Beta-adrenergic and Opioidergic Modulation of Cortisol Secretion in Response to Acute Stress

Abstract

The modulatory action of beta-adrenergic and opioidergic pathways on the cortisol response to acute stressors was investigated using gonadectomized male miniature pigs. Three types of stressors, nose-snare (NS, for 2 min. each on four occasions at 30 min. intervals); high intensity cracker blasts (CB, two blasts at 3 min intervals) and ACTH (1 i.u./kg BW, i.v.) were utilized 80 min after start of blood sampling. For assessment of cortisol blood samples were withdrawn every 20 min for 200 min. In addition, animals received i.v. injections of either isoproterenol (5 μg/ kg) or propranolol (0.5 mg/kg) or naloxone (1 mg/kg) 15 or 30 min before the application of stressor. Stress of repeated NS application as well as ACTH treatment, resulted in immediate secretion of cortisol (p<0.001). Blast of crackers resulted in a transient increase in cortisol (p<0.05). Isoproterenol stimulated the basal cortisol secretion for about 20 min in unstressed pigs (p <0.01) but propranolol had no effects. Isoproterenol also reinforced (p<0.05) the effect of CB, but had no effect on the cortisol response to nose-snare. In contrast, response to NS was reduced (p=0.02) by propranolol. Neither isoproterenol nor propranolol altered the cortisol response to ACTH application. Pretreatment with naloxone significantly increased the cortisol response to NS (p<0.01) and to CB (p<0.01), but had no effects on ACTH-induced cortisol release. In conclusion, the beta-adrenergic involvement is evident in the cortisol response to acute stress of nose-snare. Furthermore, the results indicate that activation of endogenous opioid system during stress mitigates adrenal response.

Cortisol - adrenergic control - physical stress - noise stress - opioids - ACTH

References

• 1 Akil H, Watson SJ, Young E, Lewis ME, Khachturian H, Walker JM. Endogenous opioids: biology and function.  Annu Rev Neurosci. 1984;  7 223-255
• 2 Armstrong 3rd DW, Hatfield BD. Hormonal responses to opioid receptor blockade: during rest and exercise in cold and hot environments.  Eur J Appl Physiol. 2006;  9 1-9
• 3 Axelrod J, Reisine TD. Stress hormones: Their interaction and regulation.  Science. 1984;  224 452-459
• 4 Berkenbosch F, Vermes I, Binnekode R, Tilders FJH. Beta adrenergic stimulation induces an increase of the plasma levels of immunoreactive alpha-MSH, Beta-endorphin, ACTH and corticosterone.  Life Sci. 1981;  29 2249-2256
• 5 Brearley JC, Dobson H, Jones RS. Investigation into the effect of two sedatives on the stress response in cattle.  J Vet Pharmacol Therap. 1990;  13 367-377
• 6 Chong RY, Oswald L, Yang X, Uhart M, Lin PI, Wand GS. The Micro-opioid receptor polymorphism A118G predicts cortisol responses to naloxone and stress.  Neuropsychopharmacology. 2006;  204-211
• 7 Dalin AM, Magnusson U, Haggendal J, Nyberg I. The effect of thiopentone sodium anaesthesia and surgery, relocation, grouping and hydrocortisone treatment on the blood levels of cortisol, corticosteroid binding globulin and catecholamines in pigs.  J Anim Sci. 1993;  71 1902-1909
• 8 Der-Avakian A, Will MJ, Bland ST, Deak T, Nguyen KT, Schmid MJ, Spencer RL, Watkins LR, Maier SF. Surgical and pharmacological suppression of glucocorticoids prevents the enhancement of morphine conditioned place preference by uncontrollable stress in rats.  Psychopharmacology. 2005;  179 409-417
• 9 Ellendorff F, Parvizi N, Elsaesser F, Smidt D. The miniature pig as an animal model in endocrine and neuroendocrine studies of reproduction.  Lab Anim Sci. 1977;  27 822-830
• 10 Estienne MJ, Kesner JS, Barb CR, Kraeling RR, Rampacek GB. On the site of action of naloxone-stimulated cortisol secretion in gilts.  Life Sci. 1988;  43 161-166
• 11 Geer EB, Landman RE, Wardlaw SL, Conwell IM, Freda PU. Stimulation of the hypothalamic-pituitary-adrenal Axis with the opioid antagonist nalmefene.  Pituitary Epub. 2005;  8 115-122
• 12 Herman JP, Figueiredo H, Mueller NK, Ulrich-Lai Y, Ostrander MM, Choi DC, Cullinan WE. Central mechanisms of stress integration: hierarchical circuitry controlling hypothalamo-pituitary-adreocortical responsiveness.  Front Neuroendocrinol. 2003;  24 151-180
• 13 Hoffman BB, Lefkowith RJ. Catecholamines, sympathomimetic drugs, and adrenergic receptor antagonists. In: Goodmand & Gilman's The Pharmacological basis of therapeutics. Hardman, JC and Limbird LE (eds) Mc Graw-Hill, New York 2001: 199-248
• 14 Janssens CJJG, Helmond FA, Loyens LWS, Schouten WGP, Wiegant VM. Chronic stress increases the opioid -mediated inhibition of the pituitary-adrenocortical response to acute stress in pigs.  Endocrinology. 1995;  136 1468-1473
• 15 Jezova D, Kvetnansky R, Kovacs K, Oprsalova Z, Vigas M, Makara GB. Insulin-induced hypoglycemia activates the release of adrenocorticotropin predominantly via central and propranolol insensitive mechanisms.  Endocrinology. 1987;  120 409-415
• 16 Jezova D, Vigas M, Klimes I, Jurcovicova J. Adenopituitary hormone response to exercise combined with propranolol infusion in man.  Endocrinol Exp. 1983;  17 91-98
• 17 Kemppainnen RJ, Peterson ME. Regulation of alpha-melanocyte-stimulating hormone secretion from the pars intermedia of domestic cats.  Am J Vet Res. 1999;  60 245-249
• 18 Koopmans SJ, Ruis M, Dekker R, van Diepen H, Korte M, Mroz Z. Surplus dietary tryptophan reduces plasma cortisol and noradrenaline concentrations and enhances recovery after social stress in pigs.  Physiol Behav. 2005;  85 469-478
• 19 Kvetnansky R, Mikulaj L. Adrenal and urinary catecholamines in rats during adaptation to repeated immobilization stress.  Endocrinology. 1970;  87 738-743
• 20 Kvetnansky R, Sun CL, Lake CR, Thoa N, Torda T, Kopin IJ. Effect of handling and forced immobilization on rat plasma levels of epinephrine, nor-epinephrine and dopamine-beta-hydroxylase.  Endocrinology. 1978;  103 1868-1874
• 21 Lucas A, Holtmann G, Gerken G, Pietsch A, Braun-Lang U, Gilani K, Strassburger K, Gesing S, Janssen OE, Kavelaars A, Heijnen CJ, Schedlowski M, Elsenbruch S. Visceral pain and public speaking stress: neuroendocrine and immune cell responses in healthy subjects.  Brain Behav Immun. 2006;  20 49-56
• 22 Makara GB, Kvetnansky R, Jezova D, Jindra A, Kakucska I, Oprsalova Z. Plasma catecholamines do not participate in pituitary-adrenal activation by immobilization stress in rats with transection of nerve fibers to the median eminence.  Endocrinology. 1986;  119 1757-1762
• 23 Marc M, Ellendorff F, Kallweit E, Parvizi N, Elsaesser F. Plasma cortisol and ACTH concentrations in the warmblood horse in response to a standardized treadmill exercise test as physiological markers for evaluation of training status.  J Anim Sci. 2000;  78 1936-1946
• 24 Maunder EMW, Pillay AV, Care AD. Endocrine control of plasma concentrations of calcium-binding protein in the pig.  J Endocrinol. 1987;  115 121-128
• 25 Oberbeck R, Schurmeyer T, Jacobs R, Benschop RJ, Sommer B, Schmidt RE, Schedlowski M. Effect of beta adrenoceptor-blockade on stressed-induced adrenocorticotrophin release in humans.  Euro J app Physiol Occ Physiol. 1998;  77 523-526
• 26 Parrott RF, Thornton SN. Opioid influences on pituitary function in sheep under basal condition and during psychological stress.  Psychoneuroendocrinology. 1989;  14 451-459
• 27 Petrovic SL, McDonald JK, Snyder GD, McCann SM. Testosterone control the brain and anterior pituitary beta-adrenergic receptors.  Life Sci. 1984;  34 2399-2406
• 28 Rosochacki SJ, Piekarzewska AB, Poloszynowicz J, Sakowski T. The influence of restraint immobilization stress on the concentration of bioamines and cortisol in plasma of Pietrain and Duroc pigs.  J Vet Med A physiol Pathol Clin Med. 2000;  47 231-242
• 29 Rushen J, Boissy A, Terlouw EM, de Passille AM. Opioid peptides and behavioral and physiological responses of dairy cows to social isolation in unfamiliar surroundings.  J Anim Sci. 1999;  77 2918-2924
• 30 Rushen J, Ladewig J. Stress-induced hypoalgesia and opioid inhibition of pigs’ responses to restraint.  Physiol Behav. 1991;  50 1093-1096
• 31 Rushen J, Nay TS, Wright LR, Payne DC, Foxcroft GR. Stress and nursing in pigs: Role of HPA axis and endogenous opioid peptides.  Physiol Behav. 1995;  58 43-48
• 32 Rushen J, Schwarze N, Ladewig J, Foxcroft G. Opioid modulation of the effects of repeated stress on ACTH, cortisol, prolactin and growth hormone in pigs.  Physiol Behav. 1993;  53 923-928
• 33 Sanhouri AA, Jones RS, Dobson H. Prazosin and propranolol and the stress response to transport in male goats; a preliminary study.  J Vet Pharmacol Therap. 1991;  14 421-425
• 34 SAS. Statistical Analysis System, version 6.12. Cary, NC .Statistical analysis Systems Institute 1990
• 35 Thun R, Schwarz-Porsche D. Nebennierenrinde. In: Veterinärmedizinische Endokrinologie. Döcke F (ed.) Fischer, Berlin 1994: 309-353
• 36 Tidlers FJH, Berkenbosch F, Smelik PG. Adrenergic mechanism involved in the control of pituitary-adrenal activity in the rat: A beta-adrenergic stimulatory mechanism.  Endocrinology. 1982;  110 114-120
• 37 Turner AI, Rivalland ET, Clarke IJ, Lambert GW, Morris MJ, Tilbrook AJ. Noradrenaline, but not neuropeptide Y, is elevated in cerebrospinal fluid from the third cerebral ventricle following audiovisual stress in gonadectomized rams and ewes.  Neuroendocrinology. 2002;  76 373-380
• 38 Uhart M, Chong RY, Oswald L, Lin PI, Wand GS. Gender differences in hypothalamic-pituitary-Adrenal (HPA) axis reactivity.  Psychoneuroendocrinology. 2006;  31 642-652
• 39 Weiss GM, Topel DG, Siers DG, Ewan RC. Influence of adrenergic blockade upon some endocrine and metabolic parameters in a stress-susceptible and a fat strain of swine.  J Anim Sci. 1974;  38 591-597
• 40 Yoshida-Hiroi M, Tsuchida Y, Yoshino G, Hiroi N. Intranasal administration of ACTH (1-24) stimulates catecholamine secretion.  Horm Metab Res. 2005;  37 489-493

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