Time Course of Vasopressin and Oxytocin Secretion after Stress in Adrenalectomized Rats

Abstract

To characterize the participation of vasopressin (AVP) and oxytocin (OT) in hypothalamus-pituitary-adrenal regulation after adrenalectomy (ADX), we evaluated corticosterone, ACTH, AVP and OT plasma concentrations and AVP and OT content of the paraventricular nucleus (PVN) at different periods (3 h, 1, 3, 7 and 14 days) in sham or ADX rats under basal conditions and after immobilization stress. ADX animals showed undetectable corticosterone levels, while sham animals showed a marked increase in corticosterone and ACTH 3 h after surgery, then lowering to basal control levels. ADX rats showed high basal ACTH levels with a triphasic response without changes after immobilization. After three hours, the ADX group showed higher OT levels than the sham group. OT was increased after immobilization stress in sham and ADX groups. AVP plasma levels did not change throughout the basal or stress studies in either group. There was a decrease in hypothalamic AVP content 1 and 3 days after ADX under basal and stress conditions. Plasma osmolality showed a significant decrease in the ADX group at 3, 7, and 14 days. In conclusion, there are different pituitary-adrenal axis set points after removal of the glucocorticoid negative feedback. The role of vasopressinergic and oxytocinergic neurons in the ACTH secretion after ADX or immobilization stress appears to differ. Magnocellular AVP is unlikely to contribute to ACTH secretion in response to ADX or immobilization stress. On the other hand, OT is elicited by immobilization stress and might contribute to the ACTH secretion during short-term ADX.

Key words

Hypothalamo-pituitary-adrenal axis · Immobilization stress · Oxytocinergic neurons · Vasopressinergic neurons · Paraventricular nucleus

References

• 1 Antoni F W. Hypothalamic control of adrenocorticotropin secretion: advances since the discovery of 41 residue corticotropin-releasing factor.  Endocr Rev. 1986;  7 351-378
• 2 Vale W W, Rivier C, Brown M R, Spiess J, Koob G, Swanson L, Bilezikjian L, Bloom F, Rivier J. Chemical and biological characterization of corticotropin releasing factor.  . 1983;  39 245-270
• 3 Orth D N. Corticotropin-releasing hormone in humans.  Endocr Rev. 1992;  13 164-191
• 4 Mozid A M, Tringali G, Forsling M L, Hendricks M S, Ajodha S, Edwards R, Navarra P, Grossman A B, Korbonits M. Ghrelin is released from rat hypothalamic explants and stimulates corticotrophin-releasing hormone and arginine-vasopressin.  Horm Metab Res.. 2003;  35 455-459
• 5 Vale W W, Smith M A, Yamamoto G, Rivier J, Rivier C. Effects of synthetic ovine corticotropin releasing factor, glucocorticoids, catecholamines, neurohypophysial peptides and other substances on cultured corticotropic cells.  Endocrinology. 1983;  113 1121-1131
• 6 Kasting N W. Simultaneous and independent release of vasopressin and oxytocin in the rat.  Can J Physiol Pharmacol. 1988;  66 22-26
• 7 Jezova D, Skultetyova I, Tokarev D I, Bakos P, Vigas M. Vasopressin and oxytocin in stress.  Ann N Y Acad Sci. 1995;  771 192-205
• 8 Lolait S J, O’Carroll A M, Brownstein M J. Molecular biology of vasopressin receptors.  Ann N Y Acad Sci. 1995;  771 273-292
• 9 Elias L L, Dorival Campos A, Moreira A C. The opposite effects of short- and long-term salt loading on pituitary adrenal axis activity in rats.  Horm Metab Res. 2002;  34 207-211
• 10 Soloff M S, Alexandrova M, Fernstron M J. Oxytocin receptors: triggers for parturition and lactation?.  Science. 1979;  204 1313-1315
• 11 Cunninghan E T, Sawchenko P E. Reflex control of magnocellular vasopressin and oxytocin secretion.  Trends in Neurosci. 1991;  14 406-411
• 12 De Wied D, Diamant M, Fodor M. Central nervous system effects of the neurohypophyseal hormones and related peptides.  Front Neuroendocrinol. 1993;  14 251-302
• 13 Aguilera G, Rabadan-Diehl C. Regulation on vasopressin V1b receptors in the anterior pituitary gland of the rat.  Exp Physiol. 2000;  85 19S-26S
• 14 Mouri T, Itoi K, Takahashi K, Suda T, Murakami O, Yoshinaga K, Andoh N, Ohtani H, Masuda T, Sasano N. Colocalization of corticotropin-releasing factor and vasopressin in the paraventricular nucleus of the human hypothalamus.  Neuroendocrinology. 1993;  57 34-39
• 15 Bugajski J, Gadek-Michalska A. Effect of cyclooxygenase inhibitors on the vasopressin induced ACTH and corticosterone response during crowding stress.  J Physiol Pharmacol. 2003;  54 247-256
• 16 Bartanasz V, Aubury J M, Jezova D, Baffi J, Kiss J Z. Up-regulation of vasopressin mRNA in paraventricular hypophysiotropic neurons after acute immobilization stress.  Neuroendocrinology. 1993;  58 625-629
• 17 Aguilera G, Pham Q, Rabadan-Diehl C. Regulation of pituitary vasopressin receptors during chronic stress: Relationship to corticotroph responsiveness.  J Neuroendocrinol. 1994;  6 229-304
• 18 Castro M, Figueiredo F, Moreira A C. Time-course of hypothalamic CRH and pituitary ACTH contents, and pituitary responsiveness to CRH stimulation after bilateral adrenalectomy.  Horm Metab Res. 1995;  27 10-15
• 19 Haanwinckel M A, Elias L K, Favaretto A LV, Gutkowska J, McCann S M, Antunes-Rodrigues J. Oxytocin mediates atrial natriuretic peptide release and natriuresis after volume expansion in the rat.  PNAS. 1995;  92 7902-7906
• 20 Elias L K, Antunes-Rodrigues J, Elias P CL, Moreira A C. Effect of plasma osmolality on pituitary-adrenal responses to corticotropin-releasing hormone and atrial natriuretic peptides changes in central diabetes insipidus.  J Clin Endocrinol Metab. 1997;  82 1243-1247
• 21 Dallman M F, Jones M T, Vernikos-Danellis J, Ganong W F. Corticosteroid control of ACTH secretion.  Endrocrinology. 1972;  91 961-968
• 22 Suda T, Tomori N, Tozawa F, Mouri T, Demura H, Shizume K. Effects of bilateral adrenalectomy on immunoreactive corticotropin-releasing factor in the rat median eminence and intermediate-posterior pituitary.  Endocrinology. 1983;  113 1182-1184
• 23 Spinedi E, Giacomini M, Jacquier M C, Gaillard R C. Changes in hypothalamus-corticotrope axis after bilateral adrenalectomy: evidence for a median eminence site of glucocorticoid action.  Neuroendocrinology. 1991;  53 160-170
• 24 Castro M, Moreira A C. Regulation of corticotropin-releasing hormone secretion by ACTH at different times after adrenalectomy.  Braz J Med Biol Res. 1996;  29 1573-1578
• 25 Auteliano D J, Blum M, Roberts J L. Changes in rat pituitary nuclear and cytoplasmic pro-opiomelanocortin RNAs associated with adrenalectomy and glucocorticoid replacement.  Mol Cell Endocrinol. 1989;  66 171-180
• 26 Stillman M A, Recht L D, Rosario S L, Seif S M, Robinson A G, Zimmerman E A. The effects of adrenalectomy and glucocorticoid replacement on vasopressin and vasopressin-neurophysin in the zona externa of the median eminence of the rat.  Endocrinology. 1977;  101 42-49
• 27 Kiss J Z, Mezey E, Skirboll L. Corticotropin-releasing factor immunoreactive neurons of the paraventricular nucleus become vasopressin positive after adrenalectomy.  PNAS. 1984;  81 1854-1858
• 28 Withnall M H, Key S, Garner , H . Vasopressin-containing and vasopressin deficient subpopulations of corticotropin releasing factor axons are differentially affected by adrenalectomy.  Endocrinology. 1987;  120 2180-2182
• 29 Holmes M C, Antoni A, Catt K J, Aguilera G. Predominant release of vasopressin vs. corticotropin releasing factor from the isolated median eminence after adrenalectomy.  Neuroendocrinology. 1986;  43 245-251
• 30 Husain M K, Manger W M, Rock T H, Weiss R J, Frantz A G. Vasopressin release due to manual restraint in the rat: role of body compression and comparison with other stressful stimuli.  Endocrinology. 1979;  104 641-644
• 31 Gibbs D M. Dissociation of oxytocin, vasopressin and corticotropin secretion during different types of stress.  Life Science. 1984;  35 487-491
• 32 Lang R E, Heil J WE, Ganten D, Hermann K, Unger T, Rascher W. Oxytocin unlike vasopressin is a stress hormone in the rat.  Neuroendocrinology. 1983;  37 314-316
• 33 Herman J P, Adams D, Prewitt C. Regulatory changes in neuroendocrine stress-integrative circuitry produced by a variable stress paradigm.  Neuroendocrinology. 1995;  61 180-190
• 34 Ma X M, Lightman S L. The arginine vasopressin and corticotrophin-releasing hormone gene transcription responses to varied frequencies of repeated stress in rats.  J Physiol. 1998;  510 605-614
• 35 Aubry J M, Bartanusz V, Jezova D, Belin D, Kiss J Z. Single stress induces long-lasting elevations in vasopressin mRNA levels in CRF hypophysiotrophic neurones, but repeated stress is required to modify AVP immunoreactivity.  J Neuroendocrinol. 1999;  11 377-384
• 36 Dohanics J, Hoffmann G E, Verballis J G. Hyponatremia-induced inhibition of magnocellular neurons causes stressor-selective impairment of stimulated adrenocorticotropin secretion in rats.  Endocrinology. 1991;  128 331-340