Synaptotagmin 1 Is Necessary for the Ca2+ Dependence of Clathrin-Mediated Endocytosis

The role of Ca2+ in synaptic vesicle endocytosis remains uncertain due to the diversity in various preparations where several forms of endocytosis may contribute variably in different conditions. Although recent studies have demonstrated that Ca2+ is important for clathrin-mediated endocytosis (CME), the mechanistic role of Ca2+ in CME remains to be elucidated. By monitoring CME of single vesicles in mouse chromaffin cells with cell-attached capacitance measurements that offer millisecond time resolution, we demonstrate that the dynamics of vesicle fission during CME is Ca2+ dependent but becomes Ca2+ independent in synaptotagmin 1 (Syt1) knock-out cells. Our results thus suggest that Syt1 is necessary for the Ca2+ dependence of CME.

[1]  M. Inoue,et al.  Differential distribution of synaptotagmin-1, -4, -7, and -9 in rat adrenal chromaffin cells , 2011, Cell and Tissue Research.

[2]  M. Lindau,et al.  Hormonal inhibition of endocytosis: novel roles for noradrenaline and G protein Gz , 2010, The Journal of physiology.

[3]  A. B. Harkins,et al.  Upregulation of synaptotagmin IV inhibits transmitter release in PC12 cells with targeted synaptotagmin I knockdown , 2010, BMC Neuroscience.

[4]  Zhiping P Pang,et al.  Cell biology of Ca2+-triggered exocytosis. , 2010, Current opinion in cell biology.

[5]  Changbong Hyeon,et al.  Dynamic Ca2+-Dependent Stimulation of Vesicle Fusion by Membrane-Anchored Synaptotagmin 1 , 2010, Science.

[6]  M. Jackson,et al.  Synaptotagmin IV modulation of vesicle size and fusion pores in PC12 cells. , 2010, Biophysical journal.

[7]  Jianhua Xu,et al.  Ca2+ and calmodulin initiate all forms of endocytosis during depolarization at a nerve terminal , 2009, Nature Neuroscience.

[8]  T. Sakaba,et al.  Calcium Dependence of Exo- and Endocytotic Coupling at a Glutamatergic Synapse , 2009, Neuron.

[9]  Takeshi Sakaba,et al.  Multiple Roles of Calcium Ions in the Regulation of Neurotransmitter Release , 2008, Neuron.

[10]  Edwin R Chapman,et al.  How does synaptotagmin trigger neurotransmitter release? , 2008, Annual review of biochemistry.

[11]  L. Lagnado,et al.  Modes of Vesicle Retrieval at Ribbon Synapses, Calyx-Type Synapses, and Small Central Synapses , 2007, The Journal of Neuroscience.

[12]  M. Lindau,et al.  Exocytotic catecholamine release is not associated with cation flux through channels in the vesicle membrane but Na+ influx through the fusion pore , 2007, Nature Cell Biology.

[13]  Zhen Yan,et al.  Molecular determinants for the interaction between AMPA receptors and the clathrin adaptor complex AP-2 , 2007, Proceedings of the National Academy of Sciences.

[14]  L. Hinrichsen,et al.  Bending a membrane: how clathrin affects budding. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[15]  S. Tooze,et al.  Synaptotagmin IV is necessary for the maturation of secretory granules in PC12 cells , 2006, The Journal of cell biology.

[16]  Kira E. Poskanzer,et al.  Discrete Residues in the C2B Domain of Synaptotagmin I Independently Specify Endocytic Rate and Synaptic Vesicle Size , 2006, Neuron.

[17]  L. Eliasson,et al.  Calcium increases endocytotic vesicle size and accelerates membrane fission in insulin-secreting INS-1 cells , 2005, Journal of Cell Science.

[18]  Jianhua Xu,et al.  Activity-Dependent Acceleration of Endocytosis at a Central Synapse , 2005, The Journal of Neuroscience.

[19]  Manfred Lindau,et al.  Patch amperometry: high-resolution measurements of single-vesicle fusion and release , 2005, Nature Methods.

[20]  P. De Camilli,et al.  Phosphatidylinositol phosphate kinase type I gamma regulates dynamics of large dense-core vesicle fusion. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[21]  Volker Haucke,et al.  Recognition of a Basic AP-2 Binding Motif within the C2B Domain of Synaptotagmin Is Dependent on Multimerization* , 2004, Journal of Biological Chemistry.

[22]  T. A. Ryan,et al.  Kinetic efficiency of endocytosis at mammalian CNS synapses requires synaptotagmin I. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[23]  T. Südhof,et al.  Structural basis for the evolutionary inactivation of Ca2+ binding to synaptotagmin 4 , 2004, Nature Structural &Molecular Biology.

[24]  Kurt W. Marek,et al.  Synaptotagmin I is necessary for compensatory synaptic vesicle endocytosis in vivo , 2003, Nature.

[25]  C. Stevens.  Neurotransmitter Release at Central Synapses , 2003, Neuron.

[26]  M. Lindau,et al.  Secretory Vesicles Membrane Area Is Regulated in Tandem with Quantal Size in Chromaffin Cells , 2003, The Journal of Neuroscience.

[27]  M. Jackson,et al.  Different domains of synaptotagmin control the choice between kiss-and-run and full fusion , 2003, Nature.

[28]  Manfred Lindau,et al.  Exocytosis of single chromaffin granules in cell-free inside-out membrane patches , 2003, Nature Cell Biology.

[29]  T. Südhof,et al.  Three-Dimensional Structure of the Synaptotagmin 1 C2B-Domain Synaptotagmin 1 as a Phospholipid Binding Machine , 2001, Neuron.

[30]  L. Lagnado,et al.  Calcium influx selects the fast mode of endocytosis in the synaptic terminal of retinal bipolar cells , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[31]  M. Jackson,et al.  Synaptotagmin Modulation of Fusion Pore Kinetics in Regulated Exocytosis of Dense-Core Vesicles , 2001, Science.

[32]  Thomas Voets,et al.  Calcium Dependence of Exocytosis and Endocytosis at the Cochlear Inner Hair Cell Afferent Synapse , 2001, Neuron.

[33]  T. A. Ryan,et al.  Calcium accelerates endocytosis of vSNAREs at hippocampal synapses , 2001, Nature Neuroscience.

[34]  R. Nossal.  Energetics of Clathrin Basket Assembly , 2001, Traffic.

[35]  M. Lindau,et al.  Resolution of patch capacitance recordings and of fusion pore conductances in small vesicles. , 2000, Biophysical journal.

[36]  P. De Camilli,et al.  AP-2 recruitment to synaptotagmin stimulated by tyrosine-based endocytic motifs. , 1999, Science.

[37]  E. Chapman,et al.  Delineation of the Oligomerization, AP-2 Binding, and Synprint Binding Region of the C2B Domain of Synaptotagmin* , 1998, The Journal of Biological Chemistry.

[38]  L. Brodin,et al.  Dissociation between Ca2+-Triggered Synaptic Vesicle Exocytosis and Clathrin-Mediated Endocytosis at a Central Synapse , 1998, Neuron.

[39]  P. Robinson,et al.  Ba2+ does not support synaptic vesicle retrieval in rat cerebrocortical synaptosomes , 1998, Neuroscience Letters.

[40]  H. McMahon,et al.  Calcium triggers calcineurin-dependent synaptic vesicle recycling in mammalian nerve terminals , 1998, Current Biology.

[41]  E. Neher,et al.  Multiple Forms of Endocytosis In Bovine Adrenal Chromaffin Cells , 1997, The Journal of cell biology.

[42]  G. Alvarez de Toledo,et al.  The exocytotic event in chromaffin cells revealed by patch amperometry , 1997, Nature.

[43]  S. Seino,et al.  Cellular localization of synaptotagmin I, II, and III mRNAs in the central nervous system and pituitary and adrenal glands of the rat , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[44]  Thomas C. Südhof,et al.  Ca2+-dependent and -independent activities of neural and non-neural synaptotagmins , 1995, Nature.

[45]  Richard G. W. Anderson,et al.  Functional properties of multiple synaptotagmins in brain , 1994, Neuron.

[46]  Richard G. W. Anderson,et al.  Synaptotagmin I is a high affinity receptor for clathrin AP-2: Implications for membrane recycling , 1994, Cell.

[47]  Gary Matthews,et al.  Inhibition of endocytosis by elevated internal calcium in a synaptic terminal , 1994, Nature.

[48]  R. Kelly,et al.  Intermediates in synaptic vesicle recycling revealed by optical imaging of Drosophila neuromuscular junctions , 1994, Neuron.

[49]  M. Lindau,et al.  Exo-endocytosis and closing of the fission pore during endocytosis in single pituitary nerve terminals internally perfused with high calcium concentrations. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[50]  Robert H. Chow,et al.  Delay in vesicle fusion revealed by electrochemical monitoring of single secretory events in adrenal chromaffin cells , 1992, Nature.

[51]  E Neher,et al.  Discrete changes of cell membrane capacitance observed under conditions of enhanced secretion in bovine adrenal chromaffin cells. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[52]  W. Regehr,et al.  Short-term synaptic plasticity. , 2002, Annual review of physiology.

[53]  W. Almers,et al.  Currents through the fusion pore that forms during exocytosis of a secretory vesicle , 1987, Nature.