Cytoskeletal interactions of synapsin I in non-neuronal cells

Biochemical and Biophysical Research Communications

Volumn 317, Issue 1, 2004, Pages 16-23

  Hurley, Sandra L ^a   Brown, David L ^b   Cheetham, James J ^a  

^a CARLETON UNIVERSITY   (Canada)

^b UNIVERSITY OF OTTAWA   (Canada)

Author keywords

Actin; Cytoskeleton; Green fluorescent protein; Membrane; Microtubules; Synapsin

Indexed keywords

CYTOCHALASIN B; F ACTIN; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; NOCODAZOLE; PACLITAXEL; SYNAPSIN I; VIMENTIN;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOSKELETON; EMBRYO; HUMAN; HUMAN CELL; MICROTUBULE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION;

ACTINS; ANIMALS; CYTOCHALASIN B; CYTOSKELETON; GREEN FLUORESCENT PROTEINS; HELA CELLS; HUMANS; LUMINESCENT PROTEINS; MICE; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; MICROTUBULES; NIH 3T3 CELLS; RATS; RECOMBINANT FUSION PROTEINS; SYNAPSINS; TRANSFECTION; VIMENTIN;

EID: 1642504427     PISSN: 0006291X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbrc.2004.03.008     Document Type: Article

References (53)

1. Akagi S., Mizoguchi A., Sobue K., Nakamura H., Ide C. Localization of synapsin I in normal fibers and regenerating axonal sprouts of the rat sciatic nerve. Histochem. Cell Biol. 105:1996;365-373.
2. Bahler M., Greengard P. Synapsin I bundles F-actin in a phosphorylation-dependent manner. Nature. 326:1987;704-707.
3. Baines A.J., Bennett V. Synapsin I is a spectrin-binding protein immunologically related to erythrocyte protein 4.1. Nature. 315:1985;410-413.
4. Baines A.J., Bennett V. Synapsin I is a microtubule-bundling protein. Nature. 319:1986;145-147.
5. 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. 123:1993;1845-1855.
6. 2+/calmodulin-dependent protein kinase II is a binding protein for synapsin I. Nature. 359:1992;417-420.
7. Bhangu P.S., Genever P.G., Spencer G.J., Grewal T.S., Skerry T.M. Evidence for targeted vesicular glutamate exocytosis in osteoblasts. Bone. 29:2001;16-23.
8. Bustos R., Kolen E.R., Braiterman L., Baines A.J., Gorelick F.S., Hubbard A.L. Synapsin I is expressed in epithelial cells: localization to a unique trans-Golgi compartment. J. Cell Sci. 114:2001;3695-3704.
9. Ceccaldi P.E., Benfenati F., Chieregatti E., Greengard P., Valtorta F. Rapid binding of synapsin I to F- and G-actin. A study using fluorescence resonance energy transfer. FEBS Lett. 329:1993;301-305.
10. Cheetham J.J., Hilfiker S., Benfenati F., Weber T., Greengard P., Czernik A.J. Identification of synapsin I peptides that insert into lipid membranes. Biochem. J. 354:2001;57-66.
11. Chen C., Okayama H. High-efficiency transformation of mammalian cells by plasmid DNA. Mol. Cell. Biol. 7:1987;2745-2752.
12. Chin L.S., Li L., Ferreira A., Kosik K.S., Greengard P. Impairment of axonal development and of synaptogenesis in hippocampal neurons of synapsin I-deficient mice. Proc. Natl. Acad. Sci. USA. 92:1995;9230-9234.
13. 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. 96:1983;1337-1354.
14. 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. 96:1983;1355-1373.
15. Falconer M.M., Echeverri C.J., Brown D.L. Differential sorting of beta tubulin isotypes into colchicine-stable microtubules during neuronal and muscle differentiation of embryonal carcinoma cells. Cell Motil. Cytoskeleton. 21:1992;313-325.
16. Farrell K.P., Keates R.A. Synapsin-1 is found in a microtubule- associated complex of proteins isolated from bovine brain. Biochem. Cell Biol. 68:1990;1256-1261.
17. Ferreira A., Chin L.S., Li L., Lanier L.M., Kosik K.S., Greengard P. Distinct roles of synapsin I and synapsin II during neuronal development. Mol. Med. 4:1998;22-28.
18. Ferreira A., Han H.Q., Greengard P., Kosik K.S. Suppression of synapsin II inhibits the formation and maintenance of synapses in hippocampal culture. Proc. Natl. Acad. Sci. USA. 92:1995;9225-9229.
19. Ferreira A., Kosik K.S., Greengard P., Han H.Q. Aberrant neurites and synaptic vesicle protein deficiency in synapsin II-depleted neurons. Science. 264:1994;977-979.
20. 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. 261:1986;8495-8504.
21. Goold R., Baines A.J. Evidence that two non-overlapping high-affinity calmodulin-binding sites are present in the head region of synapsin I. Eur. J. Biochem. 224:1994;229-240.
22. 2+/calmodulin and phosphorylation: inhibition of actin binding and bundling. Biochemistry. 34:1995;1912-1920.
23. Han H.Q., Nichols R.A., Rubin M.R., Bahler M., Greengard P. Induction of formation of presynaptic terminals in neuroblastoma cells by synapsin IIb (see comments). Nature. 349:1991;697-700.
24. Hilfiker S., Pieribone V.A., Czernik A.J., Kao H.T., Augustine G.J., Greengard P. Synapsins as regulators of neurotransmitter release (in process citation). Philos. Trans. R. Soc. Lond. B. 354:1999;269-279.
25. 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. 1:1998;29-35.
26. Hosaka M., Hammer R.E., Sudhof T.C. A phospho-switch controls the dynamic association of synapsins with synaptic vesicles. Neuron. 24:1999;377-387.
27. 2+ regulation. J. Biol. Chem. 273:1998;1425-1429.
28. Iga M., Inui M., Sobue K. Characterization of the interaction between synapsin I and calspectin (brain spectrin or fodrin). Biochem. Biophys. Res. Commun. 231:1997;852-855.
29. Kao H.T., Porton B., Czernik A.J., Feng J., Yiu G., Haring M., Benfenati F., Greengard P. A third member of the synapsin gene family. Proc. Natl. Acad. Sci. USA. 95:1998;4667-4672.
30. Kao H.T., Porton B., Hilfiker S., Stefani G., Pieribone V.A., DeSalle R., Greengard P. Molecular evolution of the synapsin gene family. J. Exp. Zool. 285:1999;360-377.
31. Li L., Chin L.S., Shupliakov O., Brodin L., Sihra T.S., Hvalby O., Jensen V., Zheng D., McNamara J.O., Greengard P.et al. Impairment of synaptic vesicle clustering and of synaptic transmission, and increased seizure propensity, in synapsin I-deficient mice. Proc. Natl. Acad. Sci. USA. 92:1995;9235-9239.
32. Llinas 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. USA. 82:1985;3035-3039.
33. Lu B., Czernik A.J., Popov S., Wang T., Poo M.M., Greengard P. Expression of synapsin I correlates with maturation of the neuromuscular synapse. Neuroscience. 74:1996;1087-1097.
34. Lu B., Greengard P., Poo M.M. Exogenous synapsin I promotes functional maturation of developing neuromuscular synapses. Neuron. 8:1992;521-529.
35. Matovcik L.M., Karapetian O., Czernik A.J., Marino C.R., Kinder B.K., Gorelick F.S. Antibodies to an epitope on synapsin I detect a protein associated with the endocytic compartment in non-neuronal cells. Eur. J. Cell Biol. 65:1994;327-340.
36. Matsumoto K., Ebihara K., Yamamoto H., Tabuchi H., Fukunaga K., Yasunami M., Ohkubo H., Shichiri M., Miyamoto E. Cloning from insulinoma cells of synapsin I associated with insulin secretory granules. J. Biol. Chem. 274:1999;2053-2059.
37. McPherson P.S., Czernik A.J., Chilcote T.J., Onofri F., Benfenati F., Greengard P., Schlessinger J., De Camilli P. Interaction of Grb2 via its Src homology 3 domains with synaptic proteins including synapsin I. Proc. Natl. Acad. Sci. USA. 91:1994;6486-6490.
38. Onofri F., Giovedi S., Kao H.T., Valtorta F., Borbone L.B., De Camilli P., Greengard P., Benfenati F. Specificity of the binding of synapsin I to Src homology-3 domains. J. Biol. Chem. 2000.
39. Petrucci T.C., Morrow J.S. Synapsin I: an actin-bundling protein under phosphorylation control. J. Cell Biol. 105:1987;1355-1363.
40. Pieribone V.A., Shupliakov O., Brodin L., Hilfiker-Rothenfluh S., Czernik A.J., Greengard P. Distinct pools of synaptic vesicles in neurotransmitter release (see comments). Nature. 375:1995;493-497.
41. Rosahl T.W., Geppert M., Spillane D., Herz J., Hammer R.E., Malenka R.C., Sudhof T.C. Short-term synaptic plasticity is altered in mice lacking synapsin I. Cell. 75:1993;661-670.
42. Rosahl T.W., Spillane D., Missler M., Herz J., Selig D.K., Wolff J.R., Hammer R.E., Malenka R.C., Sudhof T.C. Essential functions of synapsins I and II in synaptic vesicle regulation (see comments). Nature. 375:1995;488-493.
43. 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. 134:1996;1219-1227.
44. Schiebler W., Jahn R., Doucet J.P., Rothlein J., Greengard P. Characterization of synapsin I binding to small synaptic vesicles. J. Biol. Chem. 261:1986;8383-8390. (published erratum appears in J. Biol. Chem. 261 (26) (1986, Sep 15) 12428).
45. Sikorski A.F., Terlecki G., Zagon I.S., Goodman S.R. Synapsin I-mediated interaction of brain spectrin with synaptic vesicles. J. Cell Biol. 114:1991;313-338.
46. Steiner J.P., Ling E., Bennett V. Nearest neighbor analysis for brain synapsin I. Evidence from in vitro reassociation assays for association with membrane protein(s) and the Mr = 68,000 neurofilament subunit. J. Biol. Chem. 262:1987;905-914.
47. Sudhof T.C. The structure of the human synapsin I gene and protein. J. Biol. Chem. 265:1990;7849-7852.
48. Sudhof T.C., Czernik A.J., Kao H.T., Takei K., Johnston P.A., Horiuchi A., Kanazir S.D., Wagner M.A., Perin M.S., De Camilli P.et al. Synapsins: mosaics of shared and individual domains in a family of synaptic vesicle phosphoproteins. Science. 245:1989;1474-1480.
49. 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. 131:1995;1789-1800.
50. Terada S., Tsujimoto T., Takei Y., Takahashi T., Hirokawa N. Impairment of inhibitory synaptic transmission in mice lacking synapsin I. J. Cell Biol. 145:1999;1039-1048.
51. Thiel G., Sudhof T.C., Greengard P. Synapsin II. Mapping of a domain in the NH2-terminal region which binds to small synaptic vesicles. J. Biol. Chem. 265:1990;16527-16533.
52. Valtorta F., Benfenati F. Signal transduction at the nerve terminal level: role of the phosphorylation of synaptic vesicle proteins. Pharmacol. Res. 25(Suppl. 1):1992;99-100.
53. Zhong Z.G., Noda M., Takahashi H., Higashida H. Overexpression of rat synapsins in NG108-15 neuronal cells enhances functional synapse formation with myotubes (in process citation). Neurosci. Lett. 260:1999;93-96.