Syntaxin1A lateral diffusion reveals transient and local SNARE interactions

Journal of Neuroscience

Volumn 31, Issue 48, 2011, Pages 17590-17602

  Ribrault, Claire ^a   Reingruber, Jürgen ^b   Petković, Maja ^b,c   Galli, Thierry ^b   Ziv, Noam E ^d   Holcman, David ^b   Triller, Antoine ^a  

^a ECOLE NORMALE SUPÉRIEURE   (France)

^b INSERM   (France)

^c INSTITUT JACQUES MONOD   (France)

^d TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

SYNAPSIN I; SYNAPTOSOMAL ASSOCIATED PROTEIN 25; SYNTAXIN 1A;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DIFFUSION; DNA TRANSFECTION; EMBRYO; FLUORESCENCE IMAGING; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; IMMUNOFLUORESCENCE TEST; KINETICS; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PRESYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; RAT; SINGLE PARTICLE TRACKING; SPINAL CORD NERVE CELL; SYNAPSE; WESTERN BLOTTING;

ANIMALS; AXONS; CELL MEMBRANE; CELLS, CULTURED; ENDOCYTOSIS; EXOCYTOSIS; MODELS, BIOLOGICAL; NEURONS; PROTEIN TRANSPORT; RATS; RATS, SPRAGUE-DAWLEY; SNARE PROTEINS; SPINAL CORD; SYNAPSES; SYNTAXIN 1;

EID: 82655164350     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4065-11.2011     Document Type: Article

References (66)

1. Alcor D, Gouzer G, Triller A (2009) Single-particle tracking methods for the study of membrane receptors dynamics. Eur J Neurosci 30:987-997.
2. Ashery U, Bielopolski N, Barak B, Yizhar O (2009) Friends and foes in synaptic transmission: the role of tomosyn in vesicle priming. Trends Neurosci 32:275-282.
3. Bannai H, Lévi S, Schweizer C, Inoue T, Launey T, Racine V, Sibarita JB, Mikoshiba K, Triller A (2009) Activity-dependent tuning of inhibitory neurotransmission based on GABAAR diffusion dynamics. Neuron 62:670-682.
4. Bowen ME, Weninger K, Ernst J, Chu S, Brunger AT (2005) Singlemolecule studies of synaptotagmin and complexin binding to the SNARE complex. Biophys J 89:690-702.
5. Calamai M, Specht CG, Heller J, Alcor D, Machado P, Vannier C, Triller A (2009) Gephyrin oligomerization controls GlyR mobility and synaptic clustering. J Neurosci 29:7639-7648.
6. Charrier C, Ehrensperger MV, Dahan M, Lévi S, Triller A (2006) Cytoskeleton regulation of glycine receptor number at synapses and diffusion in the plasma membrane. J Neurosci 26:8502-8511.
7. Choquet D, Triller A (2003) The role of receptor diffusion in the organization of the postsynaptic membrane. Nat Rev Neurosci 4:251-265.
8. Coggan JS, Bartol TM, Esquenazi E, Stiles JR, Lamont S, Martone ME, Berg DK, Ellisman MH, Sejnowski TJ (2005) Evidence for ectopic neurotransmission at a neuronal synapse. Science 309:446-451.
9. Cohen R, Marom M, Atlas D (2007) Depolarization-evoked secretion requires two vicinal transmembrane cysteines of syntaxin 1A. PLoS One 2:e1273.
10. Dahan M, Lévi S, Luccardini C, Rostaing P, Riveau B, Triller A (2003) Diffusion dynamics of glycine receptors revealed by single-quantum dot tracking. Science 302:442-445.
11. Deverall MA, Gindl E, Sinner EK, Besir H, Ruehe J, Saxton MJ, Naumann CA (2005) Membrane lateral mobility obstructed by polymer-tethered lipids studied at the single molecule level. Biophys J 88:1875-1886.
12. Dresbach T, Qualmann B, Kessels MM, Garner CC, Gundelfinger ED (2001) The presynaptic cytomatrix of brain synapses. Cell Mol Life Sci 58:94-116.
13. Dulubova I, Sugita S, Hill S, Hosaka M, Fernandez I, Südhof TC, Rizo J (1999) A conformational switch in syntaxin during exocytosis: role of munc18. EMBO J 18:4372-4382.
14. Dumoulin A, Rostaing P, Bedet C, Lévi S, Isambert MF, Henry JP, Triller A, Gasnier B (1999) Presence of the vesicular inhibitory amino acid transporter in GABAergic and glycinergic synaptic terminal boutons. J Cell Sci 112:811-823.
15. Dumoulin A, Lévi S, Riveau B, Gasnier B, Triller A (2000) Formation of mixed glycine and GABAergic synapses in cultured spinal cord neurons. Eur J Neurosci 12:3883-3892.
16. Edidin M, Zagyansky Y, Lardner TJ (1976) Measurement of membrane protein lateral diffusion in single cells. Science 191:466-468.
17. Ehrensperger MV (2007) Suivi de molécules uniques à l'aide de nanocristaux semiconducteurs: méthodes et application à l'étude de la dynamique du récepteur de la glycine. PhD thesis, Université Pierre et Marie Curie, Paris, France.
18. Fritschy JM, Harvey RJ, Schwarz G (2008) Gephyrin: where do we stand, where do we go? Trends Neurosci 31:257-264.
19. Garcia EP, McPherson PS, Chilcote TJ, Takei K, De Camilli P (1995) rbSec1A and B colocalize with syntaxin 1 and SNAP-25 throughout the axon, but are not in a stable complex with syntaxin. J Cell Biol 129: 105-120.
20. Gerber SH, Rah JC, Min SW, Liu X, de Wit H, Dulubova I, Meyer AC, Rizo J, Arancillo M, Hammer RE, Verhage M, Rosenmund C, Südhof TC (2008) Conformational switch of syntaxin-1 controls synaptic vesicle fusion. Science 321:1507-1510.
21. Gómez-Varela D, Kohl T, Schmidt M, Rubio ME, Kawabe H, Nehring RB, Schäfer S, Stühmer W, Pardo LA (2010) Characterization of Eag1 channel lateral mobility in rat hippocampal cultures by single-particletracking with quantum dots. PloS One 5:e8858.
22. Hagiwara A, Fukazawa Y, Deguchi-Tawarada M, Ohtsuka T, Shigemoto R (2005) Differential distribution of release-related proteins in the hip-pocampal CA3 area as revealed by freeze-fracture replica labeling. J Comp Neurol 489:195-216.
23. Hanus C, Ehrensperger MV, Triller A (2006) Activity-dependent movements of postsynaptic scaffolds at inhibitory synapses. J Neurosci 26:4586-4595.
24. Heine M, Groc L, Frischknecht R, Béïque JC, Lounis B, Rumbaugh G, Huganir RL, Cognet L, Choquet D (2008) Surface mobility of postsynaptic AMPARs tunes synaptic transmission. Science 320:201-205.
25. Jahn R, Scheller RH (2006) SNAREs-engines for membrane fusion. Nat Rev Mol Cell Biol 7:631-643.
26. Kalla S, Stern M, Basu J, Varoqueaux F, Reim K, Rosenmund C, Ziv NE, Brose N (2006) Molecular dynamics of a presynaptic active zone protein studied in Munc13-1-enhanced yellow fluorescent protein knock-in mutant mice. J Neurosci 26:13054-13066.
27. Kusumi A, Sako Y, Yamamoto M (1993) Confined lateral diffusion of membrane receptors as studied by single particle tracking (nanovid microscopy). Effects of calcium-induced differentiation in cultured epithelial cells. Biophys J 65:2021-2040.
28. Laage R, Rohde J, Brosig B, Langosch D (2000) A conserved membranespanning amino acid motif drives homomeric and supports heteromeric assembly of presynaptic SNARE proteins. J Biol Chem 275:17481-17487.
29. Lemke EA, Klingauf J (2005) Single synaptic vesicle tracking in individual hippocampal boutons at rest and during synaptic activity. J Neurosci 25:11034-11044.
30. Lévi S, Schweizer C, Bannai H, Pascual O, Charrier C, Triller A (2008) Homeostatic regulation of synaptic GlyR numbers driven by lateral diffusion. Neuron 59:261-273.
31. Lippincott-Schwartz J, Snapp E, Kenworthy A (2001) Studying protein dynamics in living cells. Nat Rev Mol Cell Biol 2:444-456.
32. Lu X, Zhang Y, Shin YK (2008) Supramolecular SNARE assembly precedes hemifusion in SNARE-mediated membrane fusion. Nat Struct Mol Biol 15:700-706.
33. 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. J Cell Biol 149:889-900.
34. Misura KM, Scheller RH, Weis WI (2000) Three-dimensional structure of the neuronal-Sec1-syntaxin 1a complex. Nature 404:355-362.
35. Mitchell SJ, Ryan TA (2004) Syntaxin-1A is excluded from recycling synaptic vesicles at nerve terminals. J Neurosci 24:4884-4888.
36. Mitchell SJ, Ryan TA (2005) Munc18-dependent regulation of synaptic vesicle exocytosis by syntaxin-1A in hippocampal neurons. Neuropharmacology 48:372-380.
37. Nofal S, Becherer U, Hof D, Matti U, Rettig J (2007) Primed vesicles can be distinguished from docked vesicles by analyzing their mobility. J Neurosci 27:1386-1395.
38. Racine V, Sachse M, Salamero J, Fraisier V, Trubuil A, Sibarita JB (2007) Visualization and quantification of vesicle trafficking on a threedimensional cytoskeleton network in living cells. J Microsc 225:214-228.
39. Rickman C, Meunier FA, 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.
40. Rizo J, Rosenmund C (2008) Synaptic vesicle fusion. Nat Struct Mol Biol 15:665-674.
41. Rizo J, Südhof TC (2002) Snares and munc18 in synaptic vesicle fusion. Nat Rev Neurosci 3:641-653.
42. Sankaranarayanan S, De Angelis D, Rothman JE, Ryan TA (2000) The use of pHluorins for optical measurements of presynaptic activity. Biophys J 79:2199-2208.
43. Saxton MJ (1994) Anomalous diffusion due to obstacles: a Monte Carlo study. Biophys J 66:394-401.
44. Saxton MJ (1996) Anomalous diffusion due to binding: a Monte Carlo study. Biophys J 70:1250-1262.
45. Saxton MJ, Jacobson K (1997) Single-particle tracking: applications to membrane dynamics. Annu Rev Biophys Biomol Struct 26:373-399.
46. Schoch S, Deák F, Königstorfer A, Mozhayeva M, Sara Y, Südhof TC, Kavalali ET (2001) SNARE function analyzed in Synaptobrevin/VAMP knockout mice. Science 294:1117-1122.
47. Schuss Z (1980) Theory and applications of stochastic differential equations. New York: Wiley.
48. Sieber JJ, Willig KI, Kutzner C, Gerding-Reimers C, Harke B, Donnert G, Rammner B, Eggeling C, Hell SW, Grubmüller H, Lang T (2007) Anatomy and dynamics of a supramolecular membrane protein cluster. Science 317:1072-1076.
49. Siksou L, Rostaing P, Lechaire JP, Boudier T, Ohtsuka T, Fejtová A, Kao HT, Greengard P, Gundelfinger ED, Triller A, Marty S (2007) Threedimensional architecture of presynaptic terminal cytomatrix. J Neurosci 27:6868-6877.
50. Singer SJ, Nicolson GL (1972) The fluid mosaic model of the structure of cell membranes. Science 175:720-731.
51. Söllner T, Whiteheart SW, Brunner M, Erdjument-Bromage H, Geromanos S, Tempst P, Rothman JE (1993) SNAP receptors implicated in vesicle targeting and fusion. Nature 362:318-324.
52. Sørensen JB, Nagy G, Varoqueaux F, Nehring RB, Brose N, Wilson MC, Neher E (2003) Differential control of the releasable vesicle pools by SNAP-25 splice variants and SNAP-23. Cell 114:75-86.
53. Sprague BL, Pego RL, Stavreva DA, McNally JG (2004) Analysis of binding reactions by fluorescence recovery after photobleaching. Biophys J 86: 3473-3495.
54. Sprague BL, Müller F, Pego RL, Bungay PM, Stavreva DA, McNally JG (2006) Analysis of binding at a single spatially localized cluster of binding sites by fluorescence recovery after photobleaching. Biophys J 91:1169-1191.
55. Star EN, Kwiatkowski DJ, Murthy VN (2002) Rapid turnover of actin in dendritic spines and its regulation by activity. Nat Neurosci 5:239-246.
56. Südhof TC (2004) The synaptic vesicle cycle. Annu Rev Neurosci 27: 509-547.
57. Südhof TC, Rothman JE (2009) Membrane fusion: grappling with SNARE and SM proteins. Science 323:474-477.
58. Triller A, Choquet D (2008) New concepts in synaptic biology derived from single-molecule imaging. Neuron 59:359-374.
59. Tsuriel S, Geva R, Zamorano P, Dresbach T, Boeckers T, Gundelfinger ED, Garner CC, Ziv NE (2006) Local sharing as a predominant determinant of synaptic matrix molecular dynamics. PLoS Biol 4:e271.
60. Tsuriel S, Fisher A, Wittenmayer N, Dresbach T, Garner CC, Ziv NE (2009) Exchange and redistribution dynamics of the cytoskeleton of the active zone molecule Bassoon. J Neurosci 29:351-358.
61. Vereb G, Szöllosi J, Matkó J, Nagy P, Farkas T, Vigh L, Mátyus L, Waldmann TA, Damjanovich S (2003) Dynamic, yet structured: the cell membrane three decades after the Singer-Nicolson model. Proc Natl Acad Sci U S A 100:8053-8058.
62. Washbourne P, Thompson PM, Carta M, Costa ET, Mathews JR, Lopez- Benditó G, Molnár Z, Becher MW, Valenzuela CF, Partridge LD, Wilson MC (2002) Genetic ablation of the t-SNARE SNAP-25 distinguishes mechanisms of neuroexocytosis. Nat Neurosci 5:19-26.
63. Weninger K, Bowen ME, Choi UB, Chu S, Brunger AT (2008) Accessory proteins stabilize the acceptor complex for synaptobrevin, the 1:1 syntaxin/SNAP-25 complex. Structure 16:308-320.
64. Westphal V, Rizzoli SO, Lauterbach MA, Kamin D, Jahn R, Hell SW (2008) Video-rate far-field optical nanoscopy dissects synaptic vesicle movement. Science 320:246-249.
65. Wu MN, Fergestad T, Lloyd TE, He Y, Broadie K, Bellen HJ (1999) Syntaxin 1A interacts with multiple exocytic proteins to regulate neurotransmitter release in vivo. Neuron 23:593-605.
66. Zhang Q, Li Y, Tsien RW (2009) The dynamic control of kiss-and-run and vesicular reuse probed with single nanoparticles. Science 323:1448-1453.