Neuron
Volume 12, Issue 6, June 1994, Pages 1319-1329
Journal home page for Neuron

Article
Angiotensin II inhibits calcium and M current channels in rat sympathetic neurons via G proteins

https://doi.org/10.1016/0896-6273(94)90447-2Get rights and content

Abstract

We characterized inhibition of N-type Ca2+ and M current K+ channels in rat superior cervical ganglion neurons by angiotensin II (angioII) using the patch clamp. Of 120 neurons, 97 showed inhibition of ICa (mean 32%), which was slow in onset and very slow to reverse under whole-cell recording conditions. This inhibition was blocked by the AT1 receptor antagonist losartan, attenuated by inclusion of 2 mM GDP-β-S in the pipette, mostly pertussis toxin insensitive, half-sensitive to N-ethylmaleimide, and wholly voltage independent. With 20 mM instead of 0.1 mM BAPTA in the pipette, the inhibition was strongly attenuated; however, we detected no angioII-induced [Ca2+]i signal using the fluorescent indicator indo-1. IBa from cell-attached patches was reduced by bath-applied angioll (mean 33%), suggesting use of a diffusible cytoplasmic messenger. M currents were inhibited by angioll in 8 of 11 neurons (mean 50%) cultured overnight. Hence, a second agonist, angioll, may share the slow, second messenger-utilizing, pertussis toxin-insensitive signaling pathway used by muscarinic agonists.

References (58)

  • M. Galvan et al.

    Control of calcium current in rat sympathetic neurons by norepinephrine

    Brain Res.

    (1982)
  • B. Hille

    G protein-coupled mechanisms and nervous signaling

    Neuron

    (1992)
  • K.H. Jakobs et al.

    Uncoupling of α-adrenoreceptor-mediated inhibition of human platelet adenylate cyclase by N-ethylmaleimide

    J. Biol. Chem.

    (1982)
  • I. Kojima et al.

    Pertussis toxin blocks angiotensin II-induced calcium influx but not inositol triphosphate production in adrenal glomerulosa cells

    FEBS Lett.

    (1986)
  • D. Lipscombe et al.

    Imaging of cytosolic Ca2+ transients arising from Ca2+ stores and Ca2+ channels in sympathetic neurons

    Neuron

    (1988)
  • A. Mathie et al.

    Inhibition of N- and L-type calcium channels by muscarinic receptor activation in rat sympathetic neurons

    Neuron

    (1992)
  • I.M. Mintz et al.

    P-type calcium channels in rat central and peripheral neurons

    Neuron

    (1992)
  • M.R. Plummer et al.

    Elementary properties and pharmacological sensitivities of calcium channels in mammalian peripheral neurons

    Neuron

    (1989)
  • L.J. Regan et al.

    Ca2+ channels in rat central and peripheral neurons: high-threshold current resistant to dihydropyridine blockers and ω-conotoxin

    Neuron

    (1991)
  • M.S. Shapiro et al.

    Substance P and somatostatin inhibit calcium channels in rat sympathetic neurons via different G protein pathways

    Neuron

    (1993)
  • S.-Y. Song et al.

    Different GTP-binding proteins mediate regulation of calcium channels by acetylcholine and noradrenaline in rat sympathetic neurons

    Brain Res.

    (1989)
  • C. Strömberg et al.

    Angiotensin II AT1 receptors in rat superior cervical ganglia: characterization and stimulation of phosphoinositide hydrolysis

    Eur. J. Pharmacol.

    (1991)
  • P.R. Adams et al.

    Luteinizing hormonereleasing factor and muscarinic agonists act on the same voltagesensitive K+ current in bullfrog sympathetic neurones

    Br. J. Pharmacol.

    (1980)
  • C.M. Armstrong et al.

    Charge movement associated with the opening and closing of the activation gates of the Na channels

    J. Gen. Physiol.

    (1974)
  • B.P. Bean

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

    Nature

    (1989)
  • D.J. Beech et al.

    Intracellular Cal' buffers disrupt muscarinic suppression of Ca2+ current and M current in rat sympathetic neurons

  • L.M. Boland et al.

    Modulation of N-type calcium channels in bullfrog sympathetic neurons by luteinizing hormone-releasing hormone: kinetics and voltage dependence

    J. Neurosci.

    (1993)
  • L.M. Boland et al.

    ω-Conotoxin block of N-type calcium channels in frog and rat sympathetic neurons

    J. Neurosci.

    (1994)
  • K.I. Catt et al.

    Control of glomerulosa cell function by angiotensin II: transduction by G proteins and inositol polyphosphates

    Clin. Exp. Pharmacol. Physiol.

    (1988)
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    Present address: Abteilung Zellphysiologie, Max-Planck-Institut für medizinische Forschung, lahnstrasse 29, D-69120 Heidelberg, Federal Republic of Germany.

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