Home LiteratureArticle Details
PMID: 11739570 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Roles for mitochondrial and reverse mode Na+/Ca2+ exchange and the plasmalemma Ca2+ ATPase in post-tetanic potentiation at crayfish neuromuscular junctions.

Zhong N, Beaumont V, Zucker RS

Abstract

We have explored the processes regulating presynaptic calcium concentration ([Ca(2+)](i)) in the generation of post-tetanic potentiation (PTP) at crayfish neuromuscular junctions, using spectrophotometric dyes to measure changes in [Ca(2+)](i) and [Na(+)](i) and effects of inhibitors of Ca(2+)-transport processes. The mitochondrial Na(+)/Ca(2+) exchange inhibitor CGP 37157 was without effect, whereas the reverse mode plasmalemmal Na(+)/Ca(2+) exchange inhibitor KB R7943 reduced PTP and Ca(2+) accumulation caused by increased [Na(+)](i). Exchange inhibitory peptide and C28R2 had opposite effects, consistent with their block of the plasma membrane Ca(2+) ATPase. All drugs except CGP 37157 reduced Ca(2+) accumulation caused by Na(+) accumulation, which occurred on block of the Na(+)/K(+) pump, acting in proportion to their effects on plasmalemmal Na(+)/Ca(2+) exchange. We find no role for mitochondrial Na(+)/Ca(2+) exchange in presynaptic Ca(2+) regulation. The plasma membrane Na(+)/Ca(2+) exchanger acts in reverse mode to admit Ca(2+) into nerve terminals during and for some minutes after tetanic stimulation, while at the same time the plasma membrane Ca(2+) ATPase operates as an important Ca(2+) removal process. The interplay of these two Ca(2+) transport processes with Na(+)-independent mitochondrial Ca(2+) fluxes and the plasmalemma Na(+)/K(+) pump determines the magnitude of tetanic [Ca(2+)](i) accumulation and potentiation of excitatory transmission, and the post-tetanic time courses of decay of elevated [Ca(2+)](i) and PTP.

MeSH Terms
Action Potentials/drug effects Animals Astacoidea Calcium/metabolism Calcium-Transporting ATPases/antagonists & inhibitors,metabolism Clonazepam/analogs & derivatives,pharmacology Electric Stimulation Enzyme Inhibitors/pharmacology Fluorescent Dyes In Vitro Techniques Ion Transport/drug effects,physiology Microinjections Mitochondria/metabolism Neuromuscular Junction/drug effects,metabolism Ouabain/pharmacology Sodium/metabolism Sodium-Calcium Exchanger/antagonists & inhibitors,metabolism Thiazepines/pharmacology Thiourea/analogs & derivatives,pharmacology
Chemicals
2-(2-(4-(4-nitrobenzyloxy)phenyl)ethyl)isothiourea methanesulfonate Enzyme Inhibitors Fluorescent Dyes Sodium-Calcium Exchanger Thiazepines Ouabain Clonazepam CGP 37157 Sodium Calcium-Transporting ATPases Thiourea Calcium
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Zhong N
Department of Molecular and Cell Biology, University of California, Berkeley, California, 94720-3200, USA.
Beaumont V
Zucker R S
References (44)
44 references, click to expand
  1. The role of mitochondria in presynaptic calcium handling at a ribbon synapse.
    Neuron. 2000 Jan;25(1):229-37 PMID: 10707986
  2. Identification of critical positive charges in XIP, the Na/Ca exchange inhibitory peptide.
    Arch Biochem Biophys. 1997 May 15;341(2):273-9 PMID: 9169015
  3. Synaptic plasticity at crayfish neuromuscular junctions: presynaptic inhibition.
    Synapse. 1991 Mar;7(3):244-51 PMID: 1882333
  4. On the role of mitochondria in transmitter release from motor nerve terminals.
    J Physiol. 1975 Jun;248(2):285-306 PMID: 50439
  5. Mitochondrial calcium transport: mechanisms and functions.
    Cell Calcium. 2000 Nov-Dec;28(5-6):285-96 PMID: 11115368
  6. Ryanodine-sensitive calcium stores involved in neurotransmitter release from sympathetic nerve terminals of the guinea-pig.
    J Physiol. 1996 Dec 15;497 ( Pt 3):657-64 PMID: 9003551
  7. Ca2+ cooperativity in neurosecretion measured using photolabile Ca2+ chelators.
    J Neurophysiol. 1994 Aug;72(2):825-30 PMID: 7983538
  8. Mitochondrial involvement in post-tetanic potentiation of synaptic transmission.
    Neuron. 1997 Mar;18(3):483-91 PMID: 9115741
  9. Posttetanic potentiation at the crayfish neuromuscular junction is dependent on both intracellular calcium and sodium ion accumulation.
    J Neurosci. 1992 Nov;12(11):4327-36 PMID: 1432097
  10. Short-term synaptic plasticity.
    Annu Rev Neurosci. 1989;12:13-31 PMID: 2648947
  11. Selectivity of inhibition of Na(+)-Ca2+ exchange of heart mitochondria by benzothiazepine CGP-37157.
    J Cardiovasc Pharmacol. 1993 Apr;21(4):595-9 PMID: 7681905
  12. Presynaptic localization of sodium/calcium exchangers in neuromuscular preparations.
    J Neurosci. 1992 Dec;12(12):4898-904 PMID: 1464773
  13. Autoinhibitory domains of various Ca2+ transporters cross-react.
    J Biol Chem. 1993 Aug 15;268(23):17120-5 PMID: 8394328
  14. Effects of mitochondrion on calcium transients at intact presynaptic terminals depend on frequency of nerve firing.
    J Neurophysiol. 1998 Jul;80(1):186-95 PMID: 9658040
  15. Mitochondria as all-round players of the calcium game.
    J Physiol. 2000 Nov 15;529 Pt 1:37-47 PMID: 11080249
  16. Fluorescence ratio imaging of cytosolic free Na+ in individual fibroblasts and lymphocytes.
    J Biol Chem. 1989 Nov 15;264(32):19458-67 PMID: 2478559
  17. Intracellular recordings from crustacean motor axons during presynaptic inhibition.
    Brain Res. 1981 Nov 2;223(2):422-8 PMID: 7284821
  18. Roles of Na(+)-Ca2+ exchange and of mitochondria in the regulation of presynaptic Ca2+ and spontaneous glutamate release.
    Philos Trans R Soc Lond B Biol Sci. 1999 Feb 28;354(1381):357-64 PMID: 10212484
  19. Presynaptic mitochondria and the temporal pattern of neurotransmitter release.
    Philos Trans R Soc Lond B Biol Sci. 1999 Feb 28;354(1381):365-72 PMID: 10212485
  20. Palytoxin acts through Na+,K+-ATPase.
    Toxicon. 1989;27(11):1171-87 PMID: 2575806
  21. Plasma membrane calcium ATPases as critical regulators of calcium homeostasis during neuronal cell function.
    Front Biosci. 1999 Dec 01;4:D869-82 PMID: 10577388
  22. Long-term facilitation alters transmitter releasing properties at the crayfish neuromuscular junction.
    J Neurophysiol. 1986 Mar;55(3):484-98 PMID: 3007689
  23. A new generation of Ca2+ indicators with greatly improved fluorescence properties.
    J Biol Chem. 1985 Mar 25;260(6):3440-50 PMID: 3838314
  24. Evidence that mitochondria buffer physiological Ca2+ loads in lizard motor nerve terminals.
    J Physiol. 1998 May 15;509 ( Pt 1):59-65 PMID: 9547381
  25. Calcium in motor nerve terminals associated with posttetanic potentiation.
    J Neurosci. 1989 Oct;9(10):3558-67 PMID: 2795140
  26. Molecular and cellular physiology of intracellular calcium stores.
    Physiol Rev. 1994 Jul;74(3):595-636 PMID: 8036248
  27. A novel isothiourea derivative selectively inhibits the reverse mode of Na+/Ca2+ exchange in cells expressing NCX1.
    J Biol Chem. 1996 Sep 13;271(37):22391-7 PMID: 8798401
  28. Correlation of presynaptic and postsynaptic events during establishment of long-term facilitation at crayfish neuromuscular junction.
    J Neurophysiol. 1985 Aug;54(2):220-30 PMID: 2411884
  29. Mitochondria as regulators of stimulus-evoked calcium signals in neurons.
    Cell Calcium. 2000 Nov-Dec;28(5-6):307-16 PMID: 11115370
  30. Ryanodine-sensitive component of calcium transients evoked by nerve firing at presynaptic nerve terminals.
    J Neurosci. 1996 Nov 1;16(21):6703-12 PMID: 8824311
  31. Ca2+ regulation in the presynaptic terminals of goldfish retinal bipolar cells.
    J Physiol. 1995 Feb 15;483 ( Pt 1):79-94 PMID: 7539842
  32. Neuronal Ca2+ stores: activation and function.
    Trends Neurosci. 1995 Jul;18(7):299-306 PMID: 7571010
  33. Calcium extrusion from mammalian photoreceptor terminals.
    J Neurosci. 1998 Apr 1;18(7):2467-74 PMID: 9502807
  34. Control of transmitter release from retinal amacrine cells by Ca2+ influx and efflux.
    Neuron. 1994 Nov;13(5):1109-17 PMID: 7524563
  35. Identification of a peptide inhibitor of the cardiac sarcolemmal Na(+)-Ca2+ exchanger.
    J Biol Chem. 1991 Jan 15;266(2):1014-20 PMID: 1985930
  36. Calcium-dependent and calcium-independent enhancement of transmitter release at the crayfish neuromuscular junction studied with fura-2 imaging.
    Ann N Y Acad Sci. 1991;635:452-4 PMID: 1683756
  37. A novel antagonist, No. 7943, of the Na+/Ca2+ exchange current in guinea-pig cardiac ventricular cells.
    Br J Pharmacol. 1996 Oct;119(3):555-63 PMID: 8894178
  38. Interplay between sodium and calcium dynamics in granule cell presynaptic terminals.
    Biophys J. 1997 Nov;73(5):2476-88 PMID: 9370441
  39. Sodium/calcium exchange: its physiological implications.
    Physiol Rev. 1999 Jul;79(3):763-854 PMID: 10390518
  40. A quantitative measurement of the dependence of short-term synaptic enhancement on presynaptic residual calcium.
    J Neurosci. 1994 Oct;14(10):5885-902 PMID: 7931551
  41. Residual Ca2+ and short-term synaptic plasticity.
    Nature. 1994 Oct 13;371(6498):603-6 PMID: 7935792
  42. Location of calcium transporters at presynaptic terminals.
    Eur J Neurosci. 2000 Mar;12(3):839-46 PMID: 10762313
  43. Confocal imaging of calcium microdomains and calcium extrusion in turtle hair cells.
    Neuron. 1995 Dec;15(6):1323-35 PMID: 8845156
  44. Presynaptic mechanisms regulating Ca2+ concentration triggering acetylcholine release at an identified neuro-neuronal synapse of Aplysia.
    Neuroscience. 1994 Nov;63(2):405-14 PMID: 7891854
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
2001-12-15
Pages
9598-607
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6763056
Subset
IM
Grants
NINDS NIH HHS · NS 15114 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]