Synaptic vesicles have two distinct recycling pathways

Journal of Cell Biology

Volumn 135, Issue 3, 1996, Pages 797-808

  Koenig, J H ^a   Ikeda, Kazuo ^a  

^a CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; ENDOCYTOSIS; ENDOSOME; EXOCYTOSIS; FEMALE; NERVE ENDING; NEUROTRANSMITTER RELEASE; NONHUMAN; PHOTORECEPTOR CELL; PRIORITY JOURNAL; SYNAPSE VESICLE; TEMPERATURE SENSITIVE MUTANT;

ANIMALS; CALCIUM; CELL MEMBRANE; DROSOPHILA MELANOGASTER; ENDOCYTOSIS; EXOCYTOSIS; FEMALE; MAGNESIUM; MUTATION; PHOTORECEPTORS; SYNAPTIC VESICLES; TEMPERATURE;

ANIMALIA; DROSOPHILA MELANOGASTER; MELANOGASTER;

EID: 0029807825     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.135.3.797     Document Type: Article

References (41)

1. Ágoston, D.V., J.W. Kosh, J. Lisziewicz, and V.P. Whittaker. 1985. Separation of recycling and reserve synaptic vesicles from cholinergic nerve terminals of the myenteric plexus of guinea pig ileum. J. Neurochem. 44:299-305.
2. Bauerfeind, R., A. Regnier-Vigouroux, T. Flatmark, and W.B Huttner. 1993. Selective storage of acetylcholine, but not catecholamines, in neuroendocrine synaptic-like microvesicles of early endosomal origin. Neuron. 11:105-121.
3. Betz, W.J., and G.S. Bewick. 1992. Optical analysis of synaptic vesicle recycling at the frog neuromuscular junction. Science (Wash. DC). 255:200-203.
4. Betz, W.J., and G.S. Bewick. 1993. Optical monitoring of transmitter release and synaptic vesicle recycling at the frog neuromuscular junction. J. Physiol. 460:287-309.
5. Birks, R.I., and F.C. Macintosh. 1961. Acetylcholine metabolism of a sympathetic ganglion. Can. J. Biochem. Physiol. 39:787-827.
6. Cameron, P.L., T.C. Südhof, R. Jahn, and P. De Camilli. 1991. Colocalization of synaptophysin with transferrin receptors: implications for synaptic vesicle biogenesis. J. Cell Biol. 115:151-164.
7. Ceccarelli, B., and W.P. Hurlbut. 1980. Vesicle hypothesis of the release of quanta of acetylcholine. Physiol. Rev. 60:396-441.
8. Ceccarelli, B., W.P. Hurlbut, and A. Mauro. 1973. Turnover of transmitter and synaptic vesicles at the frog neuromuscular junction. J. Cell Biol. 57:499-524.
9. 2+-free solutions on the structure of the active zone. II. Effects of electrical stimulation and high potassium. J. Cell Biol. 81:163-192.
10. Chen, M.S., R.A. Obar, C.C. Schroeder, T.W. Austin, C.A. Poodry, S.C. Wadsworth, and R.B. Vallee. 1991. Multiple forms of dynamin are encoded by shibire, a Drosophila gene involved in endocytosis. Nature (Lond.). 351: 583-586.
11. Clift-O'Grady, L., A.D. Linstedt, A.W. Lowe, E. Grote, and R.B. Kelly. 1990. Biogenesis of synaptic vesicle-like structure in a pheocromocytoma cell line PC12. J. Cell Biol. 110:1693-1703.
12. Damke, H., T. Baba, D.E. Warnock, and S. Schmid. 1994. Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J. Cell Biol. 127:915-934.
13. del Castillo, J., and B. Katz. 1955. La base "quantale" de la transmission neuromusculaire. In Micophysiologie Comparée des Élements Excitables. Centre National de la Recherche Scientifique Colloques Internationaux. Vol. 67. Paris. 245-258.
14. Fesce, R., F. Grohovaz, F. Valtorta, and J. Meldolesi. 1994. Neurotransmitter release: fusion or "kiss-and-run"? Trends Cell Biol. 4:1-4.
15. Giompres, P.E., H. Zimmermann, and V.P. Whittaker. 1981. Purification of small dense vesicles from stimulated Torpedo electric tissue by glass bead column chromatography. Neuroscience. 6:765-774.
16. Haimann, C., F. Torri-Tarelli, R. Fesce, and B. Ceccarelli. 1985. Measurement of quantal secretion induced by ouabain and its correlation with depletion of synaptic vesicles. J. Cell Biol. 101:1953-1965.
17. Heuser, J.E. 1989. Review of electron microscopic evidence favoring vesicle exocytosis as the structural basis of quantal release during synaptic transmission. Quart. J. Exp. Physiol. 74:1051-1069.
18. Heuser, J.E., and T.S. Reese. 1973. Evidence tor recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. J. Cell Biol. 57:315-344.
19. Hinshaw, J.E., and S.L. Schmid. 1995. Dynamin self-assembles into rings suggesting a mechanism for coated vesicle budding. Nature (Lond.). 374:190-192.
20. Koenig, J.H., and K. Ikeda. 1989. Disappearance and reformation of synaptic vesicle membrane upon transmitter release observed under reversible blockage of membrane retrieval. J. Neurosci. 9:3844-3860.
21. Koenig, J.H., T. Kosaka, and K. Ikeda. 1989. The relationship between the number of synaptic vesicles and the amount of transmitter released. J. Neurosci. 9:1937-1942.
22. Koenig, J.H., K. Yamaoka, and K. Ikeda. 1993. Calcium-induced translocation of synaptic vesicles to the active site. J. Neurosci. 13:2313-2322.
23. Kosaka, T., and K. Ikeda. 1983a. Possible temperature-dependent blockage of synaptic vesicle recycling induced by a single gene mutation in Drosophila. J. Neurobiol. 14:207-255.
24. is. J. Cell Biol. 97:499-507.
25. Kristensen, H.K., Y.Y. Lau, and A.G. Ewing. 1994. Capillary electrophoresis of single cells: observation of two compartments of neurotransmitter vesicles. J. Neurosci. Meth. 51:183-188.
26. Linstedt, A.D., and R.B. Kelly. 1991. Synaptophysin is sorted from endocytic markers in neuroendocrine PC12 cells. J. Neurocytol. 22:92-101.
27. Pieribone, V.A., O. Shupliakov, L. Brodin, S. Hilfiker-Rothenfluh, A.J. Czernik, and P. Greengard. 1995. Distinct pools of synaptic vesicles in neurotransmitter release. Nature (Lond.). 375:493-497.
28. Prado, M.A.M., M.V. Gomez, and B. Collier. 1992. Mobilization of the readily releasable pool of acetylcholine from a sympathetic ganglion of tityustoxin in the presence of vesamicol. J. Neurochem. 59:544-552.
29. Reetz, A., M. Solimena, M. Matteoli, F. Folli, K. Takei, and P. De Camilli. 1991. GABA and pancreatic β-cells: co-localization of glutamic acid decarboxylase (GAD) and GABA with synaptic-like microvesicles suggests their role in GABA storage and secretion. EMBO (Eur. Mol. Biol. Organ.) J. 10:1275-1284.
30. Régnier-Vigournoux, A., S.A. Tooze, and W.B. Huttner. 1991. Newly synthesized synaptophysin is transported to synaptic-like microvesicles via constitutive secretory vesicles and the plasma membrane. EMBO (Eur. Mol. Biol. Organ.) J. 10:3589-3601.
31. Schwarz, T.L. 1994. Genetic analysis of neurotransmitter release at the synapse. Curr. Opin. Neurobiol. 4:633-639.
32. Takei, K., P.S. McPherson, S.L. Schmid, and P. De Camilli. 1995. Tubular membrane invaginations coated by dynamin rings are induced by GTP-γS in nerve terminals. Nature (Lond.). 374:186-190.
33. Thomas-Reetz, A.C., and P. De Tamilli. 1994. A role of synaptic vesicles in non-neuronal cells: clues from pancreatic β cells and from chromaffin cells. FASEB J. 8:209-215.
34. Torri-Tarelli, F., A. Villa, F. Valtorla, P. De Camilli, P. Greengard, and B. Ceccarelli. 1990. Redistribution of synaptophysin and synapsin I during α-latrotoxin-induced release of neurotransmitter at the neuromuscular junction. J. Cell Biol. 110:449-459.
35. Valtorta, F., R. Jahn, R. Fesce, P. Greengard, and B. Ceccarelli. 1988. Synaptophysin (p38) at the frog neuromuscular junction: its incorporation into the axolemma and recycling after intense quantal secretion. J. Cell Biol. 107: 2719-2730.
36. Valtorta, F., R. Fesce, F. Grohovaz, C. Haimann, W.P. Hurlbut, N. Iezzi, F. Torri Tarelli, A. Villa, and B. Ceccarelli. 1990. Neurotransmitter release and synaptic vesicle recycling. Neuroscience. 351:477-489.
37. van der Blick, A.M., and E.M. Meyerowitz. 1991. Dynamin-like protein encoded by the Drosophila shibire gene associated with vesicular traffic. Nature (Lond.). 351:411-414.
38. von Gersdorff, H., and G. Matthews. 1994. Dynamics of synaptic vesicle fusion and membrane retrieval in synaptic terminals. Nature (Lond.). 367:735-739.
39. von Wedel, R.J., S.S. Carlson, and R.B. Kelly. 1981. Transfer of synaptic vesicle antigens to the presynaptic plasma membrane during exocytosis. Proc. Natl. Acad. Sci. USA. 78:1014-1018.
40. Zimmermann, H., and C.R. Denston. 1977. Separation of synaptic vesicles of different functional states from the cholinergic synapses of the Torpedo electric organ. Neuroscience. 2:715-730.
41. Zimmermann, H., and V.P. Whittaker. 1977. Morphological and biochemical heterogeneity of cholinergic synaptic vesicles. Nature (Lond.). 267:633-635.