Traffic of dynamin within individual Drosophila synaptic boutons relative to compartment-specific markers

Journal of Neuroscience

Volumn 16, Issue 17, 1996, Pages 5443-5456

  Estes, Patricia S ^a   Roos, Jack ^b   Van Der Bliek, Alexander ^c   Kelly, Regis B ^b   Krishnan, K S ^d   Ramaswami, Mani ^a  

^a UNIVERSITY OF ARIZONA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d TATA INSTITUTE OF FUNDAMENTAL RESEARCH   (India)

Author keywords

endocytosis; membrane traffic; neurogenetics; neurotransmitter release; synaptic vesicle recycling; temperature sensitive paralysis; ultrastructure

Indexed keywords

BIOCHEMICAL MARKER; DYNAMIN;

ANIMAL TISSUE; ARTICLE; CELL COMMUNICATION; CELL MEMBRANE DEPOLARIZATION; CELL ULTRASTRUCTURE; CYTOSKELETON; ELECTRON MICROSCOPY; ENDOCYTOSIS; NEUROMUSCULAR SYNAPSE; NEUROTRANSMITTER RELEASE; NONHUMAN; PRESYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN DOMAIN; SYNAPTIC TRANSMISSION;

EID: 0029825051     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.16-17-05443.1996     Document Type: Article

References (65)

1. Adams AEM, Pringle JR (1984) Relationship of actin and tubulin distribution to bud growth in wild-type and morphogenetic-mutant Saccharomyces cerevesiae. J Cell Biol 98:934-945.
2. Atwood HL, Govind CK, Wu C-F (1993) Differential ultrastructure of synaptic terminals on ventral longitudinal abdominal muscles in Drosophila larvae. J Neurobiol 24:1008-1024.
3. Auld V, Fetter R, Broadie K, Goodman C (1995) Gliotactin, a novel transmembrane protein on peripheral glia, is required to form the blood-nerve barrier in Drosophila. Cell 81:757-767.
4. Bate CM (1993) The mesoderm and its derivatives. In: The development of Drosophila melanogaster (Bate CM, Martinez-Arias A, eds), pp 1013-1090. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
5. Bate M, Broadie K (1995) Wiring the fly: the neuromuscular system of the Drosophila embryo. Neuron 15:513-525.
6. Bennett MK, Scheller RH (1993) The molecular mechanism of secretion is conserved from yeast to neurons. Proc Natl Acad Sci USA 90:2559-2563.
7. Bernstein BW, Bamburg JR (1989) Cycling of actin assembly in synaptosomes and neurotransmitter release. Neuron 3:257-265.
8. Betz WJ, Wu L-G (1995) Kinetics of synaptic-vesicle recycling. Curr Biol 5:1098-1101.
9. Betz WJ, Mao FM, Bewick GS (1992) Activity-dependent fluorescent staining and destaining of living vertebrate motor nerve terminals. J Neurosci 12:363-375.
10. Broadie KS, Bate M (1993) Development of the embryonic neuromuscular synapse of Drosophila melanogaster. J Neurosci 13:144-166.
11. Burns M, Augustine G (1995) Synaptic structure and function: dynamic organization yields architectural precision. Cell 83:187-194.
12. Ceccaldi PE, Grohovaz F, Benfenati F, Chieregatti E, Greengard P, Valtorta F (1995) Dephosphorylated synapsin I anchors synaptic vesicles to actin cytoskeleton: an analysis by video microscopy. J Cell Biol 128:905-912.
13. Chen YS, Obar RA, Schroeder CC, Austin TW, Poodry CA, Wadsworth SC, Vallee RB (1991) Multiple forms of dynamin are encoded by the shibire, a Drosophila gene involved in endocytosis. Nature 351:583-586.
14. Damke H, Baba T, Warnock DE, Schmid SL (1994) Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J Cell Biol 127:915-934.
15. Damke H, Baba T, van der Bliek A, Schmid S (1995) Clathrin-independent pinocytosis is induced in cells overexpressing a temperature-sensitive mutant of dynamin. J Cell Biol 131:69-80.
16. David C, McPherson P, Mundigl O, DeCamilli (1996) A role for amphiphysin in synaptic vesicle endocytosis supported by its binding to dynamin in nerve terminals. Proc Natl Acad Sci USA 93:331-335.
17. De Camilli P, Takei K, McPherson P (1995) The function of dynamin in endocytosis. Curr Opin Neurobiol 5:559-565.
18. DiAntonio A, Parfitt K, Schwarz TL (1993) Synaptic transmission persists in synaptotagmin mutants of Drosophila. Cell 73:1281-1290.
19. Garcia EP, McPherson PS, Chilcotc TJ, Takei K, DeCamilli 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. Gass GV, Lin JJ-C, Scaife R, Wu C-F (1995) Two isoforms of Drosophila dynamin in wild-type and shibire ts neural tissue: different subcellular localization and association. J Neurogenet, in press.
21. Goodman CS, Bastiani M, Doe C, du Lac D, Helfand S, Kuwada J, Thomas JB (1984) Cell recognition during neuronal development. Science 225:1271-1279.
22. Gricco F, Hay JM, Hull R (1992) An improved procedure for the purification of protein fused with glutathione-S-transferase. Biotechniques 13:856-857.
23. Griffiths G, Parton RG, Lucocq J, van Deurs B, Brown D, Slot JW, Geuze HJ (1993) The immunofluorescent era of membrane traffic. Trends Cell Biol 3:214-219.
24. Heuser J, Reese T (1973) Evidence for recycling of synaptic vesicles during transmitter release at the frog neuromuscular junction. J Cell Biol 57:315-344.
25. Heuser J, Reese T (1981) Structural changes after transmitter release at the frog neuromuscular junction. J Cell Biol 88:564-580.
26. Hirokawa N, Sobue K, Kanda K, Harada A, Yorifuji H (1989) The cytoskeletal architecture of the presynaptic terminals and molecular structure of synapsin I. J Cell Biol 108:111-126.
27. Jan LY, Jan YN (1976) Properties of the larval neuromuscular junction in Drosophila melanogaster. J Physiol (Lond) 262:189-214.
28. Jan LY, Jan YN (1982) Antibodies to horseradish peroxidase as specific neuronal markers in Drosophila and in grasshopper embryos. Proc Natl. Acad Sci USA 79:2700-2704.
29. Jia X-X, Gorczyca M, Budnik V (1993) Ultrastructure of neuromuscular junctions in Drosophila: comparison of wild-type and mutants with increased excitability. J Neurobiol 24:1025-1044.
30. Johansen J, Halpern ME, Johansen KM, Keshishian H (1989) Stereotypic morphology of glutamatergic synapses on identified muscle cells of Drosophila larvae. J Neurosci 9:710-725.
31. Katz F, Moats W, Jan YN (1988) A carbohydrate epitope expressed uniquely on the cell surface of Drosophila neurons is altered in the mutant nac (neurally altered carbohydrate). EMBO J 7:3471-3477.
32. Keshishian H, Chiba A, Chang TN, Halfon MS, Harkins EW, Jarecki J, Wang L, Anderson M. Cash S, Halpern ME, Johansen J (1993) Cellular mechanisms governing synaptic development in Drosophila melanogaster. J Neurobiol 24:757-787.
33. Kilmarlin J, Adams AEM (1984) Structural rearrangements of tubulin and actin during the cell cycle of the yeast Saccaromyces. J Cell Biol 98:922-933.
34. Koenig J, Ikeda K (1989) Disappearance and reappearance of synaptic vesicle membrane upon transmitter release observed under reversible blockage of membrane retrieval. J Neurosci 9:3844-3860.
35. Koenig J, Kosaka T, Ikeda K (1989) The relationship between the number of synaptic vesicles and the amount of neurotransmitter released. J Neurosci 9:1937-1942.
36. Kosaka T, Ikeda K (1983) Possible temperature-dependent blockage of synaptic vesicle recycling induced by a single gene mutation in Drosophila. J Neurohiol 14:207-225.
37. Kurdyak P, Atwood HL, Stewart BA, Wu C-F (1994) Differential physiology and morphology of motor axons to ventral longitudinal muscles in larval Drosophila. J Comp Neurol 350:463-472.
38. Lahey T, Gorczyca M, Jia X-X, Budnik V (1994) The Drosophila tumor suppressor gene dlg is required for normal synaptic bouton structure. Neuron 13:823-835.
39. Landis D, Hall A, Weinstein L, Reese T (1988) The organization of cytoplasm at the presynaptic active zone of a central nervous system synapse. Neuron 1:201-209.
40. Lichtman JW, Sunderland WJ, Wilkinson RS (1989) High resolution imaging of synaptic structure with a simple confocal microscope. New Biol 1:75-82.
41. 2+-activated neurotransmitter release. Cell 74:1125-1134.
42. Magrassi L, Purves D, Lichtman JW (1987) Fluorescent probes that stain living nerve terminals. J Neurosci 7:1207-1214.
43. Mastrogiacomo A, Parsons S, Zampighi O, Jenden D, Umbach J, Gunderson C (1994) Cysteine string proteins: a potential link between synaptic vesicles and presynaptic calcium channels. Science 263: 981-982.
44. McPherson PS, Czernik AJ, Chilcote TJ, Onofri F, Benfenati F, Greengard P, Schlessinger J, De Camilli P (1994a) Interaction of Grb2 via its Src homology 3 domain with synaptic proteins including synapsin I. Proc Natl Acad Sci USA 91:6486-6490.
45. McPherson PS, Takei K, Schmid S, De Camilli P (1994b) p145, a major Grb2-binding protein in brain is colocalized with dynamin in nerve terminals where it undergoes activity-dependent dephosphorylation. J Biol Chem 269:30132-30139.
46. Mochida S, Kobayahi H, Matsuda Y, Yuda Y, Muramoto K, Nonomura Y (1994) Myosin II is involved in transmitter release at synapses formed between rat sympathetic neurons in culture. Neuron 13:1131-1142.
47. Morris SA, Schmid SL (1995) The ferrari of endocytosis. Curr Biol 5:113-115.
48. Ramaswami M, Krishnan KS, Kelly RB (1994) Intermediates in synaptic vesicle cycling revealed by optical imaging of Drosophila neuromuscular junctions. Neuron 13:363-375.
49. Robinson PJ, Liu J-P, Powell K, Fykse EM, Sudhof T (1994) Phosphorylation of dynamin I and synaptic vesicle recycling. Trends Neurosci 17:348-353.
50. Rosahl T, Spillane D, Missler M, Herz J, Selig D, Wolff J, Hammer R, Malenka R, Sudhof T (1995) Essential functions of synapsin I and synapsin II in synaptic vesicle regulation. Nature 375:488-493.
51. Sabry JH, O'Connor TP, Evans L, Toroian-Raymond A, Kirschner M, Bentley D (1991) Microtubule behavior during guidance of pioneer neuron growth cones in situ. J Cell Biol 115:381-395.
52. Schulze KL, Broadie K, Perin MS, Bellen HJ (1995) Genetic and electrophysiological studies of Drosophila syntaxin-1A demonstrate its role in nonneuronal secretion and neurotransmission. Cell 80:311-320.
53. Smith DE, Fisher PA (1984) Identification, developmental regulation, and response to heat shock of two antigenically related forms of a major nuclear envelope protein in Drosophila embryos: application of an improved method for affinity purification of antibodies using polypeptides immobilized on nitrocellulose blots. J Cell Biol 99:20-28.
54. Sollner T, Bennett MK, Whiteheart SW, Scheller RH, Rothman JE (1994) A protein assembly-disassembly pathway in vitro that may correspond to sequential steps of synaptic vesicle docking, activation, and fusion. Cell 75:409-418.
55. Stewart BA, Atwood HA, Renger JJ, Wang J, Wu C-F (1994) Improved stability of Drosophila larval neuromuscular preparations in haemolymph like physiological solutions. J Comp Physiol 175:179-191.
56. Sudhof TC (1995) The synaptic vesicle cycle: a cascade of protein-protein interactions. Nature 375:645-653.
57. +-ATPase. Proc Natl Acad Sci USA 92:5396-5400.
58. Takei K, McPherson PS, Schmid S, De Camilli P (1995) Tubular membrane invaginations coated by dynamin rings are induced by GTPγS in nerve terminals. Nature 374:186-190.
59. Torri-Tarelli F, Bossi M, Fesce R, Greengrad P, Valtorta P (1992) Synapsin 1 partially dissociates from synaptic vesicles during exocytosis induced by electrical stimulation. Neuron 9:1143-1153.
60. Towbin H, Staehelin T, Gordon J (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 76:4350-4354.
61. van de Goor J, Ramaswami M, Kelly R (1995) Redistribution of synaptic vesicles and their proteins in temperature-sensitive shibire(ts1) mutant Drosophila. Proc Natl Acad Sci USA 92:5739-5743.
62. van der Bliek A, Meyerowitz E (1991) Dynamin like protein encoded by the Drosophila shibire gene associated with membrane traffic. Nature 351:411-414.
63. Vater C, Raymond C, Ekena K, Howald-Stevenson I, Stevens T (1992) The VPS1 protein, a homolog of dynamin required for vacuolar protein sorting in Saccaromyces cerevisiae, is a GTPase with two functionally separable domains. J Cell Biol 119:772-786.
64. Yoshikami D, Okun LM (1984) Staining of living presynaptic nerve terminals with selective fluorescent dyes. Nature 310:53-56.
65. Zinsmaier K, Eberle K, Buchner E, Walter N, Benzer S (1994) Paralysis and early death in cysteine string protein mutants of Drosophila. Science 263:977-980.