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Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1990 Nov;87(21):8257–8261. doi: 10.1073/pnas.87.21.8257

Effects of synapsin I and calcium/calmodulin-dependent protein kinase II on spontaneous neurotransmitter release in the squid giant synapse.

J W Lin 1, M Sugimori 1, R R Llinás 1, T L McGuinness 1, P Greengard 1
PMCID: PMC54934  PMID: 1978321

Abstract

The molecular events that control synaptic vesicle availability in chemical synaptic junctions have not been fully clarified. Among the protein molecules specifically located in presynaptic terminals, synapsin I and calcium/calmodulin-dependent protein kinase II (CaM kinase II) have been shown to modulate evoked transmitter release in the squid giant synapse. In the present study, analysis of synaptic noise in this chemical junction was used to determine whether these proteins also play a role in the control of spontaneous and enhanced spontaneous transmitter release. Injections of dephosphorylated synapsin I into the presynaptic terminal reduced the rate of spontaneous and enhanced quantal release, whereas injection of phosphorylated synapsin I did not modify such release. By contrast CaM kinase II injection increased enhanced miniature release without affecting spontaneous miniature frequency. These results support the view that dephosphorylated synapsin I "cages" synaptic vesicles while CaM kinase II, by phosphorylating synapsin I, "decages" these organelles and increases their availability for release without affecting the release mechanism itself.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Augustine G. J., Eckert R. Divalent cations differentially support transmitter release at the squid giant synapse. J Physiol. 1984 Jan;346:257–271. doi: 10.1113/jphysiol.1984.sp015020. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bähler M., Greengard P. Synapsin I bundles F-actin in a phosphorylation-dependent manner. Nature. 1987 Apr 16;326(6114):704–707. doi: 10.1038/326704a0. [DOI] [PubMed] [Google Scholar]
  3. De Camilli P., Cameron R., Greengard P. 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. 1983 May;96(5):1337–1354. doi: 10.1083/jcb.96.5.1337. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. De Camilli P., Greengard P. Synapsin I: a synaptic vesicle-associated neuronal phosphoprotein. Biochem Pharmacol. 1986 Dec 15;35(24):4349–4357. doi: 10.1016/0006-2952(86)90747-1. [DOI] [PubMed] [Google Scholar]
  5. FATT P., KATZ B. Spontaneous subthreshold activity at motor nerve endings. J Physiol. 1952 May;117(1):109–128. [PMC free article] [PubMed] [Google Scholar]
  6. Greengard P., Browning M. D., McGuinness T. L., Llinas R. Synapsin I, a phosphoprotein associated with synaptic vesicles: possible role in regulation of neurotransmitter release. Adv Exp Med Biol. 1987;221:135–153. doi: 10.1007/978-1-4684-7618-7_11. [DOI] [PubMed] [Google Scholar]
  7. Hackett J. T., Cochran S. L., Greenfield L. J., Jr, Brosius D. C., Ueda T. Synapsin I injected presynaptically into goldfish mauthner axons reduces quantal synaptic transmission. J Neurophysiol. 1990 Apr;63(4):701–706. doi: 10.1152/jn.1990.63.4.701. [DOI] [PubMed] [Google Scholar]
  8. Huttner W. B., Schiebler W., Greengard P., De Camilli P. 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. 1983 May;96(5):1374–1388. doi: 10.1083/jcb.96.5.1374. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Llinás R., McGuinness T. L., Leonard C. S., Sugimori M., Greengard P. Intraterminal injection of synapsin I or calcium/calmodulin-dependent protein kinase II alters neurotransmitter release at the squid giant synapse. Proc Natl Acad Sci U S A. 1985 May;82(9):3035–3039. doi: 10.1073/pnas.82.9.3035. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Llinás R., Steinberg I. Z., Walton K. Presynaptic calcium currents in squid giant synapse. Biophys J. 1981 Mar;33(3):289–321. doi: 10.1016/S0006-3495(81)84898-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Mann D. W., Joyner R. W. Miniature synaptic potentials at the squid giant synapse. J Neurobiol. 1978 Jul;9(4):329–335. doi: 10.1002/neu.480090410. [DOI] [PubMed] [Google Scholar]
  12. McGuinness T. L., Brady S. T., Gruner J. A., Sugimori M., Llinas R., Greengard P. Phosphorylation-dependent inhibition by synapsin I of organelle movement in squid axoplasm. J Neurosci. 1989 Dec;9(12):4138–4149. doi: 10.1523/JNEUROSCI.09-12-04138.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. McGuinness T. L., Lai Y., Greengard P. Ca2+/calmodulin-dependent protein kinase II. Isozymic forms from rat forebrain and cerebellum. J Biol Chem. 1985 Feb 10;260(3):1696–1704. [PubMed] [Google Scholar]
  14. Miledi R. Spontaneous synaptic potentials and quantal release of transmitter in the stellate ganglion of the squid. J Physiol. 1967 Sep;192(2):379–406. doi: 10.1113/jphysiol.1967.sp008306. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Verveen A. A., DeFelice L. J. Membrane noise. Prog Biophys Mol Biol. 1974;28:189–265. doi: 10.1016/0079-6107(74)90019-4. [DOI] [PubMed] [Google Scholar]

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