Table of Contents
ISRN Neurology
Volume 2011, Article ID 919043, 7 pages
http://dx.doi.org/10.5402/2011/919043
Review Article

Ca2+/Calmodulin and Presynaptic Short-Term Plasticity

Department of Physiology, Tokyo Medical University, 1-1 Shinjuku-6-chome, Shinjuku-ku, Tokyo 160-8402, Japan

Received 22 March 2011; Accepted 18 April 2011

Academic Editors: L. Srivastava and F. G. Wouterlood

Copyright © 2011 Sumiko Mochida. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. T. C. Südhof, “The synaptic vesicle cycle,” Annual Review of Neuroscience, vol. 27, pp. 509–547, 2004. View at Publisher · View at Google Scholar · View at PubMed
  2. T. I. Nishiki and G. J. Augustine, “Synaptotagmin I synchronizes transmitter release in mouse hippocampal neurons,” Journal of Neuroscience, vol. 24, no. 27, pp. 6127–6132, 2004. View at Publisher · View at Google Scholar · View at PubMed
  3. Z. P. Pang, J. Sun, J. Rizo, A. Maximov, and T. C. Südhof, “Genetic analysis of synaptotagmin 2 in spontaneous and Ca2+ -triggered neurotransmitter release,” EMBO Journal, vol. 25, no. 10, pp. 2039–2050, 2006. View at Publisher · View at Google Scholar · View at PubMed
  4. J. Sun, Z. P. Pang, D. Qin, A. T. Fahim, R. Adachi, and T. C. Südhof, “A dual-Ca2+-sensor model for neurotransmitter release in a central synapse,” Nature, vol. 450, no. 7170, pp. 676–682, 2007. View at Publisher · View at Google Scholar · View at PubMed
  5. M. Yoshihara and J. T. Littleton, “Synaptotagmin functions as a calcium sensor to synchronize neurotransmitter release,” Neuron, vol. 36, no. 5, pp. 897–908, 2002. View at Publisher · View at Google Scholar
  6. Y. A. Chen and R. H. Scheller, “SNARE-mediated membrane fusion,” Nature Reviews Molecular Cell Biology, vol. 2, no. 2, pp. 98–106, 2001. View at Publisher · View at Google Scholar · View at PubMed
  7. J. Di Giovanni, C. C. Iborra, Y. Maulet, C. Lévêque, O. El Far, and M. Seagar, “Calcium-dependent regulation of SNARE-mediated membrane fusion by calmodulin,” Journal of Biological Chemistry, vol. 285, no. 31, pp. 23665–23675, 2010. View at Publisher · View at Google Scholar · View at PubMed
  8. R. Schneggenburger and E. Neher, “Intracellular calcium dependence of transmitter release rates at a fast central synapse,” Nature, vol. 406, no. 6798, pp. 889–993, 2000. View at Publisher · View at Google Scholar · View at PubMed
  9. X. S. Wu, B. D. McNeil, J. Xu et al., “Ca2+ and calmodulin initiate all forms of endocytosis during depolarization at a nerve terminal,” Nature Neuroscience, vol. 12, no. 8, pp. 1003–1010, 2009. View at Publisher · View at Google Scholar · View at PubMed
  10. A. Lee, S. T. Wong, D. Gallagher et al., “Ca2+/calmodulin binds to and modulates P/Q-type calcium channels,” Nature, vol. 399, no. 6732, pp. 155–159, 1999. View at Publisher · View at Google Scholar · View at PubMed
  11. M. Popoli, “Synaptotagmin is endogenously phosphorylated by Ca2+/calmodulin protein kinase II in synaptic vesicles,” FEBS Letters, vol. 317, no. 1–2, pp. 85–88, 1993. View at Publisher · View at Google Scholar
  12. J. B. Park, C. C. Farnsworth, and J. A. Glomset, “Ca2+/calmodulin causes Rab3a to dissociate from synaptic membranes,” Journal of Biological Chemistry, vol. 272, no. 33, pp. 20857–20865, 1997. View at Publisher · View at Google Scholar
  13. H. J. Junge, J. S. Rhee, O. Jahn et al., “Calmodulin and Munc13 form a Ca2+ sensor/effector complex that controls short-term synaptic plasticity,” Cell, vol. 118, no. 3, pp. 389–401, 2004. View at Publisher · View at Google Scholar · View at PubMed
  14. B. Marks and H. T. McMahon, “Calcium triggers calcineurin-dependent synaptic vesicle recycling in mammalian nerve terminals,” Current Biology, vol. 8, no. 13, pp. 740–749, 1998. View at Google Scholar
  15. M. Müller, F. Felmy, B. Schwaller, and R. Schneggenburger, “Parvalbumin is a mobile presynaptic Ca2+ buffer in the calyx of held that accelerates the decay of Ca2+ and short-term facilitation,” Journal of Neuroscience, vol. 27, no. 9, pp. 2261–2271, 2007. View at Publisher · View at Google Scholar · View at PubMed
  16. O. Caillard, H. Moreno, B. Schwaller, I. Llano, M. R. Celio, and A. Marty, “Role of the calcium-binding protein parvalbumin in short-term synaptic plasticity,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 24, pp. 13372–13377, 2000. View at Publisher · View at Google Scholar · View at PubMed
  17. F. Felmy and R. Schneggenburger, “Developmental expression of the Ca2+-binding proteins calretinin and parvalbumin at the calyx of Held of rats and mice,” European Journal of Neuroscience, vol. 20, no. 6, pp. 1473–1482, 2004. View at Publisher · View at Google Scholar · View at PubMed
  18. S. Mochida, “Protein-protein interactions in neurotransmitter release,” Neuroscience Research, vol. 36, no. 3, pp. 175–182, 2000. View at Publisher · View at Google Scholar
  19. T. C. Sudhof, “The synaptic vesicle cycle: a cascade of protein-protein interactions,” Nature, vol. 375, no. 6533, pp. 645–653, 1995. View at Google Scholar
  20. S. Takamori, M. Holt, K. Stenius et al., “Molecular anatomy of a trafficking organelle,” Cell, vol. 127, no. 4, pp. 831–846, 2006. View at Publisher · View at Google Scholar · View at PubMed
  21. H. Ma and S. Mochida, “A cholinergic model synapse to elucidate protein function at presynatic terminals,” Neuroscience Research, vol. 57, no. 4, pp. 491–498, 2007. View at Publisher · View at Google Scholar · View at PubMed
  22. S. Mochida, Y. Nonomura, and H. Kobayashi, “Analysis of the mechanism for acetylcholine release at the synapse formed between rat sympathetic neurons in culture,” Microscopy Research and Technique, vol. 29, no. 2, pp. 94–102, 1994. View at Google Scholar
  23. S. Mochida, H. Kobayashi, Y. Matsuda, Y. Yuda, K. Muramoto, and Y. Nonomura, “Myosin II is involved in transmitter release at synapses formed between rat sympathetic neurons in culture,” Neuron, vol. 13, no. 5, pp. 1131–1142, 1994. View at Publisher · View at Google Scholar
  24. T. Baba, T. Sakisaka, S. Mochida, and Y. Takai, “PKA-catalyzed phosphorylation of tomosyn and its implication in Ca2+ -dependent exocytosis of neurotransmitter,” Journal of Cell Biology, vol. 170, no. 7, pp. 1113–1125, 2005. View at Publisher · View at Google Scholar · View at PubMed
  25. G. Krapivinsky, S. Mochida, L. Krapivinsky, S. M. Cibulsky, and D. Clapham, “The TRPM7 ion channel functions in cholinergic synaptic vesicles and affects transmitter release,” Neuron, vol. 52, no. 3, pp. 485–496, 2006. View at Publisher · View at Google Scholar · View at PubMed
  26. S. Mochida, A. P. Few, T. Scheuer, and W. A. Catterall, “Regulation of presynaptic CaV2.1 Channels by Ca2+ sensor proteins mediates short-term synaptic plasticity,” Neuron, vol. 57, no. 2, pp. 210–216, 2008. View at Publisher · View at Google Scholar · View at PubMed
  27. S. Mochida, R. E. Westenbroek, C. T. Yokoyama, K. Itoh, and W. A. Catterall, “Subtype-selective reconstitution of synaptic transmission in sympathetic ganglion neurons by expression of exogenous calcium channels,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 5, pp. 2813–2818, 2003. View at Publisher · View at Google Scholar · View at PubMed
  28. Y. Nakajima, S. Mochida, K. Okawa, and S. Nakanishi, “Ca2+-dependent release of Munc18-1 from presynaptic mGluRs in short-term facilitation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 43, pp. 18385–18389, 2009. View at Publisher · View at Google Scholar · View at PubMed
  29. H. Ma, Q. Cai, W. Lu, Z. H. Sheng, and S. Mochida, “KIF5B motor adaptor syntabulin maintains synaptic transmission in sympathetic neurons,” Journal of Neuroscience, vol. 29, no. 41, pp. 13019–13029, 2009. View at Publisher · View at Google Scholar · View at PubMed
  30. R. E. Westenbroek, T. Sakurai, E. M. Elliott et al., “Immunochemical identification and subcellular distribution of the α(1A) subunits of brain calcium channels,” Journal of Neuroscience, vol. 15, no. 10, pp. 6403–6418, 1995. View at Google Scholar
  31. K. Dunlap, J. I. Luebke, and T. Turner, “Exocytotic Ca2+ channels in mammalian central neurons,” Trends in Neurosciences, vol. 18, no. 2, pp. 89–98, 1995. View at Publisher · View at Google Scholar
  32. R. M. Evans and G. W. Zamponi, “Presynaptic Ca2+ channels—integration centers for neuronal signaling pathways,” Trends in Neurosciences, vol. 29, no. 11, pp. 617–624, 2006. View at Publisher · View at Google Scholar · View at PubMed
  33. W. A. Catterall, “Structure and regulation of voltage-gated Ca2+ channels,” Annual Review of Cell and Developmental Biology, vol. 16, pp. 521–555, 2000. View at Publisher · View at Google Scholar · View at PubMed
  34. C. D. DeMaria, T. W. Soong, B. A. Alseikhan, R. S. Alvania, and D. T. Yue, “Calmodulin bifurcates the local Ca2+ signal that modulates P/Q-type Ca2+ channels,” Nature, vol. 411, no. 6836, pp. 484–489, 2001. View at Publisher · View at Google Scholar · View at PubMed
  35. A. Lee, T. Scheuer, and W. A. Catterall, “Ca2+/calmodulin-dependent facilitation and inactivation of P/Q-type Ca2+ channels,” Journal of Neuroscience, vol. 20, no. 18, pp. 6830–6838, 2000. View at Google Scholar
  36. A. Lee, H. Zhou, T. Scheuer, and W. A. Catterall, “Molecular determinants of Ca2+/calmodulin-dependent regulation of CaV2.1 channels,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 26, pp. 16059–16064, 2003. View at Publisher · View at Google Scholar · View at PubMed
  37. A. P. Few, N. J. Lautermilch, R. E. Westenbroek, T. Scheuer, and W. A. Catterall, “Differential regulation of CaV2.1 channels by calcium-binding protein 1 and visinin-like protein-2 requires N-terminal myristoylation,” Journal of Neuroscience, vol. 25, no. 30, pp. 7071–7080, 2005. View at Publisher · View at Google Scholar · View at PubMed
  38. N. J. Lautermilch, A. P. Few, T. Scheuer, and W. A. Catterall, “Modulation of CaV2.1 channels by the neuronal calcium-binding protein visinin-like protein-2,” Journal of Neuroscience, vol. 25, no. 30, pp. 7062–7070, 2005. View at Publisher · View at Google Scholar · View at PubMed
  39. A. Lee, R. E. Westenbroek, F. Haeseleer, K. Palczewski, T. Scheuer, and W. A. Catterall, “Differential modulation of CaV2.1 channels by calmodulin and Ca2+-binding protein 1,” Nature Neuroscience, vol. 5, no. 3, pp. 210–217, 2002. View at Publisher · View at Google Scholar · View at PubMed
  40. I. D. Forsythe, T. Tsujimoto, M. Barnes-Davies, M. F. Cuttle, and T. Takahashi, “Inactivation of presynaptic calcium current contributes to synaptic depression at a fast central synapse,” Neuron, vol. 20, no. 4, pp. 797–807, 1998. View at Publisher · View at Google Scholar
  41. J. Xu and L. G. Wu, “The decrease in the presynaptic calcium current is a major cause of short-term depression at a calyx-type synapse,” Neuron, vol. 46, no. 4, pp. 633–645, 2005. View at Publisher · View at Google Scholar · View at PubMed
  42. D. Chaudhuri, B. A. Alseikhan, S. Y. Chang, T. W. Soong, and D. T. Yue, “Developmental activation of calmodulin-dependent facilitation of cerebellar P-type Ca2+ current,” Journal of Neuroscience, vol. 25, no. 36, pp. 8282–8294, 2005. View at Publisher · View at Google Scholar · View at PubMed
  43. J. G. G. Borst and B. Sakmann, “Facilitation of presynaptic calcium currents in the rat brainstem,” Journal of Physiology, vol. 513, no. 1, pp. 149–155, 1998. View at Google Scholar
  44. R. S. Zucker and W. G. Regehr, “Short-term synaptic plasticity,” Annual Review of Physiology, vol. 64, pp. 355–405, 2002. View at Publisher · View at Google Scholar · View at PubMed
  45. C. F. Stevens and J. F. Wesseling, “Augmentation is a potentiation of the exocytotic process,” Neuron, vol. 22, no. 1, pp. 139–146, 1999. View at Publisher · View at Google Scholar
  46. K. L. Magleby, “The effect of tetanic and post tetanic potentiation on facilitation of transmitter release at the frog neuromuscular junction,” Journal of Physiology, vol. 234, no. 2, pp. 353–371, 1973. View at Google Scholar
  47. K. L. Magleby and J. E. Zengel, “A dual effect of repetitive stimulation on post tetanic potentiation of transmitter release at the frog neuromuscular junction,” Journal of Physiology, vol. 245, no. 1, pp. 163–182, 1975. View at Google Scholar
  48. Y. G. Tang and R. S. Zucker, “Mitochondrial involvement in post-tetanic potentiation of synaptic transmission,” Neuron, vol. 18, no. 3, pp. 483–491, 1997. View at Publisher · View at Google Scholar
  49. M. Beierlein, D. Fioravante, and W. G. Regehr, “Differential expression of posttetanic potentiation and retrograde signaling mediate target-dependent short-term synaptic plasticity,” Neuron, vol. 54, no. 6, pp. 949–959, 2007. View at Publisher · View at Google Scholar · View at PubMed
  50. D. H. Brager, X. Cai, and S. M. Thompson, “Activity-dependent activation of presynaptic protein kinase C mediates post-tetanic potentiation,” Nature Neuroscience, vol. 6, no. 6, pp. 551–552, 2003. View at Publisher · View at Google Scholar · View at PubMed
  51. L. F. Abbott and W. G. Regehr, “Synaptic computation,” Nature, vol. 431, no. 7010, pp. 796–803, 2004. View at Publisher · View at Google Scholar · View at PubMed
  52. M. Lorez, U. Humbel, M. C. Pflimlin, and J. N. C. Kew, “Group III metabotropic glutamate receptors as autoreceptors in the cerebellar cortex,” British Journal of Pharmacology, vol. 138, no. 4, pp. 614–625, 2003. View at Publisher · View at Google Scholar · View at PubMed
  53. S. Nakanishi, “Molecular diversity of glutamate receptors and implications for brain function,” Science, vol. 258, no. 5082, pp. 597–603, 1992. View at Google Scholar
  54. J. P. Pin and R. Duvoisin, “The metabotropic glutamate receptors: structure and functions,” Neuropharmacology, vol. 34, no. 1, pp. 1–26, 1995. View at Publisher · View at Google Scholar
  55. R. Shigemoto, A. Kinoshita, E. Wada et al., “Differential presynaptic localization of metabotropic glutamate receptor subtypes in the rat hippocampus,” Journal of Neuroscience, vol. 17, no. 19, pp. 7503–7522, 1997. View at Google Scholar
  56. R. Pekhletski, R. Gerlai, L. S. Overstreet et al., “Impaired cerebellar synaptic plasticity and motor performance in mice lacking the mGluR4 subtype of metabotropic glutamate receptor,” Journal of Neuroscience, vol. 16, no. 20, pp. 6364–6373, 1996. View at Google Scholar
  57. V. O'Connor, O. El Far, E. Bofill-Cardona et al., “Calmodulin dependence of presynaptic metabotropic glutamate receptor signaling,” Science, vol. 286, no. 5442, pp. 1180–1184, 1999. View at Publisher · View at Google Scholar
  58. D. Chin and A. R. Means, “Calmodulin: a prototypical calcium sensor,” Trends in Cell Biology, vol. 10, no. 8, pp. 322–328, 2000. View at Publisher · View at Google Scholar
  59. J. Rizo and T. C. Südhof, “Snares and munc18 in synaptic vesicle fusion,” Nature Reviews Neuroscience, vol. 3, no. 8, pp. 641–653, 2002. View at Google Scholar
  60. J. Shen, D. C. Tareste, F. Paumet, J. E. Rothman, and T. J. Melia, “Selective activation of cognate SNAREpins by Sec1/Munc18 proteins,” Cell, vol. 128, no. 1, pp. 183–195, 2007. View at Publisher · View at Google Scholar · View at PubMed
  61. K. M. S. Misura, R. H. Scheller, and W. I. Weis, “Three-dimensional structure of the neuronal-Sec1-syntaxin 1a complex,” Nature, vol. 404, no. 6776, pp. 355–362, 2000. View at Publisher · View at Google Scholar · View at PubMed
  62. Y. Nakajima, T. Yamamoto, T. Nakayama, and S. Nakanishi, “A relationship between protein kinase C phosphorylation and calmodulin binding to the metabotropic glutamate receptor subtype 7,” Journal of Biological Chemistry, vol. 274, no. 39, pp. 27573–27577, 1999. View at Publisher · View at Google Scholar
  63. P. J. Kammermeier and S. R. Ikedal, “Metabotropic glutamate receptor expression in the rat superior cervical ganglion,” Neuroscience Letters, vol. 330, no. 3, pp. 260–264, 2002. View at Publisher · View at Google Scholar
  64. H. L. Atwood and S. Karunanithi, “Diversification of synaptic strength: presynaptic elements,” Nature Reviews Neuroscience, vol. 3, no. 7, pp. 497–516, 2002. View at Publisher · View at Google Scholar · View at PubMed
  65. J. S. Dittman, A. C. Kreitzer, and W. G. Regehr, “Interplay between facilitation, depression, and residual calcium at three presynaptic terminals,” Journal of Neuroscience, vol. 20, no. 4, pp. 1374–1385, 2000. View at Google Scholar
  66. S. Mochida, Z. -H. Sheng, C. Baker, H. Kobayashi, and W. A. Catterall, “Inhibition of neurotransmission by peptides containing the synaptic protein interaction site of N-type Ca2+ channels,” Neuron, vol. 17, no. 4, pp. 781–788, 1996. View at Publisher · View at Google Scholar