Kinetic analysis of the phosphorylation-dependent interactions of synapsin I with rat brain synaptic vesicles

Journal of Physiology

Volumn 504, Issue 3, 1997, Pages 501-515

  Stefani, Giovanni ^a,b   Onofri, Franco ^a,b   Valtorta, Flavia ^c   Vaccaro, Paola ^a,b   Greengard, Paul ^d   Benfenati, Fabio ^a,b,e  

^a UNIVERSITY OF ROME TOR VERGATA   (Italy)

^b UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

^c UNIVERSITY OF MILAN   (Italy)

^d ROCKEFELLER UNIVERSITY   (United States)

^e Section of Physiology   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; NEUROTRANSMITTER; PHOSPHOLIPID; PHOSPHOPROTEIN; PROTEIN KINASE (CALCIUM,CALMODULIN); SYNAPSIN I; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II;

ARTICLE; CONTROLLED STUDY; DEPHOSPHORYLATION; ENDOCYTOSIS; EXOCYTOSIS; FLUORESCENCE; IONIC STRENGTH; LIPID BILAYER; NERVE CELL; NERVE ENDING; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; RAT; SYNAPSE VESICLE; TEMPERATURE; ANIMAL CELL; ANIMAL TISSUE; BINDING AFFINITY; FLUORESCENCE RESONANCE ENERGY TRANSFER; HYDROPHOBICITY; NERVE CELL PLASTICITY; PRESYNAPTIC POTENTIAL; PROTEIN ANALYSIS; PROTEIN DEPHOSPHORYLATION; PROTEIN FUNCTION; PROTEIN TRANSPORT; REGULATORY MECHANISM;

ANIMALS; BRAIN CHEMISTRY; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; FLUORESCEIN; KINETICS; PHOSPHOLIPIDS; PHOSPHORYLATION; RATS; SPECTROMETRY, FLUORESCENCE; SYNAPSINS; SYNAPTIC VESICLES; TEMPERATURE;

EID: 0030729884     PISSN: 00223751     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1469-7793.1997.501bd.x     Document Type: Article

References (43)

1. BÄHLER, M., BENFENATI, F., VALTORTA, F., CZERNIK, A. J. & GREENGARD, P. (1989). Characterization of synapsin I fragments generated by cysteine-specific cleavage. A study of their interactions with F-actin. Journal of Cell Biology 108, 1841-1849.
2. BÄHLER, M. & GREENGARD, P. (1987). Synapsin I bundles F-actin in a phosphorylation-dependent manner. Nature 326, 704-707.
3. BENFENATI, F., BÄHLER, M., JAHN, R. & GREENGARD, P. (1989a). Interactions of synapsin I with small synaptic vesicles: Distinct sites in synapsin I bind to vesicle phospholipids and vesicle proteins. Journal of Cell Biology 108, 1863-1872.
4. BENFENATI, F., GREENGARD, P., BRUNNER, J. & BÄHLER, M. (1989b). Electrostatic and hydrophobic interactions of synapsin I and synapsin I fragments with phospholipid bilayers. Journal of Cell Biology 108, 1851-1862.
5. BENFENATI, F., NEYROZ, P., BÄHLER, M., MASOTTI, L. & GREENGARD, P. (1990). Time resolved fluorescence study of the neuron specific phosphoprotein synapsin I. Evidence for phosphorylation-dependent conformational changes. Journal of Biological Chemistry 265, 12584-12595.
6. 2+/calmodulin-dependent protein kinase II. Molecular Brain Research 40, 297-309.
7. BENFENATI, F., VALTORTA, F., CHIEREGATTI, E. & GREENGARD, P. (1992a). Interaction of free and synaptic vesicle-bound synapsin I with F-actin. Neuron 8, 377-386.
8. BENFENATI, F., VALTORTA, F., ROSSI, M. C., ONOFRI, F., SIHRA, T. & GREENGARD, P. (1993). Interactions of synapsin I with phospholipids: possible role in synaptic vesicle clustering and in the maintenance of bilayer structures. Journal of Cell Biology 123, 1845-1855.
9. 2+/calmodulin-dependent protein kinase II is a binding protein for synapsin I. Nature 359, 417-420.
10. BETZ, W. J. & WU, L.-G. (1995). Kinetics of synaptic vesicle recycling. Current Biology 5, 1096-1101.
11. CECCALDI, P. E., BENFENATI, F., CHIEREGATTI, E., GREENGARD, P. & VALTORTA, F. (1993). Rapid binding of synapsin I to F- and G-actin. A study using fluorescence resonance energy transfer. FEBS Letters 329, 301-305.
12. CECCALDI, P. E., GROHOVAZ, F., BENFENATI, F., CHIEREGATTI, E., GREENGARD, P. & VALTORTA, F. (1995). Dephosphorylated synapsin I anchors synaptic vesicles to actin cytoskeleton: an analysis by videomicroscopy. Journal of Cell Biology 128, 905-912.
13. CHIN, L.-S., LI, L., FERREIRA, A., KOSIK, K. S. & GREENGARD, P. (1995). Impairment of axonal development and of synaptogenesis in hippocampal neurons of synapsin I-deficient mice. Proceedings of the National Academy of Sciences of the USA 92, 9230-9234.
14. DE CAMILLI, P., BENFENATI, F., VALTORTA, F. & GREENGARD, P. (1990). The synapsins. Annual Review of Cell Biology 6, 433-460.
15. DE CAMILLI, P., HARRIS, S. M., HUTTNER, W. B. & GREENGARD, P. (1983). Synapsin I (Protein I), a nerve terminal-specific phosphoprotein: II. Its specific association with synaptic vesicles demonstrated by immunocytochemistry in agarose-embedded synaptosomes. Journal of Cell Biology 96, 1355-1373.
16. DE CAMILLI, P. & TAKEI, K. (1996) Molecular mechanisms in synaptic vesicle endocytosis and recycling. Neuron 16, 481-486.
17. GÈLI, V., KOORENGEVEL, M. C., DEMEL, R. A., LAZDUNSKI, C. & KILLIAN, J. A. (1992). Acidic interaction of the colicin A poreforming domain with model membranes of Escherichia coli lipids results in a large perturbation of acyl chain order and stabilization of the bilayer. Biochemistry 31, 11089-11094.
18. GREENGARD, P., VALTORTA, F., CZERNIK, A. J. & BENFENATI, F. (1993). Synaptic vesicle phosphoproteins and regulation of synaptic function. Science 259, 780-785.
19. HACKETT, J. T., COCHRAN, S. L., GREENFIELD, J., BROSIUS, D. C. & UEDA, T. (1990). Synapsin I injected presynaptically into Goldfish Mauthner axons reduces quantal synaptic transmission. Journal of Neurophysiology 63, 701-706.
20. HUTTNER, W. B., SCHIEBLER, W., GREENGARD, P. & DE CAMILLI, 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. Journal of Cell Biology 96, 1374-1388.
21. JOVANOVIC, J. N., BENFENATI, F., SIOW, Y. L., SIHRA, T. S., SANGHERA, J. S., PELECH, S. L., GREENGARD, P. & CZERNICK, A. J. (1996). Neurotrophins stimulate phosphorylation of synapsin I by MAP kinase and regulate synapsin I-actin interactions. Proceedings of the National Academy of Sciences of the USA 93, 3679-3683.
22. KACZMAREK, L. K., JENNINGS, K. R., STRUMWASSER, F., NAIRN, A. C., WALTER, U., WILSON, F. D. & GREENGARD, P. (1980). Microinjections of catalytic subunit of cyclic AMP-dependent protein kinase enhances calcium action potentials of bag cell neurons in cell culture. Proceedings of the National Academy of Sciences of the USA 77, 7487-7491.
23. LAEMMLI, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
24. LI, L., CHIN, L.-S., SHUPLIAKOV, O., BRODIN, L., SIHRA, T. S., HVALBY, Ø., JENSEN, V., ZHENG, D., MCNAMARA, J. O., GREENGARD, P. & ANDERSEN, P. (1995). Impairment of synaptic vesicle clustering and of synaptic transmission and increased seizure propensity, in synapsin I-deficient mice. Proceedings of the National Academy of Sciences of the USA 92, 9235-9239.
25. 2+/calmodulin-dependent protein kinase II of transmitter release in squid giant synapse. Journal of Physiology 436, 257-282.
26. LU, B., GREENGARD, P. & POO, M.-M. (1992). Exogenous synapsin I promotes functional maturation of developing neuromuscular synapses. Neuron 8, 521-529.
27. 2+/calmodulin-dependent protein kinase II. Isozymic forms from rat forebrain and cerebellum. Journal of Biological Chemistry 260, 1696-1704.
28. MUNSON, P. J. & RODBARD, D. (1980). LIGAND: A versatile computerized approach for characterization of ligand-binding systems. Analytical Biochemistry 107, 220-239.
29. 2+-ATP-ase labelled selectively with fluorescein. Biochimica et Biophysica Acta 626, 255-261.
30. PIERIBONE, V. A., SHUPLIAKOV, O., BRODIN, L., HILFIKER-ROTHENFLUH, S., CZERNIK, A. J. & GREENGARD, P. (1995). Distinct pools of synaptic vesicles in neurotransmitter release. Nature 375, 493-497.
31. ROSAHL, T. W., SPILLANE, D., MISSLER, M., HERZ, J., SELING, O. K., WOLFF, J. R., HAMMER, R. E., MALENKA, R. C. & SUDHOF, T. C. (1995). Essential functions of synapsin I and II in synaptic vesicle regulation. Nature 375, 488-493.
32. RYAN, T. A., LI, L., CHIN, L.-S., GREENGARD, P. & SMITH, S. J. (1996). Synaptic vesicle recycling in synapsin I knock-out mice. Journal of Cell Biology 134, 1219-1227.
33. RYAN, T. A., REUTER, H., WENDLAND V. B., SCHWEIZER, E., TSIEN, R. W. & SMITH, S. J. (1993). The kinetics of synaptic vesicle recycling measured at single presynaptic boutons. Neuron 11, 713-724.
34. RYAN, T. A. & SMITH, S. J. (1995). Vesicle pool mobilization during action potential firing at hippocampal synapses. Neuron 14, 983-989.
35. SCHIEBLER, W., JAHN, R., DOUCET, J. P., ROTHLEIN, J. & GREENGARD, P. (1986). Characterization of synapsin I binding to small synaptic vesicles. Journal of Biological Chemistry 261, 8383-8390.
36. SIHRA, T. S., WANG, J. K. T., GORELICK, F. S. & GREENGARD, P. (1989). Translocation of synapsin I in response to depolarization of isolated nerve terminals. Proceedings of the National Academy of Sciences of the USA 6, 8108-8112.
37. STRYER, L. (1978). Fluorescence energy transfer as a spectroscopic ruler. Annual Review of Biochemistry 47, 819-846.
38. SÜDHOF, 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. & GREENGARD, P. (1989). Synapsins: Mosaics of shared and individual domains in a family of synaptic vesicle phosphoproteins. Science 245, 1474-1480.
39. TAKEI, Y., HARADA, A., TAKEDA, S., KOBAYASHI, K., TERADA, S., NODA, T., TAKAHASHI, T. & HIROKAWA, N. (1995). Synapsin I deficiency results in structural changes in the presynaptic terminals in the murine nervous system. Journal of Cell Biology 131, 1789-1800.
40. TORRI TARELLI, F., BOSSI, M., FESCE, R., GREENGARD, P. & VALTORTA, F. (1992). Synapsin I partially dissociates from synaptic vesicles during exocytosis induced by electrical stimulation. Neuron 9, 1143-1153.
41. TOWBIN, L., STAEHELIN, T. & GORDON, J. (1979). Electrophoretic transfer of proteins from poliacrylamide gels to nitrocellulose sheets: procedures and some applications. Proceedings of the National Academy of Sciences of the USA 76, 4350-4354.
42. VALTORTA, F., GREENGARD, P., FESCE, R., CHIEREGATTI, F. & BENFENATI, F. (1992). Effects of the neuronal phosphoprotein synapsin I on actin polymerization. I. Evidence for a phosphorylation-dependent nucleating effect. Journal of Biological Chemistry 267, 11281-11288.
43. VALTORTA, F., IEZZI, N., BENFENATI, F., LU, B., POO, M-M. & GREENGARD, P. (1995). Accelerated structural maturation induced by synapsin I at developing neuromuscular synapses of Xenopus laevis. European Journal of Neuroscience 7, 261-270.