Skip to main content
PMC home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1993 Aug;468:335–355. doi: 10.1113/jphysiol.1993.sp019775

Intracellular calcium and vasopressin release of rat isolated neurohypophysial nerve endings.

E L Stuenkel 1, J J Nordmann 1
PMCID: PMC1143830  PMID: 8254513

Abstract

1. Monitoring of [Ca2+]i and vasopressin secretion in isolated nerve endings from the rat neurohypophysis were studied to determine the relationship between the time course of vasopressin secretion and depolarization-induced changes in [Ca2+]i. 2. Membrane depolarization by increasing the extracellular [K+] led to concentration-dependent, parallel increases in the amount of vasopressin release and in peak increases in [Ca2+]i. Half-maximal activation of a change in [Ca2+]i was attained at 40 mM extracellular K+. 3. The Ca2+ chelator dimethyl-BAPTA (1,2-bis(O-aminophenoxy)ethane-N,N,N'N'-tetraacetic acid), loaded into the nerve endings, reduced K+ depolarization-evoked vasopressin release and efficiently antagonized K(+)-induced changes in [Ca2+]i. Moreover, dimethyl-BAPTA dramatically reduced basal [Ca2+]i without a reduction in basal secretion. 4. The duration of the vasopressin secretory response was similar regardless of applied 50 mM K+ depolarizations longer than 30 s. The t1/2 of the secretory response was 45 s. Application of repetitive K+ depolarization pulses repetitive secretory responses of similar amplitude and duration. 5. The K(+)-induced changes in [Ca2+]i remained elevated throughout the duration of the depolarizing stimulus decreasing less than 30% over 3 min. The sustained increase in [Ca2+]i resulted largely from continued enhanced Ca2+ influx, demonstrated by susceptibility to the dihydropyridine, L-type calcium channel blocker, nicardipine. 6. Vasopressin secretion could be reinitiated following its decline to a step K+ depolarization by a further step increase in K+ or by removal and readdition of extracellular [Ca2+]. Alterations in [Ca2+]i paralleled periods of secretory activity. 7. Analysis of secretory responsiveness and change in [Ca2+]i to K+ depolarization in medium of altered extracellular [Ca2+] indicates that [Ca2+]i of 20 microM is sufficient to trigger vasopressin release. K(+)-induced alterations in [Ca2+]i could be observed at [Ca2+]o as low as 5 microM. Although smaller in amplitude to that observed at 2.2 mM [Ca2+]o the duration of the K(+)-induced secretory response increased at lower [Ca2+]o. 8. Transient vasopressin secretory responses were observed to sustained levels of [Ca2+] in digitonin and streptolysin-O-permeabilized nerve endings. Secretion could be re-evoked, following its decline, by a step increase in [Ca2+] or by removal and readdition of [Ca2+]o.(ABSTRACT TRUNCATED AT 400 WORDS)

Full text

PDF
335

Selected References

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

  1. Almers W. Exocytosis. Annu Rev Physiol. 1990;52:607–624. doi: 10.1146/annurev.ph.52.030190.003135. [DOI] [PubMed] [Google Scholar]
  2. Augustine G. J., Adler E. M., Charlton M. P. The calcium signal for transmitter secretion from presynaptic nerve terminals. Ann N Y Acad Sci. 1991;635:365–381. doi: 10.1111/j.1749-6632.1991.tb36505.x. [DOI] [PubMed] [Google Scholar]
  3. Augustine G. J., Charlton M. P., Smith S. J. Calcium action in synaptic transmitter release. Annu Rev Neurosci. 1987;10:633–693. doi: 10.1146/annurev.ne.10.030187.003221. [DOI] [PubMed] [Google Scholar]
  4. Augustine G. J., Charlton M. P., Smith S. J. Calcium entry and transmitter release at voltage-clamped nerve terminals of squid. J Physiol. 1985 Oct;367:163–181. doi: 10.1113/jphysiol.1985.sp015819. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Augustine G. J., Neher E. Calcium requirements for secretion in bovine chromaffin cells. J Physiol. 1992 May;450:247–271. doi: 10.1113/jphysiol.1992.sp019126. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Baker P. F., Rink T. J. Catecholamine release from bovine adrenal medulla in response to maintained depolarization. J Physiol. 1975 Dec;253(2):593–620. doi: 10.1113/jphysiol.1975.sp011209. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Birman S., Meunier F. M. Inactivation of acetylcholine release from Torpedo synaptosomes in response to prolonged depolarizations. J Physiol. 1985 Nov;368:293–307. doi: 10.1113/jphysiol.1985.sp015858. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bourque C. W. Intraterminal recordings from the rat neurohypophysis in vitro. J Physiol. 1990 Feb;421:247–262. doi: 10.1113/jphysiol.1990.sp017943. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Brethes D., Dayanithi G., Letellier L., Nordmann J. J. Depolarization-induced Ca2+ increase in isolated neurosecretory nerve terminals measured with fura-2. Proc Natl Acad Sci U S A. 1987 Mar;84(5):1439–1443. doi: 10.1073/pnas.84.5.1439. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Cazalis M., Dayanithi G., Nordmann J. J. Hormone release from isolated nerve endings of the rat neurohypophysis. J Physiol. 1987 Sep;390:55–70. doi: 10.1113/jphysiol.1987.sp016686. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Cazalis M., Dayanithi G., Nordmann J. J. Requirements for hormone release from permeabilized nerve endings isolated from the rat neurohypophysis. J Physiol. 1987 Sep;390:71–91. doi: 10.1113/jphysiol.1987.sp016687. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Cazalis M., Dayanithi G., Nordmann J. J. The role of patterned burst and interburst interval on the excitation-coupling mechanism in the isolated rat neural lobe. J Physiol. 1985 Dec;369:45–60. doi: 10.1113/jphysiol.1985.sp015887. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Cheek T. R., Jackson T. R., O'Sullivan A. J., Moreton R. B., Berridge M. J., Burgoyne R. D. Simultaneous measurements of cytosolic calcium and secretion in single bovine adrenal chromaffin cells by fluorescent imaging of fura-2 in cocultured cells. J Cell Biol. 1989 Sep;109(3):1219–1227. doi: 10.1083/jcb.109.3.1219. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. DOUGLAS W. W., POISNER A. M. STIMULUS-SECRETION COUPLING IN A NEUROSECRETORY ORGAN: THE ROLE OF CALCIUM IN THE RELEASE OF VASOPRESSIN FROM THE NEUROHYPOPHYSIS. J Physiol. 1964 Jul;172:1–18. doi: 10.1113/jphysiol.1964.sp007399. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Datyner N. B., Gage P. W. Phasic secretion of acetylcholine at a mammalian neuromuscular junction. J Physiol. 1980 Jun;303:299–314. doi: 10.1113/jphysiol.1980.sp013286. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Delaney K. R., Zucker R. S., Tank D. W. Calcium in motor nerve terminals associated with posttetanic potentiation. J Neurosci. 1989 Oct;9(10):3558–3567. doi: 10.1523/JNEUROSCI.09-10-03558.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Dodge F. A., Jr, Rahamimoff R. Co-operative action a calcium ions in transmitter release at the neuromuscular junction. J Physiol. 1967 Nov;193(2):419–432. doi: 10.1113/jphysiol.1967.sp008367. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. 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]
  19. Fogelson A. L., Zucker R. S. Presynaptic calcium diffusion from various arrays of single channels. Implications for transmitter release and synaptic facilitation. Biophys J. 1985 Dec;48(6):1003–1017. doi: 10.1016/S0006-3495(85)83863-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Gainer H., Wolfe S. A., Jr, Obaid A. L., Salzberg B. M. Action potentials and frequency-dependent secretion in the mouse neurohypophysis. Neuroendocrinology. 1986;43(5):557–563. doi: 10.1159/000124582. [DOI] [PubMed] [Google Scholar]
  21. Garcia A. G., Kirpekar S. M., Sanchez-Garcia P. Release of noradrenaline from the cat spleen by nerve stimulation and potassium. J Physiol. 1976 Oct;261(2):301–317. doi: 10.1113/jphysiol.1976.sp011560. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Grynkiewicz G., Poenie M., Tsien R. Y. A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem. 1985 Mar 25;260(6):3440–3450. [PubMed] [Google Scholar]
  23. Hagiwara S., Byerly L. Calcium channel. Annu Rev Neurosci. 1981;4:69–125. doi: 10.1146/annurev.ne.04.030181.000441. [DOI] [PubMed] [Google Scholar]
  24. Hamill O. P., Marty A., Neher E., Sakmann B., Sigworth F. J. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 1981 Aug;391(2):85–100. doi: 10.1007/BF00656997. [DOI] [PubMed] [Google Scholar]
  25. Hirning L. D., Fox A. P., McCleskey E. W., Olivera B. M., Thayer S. A., Miller R. J., Tsien R. W. Dominant role of N-type Ca2+ channels in evoked release of norepinephrine from sympathetic neurons. Science. 1988 Jan 1;239(4835):57–61. doi: 10.1126/science.2447647. [DOI] [PubMed] [Google Scholar]
  26. Holz R. W., Senter R. A., Frye R. A. Relationship between Ca2+ uptake and catecholamine secretion in primary dissociated cultures of adrenal medulla. J Neurochem. 1982 Sep;39(3):635–646. doi: 10.1111/j.1471-4159.1982.tb07940.x. [DOI] [PubMed] [Google Scholar]
  27. Irvine R. F. 'Quantal' Ca2+ release and the control of Ca2+ entry by inositol phosphates--a possible mechanism. FEBS Lett. 1990 Apr 9;263(1):5–9. doi: 10.1016/0014-5793(90)80692-c. [DOI] [PubMed] [Google Scholar]
  28. Katz B., Miledi R. The effect of temperature on the synaptic delay at the neuromuscular junction. J Physiol. 1965 Dec;181(3):656–670. doi: 10.1113/jphysiol.1965.sp007790. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Kelly R. B. The cell biology of the nerve terminal. Neuron. 1988 Aug;1(6):431–438. doi: 10.1016/0896-6273(88)90174-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Knight D. E., Baker P. F. Calcium-dependence of catecholamine release from bovine adrenal medullary cells after exposure to intense electric fields. J Membr Biol. 1982;68(2):107–140. doi: 10.1007/BF01872259. [DOI] [PubMed] [Google Scholar]
  31. Lemos J. R., Nowycky M. C. Two types of calcium channels coexist in peptide-releasing vertebrate nerve terminals. Neuron. 1989 May;2(5):1419–1426. doi: 10.1016/0896-6273(89)90187-6. [DOI] [PubMed] [Google Scholar]
  32. Lester H. A. Transmitter release by presynaptic impulses in the squid stellate ganglion. Nature. 1970 Aug 1;227(5257):493–496. doi: 10.1038/227493a0. [DOI] [PubMed] [Google Scholar]
  33. Lindau M., Stuenkel E. L., Nordmann J. J. Depolarization, intracellular calcium and exocytosis in single vertebrate nerve endings. Biophys J. 1992 Jan;61(1):19–30. doi: 10.1016/S0006-3495(92)81812-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Llinás R., Nicholson C. Calcium role in depolarization-secretion coupling: an aequorin study in squid giant synapse. Proc Natl Acad Sci U S A. 1975 Jan;72(1):187–190. doi: 10.1073/pnas.72.1.187. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Llinás R., Steinberg I. Z., Walton K. Presynaptic calcium currents and their relation to synaptic transmission: voltage clamp study in squid giant synapse and theoretical model for the calcium gate. Proc Natl Acad Sci U S A. 1976 Aug;73(8):2918–2922. doi: 10.1073/pnas.73.8.2918. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Miledi R., Parker I. Calcium transients recorded with arsenazo III in the presynaptic terminal of the squid giant synapse. Proc R Soc Lond B Biol Sci. 1981 May 22;212(1187):197–211. doi: 10.1098/rspb.1981.0034. [DOI] [PubMed] [Google Scholar]
  37. Miledi R., Slater C. R. The action of calcium on neuronal synapses in the squid. J Physiol. 1966 May;184(2):473–498. doi: 10.1113/jphysiol.1966.sp007927. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Miller R. J. Multiple calcium channels and neuronal function. Science. 1987 Jan 2;235(4784):46–52. doi: 10.1126/science.2432656. [DOI] [PubMed] [Google Scholar]
  39. Müller J. R., Thorn N. A., Torp-Pedersen C. Effects of calcium and sodium on vasopressin release in vitro induced by a prolonged potassium stimulation. Acta Endocrinol (Copenh) 1975 May;79(1):51–59. doi: 10.1530/acta.0.0790051. [DOI] [PubMed] [Google Scholar]
  40. Nordmann J. J. Evidence for calcium inactivation during hormone release in the rat neurohypophysis. J Exp Biol. 1976 Dec;65(3):669–683. doi: 10.1242/jeb.65.3.669. [DOI] [PubMed] [Google Scholar]
  41. Poulain D. A., Wakerley J. B. Electrophysiology of hypothalamic magnocellular neurones secreting oxytocin and vasopressin. Neuroscience. 1982 Apr;7(4):773–808. doi: 10.1016/0306-4522(82)90044-6. [DOI] [PubMed] [Google Scholar]
  42. Pumplin D. W., Reese T. S., Llinás R. Are the presynaptic membrane particles the calcium channels? Proc Natl Acad Sci U S A. 1981 Nov;78(11):7210–7213. doi: 10.1073/pnas.78.11.7210. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Roberts W. M., Jacobs R. A., Hudspeth A. J. Colocalization of ion channels involved in frequency selectivity and synaptic transmission at presynaptic active zones of hair cells. J Neurosci. 1990 Nov;10(11):3664–3684. doi: 10.1523/JNEUROSCI.10-11-03664.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Sato N., Wang X. B., Greer M. A. The rate of increase not the amplitude of cytosolic Ca2+ regulates the degree of prolactin secretion induced by depolarizing K+ or hyposmolarity in GH4C1 cells. Biochem Biophys Res Commun. 1990 Jul 31;170(2):968–972. doi: 10.1016/0006-291x(90)92186-4. [DOI] [PubMed] [Google Scholar]
  45. Schweizer F. E., Schäfer T., Tapparelli C., Grob M., Karli U. O., Heumann R., Thoenen H., Bookman R. J., Burger M. M. Inhibition of exocytosis by intracellularly applied antibodies against a chromaffin granule-binding protein. Nature. 1989 Jun 29;339(6227):709–712. doi: 10.1038/339709a0. [DOI] [PubMed] [Google Scholar]
  46. Simon S. M., Llinás R. R. Compartmentalization of the submembrane calcium activity during calcium influx and its significance in transmitter release. Biophys J. 1985 Sep;48(3):485–498. doi: 10.1016/S0006-3495(85)83804-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Smith S. J., Augustine G. J., Charlton M. P. Transmission at voltage-clamped giant synapse of the squid: evidence for cooperativity of presynaptic calcium action. Proc Natl Acad Sci U S A. 1985 Jan;82(2):622–625. doi: 10.1073/pnas.82.2.622. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Stuenkel E. L. Effects of membrane depolarization on intracellular calcium in single nerve terminals. Brain Res. 1990 Oct 8;529(1-2):96–101. doi: 10.1016/0006-8993(90)90815-s. [DOI] [PubMed] [Google Scholar]
  49. Toescu E. C., Nordmann J. J. Effect of sodium and calcium on basal secretory activity of rat neurohypophysial peptidergic nerve terminals. J Physiol. 1991 Feb;433:127–144. doi: 10.1113/jphysiol.1991.sp018418. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Tsien R. W. Calcium channels in excitable cell membranes. Annu Rev Physiol. 1983;45:341–358. doi: 10.1146/annurev.ph.45.030183.002013. [DOI] [PubMed] [Google Scholar]
  51. Williams D. A., Fay F. S. Intracellular calibration of the fluorescent calcium indicator Fura-2. Cell Calcium. 1990 Feb-Mar;11(2-3):75–83. doi: 10.1016/0143-4160(90)90061-x. [DOI] [PubMed] [Google Scholar]
  52. Zucker R. S., Delaney K. R., Mulkey R., Tank D. W. Presynaptic calcium in transmitter release and posttetanic potentiation. Ann N Y Acad Sci. 1991;635:191–207. doi: 10.1111/j.1749-6632.1991.tb36492.x. [DOI] [PubMed] [Google Scholar]
  53. Zucker R. S. Short-term synaptic plasticity. Annu Rev Neurosci. 1989;12:13–31. doi: 10.1146/annurev.ne.12.030189.000305. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES