The Caenorhabditis elegans unc-64 locus encodes a syntaxin that interacts genetically with synaptobrevin.

We describe the molecular cloning and characterization of the unc-64 locus of Caenorhabditis elegans. unc-64 expresses three transcripts, each encoding a molecule with 63-64% identity to human syntaxin 1A, a membrane- anchored protein involved in synaptic vesicle fusion. Interestingly, the alternative forms of syntaxin differ only in their C-terminal hydrophobic membrane anchors. The forms are differentially expressed in neuronal and secretory tissues; genetic evidence suggests that these forms are not functionally equivalent. A complete loss-of-function mutation in unc-64 results in a worm that completes embryogenesis, but arrests development shortly thereafter as a paralyzed L1 larva, presumably as a consequence of neuronal dysfunction. The severity of the neuronal phenotypes of C. elegans syntaxin mutants appears comparable to those of Drosophila syntaxin mutants. However, nematode syntaxin appears not to be required for embryonic development, for secretion of cuticle from the hypodermis, or for the function of muscle, in contrast to Drosophila syntaxin, which appears to be required in all cells. Less severe viable unc-64 mutants exhibit a variety of behavioral defects and show strong resistance to the acetylcholinesterase inhibitor aldicarb. Extracellular physiological recordings from pharyngeal muscle of hypomorphic mutants show alterations in the kinetics of transmitter release. The lesions in the hypomorphic alleles map to the hydrophobic face of the H3 coiled-coil domain of syntaxin, a domain that in vitro mediates physical interactions with similar coiled-coil domains in SNAP-25 and synaptobrevin. Furthermore, the unc-64 syntaxin mutants exhibit allele-specific genetic interactions with mutants carrying lesions in the coiled-coil domain of synaptobrevin, providing in vivo evidence for the significance of these domains in regulating synaptic vesicle fusion.

[1]  Hongjuan Zhao,et al.  Synaptic Transmission Deficits in Caenorhabditis elegansSynaptobrevin Mutants , 1998, The Journal of Neuroscience.

[2]  R. Scheller,et al.  Structural Organization of the Synaptic Exocytosis Core Complex , 1997, Neuron.

[3]  H. Horvitz,et al.  Caenorhabditis elegans rab-3 Mutant Synapses Exhibit Impaired Function and Are Partially Depleted of Vesicles , 1997, The Journal of Neuroscience.

[4]  A T Brünger,et al.  Structural Changes Are Associated with Soluble N-Ethylmaleimide-sensitive Fusion Protein Attachment Protein Receptor Complex Formation* , 1997, The Journal of Biological Chemistry.

[5]  M. Davis,et al.  avr‐15 encodes a chloride channel subunit that mediates inhibitory glutamatergic neurotransmission and ivermectin sensitivity in Caenorhabditis elegans , 1997, The EMBO journal.

[6]  W. Catterall,et al.  Phosphorylation of the Synaptic Protein Interaction Site on N-type Calcium Channels Inhibits Interactions with SNARE Proteins , 1997, The Journal of Neuroscience.

[7]  E. Neher,et al.  Alteration of Ca2+ Dependence of Neurotransmitter Release by Disruption of Ca2+ Channel/Syntaxin Interaction , 1997, The Journal of Neuroscience.

[8]  R. Burgess,et al.  The Synaptic Protein Syntaxin1 Is Required for Cellularization of Drosophila Embryos , 1997, The Journal of cell biology.

[9]  C. Mello,et al.  Wnt Signaling and an APC-Related Gene Specify Endoderm in Early C. elegans Embryos , 1997, Cell.

[10]  Reinhard Jahn,et al.  Structure and Conformational Changes in NSF and Its Membrane Receptor Complexes Visualized by Quick-Freeze/Deep-Etch Electron Microscopy , 1997, Cell.

[11]  S. Scherer,et al.  Hemizygous deletion of the syntaxin 1A gene in individuals with Williams syndrome. , 1997, American journal of human genetics.

[12]  E A Barnard,et al.  Caenorhabditis elegans Levamisole Resistance Geneslev-1, unc-29, and unc-38 Encode Functional Nicotinic Acetylcholine Receptor Subunits , 1997, The Journal of Neuroscience.

[13]  R. Jahn,et al.  The Secretory Granule Protein Syncollin Binds to Syntaxin in a Ca2+-Sensitive Manner , 1997, Cell.

[14]  R. Scheller,et al.  A fusion of new ideas , 1997, Nature.

[15]  J. Staunton,et al.  aex-3 Encodes a Novel Regulator of Presynaptic Activity in C. elegans , 1997, Neuron.

[16]  N. Brose,et al.  Direct Interaction of the Rat unc-13 Homologue Munc13-1 with the N Terminus of Syntaxin* , 1997, The Journal of Biological Chemistry.

[17]  T. Schedl Developmental Genetics of the Germ Line , 1997 .

[18]  R. Scheller,et al.  Protein transport. A fusion of new ideas. , 1997, Nature.

[19]  H. Bellen,et al.  Drosophila syntaxin is required for cell viability and may function in membrane formation and stabilization. , 1996, Genetics.

[20]  J A Crowell,et al.  A genetic selection for Caenorhabditis elegans synaptic transmission mutants. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[21]  G. von Heijne,et al.  A 12-Residue-long Polyleucine Tail Is Sufficient to Anchor Synaptobrevin to the Endoplasmic Reticulum Membrane (*) , 1996, The Journal of Biological Chemistry.

[22]  W. Catterall,et al.  Calcium-dependent interaction of N-type calcium channels with the synaptic core complex , 1996, Nature.

[23]  I. Greenwald,et al.  Interchangeability of Caenorhabditis elegans DSL proteins and intrinsic signalling activity of their extracellular domains in vivo. , 1995, Development.

[24]  L. Avery,et al.  Interacting genes required for pharyngeal excitation by motor neuron MC in Caenorhabditis elegans. , 1995, Genetics.

[25]  T. Galli,et al.  v- and t-SNAREs in neuronal exocytosis: A need for additional components to define sites of release , 1995, Neuropharmacology.

[26]  Andreas Prokop,et al.  Syntaxin and synaptobrevin function downstream of vesicle docking in drosophila , 1995, Neuron.

[27]  K. Sakimura,et al.  Identification of four different forms of syntaxin 3. , 1995, Biochemical and biophysical research communications.

[28]  Thomas C. Südhof,et al.  The synaptic vesicle cycle: a cascade of protein–protein interactions , 1995, Nature.

[29]  C. Johnson,et al.  Caenorhabditis elegans mutants resistant to inhibitors of acetylcholinesterase. , 1995, Genetics.

[30]  K. Kemphues,et al.  par-1, a gene required for establishing polarity in C. elegans embryos, encodes a putative Ser/Thr kinase that is asymmetrically distributed , 1995, Cell.

[31]  R. Scheller,et al.  Botulinum Neurotoxin Type C Cleaves a Single Lys-Ala Bond within the Carboxyl-terminal Region of Syntaxins (*) , 1995, The Journal of Biological Chemistry.

[32]  W. Schafer,et al.  A calcium-channel homologue required for adaptation to dopamine and serotonin in Caenorhabditis elegans , 1995, Nature.

[33]  R. Scheller,et al.  Distinct domains of syntaxin are required for synaptic vesicle fusion complex formation and dissociation , 1995, Neuron.

[34]  R. Jahn,et al.  The t-SNAREs syntaxin 1 and SNAP-25 are present on organelles that participate in synaptic vesicle recycling , 1995, The Journal of cell biology.

[35]  K. Broadie,et al.  Genetic and electrophysiological studies of drosophila syntaxin-1A demonstrate its role in nonneuronal secretion and neurotransmission , 1995, Cell.

[36]  Henry F. Epstein,et al.  Caenorhabditis elegans : modern biological analysis of an organism , 1995 .

[37]  J. Rothman,et al.  Neurotransmission: harnessing fusion machinery at the synapse , 1994, Trends in Neurosciences.

[38]  W. Catterall,et al.  Identification of a syntaxin-binding site on N-Type calcium channels , 1994, Neuron.

[39]  J. Littleton,et al.  Calcium dependence of neurotransmitter release and rate of spontaneous vesicle fusions are altered in Drosophila synaptotagmin mutants. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[40]  T. Südhof,et al.  Synaptic vesicle membrane fusion complex: action of clostridial neurotoxins on assembly. , 1994, The EMBO journal.

[41]  T. Schwarz,et al.  The effect on synaptic physiology of synaptotagmin mutations in drosophila , 1994, Neuron.

[42]  Jh Thomas,et al.  Regulation of a periodic motor program in C. elegans , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[43]  P. Sternberg,et al.  The lin-15 locus encodes two negative regulators of Caenorhabditis elegans vulval development. , 1994, Molecular biology of the cell.

[44]  A. Alfonso,et al.  Cloning and characterization of the choline acetyltransferase structural gene (cha-1) from C. elegans , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[45]  P. De Camilli,et al.  A rat brain Sec1 homologue related to Rop and UNC18 interacts with syntaxin. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[46]  L. Avery,et al.  Electrical activity and behavior in the pharynx of caenorhabditis elegans , 1994, Neuron.

[47]  R. Scheller,et al.  Protein-protein interactions contributing to the specificity of intracellular vesicular trafficking. , 1994, Science.

[48]  R. Scheller,et al.  n-Sec1: a neural-specific syntaxin-binding protein. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[49]  D. Baillie,et al.  Genetic Analysis in Caenorhabditis Elegans , 1994 .

[50]  R. Scheller,et al.  A molecular description of synaptic vesicle membrane trafficking. , 1994, Annual review of biochemistry.

[51]  R. Jahn,et al.  Botulinum neurotoxin C1 blocks neurotransmitter release by means of cleaving HPC‐1/syntaxin. , 1993, The EMBO journal.

[52]  T. Südhof,et al.  Synaptic vesicle fusion complex contains unc-18 homologue bound to syntaxin , 1993, Nature.

[53]  Mark K. Bennett,et al.  A protein assembly-disassembly pathway in vitro that may correspond to sequential steps of synaptic vesicle docking, activation, and fusion , 1993, Cell.

[54]  R. Burgess,et al.  Identification and characterization of Drosophila genes for synaptic vesicle proteins , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[55]  R. Tjian,et al.  Cloning and properties of the Caenorhabditis elegans TATA-box-binding protein. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[56]  K. Gengyo-Ando,et al.  The C. elegans unc-18 gene encodes a protein expressed in motor neurons , 1993, Neuron.

[57]  R. Scheller,et al.  The syntaxin family of vesicular transport receptors , 1993, Cell.

[58]  A. Alfonso,et al.  The Caenorhabditis elegans unc-17 gene: a putative vesicular acetylcholine transporter. , 1993, Science.

[59]  M. Nonet,et al.  Synaptic function is impaired but not eliminated in C. elegans mutants lacking synaptotagmin , 1993, Cell.

[60]  L. Avery,et al.  Motor neuron M3 controls pharyngeal muscle relaxation timing in Caenorhabditis elegans. , 1993, The Journal of experimental biology.

[61]  H. Pelham,et al.  SED5 encodes a 39-kD integral membrane protein required for vesicular transport between the ER and the Golgi complex , 1992, The Journal of cell biology.

[62]  R. Scheller,et al.  Syntaxin: a synaptic protein implicated in docking of synaptic vesicles at presynaptic active zones. , 1992, Science.

[63]  M. Wigler,et al.  SNC1, a yeast homolog of the synaptic vesicle-associated membrane protein/synaptobrevin gene family: genetic interactions with the RAS and CAP genes. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[64]  C. Li,et al.  Localization of FMRF amide‐like peptides in Caenorhabditis elegans , 1992, The Journal of comparative neurology.

[65]  V. Ambros,et al.  Efficient gene transfer in C.elegans: extrachromosomal maintenance and integration of transforming sequences. , 1991, The EMBO journal.

[66]  S. Brenner,et al.  A phorbol ester/diacylglycerol-binding protein encoded by the unc-13 gene of Caenorhabditis elegans. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[67]  M. Nonet,et al.  Early aspects of Caenorhabditis elegans sex determination and dosage compensation are regulated by a zinc-finger protein , 1991, Nature.

[68]  Cori Bargmann,et al.  Control of larval development by chemosensory neurons in Caenorhabditis elegans. , 1991, Science.

[69]  N. MaruyamaI,et al.  Caenorhabditis elegansのunc‐13遺伝子がコードするホルボールエステル/ジアシルグリセロール結合蛋白質 , 1991 .

[70]  T. Südhof,et al.  Structures and chromosomal localizations of two human genes encoding synaptobrevins 1 and 2. , 1990, The Journal of biological chemistry.

[71]  A. Fire,et al.  A modular set of lacZ fusion vectors for studying gene expression in Caenorhabditis elegans. , 1990, Gene.

[72]  R. Waterston,et al.  The basal component of the nematode dense-body is vinculin. , 1989, The Journal of biological chemistry.

[73]  N. Munakata [Genetics of Caenorhabditis elegans]. , 1989, Tanpakushitsu kakusan koso. Protein, nucleic acid, enzyme.

[74]  A. Coulson,et al.  Genome linking with yeast artificial chromosomes , 1988, Nature.

[75]  D. Riddle,et al.  Functional study of the Caenorhabditis elegans secretory-excretory system using laser microsurgery. , 1984, The Journal of experimental zoology.

[76]  P. Fisher,et al.  Identification, developmental regulation, and response to heat shock of two antigenically related forms of a major nuclear envelope protein in Drosophila embryos: application of an improved method for affinity purification of antibodies using polypeptides immobilized on nitrocellulose blots , 1984, The Journal of cell biology.

[77]  J. Devereux,et al.  A comprehensive set of sequence analysis programs for the VAX , 1984, Nucleic Acids Res..

[78]  J. Sambrook,et al.  Molecular Cloning: A Laboratory Manual , 2001 .

[79]  J. Kimble,et al.  Tissue-specific synthesis of yolk proteins in Caenorhabditis elegans. , 1983, Developmental biology.

[80]  D. Riddle,et al.  Fine structure of the Caenorhabditis elegans secretory-excretory system. , 1983, Journal of ultrastructure research.

[81]  J. Lewis,et al.  The genetics of levamisole resistance in the nematode Caenorhabditis elegans. , 1980, Genetics.

[82]  J. Lewis,et al.  Levamisole-resitant mutants of the nematode Caenorhabditis elegans appear to lack pharmacological acetylcholine receptors , 1980, Neuroscience.

[83]  H. Lipkin Where is the ?c? , 1978 .

[84]  Rspm μgm Methods , 1972 .

[85]  R. H. Adrian Electrophysiological Methods , 1970, Nature.

[86]  H. Mclennan,et al.  Synaptic Transmission , 2003 .