Actin disassembles reversibly during electrically induced recycling of synaptic vesicles in cultured neurons

Molecular Brain Research

Volumn 53, Issue 1-2, 1998, Pages 236-250

  Bernstein, B W ^a   Dewit, M ^a   Bamburg, J R ^a  

^a Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

Actin assembly; Cultured neurons; Depolarization; FM1 43; Presynaptic ultrastructure; Vesicle recycling

Indexed keywords

ACTIN; PHALLOIDIN; RHODAMINE;

ANIMAL CELL; ARTICLE; CHICK EMBRYO; DEPOLARIZATION; EMBRYO; EXOCYTOSIS; IMMUNOGOLD STAINING; NERVE CELL CULTURE; NONHUMAN; PRIORITY JOURNAL; SYMPATHETIC NERVE CELL; SYNAPSE VESICLE;

ANIMALIA;

EID: 0031884084     PISSN: 0169328X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0169-328X(97)00319-7     Document Type: Article

References (71)

1. Alder J., Lu B., Valtorta F., Greengard P., Poo M. Calcium-dependent transmitter secretion reconstituted in Xenopus oocytes: requirement for synaptophysin. Science. 257:1992;657-661.
2. Anderson R.G.W., Kamen B.A., Rothberg K.G., Lacey S.W. Potocytosis: sequestration and transport of small molecules by caveolae. Science. 262:1993;410-411.
3. Armbruster B.L., Carlemalm R., Chiovetti R., Garavito R.M., Hobot J.A., Kellenberger E., Villiger W. Specimen preparation for electron microscopy using low temperature embedding resins. J. Microscopy. 126:1982;77-85.
4. Bartlett W.P., Banker G.A. An electron microscopic study of the development of axons and dendrites by hippocampal neurons in culture. J. Neurosci. 4:1984;1944-1965.
5. Bendayan M., Nanci A., Kan F.W.K. Effect of tissue processing on colloidal gold cytochemistry. J. Histochem. Cytochem. 35:1987;983-996.
6. Bennett M.K., Scheller R.H. The molecular machinery for secretion is conserved from yeast to neurons. Proc. Natl. Acad. Sci. U.S.A. 90:1993;2559-2563.
7. Bernstein B.W., Bamburg J.R. Reorganization of actin in depolarized synaptosomes. J. Neurosci. 5:1985;2565-2569.
8. Bernstein B.W., Bamburg J.R. Depolarization of brain synaptosomes activates opposing factors involved in regulating levels of cytoskeletal actin. Neurochem. Res. 12:1987;929-935.
9. Bernstein B.W., Bamburg J.R. Cycling of actin assembly in synaptosomes and transmitter release. Neuron. 3:1989;257-265.
10. Betz W.J., Bewick G.S. Optical analysis of synaptic recycling at the frog neuromuscular junction. Science. 255:1992;200-203.
11. Betz W.J., Bewick G.S., Ridge R.M.A.P. Intracellular movements of fluorescently labeled synaptic vesicles in frog motor nerve terminals during nerve stimulation. Neuron. 9:1992;805-813.
12. Betz W.J., Mao F., Bewick G.S. Activity-dependent staining and destaining of vertebrate motor nerve terminals. J. Neurosci. 12:1992;363-375.
13. D. Bray, Isolated chick neurons for the study of axonal growth, in: G. Banker, K. Goslin, (Eds.), Culturing Nerve Cells, MIT Press, Cambridge, MA, 1991, pp. 119-135.
14. Bridgman P.C., Dailey M.E. The organization of myosin and actin in rapid frozen nerve growth cones. J. Cell Biol. 108:1989;95-109.
15. Chavez-Noriega L.E., Stevens C.F. Increased transmitter release at excitatory synapses produced by direct activation of adenylate cyclase in rat hippocampal slices. J. Neurosci. 14:1994;310-317.
16. Cheek T.R., Burgoyne R.D. Nicotine-evoked disassembly of cortical actin filaments in adrenal chromaffin cells. FEBS Lett. 207:1986;110-114.
17. T.R. Cheek, R.D. Burgoyne, Cytoskeleton in secretion and neurotransmitter release, in: R.D. Burgoyne (Ed.), The Neuronal Cytoskeleton, Wiley, New York, 1991, pp. 309-326.
18. Cowan D., Linial M., Scheller R.H. Torpedo synaptophysin: evolution of a synaptic vesicle protein. Brain Res. 509:1990;1-7.
19. Dailey M.E., Bridgman P.C. Structure and organization of membrane organelles along distal microtubule segments in growth cones. J. Neurosci. Res. 30:1991;242-258.
20. Dan Y., Poo M. Hebbian depression of isolated neuromuscular synapses in vitro. Science. 256:1992;1570-1573.
21. Dancker P., Low I., Hasselbach W., Wieland Th. The interaction of actin with phalloidin: polymerization and stabilization of F-actin. Biochim. Biophys. Acta. 400:1975;407-414.
22. Dascalu A., Nevo Z., Korenstein R. Hyperosmotic activation of the Na(+)-H(+) exchanger in a rat bone cell line: temperature dependence and activation pathways. J. Physiol. 456:1992;503-518.
23. 3H)-dopamine from rat striatal synaptosomes: correlation with calcium entry. J. Neurosci. 3:1983;703-713.
24. Fach B.I., Graham S.F., Keates R.A. Association of fodrin with brain microtubules. Can. J. Biochem. Cell Biol. 63:1985;372-381.
25. Fernandez J.M., Neher E., Gomperts B.D. Capacitance measurements reveal stepwise fusion events in degranulating mast cells. Nature. 312:1984;453-455.
26. Greengard P., Valtorta F., Czernik A.J., Benfenati F. Synaptic vesicle phosphoproteins and regulation of synaptic function. Science. 259:1993;780-785.
27. 2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 260:1985;3440-3450.
28. R.P. Haugland, Molecular Probes Handbook of Fluorescent Probes and Research Chemicals, Eugene, OR, 1992, p. 218.
29. Henkel A.W., Lubke J., Betz W.J. FM1-43 dye ultrastructural localization and release from frog motor nerve terminals. Proc. Natl. Acad. Sci. U.S.A. 93:1996;1918-1923.
30. Hesketh J.E., Harmar A.J., Armstrong A., Arbuthnott G.W. Immunohistochemical localization of a spectrin-like protein (fodrin) in nerve cells in culture. Neurosci. Lett. 63:1986;33-38.
31. Heuser J.E., Reese T.S. Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. J. Cell Biol. 57:1973;315-344.
32. Hirokawa N., Sobue K., Kanda K., Harada A., Yorifuji H. The cytoskeletal architecture of the presynaptic terminal and molecular structure of synapsin I. J. Cell Biol. 108:1989;111-126.
33. Hopkins C.R., Gibson A., Shipman M., Strickland D.K., Trowbridge I.S. In migrating fibroblasts, recycling receptors are concentrated in narrow tubules in the pericentriolar area and then routed to the plasma membrane of the leading lamella. J. Cell Biol. 125:1994;1265-1274.
34. c-src to the cytoskeleton during platelet aggregation. EMBO J. 11:1992;855-861.
35. Howard T.H., Meyer W.H. Chemotactic peptide modulation of actin assembly and locomotion in neutrophils. J. Cell Biol. 98:1984;265-271.
36. 2+. Neuron. 10:1993;797-804.
37. Kagotani Y., Picart R., Barret A., Wiedenmann B., Huttner W.B., Tixier-Vidal A. Subcellular localization of secretogranin II and synaptophysin by immunoelectron microscopy in differentiated hypothalamic neurons in culture. J. Histochem. Cytochem. 39:1991;1507-1518.
38. Koenig E., Repasky E. A regional analysis of alpha-spectrin in the isolated Mauthner neuron and in isolated axons of the goldfish and rabbit. J. Neurosci. 5:1985;705-714.
39. Kraszewski K., Mundigl O., Daniell L., Verderio C., Matteoli M., de Camilli P. Synaptic vesicle dynamics in living cultured hippocampal neurons visualized with CY-3 conjugated antibodies directed against the lumenal domain of synaptotagmin. J. Neurosci. 15:1995;4328-4342.
40. Lankford K.L., Letourneau P.C. Evidence that calcium may control neurite outgrowth by regulating the stability of actin filaments. J. Cell Biol. 109:1989;1229-1243.
41. Letourneau P.C. Differences in the organization of actin in growth cones compared with the neurites of cultured neurons from chick embryos. J. Cell Biol. 97:1983;963-973.
42. Lewis A.K., Bridgman P.C. Nerve growth cone lamellipodia contain two populations of actin filaments that differ in organization and polarity. J. Cell Biol. 119:1992;1219-1243.
43. Luna E.J., Hitt A.L. Cytoskeleton-plasma membrane interactions. Science. 258:1992;955-964.
44. Mains R.E., Patterson P.H. Primary cultures of dissociated sympathetic neurons: I. Establishment of long-term growth in culture and studies of differentiated properties. J. Cell Biol. 59:1973;329-345.
45. Malgaroli A., Ting A.E., Wendland B., Bergamaschi A., Villa A., Tsien R.W., Scheller R.H. Presynaptic component of long-term potentiation visualized at individual hippocampal synapses. Science. 268:1995;1624-1628.
46. Malinow R., Tsien R.W. Presynaptic enhancement shown by whole-cell recordings of long-term potentiation in hippocampal slices. Nature. 346:1990;177-180.
47. Manivannan S., Terakawa S. Rapid sprouting of filopodia in nerve terminals of chromaffin cells, PC 12 cells and dorsal root neurons induced by electrical stimulation. J. Neurosci. 14:1994;5917-5928.
48. Mayer D., Faulstich H. Two sites of intracellular localization of rhodaminyl-phalloidin in hepatocytes. Biol. Cell. 48:1983;143-150.
49. Mayer S., Rothberg K.G., Maxfield F.R. Sequestration of GPI-anchored proteins in caveolae triggered by cross-linking. Science. 264:1994;1948-1951.
50. Miller T.M., Heuser J.E. Endocytosis of synaptic vesicle membrane at the frog neuromuscular junction. J. Cell Biol. 98:1984;685-698.
51. Mitchison T.J. Compare and contrast actin filaments and microtubules. Mol. Biol. Cell. 3:1992;1309-1315.
52. Mochida S., Kobayashi H., Matsuda Y., Yuda Y., Muramoto K., Nonomura Y. Myosin II is involved in transmitter release at synapses formed between rat sympathetic neurons in culture. Neuron. 13:1994;1131-1142.
53. Nakata T., Hirokawa N. Organization of cortical cytoskeleton of cultured chromaffin cells and involvement in secretion as revealed by quick-freeze, deep-etching and double-label immunoelectron microscopy. J. Neurosci. 12:1992;2186-2197.
54. Neely M.D., Gesemann M. Disruption of microfilaments in growth cones following depolarization and calcium influx. J. Neurosci. 14:1994;7511-7520.
55. Paoletti P., Ascher P. Mechanosensitivity of NMDA receptors in cultured mouse central neurons. Neuron. 13:1994;645-655.
56. Regehr W.G., Delaney D.R., Tank D.W. The role of presynaptic calcium in short-term enhancement at the hippocampal mossy fiber synapse. J. Neurosci. 14:1994;523-537.
57. Rosahl T.W., Geppert M., Spillane D., Herz J., Hammer R.E., Malenka R.C., Sudhof T.C. Short-term plasticity is altered in mice lacking synapsin I. Cell. 75:1993;661-670.
58. Rosenmund C., Westbrook G.L. Calcium-induced actin depolymerisation reduces NMDA channel activity. Neuron. 10:1993;805-814.
59. Ryan T.A., Reuter H., Wendland B., Schweizer F.E., Tsien R.W., Smith S.J. The kinetics of synaptic vesicle recycling measured at single presynaptic boutons. Neuron. 11:1993;713-724.
60. Ryan T.A., Ziv N.E., Smith S.J. Potentiation of evoked vesicle turnover at individually resolved synaptic boutons. Neuron. 17:1996;125-134.
61. Sikorski A.F., Terlecki G., Zagon I.S., Goodman S.R. Synapsin I-mediated interaction of brain spectrin with synaptic vesicles. J. Cell Biol. 114:1991;313-318.
62. Strittmatter S.M., Igarashi M., Fishman M.C. GAP-43 amino terminal peptides modulate growth cone morphology and neurite outgrowth. J. Neurosci. 14:1994;5503-5513.
63. Torri-Tarelli F., Haimann C., Ceccarelli B. Coated vesicles and pits during enhanced quantal release at the neuromuscular junction. J. Neurocytol. 16:1987;205-214.
64. Travis J. Cell biologists explore 'tiny caves'. Science. 262:1993;1208-1209.
65. Varon S., Nomura J., Shooter E.M. The isolation of the mouse nerve growth factor protein in a high molecular weight form. Biochemistry. 6:1967;2202-2209.
66. Vitale M.L., Seward E.P., Trifaro J.M. Chromaffin cell cortical actin network dynamics control the size of the release-ready vesicle pool and the initial rate of exocytosis. Neuron. 14:1995;353-363.
67. Wang X.-h., Zheng J.Q., Poo M.-m. Effects of cytochalasin treatment on short-term plasticity at developing neuromuscular junctions in frogs. J. Physiol. 491:1996;187-195.
68. Wieland Th., Faulstich H. Amatoxins, phallotoxins, phallolysin and antamanide: the biologically active components of poisonous Amanita mushrooms. CRC Crit. Rev. Biochem. 5:1978;185-260.
69. B autoreceptor activation. J. Neurosci. 14:1994;1775-1788.
70. Wu L.G., Saggau P. Presynaptic calcium is increased during normal synaptic transmission and paired-pulse facilitation, but not in long-term potentiation in area CA1 of hippocampus. J. Neurosci. 14:1994;645-654.
71. Zagon I.S., Higbee R., Riederer B.M., Goodman S.R. Spectrin subtypes in mammalian brain: an immunoelectron microscopic study. J. Neurosci. 6:1986;2977-2986.