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. 1984 Apr;349:167–182. doi: 10.1113/jphysiol.1984.sp015150

Circulatory and osmoregulatory effects of angiotensin II perfusion of the third ventricle in a bird with salt glands.

R Gerstberger, D A Gray, E Simon
PMCID: PMC1199331  PMID: 6737289

Abstract

In Pekin ducks adapted to salt water, 1Asp - 5Val -angiotensin II, 1Asp - 5Ile -angiotensin II and 1Asp - 5Ile -tetradecapeptide were applied intracerebroventricularly (I.C.V.) during steady-state conditions evoked by continuous intravenous loading with 200 mosmol kg-1 saline. Each of the angiotensin II (AII) analogues caused a dose-dependent antidiuresis with a concomitant rise in urine osmolality and electrolyte concentration. Antidiuresis was linearly correlated with plasma arginine vasotocin (AVT). The elevation of plasma AVT occurred rapidly during I.C.V. stimulation with AII and declined exponentially to the pre-stimulation level. Under conditions of salt loading with 1000 mosmol kg-1 saline in which the ducks excreted the salt and water by their supraorbital salt glands, AII applied I.C.V. in a concentration of 1 nmol ml-1, inhibited the NaCl excretion via the salt glands. Arterial blood pressure and heart rate increased after I.C.V. microperfusion with 1 nmol ml-1 AII. This was not due to leakage of I.C.V. AII into the circulation because systemic application of AII required a 100-fold higher dose to elicit similar effects. Respiration rate remained constant. Systemically applied AVT which produced plasma levels similar to, or greater than, those caused by centrally acting AII resulted in the same antidiuretic responses but did not mimic the circulatory effects of I.C.V. AII. Specific AVT antiserum, injected intravenously, totally suppressed the renal response to I.C.V. AII and reduced the rise in blood pressure and heart rate by more than 50%. The anterior part of the third ventricle was more sensitive than the posterior part in eliciting the antidiuretic responses to I.C.V. applied AII. The particular combination of effects on renal excretion, salt gland secretion and cardiovascular function of centrally applied AII in the duck supports the idea that AII plays a major role as a central modulator of volume homeostasis.

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Selected References

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  1. Andersson B., Eriksson L. Conjoint action of sodium and angiotensin on brain mechanisms controlling water and salt balances. Acta Physiol Scand. 1971 Jan;81(1):18–29. doi: 10.1111/j.1748-1716.1971.tb04873.x. [DOI] [PubMed] [Google Scholar]
  2. Andersson B. Regulation of water intake. Physiol Rev. 1978 Jul;58(3):582–582. doi: 10.1152/physrev.1978.58.3.582. [DOI] [PubMed] [Google Scholar]
  3. Bealer S. L., Phillips M. I., Johnson A. K., Schmid P. G. Anteroventral third ventricle lesions reduce antidiuretic responses to angiotensin II. Am J Physiol. 1979 Jun;236(6):E610–E615. doi: 10.1152/ajpendo.1979.236.6.E610. [DOI] [PubMed] [Google Scholar]
  4. Bennett J. P., Jr, Snyder S. H. Angiotensin II binding to mammalian brain membranes. J Biol Chem. 1976 Dec 10;251(23):7423–7430. [PubMed] [Google Scholar]
  5. Bryant R. W., Epstein A. N., Fitzsimons J. T., Fluharty S. J. Arousal of a specific and persistent sodium appetite in the rat with continuous intracerebroventricular infusion of angiotensin II. J Physiol. 1980 Apr;301:365–382. doi: 10.1113/jphysiol.1980.sp013211. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Buggy J., Fisher A. E. Anteroventral third ventricle site of action for angiotensin induced thirst. Pharmacol Biochem Behav. 1976 Jun;4(6):651–660. doi: 10.1016/0091-3057(76)90216-1. [DOI] [PubMed] [Google Scholar]
  7. Deutsch H., Simon E. Intracerebroventricular osmosensitivity in the Pekin Duck. Properties and functions in salt and water balance. Pflugers Arch. 1980 Aug;387(1):1–7. doi: 10.1007/BF00580837. [DOI] [PubMed] [Google Scholar]
  8. Evered M. D., Fitzsimons J. T. Drinking and changes in blood pressure in response to angiotensin II in the pigeon Columba livia. J Physiol. 1981 Jan;310:337–352. doi: 10.1113/jphysiol.1981.sp013553. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Fink G. D., Bryan W. J. Forebrain control of fluid and electrolyte homeostasis and angiotensin sensitivity in rabbit. Am J Physiol. 1980 Nov;239(5):R372–R376. doi: 10.1152/ajpregu.1980.239.5.R372. [DOI] [PubMed] [Google Scholar]
  10. Fischer-Ferraro C., Nahmod V. E., Goldstein D. J., Finkielman S. Angiotensin and renin in rat and dog brain. J Exp Med. 1971 Feb 1;133(2):353–361. doi: 10.1084/jem.133.2.353. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Fitzsimons J. T. Angiotensin stimulation of the central nervous system. Rev Physiol Biochem Pharmacol. 1980;87:117–167. doi: 10.1007/BFb0030897. [DOI] [PubMed] [Google Scholar]
  12. Fitzsimons J. T., Massi M., Thornton S. N. The effects of changes in osmolality and sodium concentration on angiotensin-induced drinking and excretion in the pigeon. J Physiol. 1982 Sep;330:1–15. doi: 10.1113/jphysiol.1982.sp014325. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Ganten D., Minnich J. L., Granger P., Hayduk K., Brecht H. M., Barbeau A., Boucher R., Genest J. Angiotensin-forming enzyme in brain tissue. Science. 1971 Jul 2;173(3991):64–65. doi: 10.1126/science.173.3991.64. [DOI] [PubMed] [Google Scholar]
  14. Haack D., Möhring J. Vasopressin-mediated blood pressure response to intraventricular injection of angiotensin II in the rat. Pflugers Arch. 1978 Feb 22;373(2):167–173. doi: 10.1007/BF00584856. [DOI] [PubMed] [Google Scholar]
  15. Hammel H. T., Simon-Oppermann C., Simon E. Properties of body fluids influencing salt gland secretion in Pekin ducks. Am J Physiol. 1980 Nov;239(5):R489–R496. doi: 10.1152/ajpregu.1980.239.5.R489. [DOI] [PubMed] [Google Scholar]
  16. Hoffman W. E., Philips M. I., Schmid P. G., Falcon J., Weet J. F. Antidiuretic hormone release and the pressor response to central angiotensin II and cholinergic stimulation. Neuropharmacology. 1977 Jul-Aug;16(7-8):463–472. doi: 10.1016/0028-3908(77)90002-8. [DOI] [PubMed] [Google Scholar]
  17. Håkansson C. H., Malcus B. Secretive response of the electrically stimulated nasal salt gland in Larus argentatus (Herring gull). Acta Physiol Scand. 1969 Aug;76(4):385–392. doi: 10.1111/j.1748-1716.1969.tb04483.x. [DOI] [PubMed] [Google Scholar]
  18. Jones P. M., Robinson I. C. Differential clearance of neurophysin and neurohypophysial peptides from the cerebrospinal fluid in conscious guinea pigs. Neuroendocrinology. 1982 Apr;34(4):297–302. doi: 10.1159/000123316. [DOI] [PubMed] [Google Scholar]
  19. Keil L. C., Summy-Long J., Severs W. B. Release of vasopressin by angiotensin II. Endocrinology. 1975 Apr;96(4):1063–1065. doi: 10.1210/endo-96-4-1063. [DOI] [PubMed] [Google Scholar]
  20. Leksell L. G., Rundgren M. Cerebral sodium-angiotensin interaction demonstrated with "subthreshold" amounts of angiotensin II. Acta Physiol Scand. 1977 Aug;100(4):494–496. doi: 10.1111/j.1748-1716.1977.tb05976.x. [DOI] [PubMed] [Google Scholar]
  21. Mangiapane M. L., Simpson J. B. Subfornical organ: forebrain site of pressor and dipsogenic action of angiotensin II. Am J Physiol. 1980 Nov;239(5):R382–R389. doi: 10.1152/ajpregu.1980.239.5.R382. [DOI] [PubMed] [Google Scholar]
  22. Möhring J., Schoun J., Simon-Oppermann C., Simon E. Radioimmunoassay for arginine-vasotocin (AVT) in serum of Pekin ducks: AVT concentrations after adaptation to fresh water and salt water. Pflugers Arch. 1980 Sep;387(2):91–97. doi: 10.1007/BF00584258. [DOI] [PubMed] [Google Scholar]
  23. Nakayama T., Nakajima T., Sokabe H. Comparative studies on angiotensins. 3. Structure of fowl angiotensin and its identification by DNS-method. Chem Pharm Bull (Tokyo) 1973 Sep;21(9):2085–2087. doi: 10.1248/cpb.21.2085. [DOI] [PubMed] [Google Scholar]
  24. Peach M. J. Renin-angiotensin system: biochemistry and mechanisms of action. Physiol Rev. 1977 Apr;57(2):313–370. doi: 10.1152/physrev.1977.57.2.313. [DOI] [PubMed] [Google Scholar]
  25. Phillips M. I., Felix D. Specific angiotensin II receptive neurons in the cat subfornical organ. Brain Res. 1976 Jun 18;109(3):531–540. doi: 10.1016/0006-8993(76)90032-9. [DOI] [PubMed] [Google Scholar]
  26. SCHMIDT-NIELSEN K. The salt-secreting gland of marine birds. Circulation. 1960 May;21:955–967. doi: 10.1161/01.cir.21.5.955. [DOI] [PubMed] [Google Scholar]
  27. Severs W. B., Changaris D. G., Keil L. C., Summy-Long J. Y., Klase P. A., Kapsha J. M. Pharmacology of angiotensin-induced drinking behavior. Fed Proc. 1978 Nov;37(13):2699–2703. [PubMed] [Google Scholar]
  28. Simon E. The osmoregulatory system of birds with salt glands. Comp Biochem Physiol A Comp Physiol. 1982;71(4):547–556. doi: 10.1016/0300-9629(82)90203-1. [DOI] [PubMed] [Google Scholar]
  29. Simpson J. B., Mangiapane M. L., Dellmann H. D. Central receptor sites for angiotensin-induced drinking: a critical review. Fed Proc. 1978 Nov;37(13):2676–2682. [PubMed] [Google Scholar]
  30. Sirett N. E., McLean A. S., Bray J. J., Hubbard J. I. Distribution of angiotensin II receptors in rat brain. Brain Res. 1977 Feb 18;122(2):299–312. doi: 10.1016/0006-8993(77)90296-7. [DOI] [PubMed] [Google Scholar]
  31. Takei Y. Angiotensin and water intake in the Japanese quail (Conturnix coturnix japonica). Gen Comp Endocrinol. 1977 Mar;31(3):364–372. doi: 10.1016/0016-6480(77)90100-9. [DOI] [PubMed] [Google Scholar]
  32. Wada M., Kobayashi H., Farner D. S. Induction of drinking in the white-crowned sparrow, Zonotrichia leucophrys gambelii, by intracranial injection of angiotensin II. Gen Comp Endocrinol. 1975 Jun;26(2):192–197. doi: 10.1016/0016-6480(75)90135-5. [DOI] [PubMed] [Google Scholar]
  33. Yamamoto M., Share L., Shade R. E. Effect of ventriculo-cisternal perfusion with angiotensin II and indomethacin on the plasma vasopressin concentration. Neuroendocrinology. 1978;25(3):166–173. doi: 10.1159/000122738. [DOI] [PubMed] [Google Scholar]

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