Home LiteratureArticle Details
PMID: 11069943 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Inositol 1,4,5-trisphosphate (IP3)-mediated Ca2+ release evoked by metabotropic agonists and backpropagating action potentials in hippocampal CA1 pyramidal neurons.

The Journal of neuroscience : the official journal of the Society for Neuroscience ·Vol. 20 ·No. 22 ·2000-11-15 ·Pages 8365-76

Nakamura T, Nakamura K, Lasser-Ross N, Barbara JG, Sandler VM, Ross WN

Abstract

We examined the properties of [Ca(2+)](i) changes that were evoked by backpropagating action potentials in pyramidal neurons in hippocampal slices from the rat. In the presence of the metabotropic glutamate receptor (mGluR) agonists t-ACPD, DHPG, or CHPG, spikes caused Ca(2+) waves that initiated in the proximal apical dendrites and spread over this region and in the soma. Consistent with previously described synaptic responses (Nakamura et al., 1999a), pharmacological experiments established that the waves were attributable to Ca(2+) release from internal stores mediated by the synergistic effect of receptor-mobilized inositol 1,4, 5-trisphosphate (IP(3)) and spike-evoked Ca(2+). The amplitude of the changes reached several micromoles per liter when detected with the low-affinity indicators fura-6F, fura-2-FF, or furaptra. Repetitive brief spike trains at 30-60 sec intervals generated increases of constant amplitude. However, trains at intervals of 10-20 sec evoked smaller increases, suggesting that the stores take 20-30 sec to refill. Release evoked by mGluR agonists was blocked by MCPG, AIDA, 4-CPG, MPEP, and LY367385, a profile consistent with the primacy of group I receptors. At threshold agonist concentrations the release was evoked only in the dendrites; threshold antagonist concentrations were effective only in the soma. Carbachol and 5-HT evoked release with the same spatial distribution as t-ACPD, suggesting that the distribution of neurotransmitter receptors was not responsible for the restricted range of regenerative release. Intracellular BAPTA and EGTA were approximately equally effective in blocking release. Extracellular Cd(2+) blocked release, but no single selective Ca(2+) channel blocker prevented release. These results suggest that IP(3) receptors are not associated closely with specific Ca(2+) channels and are not close to each other.

MeSH Terms
Action Potentials/drug effects,physiology Animals Caffeine/pharmacology Calcium/metabolism Calcium Channel Blockers/pharmacology Calcium Channels/metabolism Calcium Signaling/drug effects Chelating Agents/pharmacology Cycloleucine/analogs & derivatives,pharmacology Dendrites/metabolism Dose-Response Relationship, Drug Egtazic Acid/analogs & derivatives Fluorescent Dyes Hippocampus/cytology,metabolism In Vitro Techniques Inositol 1,4,5-Trisphosphate/metabolism,pharmacology Inositol 1,4,5-Trisphosphate Receptors Pyramidal Cells/cytology,metabolism Rats Rats, Sprague-Dawley Receptors, Cytoplasmic and Nuclear/agonists Receptors, Metabotropic Glutamate/agonists,antagonists & inhibitors
Chemicals
Calcium Channel Blockers Calcium Channels Chelating Agents Fluorescent Dyes Inositol 1,4,5-Trisphosphate Receptors Receptors, Cytoplasmic and Nuclear Receptors, Metabotropic Glutamate Cycloleucine 1-amino-1,3-dicarboxycyclopentane Caffeine Egtazic Acid Inositol 1,4,5-Trisphosphate 1,2-bis(2-aminophenoxy)ethane-N,N,N',N'-tetraacetic acid Calcium
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Nakamura T
Department of Physiology, New York Medical College, Valhalla, New York 10595, USA.
Nakamura K
Lasser-Ross N
Barbara J G
Sandler V M
Ross W N
References (77)
77 references, click to expand
  1. 5-HT receptor classification and nomenclature: towards a harmonization with the human genome.
    Neuropharmacology. 1997 Apr-May;36(4-5):419-28 PMID: 9225265
  2. Release and sequestration of calcium by ryanodine-sensitive stores in rat hippocampal neurones.
    J Physiol. 1997 Jul 1;502 ( Pt 1):13-30 PMID: 9234194
  3. Critical dependence of cAMP response element-binding protein phosphorylation on L-type calcium channels supports a selective response to EPSPs in preference to action potentials.
    J Neurosci. 2000 Jan 1;20(1):266-73 PMID: 10627604
  4. All-or-none Ca2+ release from intracellular stores triggered by Ca2+ influx through voltage-gated Ca2+ channels in rat sensory neurons.
    J Neurosci. 1997 Oct 1;17(19):7404-14 PMID: 9295386
  5. Glutamate-mediated astrocyte-neuron signalling.
    Nature. 1994 Jun 30;369(6483):744-7 PMID: 7911978
  6. A long-lasting calcium-activated nonselective cationic current is generated by synaptic stimulation or exogenous activation of group I metabotropic glutamate receptors in CA1 pyramidal neurons.
    J Neurosci. 1997 Jul 15;17(14):5366-79 PMID: 9204921
  7. Synergistic release of Ca2+ from IP3-sensitive stores evoked by synaptic activation of mGluRs paired with backpropagating action potentials.
    Neuron. 1999 Nov;24(3):727-37 PMID: 10595522
  8. Muscarinic receptor subtype-specific coupling to second messengers in neuronal systems.
    Prog Brain Res. 1993;98:333-40 PMID: 7504312
  9. Omega-conotoxin: direct and persistent blockade of specific types of calcium channels in neurons but not muscle.
    Proc Natl Acad Sci U S A. 1987 Jun;84(12):4327-31 PMID: 2438698
  10. 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
  11. Calcium-induced calcium release contributes to action potential-evoked calcium transients in hippocampal CA1 pyramidal neurons.
    J Neurosci. 1999 Jun 1;19(11):4325-36 PMID: 10341236
  12. Dihydropyridine-sensitive, voltage-gated Ca2+ channels contribute to the resting intracellular Ca2+ concentration of hippocampal CA1 pyramidal neurons.
    J Neurophysiol. 1996 Nov;76(5):3460-70 PMID: 8930286
  13. Identification of serotonin M-receptor subtypes and their specific blockade by a new class of drugs.
    Nature. 1985 Jul 11-17;316(6024):126-31 PMID: 3839291
  14. Muscarinic modulation of spike backpropagation in the apical dendrites of hippocampal CA1 pyramidal neurons.
    J Neurosci. 1997 Aug 1;17(15):5782-91 PMID: 9221776
  15. Caffeine interaction with fluorescent calcium indicator dyes.
    Biophys J. 1999 Jul;77(1):577-86 PMID: 10388782
  16. Adenophostin-medicated quantal Ca2+ release in the purified and reconstituted inositol 1,4,5-trisphosphate receptor type 1.
    FEBS Lett. 1995 Jul 17;368(2):248-52 PMID: 7628615
  17. Pharmacology and functions of metabotropic glutamate receptors.
    Annu Rev Pharmacol Toxicol. 1997;37:205-37 PMID: 9131252
  18. High time resolution fluorescence imaging with a CCD camera.
    J Neurosci Methods. 1991 Feb;36(2-3):253-61 PMID: 2062120
  19. Metabotropic glutamate receptor activation induces calcium waves within hippocampal dendrites.
    J Neurophysiol. 1994 Jul;72(1):471-4 PMID: 7965030
  20. Functional coupling between ryanodine receptors and L-type calcium channels in neurons.
    Nature. 1996 Aug 22;382(6593):719-22 PMID: 8751443
  21. Purified ryanodine receptor from rabbit skeletal muscle is the calcium-release channel of sarcoplasmic reticulum.
    J Gen Physiol. 1988 Jul;92(1):1-26 PMID: 2459298
  22. P-type calcium channels blocked by the spider toxin omega-Aga-IVA.
    Nature. 1992 Feb 27;355(6363):827-9 PMID: 1311418
  23. Distribution of alpha 1a-, alpha 1b- and alpha 1d-adrenergic receptor mRNA in the rat brain and spinal cord.
    J Chem Neuroanat. 1997 Jul;13(2):115-39 PMID: 9285356
  24. Three types of voltage-dependent calcium current in cultured rat hippocampal neurons.
    Brain Res. 1989 Aug 28;495(2):329-36 PMID: 2548673
  25. The spread of Na+ spikes determines the pattern of dendritic Ca2+ entry into hippocampal neurons.
    Nature. 1992 May 21;357(6375):244-6 PMID: 1350327
  26. Caffeine inhibits inositol trisphosphate-mediated liberation of intracellular calcium in Xenopus oocytes.
    J Physiol. 1991 Feb;433:229-40 PMID: 1844813
  27. Adenophostins, newly discovered metabolites of Penicillium brevicompactum, act as potent agonists of the inositol 1,4,5-trisphosphate receptor.
    J Biol Chem. 1994 Jan 7;269(1):369-72 PMID: 8276820
  28. Pattern and inhibition-dependent invasion of pyramidal cell dendrites by fast spikes in the hippocampus in vivo.
    Proc Natl Acad Sci U S A. 1996 Sep 3;93(18):9921-5 PMID: 8790432
  29. Local positive feedback by calcium in the propagation of intracellular calcium waves.
    Biophys J. 1995 Nov;69(5):1683-97 PMID: 8580312
  30. T-jump study of calcium binding kinetics of calcium chelators.
    Cell Calcium. 1997 Oct;22(4):255-68 PMID: 9481476
  31. Microscopic properties of elementary Ca2+ release sites in non-excitable cells.
    Curr Biol. 2000 Jan 13;10(1):8-15 PMID: 10660296
  32. Ryanodine modifies conductance and gating behavior of single Ca2+ release channel.
    Am J Physiol. 1987 Sep;253(3 Pt 1):C364-8 PMID: 2443015
  33. Differential regional and cellular distribution of dopamine D2-like receptors: an immunocytochemical study of subtype-specific antibodies in rat and human brain.
    J Comp Neurol. 1998 Dec 21;402(3):353-71 PMID: 9853904
  34. 2-Methyl-6-(phenylethynyl)-pyridine (MPEP), a potent, selective and systemically active mGlu5 receptor antagonist.
    Neuropharmacology. 1999 Oct;38(10):1493-503 PMID: 10530811
  35. Threshold for inositol 1,4,5-trisphosphate action.
    J Biol Chem. 1996 May 24;271(21):12287-93 PMID: 8647828
  36. Perisynaptic location of metabotropic glutamate receptors mGluR1 and mGluR5 on dendrites and dendritic spines in the rat hippocampus.
    Eur J Neurosci. 1996 Jul;8(7):1488-500 PMID: 8758956
  37. A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons.
    Science. 1997 Jan 10;275(5297):209-13 PMID: 8985013
  38. Inositol 1,4,5-trisphosphate (IP3)-mediated Ca2+ release evoked by metabotropic agonists and backpropagating action potentials in hippocampal CA1 pyramidal neurons.
    J Neurosci. 2000 Nov 15;20(22):8365-76 PMID: 11069943
  39. Evidence for multiple types of Ca2+ channels in acutely isolated hippocampal CA3 neurones of the guinea-pig.
    J Physiol. 1991 Feb;433:259-81 PMID: 1668752
  40. Neuromodulation of dendritic action potentials.
    J Neurophysiol. 1999 Jan;81(1):408-11 PMID: 9914302
  41. Serotonin modulates spike backpropagation and associated [Ca2+]i changes in the apical dendrites of hippocampal CA1 pyramidal neurons.
    J Neurophysiol. 1999 Jan;81(1):216-24 PMID: 9914282
  42. Distribution of metabotropic glutamate receptor mGluR5 immunoreactivity in rat brain.
    J Comp Neurol. 1995 May 8;355(3):455-69 PMID: 7636025
  43. A characterization of muscarinic receptor-mediated intracellular Ca2+ mobilization in cultured rat hippocampal neurones.
    J Physiol. 1998 Sep 15;511 ( Pt 3):747-59 PMID: 9714857
  44. Calcium transients in cerebellar Purkinje neurons evoked by intracellular stimulation.
    J Neurophysiol. 1992 Oct;68(4):1167-77 PMID: 1432076
  45. Activity-dependent action potential invasion and calcium influx into hippocampal CA1 dendrites.
    Science. 1995 Apr 14;268(5208):297-300 PMID: 7716524
  46. Homer binds a novel proline-rich motif and links group 1 metabotropic glutamate receptors with IP3 receptors.
    Neuron. 1998 Oct;21(4):717-26 PMID: 9808459
  47. Molecular mechanisms of intracellular calcium excitability in X. laevis oocytes.
    Cell. 1992 Apr 17;69(2):283-94 PMID: 1568248
  48. Muscarinic receptor subtypes.
    Annu Rev Pharmacol Toxicol. 1990;30:633-73 PMID: 2188581
  49. Immunohistochemical localization of a metabotropic glutamate receptor, mGluR5, in the rat brain.
    Neurosci Lett. 1993 Nov 26;163(1):53-7 PMID: 8295733
  50. Alien intracellular calcium chelators attenuate neurotransmitter release at the squid giant synapse.
    J Neurosci. 1991 Jun;11(6):1496-507 PMID: 1675264
  51. An IP3-assisted form of Ca2+-induced Ca2+ release in neocortical neurons.
    Neuroreport. 2000 Feb 28;11(3):535-9 PMID: 10718310
  52. Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs.
    Science. 1997 Jan 10;275(5297):213-5 PMID: 8985014
  53. Clustering of L-type Ca2+ channels at the base of major dendrites in hippocampal pyramidal neurons.
    Nature. 1990 Sep 20;347(6290):281-4 PMID: 2169591
  54. Ca2+ buffering and action potential-evoked Ca2+ signaling in dendrites of pyramidal neurons.
    Biophys J. 1996 Feb;70(2):1069-81 PMID: 8789126
  55. Fluorescent indicators for Ca2+ based on green fluorescent proteins and calmodulin.
    Nature. 1997 Aug 28;388(6645):882-7 PMID: 9278050
  56. The inositol trisphosphate calcium channel is inactivated by inositol trisphosphate.
    Nature. 1994 Aug 11;370(6489):474-7 PMID: 8047168
  57. Examination of TEA-induced synaptic enhancement in area CA1 of the hippocampus: the role of voltage-dependent Ca2+ channels in the induction of LTP.
    J Neurosci. 1993 Feb;13(2):568-76 PMID: 8381168
  58. IPSPs modulate spike backpropagation and associated [Ca2+]i changes in the dendrites of hippocampal CA1 pyramidal neurons.
    J Neurophysiol. 1996 Nov;76(5):2896-906 PMID: 8930242
  59. Signaling from synapse to nucleus: postsynaptic CREB phosphorylation during multiple forms of hippocampal synaptic plasticity.
    Neuron. 1996 Jan;16(1):89-101 PMID: 8562094
  60. Comparative localization of serotonin1A, 1C, and 2 receptor subtype mRNAs in rat brain.
    J Comp Neurol. 1995 Jan 16;351(3):357-73 PMID: 7706547
  61. Muscarinic receptor subtypes involved in hippocampal circuits.
    Life Sci. 1999;64(6-7):501-9 PMID: 10069516
  62. Cyclopiazonic acid is a specific inhibitor of the Ca2+-ATPase of sarcoplasmic reticulum.
    J Biol Chem. 1989 Oct 25;264(30):17816-23 PMID: 2530215
  63. Pharmacological agents acting at subtypes of metabotropic glutamate receptors.
    Neuropharmacology. 1999 Oct;38(10):1431-76 PMID: 10530808
  64. Initiation of IP(3)-mediated Ca(2+) waves in Xenopus oocytes.
    EMBO J. 1999 Oct 1;18(19):5285-99 PMID: 10508162
  65. Serotonin reuptake inhibitor fluoxetine decreases arteriolar myogenic tone by reducing smooth muscle [Ca2+]i.
    J Cardiovasc Pharmacol. 2000 Jun;35(6):849-54 PMID: 10836717
  66. Competitive, reversible, and potent antagonism of inositol 1,4,5-trisphosphate-activated calcium release by heparin.
    J Biol Chem. 1988 Aug 15;263(23):11075-9 PMID: 3136153
  67. Heparin inhibits the inositol 1,4,5-trisphosphate-dependent, but not the independent, calcium release induced by guanine nucleotide in vascular smooth muscle.
    Biochem Biophys Res Commun. 1988 Jun 16;153(2):625-31 PMID: 3132916
  68. Frequency-dependent propagation of sodium action potentials in dendrites of hippocampal CA1 pyramidal neurons.
    J Neurophysiol. 1995 Oct;74(4):1395-403 PMID: 8989380
  69. Characterization of single voltage-gated Na+ and Ca2+ channels in apical dendrites of rat CA1 pyramidal neurons.
    J Physiol. 1995 Aug 15;487(1):67-90 PMID: 7473260
  70. Intracellular injections of EGTA block induction of hippocampal long-term potentiation.
    Nature. 1983 Oct 20-26;305(5936):719-21 PMID: 6415483
  71. The sarcoplasmic reticulum Ca2+ channel/ryanodine receptor: modulation by endogenous effectors, drugs and disease states.
    Pharmacol Rev. 1997 Mar;49(1):1-51 PMID: 9085308
  72. The site for initiation of action potential discharge over the somatodendritic axis of rat hippocampal CA1 pyramidal neurons.
    J Neurosci. 1991 Jul;11(7):2270-80 PMID: 2066782
  73. Group I mGluR activation causes voltage-dependent and -independent Ca2+ rises in hippocampal pyramidal cells.
    J Neurophysiol. 1999 Jun;81(6):2903-13 PMID: 10368407
  74. Differential sensitivity to intracellular pH among high- and low-threshold Ca2+ currents in isolated rat CA1 neurons.
    J Neurophysiol. 1997 Feb;77(2):639-53 PMID: 9065837
  75. Released fraction and total size of a pool of immediately available transmitter quanta at a calyx synapse.
    Neuron. 1999 Jun;23(2):399-409 PMID: 10399944
  76. (RS)-2-chloro-5-hydroxyphenylglycine (CHPG) activates mGlu5, but no mGlu1, receptors expressed in CHO cells and potentiates NMDA responses in the hippocampus.
    Neuropharmacology. 1997 Feb;36(2):265-7 PMID: 9144665
  77. Different Ca2+ channels in soma and dendrites of hippocampal pyramidal neurons mediate spike-induced Ca2+ influx.
    J Neurophysiol. 1995 Jun;73(6):2553-7 PMID: 7666160
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
2000-11-15
Pages
8365-76
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6773168
Subset
IM
Grants
NINDS NIH HHS · R01 NS016295 · United States
NINDS NIH HHS · R56 NS016295 · United States
NINDS NIH HHS · NS16295 · United States
External Links
PubMed source PMC Full Text View journal details
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]

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2