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. 1992 Oct;456:107–123. doi: 10.1113/jphysiol.1992.sp019329

Calcium current modulation in frog sympathetic neurones: L-current is relatively insensitive to neurotransmitters.

K S Elmslie 1, P J Kammermeier 1, S W Jones 1
PMCID: PMC1175674  PMID: 1363436

Abstract

1. Neurotransmitters (noradrenaline, NA; chicken II luteinizing hormone-releasing hormone, LHRH) and activators of G proteins (GTP-gamma-S and AlF3) partially inhibit calcium current in bullfrog sympathetic neruones. Activation of the remaining current is slowed and shifted to more positive voltages. 2. The N-type calcium current appears to be the type modulated, since approximately 90% of peak current is blocked by omega-conotoxin (omega CgTx) and modulation is not affected by nisoldipine. 3. Calcium current at relatively negative voltages (-30 to -50 mV) is resistant to transmitter modulation. The current at such voltages is also resistant to omega CgTx, suggesting that it results from a different type of calcium channel. 4. The omega CgTx-resistant current includes dihydropyridine (DHP)-sensitive and DHP-resistant components. The omega CgTx- and DHP-resistant current is inhibited by transmitter agonist, but the DHP-sensitive (L-type) current is not. 5. In cells dialysed with a low concentration of calcium buffer (0.1 mM-BAPTA), transmitters still inhibit N-current incompletely. However, L-current was partially inhibited (approximately 10%) by LHRH, NA and the muscarinic agonist oxotremorine-M (OXO-M).

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Selected References

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  1. Adams P. R., Jones S. W., Pennefather P., Brown D. A., Koch C., Lancaster B. Slow synaptic transmission in frog sympathetic ganglia. J Exp Biol. 1986 Sep;124:259–285. doi: 10.1242/jeb.124.1.259. [DOI] [PubMed] [Google Scholar]
  2. Aosaki T., Kasai H. Characterization of two kinds of high-voltage-activated Ca-channel currents in chick sensory neurons. Differential sensitivity to dihydropyridines and omega-conotoxin GVIA. Pflugers Arch. 1989 Jun;414(2):150–156. doi: 10.1007/BF00580957. [DOI] [PubMed] [Google Scholar]
  3. 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]
  4. Belles B., Malécot C. O., Hescheler J., Trautwein W. "Run-down" of the Ca current during long whole-cell recordings in guinea pig heart cells: role of phosphorylation and intracellular calcium. Pflugers Arch. 1988 Apr;411(4):353–360. doi: 10.1007/BF00587713. [DOI] [PubMed] [Google Scholar]
  5. Bernheim L., Beech D. J., Hille B. A diffusible second messenger mediates one of the pathways coupling receptors to calcium channels in rat sympathetic neurons. Neuron. 1991 Jun;6(6):859–867. doi: 10.1016/0896-6273(91)90226-p. [DOI] [PubMed] [Google Scholar]
  6. 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]
  7. Carbone E., Formenti A., Pollo A. Multiple actions of Bay K 8644 on high-threshold Ca channels in adult rat sensory neurons. Neurosci Lett. 1990 Apr 6;111(3):315–320. doi: 10.1016/0304-3940(90)90281-d. [DOI] [PubMed] [Google Scholar]
  8. Chad J. E., Eckert R. An enzymatic mechanism for calcium current inactivation in dialysed Helix neurones. J Physiol. 1986 Sep;378:31–51. doi: 10.1113/jphysiol.1986.sp016206. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Chen C. F., Hess P. Mechanism of gating of T-type calcium channels. J Gen Physiol. 1990 Sep;96(3):603–630. doi: 10.1085/jgp.96.3.603. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Elmslie K. S. Calcium current modulation in frog sympathetic neurones: multiple neurotransmitters and G proteins. J Physiol. 1992;451:229–246. doi: 10.1113/jphysiol.1992.sp019162. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. 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]
  12. Fox A. P., Nowycky M. C., Tsien R. W. Kinetic and pharmacological properties distinguishing three types of calcium currents in chick sensory neurones. J Physiol. 1987 Dec;394:149–172. doi: 10.1113/jphysiol.1987.sp016864. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gross R. A., Macdonald R. L. Dynorphin A selectively reduces a large transient (N-type) calcium current of mouse dorsal root ganglion neurons in cell culture. Proc Natl Acad Sci U S A. 1987 Aug;84(15):5469–5473. doi: 10.1073/pnas.84.15.5469. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hirning L. D., Fox A. P., McCleskey E. W., Olivera B. M., Thayer S. A., Miller R. J., Tsien R. W. Dominant role of N-type Ca2+ channels in evoked release of norepinephrine from sympathetic neurons. Science. 1988 Jan 1;239(4835):57–61. doi: 10.1126/science.2447647. [DOI] [PubMed] [Google Scholar]
  15. Jan L. Y., Jan Y. N. Voltage-sensitive ion channels. Cell. 1989 Jan 13;56(1):13–25. doi: 10.1016/0092-8674(89)90979-3. [DOI] [PubMed] [Google Scholar]
  16. 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]
  17. 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]
  18. 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]
  19. 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]
  20. Jones S. W. Time course of receptor-channel coupling in frog sympathetic neurons. Biophys J. 1991 Aug;60(2):502–507. doi: 10.1016/S0006-3495(91)82077-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kasai H., Aosaki T., Fukuda J. Presynaptic Ca-antagonist omega-conotoxin irreversibly blocks N-type Ca-channels in chick sensory neurons. Neurosci Res. 1987 Feb;4(3):228–235. doi: 10.1016/0168-0102(87)90014-9. [DOI] [PubMed] [Google Scholar]
  22. 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]
  23. 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]
  24. Marchetti C., Robello M. Guanosine-5'-O-(3-thiotriphosphate) modifies kinetics of voltage-dependent calcium current in chick sensory neurons. Biophys J. 1989 Dec;56(6):1267–1272. doi: 10.1016/S0006-3495(89)82774-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. McCleskey E. W., Fox A. P., Feldman D. H., Cruz L. J., Olivera B. M., Tsien R. W., Yoshikami D. 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):4327–4331. doi: 10.1073/pnas.84.12.4327. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Mori Y., Friedrich T., Kim M. S., Mikami A., Nakai J., Ruth P., Bosse E., Hofmann F., Flockerzi V., Furuichi T. Primary structure and functional expression from complementary DNA of a brain calcium channel. Nature. 1991 Apr 4;350(6317):398–402. doi: 10.1038/350398a0. [DOI] [PubMed] [Google Scholar]
  27. 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]
  28. Plummer M. R., Hess P. Reversible uncoupling of inactivation in N-type calcium channels. Nature. 1991 Jun 20;351(6328):657–659. doi: 10.1038/351657a0. [DOI] [PubMed] [Google Scholar]
  29. 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]
  30. Plummer M. R., Rittenhouse A., Kanevsky M., Hess P. Neurotransmitter modulation of calcium channels in rat sympathetic neurons. J Neurosci. 1991 Aug;11(8):2339–2348. doi: 10.1523/JNEUROSCI.11-08-02339.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Regan L. J., Sah D. W., Bean B. P. Ca2+ channels in rat central and peripheral neurons: high-threshold current resistant to dihydropyridine blockers and omega-conotoxin. Neuron. 1991 Feb;6(2):269–280. doi: 10.1016/0896-6273(91)90362-4. [DOI] [PubMed] [Google Scholar]
  32. Song S. Y., Saito K., Noguchi K., Konishi S. Adrenergic and cholinergic inhibition of Ca2+ channels mediated by different GTP-binding proteins in rat sympathetic neurones. Pflugers Arch. 1991 Jul;418(6):592–600. doi: 10.1007/BF00370576. [DOI] [PubMed] [Google Scholar]
  33. Tsien R. W., Lipscombe D., Madison D. V., Bley K. R., Fox A. P. Multiple types of neuronal calcium channels and their selective modulation. Trends Neurosci. 1988 Oct;11(10):431–438. doi: 10.1016/0166-2236(88)90194-4. [DOI] [PubMed] [Google Scholar]
  34. Wanke E., Ferroni A., Malgaroli A., Ambrosini A., Pozzan T., Meldolesi J. Activation of a muscarinic receptor selectively inhibits a rapidly inactivated Ca2+ current in rat sympathetic neurons. Proc Natl Acad Sci U S A. 1987 Jun;84(12):4313–4317. doi: 10.1073/pnas.84.12.4313. [DOI] [PMC free article] [PubMed] [Google Scholar]

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