Kiss-and-run, collapse and 'readily retrievable' vesicles

Traffic

Volumn 8, Issue 9, 2007, Pages 1137-1144

  Rizzoli, Silvio O ^a   Jahn, Reinhard ^a  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

Author keywords

Clathrin; Endocytosis; Exocytosis; Recycling; Synaptic vesicle

Indexed keywords

CLATHRIN; CLATHRIN HEAVY CHAIN; DYNAMIN; ENDOPHILIN; SYNAPTOBREVIN; SYNAPTOPHYSIN; SYNAPTOTAGMIN;

BRAIN NERVE CELL; CELL ORGANELLE; COATED PIT; COATED VESICLE; ENDOCYTOSIS; EXOCYTOSIS; NERVE CELL MEMBRANE; NERVE CELL STIMULATION; NERVE ENDING; NERVE POTENTIAL; NEUROMUSCULAR SYNAPSE; NONHUMAN; POSTSYNAPTIC MEMBRANE; PRESYNAPTIC MEMBRANE; PRIORITY JOURNAL; REVIEW; SYNAPSE VESICLE;

ANIMALS; CLATHRIN-COATED VESICLES; ENDOCYTOSIS; EXOCYTOSIS; HUMANS; MEMBRANE FUSION; MODELS, BIOLOGICAL; SYNAPTIC MEMBRANES; SYNAPTIC VESICLES; TRANSPORT VESICLES;

EID: 34547843507     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2007.00614.x     Document Type: Review

References (67)

1. Katz B. Neural transmitter release: From quantal secretion to exocytosis and beyond. The Fenn Lecture. J Neurocytol 1996;25:677-686.
2. Heuser JE, Reese TS. Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. J Cell Biol 1973;57:315-344.
3. Ceccarelli B, Hurlbut WP, Mauro A. Turnover of transmitter and synaptic vesicles at the frog neuromuscular junction. J Cell Biol 1973;57:499-524.
4. Fesce R, Grohovaz F, Valtorta F, Meldolesi J. Neurotransmitter release: fusion or 'kiss-and-run'? Trends Cell Biol 1994;4:1-4.
5. Rizzoli SO, Betz WJ. Synaptic vesicle pools. Nat Rev Neurosci 2005;6:57-69.
6. Gennaro JF Jr, Nastuk WL, Rutherford DT. Reversible depletion of synaptic vesicles induced by application of high external potassium to the frog neuromuscular junction. J Physiol 1978;280:237-247.
7. Miller TM, Heuser JE. Endocytosis of synaptic vesicle membrane at the frog neuromuscular junction. J Cell Biol 1984;98:685-698.
8. Brodin L, Low P, Shupliakov O. Sequential steps in clathrin-mediated synaptic vesicle endocytosis. Curr Opin Neurobiol 2000;10:312-320.
9. Perrais D, Merrifield CJ. Dynamics of endocytic vesicle creation. Dev Cell 2005;9:581-592.
10. Richards DA, Guatimosim C, Rizzoli SO, Betz WJ. Synaptic vesicle pools at the frog neuromuscular junction. Neuron 2003;39:529-541.
11. Koenig JH, Ikeda K. Disappearance and reformation of synaptic vesicle membrane upon transmitter release observed under reversible blockage of membrane retrieval. J Neurosci 1989;9:3844-3860.
12. Harata N, Pyle JL, Aravanis AM, Mozhayeva M, Kavalali ET, Tsien RW. Limited numbers of recycling vesicles in small CNS nerve terminals: implications for neural signaling and vesicular cycling. Trends Neurosci 2001;24:637-643.
13. Sara Y, Mozhayeva MG, Liu X, Kavalali ET. Fast vesicle recycling supports neurotransmission during sustained stimulation at hippocampal synapses. J Neurosci 2002;22:1608-1617.
14. Takei K, Mundigl O, Daniell L, De Camilli P. The synaptic vesicle cycle: a single vesicle budding step involving clathrin and dynamin. J Cell Biol 1996;133:1237-1250.
15. Torri-Tarelli F, Haimann C, Ceccarelli B. Coated vesicles and pits during enhanced quantal release of acetylcholine at the neuromuscular junction. J Neurocytol 1987;16:205-214.
16. Matteoli M, Takei K, Perin MS, Sudhof TC, De Camilli P. Exo-endocytotic recycling of synaptic vesicles in developing processes of cultured hippocampal neurons. J Cell Biol 1992;117:849-861.
17. Willig KI, Rizzoli SO, Westphal V, Jahn R, Hell SW. STED microscopy reveals that synaptotagmin remains clustered after synaptic vesicle exocytosis. Nature 2006;440:935-939.
18. Sara Y, Virmani T, Deak F, Liu X, Kavalali ET. An isolated pool of vesicles recycles at rest and drives spontaneous neurotransmission. Neuron 2005;45:563-573.
19. Llobet A, Beaumont V, Lagnado L. Real-time measurement of exocytosis and endocytosis using interference of light. Neuron 2003;40:1075-1086.
20. Jockusch WJ, Praefcke GJ, McMahon HT, Lagnado L. Clathrin-dependent and clathrin-independent retrieval of synaptic vesicles in retinal bipolar cells. Neuron 2005;46:869-878.
21. Granseth B, Odermatt B, Royle SJ, Lagnado L. Clathrin-mediated endocytosis is the dominant mechanism of vesicle retrieval at hippocampal synapses. Neuron 2006;51:773-786.
22. Heuser JE, Reese TS. Structural changes after transmitter release at the frog neuromuscular junction. J Cell Biol 1981;88:564-580.
23. Torri-Tarelli F, Grohovaz F, Fesce R, Ceccarelli B. Temporal coincidence between synaptic vesicle fusion and quantal secretion of acetylcholine. J Cell Biol 1985;101:1386-1399.
24. Rizzoli SO, Betz WJ. The structural organization of the readily releasable pool of synaptic vesicles. Science 2004;303:2037-2039.
25. Gandhi SP, Stevens CF. Three modes of synaptic vesicular recycling revealed by single-vesicle imaging. Nature 2003;423:607-613.
26. Sun JY, Wu XS, Wu LG. Single and multiple vesicle fusion induce different rates of endocytosis at a central synapse. Nature 2002;417:555-559.
27. Yamashita T, Hige T, Takahashi T. Vesicle endocytosis requires dynamin-dependent GTP hydrolysis at a fast CNS synapse. Science 2005;307:124-127.
28. Wu W, Xu J, Wu XS, Wu LG. Activity-dependent acceleration of endocytosis at a central synapse. J Neurosci 2005;25:11676-11683.
29. He L, Wu XS, Mohan R, Wu LG. Two modes of fusion pore opening revealed by cell-attached recordings at a synapse. Nature 2006;444:102-105.
30. Klyachko VA, Jackson MB. Capacitance steps and fusion pores of small and large-dense-core vesicles in nerve terminals. Nature 2002;418:89-92.
31. Klingauf J, Kavalali ET, Tsien RW. Kinetics and regulation of fast endocytosis at hippocampal synapses. Nature 1998;394:581-585.
32. Richards DA, Guatimosim C, Betz WJ. Two endocytic recycling routes selectively fill two vesicle pools in frog motor nerve terminals. Neuron 2000;27:551-559.
33. Fernandez-Alfonso T, Ryan TA. The kinetics of synaptic vesicle pool depletion at CNS synaptic terminals. Neuron 2004;41:943-953.
34. Harata NC, Choi S, Pyle JL, Aravanis AM, Tsien RW. Frequency-dependent kinetics and prevalence of kiss-and-run and reuse at hippocampal synapses studied with novel quenching methods. Neuron 2006;49:243-256.
35. Zenisek D, Steyer JA, Feldman ME, Almers W. A membrane marker leaves synaptic vesicles in milliseconds after exocytosis in retinal bipolar cells. Neuron 2002;35:1085-1097.
36. Aravanis AM, Pyle JL, Tsien RW. Single synaptic vesicles fusing transiently and successively without loss of identity. Nature 2003;423:643-647.
37. Richards DA, Bai J, Chapman ER. Two modes of exocytosis at hippocampal synapses revealed by rate of FM1-43 efflux from individual vesicles. J Cell Biol 2005;168:929-939.
38. Chen X, Barg S, Smoody B, Almers W. Release of FM1-43 by single synaptic vesicles in cultured hippocampal neurons. 2006. Program No. 336.13/I5. Neuroscience Meeting Planner. Atlanta, GA: Society for Neuroscience; 2006. Online.
39. Stevens CF, Williams JH. "Kiss and run" exocytosis at hippocampal synapses. Proc Natl Acad Sci U S A 2000;97:12828-12833.
40. Newton AJ, Kirchhausen T, Murthy VN. Inhibition of dynamin completely blocks compensatory synaptic vesicle endocytosis. Proc Natl Acad Sci U S A 2006;103:17955-17960.
41. Verstreken P, Kjaerulff O, Lloyd TE, Atkinson R, Zhou Y, Meinertzhagen IA, Bellen HJ. Endophilin mutations block clathrin-mediated endocytosis but not neurotransmitter release. Cell 2002;109:101-112.
42. Guichet A, Wucherpfennig T, Dudu V, Etter S, Wilsch-Brauniger M, Hellwig A, Gonzalez-Gaitan M, Huttner WB, Schmidt AA. Essential role of endophilin A in synaptic vesicle budding at the Drosophila neuromuscular junction. EMBO J 2002;21:1661-1672.
43. Dickman DK, Horne JA, Meinertzhagen IA, Schwarz TL. A slowed classical pathway rather than kiss-and-run mediates endocytosis at synapses lacking synaptojanin and endophilin. Cell 2005;123:521-533.
44. Harata NC, Aravanis AM, Tsien RW. Kiss-and-run and full-collapse fusion as modes of exo-endocytosis in neurosecretion. J Neurochem 2006;97:1546-1570.
45. Pyle JL, Kavalali ET, Piedras-Renteria ES, Tsien RW. Rapid reuse of readily releasable pool vesicles at hippocampal synapses. Neuron 2000;28:221-231.
46. Li Z, Burrone J, Tyler WJ, Hartman KN, Albeanu DF, Murthy VN. Synaptic vesicle recycling studied in transgenic mice expressing synaptopHluorin. Proc Natl Acad Sci U S A 2005;102:6131-6136.
47. Wesseling JF, Lo DC. Limit on the role of activity in controlling the release-ready supply of synaptic vesicles. J Neurosci 2002;22:9708-9720.
48. Takamori S, Holt M, Stenius K, Lemke EA, Gronborg M, Riedel D, Urlaub H, Schenck S, Brugger B, Ringler P, Muller SA, Rammner B, Grater F, Hub JS, De Groot BL et al. Molecular anatomy of a trafficking organelle. Cell 2006;127:831-846.
49. Valtorta F, Jahn R, Fesce R, Greengard P, Ceccarelli B. Synaptophysin (p38) at the frog neuromuscular junction: Its incorporation into the axolemma and recycling after intense quantal secretion. J Cell Biol 1988;107:2717-2727.
50. Mitchell SJ, Ryan TA. Syntaxin-1A is excluded from recycling synaptic vesicles at nerve terminals. J Neurosci 2004;24:4884-4888.
51. Jung N, Haucke V. Clathrin-mediated endocytosis at synapses. Traffic 2007; doi:10.1111/j.1600-0854.2007.00595.x.
52. Walther K, Diril MK, Jung N, Haucke V. Functional dissection of the interactions of stonin 2 with the adaptor complex AP-2 and synaptotagmin. Proc Natl Acad Sci U S A 2004;101:964-969.
53. Diril MK, Wienisch M, Jung N, Klingauf J, Haucke V. Stonin 2 is an AP-2-dependent endocytic sorting adaptor for synaptotagmin internalization and recycling. Dev Cell 2006;10:233-244.
54. Poskanzer KE, Marek KW, Sweeney ST, Davis GW. Synaptotagmin I is necessary for compensatory synaptic vesicle endocytosis in vivo. Nature 2003;426:559-563.
55. Dittman JS, Kaplan JM. Factors regulating the abundance and localization of synaptobrevin in the plasma membrane. Proc Natl Acad Sci U S A 2006;103:11399-11404.
56. Fernandez-Alfonso T, Kwan R, Ryan TA. Synaptic vesicles interchange their membrane proteins with a large surface reservoir during recycling. Neuron 2006;51:179-186.
57. Wienisch M, Klingauf J. Vesicular proteins exocytosed and subsequently retrieved by compensatory endocytosis are nonidentical. Nat Neurosci 2006;9:1019-1027.
58. Neale EA, Bowers LM, Jia M, Bateman KE, Williamson LC. Botulinum neurotoxin A blocks synaptic vesicle exocytosis but not endocytosis at the nerve terminal. J Cell Biol 1999;147:1249-1260.
59. Sankaranarayanan S, Ryan TA. Real-time measurements of vesicle-SNARE recycling in synapses of the central nervous system. Nat Cell Biol 2000;2:197-204.
60. Li Z, Murthy VN. Visualizing postendocytic traffic of synaptic vesicles at hippocampal synapses. Neuron 2001;31:593-605.
61. Darcy KJ, Staras K, Collinson LM, Goda Y. Constitutive sharing of recycling synaptic vesicles between presynaptic boutons. Nat Neurosci 2006;9:315-321.
62. Bennett MK, Calakos N, Kreiner T, Scheller RH. Synaptic vesicle membrane proteins interact to form a multimeric complex. J Cell Biol 1992;116:761-775.
63. Mueller VJ, Wienisch M, Nehring RB, Klingauf J. Monitoring clathrin-mediated endocytosis during synaptic activity. J Neurosci 2004;24:2004-2012.
64. Rizzoli SO, Bethani I, Zwilling D, Wenzel D, Siddiqui TJ, Brandhorst D, Jahn R. Evidence for early endosome-like fusion of recently endocytosed synaptic vesicles. Traffic 2006;7:1163-1176.
65. Voglmaier SM, Kam K, Yang H, Fortin DL, Hua Z, Nicoll RA, Edwards RH. Distinct endocytic pathways control the rate and extent of synaptic vesicle protein recycling. Neuron 2006;51:71-84.
66. Blanpied TA, Scott DB, Ehlers MD. Dynamics and regulation of clathrin coats at specialized endocytic zones of dendrites and spines. Neuron 2002;36:435-449.
67. Zhang Q, Harata N, Tsien R. Use of quantum dots to report exocytotic events with and without full collapse fusion. Program No. 335.9/G14. Neuroscience Meeting Planner. Atlanta, GA: Society for Neuroscience; 2006; Online.