rbSec1A and B colocalize with syntaxin 1 and SNAP-25 throughout the axon, but are not in a stable complex with syntaxin

doi:10.1083/jcb.129.1.105

This Article

	Full Text (PDF, 4801K)
	Alert me when this article is cited
	Citation Map

Services

	Email this article
	Similar articles in this journal
	Similar articles in PubMed
	Alert me to new content in the JCB
	Download to citation manager

Citing Articles

	Citing Articles via HighWire
	Citing Articles via CrossRef
	Citing Articles via Google Scholar

Google Scholar

	Articles by Garcia, E. P.
	Articles by De Camilli, P.
	Search for Related Content

PubMed

	PubMed Citation
	Articles by Garcia, E. P.
	Articles by De Camilli, P.


Social Bookmarking

	What's this?

ARTICLES

rbSec1A and B colocalize with syntaxin 1 and SNAP-25 throughout the axon, but are not in a stable complex with syntaxin

EP Garcia, PS McPherson, TJ Chilcote, K Takei and P De Camilli
Department of Cell Biology, Boyer Center for Molecular Medicine, Yale University School of Medicine, New Haven, Connecticut 06510.

rbSec1 is a mammalian neuronal protein homologous to the yeast SEC1 gene product which is required for exocytosis. Mutations in Sec1 homologues in the nervous systems of C. elegans and D. melanogaster lead to defective neurotransmitter secretion. Biochemical studies have shown that recombinant rbSec1 binds syntaxin 1 but not SNAP-25 or synaptobrevin/VAMP, the two proteins which together with syntaxin 1 form the synaptic SNARE complex. In this study we have examined the subcellular localization of rbSec1 and the degree of interaction between rbSec1 and syntaxin 1 in situ. rbSec1, which we show here to be represented by two alternatively spliced isoforms, rbSec1A and B, has a widespread distribution in the axon and is not restricted to the nerve terminal. This distribution parallels the localization of syntaxin 1 and SNAP-25 along the entire axonal plasmalemma. rbSec1 is found in a soluble and a membrane-associated form. Although a pool of rbSec1 is present on the plasmalemma, the majority of membrane-bound rbSec1 is not associated with syntaxin 1. We also show that rbSec1 is not part of the synaptic SNARE complex or of the syntaxin 1/SNAP-25 complex we show to be present in non-synaptic regions of the axon. Thus, in spite of biochemical studies demonstrating the high affinity interaction of rbSec1 and syntaxin 1, our results indicate that rbSec1 and syntaxin 1 are not stably associated. They also suggest that the function of rbSec1, syntaxin 1, and SNAP-25 is not restricted to synaptic vesicle exocytosis at the synapse.
Add to CiteULike CiteULike Add to Complore Complore Add to Connotea Connotea Add to Del.icio.us Del.icio.us Add to Digg Digg Facebook Add to Reddit Reddit Add to Technorati Technorati Twitter What's this?

This article has been cited by other articles:

Wang, Z., Thurmond, D. C. (2009). Mechanisms of biphasic insulin-granule exocytosis - roles of the cytoskeleton, small GTPases and SNARE proteins. J. Cell Sci. 122: 893-903 [Abstract] [Full Text]
Fogel, A. I., Akins, M. R., Krupp, A. J., Stagi, M., Stein, V., Biederer, T. (2007). SynCAMs Organize Synapses through Heterophilic Adhesion. J. Neurosci. 27: 12516-12530 [Abstract] [Full Text]
Tafoya, L. C. R., Mameli, M., Miyashita, T., Guzowski, J. F., Valenzuela, C. F., Wilson, M. C. (2006). Expression and function of SNAP-25 as a universal SNARE component in GABAergic neurons.. J. Neurosci. 26: 7826-7838 [Abstract] [Full Text]
Ohara-Imaizumi, M., Ohtsuka, T., Matsushima, S., Akimoto, Y., Nishiwaki, C., Nakamichi, Y., Kikuta, T., Nagai, S., Kawakami, H., Watanabe, T., Nagamatsu, S. (2005). ELKS, a Protein Structurally Related to the Active Zone-associated Protein CAST, Is Expressed in Pancreatic {beta} Cells and Functions in Insulin Exocytosis: Interaction of ELKS with Exocytotic Machinery Analyzed by Total Internal Reflection Fluorescence Microscopy. Mol. Biol. Cell 16: 3289-3300 [Abstract] [Full Text]
Fu, J., Naren, A. P., Gao, X., Ahmmed, G. U., Malik, A. B. (2005). Protease-activated Receptor-1 Activation of Endothelial Cells Induces Protein Kinase C{alpha}-dependent Phosphorylation of Syntaxin 4 and Munc18c: ROLE IN SIGNALING P-SELECTIN EXPRESSION. J. Biol. Chem. 280: 3178-3184 [Abstract] [Full Text]
Zhai, R. G., Bellen, H. J. (2004). The Architecture of the Active Zone in the Presynaptic Nerve Terminal. Physiology 19: 262-270 [Abstract] [Full Text]
Sakisaka, T., Baba, T., Tanaka, S., Izumi, G., Yasumi, M., Takai, Y. (2004). Regulation of SNAREs by tomosyn and ROCK: implication in extension and retraction of neurites. JCB 166: 17-25 [Abstract] [Full Text]
Mitchell, S. J., Ryan, T. A. (2004). Syntaxin-1A Is Excluded from Recycling Synaptic Vesicles at Nerve Terminals. J. Neurosci. 24: 4884-4888 [Abstract] [Full Text]
Li, Q., Lau, A., Morris, T. J., Guo, L., Fordyce, C. B., Stanley, E. F. (2004). A Syntaxin 1, G{alpha}o, and N-Type Calcium Channel Complex at a Presynaptic Nerve Terminal: Analysis by Quantitative Immunocolocalization. J. Neurosci. 24: 4070-4081 [Abstract] [Full Text]
Taverna, E., Saba, E., Rowe, J., Francolini, M., Clementi, F., Rosa, P. (2004). Role of Lipid Microdomains in P/Q-type Calcium Channel (Cav2.1) Clustering and Function in Presynaptic Membranes. J. Biol. Chem. 279: 5127-5134 [Abstract] [Full Text]
Rickman, C., Meunier, F. A., Binz, T., Davletov, B. (2004). High Affinity Interaction of Syntaxin and SNAP-25 on the Plasma Membrane Is Abolished by Botulinum Toxin E. J. Biol. Chem. 279: 644-651 [Abstract] [Full Text]
Martinez-Arca, S., Proux-Gillardeaux, V., Alberts, P., Louvard, D., Galli, T. (2003). Ectopic expression of syntaxin 1 in the ER redirects TI-VAMP- and cellubrevin-containing vesicles. J. Cell Sci. 116: 2805-2816 [Abstract] [Full Text]
Rickman, C., Davletov, B. (2003). Mechanism of Calcium-independent Synaptotagmin Binding to Target SNAREs. J. Biol. Chem. 278: 5501-5504 [Abstract] [Full Text]
HU, K., DAVLETOV, B. (2003). SNAREs and control of synaptic release probabilities. FASEB J. 17: 130-135 [Abstract] [Full Text]
Bhattacharya, S., Stewart, B. A., Niemeyer, B. A., Burgess, R. W., McCabe, B. D., Lin, P., Boulianne, G., O'Kane, C. J., Schwarz, T. L. (2002). From the Cover: Members of the synaptobrevin/vesicle-associated membrane protein (VAMP) family in Drosophila are functionally interchangeable in vivo for neurotransmitter release and cell viability. Proc. Natl. Acad. Sci. USA 99: 13867-13872 [Abstract] [Full Text]
Honer, W. G., Falkai, P., Bayer, T. A., Xie, J., Hu, L., Li, H.-Y., Arango, V., Mann, J. J., Dwork, A. J., Trimble, W. S. (2002). Abnormalities of SNARE Mechanism Proteins in Anterior Frontal Cortex in Severe Mental Illness. Cereb Cortex 12: 349-356 [Abstract] [Full Text]
Rowe, J., Calegari, F., Taverna, E., Longhi, R., Rosa, P. (2002). Syntaxin 1A is delivered to the apical and basolateral domains of epithelial cells: the role of munc-18 proteins. J. Cell Sci. 114: 3323-3332 [Abstract] [Full Text]
Yeaman, C., Grindstaff, K. K., Wright, J. R., Nelson, W. J. (2001). Sec6/8 complexes on trans-Golgi network and plasma membrane regulate late stages of exocytosis in mammalian cells. JCB 155: 593-604 [Abstract] [Full Text]
Martinez-Arca, S., Coco, S., Mainguy, G., Schenk, U., Alberts, P., Bouille, P., Mezzina, M., Prochiantz, A., Matteoli, M., Louvard, D., Galli, T. (2001). A Common Exocytotic Mechanism Mediates Axonal and Dendritic Outgrowth. J. Neurosci. 21: 3830-3838 [Abstract] [Full Text]
Kolk, S. M., Berghs, C. A. F. M., Vaudry, H., Verhage, M., Roubos, E. W. (2001). Physiological Control of Xunc18 Expression in Neuroendocrine Melanotrope Cells of Xenopus laevis. Endocrinology 142: 1950-1957 [Abstract] [Full Text]
Fisher, R. J., Pevsner, J., Burgoyne, R. D. (2001). Control of Fusion Pore Dynamics During Exocytosis by Munc18. Science 291: 875-878 [Abstract] [Full Text]
Foletti, D. L., Lin, R., Finley, M. A. F., Scheller, R. H. (2000). Phosphorylated Syntaxin 1 Is Localized to Discrete Domains Along a Subset of Axons. J. Neurosci. 20: 4535-4544 [Abstract] [Full Text]
Martinez-Arca, S., Alberts, P., Zahraoui, A., Louvard, D., Galli, T. (2000). Role of Tetanus Neurotoxin Insensitive Vesicle-Associated Membrane Protein (Ti-Vamp) in Vesicular Transport Mediating Neurite Outgrowth. JCB 149: 889-900 [Abstract] [Full Text]
Price, A., Seals, D., Wickner, W., Ungermann, C. (2000). The Docking Stage of Yeast Vacuole Fusion Requires the Transfer of Proteins from a Cis-Snare Complex to a Rab/Ypt Protein. JCB 148: 1231-1238 [Abstract] [Full Text]
Rubino, M., Miaczynska, M., Lippe, R., Zerial, M. (2000). Selective Membrane Recruitment of EEA1 Suggests a Role in Directional Transport of Clathrin-coated Vesicles to Early Endosomes. J. Biol. Chem. 275: 3745-3748 [Abstract] [Full Text]
Chin, L.-S., Nugent, R. D., Raynor, M. C., Vavalle, J. P., Li, L. (2000). SNIP, a Novel SNAP-25-interacting Protein Implicated in Regulated Exocytosis. J. Biol. Chem. 275: 1191-1200 [Abstract] [Full Text]
Wang, X., Kibschull, M., Laue, M. M., Lichte, B., Petrasch-Parwez, E., Kilimann, M. W. (1999). Aczonin, a 550-Kd Putative Scaffolding Protein of Presynaptic Active Zones, Shares Homology Regions with Rim and Bassoon and Binds Profilin. JCB 147: 151-162 [Abstract] [Full Text]
Bergmann, M., Grabs, D., Rager, G. (1999). Developmental Expression of Dynamin in the Chick Retinotectal System. J. Histochem. Cytochem. 47: 1297-1306 [Abstract] [Full Text]
Macleod, G. T., Gan, J.-B., Bennett, M. R. (1999). Vesicle-Associated Proteins and Quantal Release at Single Active Zones of Amphibian (Bufo marinus) Motor-Nerve Terminals. J. Neurophysiol. 82: 1133-1146 [Abstract] [Full Text]
Vida, T., Gerhardt, B. (1999). A Cell-Free Assay Allows Reconstitution of Vps33p-Dependent Transport to the Yeast Vacuole/Lysosome. JCB 146: 85-98 [Abstract] [Full Text]
Sassa, T., Harada, S.-i., Ogawa, H., Rand, J. B., Maruyama, I. N., Hosono, R. (1999). Regulation of the UNC-18-Caenorhabditis elegans Syntaxin Complex by UNC-13. J. Neurosci. 19: 4772-4777 [Abstract] [Full Text]
Lustgarten, V., Gerst, J. E. (1999). Yeast VSM1 Encodes a v-SNARE Binding Protein That May Act as a Negative Regulator of Constitutive Exocytosis. Mol. Cell. Biol. 19: 4480-4494 [Abstract] [Full Text]
Aloyz, R., Fawcett, J. P., Kaplan, D. R., Murphy, R. A., Miller, F. D. (1999). Activity-Dependent Activation of TrkB Neurotrophin Receptors in the Adult CNS. Learn. Mem. 6: 216-231 [Abstract] [Full Text]
Fletcher, A. I., Shuang, R., Giovannucci, D. R., Zhang, L., Bittner, M. A., Stuenkel, E. L. (1999). Regulation of Exocytosis by Cyclin-dependent Kinase 5�via Phosphorylation of Munc18. J. Biol. Chem. 274: 4027-4035 [Abstract] [Full Text]
Zakharenko, S., Chang, S., O'Donoghue, M., Popov, S. V. (1999). Neurotransmitter Secretion along Growing Nerve Processes: Comparison with Synaptic Vesicle Exocytosis. JCB 144: 507-518 [Abstract] [Full Text]
Taubenblatt, P, Dedieu, J., Gulik-Krzywicki, T, Morel, N (1999). VAMP (synaptobrevin) is present in the plasma membrane of nerve terminals. J. Cell Sci. 112: 3559-3567 [Abstract]
Lalli, G, Herreros, J, Osborne, S., Montecucco, C, Rossetto, O, Schiavo, G (1999). Functional characterisation of tetanus and botulinum neurotoxins binding domains. J. Cell Sci. 112: 2715-2724 [Abstract]
Rowe, J, Corradi, N, Malosio, M., Taverna, E, Halban, P, Meldolesi, J, Rosa, P (1999). Blockade of membrane transport and disassembly of the Golgi complex by expression of syntaxin 1A in neurosecretion-incompetent cells: prevention by rbSEC1. J. Cell Sci. 112: 1865-1877 [Abstract]
YEAMAN, C., GRINDSTAFF, K. K., NELSON, W. J. (1999). New Perspectives on Mechanisms Involved in Generating Epithelial Cell Polarity. Physiol. Rev. 79: 73-98 [Abstract] [Full Text]
Zakharenko, S., Popov, S. (1998). Dynamics of Axonal Microtubules Regulate the Topology of New Membrane Insertion into the Growing Neurites. JCB 143: 1077-1086 [Abstract] [Full Text]
Dieck, S., Sanmarti-Vila, L., Langnaese, K., Richter, K., Kindler, S., Soyke, A., Wex, H., Smalla, K.-H., Kampf, U., Franzer, J.-T., Stumm, M., Garner, C. C., Gundelfinger, E. D. (1998). Bassoon, a Novel Zinc-finger CAG/Glutamine-repeat Protein Selectively Localized at the Active Zone of Presynaptic Nerve Terminals. JCB 142: 499-509 [Abstract] [Full Text]
Shuang, R., Zhang, L., Fletcher, A., Groblewski, G. E., Pevsner, J., Stuenkel, E. L. (1998). Regulation of Munc-18/Syntaxin 1A Interaction by Cyclin-dependent Kinase 5�in Nerve Endings. J. Biol. Chem. 273: 4957-4966 [Abstract] [Full Text]
Nakata, T., Terada, S., Hirokawa, N. (1998). Visualization of the Dynamics of Synaptic Vesicle and Plasma Membrane Proteins in Living Axons. JCB 140: 659-674 [Abstract] [Full Text]
Low, S. H., Roche, P. A., Anderson, H. A., van Ijzendoorn, S. C.�D., Zhang, M., Mostov, K. E., Weimbs, T. (1998). Targeting of SNAP-23 and SNAP-25 in Polarized Epithelial Cells. J. Biol. Chem. 273: 3422-3430 [Abstract] [Full Text]
Riento, K, Galli, T, Jansson, S, Ehnholm, C, Lehtonen, E, Olkkonen, V. (1998). Interaction of Munc-18-2 with syntaxin 3 controls the association of apical SNAREs in epithelial cells. J. Cell Sci. 111: 2681-2688 [Abstract]
Nonet, M. L., Saifee, O., Zhao, H., Rand, J. B., Wei, L. (1998). Synaptic Transmission Deficits in Caenorhabditis elegans Synaptobrevin Mutants. J. Neurosci. 18: 70-80 [Abstract] [Full Text]
Rieder, S. E., Emr, S. D. (1997). A Novel RING Finger Protein Complex Essential for a Late Step in Protein Transport to the Yeast Vacuole. Mol. Biol. Cell 8: 2307-2327 [Abstract] [Full Text]
Burgess, R. W., Deitcher, D. L., Schwarz, T. L. (1997). The Synaptic Protein Syntaxin1 Is Required for Cellularization of Drosophila Embryos. JCB 138: 861-875 [Abstract] [Full Text]
Darsow, T., Rieder, S. E., Emr, S. D. (1997). A Multispecificity Syntaxin Homologue, Vam3p, Essential for Autophagic and Biosynthetic Protein Transport to the Vacuole. JCB 138: 517-529 [Abstract] [Full Text]
Lupashin, V. V., Waters, M. G. (1997). t-SNARE Activation Through Transient Interaction with a Rab-Like Guanosine Triphosphatase. Science 276: 1255-1258 [Abstract] [Full Text]
Fawcett, J. P., Aloyz, R., McLean, J. H., Pareek, S., Miller, F. D., McPherson, P. S., Murphy, R. A. (1997). Detection of Brain-derived Neurotrophic Factor in a Vesicular Fraction of Brain Synaptosomes. J. Biol. Chem. 272: 8837-8840 [Abstract] [Full Text]
Gengyo-Ando, K., Kitayama, H., Mukaida, M., Ikawa, Y. (1996). A Murine Neural-Specific Homolog Corrects Cholinergic Defects in Caenorhabditis elegans unc-18 Mutants. J. Neurosci. 16: 6695-6702 [Abstract] [Full Text]
Estes, P. S., Roos, J., van der Bliek, A., Kelly, R. B., Krishnan, K. S., Ramaswami, M. (1996). Traffic of Dynamin within Individual Drosophila Synaptic Boutons Relative to Compartment-Specific Markers. J. Neurosci. 16: 5443-5456 [Abstract] [Full Text]
Fujita, Y., Sasaki, T., Fukui, K., Kotani, H., Kimura, T., Hata, Y., S�dhof, T. C., Scheller, R. H., Takai, Y. (1996). Phosphorylation of Munc-18/n-Sec1/rbSec1 by Protein Kinase C. J. Biol. Chem. 271: 7265-7268 [Abstract] [Full Text]
Chapman, E. R., An, S., Edwardson, J. M., Jahn, R. (1996). A Novel Function for the Second C2 Domain of Synaptotagmin. J. Biol. Chem. 271: 5844-5849 [Abstract] [Full Text]
Galli, T., McPherson, P. S., De Camilli, P. (1996). The V(0) Sector of the V-ATPase, Synaptobrevin, and Synaptophysin Are Associated on Synaptic Vesicles in a Triton X-100-resistant, Freeze-thawing Sensitive, Complex. J. Biol. Chem. 271: 2193-2198 [Abstract] [Full Text]
Hanson, P. I., Otto, H., Barton, N., Jahn, R. (1995). The N-Ethylmaleimide-sensitive Fusion Protein and [IMAGE]-SNAP Induce a Conformational Change in Syntaxin. J. Biol. Chem. 270: 16955-16961 [Abstract] [Full Text]
Jahn, R., Hanson, P.I., Otto, H., Ahnert-Hilger, G. (1995). Botulinum and Tetanus Neurotoxins: Emerging Tools for the Study of Membrane Fusion. Cold Spring Harb Symp Quant Biol 60: 329-335 [Abstract]
Zhang, W., Efanov, A., Yang, S.-N., Fried, G., Kolare, S., Brown, H., Zaitsev, S., Berggren, P.-O., Meister, B. (2000). Munc-18 Associates with Syntaxin and Serves as a Negative Regulator of Exocytosis in the Pancreatic beta -Cell. J. Biol. Chem. 275: 41521-41527 [Abstract] [Full Text]
Lewis, J. L., Dong, M., Earles, C. A., Chapman, E. R. (2001). The Transmembrane Domain of Syntaxin 1A Is Critical for Cytoplasmic Domain Protein-Protein Interactions. J. Biol. Chem. 276: 15458-15465 [Abstract] [Full Text]
Chamberlain, L. H., Burgoyne, R. D., Gould, G. W. (2001). SNARE proteins are highly enriched in lipid rafts in PC12 cells: Implications for the spatial control of exocytosis. Proc. Natl. Acad. Sci. USA 98: 5619-5624 [Abstract] [Full Text]