Abstract
SYNAPSIN I is a synaptic vesicle-associated phosphoprotein that is involved in the modulation of neurotransmitter release1. Ca2+/calmodulin-dependent protein kinase II, which phosphory-lates two sites in the carboxy-terminal region of synapsin I, causes synapsin I to dissociate from synaptic vesicles2 and increases nerotransmitter release3,4. Conversely, the dephosphorylated form of synapsin I, but not the form phosphorylated by Ca2+/cal-modulin-dependent protein kinase II, inhibits neurotransmitter release4–6. The amino-terminal region of synapsin I interacts with membrane phospholipids, whereas the C-terminal region binds to a protein component of synaptic vesicles7,8. Here we demonstrate that the binding of the C-terminal region of synapsin I involves the regulatory domain of a synaptic vesicle-associated form of Ca2+/calmodulin-dependent protein kinase II. Our results indicate that this form of the kinase functions both as a binding protein for synapsin I, and as an enzyme that phosphorylates synapsin I and promotes its dissociation from the vesicles.
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References
De Camilli, P., Benfenati, F., Valtorta, F. & Greengard, P. A. Rev. Cell Biol. 6, 433–460 (1990).
Schiebler, W., Jahn, R., Doucet, J.-P., Rothlein, J. & Greengard, P. J. biol. Chem. 261, 8383–8390 (1986).
Nichols, R. A., Sihra, T. S., Czernik, A. J., Nairn, A. C. & Greengard, P. Nature 343, 647–651 (1990).
Llinás, R., Gruner, J. A., Sugimori, M., McGuinness, T. & Greengard, P. J. Physiol., Lond. 436, 257–282 (1991).
Nichols, R. A., Chilcote, T. J., Czernik, A. J. & Greengard, P. J. Neurochem. 58, 783–785 (1992).
Hackett, J. T., Cochran, S. L., Greenfield, L. J., Brosius, D. C. & Ueda, T. J. Neurophysiol. 63, 701–706 (1990).
Benfenati, F., Bähler, M., Jahn, R. & Greengard, P. J. Cell Biol. 108, 1863–1872 (1989).
Benfenati, F., Greengard, P., Brunner, J. & Bähler, M. J. Cell Biol. 108, 1851–1862 (1989).
Ji, T. H. & Ji, I. Analyt. Biochem. 121, 286–289 (1982).
Bulleit, R. F., Bennett, M. K., Molfoy, S. S., Hurley, J. B. & Kennedy, M. B. Neuron 1, 63–72 (1988).
Tobimatsu, T. & Fujisawa, H. J. biol. Chem. 264, 17907–17912 (1989).
McGuinness, T. L., Lai, Y., Greengard, P., Woodgett, J. R. & Cohen P. FEBS Lett. 163, 329–334 (1983).
Schulman H. & Lou, L. L. Trends biochem. Sci. 14, 62–66 (1989).
Colbran, R. J. et al. Biochem J. 258, 313–325 (1989).
Kennedy, M. B., Bennett, M. K. & Erondu, N. E. Proc. natn. Acad. Sci. U.S.A. 80, 7357–7361 (1983).
Kelly, P. T., McGuinness, T. L. & Greengard, P. Proc. natn. Acad. Sci. U.S.A. 81, 945–949 (1984).
Wu, K., Huang, Y., Adler, J. & Black, I. B. Proc. natn. Acad. Sci. U.S.A. 89, 3015–3019 (1992).
McGuinness, T. L., Lai, Y. & Greengard, P. J. biol. Chem. 260, 1696–1704 (1985).
Bähler, M., Benfenati, F., Valtorta, F., Czernik, A. J. & Greengard, P. J. Cell Biol. 108, 1841–1849 (1989).
Markwell, M. A. K. Analyt. Biochem. 125, 427–432 (1982).
Huttner, W. B., Schiebler, W., Greengard, P. & De Camilli, P. J. Cell Biol. 96, 1374–1388 (1983).
Laemmli, U. K. Nature 227, 680–685 (1970).
Imada, M. & Sueoka, N. Biochim. biophys. Acta 625, 179–192 (1980).
Goelz, S. E., Nestler, E. J., Chehrazi, B. & Greengard, P. Proc. natn. Acad. Sci. U.S.A. 78, 2130–2134 (1981).
Jahn, R., Schiebler, W. & Greengard, P. Proc. natn. Acad. Sci. U.S.A. 81, 1684–1687 (1984).
De Lean, A., Munson, P. J. & Rodbard, D. Am. J. Physiol. 235, E97–E102 (1978).
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Benfenati, F., Valtorta, F., Rubenstein, J. et al. Synaptic vesicle-associated Ca2+/calmodulin-dependent protein kinase II is a binding protein for synapsin I. Nature 359, 417–420 (1992). https://doi.org/10.1038/359417a0
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DOI: https://doi.org/10.1038/359417a0
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