Skip to main content
NCBI home page
The EMBO Journal logoLink to The EMBO Journal
. 1994 Nov 1;13(21):5032–5039. doi: 10.1002/j.1460-2075.1994.tb06832.x

Voltage-dependent facilitation of a neuronal alpha 1C L-type calcium channel.

E Bourinet 1, P Charnet 1, W J Tomlinson 1, A Stea 1, T P Snutch 1, J Nargeot 1
PMCID: PMC395449  PMID: 7957069

Abstract

Calcium entry into excitable cells through voltage-gated calcium channels can be influenced by both the rate and pattern of action potentials. We report here that a cloned neuronal alpha 1C L-type calcium channel can be facilitated by positive pre-depolarization. Both calcium and barium were effective as charge carriers in eliciting voltage-dependent facilitation. The induction of facilitation was shown to be independent of intracellular calcium levels, G-protein interaction and the level of phosphatase activity. Facilitation was reduced by the injection of inhibitors of protein kinase A and required the coexpression of a calcium channel beta subunit. In contrast, three neuronal non-L-type calcium channels, alpha 1A, alpha 1B and alpha 1E, were not subject to voltage-dependent facilitation when coexpressed with a beta subunit. The results indicate that the mechanism of neuronal L-type calcium channel facilitation involves the interaction of alpha 1 and beta subunits and is dependent on protein kinase A activity. The selective voltage-dependent modulation of L-type calcium channels is likely to play an important role in neuronal physiology and plasticity.

Full text

PDF
5032

Images in this article

5035Image
on p.5035

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Aniksztejn L., Ben-Ari Y. Novel form of long-term potentiation produced by a K+ channel blocker in the hippocampus. Nature. 1991 Jan 3;349(6304):67–69. doi: 10.1038/349067a0. [DOI] [PubMed] [Google Scholar]
  2. Artalejo C. R., Adams M. E., Fox A. P. Three types of Ca2+ channel trigger secretion with different efficacies in chromaffin cells. Nature. 1994 Jan 6;367(6458):72–76. doi: 10.1038/367072a0. [DOI] [PubMed] [Google Scholar]
  3. 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]
  4. Artalejo C. R., Mogul D. J., Perlman R. L., Fox A. P. Three types of bovine chromaffin cell Ca2+ channels: facilitation increases the opening probability of a 27 pS channel. J Physiol. 1991 Dec;444:213–240. doi: 10.1113/jphysiol.1991.sp018874. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Artalejo C. R., Rossie S., Perlman R. L., Fox A. P. Voltage-dependent phosphorylation may recruit Ca2+ current facilitation in chromaffin cells. Nature. 1992 Jul 2;358(6381):63–66. doi: 10.1038/358063a0. [DOI] [PubMed] [Google Scholar]
  6. Artola A., Singer W. Long-term depression of excitatory synaptic transmission and its relationship to long-term potentiation. Trends Neurosci. 1993 Nov;16(11):480–487. doi: 10.1016/0166-2236(93)90081-v. [DOI] [PubMed] [Google Scholar]
  7. Bading H., Ginty D. D., Greenberg M. E. Regulation of gene expression in hippocampal neurons by distinct calcium signaling pathways. Science. 1993 Apr 9;260(5105):181–186. doi: 10.1126/science.8097060. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. Bolshakov V. Y., Siegelbaum S. A. Postsynaptic induction and presynaptic expression of hippocampal long-term depression. Science. 1994 May 20;264(5162):1148–1152. doi: 10.1126/science.7909958. [DOI] [PubMed] [Google Scholar]
  10. Campbell K. P., Leung A. T., Sharp A. H. The biochemistry and molecular biology of the dihydropyridine-sensitive calcium channel. Trends Neurosci. 1988 Oct;11(10):425–430. doi: 10.1016/0166-2236(88)90193-2. [DOI] [PubMed] [Google Scholar]
  11. Castellano A., Wei X., Birnbaumer L., Perez-Reyes E. Cloning and expression of a neuronal calcium channel beta subunit. J Biol Chem. 1993 Jun 15;268(17):12359–12366. [PubMed] [Google Scholar]
  12. Catterall W. A., Seagar M. J., Takahashi M. Molecular properties of dihydropyridine-sensitive calcium channels in skeletal muscle. J Biol Chem. 1988 Mar 15;263(8):3535–3538. [PubMed] [Google Scholar]
  13. Charlton M. P., Smith S. J., Zucker R. S. Role of presynaptic calcium ions and channels in synaptic facilitation and depression at the squid giant synapse. J Physiol. 1982 Feb;323:173–193. doi: 10.1113/jphysiol.1982.sp014067. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Dubel S. J., Starr T. V., Hell J., Ahlijanian M. K., Enyeart J. J., Catterall W. A., Snutch T. P. Molecular cloning of the alpha-1 subunit of an omega-conotoxin-sensitive calcium channel. Proc Natl Acad Sci U S A. 1992 Jun 1;89(11):5058–5062. doi: 10.1073/pnas.89.11.5058. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. 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]
  16. Fedida D., Noble D., Spindler A. J. Use-dependent reduction and facilitation of Ca2+ current in guinea-pig myocytes. J Physiol. 1988 Nov;405:439–460. doi: 10.1113/jphysiol.1988.sp017341. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. Fernandez A., Mery J., Vandromme M., Basset M., Cavadore J. C., Lamb N. J. Effective intracellular inhibition of the cAMP-dependent protein kinase by microinjection of a modified form of the specific inhibitor peptide PKi in living fibroblasts. Exp Cell Res. 1991 Aug;195(2):468–477. doi: 10.1016/0014-4827(91)90398-e. [DOI] [PubMed] [Google Scholar]
  19. Fujita Y., Mynlieff M., Dirksen R. T., Kim M. S., Niidome T., Nakai J., Friedrich T., Iwabe N., Miyata T., Furuichi T. Primary structure and functional expression of the omega-conotoxin-sensitive N-type calcium channel from rabbit brain. Neuron. 1993 Apr;10(4):585–598. doi: 10.1016/0896-6273(93)90162-k. [DOI] [PubMed] [Google Scholar]
  20. Grover L. M., Teyler T. J. Two components of long-term potentiation induced by different patterns of afferent activation. Nature. 1990 Oct 4;347(6292):477–479. doi: 10.1038/347477a0. [DOI] [PubMed] [Google Scholar]
  21. Hell J. W., Westenbroek R. E., Warner C., Ahlijanian M. K., Prystay W., Gilbert M. M., Snutch T. P., Catterall W. A. Identification and differential subcellular localization of the neuronal class C and class D L-type calcium channel alpha 1 subunits. J Cell Biol. 1993 Nov;123(4):949–962. doi: 10.1083/jcb.123.4.949. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. 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]
  23. Hoffman P. W., Ravindran A., Huganir R. L. Role of phosphorylation in desensitization of acetylcholine receptors expressed in Xenopus oocytes. J Neurosci. 1994 Jul;14(7):4185–4195. doi: 10.1523/JNEUROSCI.14-07-04185.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. 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]
  26. Kasai H. Tonic inhibition and rebound facilitation of a neuronal calcium channel by a GTP-binding protein. Proc Natl Acad Sci U S A. 1991 Oct 1;88(19):8855–8859. doi: 10.1073/pnas.88.19.8855. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Kaufman R. J., Davies M. V., Pathak V. K., Hershey J. W. The phosphorylation state of eucaryotic initiation factor 2 alters translational efficiency of specific mRNAs. Mol Cell Biol. 1989 Mar;9(3):946–958. doi: 10.1128/mcb.9.3.946. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Kleppisch T., Pedersen K., Strübing C., Bosse-Doenecke E., Flockerzi V., Hofmann F., Hescheler J. Double-pulse facilitation of smooth muscle alpha 1-subunit Ca2+ channels expressed in CHO cells. EMBO J. 1994 Jun 1;13(11):2502–2507. doi: 10.1002/j.1460-2075.1994.tb06538.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Lacerda A. E., Kim H. S., Ruth P., Perez-Reyes E., Flockerzi V., Hofmann F., Birnbaumer L., Brown A. M. Normalization of current kinetics by interaction between the alpha 1 and beta subunits of the skeletal muscle dihydropyridine-sensitive Ca2+ channel. Nature. 1991 Aug 8;352(6335):527–530. doi: 10.1038/352527a0. [DOI] [PubMed] [Google Scholar]
  30. McDonald T. F., Pelzer S., Trautwein W., Pelzer D. J. Regulation and modulation of calcium channels in cardiac, skeletal, and smooth muscle cells. Physiol Rev. 1994 Apr;74(2):365–507. doi: 10.1152/physrev.1994.74.2.365. [DOI] [PubMed] [Google Scholar]
  31. Mintz I. M., Bean B. P. GABAB receptor inhibition of P-type Ca2+ channels in central neurons. Neuron. 1993 May;10(5):889–898. doi: 10.1016/0896-6273(93)90204-5. [DOI] [PubMed] [Google Scholar]
  32. Neely A., Wei X., Olcese R., Birnbaumer L., Stefani E. Potentiation by the beta subunit of the ratio of the ionic current to the charge movement in the cardiac calcium channel. Science. 1993 Oct 22;262(5133):575–578. doi: 10.1126/science.8211185. [DOI] [PubMed] [Google Scholar]
  33. Nishimura S., Takeshima H., Hofmann F., Flockerzi V., Imoto K. Requirement of the calcium channel beta subunit for functional conformation. FEBS Lett. 1993 Jun 21;324(3):283–286. doi: 10.1016/0014-5793(93)80135-h. [DOI] [PubMed] [Google Scholar]
  34. Perez-Reyes E., Castellano A., Kim H. S., Bertrand P., Baggstrom E., Lacerda A. E., Wei X. Y., Birnbaumer L. Cloning and expression of a cardiac/brain beta subunit of the L-type calcium channel. J Biol Chem. 1992 Jan 25;267(3):1792–1797. [PubMed] [Google Scholar]
  35. Perez-Reyes E., Kim H. S., Lacerda A. E., Horne W., Wei X. Y., Rampe D., Campbell K. P., Brown A. M., Birnbaumer L. Induction of calcium currents by the expression of the alpha 1-subunit of the dihydropyridine receptor from skeletal muscle. Nature. 1989 Jul 20;340(6230):233–236. doi: 10.1038/340233a0. [DOI] [PubMed] [Google Scholar]
  36. 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]
  37. Pragnell M., De Waard M., Mori Y., Tanabe T., Snutch T. P., Campbell K. P. Calcium channel beta-subunit binds to a conserved motif in the I-II cytoplasmic linker of the alpha 1-subunit. Nature. 1994 Mar 3;368(6466):67–70. doi: 10.1038/368067a0. [DOI] [PubMed] [Google Scholar]
  38. Pragnell M., Sakamoto J., Jay S. D., Campbell K. P. Cloning and tissue-specific expression of the brain calcium channel beta-subunit. FEBS Lett. 1991 Oct 21;291(2):253–258. doi: 10.1016/0014-5793(91)81296-k. [DOI] [PubMed] [Google Scholar]
  39. Richard S., Charnet P., Nerbonne J. M. Interconversion between distinct gating pathways of the high threshold calcium channel in rat ventricular myocytes. J Physiol. 1993 Mar;462:197–228. doi: 10.1113/jphysiol.1993.sp019551. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Sadler S. E., Maller J. L. In vivo regulation of cyclic AMP phosphodiesterase in Xenopus oocytes. Stimulation by insulin and insulin-like growth factor 1. J Biol Chem. 1987 Aug 5;262(22):10644–10650. [PubMed] [Google Scholar]
  41. Sculptoreanu A., Rotman E., Takahashi M., Scheuer T., Catterall W. A. Voltage-dependent potentiation of the activity of cardiac L-type calcium channel alpha 1 subunits due to phosphorylation by cAMP-dependent protein kinase. Proc Natl Acad Sci U S A. 1993 Nov 1;90(21):10135–10139. doi: 10.1073/pnas.90.21.10135. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Sculptoreanu A., Scheuer T., Catterall W. A. Voltage-dependent potentiation of L-type Ca2+ channels due to phosphorylation by cAMP-dependent protein kinase. Nature. 1993 Jul 15;364(6434):240–243. doi: 10.1038/364240a0. [DOI] [PubMed] [Google Scholar]
  43. Snutch T. P., Reiner P. B. Ca2+ channels: diversity of form and function. Curr Opin Neurobiol. 1992 Jun;2(3):247–253. doi: 10.1016/0959-4388(92)90111-w. [DOI] [PubMed] [Google Scholar]
  44. Snutch T. P., Tomlinson W. J., Leonard J. P., Gilbert M. M. Distinct calcium channels are generated by alternative splicing and are differentially expressed in the mammalian CNS. Neuron. 1991 Jul;7(1):45–57. doi: 10.1016/0896-6273(91)90073-9. [DOI] [PubMed] [Google Scholar]
  45. Soong T. W., Stea A., Hodson C. D., Dubel S. J., Vincent S. R., Snutch T. P. Structure and functional expression of a member of the low voltage-activated calcium channel family. Science. 1993 May 21;260(5111):1133–1136. doi: 10.1126/science.8388125. [DOI] [PubMed] [Google Scholar]
  46. Starr T. V., Prystay W., Snutch T. P. Primary structure of a calcium channel that is highly expressed in the rat cerebellum. Proc Natl Acad Sci U S A. 1991 Jul 1;88(13):5621–5625. doi: 10.1073/pnas.88.13.5621. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Stea A., Dubel S. J., Pragnell M., Leonard J. P., Campbell K. P., Snutch T. P. A beta-subunit normalizes the electrophysiological properties of a cloned N-type Ca2+ channel alpha 1-subunit. Neuropharmacology. 1993 Nov;32(11):1103–1116. doi: 10.1016/0028-3908(93)90005-n. [DOI] [PubMed] [Google Scholar]
  48. Tiaho F., Piot C., Nargeot J., Richard S. Regulation of the frequency-dependent facilitation of L-type Ca2+ currents in rat ventricular myocytes. J Physiol. 1994 Jun 1;477(Pt 2):237–251. doi: 10.1113/jphysiol.1994.sp020187. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Tomlinson W. J., Stea A., Bourinet E., Charnet P., Nargeot J., Snutch T. P. Functional properties of a neuronal class C L-type calcium channel. Neuropharmacology. 1993 Nov;32(11):1117–1126. doi: 10.1016/0028-3908(93)90006-o. [DOI] [PubMed] [Google Scholar]
  50. Tsien R. W., Ellinor P. T., Horne W. A. Molecular diversity of voltage-dependent Ca2+ channels. Trends Pharmacol Sci. 1991 Sep;12(9):349–354. doi: 10.1016/0165-6147(91)90595-j. [DOI] [PubMed] [Google Scholar]
  51. 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]
  52. Varadi G., Lory P., Schultz D., Varadi M., Schwartz A. Acceleration of activation and inactivation by the beta subunit of the skeletal muscle calcium channel. Nature. 1991 Jul 11;352(6331):159–162. doi: 10.1038/352159a0. [DOI] [PubMed] [Google Scholar]
  53. Westenbroek R. E., Hell J. W., Warner C., Dubel S. J., Snutch T. P., Catterall W. A. Biochemical properties and subcellular distribution of an N-type calcium channel alpha 1 subunit. Neuron. 1992 Dec;9(6):1099–1115. doi: 10.1016/0896-6273(92)90069-p. [DOI] [PubMed] [Google Scholar]
  54. Wheeler D. B., Randall A., Tsien R. W. Roles of N-type and Q-type Ca2+ channels in supporting hippocampal synaptic transmission. Science. 1994 Apr 1;264(5155):107–111. doi: 10.1126/science.7832825. [DOI] [PubMed] [Google Scholar]
  55. Williams M. E., Brust P. F., Feldman D. H., Patthi S., Simerson S., Maroufi A., McCue A. F., Veliçelebi G., Ellis S. B., Harpold M. M. Structure and functional expression of an omega-conotoxin-sensitive human N-type calcium channel. Science. 1992 Jul 17;257(5068):389–395. doi: 10.1126/science.1321501. [DOI] [PubMed] [Google Scholar]
  56. Williams M. E., Feldman D. H., McCue A. F., Brenner R., Velicelebi G., Ellis S. B., Harpold M. M. Structure and functional expression of alpha 1, alpha 2, and beta subunits of a novel human neuronal calcium channel subtype. Neuron. 1992 Jan;8(1):71–84. doi: 10.1016/0896-6273(92)90109-q. [DOI] [PubMed] [Google Scholar]
  57. Zhang J. F., Randall A. D., Ellinor P. T., Horne W. A., Sather W. A., Tanabe T., Schwarz T. L., Tsien R. W. Distinctive pharmacology and kinetics of cloned neuronal Ca2+ channels and their possible counterparts in mammalian CNS neurons. Neuropharmacology. 1993 Nov;32(11):1075–1088. doi: 10.1016/0028-3908(93)90003-l. [DOI] [PubMed] [Google Scholar]

Articles from The EMBO Journal are provided here courtesy of Nature Publishing Group

RESOURCES