Encyclopedia of Signaling Molecules

2018 Edition
| Editors: Sangdun Choi


  • Thierry GALLIEmail author
  • Véronique Proux-GillardeauxEmail author
Reference work entry
DOI: https://doi.org/10.1007/978-3-319-67199-4_627


Intracellular membrane trafficking in eukaryotes is a multiple step process consisting in the budding of vesicles from a donor compartment, their translocation into the cytoplasm along cytoskeletal elements, their tethering, and subsequent fusion with the membrane of the target compartment. Membrane fusion is based on SNARE proteins, classified into two categories, vesicular (v)-SNAREs and target (t)-SNAREs present on the acceptor membrane. It is the specific pairing of v-SNAREs with their cognate t-SNAREs in trans which is responsible for bringing the lipid bilayers close together, and the zippering of SNAREs provides the required energy for membrane fusion (Fig. 1). This review focuses on the discovery of SNAREs and then on four of the nine v-SNAREs: the clostridial neurotoxin sensitive VAMPs 1, 2, and 3 and on Tetanus neurotoxin-Insensitive Vesicle-Associated Membrane Protein, TI-VAMP/VAMP7. VAMP7, unlike the first ones, possess a long amino-terminal domain called the...
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We apologize to all the authors that are not cited in the text due to strong reference limitation. Our work is supported in part by the Institut National de la Santé et de la Recherche Médicale (INSERM), and the Centre National de la Recherche Scientifique (CNRS) and grants from the Fondation pour la Recherche Médicale (FRM), the Association pour la Recherche sur le Cancer (ARC), and the Who am I? Labex (Idex ANR-11-IDEX-0005-01).


  1. Balch WE, Dunphy WG, Braell WA, Rothman JE. Reconstitution of the transport of protein between successive compartments of the Golgi measured by the coupled incorporation of N-acetylglucosamine. Cell. 1984;39:405–16.PubMedPubMedCentralCrossRefGoogle Scholar
  2. Barber M, Arai Y, Morishita Y, Vigier L, Causeret F, Borello U, Ledonne F, Coppola E, Contremoulins V, Pfrieger FW, Tissir F, Govindan S, Jabaudon D, Proux-Gillardeaux V, Galli T, Pierani A. Migration Speed of Cajal-Retzius Cells Modulated by Vesicular Trafficking Controls the Size of Higher-Order Cortical Areas. Curr Biol. 2015;25:2466–78.PubMedPubMedCentralCrossRefGoogle Scholar
  3. Ben Fredj N, Hammond S, Otsuna H, Chien CB, Burrone J, Meyer MP. Synaptic activity and activity-dependent competition regulates axon arbor maturation, growth arrest, and territory in the retinotectal projection. J Neurosci. 2010;30:10939–51.PubMedPubMedCentralCrossRefGoogle Scholar
  4. Block MR, Rothman JE. Purification of N-ethylmaleimide-sensitive fusion protein. Methods Enzymol. 1992;219:300–9.PubMedPubMedCentralCrossRefGoogle Scholar
  5. Borisovska M, Zhao Y, Tsytsyura Y, Glyvuk N, Takamori S, Matti U, Rettig J, Sudhof T, Bruns D. v-SNAREs control exocytosis of vesicles from priming to fusion. EMBO J. 2005;24:2114–26.PubMedPubMedCentralCrossRefGoogle Scholar
  6. Braun V, Fraisier V, Raposo G, Hurbain I, Sibarita J, Chavrier P, Galli T, Niedergang F. TI-VAMP/VAMP7 is required for optimal phagocytosis of opsonised particles in macrophages. EMBO J. 2004;23:4166–76.PubMedPubMedCentralCrossRefGoogle Scholar
  7. Burgo A, Casano A, Kuster A, Arold ST, Wang G, Nola S, Verraes A, Dingli F, Loew D, Galli T. Increased activity of the v-SNARE TI-VAMP/VAMP7 by tyrosine phosphorylation in the Longin domain. J Biol Chem. 2013.  https://doi.org/10.1074/jbc.M112.415075.CrossRefPubMedPubMedCentralGoogle Scholar
  8. Burgo A, Proux-Gillardeaux V, Sotirakis E, Bun P, Casano A, Verraes A, Liem RK, Formstecher E, Coppey-Moisan M, Galli T. A molecular network for the transport of the TI-VAMP/VAMP7 vesicles from cell center to periphery. Dev Cell. 2012;23:166–80.PubMedPubMedCentralCrossRefGoogle Scholar
  9. Chaineau M, Danglot L, Galli T. Multiple roles of the vesicular-SNARE TI-VAMP in post-Golgi and endosomal trafficking. FEBS Lett. 2009;583:3817–26.PubMedPubMedCentralCrossRefGoogle Scholar
  10. Chaineau M, Danglot L, Proux-Gillardeaux V, Galli T. Role of HRB in clathrin-dependent endocytosis. J Biol Chem. 2008;283:34365–73.PubMedPubMedCentralCrossRefGoogle Scholar
  11. Chiaruttini G, Piperno GM, Jouve M, De Nardi F, Larghi P, Peden AA, Baj G, Muller S, Valitutti S, Galli T, Benvenuti F. The SNARE VAMP7 Regulates Exocytic Trafficking of Interleukin-12 in Dendritic Cells. Cell Rep. 2016;14:2624–36.PubMedPubMedCentralCrossRefGoogle Scholar
  12. Cotrufo T, Perez-Branguli F, Muhaisen A, Ros O, Andres R, Baeriswyl T, Fuschini G, Tarrago T, Pascual M, Urena J, Blasi J, Giralt E, Stoeckli ET, Soriano E. A Signaling Mechanism Coupling Netrin-1/Deleted in Colorectal Cancer Chemoattraction to SNARE-Mediated Exocytosis in Axonal Growth Cones. J Neurosci. 2011;31:14463–80.CrossRefPubMedGoogle Scholar
  13. Danglot L, Chaineau M, Dahan M, Gendron M, Boggetto N, Perez F, Galli T. Role of TI-VAMP and CD82 in EGFR cell-surface dynamics and signaling. J Cell Sci. 2010;123:723–35.CrossRefPubMedGoogle Scholar
  14. Danglot L, Zylbersztejn K, Petkovic M, Gauberti M, Meziane H, Combe R, Champy MF, Birling MC, Pavlovic G, Bizot JC, Trovero F, Della Ragione F, Proux-Gillardeaux V, Sorg T, Vivien D, D’Esposito M, Galli T. Absence of TI-VAMP/Vamp7 leads to increased anxiety in mice. J Neurosci. 2012;32:1962–8.CrossRefPubMedGoogle Scholar
  15. Das V, Nal B, Dujeancourt A, Thoulouze M, Galli T, Roux P, Dautry-Varsat A, Alcover A. Activation-induced polarized recycling targets T cell antigen receptors to the immunological synapse: involvement of SNARE complexes. Immunity. 2004;20:577–88.CrossRefPubMedGoogle Scholar
  16. Daste F, Galli T, Tareste D. Structure and function of longin SNAREs. J Cell Sci. 2015;128:4263–72.CrossRefPubMedGoogle Scholar
  17. Deak F, Shin OH, Kavalali ET, Sudhof TC. Structural determinants of synaptobrevin 2 function in synaptic vesicle fusion. J Neurosci. 2006;26:6668–76.CrossRefPubMedGoogle Scholar
  18. Fader CM, Sanchez DG, Mestre MB, Colombo MI. TI-VAMP/VAMP7 and VAMP3/cellubrevin: two v-SNARE proteins involved in specific steps of the autophagy/multivesicular body pathways. Biochim Biophys Acta. 2009;1793:1901–16.CrossRefPubMedGoogle Scholar
  19. Feldmann A, Amphornrat J, Schonherr M, Winterstein C, Mobius W, Ruhwedel T, Danglot L, Nave K, Galli T, Bruns D, Trotter J, Kramer-Albers E. Transport of the Major Myelin Proteolipid Protein Is Directed by VAMP3 and VAMP7. J Neurosci. 2011;31:5659–72.CrossRefPubMedGoogle Scholar
  20. Fields I, Shteyn E, Pypaert M, Proux-Gillardeaux V, Kang R, Galli T, Folsch H. v-SNARE cellubrevin is required for basolateral sorting of AP-1 B-dependent cargo in polarized epithelial cells. J Cell Biol. 2007;177:477–88.PubMedPubMedCentralCrossRefGoogle Scholar
  21. Finetti F, Patrussi L, Galgano D, Cassioli C, Perinetti G, Pazour GJ, Baldari CT. The small GTPase Rab8 interacts with VAMP-3 to regulate the delivery of recycling T-cell receptors to the immune synapse. J Cell Sci. 2015;128:2541–52.PubMedPubMedCentralCrossRefGoogle Scholar
  22. Flaumenhaft R. Molecular basis of platelet granule secretion. Arterioscler Thromb Vasc Biol. 2003;23:1152–60.CrossRefPubMedGoogle Scholar
  23. Galli T, Chilcote T, Mundigl O, Binz T, Niemann H, De Camilli P. Tetanus toxin-mediated cleavage of cellubrevin impairs exocytosis of transferrin receptor-containing vesicles in CHO cells. J Cell Biol. 1994;125:1015–24.CrossRefPubMedGoogle Scholar
  24. Gao J, Hirata M, Mizokami A, Zhao J, Takahashi I, Takeuchi H. Differential role of SNAP-25 phosphorylation by protein kinases A and C in the regulation of SNARE complex formation and exocytosis in PC12 cells. Cell Signal. 2016;28:425–37.CrossRefPubMedGoogle Scholar
  25. Gerst JE. SNARE regulators: matchmakers and matchbreakers. BBA-Mol Cell Res. 2003;18:2–3.Google Scholar
  26. Grassi D, Plonka FB, Oksdath M, Guil AN, Sosa LJ, Quiroga S. Selected SNARE proteins are essential for the polarized membrane insertion of igf-1 receptor and the regulation of initial axonal outgrowth in neurons. Cell Discov. 2015;1:15023.PubMedPubMedCentralCrossRefGoogle Scholar
  27. Gupton SL, Gertler FB. Integrin signaling switches the cytoskeletal and exocytic machinery that drives neuritogenesis. Dev Cell. 2010;18:725–36.PubMedPubMedCentralCrossRefGoogle Scholar
  28. Hackam DJ, Rotstein OD, Sjolin C, Schreiber AD, Trimble WS, Grinstein S. v-SNARE-dependent secretion is required for phagocytosis. Proc Natl Acad Sci USA. 1998;95:11691–6.PubMedPubMedCentralCrossRefGoogle Scholar
  29. Hager HA, Roberts RJ, Cross EE, Proux-Gillardeaux V, Bader DM. Identification of a novel Bves function: regulation of vesicular transport. Embo J. 2010;29:532–45.PubMedPubMedCentralCrossRefGoogle Scholar
  30. Hasan N, Corbin D, Hu C. Fusogenic pairings of vesicle-associated membrane proteins (VAMPs) and plasma membrane t-SNAREs – VAMP5 as the exception. PLoS One. 2010;5:e14238.PubMedPubMedCentralCrossRefGoogle Scholar
  31. Hou JC, Min L, Pessin JE. Insulin granule biogenesis, trafficking and exocytosis. Vitam Horm. 2009;80:473–506.PubMedPubMedCentralCrossRefGoogle Scholar
  32. Hua Z, Leal-Ortiz S, Foss SM, Waites CL, Garner CC, Voglmaier SM, Edwards RH. v-SNARE Composition Distinguishes Synaptic Vesicle Pools. Neuron. 2011;71:474–87.PubMedPubMedCentralCrossRefGoogle Scholar
  33. Jahn R, Scheller RH. SNAREs - engines for membrane fusion. Nat Rev Mol Cell Biol. 2006;7:631–43.CrossRefPubMedGoogle Scholar
  34. Ji H, Coleman J, Yang R, Melia TJ, Rothman JE, Tareste D. Protein determinants of SNARE-mediated lipid mixing. Biophys J. 2010;99:553–60.PubMedPubMedCentralCrossRefGoogle Scholar
  35. Kay JG, Murray RZ, Pagan JK, Stow JL. Cytokine secretion via cholesterol-rich lipid raft-associated SNAREs at the phagocytic cup. J Biol Chem. 2006;281:11949–54.CrossRefPubMedGoogle Scholar
  36. Kerschensteiner D, Morgan JL, Parker ED, Lewis RM, Wong RO. Neurotransmission selectively regulates synapse formation in parallel circuits in vivo. Nature. 2009;460:1016–20.PubMedPubMedCentralCrossRefGoogle Scholar
  37. Larghi P, Williamson D, Carpier J, Dogniaux S, Chemin K, Bohineust A, Danglot L, Gaus K, Galli T, Hivroz C. VAMP7 controls T cell activation by regulating the recruitment and phosphorylation of vesicular Lat at TCR-activation sites. Nat Immunol. 2013;14:723–31.CrossRefPubMedGoogle Scholar
  38. Li F, Pincet F, Perez E, Eng WS, Melia TJ, Rothman JE, Tareste D. Energetics and dynamics of SNAREpin folding across lipid bilayers. Nat Struct Mol Biol. 2007;14:890–6.CrossRefPubMedGoogle Scholar
  39. Ligeon LA, Moreau K, Barois N, Bongiovanni A, Lacorre DA, Werkmeister E, Proux-Gillardeaux V, Galli T, Lafont F. Role of VAMP3 and VAMP7 in the commitment of Yersinia pseudotuberculosis to LC3-associated pathways involving single- or double-membrane vacuoles. Autophagy. 2014;10:1588–602.PubMedPubMedCentralCrossRefGoogle Scholar
  40. Liu Y, Sugiura Y, Lin W. The role of Synaptobrevin1/VAMP1 in Ca2+-triggered neurotransmitter release at the mouse neuromuscular junction. J Physiol. 2011;589:1603–18.PubMedPubMedCentralCrossRefGoogle Scholar
  41. Luftman K, Hasan N, Day P, Hardee D, Hu C. Silencing of VAMP3 inhibits cell migration and integrin-mediated adhesion. Biochem Biophys Res Commun. 2009.  https://doi.org/10.1016/j.bbrc.2009.01.036.CrossRefPubMedPubMedCentralGoogle Scholar
  42. Mallard F, Tang B, 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;156:653–64.PubMedPubMedCentralCrossRefGoogle Scholar
  43. Malmersjo S, Di Palma S, Diao J, Lai Y, Pfuetzner RA, Wang AL, McMahon MA, Hayer A, Porteus M, Bodenmiller B, Brunger AT, Meyer T. Phosphorylation of residues inside the SNARE complex suppresses secretory vesicle fusion. EMBO J. 2016;35:1810–21.PubMedPubMedCentralCrossRefGoogle Scholar
  44. Manca P, Mameli O, Caria MA, Torrejon-Escribano B, Blasi J. Distribution of SNAP25, VAMP1 and VAMP2 in mature and developing deep cerebellar nuclei after estrogen administration. Neuroscience. 2014;266:102–15.CrossRefPubMedGoogle Scholar
  45. 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;149:889–99.PubMedPubMedCentralCrossRefGoogle Scholar
  46. Martinez-Arca S, Rudge R, Vacca M, Raposo G, Camonis J, Proux-Gillardeaux V, Daviet L, Formstecher E, Hamburger A, Filippini F, D’Esposito M, Galli T. A dual mechanism controlling the localization and function of exocytic v-SNAREs. Proc Natl Acad Sci USA. 2003;100:9011–6.PubMedPubMedCentralCrossRefGoogle Scholar
  47. Mohrmann R, de Wit H, Verhage M, Neher E, Sorensen JB. Fast vesicle fusion in living cells requires at least three SNARE complexes. Science. 2010;330:502–5.CrossRefPubMedGoogle Scholar
  48. Molino D, Nola S, Lam SM, Verraes A, Proux-Gillardeaux V, Boncompain G, Perez F, Wenk M, Shui G, Danglot L, Galli T. Role of tetanus neurotoxin insensitive vesicle-associated membrane protein in membrane domains transport and homeostasis. Cell Logist. 2015;5:e1025182.PubMedPubMedCentralCrossRefGoogle Scholar
  49. Montecucco C, Schiavo G, Pantano S. SNARE complexes and neuroexocytosis: how many, how close? Trends Biochem Sci. 2005;30:367–72.CrossRefPubMedGoogle Scholar
  50. Moreau K, Ravikumar B, Renna M, Puri C, Rubinsztein DC. Autophagosome precursor maturation requires homotypic fusion. Cell. 2011;146:303–17.PubMedPubMedCentralCrossRefGoogle Scholar
  51. Murray RZ, Kay JG, Sangermani DG, Stow JL. A role for the phagosome in cytokine secretion. Science. 2005;310:1492–5.CrossRefPubMedGoogle Scholar
  52. Muzerelle A, Alberts P, Martinez-Arca S, Jeannequin O, Lafaye P, Mazie J, 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.CrossRefPubMedGoogle Scholar
  53. Orci L, Malhotra V, Amherdt M, Serafini T, Rothman JE. Dissection of a single round of vesicular transport: sequential intermediates for intercisternal movement in the Golgi stack. Cell. 1989;56:357–68.CrossRefPubMedGoogle Scholar
  54. Polgar J, Chung SH, Reed GL. Vesicle-associated membrane protein 3 (VAMP-3) and VAMP-8 are present in human platelets and are required for granule secretion. Blood. 2002;100:1081–3.CrossRefPubMedGoogle Scholar
  55. Prescott GR, Chamberlain LH. Regional and developmental brain expression patterns of SNAP25 splice variants. BMC Neurosci. 2011;12:35.PubMedPubMedCentralCrossRefGoogle Scholar
  56. Proux-Gillardeaux V, Galli T. Targeting the epithelial SNARE machinery by bacterial neurotoxins. Methods Mol Biol. 2008;440:187–201.CrossRefPubMedGoogle Scholar
  57. Proux-Gillardeaux V, Gavard J, Irinopoulou T, Mege R, Galli T. Tetanus neurotoxin-mediated cleavage of cellubrevin impairs epithelial cell migration and integrin-dependent cell adhesion. Proc Natl Acad Sci USA. 2005a;102:6362–7.PubMedPubMedCentralCrossRefGoogle Scholar
  58. Proux-Gillardeaux V, Raposo G, Irinopoullou T, Galli T. Expression of the Longin domain of TI-VAMP impairs lysosomal secretion and epithelial cell migration. Biol Cell. 2007;99:261–71.CrossRefPubMedGoogle Scholar
  59. 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. 2005b;6:366–73.CrossRefPubMedGoogle Scholar
  60. Pryor PR, Jackson L, Gray SR, Edeling MA, Thompson A, Sanderson CM, Evans PR, Owen DJ, Luzio JP. Molecular basis for the sorting of the SNARE VAMP7 into endocytic clathrin-coated vesicles by the ArfGAP Hrb. Cell. 2008;134:817–27.PubMedPubMedCentralCrossRefGoogle Scholar
  61. Pryor PR, Luzio JP. Delivery of endocytosed membrane proteins to the lysosome. Biochim Biophys Acta. 2009;1793:615–24.CrossRefPubMedGoogle Scholar
  62. Rao S, Huynh C, Proux-Gillardeaux V, Galli T, Andrews N. Identification of SNAREs involved in synaptotagmin VII-regulated lysosomal exocytosis. J Biol Chem. 2004;279:20471–9.CrossRefPubMedGoogle Scholar
  63. Raptis A, Torrejon-Escribano B, Gomez de Aranda I, Blasi J. Distribution of synaptobrevin/VAMP 1 and 2 in rat brain. J Chem Neuroanat. 2005;30:201–11.CrossRefPubMedGoogle Scholar
  64. Ropert N, Jalil A, Li D. Expression and cellular function of vSNARE proteins in brain astrocytes. Neuroscience. 2016;323:76–83.CrossRefPubMedGoogle Scholar
  65. Rothman JE, Warren G. Implication of the SNARE hypothesis for intracellular membrane topology and dynamics. Curr Biol. 1994;4:220–33.CrossRefPubMedGoogle Scholar
  66. Scheuber A, Rudge R, Danglot L, Raposo G, Binz T, Poncer JC, Galli T. Loss of AP-3 function affects spontaneous and evoked release at hippocampal mossy fiber synapses. Proc Natl Acad Sci USA. 2006;103:16562–7.PubMedPubMedCentralCrossRefGoogle Scholar
  67. Sherry DM, Wang MM, Frishman LJ. Differential distribution of vesicle associated membrane protein isoforms in the mouse retina. Mol Vis. 2003;9:673–88.PubMedGoogle Scholar
  68. Skalski M, Coppolino MG. SNARE-mediated trafficking of alpha5beta1 integrin is required for spreading in CHO cells. Biochem Biophys Res Commun. 2005;335:1199–210.CrossRefPubMedGoogle Scholar
  69. Skalski M, Yi Q, Kean MJ, Myers DW, Williams KC, Burtnik A, Coppolino MG. Lamellipodium extension and membrane ruffling require different SNARE-mediated trafficking pathways. BMC Cell Biol. 2010;11:62.PubMedPubMedCentralCrossRefGoogle Scholar
  70. Slezak M, Grosche A, Niemiec A, Tanimoto N, Pannicke T, Munch TA, Crocker B, Isope P, Hartig W, Beck SC, Huber G, Ferracci G, Perraut M, Reber M, Miehe M, Demais V, Leveque C, Metzger D, Szklarczyk K, Przewlocki R, Seeliger MW, Sage-Ciocca D, Hirrlinger J, Reichenbach A, Reibel S, Pfrieger FW. Relevance of exocytotic glutamate release from retinal glia. Neuron. 2012;74:504–16.CrossRefPubMedGoogle Scholar
  71. Söllner 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. 1993a;75:409–18.CrossRefPubMedGoogle Scholar
  72. Söllner T, Whiteheart SW, Brunner M, Erdjument-Bromage H, Geromanos S, Tempst P, Rothman JE. SNAP receptors implicated in vesicle targeting and fusion. Nature. 1993b;362:318–24.CrossRefPubMedGoogle Scholar
  73. Steffen A, Le Dez G, Poincloux R, Recchi C, Nassoy P, Rottner K, Galli T, Chavrier P. MT1-MMP-dependent invasion is regulated by TI-VAMP/VAMP7. Curr Biol. 2008;18:926–31.CrossRefPubMedGoogle Scholar
  74. Sudhof TC. Neurotransmitter release: the last millisecond in the life of a synaptic vesicle. Neuron. 2013;80:675–90.CrossRefGoogle Scholar
  75. Szalinski CM, Labilloy A, Bruns JR, Weisz OA. VAMP7 modulates ciliary biogenesis in kidney cells. PLoS One. 2014;9:e86425.PubMedPubMedCentralCrossRefGoogle Scholar
  76. Tayeb MA, Skalski M, Cha MC, Kean MJ, Scaife M, Coppolino MG. Inhibition of SNARE-mediated membrane traffic impairs cell migration. Exp Cell Res. 2005;305:63–73.CrossRefPubMedGoogle Scholar
  77. Trimble WS. Analysis of the structure and expression of the VAMP family of synaptic vesicle proteins. J Physiol Paris. 1993;87:107–15.CrossRefPubMedGoogle Scholar
  78. van den Bogaart G, Holt MG, Bunt G, Riedel D, Wouters FS, Jahn R. One SNARE complex is sufficient for membrane fusion. Nat Struct Mol Biol. 2010;17:358–64.PubMedPubMedCentralCrossRefGoogle Scholar
  79. Veale KJ, Offenhauser C, Whittaker SP, Estrella RP, Murray RZ. Recycling endosome membrane incorporation into the leading edge regulates lamellipodia formation and macrophage migration. Traffic. 2010;11:1370–9.CrossRefPubMedGoogle Scholar
  80. Vivona S, Liu CW, Strop P, Rossi V, Filippini F, Brunger AT. The longin SNARE VAMP7/TI-VAMP adopts a closed conformation. J Biol Chem. 2010;285:17965–73.PubMedPubMedCentralCrossRefGoogle Scholar
  81. Wada N, Kishimoto Y, Watanabe D, Kano M, Hirano T, Funabiki K, Nakanishi S. Conditioned eyeblink learning is formed and stored without cerebellar granule cell transmission. Proc Natl Acad Sci USA. 2007;104:16690–5.PubMedPubMedCentralCrossRefGoogle Scholar
  82. Williams KC, McNeilly RE, Coppolino MG. SNAP23, Syntaxin4, and vesicle-associated membrane protein 7 (VAMP7) mediate trafficking of membrane type 1-matrix metalloproteinase (MT1-MMP) during invadopodium formation and tumor cell invasion. Mol Biol Cell. 2014;25:2061–70.PubMedPubMedCentralCrossRefGoogle Scholar
  83. Wojnacki Fonseca JI, Galli T. Membrane traffic during axon development. Dev Neurobiol. 2016.  https://doi.org/10.1002/dneu.22390.CrossRefGoogle Scholar
  84. Yamamoto M, Wada N, Kitabatake Y, Watanabe D, Anzai M, Yokoyama M, Teranishi Y, Nakanishi S. Reversible suppression of glutamatergic neurotransmission of cerebellar granule cells in vivo by genetically manipulated expression of tetanus neurotoxin light chain. J Neurosci. 2003;23:6759–67.CrossRefPubMedGoogle Scholar
  85. Zylbersztejn K, Petkovic M, Burgo A, Deck M, Garel S, Marcos S, Bloch-Gallego E, Nothias F, Serini G, Bagnard D, Binz T, Galli T. The vesicular SNARE Synaptobrevin is required for Semaphorin 3A axonal repulsion. J Cell Biol. 2012;196:37–46.PubMedPubMedCentralCrossRefGoogle Scholar

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© Springer International Publishing AG 2018

Authors and Affiliations

  1. 1.Institut Jacques MonodUMR 7592, CNRSParisFrance
  2. 2.Membrane Traffic in Health and Disease, INSERM ERL U950Université Paris Diderot, Paris 7ParisFrance
  3. 3.Institut Jacques MonodParisFrance