Chronic intermittent cold stress sensitises the hypothalamic-pituitary-adrenal response to a novel acute stress by enhancing noradrenergic influence in the rat paraventricular nucleus

Journal of Neuroendocrinology

Volumn 17, Issue 11, 2005, Pages 761-769

  Ma, S ^a   Morilak, David A ^a  

^a Mays Cancer Center at UT Health San Antonio   (United States)

Author keywords

1 adregenic receptors; ACTH; Chronic intermittent stress; HPA axis; Norepinephrine; Paraventricular nucleus

Indexed keywords

ALPHA 1 ADRENERGIC RECEPTOR; BENOXATHIAN; CORTICOTROPIN; NORADRENALIN; PHENYLEPHRINE; POSTSYNAPTIC RECEPTOR;

ADAPTATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; COLD EXPOSURE; COLD STRESS; CONCENTRATION RESPONSE; CONTROLLED STUDY; CORTICOTROPIN BLOOD LEVEL; FOREBRAIN; HORMONE RELEASE; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IMMOBILIZATION; MALE; MICRODIALYSIS; NONHUMAN; NORADRENERGIC SYSTEM; PATHOPHYSIOLOGY; PLASTICITY; PRIORITY JOURNAL; RAT; THALAMUS MIDLINE NUCLEUS;

ADRENERGIC ALPHA-AGONISTS; ADRENERGIC ALPHA-ANTAGONISTS; ANIMALS; CHRONIC DISEASE; COLD; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; IMMOBILIZATION; MALE; MICROINJECTIONS; NOREPINEPHRINE; OXATHIINS; PARAVENTRICULAR HYPOTHALAMIC NUCLEUS; PHENYLEPHRINE; PITUITARY-ADRENAL SYSTEM; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, ADRENERGIC, ALPHA-1; STRESS; STRESS, PSYCHOLOGICAL;

EID: 27644493000     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/j.1365-2826.2005.01372.x     Document Type: Article

References (68)

1. Cossette S, Frasure-Smith N, Lesperancé F. Clinical implications of a reduction in psychological distress on cardiac prognosis in patients participating in a psychosocial intervention program. Psychosom Med 2001; 63: 257-266.
2. Sklar LS, Anisman H. Social stress influences tumor growth. Psychosom Med 1980; 42: 347-365.
3. Anisman H, Zacharko RM. Multiple neurochemical and behavioral consequences of stressors: implications for depression. Pharmacol Ther 1990; 46: 119-136.
4. Kendler KS, Karkowski LM, Prescott CA. Causal relationship between stressful life events and the onset of major depression. Am J Psychiatry 1999; 156: 837-841.
5. Kessler RC. The effects of stressful life events on depression. Ann Rev Psychol 1997; 48: 191-214.
6. McEwen BS. Allostasis and allostatic load: implications for neuropsychopharmacology. Neuropsychopharmacology 2000; 22: 108-124.
7. Herman JP, Cullinan WE. Neurocircuitry of stress: central control of the hypothalamo-pituitary-adrenocortical axis. Trends Neurosci 1997; 20: 78-84.
8. Aston-Jones G, Chiang C, Alexinsky T. Discharge of noradrenergic locus coeruleus neurons in behaving rats and monkeys suggests a role in vigilance. Prog Brain Res 1991; 88: 501-520.
9. Berridge CW, Waterhouse BD. The locus coeruleus-noradrenergic system. modulation of behavioral state and state-dependent cognitive processes. Brain Res Revs 2003; 42: 33-84.
10. Morilak DA. Norepinephrine and stress. In: Ordway G, Schwartz M, Frazer A, eds. Norepinephrine: Neurobiology and Therapeutics. Cambridge, UK: Cambridge Press, 2005.
11. Cecchi M, Khoshbouei H, Javors M, Morilak DA. Modulatory effects of norepinephrine in the lateral bed nucleus of the stria terminalis on behavioral and neuroendocrine responses to acute stress. Neuroscience 2002; 112: 13-21.
12. Ma S, Morilak DA. Norepinephrine release in medial amygdala facilitates activation of the HPA axis in response to acute immobilisation stress. J Neuroendocrinol 2005; 17: 22-28.
13. Gibson A, Hart SL, Patel S. Effects of 6-hydroxydopamine-induced lesions of the paraventricular nucleus, and of prazosin, on the corticosterone response to restraint in rats. Neuropharmacology 1986; 25: 257-260.
14. Feldman S, Conforti N, Melamed E. Norepinephrine depletion in the paraventricular nucleus inhibits the adrenocortical responses to neural stimuli. Neurosci Lett 1986; 64: 191-195.
15. al-Damluji S. Adrenergic control of the secretion of anterior pituitary hormones. Bailliere's Clin Endocrinol Metabol 1993; 7: 355-392.
16. Plotsky PM. Facilitation of immunoreactive corticotropin-releasing factor secretion into the hypophysial-portal circulation after activation of catecholaminergic pathways or central norepinephrine injection. Endocrinology 1987; 121: 924-930.
17. Gaillet S, Lachuer J, Malaval F, Assenmacher I, Szafarczyk A. The involvement of noradrenergic ascending pathways in the stress-induced activation of ACTH and corticosterone secretions is dependent on the nature of stressors. Exp Brain Res 1991; 87: 173-180.
18. Cole RL, Sawchenko PE. Neurotransmitter regulation of cellular activation and neuropeptide gene expression in the paraventricular nucleus of the hypothalamus. J Neurosci 2002; 22: 959-969.
19. Liposits Z, Sherman D, Phelix C, Paull WK. 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 1986; 85: 95-106.
20. Sawchenko PE, Swanson LW. The organization of noradrenergic pathways from the brainstem to the paraventricular and supraoptic nuclei in the rat. Brain Res Rev 1982; 4: 275-325.
21. Cummings S, Seybold V. Relationship of alpha-1 and alpha-2-adrenergic-binding sites to regions of the paraventricular nucleus of the hypothalamus containing corticotropin-releasing factor and vasopressin neurons. Neuroendocrinology 1988; 47: 523-532.
22. 125I]-HEAT. J Comp Neurol 1985; 231: 190-208.
23. 1d-adrenergic receptor mRNA in the rat brain and spinal cord. J Chem Neuroanat 1997; 13: 115-139.
24. 1b adrenoceptor mRNA in corticotropin-releasing hormone-containing cells of the rat hypothalamus and its regulation by corticosterone. J Neurosci 1999; 19: 10098-10106.
25. 1D adrenergic receptor mRNA in oxytocin- and corticotropin-releasing hormone-synthesizing neurons in the rat paraventricular nucleus. Neuroscience 1999; 91: 639-649.
26. 1B adrenoceptors in rat paraventricular nucleus overlap with, but do not mediate, the induction of c-Fos expression by osmotic or restraint stress. Neuroscience 1997; 76: 901-913.
27. Hauger RL, Lorang M, Irwin M, Aguilera G. CRF receptor regulation and sensitization of ACTH responses to acute ether stress during chronic intermittent immobilization stress. Brain Res 1990; 532: 34-40.
28. Dallman MF, Akana SF, Scribner KA, Bradbury MJ, Walker C-D, Strack AM, Cascio CS. Stress, feedback and facilitation in the hypothalamo-pituitary-adrenal axis. J Neuroendocrinol 1992; 4: 517-526.
29. Kiss A, Aguilera G. Regulation of the hypothalamic pituitary axis during chronic stress: responses to repeated intraperitoneal hypertonic saline injection. Brain Res 1993; 630: 262-270.
30. Aguilera G. Regulation of pituitary ACTH secretion during chronic stress. Front Neuroendocrinol 1994; 15: 321-350.
31. Pardon M-C, Ma S, Morilak DA. Chronic cold stress sensitizes brain noradrenergic reactivity and noradrenergic facilitation of the HPA stress response in Wistar Kyoto rats. Brain Res 2003; 971: 55-65.
32. Gold PW, Chrousos GP. The endocrinology of melancholic and atypical depression: relation to neurocircuitry and somatic consequences. Proc Assoc Am Physicians 1999; 111: 22-34.
33. Johnson EO, Kamilaris TC, Chrousos GP, Gold PW. Mechanisms of stress: a dynamic overview of hormonal and behavioral homeostasis. Neurosci Biobeh Rev 1992; 16: 115-130.
34. Sullivan GM, Coplan JD, Kent JM, Gorman JM. The noradrenergic system in pathological anxiety. A focus on panic with relevance to generalized anxiety and phobias. Biol Psychiatry 1999; 46: 1205-1218.
35. Ma S, Fleming T, Ji LL, Mifflin SW, Cunningham JT, Morilak DA. Chronic cold stress and chronic intermittent hypoxia sensitize acute stress-induced ACTH secretion and Fos staining in LC and forebrain of rats. Soc Neurosci Abstract 2005; 31: 526.7.
36. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates, 4th edn. San Diego, CA: Academic Press, 1998.
37. 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.
38. Gaillet S, Alonso G, Le Borgne R, Barbanel G, Malaval M, Assenmacher I, Szafarczyk A. Effects of discrete lesions in the ventral noradrenergic ascending bundle on the corticotropic stress response depend on the site of the lesion and on the plasma levels of adrenal steroids. Neuroendocrinology 1993; 58: 408-419.
39. Szafarczyk A, Alonso G, Ixart G, Malaval F, Assenmacher I. Diurnal-stimulated and stress-induced ACTH release in rats is mediated by ventral noradrenergic bundle. Am J Physiol 1985; 249: E219-E226.
40. 1-adrenergic receptors in the secretion of hypothalamic corticotropin-releasing hormone during stress. Neuroendocrinol 1992; 56: 153-160.
41. Alonso G, Szafarczyk A, Balmefrezol M, Assenmacher I. Immunocytochemical evidence for stimulatory control by the ventral noradrenergic bundle of parvocellular neurons of the paraventricular nucleus secreting corticotropin releasing hormone and vasopressin in rats. Brain Res 1986; 397: 297-307.
42. Sawchenko PE, Li H-Y, Ericsson A. Circuits and mechanisms governing hypothalamic responses to stress: a tale of two paradigms. Prog Brain Res 2000; 122: 61-78.
43. Ziegler DR, Cass WA, Herman JP. Excitatory influence of the locus coeruleus in hypothalamic-pituitary-adrenocortical axis responses to stress. J Neuroendocrinol 1999; 11: 361-369.
44. Itoi K, Suda T, Tozawa F, Dobashi I, Ohmori N, Sakai Y, Abe K, Demura H. Microinjection of norepinephrine into the paraventricular nucleus of the hypothalamus stimulates corticotropin-releasing factor gene expression in conscious rats. Endocrinology 1994; 135: 2177-2182.
45. Itoi K, Helmreich DL, Lopez-Figueroa MO, Watson SJ. Differential regulation of corticotropin-releasing hormone and vasopressin gene transcription in the hypothalamus by norepinephrine. J Neurosci 1999; 19: 5464-5472.
46. Li H-Y, Ericsson A, Sawchenko PE. Distinct mechanisms underlie activation of hypothalamic neurosecretory neurons and their medullary catecholaminergic afferents in categorically different stress paradigms. Proc Natl Acad Sci, USA 1996; 93: 2359-2364.
47. Dayas CV, Buller KM, Day TA. Medullary neurones regulate hypothalamic corticotropin-releasing factor cell responses to an emotional stressor. Neuroscience 2001; 105: 707-719.
48. Chuluyan HE, Saphier D, Rohn WM, Dunn AJ. Noradrenergic innervation of the hypothalamus participates in adrenocortical responses to interleukin-1. Neuroendocrinology 1992; 56: 106-111.
49. Mana MJ, Grace AA. Chronic cold stress alters the basal and evoked electrophysiological activity of rat locus coeruleus neurons. Neuroscience 1997; 81: 1055-1064.
50. Jedema HP, Sved AF, Zigmond MJ, Finlay JM. Sensitization of norepinephrine release in medial prefrontal cortex: effect of different chronic stress protocols. Brain Res 1999; 830: 211-217.
51. Jedema HP, Finlay JM, Sved AF, Grace AA. Chronic cold exposure potentiates CRH-evoked increases in electrophysiologic activity of locus coeruleus neurons. Biol Psychiatry 2001; 49: 351-359.
52. Jedema HP, Grace AA. Chronic exposure to cold stress alters electrophysiological properties of locus coeruleus neurons recorded in vitro. Neuropsychopharmacology 2003; 28: 63-72.
53. Pardon M-C, Gould GG, Garcia A, Phillips L, Cook MC, Miller SA, Mason PA, Morilak DA. Stress reactivity of the brain noradrenergic system in three rat strains differing in their neuroendocrine and behavioral responses to stress: implications for susceptibility to stress-related neuropsychiatric disorders. Neuroscience 2002; 115: 229-242.
54. Gresch PJ, Sved AF, Zigmond MJ, Finlay JM. Stress-induced sensitization of dopamine and norepinephrine efflux in medial prefrontal cortex of the rat. J Neurochem 1994; 63: 575-583.
55. Finlay JM, Jedema HP, Rabinovic AD, Mana MJ, Zigmond MJ, Sved AF. Impact of corticotropin-releasing hormone on extracellular norepinphrine in prefrontal cortex after chronic cold stress. J Neurochem 1997; 69: 144-150.
56. Young WS, Kuhar MJ. Noradrenergic α1 and α2 receptors: light microscopic autoradiographic localization. Proc Natl Acad Sci USA 1980; 77: 1696-1700.
57. 1A adrenergic receptor mRNA in rat brain visualized by in situ hybridization. J Comp Neurol 1997; 386: 358-378.
58. Ossowska G, Nowa G, Kata R, Klenk-Majewska B, Danilczuk Z, Zebrowska-Lupina I. Brain monoamine receptors in a chronic unpredictable stress model in rats. J Neural Transm 2001; 108: 311-319.
59. 1-adrenergic receptors. J Physiol Pharmacol 2002; 53: 105-116.
60. Klimek V, Zak-Knapik J, Maj J. Antidepressants given repeatedly increase the alpha 1-adrenoceptor agonist affinity in the rat brain. Pol J Pharmacol Physiol 1991; 43: 347-352.
61. 2-adrenergic receptors in cloned MDCK cells. Am J Physiol 1985; 249: C69-C77.
62. 1-adrenergic and other hypertrophic stimuli in cardiac myocytes in culture and in vivo. J Biol Chem 1996; 271: 5839-5843.
63. 1-adrenergic receptor subtype mRNAs. J Mol Cell Cardiol 1998; 30: 1515-1523.
64. 1-adrenoceptor subtypes. Naunyn-Schmiedeberg's Arch Pharmacol 1999; 359: 439-446.
65. 1-adrenoceptor subtypes. Mol Pharmacol 2002; 61: 1008-1016.
66. Charney DS, Woods SW, Krystal JH, Nagy LM, Heninger GR. Noradrenergic neuronal dysregulation in panic disorder: the effects of intravenous yohimbine and clonidine in panic disorder patients. Acta Psychiatr Scand 1992; 86: 273-282.
67. Southwick SM, Krystal JH, Morgan CA, Johnson D, Nagy LM, Nicolaou A, Heninger GR, Charney DS. Abnormal noradrenergic function in posttraumatic stress disorder. Arch Gen Psychiatry 1993; 50: 266-274.
68. Yehuda R, Giller EL, Levengood RA, Southwick SM, Siever LJ. Hypothalamic-pituitary-adrenal functioning in post-traumatic stress disorder: expanding the concept of the stress response spectrum. In: Friedman MJ, Charney DS, Deutch AY, eds. Neurobiological and Clinical Consequences of Stress: From Normal Adaptation to PTSD. Philadelphia, PA: Lippincott-Raven Publishers, 1995: 351-365.