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Direct and remote modulation of l-channels in chromaffin cells

Distinct actions on α1C and α1D subunits?

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Abstract

Understanding precisely the functioning of voltage-gated Ca2+ channels and their modulation by signaling molecules will help clarifying the Ca2+-dependent mechanisms controlling exocytosis in chromaffin cells. In recent years, we have learned more about the various pathways through which Ca2+ channels can be up- or down-modulated by hormones and neurotransmitters and how these changes may condition chromaffin cell activity and catecolamine release. Recently, the attention has been focused on the modulation of L-channels (Cav 1), which represent the major Ca2+ current component in rat and human chromaffin cells. L-channels are effectively inhibited by the released content of secretory granules or by applying mixtures of exogenous ATP, opioids, and adrenaline through the activation of receptor-coupled G proteins. This unusual inhibition persists in a wide range of potentials and results from a direct (membrane-delimited) interaction of G protein subunits with the L-channels co-localized in membrane microareas. Inhibition of L-channels can be reversed when the cAMP/PKA pathway is activated by membrane permeable cAMP analog or when cells are exposed to isoprenaline (remote action), suggesting the existence of parallel and opposite effects on L-channel gating by distinctly activated membrane autoreceptors.

Here, the authors review the molecular components underlying these two opposing signaling pathways and present new evidence supporting the presence of two L-channel types in rat chromaffin cells (α1C and α1D), which open new interesting issues concerning Ca2+-channel modulation. In light of recent findings on the regulation of exocytosis by Ca2+-channel modulation, the authors explore the possible role of L-channels in the autocontrol of catecholamine release.

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References

  1. Hofmann F., Lacinov L., and Klugbauer N. (1999) Voltage-dependent calcium channels: from structure to function. Rev. Physiol. Biochem. Pharmacol. 139, 33–87.

    PubMed  CAS  Google Scholar 

  2. Catterall W. A. (2000) Structure and regulation of voltage-gated Ca2+ channels. Annu. Rev. Cell Dev. Biol. 16, 521–555.

    Article  PubMed  CAS  Google Scholar 

  3. Garcïa A. G., Sala F., Reig J. A., Viniegra S., Frïas J., Fonteriz R. I., and Gandía L. (1984) Dihydropyridine Bay-K-8644 activates chromaffin cell calcium channels. Nature 309, 69–71.

    Article  PubMed  Google Scholar 

  4. Spitzer N. C., Kingston P. A., Manning T. J., and Conklin M. W. (2002) Outside and in: development of neuronal excitability. Curr. Op. Neurobiol. 12, 315–323.

    Article  PubMed  CAS  Google Scholar 

  5. Dolphin A. C. (1996) Facilitation of Ca2+ currents in excitable cells. Trends in Neurosci. 19, 35–43.

    Article  CAS  Google Scholar 

  6. Dolphin A. C. (1999) L-type calcium channel modulation. Advances in Second Messenger and Phosphoprotein Res. 33, 153–170.

    CAS  Google Scholar 

  7. Carbone E., Carabelli V., Cesetti T., Baldelli P., Hernández-Guijo J. M., and Giusta L. (2001) G-protein- and cAMP-dependent L-channel gating modulation: a manyfold system to control calcium entry in neurosecretory cells. Pflügers Arch.-Eur. J. Physiol. 442, 801–813.

    Article  CAS  Google Scholar 

  8. Cesetti T., Hernández-Guijo J. M., Baldelli P., Carabelli V., and Carbone E. (2003) Opposite action of β1- and β2-adrenergic receptors on Cav 1 L-channel current in rat adrenal chromaffin cells. J. Neurosci. 23, 73–83.

    PubMed  CAS  Google Scholar 

  9. Kleppisch T., Ahnert-Hilger G., Gollasch M., Spicher K., Hescheler J., Schultz G., and Rosenthal W. (1992) Inhibition of voltage-dependent Ca2+ channels via α2-adrenergic and opioid receptors in cultured bovine adrenal chromaffin cells. Pflügers Arch.-Eur. J. Physiol. 421, 131–137.

    Article  CAS  Google Scholar 

  10. Albillos A., Gandía L., Michelena P., Gilabert J. A., del Valle M., Carbone E., and García A. G. (1996) The mechanism of calcium channel facilitation in bovine chromaffin cells. J. Physiol. 494, 687–695.

    PubMed  CAS  Google Scholar 

  11. Albillos A., Carbone E., Gandía L., García A. G., and Pollo A. (1996) Opioid inhibition of Ca2+ channel subtypes in bovine chromaffin cells: selectivity of action and voltage-dependence. Eur. J. Neurosci. 8, 1561–1570.

    Article  PubMed  CAS  Google Scholar 

  12. Carabelli V., Carra I., and Carbone E. (1998) Localized secretion of ATP and opioids revealed through single Ca2+ channel modulation in bovine chromaffin cells. Neuron 20, 1255–1268.

    Article  PubMed  CAS  Google Scholar 

  13. Hernández-Guijo J. M., Carabelli V., Gandía L., García A. G., and Carbone E. (1999) Voltage-independent autocrine modulation of L-type channels mediated by ATP, opioids and catecholamines in rat chromaffin cells. Eur. J. Neurosci. 11, 3574–3584.

    Article  PubMed  Google Scholar 

  14. Carabelli V., Hernández-Guijo J. M., Baldelli P., and Carbone E. (2001) Direct autocrine inhibition and cAMP-dependent potentiation of single L-type Ca2+ channels in bovine chromaffin cells. J. Physiol. 532.1, 73–90.

    Article  Google Scholar 

  15. Kamp T. J. and Hell J. W. (2000) Regulation of cardiac L-type calcium channels by protein kinase A and protein kinase C. Circ. Res. 87, 1095–1102.

    PubMed  CAS  Google Scholar 

  16. Rockman H. A., Koch W. J., and Leifkowitz R. J. (2002) Seven-transmembrane-spanning receptors and heart function. Nature 415, 208–212.

    Article  Google Scholar 

  17. Wick P. F., Westenbroek R. E., and Holz R. W. (1996) Effects of expression of a mouse brain L-type calcium channel α1 subunit on secretion from bovine adrenal chromaffin cells. Mol. Pharmacol. 49, 295–302.

    PubMed  CAS  Google Scholar 

  18. García-Palomero E., Cuchillo I., García A. G., Renart J., Albillos A., and Montiel C. (2000) Greater diversity than previously thought of chromaffin cell Ca2+ channels, derived from mRNA identification studies. FEBS Lett. 481, 235–239.

    Article  PubMed  Google Scholar 

  19. García-Palomero E., Renart J., Andrés-Mateos E., et al. (2001) Differential expression of calcium channels subtypes in the bovine adrenal madulla. Neuroendocrinology 74, 251–261.

    Article  PubMed  Google Scholar 

  20. Colston J. T., Valdes J. J., and Chambers J. P. (1998) Ca2+ channel α1-subunit transcripts are differentially expressed in rat pheochromocytoma (PC12) cells following nerve growth factor treatment. Int. J. Develop. Neurosci. 16, 379–389.

    Article  CAS  Google Scholar 

  21. Carabelli V., Giancippoli A., Baldelli P., Carbone E., and Artalejo A. R. (2003) Distinct potentiation of L-type currents and secretion by cAMP in rat chromaffin cells. Biophys. J. 85, 1326–1337.

    Article  PubMed  CAS  Google Scholar 

  22. Lim W., Kim S. J., Yan H. D., and Kim J. (1997) Ca2+-channel-dependent and -independent inhibition of exocytosis by extracellular ATP in voltage-clamped rat adrenal chromaffin cells. Pflügers Arch.-Eur. J. Physiol. 435, 34–42.

    Article  CAS  Google Scholar 

  23. Pietrobon D. and Hess P. (1990) Novel mechanism of voltage-dependent gating in L-type calcium channels. Nature 346, 651–655.

    Article  PubMed  CAS  Google Scholar 

  24. Hoshi T., Rothlein J., and Smith S. J. (1984) Facilitation of Ca2+-channel currents in bovine adrenal chromaffin cells. Proc. Natl. Acad. Sci. USA 81, 5871–5875.

    Article  PubMed  CAS  Google Scholar 

  25. Kavalali E. T. and Plummer M. R. (1996) Multiple voltage-dependent mechanisms potentiate calcium channel activity in hippocampal neurons. J. Neurosci. 16, 1072–1082.

    PubMed  CAS  Google Scholar 

  26. Artalejo C. R., Rossie S., Perlman R. A., and Fox A. P. (1992) Voltage-dependent phosphorylation may recruit Ca2+ current facilitation in chromaffin cells. Nature 358, 63–66.

    Article  PubMed  CAS  Google Scholar 

  27. Sculptoreanu A., Scheuer T., and Catterall W. (1993) Voltage-dependent potentiation of L-type Ca2+ channels due to phosphorylation by cAMP-dependent protein kinase. Nature 364, 240–243.

    Article  PubMed  CAS  Google Scholar 

  28. Johnson B. D., Brousal J. P., Peterson B. Z., et al. (1997) Modulation of the cloned skeletal muscle L-type Ca2+ channel by anchored cAMP-dependent protein kinase. J. Neurosci. 17, 1243–1255.

    PubMed  CAS  Google Scholar 

  29. Gray P. C., Tibbs V. C., Catterall W. A., and Murphy B. J. (1997) Identification of a 15-kDa cAMP-dependent protein kinase-anchoring protein associated with skeletal muscle L-type calcium channels. J. Biol. Chem. 272, 6297–6302.

    Article  PubMed  CAS  Google Scholar 

  30. Scholz K. P. and Miller R. J. (1991) GABAB receptor-mediated inhibition of Ca2+ currents and synaptic transmission in cultured rat hippocampal neurones. J. Physiol. 444, 669–686.

    PubMed  CAS  Google Scholar 

  31. Gollasch M., Hescheler J., Spicher K., Klinz F. J., Schultz G., and Rosenthal W. (1991) Inhibition of calcium channels via α2-adrenergic and muscarinic receptors in pheochromocytoma (PC12) cells. Am. J. Physiol. 260, C1282-C1289.

    PubMed  CAS  Google Scholar 

  32. Kleuss C., Hescheler J., Ewel C., Rosenthal W., Schultz G., and Wittig B. (1991) Assignment of G-protein subtypes to specific receptors inducing inhibition of calcium currents. Nature 353, 43–48.

    Article  PubMed  CAS  Google Scholar 

  33. Pollo A., Lovallo M., Biancardi E., Sher E., Socci C., and Carbone E. (1993) Sensitivity to dihydropyridines, θ-conotoxins and noradrenaline reveals multiple high-voltage activated Ca2+ channels in rat insulinoma and human pancreatic β-cells. Pflügers Arch.-Eur. J. Physiol. 423, 462–471.

    Article  CAS  Google Scholar 

  34. Haws C. M., Slesinger P. A., and Lansman J. B. (1993) Dihydropyridine-and θ-conotoxin-sensitive Ca2+ currents in cerebellar neurons: persistent block of L-type channels by a pertussis toxin-sensitive G-protein. J. Neurosci. 13, 1148–1156.

    PubMed  CAS  Google Scholar 

  35. Chavis P., Shinozaki H., Bockaert J., and Fagni L. (1994) The metabotropic glutamate receptor types 2/3 inhibit L-type calcium channels via a pertussis toxin-sensitive G-protein in cultured cerebellar granule cells. J. Neurosci. 14, 7067–7706.

    PubMed  CAS  Google Scholar 

  36. Amico C., Marchetti C., Nobile M., and Usai C. (1995) Pharmacological types of calcium channels and their modulation by baclofen in cerebellar granules. J. Neurosci. 15, 2839–2848.

    PubMed  CAS  Google Scholar 

  37. Mei Y. A., Griffon N., Buquet C., et al. (1995) Activation of dopamine D4 receptor inhibits an L-type calcium current in cerebellar granule cells. Neuroscience 68, 107–116.

    Article  PubMed  CAS  Google Scholar 

  38. Tallent M., Liapakis G., O’carroll A. M., Lolait S. J., Dichter M., and Reisine T. (1996) Somatostatin receptor subtypes SSTR2 and SSTR5 couple negatively to an L-type Ca2+ current in the pituitary cell line AtT-20. Neuroscience 71, 1073–1081.

    Article  PubMed  CAS  Google Scholar 

  39. Gilon P., Yakel J., Gromada J., Zhu Y., Henquin J. C., and Rorsman P. (1997) G-proteins-dependent inhibition of L-type Ca2+ currents by acetylcholine in mouse pancreatic β-cells. J. Physiol. 499, 65–76.

    PubMed  CAS  Google Scholar 

  40. Rusin K. I., Giovannucci D. R., Stuenkel E. L., and Moises H. C. (1997) κ-opioid receptor activation modulates Ca2+ currents and secretion in isolated neuroendocrine nerve terminals. J. Neurosci. 17, 6565–6574.

    PubMed  CAS  Google Scholar 

  41. Formenti A., Martina M., Plebani A., and Mancia M. (1998) Multiple modulatory effects of dopamine on calcium channel kinetics in adult rat sensory neurons. J. Physiol. 489, 41–53.

    Google Scholar 

  42. Wikstrom M. A., Grillner S., and El Manira A. (1999) Inhibition of N- and L-type Ca2+ currents by dopamine in lamprey spinal motoneurons. Neuroreport 10, 3179–3183.

    Article  PubMed  CAS  Google Scholar 

  43. Maturana A. D., Casal A. J., Demaurex N., Vallotton M. B., Capponi A. M., and Rossier M. F. (1999) Angiotensin II negatively modulates L-type calcium channels through a pertussis toxin-sensitive G protein in adrenal glomerulosa cells. J. Biol. Chem. 27, 19,943–19,948.

    Google Scholar 

  44. Acosta C. G. and Lopez H. S. (1999) γ-Opioid receptos modulation of several voltage-dependent Ca2+ currents in rat sensory neurons. J. Neurosci. 19, 8337–8348.

    PubMed  CAS  Google Scholar 

  45. Akopian A., Johnson J., Gabriel R., Brecha N., and Witkovsky P. (2000) Somatostatin modulates voltage-gated K+ and Ca2+ currents in rod and cone photoreceptors of the salamander retina. J. Neurosci. 20, 929–936.

    PubMed  CAS  Google Scholar 

  46. Mansvelder H. D., Lodder J. C., Sons M. S., and Kits K. S. (2001) Dopamine modulates exocytosis independent of Ca2+ entry in melanotropic cells. J. Neurophysiol. 87, 793–801.

    Google Scholar 

  47. Cox D. H. and Dunlap K. (1992) Pharmacological discrimination of N-type from L-type Ca2+ current and its selective modulation by neurotransmitters. J. Neurosci. 12, 906–914.

    PubMed  CAS  Google Scholar 

  48. Mintz I. M. and Bean B. P. (1993) GABAB receptor inhibition of P-type Ca2+ channels in central neurons. Neuron 10, 889–898.

    Article  PubMed  CAS  Google Scholar 

  49. Sher E., Cesare P., Codignola A., Clementi F., Tarroni P., Pollo A., Magnelli V., and Carbone E. (1996) Activation of delta-opioid receptors inhibits neuronal-like calcium channels and distal steps of Ca2+-dependent secretion in human small-cell lung carcinoma cells. J. Neurosci. 16, 3672–3684.

    PubMed  CAS  Google Scholar 

  50. Bell C. C., Butcher A. J., Berrow N. S., Page K. M., Brust P. F., Nesterova A., Stauderman K. A., Seabrook G. R., Nurnberg B., and Dolphin A. C. (2001) Biophysical properties, pharmacology and modulation of human, neuronal L-type (α1D, Cav 1.3) voltage-dependent calcium currents. J. Neurophysiol. 85, 816–827.

    PubMed  CAS  Google Scholar 

  51. Safa P., Boulter J., and Hales T. G. (2001) Functional properties of Cav1.3 (α1D) L-type Ca2+ channel splice variants expressed by rat brain and neuroendocrine GH3 cells. J. Biol. Chem. 276, 38,727–38,737.

    Article  CAS  Google Scholar 

  52. Elmslie K. S., Zhou W., and Jones S. W. (1990) LHRH and GTP-γ-S modify calcium current activation in bullfrog sympathetic. Neuron 5, 75–80.

    Article  PubMed  CAS  Google Scholar 

  53. Boland L. and Bean B. P. (1993) Modulation of N-type calcium channels in bullfrog sympathetic neurons by luteinizing hormone-releasing hormone: kinetics and voltage-dependence. J. Neurosci. 13, 516–533.

    PubMed  CAS  Google Scholar 

  54. Hille B. (1994) Modulation of ion channel function by G-protein coupled receptors. Trends in Neurosci. 17, 531–536.

    Article  CAS  Google Scholar 

  55. Carabelli V., Lovallo M., Magnelli V., Zucker H., and Carbone E. (1996) Voltage-dependent modulation of single N-type Ca2+ channel kinetics by receptor agonists in IMR32 cells. Biophys. J. 70, 2144–2154.

    PubMed  CAS  Google Scholar 

  56. Patil P. G., de Leon M., Reed R. R., Dubel S., Snutch T. P., and Yue D. T. (1996) Elementary events underlying voltage-dependent G-protein inhibition of N-type calcium channels. Biophys. J. 71, 2509–2521.

    PubMed  CAS  Google Scholar 

  57. Lee H. K. and Elmslie K. S. (2000) Reluctant gating of single N-type calcium channels during neurotransmitter-induced inhibition in bullfrog sympathetic neurons. J. Neurosci. 20, 3115–3128.

    PubMed  CAS  Google Scholar 

  58. Bean B. P., Nowycky M. C., and Tsien R. W. (1984) β-adrenergic modulation of calcium channels in frog ventricular heart cells. Nature 307, 371–375.

    Article  PubMed  CAS  Google Scholar 

  59. Reuter H. (1983) Calcium channel modulation by neurotransmitters, enzymes and drugs. Nature 301, 569–574.

    Article  PubMed  CAS  Google Scholar 

  60. Hartzell H. C., Mery P. F., Fischmeister R., and Szabo G. (1991) Sympathetic regulation of cardiac calcium current is due exclusively to cAMP-dependent phosphorylation. Nature 351, 573–576.

    Article  PubMed  CAS  Google Scholar 

  61. Hosey M. M., DebBurman S. K., Pals-Rylaarsdam R., Richardson R. M., and Benovic J. L. (1996) The role of G-protein coupled receptor kinases in the regulation of muscarinic cholinergic receptors. Prog. Brain Res. 109, 169–179.

    Article  PubMed  CAS  Google Scholar 

  62. DeJongh K. S., Murphy B. M., Colvin A. A., Hell J. W., Takahashi M., and Catterall W. A. (1996) Specific phosphorylation of a site in the full length form of the alphal subunit of the cardiac L-type calcium channel by adenosine 3–5-cyclic monophosphate-dependent protein kinase. Biochem. 35, 10,392–10,402.

    CAS  Google Scholar 

  63. Yue D. T., Herzig S., and Marban E. (1990) Beta-adrenergic stimulation of calcium channels occurs by potentiation of high-activity gating modes. Proc. Natl. Acad. Sci. USA 87, 753–757.

    Article  PubMed  CAS  Google Scholar 

  64. Hess P., Lansman J. B., and Tsien R. W. (1984) Different modes of Ca2+ channel gating behavior favored by dihydropyridine Ca2+ agonists and antagonists. Nature 311, 538–544.

    Article  PubMed  CAS  Google Scholar 

  65. Tiaho F., Richard S., Lory P., Nerbonne J. M., and Nargeot J. (1990) Cyclic-AMP-dependent phosphorylation modulates the stereospecific activation of cardiac Ca2+ channels by Bay K 8644. Pflügers Arch.-Eur. J. Physiol. 417, 58–66.

    Article  CAS  Google Scholar 

  66. Blumenstein Y., Ivanina T., Shistik E., Bossi E., Peres A., and Dascal N, (1999) Regulation of cardiac L-type Ca2+ channel by coexpression of Gαs in Xenopus oocytes. FEBS Lett. 444, 78–84.

    Article  PubMed  CAS  Google Scholar 

  67. Gao T., Yatani A., Hidenory S., Green S. A., Dascal N., Scott D. J., and Hosey M. M. (1997) cAMP-dependent regulation of L-type ca channels requires membrane targeting of PKA and phosphorylation of channel subunits. Neuron 19, 185–196.

    Article  PubMed  CAS  Google Scholar 

  68. Perez-Reyes E., Yuan W., Wei X., and Bers D. M. (1994) Regulation of the cloned L-type cardiac calcium channel by cyclic-AMP-dependent protein kinase. FEBS Lett. 342, 119–123.

    Article  PubMed  CAS  Google Scholar 

  69. Zong X., Welling A., Bosse E., Flockerzi V., and Hofmann F. (1995) On the regulation of the expressed L-type calcium channel by cAMP-dependent phosphorylation. Pflügers Arch.-Eur. J. Physiol. 430, 340–347.

    Article  CAS  Google Scholar 

  70. Mikala G., Klockner U., Varadi M., Eisfeld J., Schwartz A., and Varadi G. (1998) cAMP-dependent phosphorylation sites and macroscopic activity of recombinant cardiac L-type calcium channels. Mol. Cell Biochem. 185, 95–109.

    Article  PubMed  CAS  Google Scholar 

  71. García A. G. and Carbone E. (1996) Calcium-current facilitation in chromaffin cells. Trends Neurosci. 19, 383–385.

    Article  PubMed  Google Scholar 

  72. Kawalali E. T., Hwang K. S., and Plummer M. R. (1997) cAMP-dependent enhancement of dihydropyridine-sensitive calcium channel availability in hippocampal neurons. J. Neurosci. 17, 5334–5348.

    Google Scholar 

  73. Henquin J. C. and Meissner H. P. (1984) The ionic, electrical and secretory effects of endogeneous cyclic adenosine monophosphate in mouse pancreatic β cells: studies with forskolin. Endocrinology. 115, 1125–1134.

    Article  PubMed  CAS  Google Scholar 

  74. Ämmälä C., Ashcroft F. M., and Rorsman P. (1993) Cyclic AMP-dependent potentiation of exocytosis in insulin secreting pancreatic β-cells by stimulation of calcium-influx and direct interaction with the secretory machinery. Nature 363, 356–358.

    Article  PubMed  Google Scholar 

  75. Trautwein W. and Hescheler J. (1990) Regulation of cardiac L-type calcium current by phosphorylation and G proteins. Annu. Rev. Physiol. 52, 257–274.

    Article  PubMed  CAS  Google Scholar 

  76. Novara M., Baldelli P., Hernández-Guijo J. M., Giusta L., and Carbone E. (2002) Chronic exposure to cAMP upregulates T-type Ca2+ channels and TTX-insensitive Na+ channels in cultured rat chromaffin cells. J. Physiol. 543, P: 67P.

    Google Scholar 

  77. Skeberdis V. A., Jurevicius J., and Fischmeister R. (1997) β2 adrenergic activation of L-type Ca2+ current in cardiac myocytes. J. Pharmacol. Exp. Ther. 283, 452–461.

    PubMed  CAS  Google Scholar 

  78. Xiao R. P., Ji X., and Lakatta E. G. (1995) Functional coupling of the β2-adrenoceptor to a pertussis toxin-sensitive G protein in cardiac myocytes. Mol. Pharmacol. 47, 322–329.

    PubMed  CAS  Google Scholar 

  79. Strosberg A. D. (1997) Structure and function of the β3-adrenergic receptor. Annu. Rev. Pharmacol. Toxicol. 37, 421–450.

    Article  PubMed  CAS  Google Scholar 

  80. Xiao R. P., Avdonin P., Zhou Y. Y., et al. (1999) Coupling of β2-adrenoceptor to Gi protein and its physiological relevance in murine cardiac myocytes. Circ. Res. 84, 43–52.

    PubMed  CAS  Google Scholar 

  81. Xiao R. P., Cheng G., Zhou Y. Y., Kuschel M., and Lakatta E. G. (1999) Recent advances in cardiac β2-adrenergic signal transduction. Circ. Res. 85, 1092–1100.

    PubMed  CAS  Google Scholar 

  82. Steinberg S. F. and Brunton L. L. (2001) Compartmentation of G-protein-coupled signaling pathways in cardiac myocytes. Annu. Rev. Pharmacol. Toxicol. 41, 751–773.

    Article  PubMed  CAS  Google Scholar 

  83. Davare M. A., Avdonin V., Hall D. D., et al. (2001) A β2 adrenergic receptor signaling complex assembled with the Ca2+ channel Cav1.2 Science 293, 98–101.

    Article  PubMed  CAS  Google Scholar 

  84. Snutch T. P., Tomlinson W. J., Leonard J. P., and Gilbert M. M. (1991) Distinct calcium channels are generated by alternative splicing and are differentially expressed in the mammalian CNS. Neuron 7, 45–57.

    Article  PubMed  CAS  Google Scholar 

  85. Chin H., Smith M. A., Kim H. L., and Kim H. (1992) Expression of dihydropyridine-sensitive brain calcium channels in the rat central nervous system. FEBS Lett. 299, 69–74.

    Article  PubMed  CAS  Google Scholar 

  86. Williams M. E., Feldman D. H., McCue A. F., et al. (1992) Structure and functional expression of α1, α2, and β subunits of a novel human neuronal calcium channel subtype. Neuron 8, 71–84.

    Article  PubMed  CAS  Google Scholar 

  87. Wyatt C. N., Campbell V., Brodbeck J., et al. (1997) Voltage-dependent binding and calcium channel current inhibition by an anti-α1D subunit antibody in rat dorsal root ganglion neurones and guinea-pig myocytes. J. Physiol. 502, 307–319.

    Article  PubMed  CAS  Google Scholar 

  88. Hell J. W., Westenbroek R. E., Warner C., et al. (1993) Identification and differential subcellular localization of the neuronal class C and class D L-type calcium channels α1 subunits. J. Cell. Biol. 123, 989–962.

    Article  Google Scholar 

  89. Westenbroek R. E., Bausch S. B., Lin R. C. S., Franck J. E., Noebels J. L., and Catterall W. A. (1998) Upregulation of L-type Ca2+ channels in reactive astrocytes after brain injury, hypomyelination, and ischemia. J. Neurosci. 18, 2321–2334.

    PubMed  CAS  Google Scholar 

  90. Chung Y. H., Shin C., Kim M. J., and Cha C. (2001) Enhanced expression of L-type Ca2+ channels in reactive astrocytes after ischemic injury in rats. Neurosci. Lett. 302, 93–96.

    Article  PubMed  CAS  Google Scholar 

  91. Seino S., Chen L., Seino M., Blondel O., Takeda J., Johnson J. H., and Bell G. I. (1992) Cloning of the α1 subunit of a voltage-dependent calcium channel expressed in pancreatic β cells. Proc. Natl. Acad. Sci. USA 89, 584–588.

    Article  PubMed  CAS  Google Scholar 

  92. Ihara Y., Yamada Y., Fujii Y., et al. (1995) Molecular diversity and functional characterization of voltage-dependent calcium channels (CACN4) expressed in pancreatic beta-cells. Mol. Endocrinol. 9, 121–130.

    Article  PubMed  CAS  Google Scholar 

  93. Horvath A., Szabadkal G. Y., Varnai P., Aranyi T., Wollheim C. B., Spat S., and Enyedi P. (1998) Voltage dependent calcium channels in adrenal glomerulosa cells and in insulin producing cells. Cell Calcium 23, 33–42.

    Article  PubMed  CAS  Google Scholar 

  94. Safayhi H., Haase H., Kramer U., et al. (1997) L-type calcium channels in insulin-secreting cells: Biochemical characterization and phosphorylation of RINm5F cells. Mol. Endocrinol. 11, 619–629.

    Article  PubMed  CAS  Google Scholar 

  95. Magnelli V., avaltroni A., and Carbone E. (1996) A single non-L-non-N-type calcium channel rat insulin-secreting RINm5F cells. Pflügers Arch.-Eur. J. Physiol. 431, 341–352.

    Article  CAS  Google Scholar 

  96. Grassi C., D Ascenzo M., Valente A., and Azzena G. B. (1999) Ca2+ channel inhibition induced by nitric oxide in rat insulinoma RINm5F cells. Pflügers Arch.-Eur. J. Physiol. 437, 241–247.

    Article  CAS  Google Scholar 

  97. Lipscombe D. (2002) L-type calcium channels. Circ. Res. 90, 933–935.

    Article  PubMed  CAS  Google Scholar 

  98. Barg S., Ma X., Eliasson L., et al. (2001) Fast exocytosis with few Ca2+ channels in insulin-secreting mouse pancreatic β cells. Biophys. J. 81, 3308–3323.

    PubMed  CAS  Google Scholar 

  99. Namkung Y., Skrypnyk N., Jeong M. J., et al. (2001) Requirement for the L-type Ca2+ channel α1D subunit in postnatal pancreatic β cell generation. J. Clinical Invest. 108, 1015–1022.

    Article  CAS  Google Scholar 

  100. Safa P., Boulter J., and Hales T. G. (2001) Functional properties of Cav 1.3 (α1D) L-type Ca2+ channel splice variants expressed by rat brain and neuroendocrine GH3 cells. J. Biol. Chem. 276, 38,727–38,737.

    Article  CAS  Google Scholar 

  101. Zhang Z., Xu Y., Song H., et al. (2002) Functional roles of Cav 1.3 (α1D) calcium channel in sinoatrial nodes. Circ. Res. 90, 981–987.

    Article  PubMed  CAS  Google Scholar 

  102. Mangoni M. E., Couette B., Bourinet E., Platzer J., Reimer D., Striessnig J., and Nargeot J. (2003) Functional role of L-type Cav 1.3 Ca2+ channels in cardiac pacemaker activity. Proc. Natl. Acad. Sci. USA 100, 5543–5548.

    Article  PubMed  CAS  Google Scholar 

  103. Iwashima Y., Pugh W., Depaoli A. M., Takeda J., Seino S., Bell G. I., and Polonsky K. S. (1993) Expression of calcium channel mRNAs in rat pancreatic islets and downregulation after glucose infusion. Diabetes 42, 948–955.

    Article  PubMed  CAS  Google Scholar 

  104. Xu W. and Lipscombe D. (2001) Neuronal Cav 1.3α1 L-type channels activate at relatively hyperpolarized membrane potentials and are incompletely inhibited by dihydropyridines. J. Neurosci. 21, 5944–5951.

    PubMed  CAS  Google Scholar 

  105. Koschak A., Reimer D., Huber I., Grabner M., Glossmann H., Engel J., and Stressnig J. (2001) α1D (Cav1.3) subunits can form L-type Ca2+ channels activating at negative voltages. J. Biol. Chem. 276, 22,100–22,106.

    Article  CAS  Google Scholar 

  106. Platano D., Pollo A., Carbone E., and Aicardi A. (1996) Up-regulation of L- and non-L, non-N-type calcium channels by basal and stimulated protein kinase C activation in insulin-secreting RINm5F cells. FEBS Lett. 391, 189–194.

    Article  PubMed  CAS  Google Scholar 

  107. Codignola A., Tarroni P., Clementi F., Pollo A., Lovallo M., Carbone E., and Sher E. (1993) Calcium channel subtypes controlling serotonin release from human small cell lung carcinoma cell lines. J. Biol. Chem. 268, 26,240–26,247.

    CAS  Google Scholar 

  108. Martini M., Rossi M. L., Rubbini G., and Rispoli G. (2000) Calcium currents in hair cells isolated from semicircular canals of the frog. Biophys. J. 78, 1240–1245.

    PubMed  CAS  Google Scholar 

  109. Rodriguez-Contreras A. and Yamoah E. N. (2001) Direct measurement of single-channel Ca2+ currents in bullfrog hair cells reveals two distinct channel subtypes. J. Physiol. 534.3, 669–689.

    Article  Google Scholar 

  110. Platzer J., Engel J., Schrott-Fischer A., Stephan K., Bova S., Chen H., Zheng H., and Striessnig J. (2000) Congenital deafness and sinoatrial node dysfunction in mice lacking class D L-type Ca2+ channels. Cell 102, 89–97.

    Article  PubMed  CAS  Google Scholar 

  111. Albillos A., Artalejo A. R., López M. G., Gandía L., García A. G., and Carbone E. (1994) Ca2+ channel subtypes in cat chromaffin cells. J. Physiol. 477, 197–213.

    PubMed  CAS  Google Scholar 

  112. Mikami A., Imoto K., Tanabe T., et al. (1989) Primary structure and functional expression of the cardiac dihydropyridine-sensitive calcium channel. Nature 340, 230–233.

    Article  PubMed  CAS  Google Scholar 

  113. Carabelli V., D’Ascenzo M., Carbone E., and Grassi C. (2002) Nitric oxide inhibits neuroendocrine Cav1 L-channel gating via cGMP-dependent protein kinase in cell-attached patches of bovine chromaffin cells. J. Physiol. 541, 351–366.

    Article  PubMed  CAS  Google Scholar 

  114. Gillis K. D. (1995) Techniques for membrane capacitance measurements, in Single-channel recording, 2nd edition, Sackmann B., and Neher E., eds, Plenum Press, New York, pp. 155–198.

    Google Scholar 

  115. Chow R. H. and Von Ruden L. (1995) Electrochemical detection of secretion from single cells, in Single-channel recording, 2nd edition, Sackmann B., and Neher E., eds, Plenum Press, New York, pp. 245–275.

    Google Scholar 

  116. Hernández-Guijo J. M., de Pascual R., Garcïa A. G., and Gandía L. (1998) Separation of calcium channel current components in mouse chromaffin cells superfused with low- and high-barium solutions. Pflügers Arch.-Eur. J. Physiol. 436, 75–82.

    Article  Google Scholar 

  117. Ulate G., Scott R. S., González J., Gilabert J. A., and Artalejo A. R. (2000) Extracellular ATP regulates exocytosis by inhibiting multiple Ca2+ channel types in bovine chromaffin cells Pflügers Arch.-Eur. J. Physiol. 439, 304–314.

    Article  CAS  Google Scholar 

  118. Powell A. D., Teschemacher A. G., and Seward E. P. (2000) P2Y purinoceptors inhibit exocytosis in adrenal chromaffin cells via modulation of voltage-operated calcium channels. J. Neurosci. 15, 606–616.

    Google Scholar 

  119. Morita K., Dohi T., Kitayama S., Koyama Y., and Tsujimoto A. (1987) Stimulation-evoked Ca2+ fluxes in cultured bovine adrenal chromaffin cells are enhanced by forskolin. J. Neurochem. 48, 248–252.

    Article  PubMed  CAS  Google Scholar 

  120. Parramón M., Gonzólez M. P., and Oset-Gasque M. J. (1995) A reassessment of the modulatory role of cyclic AMP in catecholamine secretion by chromaffin cells. Br. J. Pharmacol. 114, 517–523.

    PubMed  Google Scholar 

  121. Przywara D. A., Guo X., Angelilli M. L., Wakade T. D., and Wakade A. R. (1996) A noncholinergic transmitter, pituitary adenylate cyclase-activating polypeptide, utilizes a novel mechanism to evoke catecholamine secretion in rat adrenal chromaffin cells. J. Biol. Chem. 271, 10,545–10,550.

    CAS  Google Scholar 

  122. Machado J. D., Morales A., Gómez J. F., and Borges R. (2001) cAMP modulates exocytotic kinetics and increases quantal size in chromaffin cells. Mol. Pharmacol. 60, 514–520.

    PubMed  CAS  Google Scholar 

  123. Baker E. M., Cheek T. R., and Burgoyne R. D. (1985) cAMP inhibits secretion from bovine adrenal chromaffin cells evoked by carbamylcholine but not by high K+. Biochim. Biophys. Acta. 846, 388–393.

    Article  PubMed  CAS  Google Scholar 

  124. Gandía L., Vitale M. L., Villaroya M., Ramírez-Lavergne C., García A. G., and Trifar J. M. (1997) Differential aspects of forskolin and 1,9-dideoxy-forskolin on nicotinic receptor- and K+-induced responses in chromaffin cells. Eur. J. Pharmacol. 329, 189–199.

    PubMed  Google Scholar 

  125. Jorgensen M. S., Liu J., Adams J. M., Titlow W. B., and Jackson B. A. (2002) Inhibition of voltage-gated Ca2+ current by PACAP in rat adrenal chromaffin cells. Regulatory Peptides 103, 59–65.

    Article  PubMed  CAS  Google Scholar 

  126. Artalejo C. R., Adams M. E., and Fox A. P. (1994) Three types of Ca2+ channel trigger secretion with different efficacies in chromaffin cells. Nature 367, 72–76.

    Article  PubMed  CAS  Google Scholar 

  127. Doupnik C. A. and Pun R. Y. K. (1994) G-protein activation mediates prepulse facilitation of Ca2+ channel currents in bovine chromaffin cells. J. Mol. Biol. 140, 47–56.

    CAS  Google Scholar 

  128. Lambolez B., Audinot E., Bochet P., Crépel F., and Rossier J. (1992) AMPA receptor subunits expressed by single Purkinje cells. Neuron 9, 247–258.

    Article  PubMed  CAS  Google Scholar 

  129. Plant T. D., Shirra C., Katz E., Uchitel E. D., and Konnerth A. (1998) Single-cell RT-PCR and functional characterization of Ca2+ channels in motoneurons of the rat facial nucleus. J. Neuroscience 18, 9573–9584.

    CAS  Google Scholar 

  130. Walter H. J., McMahon T., Dadgar J., Wang D., and Messing R. O. (2000) Ethanol regulates calcium channel subunits by protein kinase C delta-dependent and -independent mechanisms. J. Biol. Chem. 275, 25,717–25,722.

    CAS  Google Scholar 

  131. Yang S. N., Larsson O., Branstrom R., et al. (1999) Syntaxin 1 interacts with the L(D) subtype of voltage-gated Ca2+ channels in pancreatic beta cells. Proc. Nat. Acad. Sci. USA 96, 10,164–10,169.

    CAS  Google Scholar 

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Baldelli, P., Hernández-Guijo, J.M., Carabelli, V. et al. Direct and remote modulation of l-channels in chromaffin cells. Mol Neurobiol 29, 73–96 (2004). https://doi.org/10.1385/MN:29:1:73

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