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. 1979 Dec;64(6):1599–1607. doi: 10.1172/JCI109621

Effect of Central Catecholamine Depletion on the Osmotic and Nonosmotic Stimulation of Vasopressin (Antidiuretic Hormone) in the Rat

Thomas R Miller 1,2, William A Handelman 1,2, Patricia E Arnold 1,2, Keith M McDonald 1,2, Perry B Molinoff 1,2, Robert W Schrier 1,2
PMCID: PMC371313  PMID: 500827

Abstract

The central nervous system (CNS) mechanism(s) for the release of antidiuretic hormone (ADH) by various stimuli is unknown. In this study, the role of CNS catecholamines in effecting ADH release was examined in conscious rats 10-14 d after the cerebroventricular injection of 6-hydroxydopamine (6-OHDA). This dose of 6-OHDA caused a 67% depletion of brain tissue norepinephrine and only 3% depletion of heart norepinephrine, as compared with controls, which were injected with the vehicle buffer alone. Either intravenous 3% saline (osmotic stimulus) or intraperitoneal hyperoncotic dextran (nonosmotic stimulus) was administered to water-diuresing rats through indwelling catheters. Neither of these maneuvers changed arterial pressure, pulse, or inulin clearance in control or 6-OHDA rats. The 3% saline caused similar increases in plasma osmolality (15 mosmol/kg H2O) in control and 6-OHDA rats. The control rats, however, increased urinary osmolality (Uosm) to 586 mosmol/kg H2O, whereas 6-OHDA rats increased Uosm only to 335 mosmol/kg H2O (P < 0.005). These changes in Uosm were accompanied by an increase in plasma ADH to 7.6 μIU/ml in control animals vs. 2.9 μIU/ml in 6-OHDA rats (P < 0.005). All waterdiuresing animals had undetectable plasma ADH levels. Dextran-induced hypovolemia caused similar decrements (− 10%) in blood volume in both control and 6-OHDA animals, neither of which had significant changes in plasma osmolality. This nonosmotic hypovolemic stimulus caused an increase in Uosm to 753 mosmol/kg H2O in control rats, whereas Uosm in 6-OHDA rats increased to only 358 mosmol/kg H2O (P < 0.001). At the same time, ADH levels also were significantly greater in Cont rats (2.4 μIU/ml) than in the 6-OHDA animals (0.69 μIU/ml; P < 0.05). These results therefore suggest that CNS catecholamines may play an important role in mediating ADH release in response to both osmotic and nonosmotic (hypovolemic) stimuli.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Anderson R. J., Cadnapaphornchai P., Harbottle J. A., McDonald K. M., Schrier R. W. Mechanism of effect of thoracic inferior vena cava constriction on renal water excretion. J Clin Invest. 1974 Dec;54(6):1473–1479. doi: 10.1172/JCI107895. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Anderson R. J., Pluss R. G., Berns A. S., Jackson J. T., Arnold P. E., Schrier R. W., McDonald K. E. Mechanism of effect of hypoxia on renal water excretion. J Clin Invest. 1978 Oct;62(4):769–777. doi: 10.1172/JCI109188. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Arnold E. B., Molinoff P. B., Rutledge C. O. The release of endogenous norepinephrine and dopamine from cerebral cortex by amphetamine. J Pharmacol Exp Ther. 1977 Sep;202(3):544–557. [PubMed] [Google Scholar]
  4. Barker J. L., Crayton J. W., Nicoll R. A. Noradrenaline and acetylcholine responses of supraoptic neurosecretory cells. J Physiol. 1971 Oct;218(1):19–32. doi: 10.1113/jphysiol.1971.sp009602. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Beck N. P., Reed S. W., Murdaugh H. V., Davis B. B. Effects of catecholamines and their interaction with other hormones on cyclic 3',5'-adenosine monophosphate of the kidney. J Clin Invest. 1972 Apr;51(4):939–944. doi: 10.1172/JCI106888. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Berl T., Cadnapaphornchai P., Harbottle J. A., Schrier R. W. Mechanism of stimulation of vasopressin release during beta adrenergic stimulation with isoproterenol. J Clin Invest. 1974 Mar;53(3):857–867. doi: 10.1172/JCI107626. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Berl T., Cadnapaphornchai P., Harbottle J. A., Schrier R. W. Mechanism of suppression of vasopressin during alpha-adrenergic stimulation with norepinephrine. J Clin Invest. 1974 Jan;53(1):219–227. doi: 10.1172/JCI107541. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Berl T., Harbottle J. A., Schrier R. W. Effect of alpha- and beta-adrenergic stimulation on renal water excretion in man. Kidney Int. 1974 Oct;6(4):247–253. doi: 10.1038/ki.1974.106. [DOI] [PubMed] [Google Scholar]
  9. Boykin J., Cadnapaphornchai P., McDonald K. M., Schrier R. W. Mechanism of diuretic response associated with atrial tachycardia. Am J Physiol. 1975 Dec;229(6):1486–1491. doi: 10.1152/ajplegacy.1975.229.6.1486. [DOI] [PubMed] [Google Scholar]
  10. Bridges T. E., Thorn N. A. The effect of autonomic blocking agents on vasopressin release in vivo induced by osmoreceptor stimulation. J Endocrinol. 1970 Oct;48(2):265–276. doi: 10.1677/joe.0.0480265. [DOI] [PubMed] [Google Scholar]
  11. Cadnapaphornchai P., Boykin J. L., Berl T., McDonald K. M., Schrier R. W. Mechanism of effect of nicotine on renal water excretion. Am J Physiol. 1974 Nov;227(5):1216–1220. doi: 10.1152/ajplegacy.1974.227.5.1216. [DOI] [PubMed] [Google Scholar]
  12. Dunn F. L., Brennan T. J., Nelson A. E., Robertson G. L. The role of blood osmolality and volume in regulating vasopressin secretion in the rat. J Clin Invest. 1973 Dec;52(12):3212–3219. doi: 10.1172/JCI107521. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Fisher D. A. Norepinephrine inhibition of vasopressin antidiuresis. J Clin Invest. 1968 Mar;47(3):540–547. doi: 10.1172/JCI105750. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Halter J. B., Goldberg A. P., Robertson G. L., Porte D., Jr Selective osmoreceptor dysfunction in the syndrome of chronic hypernatremia. J Clin Endocrinol Metab. 1977 Apr;44(4):609–616. doi: 10.1210/jcem-44-4-609. [DOI] [PubMed] [Google Scholar]
  15. Handler J. S., Bensinger R., Orloff J. Effect of adrenergic agents on toad bladder response to ADH, 3',5'-AMP, and theophylline. Am J Physiol. 1968 Nov;215(5):1024–1031. doi: 10.1152/ajplegacy.1968.215.5.1024. [DOI] [PubMed] [Google Scholar]
  16. Henry D. P., Starman B. J., Johnson D. G., Williams R. H. A sensitive radioenzymatic assay for norepinephrine in tissues and plasma. Life Sci. 1975 Feb 1;16(3):375–384. doi: 10.1016/0024-3205(75)90258-1. [DOI] [PubMed] [Google Scholar]
  17. Hoffman W. E., Phillips M. I., Schmid P. The role of catecholamines in central antidiuretic and pressor mechanisms. Neuropharmacology. 1977 Sep;16(9):563–569. doi: 10.1016/0028-3908(77)90025-9. [DOI] [PubMed] [Google Scholar]
  18. Kostrzewa R. M., Jacobowitz D. M. Pharmacological actions of 6-hydroxydopamine. Pharmacol Rev. 1974 Sep;26(3):199–288. [PubMed] [Google Scholar]
  19. Kühn E. R. Cholinergic and adrenergic release mechanism for vasopressin in the male rat: a study with injections of neurotransmitters and blocking agents into the third ventricle. Neuroendocrinology. 1974;16(5-6):255–264. doi: 10.1159/000122572. [DOI] [PubMed] [Google Scholar]
  20. Lum G. M., Aisenbrey G. A., Dunn M. J., Berl T., Schrier R. W., McDonald K. M. In vivo effect of indomethacin to potentiate the renal medullary cyclic AMP response to vasopressin. J Clin Invest. 1977 Jan;59(1):8–13. doi: 10.1172/JCI108624. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. McDonald K. M., Kuruvila K. C., Aisenbrey G. A., Schrier R. W. Effect of alpha and beta adrenergic stimulation on renal water excretion and medullary tissue cyclic AMP in intact and diabetes insipidus rats. Kidney Int. 1977 Aug;12(2):96–103. doi: 10.1038/ki.1977.86. [DOI] [PubMed] [Google Scholar]
  22. Milton A. S., Paterson A. T. A microinjection study of the control of antidiuretic hormone release by the supraoptic nucleus of the hypothalamus in the cat. J Physiol. 1974 Sep;241(3):607–628. doi: 10.1113/jphysiol.1974.sp010674. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Moss R. L., Dyball R. E., Cross B. A. Responses of antidromically identified supraoptic and paraventricular units to acetylcholine, noradrenaline and glutamate applied iontophoretically. Brain Res. 1971 Dec 24;35(2):573–575. doi: 10.1016/0006-8993(71)90504-x. [DOI] [PubMed] [Google Scholar]
  24. Noble E. P., Wurtman R. J., Axelrod J. A simple and rapid method for injecting H3-norepinephrine into the lateral ventricle of the rat brain. Life Sci. 1967 Feb 1;6(3):281–291. doi: 10.1016/0024-3205(67)90157-9. [DOI] [PubMed] [Google Scholar]
  25. Schmitt H., Fénard S. Action of -adrenergic blocking drugs on the sympathetic centres and their interactions with the central sympatho-inhibitory effect of clonidine. Arzneimittelforschung. 1973 Jan;23(1):40–45. [PubMed] [Google Scholar]
  26. Schrier R. W., Berl T. Mechanism of effect of alpha adrenergic stimulation with norepinephrine on renal water excretion. J Clin Invest. 1973 Feb;52(2):502–511. doi: 10.1172/JCI107207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Schrier R. W., Berl T. Mechanism of the antidiuretic effect associated with interruption of parasympathetic pathways. J Clin Invest. 1972 Oct;51(10):2613–2620. doi: 10.1172/JCI107079. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Schrier R. W., Berl T. Nonosmolar factors affecting renal water excretion (first of two parts). N Engl J Med. 1975 Jan 9;292(2):81–88. doi: 10.1056/NEJM197501092920207. [DOI] [PubMed] [Google Scholar]
  29. Schrier R. W., Lieberman R., Ufferman R. C. Mechanism of antidiuretic effect of beta adrenergic stimulation. J Clin Invest. 1972 Jan;51(1):97–111. doi: 10.1172/JCI106803. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Urano A., Kobayashi H. Effects of noradrenaline and dopamine injected into the supraoptic nucleus on urine flow rate in hydrated rats. Exp Neurol. 1978 May 15;60(1):140–150. doi: 10.1016/0014-4886(78)90173-5. [DOI] [PubMed] [Google Scholar]
  31. Uretsky N. J., Iversen L. L. Effects of 6-hydroxydopamine on catecholamine containing neurones in the rat brain. J Neurochem. 1970 Feb;17(2):269–278. doi: 10.1111/j.1471-4159.1970.tb02210.x. [DOI] [PubMed] [Google Scholar]
  32. Vandeputte-Van Messom G., Peeters G. Effects of intraventricular administration of cholinergic drugs on water diuresis in goats. Arch Int Pharmacodyn Ther. 1974 Sep;211(1):80–98. [PubMed] [Google Scholar]
  33. de Torrente A., Robertson G. L., McDonald K. M., Schrier R. W. Mechanism of diuretic response to increased left atrial pressure in the anesthetized dog. Kidney Int. 1975 Dec;8(6):355–361. doi: 10.1038/ki.1975.127. [DOI] [PubMed] [Google Scholar]

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