Chronic intermittent hypoxia sensitizes acute hypothalamic-pituitary-adrenal stress reactivity and Fos induction in the rat locus coeruleus in response to subsequent immobilization stress

Neuroscience

Volumn 154, Issue 4, 2008, Pages 1639-1647

  Ma, S ^a   Mifflin, S W ^a   Cunningham, J T ^a   Morilak, D A ^a  

^a University of Texas Health Science Center   (United States)

Author keywords

adrenocorticotropic hormone; metabolic syndrome; norepinephrine; obstructive sleep apnea; paraventricular nucleus; stress

Indexed keywords

CORTICOTROPIN; PROTEIN FOS;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN REGION; COLD STRESS; CONTROLLED STUDY; HYPOPHYSIS ADRENAL SYSTEM; HYPOTHALAMUS; HYPOXEMIA; HYPOXIA; IMMOBILIZATION STRESS; LATERAL HYPOTHALAMUS; LOCUS CERULEUS; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SLEEP APNEA SYNDROME; STRIA TERMINALIS; THALAMUS MIDLINE NUCLEUS;

ADAPTATION, PHYSIOLOGICAL; ADRENOCORTICOTROPIC HORMONE; ANIMALS; ANOXIA; CHRONIC DISEASE; DISEASE MODELS, ANIMAL; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; IMMUNOHISTOCHEMISTRY; LOCUS COERULEUS; MALE; PITUITARY-ADRENAL SYSTEM; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, SPRAGUE-DAWLEY; RESTRAINT, PHYSICAL; SLEEP APNEA, OBSTRUCTIVE; STRESS, PSYCHOLOGICAL;

EID: 45849105537     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2008.04.068     Document Type: Article

References (75)

1. al-Damluji S. Adrenergic control of the secretion of anterior pituitary hormones. Baillieres Clin Endocrinol Metabol 7 (1993) 355-392
2. Berridge C.W., and Waterhouse B.D. The locus coeruleus-noradrenergic system: modulation of behavioral state and state-dependent cognitive processes. Brain Res Revs 42 (2003) 33-84
3. Bhatnagar S., and Dallman M. Neuroanatomical basis for facilitation of hypothalamic-pituitary-adrenal responses to a novel stressor after chronic stress. Neuroscience 84 (1998) 1025-1039
4. Bhatnagar S., Viau V., Chu A., Soriano L., Maijer O.C., and Dallman M.F. A cholecystokinin-mediated pathway to the paraventricular thalamus is recruited in chronically stressed rats and regulates hypothalamic-pituitary-adrenal function. J Neurosci 20 (2000) 5564-5573
5. Bratel T., Wennlund A., and Carlstrom K. Pituitary reactivity, androgens and catecholamines in obstructive sleep apnoea. Effects of continuous positive airway pressure treatment (CPAP). Resp Med 93 (1999) 1-7
6. Buckley T.M., and Schatzberg A.F. On the interactions of the hypothalamic-pituitary-adrenal (HPA) axis and sleep: Normal HPA axis activity and circadian rhythm, exemplary sleep disorders. J Clin Endocrinol Metab 90 (2005) 3106-3114
7. Canteras N.S., Simerly R.B., and Swanson L.W. Organization of projections from the medial nucleus of the amygdala: A PHAL study in the rat. J Comp Neurol 360 (1995) 213-245
8. Cecchi M., Khoshbouei H., Javors M., and Morilak D.A. Modulatory effects of norepinephrine in the lateral bed nucleus of the stria terminalis on behavioral and neuroendocrine responses to acute stress. Neuroscience 112 (2002) 13-21
9. Chrousos G.P. The role of stress and the hypothalamic-pituitary-adrenal axis in the pathogenesis of the metabolic syndrome: Neuro-endocrine and target tissue-related causes. Int J Obes 24 Suppl 2 (2000) S50-S55
10. Cossette S., Frasure-Smith N., and Lesperancé F. Clinical implications of a reduction in psychological distress on cardiac prognosis in patients participating in a psychosocial intervention program. Psychosom Med 63 (2001) 257-266
11. Coughlin S.R., and Calverley P. Sleep disordered breathing: a new component of syndrome X?. Obesity Rev 2 (2001) 267-274
12. Coughlin S.R., Mawdsley L., Mugarza J.A., Calverley P.M.A., and Wilding J.P.H. Obstructive sleep apnoea is independently associated with an increased prevalence of metabolic syndrome. Eur Heart J 25 (2004) 735-741
13. Cullinan W.E., Herman J.P., Helmreich D.L., and Watson S.J. A neuroanatomy of stress. In: Friedman M.J., et al. (Ed). Neurobiological and clinical consequences of stress: from normal adaptation to PTSD (1995), Lippincott-Raven Publishers, Philadelphia 135-147
14. Cunningham E.T., Bohn M.C., and Sawchenko P.E. Organization of adrenergic inputs to the paraventricular and supraoptic nuclei of the hypothalamus in the rat. J Comp Neurol 292 (1990) 651-667
15. Curtis K.S., Cunningham J.T., and Heesch C.M. Fos expression in brain stem nuclei of pregnant rats after hydralazine-induced hypotension. Am J Physiol 277 (1999) R532-R540
16. Dallman M.F., Akana S.F., Scribner K.A., Bradbury M.J., Walker C.D., Strack A.M., and Cascio C.S. Stress, feedback and facilitation in the hypothalamo-pituitary-adrenal axis. J Neuroendocrinol 4 (1992) 517-526
17. Dayas C.V., Buller K.M., and Day T.A. Medullary neurones regulate hypothalamic corticotropin-releasing factor cell responses to an emotional stressor. Neuroscience 105 (2001) 707-719
18. Dayas C.V., and Day T.A. Opposing roles for medial and central amygdala in the initiation of noradrenergic cell responses to a psychological stressor. Eur J Neurosci 15 (2002) 1712-1718
19. Dunn J.D. Plasma corticosterone responses to electrical stimulation of the bed nucleus of the stria terminalis. Brain Res 407 (1987) 327-331
20. Elam M., Yao T., Thoren P., and Svensson T.H. Hypercapnia and hypoxia: Chemoreceptor-mediated control of locus coeruleus neurons and splanchnic, sympathetic nerves. Brain Res 222 (1981) 373-381
21. Feldman S., Conforti N., Itzak A., and Weidenfeld J. Differential effect of amygdaloid lesions on CRF-41, ACTH and corticosterone responses following neural stimuli. Brain Res 658 (1994) 21-26
22. Finlay J.M., Zigmond M.J., and Abercrombie E.D. Increased dopamine and norepinephrine release in medial prefrontal cortex induced by acute and chronic stress: Effects of diazepam. Neuroscience 64 (1995) 619-628
23. Gibson A., Hart S.L., and Patel S. Effects of 6-hydroxydopamine-induced lesions of the paraventricular nucleus, and of prazosin, on the corticosterone response to restraint in rats. Neuropharmacology 25 (1986) 257-260
24. Gottlieb H.B., Ji L.L., Jones H., Penny M.L., Fleming T., and Cunningham J.T. Differential effects of water and saline intake on water deprivation-induced c-Fos staining in the rat. Am J Physiol 290 (2006) R1251-R1261
25. Greenberg H.E., Sica A., Batson D., and Scharf S.M. Chronic intermittent hypoxia increases sympathetic responsiveness to hypoxia and hypercapnia. J Appl Physiol 86 (1999) 298-305
26. Hauger R.L., Lorang M., Irwin M., and Aguilera G. CRF receptor regulation and sensitization of ACTH responses to acute ether stress during chronic intermittent immobilization stress. Brain Res 532 (1990) 34-40
27. Herman J.P., and Cullinan W.E. Neurocircuitry of stress: central control of the hypothalamo-pituitary-adrenocortical axis. Trends Neurosci 20 (1997) 78-84
28. Herman J.P., Figueiredo H., Mueller N.K., Ulrich-Lai Y., Ostrander M.M., Choi D.C., and Cullinan W.E. Central mechanisms of stress integration: Hierarchical circuitry controlling hypothalamo-pituitary-adrenocortical responsiveness. Front Neuroendocrinol 24 (2003) 151-180
29. Herman J.P., Ostrander M.M., Mueller N.K., and Figueiredo H. Limbic system mechanisms of stress regulation: Hypothalamo-pituitary-adrenocortical axis. Prog Neuropsychopharmacol Biol Psychiatry 29 (2005) 1201-1213
30. Hinojosa-Laborde C., and Mifflin S.W. Sex differences in blood pressure response to intermittent hypoxia in rats. Hypertension 46 (2005) 1016-1021
31. Hoffman G.E., Smith M.S., and Fitzsimmons M.D. Detecting steroidal effects on immediate early gene expression in the hypothalamus. Neuroprotocols 1 (1992) 55-66
32. Iiyori N., Alonso L.C., Li J., Sanders M.H., Garcia-Ocana A., O'Doherty R.M., Polotsky V.Y., and O'Donnell C.P. Intermittent hypoxia causes insulin resistance in lean mice independent of autonomic activity. Am J Respir Crit Care Med 175 (2007) 851-857
33. 2 in conscious rats. J Appl Physiol 66 (1989) 2245-2250
34. Jedema H.P., Finlay J.M., Sved A.F., and Grace A.A. Chronic cold exposure potentiates CRH-evoked increases in electrophysiologic activity of locus coeruleus neurons. Biol Psychiatry 49 (2001) 351-359
35. 1-adrenergic receptors in the secretion of hypothalamic corticotropin-releasing hormone during stress. Neuroendocrinology 56 (1992) 153-160
36. Lanfranco F., Gianotti L., Pivetti S., Navone F., Rossetto R., Tassone F., Gai V., Ghigo E., and Maccario M. Obese patients with obstructive sleep apnoea syndrome show a peculiar alteration of the corticotroph but not of the thyrotroph and lactotroph function. Clin Endocrinol 60 (2004) 41-48
37. Lesske J., Fletcher E.C., Bao G., and Unger T. Hypertension caused by chronic intermittent hypoxia: influence of chemoreceptors and sympathetic nervous system. J Hypertens 15 (1997) 1593-1603
38. Li J., Thorne L.N., Punjabi N.M., Sun C.K., Schwartz A.R., Smith P.L., Marino R.L., Rodriguez A., Hubbard W.C., O'Donnell C.P., and Polotsky V.Y. Intermittent hypoxia induces hyperlipidemia in lean mice. Circ Res 97 (2005) 698-706
39. Liposits Z., Sherman D., Phelix C., and Paull W.K. A combined light and electron microscopic immunocytochemical method for simultaneous localization of multiple tissue antigens: tyrosine hydroxylase immunoreactive innervation of corticotropin releasing factor synthesizing neurons in the paraventricular nucleus of the rat. Histochemistry 85 (1986) 95-106
40. Ma S., and Morilak D.A. Induction of Fos expression by acute immobilization stress is reduced in locus coeruleus and medial amygdala of Wistar-Kyoto rats compared to Sprague-Dawley rats. Neuroscience 124 (2004) 963-972
41. Ma S., and Morilak D.A. Chronic intermittent cold stress sensitizes the HPA response to a novel acute stress by enhancing noradrenergic influence in the rat paraventricular nucleus. J Neuroendocrinol 17 (2005) 761-769
42. Ma S., and Morilak D.A. Norepinephrine release in medial amygdala facilitates activation of the HPA axis in response to acute immobilisation stress. J Neuroendocrinol 17 (2005) 22-28
43. Mana M.J., and Grace A.A. Chronic cold stress alters the basal and evoked electrophysiological activity of rat locus coeruleus neurons. Neuroscience 81 (1997) 1055-1064
44. McDonald T.J., Le W.W., and Hoffman G.E. Brainstem catecholaminergic neurons activated by hypoxemia express GR and are coordinately activated with fetal sheep hypothalamic paraventricular neurons. Brain Res 885 (2000) 70-78
45. McEwen B.S. Allostasis and allostatic load: Implications for neuropsychopharmacology. Neuropsychopharmacology 22 (2000) 108-124
46. Melia K.R., Ryabinin A.E., Schroeder R., Bloom F.E., and Wilson M.C. Induction and habituation of immediate early gene expression in rat brain by acute and repeated restraint stress. J Neurosci 14 (1994) 5929-5938
47. Morilak D.A., Barrera G., Echevarria D.J., Garcia A.S., Hernandez A., Ma S., and Petre C.O. Role of brain norepinephrine in the behavioral response to stress. Prog Neuropsychopharmacol Biol Psychiatry 29 (2005) 1214-1224
48. Morilak D.A., Ma S., Fleming T., Ji L.L., Mifflin S.W., and Cunningham J.T. Chronic cold stress and chronic intermittent hypoxia sensitize acute stress-induced ACTH secretion and Fos staining in LC and forebrain of rats. Soc Neurosci Abstr 31 (2005) Online, Program no. 526.7
49. Morilak D.A., Fornal C.A., and Jacobs B.L. Effects of physiological manipulations on locus coeruleus neuronal activity in freely moving cats. II. Cardiovascular challenge. Brain Res 422 (1987) 24-31
50. Mueller N.K., Dolgas C.M., and Herman J.P. Stressor-selective role of the ventral subiculum in regulation of neuroendocrine stress responses. Endocrinology 145 (2004) 3763-3768
51. Nisenbaum L.K., Zigmond M.J., Sved A.J., and Abercrombie E.D. Prior exposure to chronic stress results in enhanced synthesis and release of hippocampal norepinephrine in response to a novel stressor. J Neurosci 11 (1991) 1478-1484
52. Ohayon M.M., Guilleminault C., Priest R.G., Zulley J., and Smirne S. Is sleep-disordered breathing an independent risk factor for hypertension in the general population (13,057 subjects)?. J Psychosom Res 48 (2000) 593-601
53. Pacak K., Armando I., Fukuhara K., Kvetnansky R., Palkovits M., Kopin I.J., and Goldstein D.S. Noradrenergic activation in the paraventricular nucleus during acute and chronic immobilization stress in rats. Brain Res 589 (1992) 91-96
54. Pankow W., Lies A., and Lohmann F.W. Sleep-disordered breathing and hypertension. N Engl J Med 343 (2000) 966-967
55. Pardon M.C., Ma S., and Morilak D.A. Chronic cold stress sensitizes brain noradrenergic reactivity and noradrenergic facilitation of the HPA stress response in Wistar Kyoto rats. Brain Res 971 (2003) 55-65
56. Paxinos G., and Watson C. The rat brain in stereotaxic coordinates. 4th edition (1998), Academic Press, San Diego
57. Plotsky P.M. Facilitation of immunoreactive corticotropin-releasing factor secretion into the hypophysial-portal circulation after activation of catecholaminergic pathways or central norepinephrine injection. Endocrinology 121 (1987) 924-930
58. Raff H. Endocrine adaptation to hypoxia. In: Fregly M.J., and Blatteis C.M. (Eds). Handbook of physiology, section 4: environmental physiology (1996), Oxford University Press, New York 1259-1275
59. Raff H., Sandri R.B., and Segerson T.P. Renin, ACTH, and adrenocortical function during hypoxia and hemorrhage in conscious rats. Am J Physiol 250 (1986) R240-R244
60. Randolph R.R., Li Q., Curtis K.S., Sullivan M.J., and Cunningham J.T. Fos expression following isotonic volume expansion of the unanesthetized male rat. Am J Physiol 274 (1998) R1345-R1352
61. Sawchenko P.E., and Swanson L.W. The organization of noradrenergic pathways from the brainstem to the paraventricular and supraoptic nuclei in the rat. Brain Res Rev 4 (1982) 275-325
62. Shamsuzzaman A.S.M., Gersh B.J., and Somers V.K. Obstructive sleep apnea: Implications for cardiac and vascular disease. JAMA 290 (2003) 1906-1914
63. Sica A.L., Greenberg H.E., Scharf S.M., and Ruggiero D.A. Chronic-intermittent hypoxia induces immediate early gene expression in the midline thalamus and epithalamus. Brain Res 883 (2000) 224-228
64. Smith D.W., Buller K.M., and Day T.A. Role of ventrolateral medulla catecholamine cells in hypothalamic neuroendocrine cell responses to systemic hypoxia. J Neurosci 15 (1995) 7979-7988
65. Smith R.P., Veale D., Pépin J.L., and Lévy P.A. Obstructive sleep apnoea and the autonomic nervous system. Sleep Med Rev 2 (1998) 69-92
66. Stam R., Bruijnzeel A.W., and Wiegant V.M. Long-lasting stress sensitisation. Eur J Pharmacol 405 (2000) 217-224
67. Sullivan C.E., and Issa F.G. Obstructive sleep apnea. Clin Chest Med 6 (1985) 633-650
68. Svensson T.H. Peripheral, autonomic regulation of locus coeruleus noradrenergic neurons in brain: Putative implications for psychiatry and psychopharmacology. Psychopharmacology 92 (1987) 1-7
69. Szafarczyk A., Malaval F., Laurent A., Gibaud R., and Assenmacher I. Further evidence for a central stimulatory action of catecholamines on adrenocorticotropin release in the rat. Endocrinology 121 (1987) 883-892
70. Valentino R.J., Page M.E., and Curtis A.L. Activation of noradrenergic locus coeruleus neurons by hemodynamic stress is due to local release of corticotropin-releasing factor. Brain Res 555 (1991) 25-34
71. Vgontzas A.N., Bixler E.O., and Chrousos G.P. Metabolic disturbances in obesity versus sleep apnoea: The importance of visceral obesity and insulin resistance. J Intern Med 254 (2003) 32-44
72. Walker B. Glucocorticoids and cardiovascular disease. Eur J Endocrinol 157 (2007) 545-559
73. Wang M. The role of glucocorticoid action in the pathophysiology of the metabolic syndrome. Nutr Metab (Lond). (2005) doi:10.1186/1743-7075-2-3 (open access)
74. Witchel S.F., and DeFranco D.B. Mechanisms of disease: regulation of glucocorticoid and receptor levels: impact on metabolic syndrome. Nat Clin Pract 2 (2006) 621-631
75. Woodward D.J., Moises H.C., Waterhouse B.D., Yeh H.H., and Cheun J.E. Modulatory actions of norepinephrine on neural circuits. Adv Exp Med Biol 287 (1991) 193-208