Munc13 C2B domain is an activity-dependent Ca2+ regulator of synaptic exocytosis (original) (raw)

• Katz, B. The Release of Neuronal Transmitter Substances (Liverpool University Press, Liverpool, 1969).
• Abbott, L.F. & Regehr, W.G. Synaptic computation. Nature 431, 796–803 (2004).
  Article CAS Google Scholar
• Zucker, R.S. & Regehr, W.G. Short-term synaptic plasticity. Annu. Rev. Physiol. 64, 355–405 (2002).
  Article CAS Google Scholar
• Mongillo, G., Barak, O. & Tsodyks, M. Synaptic theory of working memory. Science 319, 1543–1546 (2008).
  Article CAS Google Scholar
• Brose, N., Hofmann, K., Hata, Y. & Südhof, T.C. Mammalian homologues of C. elegans unc-13 gene define novel family of C2-domain proteins. J. Biol. Chem. 270, 25273–25280 (1995).
  Article CAS Google Scholar
• Wang, Y., Okamoto, M., Schmitz, F., Hofman, K. & Südhof, T.C. RIM: a putative Rab3 effector in regulating synaptic vesicle fusion. Nature 388, 593–598 (1997).
  Article CAS Google Scholar
• Betz, A. et al. Functional interaction of the active zone proteins Munc13-1 and RIM1 in synaptic vesicle priming. Neuron 30, 183–196 (2001).
  Article CAS Google Scholar
• Schoch, S. et al. RIM1α forms a protein scaffold for regulating neurotransmitter release at the active zone. Nature 415, 321–326 (2002).
  Article CAS Google Scholar
• Dulubova, I. et al. A Munc13/RIM/Rab3 tripartite complex: from priming to plasticity? EMBO J. 24, 2839–2850 (2005).
  Article CAS Google Scholar
• Augustin, I. et al. The cerebellum-specific Munc13 isoform Munc13-3 regulates cerebellar synaptic transmission and motor learning in mice. J. Neurosci. 21, 10–17 (2000).
  Article Google Scholar
• Schlüter, O., Schmitz, F., Jahn, R., Rosenmund, C. & Südhof, T.C. A complete genetic analysis of neuronal Rab3 function. J. Neurosci. 24, 6629–6637 (2004).
  Article Google Scholar
• Rhee, J.-S. et al. Phorbol ester- and diacylglycerol-induced augmentation of neurotransmitter release from hippocampal neurons is mediated by Munc13s and not by PKCs. Cell 108, 121–133 (2002).
  Article CAS Google Scholar
• Junge, H.J. et al. Calmodulin and Munc13 form a Ca2+ sensor/effector complex that controls short-term synaptic plasticity. Cell 118, 389–401 (2004).
  Article CAS Google Scholar
• Basu, J. et al. A minimal domain responsible for Munc13 activity. Nat. Struct. Mol. Biol. 12, 1017–1018 (2005).
  Article CAS Google Scholar
• Xia, Z. & Storm, D.R. The role of calmodulin as a signal integrator for synaptic plasticity. Nat. Rev. Neurosci. 6, 267–276 (2005).
  Article CAS Google Scholar
• Lee, A. et al. Ca2+/calmodulin binds to and modulates P/Q-type calcium channels. Nature 99, 155–159 (1999).
  Article Google Scholar
• DeMaria, C.D., Soong, T.W., Alseikhan, B.A., Alvania, R.S. & Yue, D.T. Calmodulin bifurcates the local Ca2+ signal that modulates P/Q-type Ca2+ channels. Nature 411, 484–489 (2001).
  Article CAS Google Scholar
• Wayman, G.A., Lee, Y.S., Tokumitsu, H., Silva, A. & Soderling, T.R. Calmodulin-kinases: modulators of neuronal development and plasticity. Neuron 59, 914–931 (2008).
  Article CAS Google Scholar
• Sakaba, T. & Neher, E. Calmodulin mediates rapid recruitment of fast-releasing synaptic vesicles at a calyx-type synapse. Neuron 32, 1119–1131 (2001).
  Article CAS Google Scholar
• Huang, Y.Y., Li, X.C. & Kandel, E.R. cAMP contributes to mossy fiber LTP by initiating both a covalently mediated early phase and macromolecular synthesis-dependent late phase. Cell 79, 69–79 (1994).
  Article CAS Google Scholar
• Weisskopf, M.G., Castillo, P.E., Zalutsky, R.A. & Nicoll, R.A. Mediation of hippocampal mossy fiber long-term potentiation by cyclic AMP. Science 265, 878–882 (1994).
  Article Google Scholar
• Augustin, I., Rosenmund, C., Südhof, T.C. & Brose, N. Munc-13 is essential for fusion competence of glutamatergic synaptic vesicles. Nature 400, 457–461 (1999).
  Article CAS Google Scholar
• Varoqueaux, F. et al. Total arrest of spontaneous and evoked synaptic transmission but normal synaptogenesis in the absence of Munc13-mediated vesicle priming. Proc. Natl. Acad. Sci. USA 99, 9037–9042 (2002).
  Article CAS Google Scholar
• Shiratsuchi, T. et al. Cloning and characterization of BAP3 (BAI-associated protein 3), a C2 domain-containing protein that interacts with BAI1. Biochem. Biophys. Res. Commun. 251, 158–165 (1998).
  Article CAS Google Scholar
• Feldmann, J. et al. Munc13-4 is essential for cytolytic granules fusion and is mutated in a form of familial hemophagocytic lymphohistiocytosis (FHL3). Cell 115, 461–473 (2003).
  Article CAS Google Scholar
• Madison, J.M., Nurrish, S. & Kaplan, J.M. UNC-13 interaction with syntaxin is required for synaptic transmission. Curr. Biol. 15, 2236–2242 (2005).
  Article CAS Google Scholar
• Stevens, D.R. et al. Identification of the minimal protein domain required for priming activity of Munc13-1. Curr. Biol. 15, 2243–2248 (2005).
  Article CAS Google Scholar
• Ubach, J., Zhang, X., Shao, X., Südhof, T.C. & Rizo, J. Ca2+ binding to synaptotagmin: how many Ca2+ ions bind to the tip of a C2-domain? EMBO J. 17, 3921–3930 (1998).
  Article CAS Google Scholar
• Sutton, R.B., Davletov, B.A., Berghuis, A.M., Südhof, T.C. & Sprang, S.R. Structure of the first C2 domain of synaptotagmin I: a novel Ca2+/phospholipid-binding fold. Cell 80, 929–938 (1995).
  Article CAS Google Scholar
• Rizo, J. & Südhof, T.C. C2-domains, structure and function of a universal Ca2+-binding domain. J. Biol. Chem. 273, 15879–15882 (1998).
  Article CAS Google Scholar
• Shao, X., Fernandez, I., Südhof, T.C. & Rizo, J. Solution structures of the Ca2+-free and Ca2+-bound C2A domain of synaptotagmin I: does Ca2+ induce a conformational change? Biochemistry 37, 16106–16115 (1998).
  Article CAS Google Scholar
• Fernandez, I. et al. Three-dimensional structure of the synaptotagmin 1 C2B-domain. Synaptotagmin 1 as a phospholipid binding machine. Neuron 32, 1057–1069 (2001).
  Article CAS Google Scholar
• Holm, L. & Sander, C. Protein structure comparison by alignment of distance matrices. J. Mol. Biol. 233, 123–138 (1993).
  Article CAS Google Scholar
• Benfenati, F., Greengard, P., Brunner, J. & Bahler, M. Electrostatic and hydrophobic interactions of synapsin I and synapsin I fragments with phospholipid bilayer. J. Cell Biol. 108, 1851–1862 (1989).
  Article CAS Google Scholar
• Chapman, E.R. & Davis, A.F. Direct interaction of a Ca2+ binding loop of synaptotagmin with lipid bilayers. J. Biol. Chem. 273, 13995–14001 (1998).
  Article CAS Google Scholar
• Zhang, X., Rizo, J. & Südhof, T.C. Mechanism of phospholipid binding by the C2A-domain of synaptotagmin I. Biochemistry 37, 12395–12403 (1998).
  Article CAS Google Scholar
• Gerber, S.H., Rizo, J. & Südhof, T.C. Role of electrostatic and hydrophobic interactions in Ca2+-dependent phospholipid binding by the C2A-domain from synaptotagmin I. Diabetes 51 Suppl 1, S12–S18 (2002).
  Article CAS Google Scholar
• Shin, O.H., Rizo, J. & Südhof, T.C. Synaptotagmin function in dense core vesicle exocytosis studied in cracked PC12 cells. Nat. Neurosci. 5, 649–656 (2002).
  Article CAS Google Scholar
• Fernandez-Chacon, R. et al. Synaptotagmin I functions as a calcium regulator of release probability. Nature 410, 41–49 (2001).
  Article CAS Google Scholar
• Pang, Z.P., Shin, O.H., Meyer, A.C., Rosenmund, C. & Südhof, T.C. A gain-of-function mutation in synaptotagmin-1 reveals a critical role of Ca2+-dependent soluble _N_-ethylmaleimide-sensitive factor attachment protein receptor complex binding in synaptic exocytosis. J. Neurosci. 26, 12556–12565 (2006).
  Article CAS Google Scholar
• Bennett, M.K., Calakos, N. & Scheller, R.H. Syntaxin: a synaptic protein implicated in docking of synaptic vesicles at presynaptic active zones. Science 257, 255–259 (1992).
  Article CAS Google Scholar
• Li, C. et al. Ca2+-dependent and Ca2+-independent activities of neural and nonneural synaptotagmins. Nature 375, 594–599 (1995).
  Article CAS Google Scholar
• Chapman, E.R., Hanson, P.I., An, S. & Jahn, R. Ca2+ regulates the interaction between synaptotagmin and syntaxin 1. J. Biol. Chem. 270, 23667–23671 (1995).
  Article CAS Google Scholar
• Rosenmund, C. et al. Differential control of vesicle priming and short-term plasticity by Munc13 Isoforms. Neuron 33, 411–424 (2002).
  Article CAS Google Scholar
• Rosenmund, C. & Stevens, C.F. Definition of the readily releasable pool of vesicles at hippocampal synapses. Neuron 16, 1197–1207 (1996).
  Article CAS Google Scholar
• Geppert, M. et al. A major Ca2+ sensor for transmitter release at a central synapse. Cell 79, 717–727 (1994).
  Article CAS Google Scholar
• Corbalan-Garcia, S. & Gomez-Fernandez, J.C. Protein kinase C regulatory domains: the art of decoding many different signals in membranes. Biochim. Biophys. Acta 1761, 633–654 (2006).
  Article CAS Google Scholar
• Wierda, K.D., Toonen, R.F., de Wit, H., Brussaard, A.B. & Verhage, M. Interdependence of PKC-dependent and PKC-independent pathways for presynaptic plasticity. Neuron 54, 275–290 (2007).
  Article CAS Google Scholar
• Rhee, J.-S. et al. Phorbol ester- and DAG-induced augmentation of neurotransmitter release from hippocampal neurons is mediated by Munc13s and not by PKCs. Cell 108, 121–133 (2002).
  Article CAS Google Scholar
• Basu, J., Betz, A., Brose, N. & Rosenmund, C. Munc13-1 C1 domain activation lowers the energy barrier for synaptic vesicle fusion. J. Neurosci. 27, 1200–1210 (2007).
  Article CAS Google Scholar
• Ford, M.G. et al. Curvature of clathrin-coated pits driven by epsin. Nature 419, 361–366 (2002).
  Article CAS Google Scholar
• Rhee, J.-S. et al. Augmenting neurotransmitter release by enhancing the apparent Ca2+ affinity of synaptotagmin 1. Proc. Natl. Acad. Sci. USA 102, 18664–18669 (2005).
  Article CAS Google Scholar
• Eberhard, D.A. & Holz, R.W. Calcium promotes the accumulation of polyphosphoinositides in intact and permeabilized bovine adrenal Chromaffin cells. Cell. Mol. Neurobiol. 11, 357–370 (1991).
  Article CAS Google Scholar
• Wenk, M.R. et al. PIP kinase Iγ is the major PI(4,5)P2 synthesizing enzyme at the synapse. Neuron 32, 79–88 (2001).
  Article CAS Google Scholar
• Itoh, T., Ishihara, H., Shibasaki, Y., Oka, Y. & Takenawa, T. Autophosphorylation of type I phosphatidylinositol phosphate kinase regulates its lipid kinase activity. J. Biol. Chem. 275, 19389–19394 (2000).
  Article CAS Google Scholar
• Park, S.J., Itoh, T. & Takenawa, T. Phosphatidylinositol 4-phosphate 5-kinase type I is regulated through phosphorylation response by extracellular stimuli. J. Biol. Chem. 276, 4781–4787 (2001).
  Article CAS Google Scholar
• Südhof, T.C. The synaptic vesicle cycle: a cascade of protein-protein interactions. Nature 375, 645–653 (1995).
  Article Google Scholar
• Gerber, S.H. et al. Conformational switch of syntaxin-1 controls synaptic vesicle fusion. Science 321, 1507–1510 (2008).
  Article CAS Google Scholar
• Rizo, J. & Rosenmund, C. Synaptic vesicle fusion. Nat. Struct. Mol. Biol. 15, 665–674 (2008).
  Article CAS Google Scholar
• Martens, S., Kozlov, M.M. & McMahon, H.T. How synaptotagmin promotes membrane fusion. Science 316, 1205–1208 (2007).
  Article CAS Google Scholar
• Delaglio, F. et al. NMRPipe: a multidimensional spectral processing system based on Unix pipes. J. Biomol. NMR 6, 277–293 (1995).
  Article CAS Google Scholar
• Johnson, B.A. & Blevins, R.A. NMR View: a computer program for the visualization and analysis of NMR data. J. Biomol. NMR 4, 603–614 (1994).
  Article CAS Google Scholar
• Otwinowski, Z. & Minor, W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307–326 (1997).
  Article CAS Google Scholar
• Navaza, J. Amore: an automated package for molecular replacement. Acta Crystallogr. A 50, 157–163 (1994).
  Article Google Scholar
• McCoy, A.J., Grosse-Kunstleve, R.W., Storoni, L.C. & Read, R.J. Likelihood-enhanced fast translation functions. Acta Crystallogr. D Biol. Crystallogr. 61, 458–464 (2005).
  Article Google Scholar
• Perrakis, A., Harkiolaki, M., Wilson, K.S. & Lamzin, V.S. ARP/wARP and molecular replacement. Acta Crystallogr. D Biol. Crystallogr. 57, 1445–1450 (2001).
  Article CAS Google Scholar
• Jones, T.A., Zou, J.Y., Cowan, S.W. & Kjeldgaard, M. Improved methods for building protein models in electron-density maps and the location of errors in these models. Acta Crystallogr. A 47, 110–119 (1991).
  Article Google Scholar
• Murshudov, G.N., Vagin, A.A. & Dodson, E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240–255 (1997).
  Article CAS Google Scholar
• Collaborative Computational Project No. 4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50, 760–763 (1994).
• Pyott, S.J. & Rosenmund, C. The effects of temperature on vesicular supply and release in autaptic cultures of rat and mouse hippocampal neurons. J. Physiol. (Lond.) 539, 523–535 (2002).
  Article CAS Google Scholar
• Maximov, A., Pang, Z., Tervo, D.G.R. & Südhof, T.C. Monitoring synaptic transmission in primary neuronal cultures using local extracellular stimulation. J. Neurosci. Methods 161, 75–87 (2007).
  Article Google Scholar