Elsevier

Brain Research Reviews

Volume 16, Issue 3, September–December 1991, Pages 265-281
Brain Research Reviews

Modulation of vertebrate neuronal calcium channels by transmitters

https://doi.org/10.1016/0165-0173(91)90010-6Get rights and content

Abstract

A large number of neurotransmitters have now been shown to reduce the amplitude and slow the activation kinetics of whole cell HVA ICa in a great diversity of neurons. These transmitters include l-glutamate (AMPA/kainate, metabotropic and NMDA receptors), G AB A (via GABAB receptors, NA (via α2 receptors), 5-HT, N A (via α2 receptors), DA and several peptides. Both whole-cell and single-channel studies have demonstrated that the N-channel is the most common channel type to be blocked by transmitters, although an inhibition of the L-type channel has also occasionally been reported. The suppression of the N-type Ca current was commonly shown to be voltage-dependent, with a relief at large positive voltages. Strong evidence has been put forward showing that the transmitter action is mediated by a G-protein, with GDP-β-S blocking transmitter action, and GTP-γ-S directly inhibiting the Ca channel. Moreover, pertussis toxin blocked the transmitter action in most neurons, and following such block, injection of the G-protein G0 restored transmitter action. A direct link between the G-protein and the Ca channel has been widely theorized to mediate the action of transmitters on certain neurons. There is also some evidence that certain transmitters in specific neurons mediate calcium channel inhibition through a 2nd messenger, perhaps protein kinase C.

Transmitters have also been found, although uncommonly, to inhibit HVA L-type and LVA T-type channels. In addition, an enhancement of both HVA and LVA, Ca currents by transmitters has been demonstrated, and substantial evidence exists for mediation of this action by cAMP.

References (178)

  • S.R. Ikeda et al.

    Somatostatin blocks a calcium current in acutely isolated adult rat superior cervical ganglion neurons

    Neurosci. Lett.

    (1987)
  • R.H. Kramer et al.

    Neuropeptide inhibition of voltage-gated channels mediated by mobilization of intracellular calcium

    Neuron

    (1991)
  • R.A.J. Lester et al.

    Quisqualate receptor-mediated depression of calcium currents in hippocampal neurons

    Neuron

    (1990)
  • N. Agopyan et al.

    The effects of PDAc, H-7 and GM-1 on the high threshold slowly inactivating Ca current in the rat hippocampal slices

    Soc. Neurosci. Abstr.

    (1990)
  • T. Akasu et al.

    Reduction of the N-type calcium current by noradrenaline in neurones of rabbit vesical parasympathetic ganglia

    J. Physiol.

    (1990)
  • C.S. Andersen et al.

    Single L-type calcium channels in dorsal root ganglion neurons can be modulated by norepinephrine

    Soc. Neurosci. Abstr.

    (1988)
  • D. Armstrong et al.

    Voltage-activated channels that must be phosphorylated to respond to membrane depolarization

    Proc. Natl. Acad. Sci.

    (1987)
  • B.P. Bean

    Neurotransmitter inhibition of neuronal calcium currents by changes in channel voltage dependence

    Nature

    (1989)
  • B.P. Bean

    Classes of calcium channels in vertebrate cells

    Annu. Rev. Physiol.

    (1989)
  • Beech, J.P., Bernheim, L. and Mille, B., Muscarinic coupling to calcium channels via a diffusible second messenger in...
  • D.J. Beech et al.

    Intracellular Ca buffers disrupt muscarinic suppression of Ca current and M-current in rat sympathetic neuron

  • O. Belluzzi et al.

    Identification of delayed potassium and calcium currents in the rat sympathetic neurone under voltage clamp

    J. Physiol.

    (1985)
  • A.J. Berger et al.

    Serotonin enhances a low voltage activated calcium current in rat spinal motoneurons

    Neuroscience

    (1990)
  • L. Bernheim et al.

    Muscarinic and α-adrenergic suppressions of calcium current are blocked only partially by pertussis toxin in rat sympathetic neurons

    Soc. Neurosci. Abstr.

    (1990)
  • J.L. Bixby et al.

    Enkephalin reduces calcium action potentials in Rohan-Beard neurons in vivo

    J. Neurosci.

    (1983)
  • D. Bleakman et al.

    Bradykinin induced modulation of calcium currents in rat dorsal root ganglion cells

    Mol. Pharmacol.

    (1990)
  • D. Bleakman et al.

    Neuropeptide Y inhibits calcium influx into cultured dorsal root ganglion neurons of the rat via a Y2 receptor

    Br. J. Pharmacol.

    (1991)
  • K.R. Bley et al.

    Neurotransmitter modulation of N-type Ca channels by shifts between modes of gating

    Soc. Neurosci. Abstr.

    (1990)
  • L.M. Boland et al.

    Multiple components of both transient and sustained barium currents in a rat dorsal ganglion cell line

    J. Physiol.

    (1990)
  • L.M. Boland et al.

    Inhibition by bradykinin of voltage activated barium currents in a rat dorsal root ganglion cell Une: role of protein kinase C

    J. Neurosci.

    (1991)
  • D.A. Brown et al.

    Calcium channels in vertebrate neurons: experiments on a neuroblastoma hybrid model

    Ann. NY Acad. Sci.

    (1989)
  • D.R. Canfield et al.

    Pharmacological characterization of amine receptors on embryonic chick sensory neurons,

    Br. J. Pharmacol.

    (1984)
  • M.P. Caulfield et al.

    Pharmacology of the putative M4 muscarinic receptors mediating Ca-current inhibition in neuroblastoma × glioma hybrid (NG 108-15) cells

    Br. J. Pharmacol.

    (1991)
  • C. Chen et al.

    Two types of voltage dependent calcium currents in rat somatotrophs are reduced by somatostatin

    J. Physiol.

    (1990)
  • N.I. Chernevskaya et al.

    NMDA receptor agonists selectively block N-type calcium channels in hippocampal neurons

    Nature

    (1991)
  • Crepel, F., Debono, M.W. and Flores, R., Alpha-adrenergic inhibition of a low-threshold calcium conductance and of a...
  • D.A. Deisz et al.

    g-Aminobutyric acid induced depression of calcium currents of chick sensory neurons

    Neurosci. Lett.

    (1985)
  • M. Desarmenien et al.

    Coexistence of GABAA and GABAB receptors on Aa and C primary afferents

    Br. J. Pharmacol.

    (1984)
  • R.J. Docherty et al.

    Voltage dependent effect of prostaglandin D2 and histamine on calcium currents in adult rat sensory neurons in culture

    Soc. Neurosci. Abstr.

    (1989)
  • R.J. Docherty et al.

    Noradrenaline-induced inhibition of voltage sensitive calcium currents in NG108-15 hybrid cells

    Eur. J. Neurosci.

    (1989)
  • D. Doerner et al.

    Active versus inactive phorbol ester effects of whole cell calcium currents in hippocampal neurons

    Soc. Neurosci. Abstr.

    (1989)
  • D. Doerner et al.

    Diacylglycerol alters hippocampal calcium channel current

    Biophys. J.

    (1990)
  • D. Doerner et al.

    Protein kinase C activators block specific calcium and potassium current components in isolated hippocampal neurons

    J. Neurosci.

    (1988)
  • A.C. Dolphin

    G protein modulation of calcium currents in neurons

    Annu. Rev. Physiol.

    (1990)
  • A.C. Dolphin

    Ca channel currents in rat sensory neurones: interaction between guanine nucleotides, cyclic AMP and Ca channel ligands

    J. Physiol.

    (1991)
  • A.C. Dolphin et al.

    The pharmacology of the GABAB-mediated inhibition of calcium channel currents and transmitter release in cultured rat dorsal root ganglion and cerebellar neurones

    J. Physiol.

    (1990)
  • A.C. Dolphin et al.

    Inhibition of calcium currents in cultured rat dorsal root ganglion neurones by (−)-baclofen

    Br. J. Pharmacol.

    (1986)
  • A.C. Dolphin et al.

    Calcium channel currents and their inhibition by (−)-baclofen in rat sensory neurones: modulation by guanine nucleotides

    J. Physiol.

    (1987)
  • A.C. Dolphin et al.

    Activation of calcium channel currents in rat sensory neurons by large depolarizations: effect of guanine nucleotides and (−)-baclofen

    Eur. J. Neurosci.

    (1990)
  • A.C. Dolphin et al.

    Interaction between calcium channel ligands and guanine nucleotides in cultured rat sensory and sympathetic neurones

    J. Physiol.

    (1989)
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