Skip to main content
Philosophical Transactions of the Royal Society B: Biological Sciences logoLink to Philosophical Transactions of the Royal Society B: Biological Sciences
. 1999 Feb 28;354(1381):269–279. doi: 10.1098/rstb.1999.0378

Synapsins as regulators of neurotransmitter release.

S Hilfiker 1, V A Pieribone 1, A J Czernik 1, H T Kao 1, G J Augustine 1, P Greengard 1
PMCID: PMC1692497  PMID: 10212475

Abstract

One of the crucial issues in understanding neuronal transmission is to define the role(s) of the numerous proteins that are localized within presynaptic terminals and are thought to participate in the regulation of the synaptic vesicle life cycle. Synapsins are a multigene family of neuron-specific phosphoproteins and are the most abundant proteins on synaptic vesicles. Synapsins are able to interact in vitro with lipid and protein components of synaptic vesicles and with various cytoskeletal proteins, including actin. These and other studies have led to a model in which synapsins, by tethering synaptic vesicles to each other and to an actin-based cytoskeletal meshwork, maintain a reserve pool of vesicles in the vicinity of the active zone. Perturbation of synapsin function in a variety of preparations led to a selective disruption of this reserve pool and to an increase in synaptic depression, suggesting that the synapsin-dependent cluster of vesicles is required to sustain release of neurotransmitter in response to high levels of neuronal activity. In a recent study performed at the squid giant synapse, perturbation of synapsin function resulted in a selective disruption of the reserve pool of vesicles and in addition, led to an inhibition and slowing of the kinetics of neurotransmitter release, indicating a second role for synapsins downstream from vesicle docking. These data suggest that synapsins are involved in two distinct reactions which are crucial for exocytosis in presynaptic nerve terminals. This review describes our current understanding of the molecular mechanisms by which synapsins modulate synaptic transmission, while the increasingly well-documented role of the synapsins in synapse formation and stabilization lies beyond the scope of this review.

Full Text

The Full Text of this article is available as a PDF (247.7 KB).

Selected References

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

  1. Augustine G. J., Burns M. E., DeBello W. M., Pettit D. L., Schweizer F. E. Exocytosis: proteins and perturbations. Annu Rev Pharmacol Toxicol. 1996;36:659–701. doi: 10.1146/annurev.pa.36.040196.003303. [DOI] [PubMed] [Google Scholar]
  2. Baines A. J., Bennett V. Synapsin I is a microtubule-bundling protein. Nature. 1986 Jan 9;319(6049):145–147. doi: 10.1038/319145a0. [DOI] [PubMed] [Google Scholar]
  3. Baines A. J., Bennett V. Synapsin I is a spectrin-binding protein immunologically related to erythrocyte protein 4.1. 1985 May 30-Jun 5Nature. 315(6018):410–413. doi: 10.1038/315410a0. [DOI] [PubMed] [Google Scholar]
  4. Benfenati F., Bähler M., Jahn R., Greengard P. Interactions of synapsin I with small synaptic vesicles: distinct sites in synapsin I bind to vesicle phospholipids and vesicle proteins. J Cell Biol. 1989 May;108(5):1863–1872. doi: 10.1083/jcb.108.5.1863. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Benfenati F., Greengard P., Brunner J., Bähler M. Electrostatic and hydrophobic interactions of synapsin I and synapsin I fragments with phospholipid bilayers. J Cell Biol. 1989 May;108(5):1851–1862. doi: 10.1083/jcb.108.5.1851. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Benfenati F., Neyroz P., Bähler M., Masotti L., Greengard P. Time-resolved fluorescence study of the neuron-specific phosphoprotein synapsin I. Evidence for phosphorylation-dependent conformational changes. J Biol Chem. 1990 Jul 25;265(21):12584–12595. [PubMed] [Google Scholar]
  7. Benfenati F., Valtorta F., Chieregatti E., Greengard P. Interaction of free and synaptic vesicle-bound synapsin I with F-actin. Neuron. 1992 Feb;8(2):377–386. doi: 10.1016/0896-6273(92)90303-u. [DOI] [PubMed] [Google Scholar]
  8. Benfenati F., Valtorta F., Rossi M. C., Onofri F., Sihra T., Greengard P. Interactions of synapsin I with phospholipids: possible role in synaptic vesicle clustering and in the maintenance of bilayer structures. J Cell Biol. 1993 Dec;123(6 Pt 2):1845–1855. doi: 10.1083/jcb.123.6.1845. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Benfenati F., Valtorta F., Rubenstein J. L., Gorelick F. S., Greengard P., Czernik A. J. Synaptic vesicle-associated Ca2+/calmodulin-dependent protein kinase II is a binding protein for synapsin I. Nature. 1992 Oct 1;359(6394):417–420. doi: 10.1038/359417a0. [DOI] [PubMed] [Google Scholar]
  10. Bommert K., Charlton M. P., DeBello W. M., Chin G. J., Betz H., Augustine G. J. Inhibition of neurotransmitter release by C2-domain peptides implicates synaptotagmin in exocytosis. Nature. 1993 May 13;363(6425):163–165. doi: 10.1038/363163a0. [DOI] [PubMed] [Google Scholar]
  11. Brodin L., Löw P., Gad H., Gustafsson J., Pieribone V. A., Shupliakov O. Sustained neurotransmitter release: new molecular clues. Eur J Neurosci. 1997 Dec;9(12):2503–2511. doi: 10.1111/j.1460-9568.1997.tb01679.x. [DOI] [PubMed] [Google Scholar]
  12. Burns M. E., Sasaki T., Takai Y., Augustine G. J. Rabphilin-3A: a multifunctional regulator of synaptic vesicle traffic. J Gen Physiol. 1998 Feb;111(2):243–255. doi: 10.1085/jgp.111.2.243. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Bähler M., Benfenati F., Valtorta F., Czernik A. J., Greengard P. Characterization of synapsin I fragments produced by cysteine-specific cleavage: a study of their interactions with F-actin. J Cell Biol. 1989 May;108(5):1841–1849. doi: 10.1083/jcb.108.5.1841. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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]
  15. Ceccarelli B., Hurlbut W. P., Mauro A. Depletion of vesicles from frog neuromuscular junctions by prolonged tetanic stimulation. J Cell Biol. 1972 Jul;54(1):30–38. doi: 10.1083/jcb.54.1.30. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Ceccarelli B., Hurlbut W. P. Vesicle hypothesis of the release of quanta of acetylcholine. Physiol Rev. 1980 Apr;60(2):396–441. doi: 10.1152/physrev.1980.60.2.396. [DOI] [PubMed] [Google Scholar]
  17. Czernik A. J., Pang D. T., Greengard P. Amino acid sequences surrounding the cAMP-dependent and calcium/calmodulin-dependent phosphorylation sites in rat and bovine synapsin I. Proc Natl Acad Sci U S A. 1987 Nov;84(21):7518–7522. doi: 10.1073/pnas.84.21.7518. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. DEL CASTILLO J., KATZ B. Quantal components of the end-plate potential. J Physiol. 1954 Jun 28;124(3):560–573. doi: 10.1113/jphysiol.1954.sp005129. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. De Camilli P., Benfenati F., Valtorta F., Greengard P. The synapsins. Annu Rev Cell Biol. 1990;6:433–460. doi: 10.1146/annurev.cb.06.110190.002245. [DOI] [PubMed] [Google Scholar]
  20. De Camilli P., Harris S. M., Jr, Huttner W. B., Greengard P. 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. 1983 May;96(5):1355–1373. doi: 10.1083/jcb.96.5.1355. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. DeBello W. M., O'Connor V., Dresbach T., Whiteheart S. W., Wang S. S., Schweizer F. E., Betz H., Rothman J. E., Augustine G. J. SNAP-mediated protein-protein interactions essential for neurotransmitter release. Nature. 1995 Feb 16;373(6515):626–630. doi: 10.1038/373626a0. [DOI] [PubMed] [Google Scholar]
  22. Diamond J. S., Jahr C. E. Asynchronous release of synaptic vesicles determines the time course of the AMPA receptor-mediated EPSC. Neuron. 1995 Nov;15(5):1097–1107. doi: 10.1016/0896-6273(95)90098-5. [DOI] [PubMed] [Google Scholar]
  23. Dresbach T., Burns M. E., O'Connor V., DeBello W. M., Betz H., Augustine G. J. A neuronal Sec1 homolog regulates neurotransmitter release at the squid giant synapse. J Neurosci. 1998 Apr 15;18(8):2923–2932. doi: 10.1523/JNEUROSCI.18-08-02923.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Esser L., Wang C. R., Hosaka M., Smagula C. S., Südhof T. C., Deisenhofer J. Synapsin I is structurally similar to ATP-utilizing enzymes. EMBO J. 1998 Feb 16;17(4):977–984. doi: 10.1093/emboj/17.4.977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Foster-Barber A., Bishop J. M. Src interacts with dynamin and synapsin in neuronal cells. Proc Natl Acad Sci U S A. 1998 Apr 14;95(8):4673–4677. doi: 10.1073/pnas.95.8.4673. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Goldenring J. R., Lasher R. S., Vallano M. L., Ueda T., Naito S., Sternberger N. H., Sternberger L. A., DeLorenzo R. J. Association of synapsin I with neuronal cytoskeleton. Identification in cytoskeletal preparations in vitro and immunocytochemical localization in brain of synapsin I. J Biol Chem. 1986 Jun 25;261(18):8495–8504. [PubMed] [Google Scholar]
  27. Gotow T., Miyaguchi K., Hashimoto P. H. Cytoplasmic architecture of the axon terminal: filamentous strands specifically associated with synaptic vesicles. Neuroscience. 1991;40(2):587–598. doi: 10.1016/0306-4522(91)90143-c. [DOI] [PubMed] [Google Scholar]
  28. Greengard P., Valtorta F., Czernik A. J., Benfenati F. Synaptic vesicle phosphoproteins and regulation of synaptic function. Science. 1993 Feb 5;259(5096):780–785. doi: 10.1126/science.8430330. [DOI] [PubMed] [Google Scholar]
  29. 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]
  30. Hanson P. I., Heuser J. E., Jahn R. Neurotransmitter release - four years of SNARE complexes. Curr Opin Neurobiol. 1997 Jun;7(3):310–315. doi: 10.1016/s0959-4388(97)80057-8. [DOI] [PubMed] [Google Scholar]
  31. Hay J. C., Scheller R. H. SNAREs and NSF in targeted membrane fusion. Curr Opin Cell Biol. 1997 Aug;9(4):505–512. doi: 10.1016/s0955-0674(97)80026-9. [DOI] [PubMed] [Google Scholar]
  32. Hess S. D., Doroshenko P. A., Augustine G. J. A functional role for GTP-binding proteins in synaptic vesicle cycling. Science. 1993 Feb 19;259(5098):1169–1172. doi: 10.1126/science.8438167. [DOI] [PubMed] [Google Scholar]
  33. Heuser J. E., Reese T. S. Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. J Cell Biol. 1973 May;57(2):315–344. doi: 10.1083/jcb.57.2.315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Hilfiker S., Schweizer F. E., Kao H. T., Czernik A. J., Greengard P., Augustine G. J. Two sites of action for synapsin domain E in regulating neurotransmitter release. Nat Neurosci. 1998 May;1(1):29–35. doi: 10.1038/229. [DOI] [PubMed] [Google Scholar]
  35. Hirokawa N., Sobue K., Kanda K., Harada A., Yorifuji H. The cytoskeletal architecture of the presynaptic terminal and molecular structure of synapsin 1. J Cell Biol. 1989 Jan;108(1):111–126. doi: 10.1083/jcb.108.1.111. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Ho M. F., Bähler M., Czernik A. J., Schiebler W., Kézdy F. J., Kaiser E. T., Greengard P. Synapsin I is a highly surface-active molecule. J Biol Chem. 1991 Mar 25;266(9):5600–5607. [PubMed] [Google Scholar]
  37. Hosaka M., Südhof T. C. Synapsin III, a novel synapsin with an unusual regulation by Ca2+. J Biol Chem. 1998 May 29;273(22):13371–13374. doi: 10.1074/jbc.273.22.13371. [DOI] [PubMed] [Google Scholar]
  38. Hosaka M., Südhof T. C. Synapsins I and II are ATP-binding proteins with differential Ca2+ regulation. J Biol Chem. 1998 Jan 16;273(3):1425–1429. doi: 10.1074/jbc.273.3.1425. [DOI] [PubMed] [Google Scholar]
  39. Hunt J. M., Bommert K., Charlton M. P., Kistner A., Habermann E., Augustine G. J., Betz H. A post-docking role for synaptobrevin in synaptic vesicle fusion. Neuron. 1994 Jun;12(6):1269–1279. doi: 10.1016/0896-6273(94)90443-x. [DOI] [PubMed] [Google Scholar]
  40. Huttner W. B., Greengard P. Multiple phosphorylation sites in protein I and their differential regulation by cyclic AMP and calcium. Proc Natl Acad Sci U S A. 1979 Oct;76(10):5402–5406. doi: 10.1073/pnas.76.10.5402. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. 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]
  42. Iga M., Inui M., Sobue K. Characterization of the interaction between synapsin I and calspectin (brain spectrin or fodrin). Biochem Biophys Res Commun. 1997 Feb 24;231(3):852–855. doi: 10.1006/bbrc.1997.6202. [DOI] [PubMed] [Google Scholar]
  43. Jovanovic J. N., Benfenati F., Siow Y. L., Sihra T. S., Sanghera J. S., Pelech S. L., Greengard P., Czernik A. J. Neurotrophins stimulate phosphorylation of synapsin I by MAP kinase and regulate synapsin I-actin interactions. Proc Natl Acad Sci U S A. 1996 Apr 16;93(8):3679–3683. doi: 10.1073/pnas.93.8.3679. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Kahn D. W., Besterman J. M. Cytosolic rat brain synapsin I is a diacylglycerol kinase. Proc Natl Acad Sci U S A. 1991 Jul 15;88(14):6137–6141. doi: 10.1073/pnas.88.14.6137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Kao H. T., Porton B., Czernik A. J., Feng J., Yiu G., Häring M., Benfenati F., Greengard P. A third member of the synapsin gene family. Proc Natl Acad Sci U S A. 1998 Apr 14;95(8):4667–4672. doi: 10.1073/pnas.95.8.4667. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Klagges B. R., Heimbeck G., Godenschwege T. A., Hofbauer A., Pflugfelder G. O., Reifegerste R., Reisch D., Schaupp M., Buchner S., Buchner E. Invertebrate synapsins: a single gene codes for several isoforms in Drosophila. J Neurosci. 1996 May 15;16(10):3154–3165. doi: 10.1523/JNEUROSCI.16-10-03154.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Landis D. M., Hall A. K., Weinstein L. A., Reese T. S. The organization of cytoplasm at the presynaptic active zone of a central nervous system synapse. Neuron. 1988 May;1(3):201–209. doi: 10.1016/0896-6273(88)90140-7. [DOI] [PubMed] [Google Scholar]
  48. Lin J. W., Sugimori M., Llinás R. R., McGuinness T. L., Greengard P. Effects of synapsin I and calcium/calmodulin-dependent protein kinase II on spontaneous neurotransmitter release in the squid giant synapse. Proc Natl Acad Sci U S A. 1990 Nov;87(21):8257–8261. doi: 10.1073/pnas.87.21.8257. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Llinás R., Gruner J. A., Sugimori M., McGuinness T. L., Greengard P. Regulation by synapsin I and Ca(2+)-calmodulin-dependent protein kinase II of the transmitter release in squid giant synapse. J Physiol. 1991 May;436:257–282. doi: 10.1113/jphysiol.1991.sp018549. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. 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]
  51. Mandell J. W., Czernik A. J., De Camilli P., Greengard P., Townes-Anderson E. Differential expression of synapsins I and II among rat retinal synapses. J Neurosci. 1992 May;12(5):1736–1749. doi: 10.1523/JNEUROSCI.12-05-01736.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Mandell J. W., Townes-Anderson E., Czernik A. J., Cameron R., Greengard P., De Camilli P. Synapsins in the vertebrate retina: absence from ribbon synapses and heterogeneous distribution among conventional synapses. Neuron. 1990 Jul;5(1):19–33. doi: 10.1016/0896-6273(90)90030-j. [DOI] [PubMed] [Google Scholar]
  53. Matsubara M., Kusubata M., Ishiguro K., Uchida T., Titani K., Taniguchi H. Site-specific phosphorylation of synapsin I by mitogen-activated protein kinase and Cdk5 and its effects on physiological functions. J Biol Chem. 1996 Aug 30;271(35):21108–21113. doi: 10.1074/jbc.271.35.21108. [DOI] [PubMed] [Google Scholar]
  54. Nichols B. J., Ungermann C., Pelham H. R., Wickner W. T., Haas A. Homotypic vacuolar fusion mediated by t- and v-SNAREs. Nature. 1997 May 8;387(6629):199–202. doi: 10.1038/387199a0. [DOI] [PubMed] [Google Scholar]
  55. Nichols R. A., Chilcote T. J., Czernik A. J., Greengard P. Synapsin I regulates glutamate release from rat brain synaptosomes. J Neurochem. 1992 Feb;58(2):783–785. doi: 10.1111/j.1471-4159.1992.tb09788.x. [DOI] [PubMed] [Google Scholar]
  56. O'Connor V., Heuss C., De Bello W. M., Dresbach T., Charlton M. P., Hunt J. H., Pellegrini L. L., Hodel A., Burger M. M., Betz H. Disruption of syntaxin-mediated protein interactions blocks neurotransmitter secretion. Proc Natl Acad Sci U S A. 1997 Oct 28;94(22):12186–12191. doi: 10.1073/pnas.94.22.12186. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Onofri F., Giovedì S., Vaccaro P., Czernik A. J., Valtorta F., De Camilli P., Greengard P., Benfenati F. Synapsin I interacts with c-Src and stimulates its tyrosine kinase activity. Proc Natl Acad Sci U S A. 1997 Oct 28;94(22):12168–12173. doi: 10.1073/pnas.94.22.12168. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Petrucci T. C., Morrow J. S. Synapsin I: an actin-bundling protein under phosphorylation control. J Cell Biol. 1987 Sep;105(3):1355–1363. doi: 10.1083/jcb.105.3.1355. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Pieribone V. A., Shupliakov O., Brodin L., Hilfiker-Rothenfluh S., Czernik A. J., Greengard P. Distinct pools of synaptic vesicles in neurotransmitter release. Nature. 1995 Jun 8;375(6531):493–497. doi: 10.1038/375493a0. [DOI] [PubMed] [Google Scholar]
  60. Romano C., Nichols R. A., Greengard P., Greene L. A. Synapsin I in PC12 cells. I. Characterization of the phosphoprotein and effect of chronic NGF treatment. J Neurosci. 1987 May;7(5):1294–1299. doi: 10.1523/JNEUROSCI.07-05-01294.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Romano C., Nichols R. A., Greengard P. Synapsin I in PC12 cells. II. Evidence for regulation by NGF of phosphorylation at a novel site. J Neurosci. 1987 May;7(5):1300–1306. doi: 10.1523/JNEUROSCI.07-05-01300.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Rosahl T. W., Geppert M., Spillane D., Herz J., Hammer R. E., Malenka R. C., Südhof T. C. Short-term synaptic plasticity is altered in mice lacking synapsin I. Cell. 1993 Nov 19;75(4):661–670. doi: 10.1016/0092-8674(93)90487-b. [DOI] [PubMed] [Google Scholar]
  63. Rosahl T. W., Spillane D., Missler M., Herz J., Selig D. K., Wolff J. R., Hammer R. E., Malenka R. C., Südhof T. C. Essential functions of synapsins I and II in synaptic vesicle regulation. Nature. 1995 Jun 8;375(6531):488–493. doi: 10.1038/375488a0. [DOI] [PubMed] [Google Scholar]
  64. Rothman J. E. Mechanisms of intracellular protein transport. Nature. 1994 Nov 3;372(6501):55–63. doi: 10.1038/372055a0. [DOI] [PubMed] [Google Scholar]
  65. Ryan T. A., Li L., Chin L. S., Greengard P., Smith S. J. Synaptic vesicle recycling in synapsin I knock-out mice. J Cell Biol. 1996 Sep;134(5):1219–1227. doi: 10.1083/jcb.134.5.1219. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Schiebler W., Jahn R., Doucet J. P., Rothlein J., Greengard P. Characterization of synapsin I binding to small synaptic vesicles. J Biol Chem. 1986 Jun 25;261(18):8383–8390. [PubMed] [Google Scholar]
  67. Schweizer F. E., Dresbach T., DeBello W. M., O'Connor V., Augustine G. J., Betz H. Regulation of neurotransmitter release kinetics by NSF. Science. 1998 Feb 20;279(5354):1203–1206. doi: 10.1126/science.279.5354.1203. [DOI] [PubMed] [Google Scholar]
  68. Shupliakov O., Löw P., Grabs D., Gad H., Chen H., David C., Takei K., De Camilli P., Brodin L. Synaptic vesicle endocytosis impaired by disruption of dynamin-SH3 domain interactions. Science. 1997 Apr 11;276(5310):259–263. doi: 10.1126/science.276.5310.259. [DOI] [PubMed] [Google Scholar]
  69. Sihra T. S., Wang J. K., Gorelick F. S., Greengard P. Translocation of synapsin I in response to depolarization of isolated nerve terminals. Proc Natl Acad Sci U S A. 1989 Oct;86(20):8108–8112. doi: 10.1073/pnas.86.20.8108. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Stone L. M., Browning M. D., Finger T. E. Differential distribution of the synapsins in the rat olfactory bulb. J Neurosci. 1994 Jan;14(1):301–309. doi: 10.1523/JNEUROSCI.14-01-00301.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Söllner T., Bennett M. K., Whiteheart S. W., Scheller R. H., Rothman J. E. A protein assembly-disassembly pathway in vitro that may correspond to sequential steps of synaptic vesicle docking, activation, and fusion. Cell. 1993 Nov 5;75(3):409–418. doi: 10.1016/0092-8674(93)90376-2. [DOI] [PubMed] [Google Scholar]
  72. Söllner T., Whiteheart S. W., Brunner M., Erdjument-Bromage H., Geromanos S., Tempst P., Rothman J. E. SNAP receptors implicated in vesicle targeting and fusion. Nature. 1993 Mar 25;362(6418):318–324. doi: 10.1038/362318a0. [DOI] [PubMed] [Google Scholar]
  73. Südhof T. C. The synaptic vesicle cycle: a cascade of protein-protein interactions. Nature. 1995 Jun 22;375(6533):645–653. doi: 10.1038/375645a0. [DOI] [PubMed] [Google Scholar]
  74. Takei K., Mundigl O., Daniell L., De Camilli P. The synaptic vesicle cycle: a single vesicle budding step involving clathrin and dynamin. J Cell Biol. 1996 Jun;133(6):1237–1250. doi: 10.1083/jcb.133.6.1237. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Takei Y., Harada A., Takeda S., Kobayashi K., Terada S., Noda T., Takahashi T., Hirokawa N. Synapsin I deficiency results in the structural change in the presynaptic terminals in the murine nervous system. J Cell Biol. 1995 Dec;131(6 Pt 2):1789–1800. doi: 10.1083/jcb.131.6.1789. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Torri Tarelli F., Bossi M., Fesce R., Greengard P., Valtorta F. Synapsin I partially dissociates from synaptic vesicles during exocytosis induced by electrical stimulation. Neuron. 1992 Dec;9(6):1143–1153. doi: 10.1016/0896-6273(92)90072-l. [DOI] [PubMed] [Google Scholar]
  77. Torri-Tarelli F., Villa A., Valtorta F., De Camilli P., Greengard P., Ceccarelli B. Redistribution of synaptophysin and synapsin I during alpha-latrotoxin-induced release of neurotransmitter at the neuromuscular junction. J Cell Biol. 1990 Feb;110(2):449–459. doi: 10.1083/jcb.110.2.449. [DOI] [PMC free article] [PubMed] [Google Scholar]
  78. Ueda T., Greengard P. Adenosine 3':5'-monophosphate-regulated phosphoprotein system of neuronal membranes. I. Solubilization, purification, and some properties of an endogenous phosphoprotein. J Biol Chem. 1977 Jul 25;252(14):5155–5163. [PubMed] [Google Scholar]
  79. Usukura J., Yamada E. Ultrastructure of the synaptic ribbons in photoreceptor cells of Rana catesbeiana revealed by freeze-etching and freeze-substitution. Cell Tissue Res. 1987 Mar;247(3):483–488. doi: 10.1007/BF00215740. [DOI] [PubMed] [Google Scholar]
  80. Valtorta F., Greengard P., Fesce R., Chieregatti E., Benfenati F. Effects of the neuronal phosphoprotein synapsin I on actin polymerization. I. Evidence for a phosphorylation-dependent nucleating effect. J Biol Chem. 1992 Jun 5;267(16):11281–11288. [PubMed] [Google Scholar]
  81. Valtorta F., Villa A., Jahn R., De Camilli P., Greengard P., Ceccarelli B. Localization of synapsin I at the frog neuromuscular junction. Neuroscience. 1988 Feb;24(2):593–603. doi: 10.1016/0306-4522(88)90353-3. [DOI] [PubMed] [Google Scholar]
  82. Weber T., Zemelman B. V., McNew J. A., Westermann B., Gmachl M., Parlati F., Söllner T. H., Rothman J. E. SNAREpins: minimal machinery for membrane fusion. Cell. 1998 Mar 20;92(6):759–772. doi: 10.1016/s0092-8674(00)81404-x. [DOI] [PubMed] [Google Scholar]
  83. Zucker R. S. Short-term synaptic plasticity. Annu Rev Neurosci. 1989;12:13–31. doi: 10.1146/annurev.ne.12.030189.000305. [DOI] [PubMed] [Google Scholar]

Articles from Philosophical Transactions of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society

RESOURCES