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. 1989 Jul 1;94(1):151–167. doi: 10.1085/jgp.94.1.151

Calcium currents in bullfrog sympathetic neurons. I. Activation kinetics and pharmacology

PMCID: PMC2228934  PMID: 2478659

Abstract

The calcium current of bullfrog sympathetic neurons activates and deactivates rapidly (tau less than 3 ms). For brief depolarizations, the current can be fit reasonably well by a Hodgkin-Huxley-type model with a single gating particle of charge +3. With 2 mM Ca2+ as the charge carrier, half-maximal activation occurs at approximately -5 mV, near the voltage where activation and deactivation are slowest. When extracellular divalent ion concentrations are reduced, monovalent ions (e.g., Na+ and methylammonium) produce kinetically similar inward currents. Current carried by Ba2+ is blocked by Cd2+ at micromolar concentrations, and by 100 nM omega-conotoxin. Commercially available saxitoxin blocks the current, but different batches have quantitatively different potency. The dihydropyridine agonist Bay K 8644 induces a slight shift in activation kinetics to more negative voltages, with little effect on the peak current. Nifedipine at least partially reverses the effect of Bay K 8644, but has little effect on its own. Muscarinic agonists and other ligands that inhibit the M-type potassium current of frog sympathetic neurons have weak inhibitory effects on the calcium current as well. One interpretation of these results is that the N-type calcium current predominates in these cells, with a minor contribution of L-type current.

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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. Ahmed Z. Expression of membrane currents in rat neocortical neurons in serum-free culture. I. Inward currents. Brain Res. 1988 May 16;468(2):285–295. doi: 10.1016/0165-3806(88)90141-1. [DOI] [PubMed] [Google Scholar]
  3. Bean B. P. Nitrendipine block of cardiac calcium channels: high-affinity binding to the inactivated state. Proc Natl Acad Sci U S A. 1984 Oct;81(20):6388–6392. doi: 10.1073/pnas.81.20.6388. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bean B. P., Sturek M., Puga A., Hermsmeyer K. Calcium channels in muscle cells isolated from rat mesenteric arteries: modulation by dihydropyridine drugs. Circ Res. 1986 Aug;59(2):229–235. doi: 10.1161/01.res.59.2.229. [DOI] [PubMed] [Google Scholar]
  5. Caffrey J. M., Josephson I. R., Brown A. M. Calcium channels of amphibian stomach and mammalian aorta smooth muscle cells. Biophys J. 1986 Jun;49(6):1237–1242. doi: 10.1016/S0006-3495(86)83753-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Docherty R. J. Gadolinium selectively blocks a component of calcium current in rodent neuroblastoma x glioma hybrid (NG108-15) cells. J Physiol. 1988 Apr;398:33–47. doi: 10.1113/jphysiol.1988.sp017027. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Eckert R., Ewald D. Calcium tail currents in voltage-clamped intact nerve cell bodies of Aplysia californica. J Physiol. 1983 Dec;345:533–548. doi: 10.1113/jphysiol.1983.sp014995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Fenwick E. M., Marty A., Neher E. Sodium and calcium channels in bovine chromaffin cells. J Physiol. 1982 Oct;331:599–635. doi: 10.1113/jphysiol.1982.sp014394. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. 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]
  10. HODGKIN A. L., HUXLEY A. F. A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol. 1952 Aug;117(4):500–544. doi: 10.1113/jphysiol.1952.sp004764. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hamill O. P., Marty A., Neher E., Sakmann B., Sigworth F. J. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 1981 Aug;391(2):85–100. doi: 10.1007/BF00656997. [DOI] [PubMed] [Google Scholar]
  12. Hess P., Lansman J. B., Tsien R. W. Different modes of Ca channel gating behaviour favoured by dihydropyridine Ca agonists and antagonists. Nature. 1984 Oct 11;311(5986):538–544. doi: 10.1038/311538a0. [DOI] [PubMed] [Google Scholar]
  13. Hess P., Tsien R. W. Mechanism of ion permeation through calcium channels. 1984 May 31-Jun 6Nature. 309(5967):453–456. doi: 10.1038/309453a0. [DOI] [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. Hoshi T., Rothlein J., Smith S. J. Facilitation of Ca2+-channel currents in bovine adrenal chromaffin cells. Proc Natl Acad Sci U S A. 1984 Sep;81(18):5871–5875. doi: 10.1073/pnas.81.18.5871. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Jones S. W. Luteinizing hormone-releasing hormone as a neurotransmitter in bullfrog sympathetic ganglia. Ann N Y Acad Sci. 1987;519:310–322. doi: 10.1111/j.1749-6632.1987.tb36306.x. [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. 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]
  19. Kay A. R., Wong R. K. Calcium current activation kinetics in isolated pyramidal neurones of the Ca1 region of the mature guinea-pig hippocampus. J Physiol. 1987 Nov;392:603–616. doi: 10.1113/jphysiol.1987.sp016799. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Koketsu K. Modulation of receptor sensitivity and action potentials by transmitters in vertebrate neurones. Jpn J Physiol. 1984;34(6):945–960. doi: 10.2170/jjphysiol.34.945. [DOI] [PubMed] [Google Scholar]
  21. 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]
  22. Lansman J. B., Hess P., Tsien R. W. Blockade of current through single calcium channels by Cd2+, Mg2+, and Ca2+. Voltage and concentration dependence of calcium entry into the pore. J Gen Physiol. 1986 Sep;88(3):321–347. doi: 10.1085/jgp.88.3.321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Lee K. S., Marban E., Tsien R. W. Inactivation of calcium channels in mammalian heart cells: joint dependence on membrane potential and intracellular calcium. J Physiol. 1985 Jul;364:395–411. doi: 10.1113/jphysiol.1985.sp015752. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Lipscombe D., Madison D. V., Poenie M., Reuter H., Tsien R. Y., Tsien R. W. Spatial distribution of calcium channels and cytosolic calcium transients in growth cones and cell bodies of sympathetic neurons. Proc Natl Acad Sci U S A. 1988 Apr;85(7):2398–2402. doi: 10.1073/pnas.85.7.2398. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. McCleskey E. W., Almers W. The Ca channel in skeletal muscle is a large pore. Proc Natl Acad Sci U S A. 1985 Oct;82(20):7149–7153. doi: 10.1073/pnas.82.20.7149. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. 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]
  27. Nerbonne J. M., Gurney A. M. Blockade of Ca2+ and K+ currents in bag cell neurons of Aplysia californica by dihydropyridine Ca2+ antagonists. J Neurosci. 1987 Mar;7(3):882–893. doi: 10.1523/JNEUROSCI.07-03-00882.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. 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]
  29. Swandulla D., Armstrong C. M. Fast-deactivating calcium channels in chick sensory neurons. J Gen Physiol. 1988 Aug;92(2):197–218. doi: 10.1085/jgp.92.2.197. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. 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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