN: 1873507X     Source Type: Journal    
DOI: 10.1016/j.physbeh.2013.10.035     Document Type: Article

References (60)

1. Black P.H., Garbutt L.D. Stress, inflammation and cardiovascular disease. J Psychosom Res 2002, 52(1):1-23.
2. Lee J., Tran T., Tansey M. Neuroinflammation in Parkinson's disease. J Neuroimmune Pharmacol 2009, 4:419-429.
3. Vezzani A., Maroso M., Balosso S., Sanchez M.-A., Bartfai T. IL-1 receptor/Toll-like receptor signaling in infection, inflammation, stress and neurodegeneration couples hyperexcitability and seizures. Brain Behav Immun 2011, 25(7):1281-1289.
4. Hotamisligil G. Endoplasmic reticulum stress and the inflammatory basis of metabolic disease. Cell 2010, 140:900-917.
5. Laflamme N., Rivest S. Effects of systemic immunogenic insults and circulating proinflammatory cytokines on the transcription of the inhibitory factor kappaB alpha within specific cellular populations of the rat brain. J Neurochem 1999, 73(1):309-321.
6. Deak T., Bellamy C., Bordner K.A. Protracted increases in core body temperature and interleukin-1 following acute administration of lipopolysaccharide: implications for the stress response. Physiol Behav 2005, 85(3):296-307.
7. Nguyen K.T., Deak T., Owens S.M., Kohno T., Fleshner M., Watkins L.R., et al. Exposure to acute stress induces brain interleukin-1b protein in the rat. J Neurosci 1998, 18(6):2239-2246.
8. Nguyen K.T., Deak T., Will M.J., Hansen M.K., Hunsaker B.N., Fleshner M., et al. Timecourse and corticosterone sensitivity of the brain, pituitary, and serum interleukin-1beta protein response to acute stress. Brain Res 2000, 859(2):193-201.
9. Blandino P., Barnum C.J., Deak T. The involvement of norepinephrine and microglia in hypothalamic and splenic IL-1B responses to stress. J Neuroimmunol 2006, 173:87-95.
10. Barnum C.J., Blandino P., Deak T. Social status modulates basal IL-1 concentrations in the hypothalamus of pair-housed rats and influences certain features of stress reactivity. Brain Behav Immun 2008, 22:517-527.
11. 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.
12. Hueston C.M., Barnum C.J., Eberle J.A., Ferraioli F.J., Buck H.M., Deak T. Stress-dependent changes in neuroinflammatory markers observed after common laboratory stressors are not seen following acute social defeat of the Sprague-Dawley rat. Physiol Behav 2011, 104:187-198.
13. Engstrom L., Rosen K., Angel A., Fyrberg A., Mackerlova L., Konsman J.P., et al. Systemic immune challenge activates an intrinsically regulated local inflammatory circuit in the adrenal gland. Endocrinology 2008, 149(4):1436-1450.
14. O'Connor K.A., Johnson J.D., Hansen M.K., Wieseler Frank J.L., Maksimova E., Watkins L.R., et al. Peripheral and central proinflammatory cytokine response to a severe acute stressor. Brain Res 2003, 991:123-132.
15. Grinevich V., Ma X.M., Herman J.P., Jezova D., Akmayev I., Aguilera G. Effect of repeated lipopolysaccharide administration on tissue cytokine expression and hypothalamic-pituitary-adrenal axis activity in rats. J Neuroendocrinol 2001, 13(8):711-723.
16. 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.
17. Reyes T.M., Walker J.R., DeCino C., Hogenesch J.B., Sawchenko P.E. Categorically distinct acute stressors elicit dissimilar transcriptional profiles in the paraventricular nucleus of the hypothalamus. J Neurosci 2003, 23(13):5607-5616.
18. Audet M.-C., Mangano E.N., Anisman H. Behavior and pro-inflammatory cytokine variations among submissive and dominant mice engaged in aggressive encounters: moderation by corticosterone reactivity. Front Behav Neurosci 2010, 4.
19. Powell N.D., Bailey M.T., Mays J.W., Stiner-Jones L.M., Hanke M.L., Padgett D.A., et al. Repeated social defeat activates dendritic cells and enhances Toll-like receptor dependent cytokine secretion. Brain Behav Immun 2009, 23(2):225-231.
20. Johnson J.D., Campisi J., Sharkey C., Kennedy S.L., Nickerson M., Greenwood B., et al. Catecholamines mediate stress-induced increases in peripheral and central inflammatory cytokines. Neuroscience 2005, 135:1295-1307.
21. Blandino P., Hueston C.M., Barnum C.J., Bishop C., Deak T. The impact of ventral noradrenergic bundle lesions on increased IL-1 in the PVN and hormonal responses to stress in male Sprague Dawley rats. Endocrinology 2013, 154(7):2489-2500.
22. Garcia-Bueno B., Madrigal J.L., Perez-Nievas B.G., Leza J.C. Stress mediators regulate brain prostaglandin synthesis and peroxisome proliferator-activated receptor-y activation after stress in rats. Endocrinology 2008, 149(4):1969-1978.
23. Sorrells S., Sapolsky R. An inflammatory review of glucocorticoid actions in the CNS. Brain Behav Immun 2007, 21:259-272.
24. Frank M., Baratta M., Sprunger D., Watkins L., Maier S. Microglia serve as a neuroimmune substrate for stress-induced potentiation of CNS pro-inflammatory cytokine responses. Brain Behav Immun 2006, 21:47-59.
25. Smith E.M. Neuropeptides as signal molecules in common with leukocytes and the hypothalamic-pituitary-adrenal axis. Brain Behav Immun 2008, 22(1):3-14.
26. Wallon C., Soderholm J.D. Corticotropin-releasing hormone and mast cells in the regulation of mucosal barrier function in the human colon. Ann N Y Acad Sci 2009, 1165:206-210.
27. Bluthe R.-M., Crestani F., Kelley K.W., Dantzer R. Mechanisms of the behavioral effects of interleukin-1: role of prostaglandins and CRF. Ann N Y Acad Sci 1992, 650:268-275.
28. Mohn C.E., Fernandez-Solari J., De Laurentiis A., Prestifilippo J.P., de la Cal C., Funk R., et al. The rapid release of corticosterone from the adrenal induced by ACTH is mediated by nitric oxide acting by prostaglandin E2. Proc Natl Acad Sci U S A 2005, 102(17):6213-6218.
29. Watson G., Paxinos C. The Rat Brain in Steriotaxic Coordinates 2005, ElsevierAcademic Press, Burlington, MA.
30. Richardon H., Lee S., O'Dell L., Koob G., Rivier C. Alcohol self-administration acutely stimulates the hypothalamic-pituitary-adrenal axis, but alcohol dependence leads to a dampened neuroendocrine state. Eur J Neurosci 2008, 28:1641-1653.
31. Cole M., Kim P., Kalman B., Spencer R. Dexamethasone suppression of corticosteroid secretion: evaluation of the site of action by receptor measures and functional studies. Psychoneuroendocrinology 2000, 25:151-167.
32. Cole M.A., Kim P.J., Kalman B.A., Spencer R.L. Dexamethasone suppression of corticosteroid secretion: evaluation of the site of action by receptor measures and functional studies. Psychoneuroendocrinology 2000, 25(2):151-167.
33. O'Connor K., Johnson J., Hammack S., Brooks L., Spencer R., Watkins L., et al. Inescapable shock induces resistance to the effects of dexamethasone. Psychoneuroendocrinology 2003, 28:481-500.
34. 1b receptor reduces ACTH, but not corticosterone secretion induced by stress without affecting basal hypothalamic-pituitary-adrenal axis activity. J Endocrinol 2009, 200:273-283.
35. Zelena D., Domokos A., Jain S.K., Jankord R., Filaretova L. The stimuli-specific role of vasopressin in the hypothalamus-pituitary-adrenal axis response to stress. J Endocrinol 2009, 202:263-278.
36. Engeland W.C., Arnhold M.M. Neural circuitry in the regulation of adrenal corticosterone rhythmicity. Endocrine 2005, 28(3):325-332.
37. De Herdt V., Puimege L., De Waele J., Raedt R., Wyckhuys T., El Tahry R., et al. Increased rat serum corticosterone suggest immunomodulation by stimulation of the vagal nerve. J Neuroimmunol 2009, 212:102-105.
38. Bornstein S.R., Engeland W.C., Ehrhart-Bornstein M., Herman J.P. Dissociation of ACTH and glucocorticoids. Trends Endocrinol Metab 2008, 19(5):175-180.
39. Deak T. Immune cells and cytokine circuits: toward a working model for understanding direct immune-to-adrenal communication pathways. Endocrinology 2008, 149(4):1433-1435.
40. Arakawa H., Arakawa K., Blandino P., Deak T. The role of neuroinflammation in the release of aversive odor cues from footshock-stressed rats: implications for the neural mechanism of alarm pheromone. Psychoneuroendocrinology 2011, 36(4):557-568.
41. Audet M.-C., Jacobson-Pick S., Wann B.P., Anisman H. Social defeat promotes specific cytokine variations within the prefrontal cortex upon subsequent aggressive or endotoxin challenges. Brain Behav Immun 2011, 25(6):1197-1205.
42. Barnum C.J., Pace T.W., Hu F., Neigh G.N., Tansey M.G. Psychological stress in adolescent and adult mice increases neuroinflammation and attenuates the response to LPS challenge. J Neuroinflammation 2012, 9(1):9.
43. Deak T., Bellamy C., D'Agostino L.G. Exposure to forced swim stress does not alter central production of IL-1. Brain Res 2003, 972(1-2):53-63.
44. Deak T., Bordner K.A., McElderry N.K., Barnum C.J., Blandino P., Deak M.M., et al. Stress-induced increases in hypothalamic IL-1: a systematic analysis of multiple stressor paradigms. Brain Res Bull 2005, 64(6):541-556.
45. Gibb J., Hayley S., Poulter M.O., Anisman H. Effects of stressors and immune activating agents on peripheral and central cytokines in mouse strains that differ in stressor responsivity. Brain Behav Immun 2011, 25:468-482.
46. Hennessy M.B., Deak T., Schiml-Webb P.A., Wilson S.E., Greenlee T.M., McCall E. Responses of guinea pig pups during isolation in a novel environment may represent stress-induced sickness behaviors. Physiol Behav 2004, 81(1):5-13.
47. Jankord R., Zhang R., Flak J.N., Solomon M.B., Albertz J., Herman J.P. Stress activation of IL-6 neurons in the hypothalamus. Am J Physiol Regul Integr Comp Physiol 2010, 299(1):R343-R351.
48. Johnson J.D., O'Connor K., Watkins L.R., Maier S.F. The role of IL-1B in stress-induced sensitization of proinflammatory cytokine and corticosterone responses. Neuroscience 2004, 127:569-577.
49. Knapp D.J., Whitman B.A., Wills T.A., Angel R.A., Overstreet D.H., Criswell H.E., et al. Cytokine involvement in stress may depend on corticotrophin releasing factor to sensitize ethanol withdrawal anxiety. Brain Behav Immun 2011, 25(Supplement 1(0)):S146-S154.
50. Kwon M.-S., Seo Y.-J., Lee J.-K., Lee H.-K., Jung J.-S., Jang J.-E., et al. The repeated immobilization stress increases IL-1B immunoreactivities in only neuron, but not astrocyte or microglia in hippocampal CA1 region, striatum and paraventricular nucleus. Neurosci Lett 2008, 430:258-263.
51. Lin M.-T., Kao T., Jin Y., Chen C. Interleukin-1 receptor antagonist attenuates the heat stroke-induced neuronal damage by reducing the cerebral ischemia in rats. Brain Res Bull 1995, 37(6):595-598.
52. Michel V., Peinnequin A., Alonso A., Buguet A., Cespuglio R., Canini F. Effect of glucocorticoid depletion on heat-induced Hsp70, IL-1B and TNFa gene expression. Brain Res 2007, 1164:63-71.
53. Minami M., Kuraishi Y., Yamaguchi T., Nakai S., Hirai Y., Satoh M. Immobilization stress induces interleukin-1 beta mRNA in the rat hypothalamus. Neurosci Lett 1991, 123(2):254-256.
54. Plata-Salaman C.R., Ilyin S.E., Turrin N.P., Gayle D., Flynn M.C., Bedard T., et al. Neither acute nor chronic exposure to a naturalistic (predator) stressor influences the interleukin-1B system, tumor necrosis factor-a, transforming growth factor-B1, and neuropeptide mRNAs in specific brain regions. Brain Res Bull 2000, 51(2):187-193.
55. Pugh C.R., Nguyen K.T., Gonyea J.L., Fleshner M., Watkins L.R., Maier S.F., et al. Role of interleukin-1 beta in impairment of contextual fear conditioning caused by social isolation. Behav Brain Res 1999, 106:109-118.
56. Shintani F., Nakaki T., Kanba S., Kato R., Masahiro A. Role of interleukin-1 in stress responses: a putative neurotransmitter. Mol Neurobiol 1995, 10(1):47-71.
57. Sugama S., Fujita M., Hashimoto M., Conti B. Stress induced morphological microglial activation in the rodent brain: involvement of interleukin-18. Neuroscience 2007, 146:1388-1399.
58. Suzuki E., Shintani F., Kanba S., Asai M., Nakaki T. Immobilization stress increases mRNA levels of interleukin-1 receptor antagonist in various rat brain regions. Cell Mol Neurobiol 1997, 17(5):557-562.
59. Voorhees J.L., Tarr A.J., Wohleb E.S., Godbout J.P., Mo X., Sheridan J.F., et al. Prolonged restraint stress increases IL-6, reduces IL-10, and causes persistent depressive-like behavior that is reversed by recombinant IL-10. PLoS One 2013, 8(3):e58488.
60. Yabuuchi K., Minami M., Katsumata S., Yamazaki A., Satoh M. An in situ hybridization study on interleukin-1B mRNA induced by transient forebrain ischemia in the rat brain. Mol Brain Res 1994, 26:135-142.