Abstract
There are many different calcium channels expressed in the mammalian nervous system, but N-type and P/Q-type calcium channels appear to dominate the presynaptic terminals of central and peripheral neurons. The neurotransmitter-induced modulation of these channels can result in alteration of synaptic transmission. This review highlights the mechanisms by which neurotransmitters affect the activity of N-type and P/Q-type calcium channels. The inhibition of these channels by voltage-dependent and voltage-independent mechanisms is emphasized because of the wealth of information available on the intracellular mediators and on the effect of these pathways on the single-channel gating.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Abdulla, F. A., and Smith, P. A., (1997). J. Neurosci. 17, 8721–8872.
Abrahams, T. P., and Schofield, G. G., (1992). Eur. J. Pharmacol. 227, 189–197.
Allen, T. G., (1999). J. Physiol. 515, (Pt. 1), 93–107.
Aosaki, T., and Kasai, H., (1989). Pflugers Arch. 414, 150–156.
Bayliss, D. A., Umemiya, M., and Berger, A. J., (1995). J. Physiol. 485, (Pt. 3), 635–647.
Bayliss, D. A., Viana, F., Talley, E. M., and Berger, A. J., (1997). Respir. Physiol. 110, 139–150.
Bean, B. P., (1989). Nature, 340, 153–156.
Bech-Hansen, N. T., Naylor, M. J., Maybaum, T. A., Pearce, W. G., Koop, B., Fishman, G. A., Mets, M., Musarella, M. A., and Boycott, K. M., (1998). Nat. Genet. 19, 264–267.
Beech, D. J., Bernheim, L., and Hille, B., (1992). Neuron, 8, 97–106.
Beech, D. J., Bernheim, L., Mathie, A., and Hille, B., (1991). Proc. Natl. Acad. Sci. U. S. A. 88, 652–656.
Belles, B., Hescheler, J., Trautwein, W., Blomgren, K., and Karlsson, J. O., (1988). Pflugers Arch. 412, 554–556.
Bernheim, L., Beech, D. J., and Hille, B., (1991). Neuron, 6, 859–867.
Bernheim, L., Mathie, A., and Hille, B., (1992). Proc. Natl. Acad. Sci. U. S. A. 89, 9544–9548.
Bertolino, M., and Llinas, R. R., (1992). Annu. Rev. Pharmacol. Toxicol. 32, 399–421.
Boland, L. M., and Bean, B. P., (1993). J. Neurosci. 13, 516–533.
Bourinet, E., Soong, T. W., Sutton, K., Slaymaker, S., Mathews, E., Monteil, A., Zamponi, G. W., Nargeot, J., and Snutch, T. P., (1999). Nat. Neurosci. 2, 407–415.
Brody, D. L., Patil, P. G., Mulle, J. G., Snutch, T. P., and Yue, D. T., (1997). J. Physiol. 499, (Pt. 3), 637–644.
Brody, D. L., and Yue, D. T., (2000). J. Neurosci. 20, 889–898.
Carabelli, V., Hernandez-Guijo, J. M., Baldelli, P., and Carbone, E., (2001). J. Physiol. 532, 73–90.
Carabelli, V., Lovallo, M., Magnelli, V., Zucker, H., and Carbone, E., (1996). Biophys. J. 70, 2144–2154.
Carbone, E., Carabelli, V., Cesetti, T., Baldelli, P., Hernandez-Guijo, J. M., and Giusta, L., (2001). Pflugers Arch. 442, 801–813.
Cardozo, D. L., and Bean, B. P., (1995). J. Neurophysiol. 74, 1137–1148.
Catterall, W. A., (2000). Annu. Rev. Cell. Dev. Biol. 16, 521–555.
Caulfield, M. P., Jones, S., Vallis, Y., Buckley, N. J., Kim, G. D., Milligan, G., and Brown, D. A., (1994). J. Physiol. 477, (Pt. 3), 415–422.
Chemin, J., Monteil, A., Perez-Reyes, E., Nargeot, J., and Lory, P., (2001). EMBO. J. 20, 7033–7040.
Chen, C., and Schofield, G. G., (1993). Eur. J. Pharmacol. 243, 83–86.
Chen, C., and Schofield, G. G., (1995). J. Physiol. 482, (Pt. 3), 521–531.
Cohen, D. P., Ikeda, S. R., and Lewis, D. L., (1996). J. Soc. Gynecol. Investig. 3, 342–349.
Colecraft, H. M., Patil, P. G., and Yue, D. T., (2000). J. Gen. Physiol. 115, 175–192.
Colecraft, H. M., Brody, D. L., and Yue, D. T., (2001). J. Neurosci. 21, 1137–1147.
Cox, D. H., and Dunlap, K., (1992). J. Neurosci. 12, 906–914.
Currie, K. P., and Fox, A. P., (1997). J. Neurosci. 17, 4570–4579.
Currie, K. P., and Fox, A. P., (2002). J. Physiol. 539, 419–431.
Delmas, P., Abogadie, F. C., Dayrell, M., Haley, J. E., Milligan, G., Caulfield, M. P., Brown, D. A., and Buckley, N. J., (1998a). Eur. J. Neurosci. 10, 1654–1666.
Delmas, P., Abogadie, F. C., Milligan, G., Buckley, N. J., and Brown, D. A., (1999). J. Physiol. 518, (Pt. 1), 23–36.
Delmas, P., Brown, D. A., Dayrell, M., Abogadie, F. C., Caulfield, M. P., and Buckley, N. J., (1998b). J. Physiol. 506, (Pt. 2), 319–329.
Diverse-Pierluissi, M., and Dunlap, K., (1993). Neuron, 10, 753–760.
Diverse-Pierluissi, M., Goldsmith, P. K., and Dunlap, K., (1995). Neuron, 14, 191–200.
Diverse-Pierluissi, M., McIntire, W. E., Myung, C. S., Lindorfer, M. A., Garrison, J. C., Goy, M. F., and Dunlap, K., (2000). J. Biol. Chem. 275, 28380–28385.
Diverse-Pierluissi, M., Remmers, A. E., Neubig, R. R., and Dunlap, K., (1997). Proc. Natl. Acad. Sci. U. S. A. 94, 5417–5421.
Dolphin, A. C., (1998). J. Physiol. 506, (Pt. 1), 3–11.
Drolet, P., Bilodeau, L., Chorvatova, A., Laflamme, L., Gallo-Payet, N., and Payet, M. D., (1997). Mol. Endocrinol. 11, 503–514.
Dunlap, K., and Fischbach, G. D., (1978). Nature, 276, 837–839.
Eckert, R., and Trautwein, W., (1991). Neurosci. Lett. 129, 123–126.
Ehrlich, I., and Elmslie, K. S., (1995). J. Neurophysiol. 74, 2251–2257.
Elmslie, K. S., (1992). J. Physiol. 451, 229–246.
Elmslie, K. S., Kammermeier, P. J., and Jones, S. W., (1994). Neuron, 13, 217–228.
Elmslie, K. S., and Jones, S. W., (1994). J. Physiol. 481, (Pt. 1), 35–46.
Elmslie, K. S., Zhou, W., and Jones, S. W., (1990). Neuron, 5, 75–80.
Foehring, R. C., (1996). J. Neurophysiol. 75, 648–659.
Foucart, S., Bleakman, D., Bindokas, V. P., and Miller, R. J., (1993). J. Pharmacol. Exp. Ther. 265, 903–909.
Fukuda, K., Kaneko, S., Yada, N., Kikuwaka, M., Akaike, A., and Satoh, M., (1996). Neurosci. Lett. 217, 13–16.
Galvan, M., and Adams, P. R., (1982). Brain Res. 244, 135–144.
Garcia, D. E., Li, B., Garcia-Ferreiro, R. E., Hernandez-Ochoa, E. O., Yan, K., Gautam, N., Catterall, W. A., Mackie, K., and Hille, B., (1998). J. Neurosci. 18, 9163–9170.
Golard, A., Role, L., and Siegelbaum, S. A., (1994). J. Neurophysiol. 72, 2683–2690.
Golard, A., and Siegelbaum, S. A., (1993). J. Neurosci. 13, 3884–3894.
Grassi, F., and Lux, H. D., (1989). Neurosci. Lett. 105, 113–119.
Gray, R., and Johnston, D., (1987). Nature, 327, 620–622.
Harkins, A. B., and Fox, A. P., (2000). Brain Res. 885, 231–239.
Herlitze, S., Garcia, D. E., Mackie, K., Hille, B., Scheuer, T., and Catterall, W. A., (1996). Nature, 380, 258–262.
Hille, B., (1994). Trends Neurosci, 17, 531–536.
Hillyard, D. R., Monje, V. D., Mintz, I. M., Bean, B. P., Nadasdi, L., Ramachandran, J., Miljanich, G., Azimi-Zoonooz, A., McIntosh, J. M., Cruz, L. J., Imperial, J. S., Olivera, B. M., (1992). A new Conus peptide ligand for mammalian presynaptic Ca2+ channels., Neuron, 9, 69–77.
Howe, A. R., and Surmeier, D. J., (1995). J. Neurosci. 15, 458–469.
Huguenard, J. R., (1999). Adv. Neurol. 79, 991–999.
Huguenard, J. R., Chung, J. M., and Prince, D. A., (1996). Epilepsy Res. Suppl. 12, 129–135.
Ikeda, S. R. (1991). J. Physiol. 439, 181–214.
Ikeda, S. R. (1992). J. Physiol. 458, 339–359.
Ikeda, S. R. (1996) Nature, 380, 255–258.
Ikeda, S. R., Lovinger, D. M., McCool, B. A., and Lewis, D. L. (1995). Neuron, 14, 1029–1038.
Ikeda, S. R., and Schofield, G. G. (1989). J. Physiol. 409, 221–240.
Jarvis, S. E., Magga, J. M., Beedle, A. M., Braun, J. E., and Zamponi, G. W. (2000)., J. Biol. Chem. 275, 6388–6394.
Jones, S. W. (1991)., Biophys. J. 60, 502–507.
Jones, S. W., and Elmslie, K. S. (1997)., J. Membr. Biol. 155, 1–10.
Jones, S. W., and Marks, T. N. (1989)., J. Gen. Physiol. 94, 151–167.
Jones, L. P., Patil, P. G., Snutch, T. P., and Yue, D. T. (1997). J. Physiol. 498, (Pt. 3), 601–610.
Kammermeier, P. J., and Ikeda, S. R., (1999). Neuron, 22, 819–829.
Kammermeier, P. J., Ruiz-Velasco, V., and Ikeda, S. R., (2000). J. Neurosci. 20, 5623–5629.
Kasai, H., (1992). J. Physiol. 448, 189–209.
Kasai, H., and Aosaki, T., (1989). Pflugers Arch. 414, 145–149.
Keren, O., Gafni, M., and Sarne, Y., (1997). Brain Res. 764, 277–282.
Keren, O., Gafni, M., and Sarne, Y., (1999). Brain Res. 843, 193–198.
Kerr, L. M., and Yoshikami, D., (1984). Nature, 308, 282–284.
Koh, D. S., and Hille, B., (1997). Proc. Natl. Acad. Sci. U. S. A. 94, 1506–1511.
Lee, H. K., and Elmslie, K. S., (1999). J. Gen. Physiol. 113, 111–124.
Lee, H. K., and Elmslie, K. S., (2000). J. Neurosci. 20, 3115–3128.
Lee, H. K., Liu, L., and Elmslie, K. S., (2000). J. Neurophysiol. 83, 791–795.
Liu, L., Barrett, C. F., and Rittenhouse, A. R., (2001). Am. J. Physiol. Cell Physiol. 280, C1293–C1305.
Liu, L., and Rittenhouse, A. R., (2000). J. Physiol. 525, Pt. 2, 391–404.
Lu, Q., AtKisson, M. S., Jarvis, S. E., Feng, Z. P., Zamponi, G. W., and Dunlap, K., (2001). J. Neurosci. 21, 2949–2957.
Luebke, J. I., and Dunlap, K., (1994). Pflugers Arch. 428, 499–507.
Mackie, K., and Hille, B., (1992). Proc. Natl. Acad. Sci. U. S. A. 89, 3825–3829.
Marchetti, C., Carbone, E., and Lux, H. D., (1986). Pflugers Arch. 406, 104–111.
Mathie, A., Bernheim, L., and Hille, B., (1992). Neuron, 8, 907–914.
McDonald, T. F., Pelzer, S., Trautwein, W., and Pelzer, D. J., (1994). Physiol. Rev. 74, 365–507.
Mehrke, G., Pereverzev, A., Grabsch, H., Hescheler, J., and Schneider, T., (1997). FEBS Lett. 408, 261–270.
Meir, A., Ginsburg, S., Butkevich, A., Kachalsky, S. G., Kaiserman, I., Ahdut, R., Demirgoren, S., and Rahamimoff, R., (1999). Physiol. Rev. 79, 1019–1088.
Menon-Johansson, A. S., Berrow, N., and Dolphin, A. C., (1993). Pflugers Arch. 425, 335–343.
Meza, U., and Adams, B., (1998). J. Neurosci. 18, 5240–5252.
Mintz, I. M., and Bean, B. P., (1993). Neuron, 10, 889–898.
Mintz, I. M., Venema, V. J., Swiderek, K. M., Lee, T. D., Bean, B. P., and Adams, M. E., (1992). Nature, 355, 827–829.
Mogul, D. J., Adams, M. E., and Fox, A. P., (1993). Neuron, 10, 327–334.
Morikawa, H., Mima, H., Uga, H., Shoda, T., and Fukuda, K., (1999). Pflugers Arch. 438, 423–426.
Nowycky, M. C., Fox, A. P., and Tsien, R. W., (1985). Nature, 316, 440–443.
Olivera, B. M., Gray, W. R., Zeikus, R., McIntosh, J. M., Varga, J., Rivier, J., de Santos, V., and Cruz, L. J., (1985). Science, 230, 1338–1343.
Page, K. M., Stephens, G. J., Berrow, N. S., and Dolphin, A. C., (1997). J. Neurosci. 17, 1330–1338.
Park, D., and Dunlap, K., (1998). J. Neurosci. 18, 6757–6766.
Park, K. S., Jeong, S. W., Cha, S. K., Lee, B. S., Kong, I. D., Ikeda, S. R., and Lee, J. W., (2001). J. Pharmacol. Exp. Ther. 299, 501–508.
Patil, P. G., de Leon, M., Reed, R. R., Dubel, S., Snutch, T. P., and Yue, D. T., (1996). Biophys. J. 71, 2509–2521.
Penington, N. J., Kelly, J. S., and Fox, A. P., (1991). J. Neurosci. 11, 3594–3609.
Perez-Reyes, E., Cribbs, L. L., Daud, A., Lacerda, A. E., Barclay, J., Williamson, M. P., Fox, M., Rees, M., and Lee, J. H., (1998). Nature, 391, 896–900.
Pfrieger, F. W., Gottmann, K., and Lux, H. D., (1994). Neuron, 12, 97–107.
Pietrobon, D., (2002). Mol. Neurobiol. 25, 31–50.
Plummer, M. R., Rittenhouse, A., Kanevsky, M., and Hess, P., (1991). J. Neurosci. 11, 2339–2348.
Plummer, M. R., Logothetis, D. E., and Hess, P., (1989). Neuron, 2, 1453–1463.
Qin, N., Platano, D., Olcese, R., Stefani, E., and Birnbaumer, L., (1997). Proc. Natl. Acad. Sci. U. S. A. 94, 8866–8871.
Randall, A., and Tsien, R. W., (1995). J. Neurosci. 15, 2995–3012.
Rane, S. G., Walsh, M. P., McDonald, J. R., and Dunlap, K., (1989). Neuron, 3, 239–245.
Ruiz-Velasco, V., and Ikeda, S. R., (2000). J. Neurosci. 20, 2183–2191.
Sather, W. A., Tanabe, T., Zhang, J. F., Mori, Y., Adams, M. E., and Tsien, R. W., (1993). Neuron, 11, 291–303.
Schofield, G. G., (1990). Eur. J. Pharmacol. 180, 37–47.
Schofield, G. G., (1991). Eur. J. Pharmacol. 207, 195–207.
Schofield, G. G., and Ikeda, S. R., (1988). Eur. J. Pharmacol. 151, 131–134.
Shapiro, M. S., and Hille, B., (1993). Neuron, 10, 11–20.
Shapiro, M. S., Wollmuth, L. P., and Hille, B., (1994a). J. Neurosci. 14, 7109–7116.
Shapiro, M. S., Wollmuth, L. P., and Hille, B., (1994b). Neuron, 12, 1319–1329.
Simen, A. A., Lee, C. C., Simen, B. B., Bindokas, V. P., and Miller, R. J., (2001). J. Neurosci. 21, 7587–7597.
Simen, A. A., and Miller, R. J., (1998). J. Neurosci. 18, 3689–3698.
Simen, A. A., and Miller, R. J., (2000). Mol. Pharmacol. 57, 1064–1074.
Stewart, A. E., Yan, Z., Surmeier, D. J., and Foehring, R. C., (1999). J. Neurophysiol. 81, 72–84.
Strom, T. M., Nyakatura, G., Apfelstedt-Sylla, E., Hellebrand, H., Lorenz, B., Weber, B. H., Wutz, K., Gutwillinger, N., Ruther, K., Drescher, B., Sauer, C., Zrenner, E., Meitinger, T., Rosenthal, A., and Meindl, A., (1998). Nat. Genet. 19, 260–263.
Swartz, K. J., and Bean, B. P., (1992). J. Neurosci. 12, 4358–4371.
Talley, E. M., Cribbs, L. L., Lee, J. H., Daud, A., Perez-Reyes, E., and Bayliss, D. A., (1999). J. Neurosci. 19, 1895–1911.
Toth, P. T., Bindokas, V. P., Bleakman, D., Colmers, W. F., and Miller, R. J., (1993). Nature, 364, 635–639.
Toth, P. T., Shekter, L. R., Ma, G. H., Philipson, L. H., and Miller, R. J., (1996). J. Neurosci. 16, 4617–4624.
Tottene, A., Volsen, S., and Pietrobon, D., (2000). J. Neurosci. 20, 171–178.
Umemiya, M., and Berger, A. J., (1994). Neuron, 13, 1439–1446.
Wanke, E., Ferroni, A., Malgaroli, A., Ambrosini, A., Pozzan, T., and Meldolesi, J., (1987). Proc. Natl. Acad. Sci. U. S. A. 84, 4313–4317.
Washburn, D. L., and Ferguson, A. V., (2001). J. Physiol. 536, 667–675.
Williams, S., Serafin, M., Muhlethaler, M., and Bernheim, L., (1997). J. Neurosci. 17, 1625–1632.
Williams, S., Serafin, M., Muhlethaler, M., and Bernheim, L., (1998). Eur. J. Neurosci. 10, 3291–3294.
Wilson, S. M., Toth, P. T., Oh, S. B., Gillard, S. E., Volsen, S., Ren, D., Philipson, L. H., Lee, E. C., Fletcher, C. F., Tessarollo, L., Copeland, N. G., Jenkins, N. A., and Miller, R. J., (2000). J. Neurosci. 20, 8566–8571.
Wollmuth, L. P., Shapiro, M. S., and Hille, B., (1995). J. Neurophysiol. 73, 1323–1328.
Womack, M. D., and McCleskey, E. W., (1995). J. Neurophysiol. 73, 1793–1798.
Xu, W., and Lipscombe, D., (2001). J. Neurosci. 21, 5944–5951.
Yawo, H., and Chuhma, N., (1993). Nature, 365, 256–258.
Yoshimura, N., Seki, S., and de Groat, W. C., (2001). J. Neurophysiol. 86, 304–311.
Yue, D. T., Herzig, S., and Marban, E., (1990). Proc. Natl. Acad. Sci. U. S. A. 87, 753–757.
Zamponi, G. W., Bourinet, E., Nelson, D., Nargeot, J., and Snutch, T. P., (1997). Nature, 385, 442–446.
Zhang, J. F., Ellinor, P. T., Aldrich, R. W., and Tsien, R. W., (1996). Neuron, 17, 991–1003.
Zhang, J. F., Randall, A. D., Ellinor, P. T., Horne, W. A., Sather, W. A., Tanabe, T., Schwarz, T. L., and Tsien, R. W., (1993). Neuropharmacology, 32, 1075–1088.
Zhou, W., and Jones, S. W., (1995). J. Gen. Physiol. 105, 441–462.
Zhu, Y., and Ikeda, S. R., (1993). J. Neurophysiol. 70, 610–620.
Zhu, Y., and Ikeda, S. R., (1994a). Neuron, 13, 657–669.
Zhu, Y., and Ikeda, S. R., (1994b). J. Neurophysiol. 72, 1549–1560.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Elmslie, K.S. Neurotransmitter Modulation of Neuronal Calcium Channels. J Bioenerg Biomembr 35, 477–489 (2003). https://doi.org/10.1023/B:JOBB.0000008021.55853.18
Issue Date:
DOI: https://doi.org/10.1023/B:JOBB.0000008021.55853.18