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.
Similar content being viewed by others
References
Hofmann F., Lacinov L., and Klugbauer N. (1999) Voltage-dependent calcium channels: from structure to function. Rev. Physiol. Biochem. Pharmacol. 139, 33–87.
Catterall W. A. (2000) Structure and regulation of voltage-gated Ca2+ channels. Annu. Rev. Cell Dev. Biol. 16, 521–555.
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.
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.
Dolphin A. C. (1996) Facilitation of Ca2+ currents in excitable cells. Trends in Neurosci. 19, 35–43.
Dolphin A. C. (1999) L-type calcium channel modulation. Advances in Second Messenger and Phosphoprotein Res. 33, 153–170.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Rockman H. A., Koch W. J., and Leifkowitz R. J. (2002) Seven-transmembrane-spanning receptors and heart function. Nature 415, 208–212.
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.
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.
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.
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.
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.
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.
Pietrobon D. and Hess P. (1990) Novel mechanism of voltage-dependent gating in L-type calcium channels. Nature 346, 651–655.
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.
Kavalali E. T. and Plummer M. R. (1996) Multiple voltage-dependent mechanisms potentiate calcium channel activity in hippocampal neurons. J. Neurosci. 16, 1072–1082.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Mintz I. M. and Bean B. P. (1993) GABAB receptor inhibition of P-type Ca2+ channels in central neurons. Neuron 10, 889–898.
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.
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.
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.
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.
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.
Hille B. (1994) Modulation of ion channel function by G-protein coupled receptors. Trends in Neurosci. 17, 531–536.
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.
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.
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.
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.
Reuter H. (1983) Calcium channel modulation by neurotransmitters, enzymes and drugs. Nature 301, 569–574.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
García A. G. and Carbone E. (1996) Calcium-current facilitation in chromaffin cells. Trends Neurosci. 19, 383–385.
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.
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.
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.
Trautwein W. and Hescheler J. (1990) Regulation of cardiac L-type calcium current by phosphorylation and G proteins. Annu. Rev. Physiol. 52, 257–274.
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.
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.
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.
Strosberg A. D. (1997) Structure and function of the β3-adrenergic receptor. Annu. Rev. Pharmacol. Toxicol. 37, 421–450.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Lipscombe D. (2002) L-type calcium channels. Circ. Res. 90, 933–935.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Lambolez B., Audinot E., Bochet P., Crépel F., and Rossier J. (1992) AMPA receptor subunits expressed by single Purkinje cells. Neuron 9, 247–258.
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.
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.
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.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1385/MN:29:1:73