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PMID: 7708776 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Activation of nicotinic receptors triggers exocytosis from bovine chromaffin cells in the absence of membrane depolarization.

Mollard P, Seward EP, Nowycky MC

Abstract

The traditional function of neurotransmitter-gated ion channels is to induce rapid changes in electrical activity. Channels that are Ca(2+)-permeable, such as N-methyl-D-aspartate receptors at depolarized membrane potentials, can have a broader repertoire of consequences, including changes in synaptic efficacy, developmental plasticity, and excitotoxicity. Neuronal nicotinic receptors for acetylcholine (nAChRs) are usually less Ca(2+)-permeable than N-methyl-D-aspartate receptors but have a significant Ca2+ permeability, which is greater at negative potentials. Here we report that in neuroendocrine cells, activation of nAChRs can trigger exocytosis at hyperpolarized potentials. We used whole-cell patch-clamp recordings to record currents and the capacitance detection technique to monitor exocytosis in isolated bovine chromaffin cells. Stimulation of nAChRs at hyperpolarized potentials (-60 or -90 mV) evokes a large current and a maximal capacitance increase corresponding to the fusion of approximately 200 large dense-core vesicles. The amount of exocytosis is controlled both by the Ca2+ influx through nAChRs and by a contribution from thapsigargin-sensitive Ca2+ sequestering stores. This is a form of neurotransmitter action in which activation of nAChRs triggers secretion through an additional coupling pathway that coexists with classical voltage-dependent Ca2+ entry.

MeSH Terms
Adrenal Medulla/physiology Animals Calcium/metabolism Calcium-Transporting ATPases/antagonists & inhibitors Cattle Cells, Cultured Cytosol/metabolism Evoked Potentials/drug effects Exocytosis/drug effects Kinetics Membrane Potentials/drug effects Nicotine/pharmacology Patch-Clamp Techniques Receptors, Nicotinic/physiology Terpenes/pharmacology Thapsigargin Time Factors Tubocurarine/pharmacology
Chemicals
Receptors, Nicotinic Terpenes Thapsigargin Nicotine Calcium-Transporting ATPases Calcium Tubocurarine
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Mollard P
Department of Anatomy and Neurobiology, Medical College of Pennsylvania, Philadelphia 19129, USA.
Seward E P
Nowycky M C
References (31)
31 references, click to expand
  1. Calcium mobilization is required for nuclear vesicle fusion in vitro: implications for membrane traffic and IP3 receptor function.
    Cell. 1993 Jul 2;73(7):1411-22 PMID: 8391933
  2. Phase tracking: an improved phase detection technique for cell membrane capacitance measurements.
    Biophys J. 1989 Dec;56(6):1153-62 PMID: 2611329
  3. Action potentials in the rat chromaffin cell and effects of acetylcholine.
    J Physiol. 1976 Dec;263(3):417-39 PMID: 1018274
  4. Activation of the nicotinic acetylcholine receptor mobilizes calcium from caffeine-insensitive stores in C2C12 mouse myotubes.
    Pflugers Arch. 1993 Mar;422(6):591-8 PMID: 8469610
  5. Characterization of Ca2+ signals induced in hippocampal CA1 neurones by the synaptic activation of NMDA receptors.
    J Physiol. 1993 Sep;469:693-716 PMID: 8271224
  6. A two-step model of secretion control in neuroendocrine cells.
    Pflugers Arch. 1993 Jul;424(2):105-12 PMID: 8414901
  7. Colocalization of ion channels involved in frequency selectivity and synaptic transmission at presynaptic active zones of hair cells.
    J Neurosci. 1990 Nov;10(11):3664-84 PMID: 1700083
  8. Alien intracellular calcium chelators attenuate neurotransmitter release at the squid giant synapse.
    J Neurosci. 1991 Jun;11(6):1496-507 PMID: 1675264
  9. Internal Ca2+ mobilization and secretion in bovine adrenal chromaffin cells.
    Cell Calcium. 1989 May-Jun;10(4):213-21 PMID: 2789101
  10. The role of caffeine-sensitive Ca2+ stores in agonist- and inositol 1,4,5-trisphosphate-induced Ca2+ release from bovine adrenal chromaffin cells.
    Biochem J. 1991 Sep 15;278 ( Pt 3):643-50 PMID: 1898353
  11. Calcium entry through nicotinic receptor channels and calcium channels in cultured rat superior cervical ganglion cells.
    J Physiol. 1993 Aug;468:53-71 PMID: 8254522
  12. Calcium requirements for secretion in bovine chromaffin cells.
    J Physiol. 1992 May;450:247-71 PMID: 1432709
  13. A caffeine- and ryanodine-sensitive intracellular Ca2+ store can act as a Ca2+ source and a Ca2+ sink in PC12 cells.
    Biochem J. 1994 Jun 1;300 ( Pt 2):589-97 PMID: 8002966
  14. Three types of bovine chromaffin cell Ca2+ channels: facilitation increases the opening probability of a 27 pS channel.
    J Physiol. 1991 Dec;444:213-40 PMID: 1726596
  15. Calcium modulation and high calcium permeability of neuronal nicotinic acetylcholine receptors.
    Neuron. 1992 Jan;8(1):127-34 PMID: 1370370
  16. Capacitance measurements. An analysis of the phase detector technique used to study exocytosis and endocytosis.
    Biophys J. 1988 Jun;53(6):885-92 PMID: 3395658
  17. Inhibition of L-type calcium-channel activity by thapsigargin and 2,5-t-butylhydroquinone, but not by cyclopiazonic acid.
    Biochem J. 1994 Aug 15;302 ( Pt 1):147-54 PMID: 7520693
  18. Thapsigargin, a tumor promoter, discharges intracellular Ca2+ stores by specific inhibition of the endoplasmic reticulum Ca2(+)-ATPase.
    Proc Natl Acad Sci U S A. 1990 Apr;87(7):2466-70 PMID: 2138778
  19. Calcium influx through nicotinic receptor in rat central neurons: its relevance to cellular regulation.
    Neuron. 1992 Jan;8(1):135-43 PMID: 1309647
  20. 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 PMID: 16992152
  21. Delay in vesicle fusion revealed by electrochemical monitoring of single secretory events in adrenal chromaffin cells.
    Nature. 1992 Mar 5;356(6364):60-3 PMID: 1538782
  22. Discrete changes of cell membrane capacitance observed under conditions of enhanced secretion in bovine adrenal chromaffin cells.
    Proc Natl Acad Sci U S A. 1982 Nov;79(21):6712-6 PMID: 6959149
  23. Characterisation of distinct inositol 1,4,5-trisphosphate-sensitive and caffeine-sensitive calcium stores in digitonin-permeabilised adrenal chromaffin cells.
    J Neurochem. 1991 May;56(5):1587-93 PMID: 1826518
  24. Ca2+ influx induced by the Ca(2+)-ATPase inhibitors 2,5-di-(t-butyl)-1,4-benzohydroquinone and thapsigargin in bovine adrenal chromaffin cells.
    Biochem J. 1992 Dec 1;288 ( Pt 2):457-63 PMID: 1463451
  25. Quantitative measurement of calcium flux through muscle and neuronal nicotinic acetylcholine receptors.
    J Neurosci. 1994 Sep;14(9):5514-24 PMID: 8083751
  26. 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):107-21 PMID: 6050606
  27. Distribution of two distinct Ca2+-ATPase-like proteins and their relationships to the agonist-sensitive calcium store in adrenal chromaffin cells.
    Nature. 1989 Nov 2;342(6245):72-4 PMID: 2530452
  28. Cortical filamentous actin disassembly and scinderin redistribution during chromaffin cell stimulation precede exocytosis, a phenomenon not exhibited by gelsolin.
    J Cell Biol. 1991 Jun;113(5):1057-67 PMID: 1645735
  29. Localized Ca2+ entry preferentially effects protein dephosphorylation, phosphorylation, and glutamate release.
    J Biol Chem. 1992 Jan 25;267(3):1983-9 PMID: 1309806
  30. Nicotinic and muscarinic agonists stimulate rapid protein kinase C translocation in PC12 cells.
    J Neurosci. 1989 Feb;9(2):507-12 PMID: 2493078
  31. Use of fura red as an intracellular calcium indicator in frog skeletal muscle fibers.
    Biophys J. 1993 Jun;64(6):1934-60 PMID: 8369415
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
1995-03-28
Pages
3065-9
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC42360
Subset
IM
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