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. 1991 Aug;439:181–214. doi: 10.1113/jphysiol.1991.sp018663

Double-pulse calcium channel current facilitation in adult rat sympathetic neurones.

S R Ikeda 1
PMCID: PMC1180105  PMID: 1654413

Abstract

1. Double-pulse facilitation of Ca2+ channel currents in enzymatically dispersed adult rat superior cervical ganglion neurones was investigated using the whole-cell variant of the patch-clamp technique. Voltage-clamp recordings were performed at room temperature (21-24 degrees C) in solutions designed to isolate Ca2+ channel currents. 2. Ba2+ currents, elicited by a 0 mV test pulse, were increased in amplitude when preceded by a 40 ms pulse to voltages greater than 0 mV. The magnitude of facilitation was dependent on pre-pulse voltage and reached a maximum of 50% (i.e. 1.5 x the current amplitude elicited without a pre-pulse) at a pre-pulse voltage of +80 mV. Half-maximal facilitation occurred at about +25 mV. A small decrease (-6%) in test pulse amplitude was present at pre-pulse voltages between -40 and 0 mV. The magnitude of facilitation was also dependent on test pulse voltage. Facilitation was greatest between test pulse voltages of -10 and 0 mV. 3. Facilitation slowly decreased during prolonged (1 h) dialysis of the neurone even though the Ba2+ current amplitude was well maintained. 4. Increasing the pre-pulse duration over the range 0-120 ms produced an exponential increase in facilitation with a time constant of 17.3 ms. Conversely, lengthening the interpulse duration over the range 5-915 ms, while maintaining a constant pre-pulse amplitude and duration, resulted in an exponential decrease in facilitation with a time constant of 197 ms. 5. At a test potential of 0 mV, the decay of the facilitated Ba2+ current component was fitted to a double exponential function with time constants of about 25 and 150 ms. The time constants had little pre-pulse voltage dependence between +30 to +80 mV. 6. The initial rising phase of both the control and facilitated Ba2+ current were reasonably well described by a single exponential (tau rise) after a delay of 300 microseconds. The tau rise versus test pulse potential relationship was 'bell shaped' over the test pulse voltage of -20 to +30 mV reaching a maximum near -5 mV. tau rise was similar for control and facilitated currents except at potentials greater than +10 mV where the rise of the facilitated current was accelerated. 7. Control and facilitated activation curves, as derived from tail current amplitudes, were described by the sum of two Boltzmann functions. A facilitating pre-pulse produced an increase in the proportion of the current contributed by the component activated at more hyperpolarized test potentials.(ABSTRACT TRUNCATED AT 400 WORDS)

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  1. 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]
  2. Artalejo C. R., Ariano M. A., Perlman R. L., Fox A. P. Activation of facilitation calcium channels in chromaffin cells by D1 dopamine receptors through a cAMP/protein kinase A-dependent mechanism. Nature. 1990 Nov 15;348(6298):239–242. doi: 10.1038/348239a0. [DOI] [PubMed] [Google Scholar]
  3. 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]
  4. Belluzzi O., Sacchi O. A quantitative description of the sodium current in the rat sympathetic neurone. J Physiol. 1986 Nov;380:275–291. doi: 10.1113/jphysiol.1986.sp016285. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Belluzzi O., Sacchi O. Calcium currents in the normal adult rat sympathetic neurone. J Physiol. 1989 May;412:493–512. doi: 10.1113/jphysiol.1989.sp017628. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bourne H. R., Sanders D. A., McCormick F. The GTPase superfamily: a conserved switch for diverse cell functions. Nature. 1990 Nov 8;348(6297):125–132. doi: 10.1038/348125a0. [DOI] [PubMed] [Google Scholar]
  7. Carbone E., Sher E., Clementi F. Ca currents in human neuroblastoma IMR32 cells: kinetics, permeability and pharmacology. Pflugers Arch. 1990 Apr;416(1-2):170–179. doi: 10.1007/BF00370239. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. Eckert R., Chad J. E. Inactivation of Ca channels. Prog Biophys Mol Biol. 1984;44(3):215–267. doi: 10.1016/0079-6107(84)90009-9. [DOI] [PubMed] [Google Scholar]
  10. Eckert R., Ewald D. Inactivation of calcium conductance characterized by tail current measurements in neurones of Aplysia californica. J Physiol. 1983 Dec;345:549–565. doi: 10.1113/jphysiol.1983.sp014996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Eckstein F., Cassel D., Levkovitz H., Lowe M., Selinger Z. Guanosine 5'-O-(2-thiodiphosphate). An inhibitor of adenylate cyclase stimulation by guanine nucleotides and fluoride ions. J Biol Chem. 1979 Oct 10;254(19):9829–9834. [PubMed] [Google Scholar]
  12. 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]
  13. 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]
  14. Forscher P., Oxford G. S. Modulation of calcium channels by norepinephrine in internally dialyzed avian sensory neurons. J Gen Physiol. 1985 May;85(5):743–763. doi: 10.1085/jgp.85.5.743. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gilman A. G. G proteins: transducers of receptor-generated signals. Annu Rev Biochem. 1987;56:615–649. doi: 10.1146/annurev.bi.56.070187.003151. [DOI] [PubMed] [Google Scholar]
  16. Grassi F., Lux H. D. Voltage-dependent GABA-induced modulation of calcium currents in chick sensory neurons. Neurosci Lett. 1989 Oct 23;105(1-2):113–119. doi: 10.1016/0304-3940(89)90021-9. [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. Hescheler J., Rosenthal W., Trautwein W., Schultz G. The GTP-binding protein, Go, regulates neuronal calcium channels. 1987 Jan 29-Feb 4Nature. 325(6103):445–447. doi: 10.1038/325445a0. [DOI] [PubMed] [Google Scholar]
  19. 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]
  20. Hirst G. D. Neuromuscular transmission in arterioles of guinea-pig submucosa. J Physiol. 1977 Dec;273(1):263–275. doi: 10.1113/jphysiol.1977.sp012093. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Holz G. G., 4th, Rane S. G., Dunlap K. GTP-binding proteins mediate transmitter inhibition of voltage-dependent calcium channels. Nature. 1986 Feb 20;319(6055):670–672. doi: 10.1038/319670a0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. 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]
  23. Hoshi T., Smith S. J. Large depolarization induces long openings of voltage-dependent calcium channels in adrenal chromaffin cells. J Neurosci. 1987 Feb;7(2):571–580. doi: 10.1523/JNEUROSCI.07-02-00571.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Ikeda S. R., Schofield G. G. Somatostatin blocks a calcium current in rat sympathetic ganglion neurones. J Physiol. 1989 Feb;409:221–240. doi: 10.1113/jphysiol.1989.sp017494. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Ikeda S. R., Schofield G. G. Tetrodotoxin-resistant sodium current of rat nodose neurones: monovalent cation selectivity and divalent cation block. J Physiol. 1987 Aug;389:255–270. doi: 10.1113/jphysiol.1987.sp016656. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. 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]
  27. 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]
  28. 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]
  29. Kasai H., Aosaki T. Modulation of Ca-channel current by an adenosine analog mediated by a GTP-binding protein in chick sensory neurons. Pflugers Arch. 1989 Jun;414(2):145–149. doi: 10.1007/BF00580956. [DOI] [PubMed] [Google Scholar]
  30. Korn S. J., Weight F. F. Patch-clamp study of the calcium-dependent chloride current in AtT-20 pituitary cells. J Neurophysiol. 1987 Dec;58(6):1431–1451. doi: 10.1152/jn.1987.58.6.1431. [DOI] [PubMed] [Google Scholar]
  31. Lee K. S. Potentiation of the calcium-channel currents of internally perfused mammalian heart cells by repetitive depolarization. Proc Natl Acad Sci U S A. 1987 Jun;84(11):3941–3945. doi: 10.1073/pnas.84.11.3941. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. 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]
  33. Marrion N. V., Smart T. G., Brown D. A. Membrane currents in adult rat superior cervical ganglia in dissociated tissue culture. Neurosci Lett. 1987 Jun 1;77(1):55–60. doi: 10.1016/0304-3940(87)90606-9. [DOI] [PubMed] [Google Scholar]
  34. 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]
  35. McFadzean I., Mullaney I., Brown D. A., Milligan G. Antibodies to the GTP binding protein, Go, antagonize noradrenaline-induced calcium current inhibition in NG108-15 hybrid cells. Neuron. 1989 Aug;3(2):177–182. doi: 10.1016/0896-6273(89)90030-5. [DOI] [PubMed] [Google Scholar]
  36. 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]
  37. Pietrobon D., Hess P. Novel mechanism of voltage-dependent gating in L-type calcium channels. Nature. 1990 Aug 16;346(6285):651–655. doi: 10.1038/346651a0. [DOI] [PubMed] [Google Scholar]
  38. 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]
  39. Schofield G. G., Ikeda S. R. Sodium and calcium currents of acutely isolated adult rat superior cervical ganglion neurons. Pflugers Arch. 1988 May;411(5):481–490. doi: 10.1007/BF00582368. [DOI] [PubMed] [Google Scholar]
  40. Schofield G. G. Norepinephrine blocks a calcium current of adult rat sympathetic neurons via an alpha 2-adrenoceptor. Eur J Pharmacol. 1990 May 3;180(1):37–47. doi: 10.1016/0014-2999(90)90590-3. [DOI] [PubMed] [Google Scholar]
  41. Scott R. H., Dolphin A. C. Voltage-dependent modulation of rat sensory neurone calcium channel currents by G protein activation: effect of a dihydropyridine antagonist. Br J Pharmacol. 1990 Apr;99(4):629–630. doi: 10.1111/j.1476-5381.1990.tb12981.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Strittmatter S. M., Valenzuela D., Kennedy T. E., Neer E. J., Fishman M. C. G0 is a major growth cone protein subject to regulation by GAP-43. Nature. 1990 Apr 26;344(6269):836–841. doi: 10.1038/344836a0. [DOI] [PubMed] [Google Scholar]
  43. Suidan H., Tamir A., Tolkovsky A. M. A simple test for enhanced guanyl nucleotide exchange in brain adenylate cyclase systems activated by neurotransmitters. J Biol Chem. 1983 Sep 10;258(17):10524–10529. [PubMed] [Google Scholar]
  44. Taylor W. R. Two-suction-electrode voltage-clamp analysis of the sustained calcium current in cat sensory neurones. J Physiol. 1988 Dec;407:405–432. doi: 10.1113/jphysiol.1988.sp017423. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Terashima T., Katada T., Takayama C., Ui M., Inoue Y. Immunohistochemical detection of GTP-binding regulatory protein (Go) in the autonomic nervous system including the enteric nervous system, superior cervical ganglion and adrenal medulla. Brain Res. 1988 Jul 12;455(2):353–359. doi: 10.1016/0006-8993(88)90094-7. [DOI] [PubMed] [Google Scholar]
  46. 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]
  47. Webb J. G., Saelens D. A., Halushka P. V. Biosynthesis of prostaglandin E by rat superior cervical ganglia. J Neurochem. 1978 Jul;31(1):13–19. doi: 10.1111/j.1471-4159.1978.tb12427.x. [DOI] [PubMed] [Google Scholar]
  48. Yamamoto M., Kondo H. Gene expression of a neuronal growth-associated protein, GAP-43, in the paraganglionic carotid body as well as in the autonomic ganglia of normal adult rats. Neurosci Lett. 1990 Sep 18;117(3):275–279. doi: 10.1016/0304-3940(90)90676-z. [DOI] [PubMed] [Google Scholar]
  49. Zygmunt A. C., Maylie J. Stimulation-dependent facilitation of the high threshold calcium current in guinea-pig ventricular myocytes. J Physiol. 1990 Sep;428:653–671. doi: 10.1113/jphysiol.1990.sp018233. [DOI] [PMC free article] [PubMed] [Google Scholar]

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