SNAREs in neurons – beyond synaptic vesicle exocytosis (Review)

References

• Rothman JE, Warren G. Implications of the SNARE hypothesis for intracellular membrane topology and dynamics. Curr Biol 1994; 4: 220–233
   PubMedGoogle Scholar
• Ferro-Novick S, Jahn R. Vesicle fusion from yeast to man. Nature 1994; 370: 191–193
   PubMedGoogle Scholar
• Hong W. SNAREs and traffic. Biochim Biophys Acta 2005; 1744: 493–517
   PubMed Web of Science ®Google Scholar
• Ungermann C, Langosch D. Functions of SNAREs in intracellular membrane fusion and lipid bilayer mixing. J Cell Sci 2005; 118: 3819–3828
   PubMed Web of Science ®Google Scholar
• Sollner T, Whiteheart SW, Brunner M, Erdjument-Bromage H, Geromanos S, Tempst P, Rothman JE. SNAP receptors implicated in vesicle targeting and fusion. Nature 1993; 362: 318–324
   PubMed Web of Science ®Google Scholar
• Sollner T, Bennett MK, Whiteheart SW, Scheller RH, Rothman JE. A protein assembly-disassembly pathway in vitro that may correspond to sequential steps of synaptic vesicle docking, activation, and fusion. Cell 1993; 75: 409–418
   PubMed Web of Science ®Google Scholar
• Poirier MA, Xiao W, Macosko JC, Chan C, Shin YK, Bennett MK. The synaptic SNARE complex is a parallel four-stranded helical bundle. Nat Struct Biol 1998; 5: 765–769
   PubMedGoogle Scholar
• Sutton RB, Fasshauer D, Jahn R, Brunger AT. Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 A resolution. Nature 1998; 395: 347–353
   PubMed Web of Science ®Google Scholar
• Katz L, Hanson PI, Heuser JE, Brennwald P. Genetic and morphological analyses reveal a critical interaction between the C-termini of two SNARE proteins and a parallel four helical arrangement for the exocytic SNARE complex. EMBO J 1998; 17: 6200–6209
   Google Scholar
• Weimbs T, Low SH, Chapin SJ, Mostov KE, Bucher P, Hofmann K. A conserved domain is present in different families of vesicular fusion proteins: a new superfamily. Proc Natl Acad Sci USA 1997; 94: 3046–3051
   PubMed Web of Science ®Google Scholar
• Breidenbach MA, Brunger AT. New insights into clostridial neurotoxin-SNARE interactions. Trends Mol Med 2005; 11: 377–381
   PubMed Web of Science ®Google Scholar
• Proux-Gillardeaux V, Rudge R, Galli T. The tetanus neurotoxin-sensitive and insensitive routes to and from the plasma membrane: fast and slow pathways?. Traffic 2005; 6: 366–373
   PubMedGoogle Scholar
• Giraudo CG, Hu C, You D, Slovic AM, Mosharov EV, Sulzer D, Melia TJ, Rothman JE. SNAREs can promote complete fusion and hemifusion as alternative outcomes. J Cell Biol 2005; 170: 249–260
   PubMed Web of Science ®Google Scholar
• Fernandez-Peruchena C, Navas S, Montes MA, Alvarez de Toledo G. Fusion pore regulation of transmitter release. Brain Res Brain Res Rev 2005; 49: 406–415
   Google Scholar
• Sudhof TC. The synaptic vesicle cycle. Annu Rev Neurosci 2004; 27: 509–547
   PubMed Web of Science ®Google Scholar
• An S, Zenisek D. Regulation of exocytosis in neurons and neuroendocrine cells. Curr Opin Neurobiol 2004; 14: 522–530
   PubMed Web of Science ®Google Scholar
• Matthews G. Cycling the synapse: scenic versus direct routes for vesicles. Neuron 2004; 44: 223–226
   Google Scholar
• Yang C, Mora S, Ryder JW, Coker KJ, Hansen P, Allen LA, Pessin JE. VAMP3 null mice display normal constitutive, insulin- and exercise-regulated vesicle trafficking. Mol Cell Biol 2001; 21: 1573–1580
   PubMedGoogle Scholar
• Atlashkin V, Kreykenbohm V, Eskelinen EL, Wenzel D, Fayyazi A, Fischer von Mollard G. Deletion of the SNARE vti1b in mice results in the loss of a single SNARE partner, syntaxin 8. Mol Cell Biol 2003; 23: 5198–5207
   PubMed Web of Science ®Google Scholar
• Yang C, Coker KJ, Kim JK, Mora S, Thurmond DC, Davis AC, Yang B, Williamson RA, Shulman GI, Pessin JE. Syntaxin 4 heterozygous knockout mice develop muscle insulin resistance. J Clin Invest 2001; 107: 1311–1318
   PubMedGoogle Scholar
• Wang CC, Ng CP, Lu L, Atlashkin V, Zhang W, Seet LF, Hong W. A role of VAMP8/endobrevin in regulated exocytosis of pancreatic acinar cells. Dev Cell 2004; 7: 359–371
   PubMed Web of Science ®Google Scholar
• Schoch S, Deak F, Konigstorfer A, Mozhayeva M, Sara Y, Sudhof TC, Kavalali ET. SNARE function analyzed in synaptobrevin/VAMP knockout mice. Science 2001; 294: 1117–1122
   Google Scholar
• Hohenstein AC, Roche PA. SNAP-29 is a promiscuous syntaxin-binding SNARE. Biochem Biophys Res Commun 2001; 285: 167–171
   PubMed Web of Science ®Google Scholar
• Su Q, Mochida S, Tian JH, Mehta R, Sheng ZH. SNAP-29: a general SNARE protein that inhibits SNARE disassembly and is implicated in synaptic transmission. Proc Natl Acad Sci USA 2001; 98: 14038–14043
   PubMed Web of Science ®Google Scholar
• Pan PY, Cai Q, Lin L, Lu PH, Duan S, Sheng ZH. SNAP-29-mediated modulation of synaptic transmission in cultured hippocampal neurons. J Biol Chem 2005; 280: 25769–25779
   PubMed Web of Science ®Google Scholar
• Antonin W, Riedel D, von Mollard GF. The SNARE Vti1a-beta is localized to small synaptic vesicles and participates in a novel SNARE complex. J Neurosci 2000; 20: 5724–5732
   PubMedGoogle Scholar
• Fischer von Mollard G, Stevens TH. A human homolog can functionally replace the yeast vesicle-associated SNARE Vti1p in two vesicle transport pathways. J Biol Chem 1998; 273: 2624–2630
   PubMed Web of Science ®Google Scholar
• Xu Y, Wong SH, Tang BL, Subramaniam VN, Zhang T, Hong W. A 29-kilodalton Golgi soluble N-ethylmaleimide-sensitive factor attachment protein receptor (Vti1-rp2) implicated in protein trafficking in the secretory pathway. J Biol Chem 1998; 273: 21783–21789
   PubMedGoogle Scholar
• Advani RJ, Bae HR, Bock JB, Chao DS, Doung YC, Prekeris R, Yoo JS, Scheller RH. Seven novel mammalian SNARE proteins localize to distinct membrane compartments. J Biol Chem 1998; 273: 10317–10324
   PubMed Web of Science ®Google Scholar
• Tang BL, Tan AE, Lim LK, Lee SS, Low DY, Hong W. Syntaxin 12, a member of the syntaxin family localized to the endosome. J Biol Chem 1998; 273: 6944–6950
   PubMed Web of Science ®Google Scholar
• Prekeris R, Klumperman J, Chen YA, Scheller RH. Syntaxin 13 mediates cycling of plasma membrane proteins via tubulovesicular recycling endosomes. J Cell Biol 1998; 143: 957–971
   PubMed Web of Science ®Google Scholar
• McBride HM, Rybin V, Murphy C, Giner A, Teasdale R, Zerial M. Oligomeric complexes link Rab5 effectors with NSF and drive membrane fusion via interactions between EEA1 and syntaxin 13. Cell 1999; 98: 377–386
   PubMed Web of Science ®Google Scholar
• Prekeris R, Foletti DL, Scheller RH. Dynamics of tubulovesicular recycling endosomes in hippocampal neurons. J Neurosci 1999; 19: 10324–10337
   Google Scholar
• Hirling H, Steiner P, Chaperon C, Marsault R, Regazzi R, Catsicas S. Syntaxin 13 is a developmentally regulated SNARE involved in neurite outgrowth and endosomal trafficking. Eur J Neurosci 2000; 12: 1913–1923
   PubMedGoogle Scholar
• Sarria JC, Catsicas S, Hornung JP, Hirling H. Developmental and spatial expression pattern of syntaxin 13 in the mouse central nervous system. Cell Tissue Res 2002; 309: 209–218
   Google Scholar
• Steiner P, Sarria JC, Glauser L, Magnin S, Catsicas S, Hirling H. Modulation of receptor cycling by neuron-enriched endosomal protein of 21 kD. J Cell Biol 2002; 157: 1197–1209
   PubMed Web of Science ®Google Scholar
• Alberi S, Boda B, Steiner P, Nikonenko I, Hirling H, Muller D. The endosomal protein NEEP21 regulates AMPA receptor-mediated synaptic transmission and plasticity in the hippocampus. Mol Cell Neurosci 2005; 29: 313–319
   Google Scholar
• Steiner P, Alberi S, Kulangara K, Yersin A, Sarria JC, Regulier E, Kasas S, Dietler G, Muller D, Catsicas S, Hirling H. Interactions between NEEP21, GRIP1 and GluR2 regulate sorting and recycling of the glutamate receptor subunit GluR2. EMBO J 2005; 24: 2873–2884
   Google Scholar
• Wyszynski M, Kim E, Dunah AW, Passafaro M, Valtschanoff JG, Serra-Pages C, Streuli M, Weinberg RJ, Sheng M. Interaction between GRIP and liprin-alpha/SYD2 is required for AMPA receptor targeting. Neuron 2002; 34: 39–52
   Google Scholar
• Setou M, Seog DH, Tanaka Y, Kanai Y, Takei Y, Kawagishi M, Hirokawa N. Glutamate-receptor-interacting protein GRIP1 directly steers kinesin to dendrites. Nature 2002; 417: 83–87
   PubMed Web of Science ®Google Scholar
• Galli T, Zahraoui A, Vaidyanathan VV, Raposo G, Tian JM, Karin M, Niemann H, Louvard D. A novel tetanus neurotoxin-insensitive vesicle-associated membrane protein in SNARE complexes of the apical plasma membrane of epithelial cells. Mol Biol Cell 1998; 9: 1437–1448
   PubMed Web of Science ®Google Scholar
• Rossi V, Banfield DK, Vacca M, Dietrich LE, Ungermann C, D'Esposito M, Galli T, Filippini F. Longins and their longin domains: regulated SNAREs and multifunctional SNARE regulators. Trends Biochem Sci 2004; 29: 682–688
   PubMed Web of Science ®Google Scholar
• Coco S, Raposo G, Martinez S, Fontaine JJ, Takamori S, Zahraoui A, Jahn R, Matteoli M, Louvard D, Galli T. Subcellular localization of tetanus neurotoxin-insensitive vesicle-associated membrane protein (VAMP)/VAMP7 in neuronal cells: evidence for a novel membrane compartment. J Neurosci 1999; 19: 9803–9812
   Google Scholar
• Muzerelle A, Alberts P, Martinez-Arca S, Jeannequin O, Lafaye P, Mazie JC, Galli T, Gaspar P. Tetanus neurotoxin-insensitive vesicle-associated membrane protein localizes to a presynaptic membrane compartment in selected terminal subsets of the rat brain. Neuroscience 2003; 122: 59–75
   PubMed Web of Science ®Google Scholar
• Martinez-Arca S, Alberts P, Zahraoui A, Louvard D, Galli T. Role of tetanus neurotoxin insensitive vesicle-associated membrane protein (TI-VAMP) in vesicular transport mediating neurite outgrowth. J Cell Biol 2000; 149: 889–900
   PubMed Web of Science ®Google Scholar
• Martinez-Arca S, Coco S, Mainguy G, Schenk U, Alberts P, Bouille P, Mezzina M, Prochiantz A, Matteoli M, Louvard D, Galli T. A common exocytotic mechanism mediates axonal and dendritic outgrowth. J Neurosci 2001; 21: 3830–3838
   PubMed Web of Science ®Google Scholar
• Alberts P, Rudge R, Hinners I, Muzerelle A, Martinez-Arca S, Irinopoulou T, Marthiens V, Tooze S, Rathjen F, Gaspar P, Galli T. Cross talk between tetanus neurotoxin-insensitive vesicle-associated membrane protein-mediated transport and L1-mediated adhesion. Mol Biol Cell 2003; 14: 4207–4220
   Google Scholar
• Kiryushko D, Berezin V, Bock E. Regulators of neurite outgrowth: role of cell adhesion molecules. Ann N Y Acad Sci 2004; 1014: 140–154
   PubMed Web of Science ®Google Scholar
• Alberts P, Rudge R, Irinopoulou T, Danglot L, Gauthier-Rouviere C, Galli T. Cdc42 and actin control polarized expression of TI-VAMP vesicles to neuronal growth cones and their fusion with the plasma membrane. Mol Biol Cell 2006; 17: 1194–1203
   Google Scholar
• Etienne-Manneville S. Cdc42 – the centre of polarity. J Cell Sci 2004; 117: 1291–1300
   PubMed Web of Science ®Google Scholar
• Zhou Q, Xiao J, Liu Y. Participation of syntaxin 1A in membrane trafficking involving neurite elongation and membrane expansion. J Neurosci Res 2000; 61: 321–328
   PubMed Web of Science ®Google Scholar
• Shirasu M, Kimura K, Kataoka M, Takahashi M, Okajima S, Kawaguchi S, Hirasawa Y, Ide C, Mizoguchi A. VAMP-2 promotes neurite elongation and SNAP-25A increases neurite sprouting in PC12 cells. Neurosci Res 2000; 37(4)265–275
   Google Scholar
• Kimura K, Mizoguchi A, Ide C. Regulation of growth cone extension by SNARE proteins. J Histochem Cytochem 2003; 51: 429–433
   PubMed Web of Science ®Google Scholar
• Su Q, Cai Q, Gerwin C, Smith CL, Sheng ZH. Syntabulin is a microtubule-associated protein implicated in syntaxin transport in neurons. Nat Cell Biol 2004; 6: 941–953
   PubMed Web of Science ®Google Scholar
• McNew JA, Sogaard M, Lampen NM, Machida S, Ye RR, Lacomis L, Tempst P, Rothman JE, Sollner TH. Ykt6p, a prenylated SNARE essential for endoplasmic reticulum-Golgi transport. J Biol Chem 1997; 272: 17776–17783
   PubMed Web of Science ®Google Scholar
• Zhang T, Hong W. Ykt6 forms a SNARE complex with syntaxin 5, GS28, and Bet1 and participates in a late stage in endoplasmic reticulum-Golgi transport. J Biol Chem 2001; 276: 27480–27487
   PubMedGoogle Scholar
• Xu Y, Martin S, James DE, Hong W. GS15 forms a SNARE complex with syntaxin 5, GS28, and Ykt6 and is implicated in traffic in the early cisternae of the Golgi apparatus. Mol Biol Cell 2002; 13: 3493–3507
   PubMed Web of Science ®Google Scholar
• Kweon Y, Rothe A, Conibear E, Stevens TH. Ykt6p is a multifunctional yeast R-SNARE that is required for multiple membrane transport pathways to the vacuole. Mol Biol Cell 2003; 14: 1868–1881
   PubMed Web of Science ®Google Scholar
• Chen Y, Shin YK, Bassham DC. YKT6 is a core constituent of membrane fusion machineries at the Arabidopsis trans-Golgi network. J Mol Biol 2005; 350: 92–101
   PubMed Web of Science ®Google Scholar
• Fukasawa M, Varlamov O, Eng WS, Sollner TH, Rothman JE. Localization and activity of the SNARE Ykt6 determined by its regulatory domain and palmitoylation. Proc Natl Acad Sci USA 2004; 101: 4815–4820
   PubMed Web of Science ®Google Scholar
• Dietrich LE, Gurezka R, Veit M, Ungermann C. The SNARE Ykt6 mediates protein palmitoylation during an early stage of homotypic vacuole fusion. EMBO J 2004; 23: 45–53
   PubMed Web of Science ®Google Scholar
• Veit M. The human SNARE protein Ykt6 mediates its own palmitoylation at C-terminal cysteine residues. Biochem J 2004; 384: 233–237
   PubMedGoogle Scholar
• Hasegawa H, Zinsser S, Rhee Y, Vik-Mo EO, Davanger S, Hay JC. Mammalian ykt6 is a neuronal SNARE targeted to a specialized compartment by its profilin-like amino terminal domain. Mol Biol Cell 2003; 14: 698–720
   PubMed Web of Science ®Google Scholar
• Hasegawa H, Yang Z, Oltedal L, Davanger S, Hay JC. Intramolecular protein-protein and protein-lipid interactions control the conformation and subcellular targeting of neuronal Ykt6. J Cell Sci 2004; 117: 4495–4508
   PubMed Web of Science ®Google Scholar
• Saito T, Guan F, Papolos DF, Rajouria N, Fann CS, Lachman HM. Polymorphism in SNAP29 gene promoter region associated with schizophrenia. Mol Psychiatry 2001; 6: 193–201
   Google Scholar
• Wonodi I, Hong LE, Avila MT, Buchanan RW, Carpenter WT, Jr, Stine OC, Mitchell BD, Thaker GK. Association between polymorphism of the SNAP29 gene promoter region and schizophrenia. Schizophr Res 2005; 78: 339–341
   Google Scholar
• Sprecher E, Ishida-Yamamoto A, Mizrahi-Koren M, Rapaport D, Goldsher D, Indelman M, Topaz O, Chefetz I, Keren H, O'brien TJ, Bercovich D, Shalev S, Geiger D, Bergman R, Horowitz M, Mandel H. A mutation in SNAP29, coding for a SNARE protein involved in intracellular trafficking, causes a novel neurocutaneous syndrome characterized by cerebral dysgenesis, neuropathy, ichthyosis, and palmoplantar keratoderma. Am J Hum Genet 2005; 77: 242–251
   PubMed Web of Science ®Google Scholar
• D'Esposito M, Ciccodicola A, Gianfrancesco F, Esposito T, Flagiello L, Mazzarella R, Schlessinger D, D'Urso M. A synaptobrevin-like gene in the Xq28 pseudoautosomal region undergoes X inactivation. Nat Genet 1996; 13: 227–229
   Google Scholar
• Saito T, Parsia S, Papolos DF, Lachman HM. Analysis of the pseudoautosomal X-linked gene SYBL1in bipolar affective disorder: description of a new candidate allele for psychiatric disorders. Am J Med Genet 2000; 96: 317–323
   Google Scholar
• Muller DJ, Schulze TG, Jahnes E, Cichon S, Krauss H, Kesper K, Held T, Maier W, Propping P, Nothen MM, Rietschel M. Association between a polymorphism in the pseudoautosomal X-linked gene SYBL1 and bipolar affective disorder. Am J Med Genet 2002; 114: 74–78
   Google Scholar
• Wenning GK, Jellinger KA. The role of α-synuclein and tau in neurodegenerative movement disorders. Curr Opin Neurol 2005; 18: 357–362
   Google Scholar
• Chandra S, Gallardo G, Fernandez-Chacon R, Schluter OM, Sudhof TC. α-synuclein cooperates with CSPalpha in preventing neurodegeneration. Cell 2005; 123: 383–396
   PubMed Web of Science ®Google Scholar
• Suga K, Tomiyama T, Mori H, Akagawa K. Syntaxin 5 interacts with presenilin holoproteins, but not with their N- or C-terminal fragments, and affects beta-amyloid peptide production. Biochem J 2004; 381: 619–628
   Google Scholar
• Suga K, Saito A, Tomiyama T, Mori H, Akagawa K. Syntaxin 5 interacts specifically with presenilin holoproteins and affects processing of APP in neuronal cells. J Neurochem 2005; 94: 425–439
   Google Scholar
• Horton AC, Ehlers MD. Secretory trafficking in neuronal dendrites. Nat Cell Biol 2004; 6: 585–591
   Google Scholar
• Racz B, Blanpied TA, Ehlers MD, Weinberg RJ. Lateral organization of endocytic machinery in dendritic spines. Nat Neurosci 2004; 7: 917–918
   PubMed Web of Science ®Google Scholar
• Horton AC, Racz B, Monson EE, Lin AL, Weinberg RJ, Ehlers MD. Polarized secretory trafficking directs cargo for asymmetric dendrite growth and morphogenesis. Neuron 2005; 48: 757–771
   PubMed Web of Science ®Google Scholar
• Dulubova I, Yamaguchi T, Gao Y, Min SW, Huryeva I, Sudhof TC, Rizo J. How Tlg2p/syntaxin 16 ‘snares’ Vps45. EMBO J 2002; 21: 3620–3631
   PubMed Web of Science ®Google Scholar
• Mallard F, Tang BL, Galli T, Tenza D, Saint-Pol A, Yue X, Antony C, Hong W, Goud B, Johannes L. Early/recycling endosomes-to-TGN transport involves two SNARE complexes and a Rab6 isoform. J Cell Biol 2002; 156: 653–664
   PubMed Web of Science ®Google Scholar
• Washbourne P, Thompson PM, Carta M, Costa ET, Mathews JR, Lopez-Bendito G, Molnar Z, Becher MW, Valenzuela CF, Partridge LD, Wilson MC. Genetic ablation of the t-SNARE SNAP-25 distinguishes mechanisms of neuroexocytosis. Nat Neurosci 2002; 5: 19–26
   PubMed Web of Science ®Google Scholar