Vti1a Identifies a Vesicle Pool that Preferentially Recycles at Rest and Maintains Spontaneous Neurotransmission

Neuron

Volumn 73, Issue 1, 2012, Pages 121-134

  Ramirez, Denise M O ^a   Khvotchev, Mikhail ^a   Trauterman, Brent ^a   Kavalali, Ege T ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN VAMP7; SNARE PROTEIN; SYNAPTOBREVIN 2; UNCLASSIFIED DRUG; VPS10P TAIL INTERACTOR 1A PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; COMPLEX FORMATION; CONTROLLED STUDY; DOWN REGULATION; ELECTROENCEPHALOGRAM; EMBRYO; EVOKED RESPONSE; HIPPOCAMPUS; MOUSE; NEUROTRANSMISSION; NEUROTRANSMITTER RELEASE; NONHUMAN; PRESYNAPTIC INHIBITION; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN SECRETION; PROTEIN TRANSPORT; RAT; SYNAPSE VESICLE;

ACTION POTENTIALS; ANESTHETICS, LOCAL; ANIMALS; ANIMALS, NEWBORN; BIOLOGICAL TRANSPORT; BIOPHYSICS; CALCIUM; CELLS, CULTURED; ELECTRIC STIMULATION; ENZYME INHIBITORS; EXCITATORY POSTSYNAPTIC POTENTIALS; GREEN FLUORESCENT PROTEINS; HIPPOCAMPUS; HYDROGEN-ION CONCENTRATION; MACROLIDES; MICROSCOPY, IMMUNOELECTRON; MUTATION; NEURONS; PATCH-CLAMP TECHNIQUES; POTASSIUM CHLORIDE; PROTEIN TRANSPORT; QB-SNARE PROTEINS; R-SNARE PROTEINS; RATS; RATS, SPRAGUE-DAWLEY; RNA, SMALL INTERFERING; SNARE PROTEINS; SYNAPSES; SYNAPTIC TRANSMISSION; SYNAPTIC VESICLES; SYNAPTOTAGMIN I; TETRODOTOXIN; VESICLE-ASSOCIATED MEMBRANE PROTEIN 2;

EID: 84855748925     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2011.10.034     Document Type: Article

References (66)

1. Abenavoli A., Forti L., Bossi M., Bergamaschi A., Villa A., Malgaroli A. Multimodal quantal release at individual hippocampal synapses: evidence for no lateral inhibition. J.Neurosci. 2002, 22:6336-6346.
2. Advani R.J., Bae H.R., Bock J.B., Chao D.S., Doung Y.C., Prekeris R., Yoo J.S., Scheller R.H. Seven novel mammalian SNARE proteins localize to distinct membrane compartments. J.Biol. Chem. 1998, 273:10317-10324.
3. Antonin W., Holroyd C., Fasshauer D., Pabst S., Von Mollard G.F., Jahn R. A SNARE complex mediating fusion of late endosomes defines conserved properties of SNARE structure and function. EMBO J. 2000, 19:6453-6464.
4. Antonin W., Riedel D., von Mollard G.F. The SNARE Vti1a-beta is localized to small synaptic vesicles and participates in a novel SNARE complex. J.Neurosci. 2000, 20:5724-5732.
5. Aoto J., Nam C.I., Poon M.M., Ting P., Chen L. Synaptic signaling by all-trans retinoic acid in homeostatic synaptic plasticity. Neuron 2008, 60:308-320.
6. Atasoy D., Ertunc M., Moulder K.L., Blackwell J., Chung C., Su J., Kavalali E.T. Spontaneous and evoked glutamate release activates two populations of NMDA receptors with limited overlap. J.Neurosci. 2008, 28:10151-10166.
7. Atlashkin V., Kreykenbohm V., Eskelinen E.L., 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.
8. Autry A.E., Adachi M., Nosyreva E., Na E.S., Los M.F., Cheng P.F., Kavalali E.T., Monteggia L.M. NMDA receptor blockade at rest triggers rapid behavioural antidepressant responses. Nature 2011, 475:91-95.
9. Bethani I., Werner A., Kadian C., Geumann U., Jahn R., Rizzoli S.O. Endosomal fusion upon SNARE knockdown is maintained by residual SNARE activity and enhanced docking. Traffic 2009, 10:1543-1559.
10. 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. Members of the synaptobrevin/vesicle-associated membrane protein (VAMP) family in Drosophila are functionally interchangeable invivo for neurotransmitter release and cell viability. Proc. Natl. Acad. Sci. USA 2002, 99:13867-13872.
11. Bronk P., Deák F., Wilson M.C., Liu X., Südhof T.C., Kavalali E.T. Differential effects of SNAP-25 deletion on Ca2+ -dependent and Ca2+ -independent neurotransmission. J.Neurophysiol. 2007, 98:794-806.
12. Chung C., Barylko B., Leitz J., Liu X., Kavalali E.T. Acute dynamin inhibition dissects synaptic vesicle recycling pathways that drive spontaneous and evoked neurotransmission. J.Neurosci. 2010, 30:1363-1376.
13. Deák F., Schoch S., Liu X., Südhof T.C., Kavalali E.T. Synaptobrevin is essential for fast synaptic-vesicle endocytosis. Nat. Cell Biol. 2004, 6:1102-1108.
14. Deák F., Shin O.H., Kavalali E.T., Südhof T.C. Structural determinants of synaptobrevin 2 function in synaptic vesicle fusion. J.Neurosci. 2006, 26:6668-6676.
15. Deák F., Liu X., Khvotchev M., Li G., Kavalali E.T., Sugita S., Südhof T.C. Alpha-latrotoxin stimulates a novel pathway of Ca2+-dependent synaptic exocytosis independent of the classical synaptic fusion machinery. J.Neurosci. 2009, 29:8639-8648.
16. Deitcher D.L., Ueda A., Stewart B.A., Burgess R.W., Kidokoro Y., Schwarz T.L. Distinct requirements for evoked and spontaneous release of neurotransmitter are revealed by mutations in the Drosophila gene neuronal-synaptobrevin. J.Neurosci. 1998, 18:2028-2039.
17. Dröse S., Altendorf K. Bafilomycins and concanamycins as inhibitors of V-ATPases and P-ATPases. J.Exp. Biol. 1997, 200:1-8.
18. Dulubova I., Sugita S., Hill S., Hosaka M., Fernandez I., Südhof T.C., Rizo J. A conformational switch in syntaxin during exocytosis: role of munc18. EMBO J. 1999, 18:4372-4382.
19. Fatt P., Katz B. Spontaneous subthreshold activity at motor nerve endings. J.Physiol. 1952, 117:109-128.
20. Fischer von Mollard G., Stevens T.H. A human homolog can functionally replace the yeast vesicle-associated SNARE Vti1p in two vesicle transport pathways. J.Biol. Chem. 1998, 273:2624-2630.
21. Frank C.A., Kennedy M.J., Goold C.P., Marek K.W., Davis G.W. Mechanisms underlying the rapid induction and sustained expression of synaptic homeostasis. Neuron 2006, 52:663-677.
22. Fredj N.B., Burrone J. A resting pool of vesicles is responsible for spontaneous vesicle fusion at the synapse. Nat. Neurosci. 2009, 12:751-758.
23. Groemer T.W., Klingauf J. Synaptic vesicles recycling spontaneously and during activity belong to the same vesicle pool. Nat. Neurosci. 2007, 10:145-147.
24. Groffen A.J., Martens S., Díez Arazola R., Cornelisse L.N., Lozovaya N., de Jong A.P., Goriounova N.A., Habets R.L., Takai Y., Borst J.G., et al. Doc2b is a high-affinity Ca2+ sensor for spontaneous neurotransmitter release. Science 2010, 327:1614-1618.
25. Harata N., Pyle J.L., Aravanis A.M., Mozhayeva M., Kavalali E.T., Tsien R.W. Limited numbers of recycling vesicles in small CNS nerve terminals: implications for neural signaling and vesicular cycling. Trends Neurosci. 2001, 24:637-643.
26. Harris K.M., Sultan P. Variation in the number, location and size of synaptic vesicles provides an anatomical basis for the nonuniform probability of release at hippocampal CA1 synapses. Neuropharmacology 1995, 34:1387-1395.
27. Hoopmann P., Punge A., Barysch S.V., Westphal V., Bückers J., Opazo F., Bethani I., Lauterbach M.A., Hell S.W., Rizzoli S.O. Endosomal sorting of readily releasable synaptic vesicles. Proc. Natl. Acad. Sci. USA 2010, 107:19055-19060.
28. Hua S.Y., Raciborska D.A., Trimble W.S., Charlton M.P. Different VAMP/synaptobrevin complexes for spontaneous and evoked transmitter release at the crayfish neuromuscular junction. J.Neurophysiol. 1998, 80:3233-3246.
29. Hua Y., Sinha R., Martineau M., Kahms M., Klingauf J. A common origin of synaptic vesicles undergoing evoked and spontaneous fusion. Nat. Neurosci. 2010, 13:1451-1453.
30. Hua Z., Leal-Ortiz S., Foss S.M., Waites C.L., Garner C.C., Voglmaier S.M., Edwards R.H. v-SNARE composition distinguishes synaptic vesicle pools. Neuron 2011, 71:474-487.
31. Kavalali E.T., Klingauf J., Tsien R.W. Activity-dependent regulation of synaptic clustering in a hippocampal culture system. Proc. Natl. Acad. Sci. USA 1999, 96:12893-12900.
32. Kavalali E.T., Chung C., Khvotchev M., Leitz J., Nosyreva E., Raingo J., Ramirez D.M. Spontaneous neurotransmission: an independent pathway for neuronal signaling?. Physiology (Bethesda) 2011, 26:45-53.
33. Kennedy M.J., Davison I.G., Robinson C.G., Ehlers M.D. Syntaxin-4 defines a domain for activity-dependent exocytosis in dendritic spines. Cell 2010, 141:524-535.
34. Kreykenbohm V., Wenzel D., Antonin W., Atlachkine V., von Mollard G.F. The SNAREs vti1a and vti1b have distinct localization and SNARE complex partners. Eur. J. Cell Biol. 2002, 81:273-280.
35. Kunwar A.J., Rickmann M., Backofen B., Browski S.M., Rosenbusch J., Schöning S., Fleischmann T., Krieglstein K., Fischer von Mollard G. Lack of the endosomal SNAREs vti1a and vti1b led to significant impairments in neuronal development. Proc. Natl. Acad. Sci. USA 2011, 108:2575-2580.
36. Lee M.C., Yasuda R., Ehlers M.D. Metaplasticity at single glutamatergic synapses. Neuron 2010, 66:859-870.
37. Llano I., González J., Caputo C., Lai F.A., Blayney L.M., Tan Y.P., Marty A. Presynaptic calcium stores underlie large-amplitude miniature IPSCs and spontaneous calcium transients. Nat. Neurosci. 2000, 3:1256-1265.
38. Lois C., Hong E.J., Pease S., Brown E.J., Baltimore D. Germline transmission and tissue-specific expression of transgenes delivered by lentiviral vectors. Science 2002, 295:868-872.
39. 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.
40. Mathew S.S., Pozzo-Miller L., Hablitz J.J. Kainate modulates presynaptic GABA release from two vesicle pools. J.Neurosci. 2008, 28:725-731.
41. Miesenböck G., De Angelis D.A., Rothman J.E. Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 1998, 394:192-195.
42. Mozhayeva M.G., Sara Y., Liu X., Kavalali E.T. Development of vesicle pools during maturation of hippocampal synapses. J.Neurosci. 2002, 22:654-665.
43. Muzerelle A., Alberts P., Martinez-Arca S., Jeannequin O., Lafaye P., Mazié J.C., 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.
44. Nosyreva E., Kavalali E.T. Activity-dependent augmentation of spontaneous neurotransmission during endoplasmic reticulum stress. J.Neurosci. 2010, 30:7358-7368.
45. Pang Z.P., Bacaj T., Yang X., Zhou P., Xu W., Südhof T.C. Doc2 supports spontaneous synaptic transmission by a Ca(2+)-independent mechanism. Neuron 2011, 70:244-251.
46. Prange O., Murphy T.H. Correlation of miniature synaptic activity and evoked release probability in cultures of cortical neurons. J.Neurosci. 1999, 19:6427-6438.
47. Pryor P.R., Jackson L., Gray S.R., Edeling M.A., Thompson A., Sanderson C.M., Evans P.R., Owen D.J., Luzio J.P. Molecular basis for the sorting of the SNARE VAMP7 into endocytic clathrin-coated vesicles by the ArfGAP Hrb. Cell 2008, 134:817-827.
48. Ramirez D.M., Kavalali E.T. Differential regulation of spontaneous and evoked neurotransmitter release at central synapses. Curr. Opin. Neurobiol. 2011, 21:275-282.
49. Ramirez D.M.O., Andersson S., Russell D.W. Neuronal expression and subcellular localization of cholesterol 24-hydroxylase in the mouse brain. J.Comp. Neurol. 2008, 507:1676-1693.
50. Rizzoli S.O., Bethani I., Zwilling D., Wenzel D., Siddiqui T.J., Brandhorst D., Jahn R. Evidence for early endosome-like fusion of recently endocytosed synaptic vesicles. Traffic 2006, 7:1163-1176.
51. Sara Y., Virmani T., Deák F., Liu X., Kavalali E.T. An isolated pool of vesicles recycles at rest and drives spontaneous neurotransmission. Neuron 2005, 45:563-573.
52. Sara Y., Bal M., Adachi M., Monteggia L.M., Kavalali E.T. Use-dependent AMPA receptor block reveals segregation of spontaneous and evoked glutamatergic neurotransmission. J.Neurosci. 2011, 31:5378-5382.
53. Scheuber A., Rudge R., Danglot L., Raposo G., Binz T., Poncer J.C., Galli T. Loss of AP-3 function affects spontaneous and evoked release at hippocampal mossy fiber synapses. Proc. Natl. Acad. Sci. USA 2006, 103:16562-16567.
54. Schoch S., Deák F., Königstorfer A., Mozhayeva M., Sara Y., Südhof T.C., Kavalali E.T. SNARE function analyzed in synaptobrevin/VAMP knockout mice. Science 2001, 294:1117-1122.
55. Shaner N.C., Campbell R.E., Steinbach P.A., Giepmans B.N., Palmer A.E., Tsien R.Y. Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat. Biotechnol. 2004, 22:1567-1572.
56. Sutton M.A., Ito H.T., Cressy P., Kempf C., Woo J.C., Schuman E.M. Miniature neurotransmission stabilizes synaptic function via tonic suppression of local dendritic protein synthesis. Cell 2006, 125:785-799.
57. Sutton M.A., Taylor A.M., Ito H.T., Pham A., Schuman E.M. Postsynaptic decoding of neural activity: eEF2 as a biochemical sensor coupling miniature synaptic transmission to local protein synthesis. Neuron 2007, 55:648-661.
58. Takamori S., Holt M., Stenius K., Lemke E.A., Grønborg M., Riedel D., Urlaub H., Schenck S., Brügger B., Ringler P., et al. Molecular anatomy of a trafficking organelle. Cell 2006, 127:831-846.
59. Tochio H., Tsui M.M., Banfield D.K., Zhang M. An autoinhibitory mechanism for nonsyntaxin SNARE proteins revealed by the structure of Ykt6p. Science 2001, 293:698-702.
60. Virmani T., Han W., Liu X., Südhof T.C., Kavalali E.T. Synaptotagmin 7 splice variants differentially regulate synaptic vesicle recycling. EMBO J. 2003, 22:5347-5357.
61. Virmani T., Ertunc M., Sara Y., Mozhayeva M., Kavalali E.T. Phorbol esters target the activity-dependent recycling pool and spare spontaneous vesicle recycling. J.Neurosci. 2005, 25:10922-10929.
62. Washbourne P., Thompson P.M., Carta M., Costa E.T., Mathews J.R., Lopez-Benditó G., Molnár Z., Becher M.W., Valenzuela C.F., Partridge L.D., Wilson M.C. Genetic ablation of the t-SNARE SNAP-25 distinguishes mechanisms of neuroexocytosis. Nat. Neurosci. 2002, 5:19-26.
63. Wienisch M., Klingauf J. Vesicular proteins exocytosed and subsequently retrieved by compensatory endocytosis are nonidentical. Nat. Neurosci. 2006, 9:1019-1027.
64. Wilhelm B.G., Groemer T.W., Rizzoli S.O. The same synaptic vesicles drive active and spontaneous release. Nat. Neurosci. 2010, 13:1454-1456.
65. Xu J., Pang Z.P., Shin O.H., Südhof T.C. Synaptotagmin-1 functions as a Ca2+ sensor for spontaneous release. Nat. Neurosci. 2009, 12:759-766.
66. Zenisek D. Vesicle association and exocytosis at ribbon and extraribbon sites in retinal bipolar cell presynaptic terminals. Proc. Natl. Acad. Sci. USA 2008, 105:4922-4927.