Mobility of synaptic vesicles in nerve endings monitored by recovery from photobleaching of synaptic vesicle-associated fluorescence

Journal of Neuroscience

Volumn 16, Issue 19, 1996, Pages 5905-5913

  Kraszewski, Kajetan ^a   Daniell, Laurie ^a   Mundigl, Olaf ^a   De Camilli, Pietro ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

CY3; endocytosis; exocytosis; FM1 43; staurosporine; synapses; synaptotagmin

Indexed keywords

STAUROSPORINE; SYNAPTOTAGMIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BLEACHING; CELL MEMBRANE; CYTOSKELETON; ENDOCYTOSIS; ENDOSOME; EXOCYTOSIS; FETUS; FLUORESCENCE; NERVE ENDING; NONHUMAN; PRIORITY JOURNAL; RAT; SYNAPSE VESICLE; SYNAPTIC MEMBRANE;

EID: 0029812769     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.16-19-05905.1996     Document Type: Article

References (44)

1. Blasi J, Chapman ER, Yamasaki S, Binz T, Niemann H, Jahn R (1993) Botulinum neurotoxin C1 blocks neurotransmitter release by means of cleaving HPC-1/syntaxin. EMBO J 12:4821-4828.
2. Bartlett WP, Banker GA (1984) An electron microscopic study of the development of axon and dendrites by hippocampal neurons in culture. I. Cells which develop without intracellular contacts. J Neurosci 4:1944-1953.
3. Bennett MK, Scheller RH (1994) A molecular description of synaptic vesicles membrane trafficking. Annu Rev Biochem 63:63-100.
4. Betz WJ, Bewick GS (1992) Optical analysis of synaptic vesicle recycling at the frog neuromuscular junction. Science 255:200-203.
5. Betz WJ, Henkel AW (1994) Okadaic acid disrupts clusters of synaptic vesicles in frog motor nerve terminals. J Cell Biol 124:843-854.
6. Betz WJ, Wu LG (1995) Kinetics of synaptic vesicle recycling. Curr Biol 5:1102-1105.
7. Betz WJ, Bewick GS, Ridge RM (1992a) Intracellular movements of fluorescently labeled synaptic vesicles in frog motor nerve terminals during nerve stimulation. Neuron 9:805-813.
8. Betz WJ, Mao F, Bewick GS (1992b) Activity dependent fluorescent staining and destaining of living vertebrate motor nerve terminals. J Neurosci 12:363-375.
9. Bialojan C, Takai A (1988) Inhibitory effect of a marine-sponge toxin, okadaic acid, on protein phosphatases: specificity and kinetics. Biochem J 256:283-290.
10. Couteaux R, Pecot-Dechavassine M (1974) Les zones specialisees des membranes presynaptiques. Comptes Rendus Hebdomadaires des Seances de l'Academie des Sciences D 278:291-293.
11. De Camilli P, Jahn R (1990) Pathways to regulated exocytosis in neurons. Annu Rev Physiol 52:625-645.
12. De Camilli P, Takei K (1996) Molecular mechanisms in synaptic vesicle endocytosis and recycling. Neuron 16:481-486.
13. De Camilli P, Harris Jr SM, Huttner WB, Greengard P (1983) Synapsin I (protein I), a nerve terminal-specific phosphoprotein. II. Its specific association with synaptic vesicles demonstrated by immunocytochemistry in agarose-embedded synaptosomes. J Cell Biol 96:1355-1373.
14. De Camilli P, Benfenati F, Valtorta F, Greengard P (1990) The synapsins. Annu Rev Cell Biol 6:433-460.
15. De Camilli P, Emr SD, McPherson PS, Novick P (1996) Phosphoinositides as regulators in membrane traffic. Science 271:1533-1539.
16. Fried RC, Blaustein MP (1978) Retrieval and recycling of synaptic vesicle membrane in pinched-off nerve terminals (synaptosomes). J Cell Biol 78:685-700.
17. Harris KM, Sultan P (1995) Variation in the number, location and size of synaptic vesicles provides an anatomical basis for the non-uniform probability of release at hippocampal CA1 synapses. Neuropharmacology 34:1387-1397.
18. Henkel AW, Betz WJ (1995) Staurosporine blocks evoked release of FM1-43 but not acetylcholine from frog motor nerve terminals. J Neurosci 15:8246-8258.
19. Henkel AW, Lübke J, Betz WJ (1996a) FM1-43 dye ultrastructural localization in and release from frog motor nerve terminals. Proc Natl Acad Sci USA 93:1918-1923.
20. Henkel AW, Simpson LL, Ridge AP, Betz WJ (1996b) Synaptic vesicle movements monitored by fluorescence recovery after photobleaching in nerve terminals stained with FM1-43. J Neurosci 16:3960-3967.
21. Hirokawa N, Sobue K, Kanda K, Harada A, Yorifuji H (1989) The cytoskeletal architecture of the presynaptic terminal and molecular structure of synapsin I. J Cell Biol 108:111-126.
22. Heuser JE, Reese TS (1973) Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. J Cell Biol 57:315-344.
23. Kraszewski K, Mundigl O, Daniell L, Verderio C, Matteoli M, De Camilli P (1995) Synaptic vesicle dynamics in living cultured neurons visualized with CY3-conjugated antibodies directed against the lumenal domain of synaptotagmin. J Neurosci 15:4328-4342.
24. Landis DM, Hall AK, Weinstein LA, Reese TS (1988) The organization of cytoplasm at the presynaptic active zone of a central nervous system synapse. Neuron 1:201-209.
25. Malgaroli A, Ting AE, Wendland B, Bergamaschi A, Villa A, Tsien RW, Scheller RH (1995) Presynaptic component of long-term potentiation visualized at individual hippocampal synapses. Science 268:1624-1628.
26. Matteoli M, Takei K, Perin MS, Südhof TC, De Camilli P (1992) Exoendocytotic recycling of synaptic vesicles in developing processes of cultured hippocampal neurons. J Cell Biol 117:849-861.
27. Maycox PR, Link E, Reetz A, Morris SA, Jahn R (1992) Clathrin-coated vesicles in nervous tissue are involved primarily in synaptic vesicle recycling. J Cell Biol 118:1379-1388.
28. Miller TM, Heuser JE (1984) Endocytosis of synaptic vesicle membrane at the frog neuromuscular junction. J Cell Biol 98:685-698.
29. Mundigl O, Matteoli M, Daniell L, Thomas-Reetz A, Metcalf A, Jahn R, De Camilli P (1993) Synaptic vesicle proteins in early endosomes in cultured hippocampal neurons: differential effects of Brefeldin A in axon and dendrites. J Cell Biol 122:1207-1221.
30. Mundigl O, Verderio C, Kraszewski K, De Camilli P, Metteoli M (1995) A radioimmunoassay to monitor synaptic vesicle activity in hippocampal neurons in vitro. Eur J Cell Biol 66:246-256.
31. Navone F, Greengard P, De Camilli P (1984) Synapsin I in nerve terminals: selective association with small synaptic vesicles. Science 226:1209-1211.
32. Pfeffer SR, Kelly RB (1985) The subpopulation of brain coated vesicles that carries synaptic vesicle proteins contains two unique polypeptides. Cell 40:949-957.
33. Pieribone VA, Shupliakov O, Brodin L, Hilfiker-Rothenfluh S, Czernik AJ, Greengard P (1995) Distinct pools of synaptic vesicles in neurotransmitter release. Nature 375:493-497.
34. Rosahl TW, Spillane D, Missler M, Herz J, Selig DK, Wolff JR, Hammer RE, Malenka RC, Südhof TC (1995) Essential functions of synapsins I and II in synaptic vesicle regulation. Nature 375:488-493.
35. Ruegg UT, Burgess GM (1989) Staurosporine, K-252 and UCN-01: potent but nonspecific inhibitors of protein kinases. Trends Pharmacol Sci 10:218-220.
36. Ryan TA, Smith SJ (1995) Vesicle pool mobilization during action potential firing at hippocampal synapses. Neuron 14:983-989.
37. Ryan TA, Reuter H, Wendland B, Schweizer FE, Tsien RW, Smith SJ (1993) The kinetics of synaptic vesicle recycling measured at a single presynaptic boutons. Neuron 11:713-724.
38. Ryan TA, Smith SJ, Reuter H (1996) The timing of synaptic vesicle endocytosis. Proc Natl Acad Sci USA 93:5567-5571.
39. Schiavo G, Benfenati F, Poulain B, Rossetto O, Polverino de Laureto P, DasGupta BR, Montecucco C (1992) Tetanus and botulinum-B neurotoxins block neurotransmitter release by proteolytic cleavage of synaptobrevin. Nature 359:832-835.
40. Schweizer FE, Betz H, Augustine GJ (1995) From vesicle docking to endocytosis: intermediate reactions of exocytosis. Neuron 14:689-696.
41. Southwick PL, Ernst LA, Tauriello EW, Parker SR, Mujumdar RB, Mujumdar SR, Clever HA, Waggoner AS (1990) Cyanide dye labeling reagents - carboxymethylindocyanine succinimidyl esters. Cytometry 11:418-430.
42. Stinchcombe JC, Nomoto H, Cutler DF, Hopkins CR (1995) Anterograde and retrograde traffic between the rough endoplasmic reticulum and the Golgi complex. J Cell Biol 131:1387-1401.
43. Südhof TC (1995) The synaptic vesicle cycle: a cascade of protein-protein interactions. Nature 375:645-653.
44. Takei K, Mundigl O, Daniell L, De Camilli P (1996) The synaptic vesicle cycle: a single vesicle budding step involving clathrin and dynamin. J Cell Biol 133:1237-1250.