Redistribution of Synapsin I and Synaptophysin in Response to Electrical Stimulation in the Rat Neurohypophysial Nerve Endings
To understand the dynamics of synaptic vesicles and synapsin I, we have studied the localization of synapsin I and synaptophysin in resting and stimulated nerve endings by ultracryomicrotomy and colloidal gold-immunocytochemistry. First, we characterized microvesicles in resting nerve endings of the...
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| Published in: | Cell Structure and Function Vol. 19; no. 4; pp. 253 - 262 |
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| Abstract | To understand the dynamics of synaptic vesicles and synapsin I, we have studied the localization of synapsin I and synaptophysin in resting and stimulated nerve endings by ultracryomicrotomy and colloidal gold-immunocytochemistry. First, we characterized microvesicles in resting nerve endings of the rat neurohypophysis, which was chosen as the model of nerve ending in this study. Synaptophysin was localized in microvesicles that were clustered beneath the plasma membrane. Quick-freeze deep-etching electron microscopy showed that short strands cross-linked microvesicles to each other, which highly resembly the structures observed in our studies of the presynaptic nerve terminals of central and peripheral nervous system and in vitro reconstitution of synapsin I and synaptic vesicles. Immunocytochemistry showed that synapsin I was localized to the region of cluster of microvesicles. Second, using this system, we examined localization of synapsin I and synaptophysin in nerve endings after electrical stimulation. Besides release of neurosecretory granules, clusters of microvesicles disappeared and both microvesicles and synaptophysin were scattered over nerve endings. These changes were also confirmed by quick-freeze, freeze-substitution. Immunocytochemistry of the stimulated sample revealed that synapsin I was also scattered. The results show that microvesicles in neurohypophysis have similar characteristics of typical synaptic vesicles and synapsin I has a role as a scaffold to cross-link microvesicles to be clustered in resting nerve endings. This scaffold of synapsin I was disengaged after stimulation to redistribute microvesicles and synapsin I itself, which may be the mechanism of synapsin I to regulate the availability of synaptic vesicles for release. |
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| AbstractList | To understand the dynamics of synaptic vesicles and synapsin I, we have studied the localization of synapsin I and synaptophysin in resting and stimulated nerve endings by ultracryomicrotomy and colloidal gold-immunocytochemistry. First, we characterized microvesicles in resting nerve endings of the rat neurohypophysis, which was chosen as the model of nerve ending in this study. Synaptophysin was localized in microvesicles that were clustered beneath the plasma membrane. Quick-freeze deep-etching electron microscopy showed that short strands cross-linked microvesicles to each other, which highly resembly the structures observed in our studies of the presynaptic nerve terminals of central and peripheral nervous system and in vitro reconstitution of synapsin I and synaptic vesicles. Immunocytochemistry showed that synapsin I was localized to the region of cluster of microvesicles. Second, using this system, we examined localization of synapsin I and synaptophysin in nerve endings after electrical stimulation. Besides release of neurosecretory granules, clusters of microvesicles disappeared and both microvesicles and synaptophysin were scattered over nerve endings. These changes were also confirmed by quick-freeze, freeze-substitution. Immunocytochemistry of the stimulated sample revealed that synapsin I was also scattered. The results show that microvesicles in neurohypophysis have similar characteristics of typical synaptic vesicles and synapsin I has a role as a scaffold to cross-link microvesicles to be clustered in resting nerve endings. This scaffold of synapsin I was disengaged after stimulation to redistribute microvesicles and synapsin I itself, which may be the mechanism of synapsin I to regulate the availability of synaptic vesicles for release. To understand the dynamics of synaptic vesicles and synapsin I, we have studied the localization of synapsin I and synaptophysin in resting and stimulated nerve endings by ultracryomicrotomy and colloidal gold-immunocytochemistry. First, we characterized microvesicles in resting nerve endings of the rat neurohypophysis, which was chosen as the model of nerve ending in this study. Synaptophysin was localized in microvesicles that were clustered beneath the plasma membrane. Quick-freeze deep-etching electron microscopy showed that short strands cross-linked microvesicles to each other, which highly resemble the structures observed in our studies of the presynaptic nerve terminals of central and peripheral nervous system and in vitro reconstitution of synapsin I and synaptic vesicles. Immunocytochemistry showed that synapsin I was localized to the region of cluster of microvesicles. Second, using this system, we examined localization of synapsin I and synaptophysin in nerve endings after electrical stimulation. Besides release of neurosecretory granules, clusters of microvesicles dissappeared and both microvesicles and synaptophysin were scattered over nerve endings. These changes were also confirmed by quick-freeze, freeze-substitution. Immunocytochemistry of the stimulated sample revealed that synapsin I was also scattered. The results show that microvesicles in neurohypophysis have similar characteristics of typical synaptic vesicles and synapsin I has a role as a scaffold to cross-link microvesicles to be clustered in resting nerve endings. This scaffold of synapsin I was disengaged after stimulation to redistribute microvesicles and synapsin I itself, which may be the mechanism of synapsin I to regulate the availability of synaptic vesicles for release. |
| Author | Hayashi, Toshihiro Soulie, Frederic Nakata, Takao Hirokawa, Nobutaka |
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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. HIROKAWA, N., SOBUE, K., KANDA, K., HARADA, A., and YORIFUJI, H. 1989. The cytoskeletal architecture of the presynaptic terminal and molecular structure of synapsin I. J. Cell Biol., 108 : 111-126. 26. NICHOLS, R. A., CHILCOTE, T. J., CZERNIK, A. J., and GREENGARD, P. 1992. Synapsin I regulates glutamate release from rat brain synaptosomes. J. Neurochem., 58 : 783-785. 25. NAVONE, F., DI GIOLA, G., HAHN, R., BROWNING, M., GREENGARD, P., and DE CAMILLI, P. 1989. Microvesicles of the neurohypophysis are biochemically related to small synaptic vesicles of presynaptic nerve terminals. J. Cell Biol., 109 : 3425-3432. 29. OKABE, T. and SOBUE, K. 1987. Identification of a new 84/82 kDa calmodulin-binding protein, which also interacts with actin filaments, tubulin and spectrin, as synapsin I. Febs Lett, 213 : 184-188. 3. CAMERON, P. L., SÜDHOF, T.C., JAHN, R., and DE CAMILLI, P. 1991. Colocalization of synaptophysin with transferrin receptors : implications for synaptic vesicle biogenesis. J. Cell Biol., 115 : 151-164. 27. OBATA, K., NISHIYE, H., FUJITA, S. C., SHIRAO, T., INOUE, H., and UCHIZONO, K. 1986. Identification of a synaptic vesicle-specific 38,000-dalton protein by monoclonal antibodies. Brain Res., 375 : 37-48. 28. OBATA, K., KOJIMA, N., NISHIYE, H., INOUE, H., SHIRAO, T., FUJITA, S. C., and UCHIZONO, K. 1987. Four synaptic vesicle-specific proteins : identification by monoclonal antibodies and distribution in the nervous tissue and the adrenal medulla. Brain Res, 404 : 169-179. 37. TORRI-TARELLI, F., VILLA, A., VALTORTA, F., DE CAMILLI, P., GREENGARD, P., and CECCARELLI, B. 1990. Redistribution of synaptophysin and synapsin I during alphalatrotoxin-induced release of neurotransmitter at the neuromuscular junction. J. Cell Biol., 110 : 449-459. 20. LINSTEDT, A. D. and KELLY, R. B. 1991. Synaptophysin is sorted from endocytotic markers in neuroendocrine PC12 cells but not transfected fibroblasts. Neuron, 7 : 309-317. 31. REETZ, A., SOLIMENA, M., MATTEOLI, M., FOLLI, F., TAKEI, K., and DE CAMILLI, P. 1991. GABA and pancreatic β-cell : colo-calization of glutamic acid decarboxylase (GAD) and GABA with synaptic-like microvesicles suggests their role in GABA storage and secretion. EMBO J., 10 : 1275-1284. 16. JAHN, R., SCHIEBLER, W., OUIMET, C., and GREENGARD, P. 1985. A 38,000-dalton membrane protein (p38) present in synaptic vesicles. Proc. Natl. Acad. Sci. USA, 82 : 4137-4141. 4. CLIFT-O'GRADY, L., LINSTEDT, A. D., LOWE, A. W., GROTE, E., and KELLY, R. B. 1990. Biogenesis of synaptic vesicle-like structures in a pheochromocytoma cell line PC-12. J. Cell Biol., 110 : 1693-1703. 19. LIN, J. W., SUGIMORI, M., LLINÁS, R. R., MCGUINNESS, T. L., and GREENGARD, P. 1990. Effects of synapsin I and calcium/calmodulin-dependent protein kinase II on spontaneous neurotransmitter release in the squid giant synapse. Proc. Natl. Acad. Sci. USA, 87 : 8257-8261. 35. TOKUYASU, K. T. 1980. Immunochemistry on ultrathin frozen sections. Histochem. J., 12 : 381-403. 12. HIROKAWA, N. and KIRINO, T. 1980. An ultrastructural study of nerve and glia cells by freeze-substitution J. Neurocytol., 9 : 243-254. 13. HIROKAWA, N. and HEUSER, J. E. 1981. Quick-freeze, deep-etch visualization of the cytoskeleton beneath surface differentiation of epithelial cells. J. Cell Biol., 91 : 339-409. 30. PETRUCCI, T. C. and MORROW, J. S. 1987. Synapsin I : an actin-bundling protein under phosphorylation control. J. Cell Biol., 105 : 1355-1363. 7. DE CAMILLI, P., BENFENATI, F., VALTORTA, F., and GREENGARD, P. 1990. The synapsins. Annu. Rev. Cell Biol., 6 : 433-460. 23. MORRIS, J. F. and NORDMAMM, J. J. 1980. Membrane recapture after hormone release from nerve endings in the neural lobe of the rat pituitary gland. Neurosci., 5 : 639-649. 32. SCHIEBLER, W., JAHN, R., DOUCET, J. P., ROTHLEIN, J., and GREENGARD, P. 1986. Characterization of synapsin I binding to small synaptic vesicles. J. Biol. Chem., 261 : 8383-8390. 9. HARADA, A., SOBUE, K., and HIROKAWA, N. 1990. Developmental changes of synapsin I subcellular localization in rat cerebellar neurons. Cell Struct. Funct., 15 : 329-342. 10. HEUSER, J. E. and SALPETER, S. R. 1979. Organization of acetylcholine receptors in quick-frozen, deep-etched and rotary replicated Torpedo postsynaptic membrane. J. Cell Biol., 82 : 150-173. 8. DOUGLAS, W. W., NAGASAWA, J., and SCHULZ, R. 1970. Electron microscopic studies on the mechanism of secretion of posterior pituitary hormones and significance of microvesicles ("synaptic vesicles") : evidence of secretion by exocytosis and formation of microvesicles and a by-product of this process. Mem. Soc. Endocrinol., 19 : 353-377. 18. LANDIS, D. M., HALL, A. K., WEINSTEIN, L. A., and REESE, T. S. 1988. The organization of cytoplasm at the presynaptic active zone of a central nervous system synapse. Neuron, 1 : 201-209. 1. BÃHLER, M. and GREENGARD, P. 1987. Synapsin I bundles Factin in a phosphorylation-dependent manner. Nature, 326 : 704-707. 36. TOKUYASU, K. T. 1989. Use of poly(vinylpyrrolidone) and poly(vinyl alcohol) for cryoultramicrotomy. Histochem. J., 21 : 163-171. 33. SHIBUKI, K. 1990. Activation of neurohypophysial vasopressin release by Ca2+ influx and intracellular Ca2+ accumulation in the rat. J. Physiol. (Lond), 422 : 321-331. 5. DE CAMILLI, P., CAMERON, R., and GREENGARD, P. 1983. Synapsin I (protein I), a nerve terminal-specific phosphoprotein. I. Its general distribution in synapses of the central and peripheral nervous system demonstrated by immunofluorescence in frozen and plastic sections. J. Cell Biol., 96 : 1337-1354. 21. LLINÁS, R., MCGUINNESS, T. L., LEONARD, C. S., SUGIMORI, M., and GREENGARD, P. 1985. Intraterminal injection of synapsin I or calcium/calmodulin-dependent protein kinase 2 alters neurotransmitter release at the squid giant synapse. Proc. Natl. Acad. Sci. USA, 82 : 3035-3039. 22. LLINÁS, R., GRUNER, J. A., SUGIMORI, M., MCGUINNESS, T. L., and GREENGARD, P. 1991. Regulation by synapsin I and Ca2+- calmodulin-dependent protein kinase II of the transmitter release in squid giant synapse. J. Physiol. (Lond), 436 : 257-282. 15. HUTTNER, W. B., SCHIEBLER, W., GREENGARD, P., and DE CAMILLLI, P. 1983. Synapsin I (protein I), a nerve terminal-specific phosphoprotein. III. Its association with synaptic vesicles studied in a highly purified synaptic vesicle preparation. J. Cell Biol., 96 : 1374-1388. 24. NAGASAWA, J., DOUGLAS, W. W., and SCHULZ, R. A. 1971. Micropinocytotic origin of coated and smooth microvesicles ("synaptic vesicles") in neurosecretory terminals of posterior pituitary glands demonstrated by incorporation of horseradish peroxidase. Nature, 232 : 341-342. 34. SIRA, T. S., WANG, J. K. T., GORELICK, F. S., and GREENGARD, P. 1989. Translocation of synapsin I in response to depolarization of isolated nerve terminals. Proc. Natl. Acad. Sci. USA, 86 : 8108-8112. |
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| SubjectTerms | Animals Electric Stimulation exocytosis Immunohistochemistry Male Microscopy, Electron Nerve Endings - metabolism Nerve Endings - ultrastructure neurohypophysis Pituitary Gland, Posterior - innervation Rats Rats, Wistar synapses synapsin I Synapsins - analysis Synaptic Vesicles - metabolism Synaptic Vesicles - ultrastructure synaptophysin Synaptophysin - analysis |
| Title | Redistribution of Synapsin I and Synaptophysin in Response to Electrical Stimulation in the Rat Neurohypophysial Nerve Endings |
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