Abstract
The M-type potassium current and the N-type calcium current are inhibited by several different neurotransmitters in frog sympathetic neurons. These effects seem to be mediated via G proteins, but it is not clear whether diffusible second messengers are involved. Using a rapid (approximately 100 ms) flow tube perfusion system to apply agonists, the inhibition of calcium current develops and recovers rapidly but not instantaneously (t1/2 = 1-2 s). M-current inhibition is considerably slower, with t1/2 approximately 30 s for recovery from inhibition. At least for M-current inhibition, there appears to be sufficient time for involvement of an enzymatic cascade in receptor-channel coupling.
Full text
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Selected References
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- Adams P. R., Brown D. A., Constanti A. Pharmacological inhibition of the M-current. J Physiol. 1982 Nov;332:223–262. doi: 10.1113/jphysiol.1982.sp014411. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Adams P. R., Brown D. A., Jones S. W. Substance P inhibits the M-current in bullfrog sympathetic neurones. Br J Pharmacol. 1983 Jun;79(2):330–333. doi: 10.1111/j.1476-5381.1983.tb11004.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Adams P. R., Brown D. A. Synaptic inhibition of the M-current: slow excitatory post-synaptic potential mechanism in bullfrog sympathetic neurones. J Physiol. 1982 Nov;332:263–272. doi: 10.1113/jphysiol.1982.sp014412. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Akasu T. Adrenaline depolarization in paravertebral sympathetic neurones of bullfrogs. Pflugers Arch. 1988 Jan;411(1):80–87. doi: 10.1007/BF00581650. [DOI] [PubMed] [Google Scholar]
- Bean B. P. Neurotransmitter inhibition of neuronal calcium currents by changes in channel voltage dependence. Nature. 1989 Jul 13;340(6229):153–156. doi: 10.1038/340153a0. [DOI] [PubMed] [Google Scholar]
- Beech D. J., Bernheim L., Mathie A., Hille B. Intracellular Ca2+ buffers disrupt muscarinic suppression of Ca2+ current and M current in rat sympathetic neurons. Proc Natl Acad Sci U S A. 1991 Jan 15;88(2):652–656. doi: 10.1073/pnas.88.2.652. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bley K. R., Tsien R. W. Inhibition of Ca2+ and K+ channels in sympathetic neurons by neuropeptides and other ganglionic transmitters. Neuron. 1990 Mar;4(3):379–391. doi: 10.1016/0896-6273(90)90050-p. [DOI] [PubMed] [Google Scholar]
- Bosma M. M., Hille B. Protein kinase C is not necessary for peptide-induced suppression of M current or for desensitization of the peptide receptors. Proc Natl Acad Sci U S A. 1989 Apr;86(8):2943–2947. doi: 10.1073/pnas.86.8.2943. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Breitwieser G. E., Szabo G. Mechanism of muscarinic receptor-induced K+ channel activation as revealed by hydrolysis-resistant GTP analogues. J Gen Physiol. 1988 Apr;91(4):469–493. doi: 10.1085/jgp.91.4.469. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brown A. M., Birnbaumer L. Ionic channels and their regulation by G protein subunits. Annu Rev Physiol. 1990;52:197–213. doi: 10.1146/annurev.ph.52.030190.001213. [DOI] [PubMed] [Google Scholar]
- Brown D. A., Adams P. R. Effects of phorbol dibutyrate on M currents and M current inhibition in bullfrog sympathetic neurons. Cell Mol Neurobiol. 1987 Sep;7(3):255–269. doi: 10.1007/BF00711303. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brown D. A., Marrion N. V., Smart T. G. On the transduction mechanism for muscarine-induced inhibition of M-current in cultured rat sympathetic neurones. J Physiol. 1989 Jun;413:469–488. doi: 10.1113/jphysiol.1989.sp017664. [DOI] [PMC free article] [PubMed] [Google Scholar]
- DEL CASTILLO J., KATZ B. Production of membrane potential changes in the frog's heart by inhibitory nerve impulses. Nature. 1955 Jun 11;175(4467):1035–1035. doi: 10.1038/1751035a0. [DOI] [PubMed] [Google Scholar]
- Elmslie K. S., Zhou W., Jones S. W. LHRH and GTP-gamma-S modify calcium current activation in bullfrog sympathetic neurons. Neuron. 1990 Jul;5(1):75–80. doi: 10.1016/0896-6273(90)90035-e. [DOI] [PubMed] [Google Scholar]
- Hartzell H. C., Kuffler S. W., Stickgold R., Yoshikami D. Synaptic excitation and inhibition resulting from direct action of acetylcholine on two types of chemoreceptors on individual amphibian parasympathetic neurones. J Physiol. 1977 Oct;271(3):817–846. doi: 10.1113/jphysiol.1977.sp012027. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hill-Smith I., Purves R. D. Synaptic delay in the heart: an ionophoretic study. J Physiol. 1978 Jun;279:31–54. doi: 10.1113/jphysiol.1978.sp012329. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jan L. Y., Jan Y. N. Peptidergic transmission in sympathetic ganglia of the frog. J Physiol. 1982 Jun;327:219–246. doi: 10.1113/jphysiol.1982.sp014228. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jones S. W., Adams P. R., Brownstein M. J., Rivier J. E. Teleost luteinizing hormone-releasing hormone: action on bullfrog sympathetic ganglia is consistent with role as neurotransmitter. J Neurosci. 1984 Feb;4(2):420–429. doi: 10.1523/JNEUROSCI.04-02-00420.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jones S. W. Chicken II luteinizing hormone-releasing hormone inhibits the M-current of bullfrog sympathetic neurons. Neurosci Lett. 1987 Sep 23;80(2):180–184. doi: 10.1016/0304-3940(87)90650-1. [DOI] [PubMed] [Google Scholar]
- Jones S. W., Jacobs L. S. Dihydropyridine actions on calcium currents of frog sympathetic neurons. J Neurosci. 1990 Jul;10(7):2261–2267. doi: 10.1523/JNEUROSCI.10-07-02261.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jones S. W., Marks T. N. Calcium currents in bullfrog sympathetic neurons. I. Activation kinetics and pharmacology. J Gen Physiol. 1989 Jul;94(1):151–167. doi: 10.1085/jgp.94.1.151. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jones S. W., Marks T. N. Calcium currents in bullfrog sympathetic neurons. II. Inactivation. J Gen Physiol. 1989 Jul;94(1):169–182. doi: 10.1085/jgp.94.1.169. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jones S. W. On the resting potential of isolated frog sympathetic neurons. Neuron. 1989 Aug;3(2):153–161. doi: 10.1016/0896-6273(89)90028-7. [DOI] [PubMed] [Google Scholar]
- Jones S. W. Sodium currents in dissociated bull-frog sympathetic neurones. J Physiol. 1987 Aug;389:605–627. doi: 10.1113/jphysiol.1987.sp016674. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Katayama Y., Nishi S. Voltage-clamp analysis of peptidergic slow depolarizations in bullfrog sympathetic ganglion cells. J Physiol. 1982 Dec;333:305–313. doi: 10.1113/jphysiol.1982.sp014455. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kuba K., Koketsu K. Synaptic events in sympathetic ganglia. Prog Neurobiol. 1978;11(2):77–169. doi: 10.1016/0301-0082(78)90010-2. [DOI] [PubMed] [Google Scholar]
- Kuffler S. W., Sejnowski T. J. Peptidergic and muscarinic excitation at amphibian sympathetic synapses. J Physiol. 1983 Aug;341:257–278. doi: 10.1113/jphysiol.1983.sp014805. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lipscombe D., Kongsamut S., Tsien R. W. Alpha-adrenergic inhibition of sympathetic neurotransmitter release mediated by modulation of N-type calcium-channel gating. Nature. 1989 Aug 24;340(6235):639–642. doi: 10.1038/340639a0. [DOI] [PubMed] [Google Scholar]
- Nargeot J., Lester H. A., Birdsall N. J., Stockton J., Wassermann N. H., Erlanger B. F. A photoisomerizable muscarinic antagonist. Studies of binding and of conductance relaxations in frog heart. J Gen Physiol. 1982 Apr;79(4):657–678. doi: 10.1085/jgp.79.4.657. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nargeot J., Nerbonne J. M., Engels J., Lester H. A. Time course of the increase in the myocardial slow inward current after a photochemically generated concentration jump of intracellular cAMP. Proc Natl Acad Sci U S A. 1983 Apr;80(8):2395–2399. doi: 10.1073/pnas.80.8.2395. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nicoll R. A. The coupling of neurotransmitter receptors to ion channels in the brain. Science. 1988 Jul 29;241(4865):545–551. doi: 10.1126/science.2456612. [DOI] [PubMed] [Google Scholar]
- North R. A., Tokimasa T. The time course of muscarinic depolarization of guinea-pig myenteric neurones. Br J Pharmacol. 1984 May;82(1):85–91. doi: 10.1111/j.1476-5381.1984.tb16444.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nowycky M. C., Fox A. P., Tsien R. W. Three types of neuronal calcium channel with different calcium agonist sensitivity. Nature. 1985 Aug 1;316(6027):440–443. doi: 10.1038/316440a0. [DOI] [PubMed] [Google Scholar]
- Pfaffinger P. J., Leibowitz M. D., Subers E. M., Nathanson N. M., Almers W., Hille B. Agonists that suppress M-current elicit phosphoinositide turnover and Ca2+ transients, but these events do not explain M-current suppression. Neuron. 1988 Aug;1(6):477–484. doi: 10.1016/0896-6273(88)90178-x. [DOI] [PubMed] [Google Scholar]
- Pfaffinger P. Muscarine and t-LHRH suppress M-current by activating an IAP-insensitive G-protein. J Neurosci. 1988 Sep;8(9):3343–3353. doi: 10.1523/JNEUROSCI.08-09-03343.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Plummer M. R., Logothetis D. E., Hess P. Elementary properties and pharmacological sensitivities of calcium channels in mammalian peripheral neurons. Neuron. 1989 May;2(5):1453–1463. doi: 10.1016/0896-6273(89)90191-8. [DOI] [PubMed] [Google Scholar]
- Selyanko A. A., Smith P. A., Zidichouski J. A. Effects of muscarine and adrenaline on neurones from Rana pipiens sympathetic ganglia. J Physiol. 1990 Jun;425:471–500. doi: 10.1113/jphysiol.1990.sp018114. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Stewart G. N. The Influence of Temperature and of Endocardiac Pressure on the Heart, and perticularly on the Action of the Vagus and Cardiac Sympathetic Nerves. J Physiol. 1892 Feb;13(1-2):59–164.16. doi: 10.1113/jphysiol.1892.sp000401. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yellen G. Single Ca2+-activated nonselective cation channels in neuroblastoma. Nature. 1982 Mar 25;296(5855):357–359. doi: 10.1038/296357a0. [DOI] [PubMed] [Google Scholar]