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. 1975 Dec;253(2):593–620. doi: 10.1113/jphysiol.1975.sp011209

Catecholamine release from bovine adrenal medulla in response to maintained depolarization.

P F Baker, T J Rink
PMCID: PMC1348525  PMID: 1214228

Abstract

Prolonged exposure of venous-perfused bovine adrenal glands to high K in the presence of external Ca produces a transient increase in catecholamine output that reaches a maximum after about 1 min and then declines with a half-time of about 1-2 min. 2. The time course of the transient secretory response to high K does not depend appreciably on the total catecholamine output which indicates that depletion of releasable catecholamine is unlikely to be responsible for the transient nature of the response. 3. Application of 3-6 mM-Ba stimulates secretion from a gland after many minutes exposure to high K, when catecholamine output has declined close to resting levels. This provides further evidence that depletion does not play a major role in the transient response and shows that maintained depolarization does not inhibit the secretory mechanism. 4. Exposure to high K solutions in which Ca has been replaced isomotically by Mg does not evoke any catecholamine output. Subsequent application of Ca always elicits some secretion although the size of this response to added Ca declines rapidly during exposure to Ca-free, high K solutions. The failure of the secretory response in these experiments is more rapid, and earlier in onset than the declining phase of the normal secretory response evoked in the presence of calcium. 5. Pre-treatment with Ca-free solutions of intermediate K content reduces the response to subsequent simultaneous application of high K and Ca. There is a roughly sigmoidal relation between the reduction in response and the logarithm of the K concentration used for pre-treatment. 6. Thin slices of bovine adrenal medulla show qualitatively similar responses on exposure to high K. Examination of the flourescent signal from slices dyed with the potential-sensitive dye DiS-C(3)-(5) suggests that maintained exposure to high K produces a stable depolarization. 7. The most likely explanation for these results is that K-depolarization first activates and subsequently inactivates a potential-sensitive Ca permeability channel. This inactivation is time and possibly potential dependent. 8. The effect of high K on calcium movements in medullary slices was examined. Exposure to 72 mM-K increases (45)Ca uptake, the increase being greatest during the first 10 min. The efflux of Ca is also increased on exposure to high K in the presence of Ca. The net Ca uptake in 72 mM-K is smaller than the tracer uptake of Ca. These findings indicate that K depolarization stimulates a Ca-Ca exchange process. They are also consistent with, but do not offer strong positive support for, the idea that K-depolarization first activates and subsequently inactivates Ca entry. 9. It is suggested that Ca inactivation might play a role in the modulation of neurosecretion and neurotransmitter release by changes in membrane potential.

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Selected References

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

  1. Armstrong C. M., Bezanilla F., Rojas E. Destruction of sodium conductance inactivation in squid axons perfused with pronase. J Gen Physiol. 1973 Oct;62(4):375–391. doi: 10.1085/jgp.62.4.375. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. BOROWITZ J. L., FUWA K., WEINER N. DISTRIBUTION OF METALS AND CATECHOLAMINES IN BOVINE ADRENAL MEDULLA SUB-CELLULAR FRACTIONS. Nature. 1965 Jan 2;205:42–43. doi: 10.1038/205042a0. [DOI] [PubMed] [Google Scholar]
  3. Baker P. F., Meves H., Ridgway E. B. Calcium entry in response to maintained depolarization of squid axons. J Physiol. 1973 Jun;231(3):527–548. doi: 10.1113/jphysiol.1973.sp010247. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Baker P. F., Rink T. J. Proceedings: Transient release of catecholamines in response to maintained depolarization of bovine adrenal medulla. J Physiol. 1974 Sep;241(2):107P–109P. [PubMed] [Google Scholar]
  5. Banks P., Biggins R., Bishop R., Christian B., Currie N. Sodium ions and the secretion of catecholamines. J Physiol. 1969 Feb;200(3):797–805. doi: 10.1113/jphysiol.1969.sp008722. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Banks P. Effects of stimulation by carbachol on the metabolism of the bovine adrenal medulla. Biochem J. 1965 Nov;97(2):555–560. doi: 10.1042/bj0970555. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Beeler G. W., Jr, Reuter H. Membrane calcium current in ventricular myocardial fibres. J Physiol. 1970 Mar;207(1):191–209. doi: 10.1113/jphysiol.1970.sp009056. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Borle A. B. Kinetic analyses of calcium movements in HeLa cell cultures. I. Calcium influx. J Gen Physiol. 1969 Jan;53(1):43–56. doi: 10.1085/jgp.53.1.43. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. DOUGLAS W. W., POISNER A. M. CALCIUM MOVEMENT IN THE NEUROHYPOPHYSIS OF THE RAT AND ITS RELATION TO THE RELEASE OF VASOPRESSIN. J Physiol. 1964 Jul;172:19–30. doi: 10.1113/jphysiol.1964.sp007400. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. DOUGLAS W. W., POISNER A. M. On the mode of action of acetylcholine in evoking adrenal medullary secretion: increased uptake of calcium during the secretory response. J Physiol. 1962 Aug;162:385–392. doi: 10.1113/jphysiol.1962.sp006940. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. DOUGLAS W. W., POISNER A. M. Stimulation of uptake of calcium-45 in the adrenal gland by acetylcholine. Nature. 1961 Dec 30;192:1299–1299. doi: 10.1038/1921299a0. [DOI] [PubMed] [Google Scholar]
  12. DOUGLAS W. W., RUBIN R. P. STIMULANT ACTION OF BARIUM ON THE ADRENAL MEDULLA. Nature. 1964 Jul 18;203:305–307. doi: 10.1038/203305a0. [DOI] [PubMed] [Google Scholar]
  13. DOUGLAS W. W., RUBIN R. P. The role of calcium in the secretory response of the adrenal medulla to acetylcholine. J Physiol. 1961 Nov;159:40–57. doi: 10.1113/jphysiol.1961.sp006791. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Douglas W. W., Kanno T., Sampson S. R. Influence of the ionic environment on the membrane potential of adrenal chromaffin cells and on the depolarizing effect of acetylcholine. J Physiol. 1967 Jul;191(1):107–121. doi: 10.1113/jphysiol.1967.sp008239. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Douglas W. W., Poisner A. M. On the relation between ATP splitting and secretion in the adrenal chromaffin cell: extrusion of ATP (unhydrolysed) during release of catecholamines. J Physiol. 1966 Mar;183(1):249–256. doi: 10.1113/jphysiol.1966.sp007864. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Douglas W. W., Rubin R. P. The mechanism of catecholamine release from the adrenal medulla and the role of calcium in stimulus-secretion coupling. J Physiol. 1963 Jul;167(2):288–310. doi: 10.1113/jphysiol.1963.sp007150. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Foreman J. C., Garland L. G. Desensitization in the process of histamine secretion induced by antigen and dextran. J Physiol. 1974 Jun;239(2):381–391. doi: 10.1113/jphysiol.1974.sp010574. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. HODGKIN A. L., HOROWICZ P. Potassium contractures in single muscle fibres. J Physiol. 1960 Sep;153:386–403. doi: 10.1113/jphysiol.1960.sp006541. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. HODGKIN A. L., HUXLEY A. F. The dual effect of membrane potential on sodium conductance in the giant axon of Loligo. J Physiol. 1952 Apr;116(4):497–506. doi: 10.1113/jphysiol.1952.sp004719. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. HODGKIN A. L., KEYNES R. D. Movements of labelled calcium in squid giant axons. J Physiol. 1957 Sep 30;138(2):253–281. doi: 10.1113/jphysiol.1957.sp005850. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kirpekar S. M., Prat J. C., Puig M., Wakade A. R. Modification of the evoked release of noradrenaline from the perfused cat spleen by various ions and agents. J Physiol. 1972 Mar;221(3):601–615. doi: 10.1113/jphysiol.1972.sp009770. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Maddrell S. H., Gee J. D. Potassium-induced release of the diuretic hormones of Rhodnius prolixus and Glossina austeni: Ca dependence, time course and localization of neurohaemal areas. J Exp Biol. 1974 Aug;61(1):155–171. doi: 10.1242/jeb.61.1.155. [DOI] [PubMed] [Google Scholar]
  23. Matthews E. K., Sakamoto Y. Electrical characteristics of pancreatic islet cells. J Physiol. 1975 Mar;246(2):421–437. doi: 10.1113/jphysiol.1975.sp010897. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. NAKAJIMA S., IWASAKI S., OBATA K. Delayed rectification and anomalous rectification in frog's skeletal muscle membrane. J Gen Physiol. 1962 Sep;46:97–115. doi: 10.1085/jgp.46.1.97. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Nordmann J. J. Proceedings: Hormone release in relation to inactivation of Ca-entry in the rat neurohypophysis. J Physiol. 1975 Jul;249(1):38P–39P. [PubMed] [Google Scholar]
  26. Rubin R. P. The metabolic requirements from catecholamine release from the adrenal medulla. J Physiol. 1969 May;202(1):197–209. doi: 10.1113/jphysiol.1969.sp008804. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Russell J. T., Thorn N. A. Calcium and stimulus-secretion coupling in the neurohypophysis. I. 45-Calcium transport and vasopressin release in slices from ox neurohypophyses stimulated electrically or by a high potassium concentration. Acta Endocrinol (Copenh) 1974 Jul;76(3):449–470. [PubMed] [Google Scholar]
  28. Sims P. J., Waggoner A. S., Wang C. H., Hoffman J. F. Studies on the mechanism by which cyanine dyes measure membrane potential in red blood cells and phosphatidylcholine vesicles. Biochemistry. 1974 Jul 30;13(16):3315–3330. doi: 10.1021/bi00713a022. [DOI] [PubMed] [Google Scholar]
  29. Standen N. B. Properties of a calcium channel in snail neurones. Nature. 1974 Jul 26;250(464):340–342. doi: 10.1038/250340a0. [DOI] [PubMed] [Google Scholar]
  30. Woodward J. K., Bianchi C. P., Erulkar S. D. Electrolyte distribution in rabbit superior cervical ganglion. J Neurochem. 1969 Mar;16(3):289–299. doi: 10.1111/j.1471-4159.1969.tb10367.x. [DOI] [PubMed] [Google Scholar]

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