Biochemical and functional characterization of the synaptic vesicle-associated form of Ca2+/calmodulin-dependent protein kinase II

Molecular Brain Research

Volumn 40, Issue 2, 1996, Pages 297-309

  Benfenati, Fabio ^a,b   Onofri, Franco ^a,b   Czernik, Andrew J ^c   Valtorta, Flavia ^d  

^a UNIVERSITY OF ROME TOR VERGATA   (Italy)

^b UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

^c ROCKEFELLER UNIVERSITY   (United States)

^d SAN RAFFAELE HOSPITAL   (Italy)

Author keywords

CaM kinase II; Neurotransmitter release; Synapsin I; Synaptic vesicles

Indexed keywords

PROTEIN KINASE (CALCIUM,CALMODULIN) II; SYNAPSIN I;

ANIMAL TISSUE; ARTICLE; AUTOPHOSPHORYLATION; BIOCHEMISTRY; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ENZYME SUBUNIT; KINETICS; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; RAT; SYNAPSE VESICLE; SYNAPTIC TRANSMISSION;

ANIMALIA;

EID: 0030248526     PISSN: 0169328X     EISSN: None     Source Type: Journal    
DOI: 10.1016/0169-328X(96)00053-8     Document Type: Article

References (68)

1. Bach M.E., Hawkins R.D., Osman M., Kandel E.R., Mayford M. Impairment of spatial but not contextual memory in CaMKII mutant mice with a selective loss of hippocampal LTP in the frequency. Cell. 81:1995;905-915.
2. Bähler M., Greengard P. Synapsin I bundles F-actin in a phosphorylation-dependent manner. Nature. 326:1987;704-707.
3. Bähler M., Benfenati F., Valtorta F., Czernik A.J., Greengard P. Characterization of synapsin I fragments generated by cysteine-specific cleavage. A study of their interactions with F-actin. J. Cell Biol. 108:1989;1841-1849.
4. 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. 108:1989;1851-1862.
5. 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. 108:1989;1863-1872.
6. 2+/calmodulin-dependent protein kinase II is a binding protein for synapsin I. Nature. 359:1992;417-420.
7. Benfenati F., Valtorta F., Chieregatti E., Greengard P. Interaction of free and synaptic vesicle-bound synapsin I with F-actin. Neuron. 8:1992;377-386.
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. 123:1993;1845-1855.
9. 2+/calmodulin-dependent protein kinase determined by molecular cloning. Proc. Natl. Acad. Sci. USA. 84:1987;1794-1798.
10. 2+/calmodulin-dependent protein kinase isoforms in rat brain. J. Neurosci. 15:1995;6797-6808.
11. Ceccaldi P.-E., Grohovaz F., Benfenati F., Chieregatti E., Greengard P., Valtorta F. Dephosphorylated synapsin I anchors synaptic vesicles to actin cytoskeleton: an analysis by videomicroscopy. J. Cell Biol. 128:1995;905-912.
12. 2+/calmodulin-dependent kinase. a bidirectional modulator of presynaptic plasticity Neuron. 14:1995;591-597.
13. 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.
14. Cleveland D.W., Fischer S.G., Kirschner M.W., Laemmli U.K. Peptide mapping by limited proteolysis in sodium dodecyl sulfate and analysis by gel electrophoresis. J. Biol. Chem. 252:1977;1102-1106.
15. Colbran R.J., Smith M.K., Schworer C.M., Fong Y-L., Soderling T.R. Regulatory domain of calcium/calmodulin-dependent protein kinase. Mechanism of inhibition and regulation by phosphorylation J. Biol. Chem. 264:1989;4800-4804.
16. Colbran R.J., Soderling T.R. Calcium/calmodulin-independent autophosphorylation sites of calcium/calmodulin-dependent protein kinase. Studies on the effect of phosphorylation of threonine 305 306 and serine 314 on calmodulin binding using synthetic peptides J. Biol. Chem. 265:1990;11213-11219.
17. Colbran R.J. Regulation and role of brain calcium/calmodulin-dependent protein kinase II. Neurochem. Int. 21:1992;469-497.
18. 2+/calmodulin-dependent protein kinase II. J. Biol. Chem. 268:1993;7863-7867.
19. Goldenring J.R., McGuire J.S., DeLorenzo R.J. Identification of the major postsynaptic density protein as homologous with the major calmodulin-binding subunit of a calmodulin-dependent protein kinase. J. Neurochem. 42:1984;1077-1084.
20. 2+/calmodulin-dependent protein kinase II in intact nerve terminals. J. Biol. Chem. 263:1988;17209-17212.
21. Greengard P., Valtorta F., Czernik A.J., Benfenati F. Synaptic vesicle phosphoproteins and regulation of synaptic function. Science. 259:1993;780-785.
22. Hackett J.T., Cochran S.L., Greenfield L.J., Brosius D.C., Ueda T. Synapsin I injected presynaptically into goldfish Mauthner axons reduces quantal synaptic transmission. J. Neurophysiol. 63:1990;701-706.
23. 2+ / calmodulin dependent protein kinase analyzed by site-directed mutagenesis. J. Biol. Chem. 267:1992;17216-17224.
24. 2+ / calmodulin-dependent protein kinases. Annu. Rev. Biochem. 61:1992;559-601.
25. Hanson P.I., Meyer T., Stryer L., Schulman H. Dual role of calmodulin in autophosphorylation of multifunctional CaM kinase may underlie decoding of calcium signals. Neuron. 12:1994;943-956.
26. Hilfiker-Rothenfluh S., Cheetham J.J., Fienberg A.A., Greengard P., Czernik A.J. Interaction of calcium/calmodulin-dependent protein kinase II with membranes: studies with purified synaptic vesicles and liposomes. Soc. Neurosci. Abstr. 20:1994;1712.
27. Huttner W.B., Schiebler W., Greengard P., De Camilli P. Synapsin I (Protein I), a nerve terminal-specific phosphoprotein. Its association with synaptic vesicles studied in a highly purified synaptic vesicle preparation J. Cell Biol. 96:1983;1374-1388.
28. Jahn R., Schiebler W., Greengard P. A quantitative dot-immunobinding assay for proteins using nitrocellulose membrane filters. Proc. Natl. Acad. Sci. USA. 81:1984;1684-1687.
29. 2+ / calmodulin-dependent protein kinase II revealed by electron microscopy. J. Cell Biol. 115:1991;1049-1060.
30. 2+ / calmodulin-dependent protein kinase. Proc. Natl. Acad. Sci. USA. 81:1984;945-949.
31. Kennedy M.B., Bennett M.K., Erondu N.E. Biochemical and immunochemical evidence that the `major postsynaptic density protein' is a subunit of a calmodulin-dependent protein kinase. Proc. Natl. Acad. Sci. USA. 80:1983;7357-7361.
32. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:1970;680-685.
33. 2+ / calmodulin-dependent protein kinase II. Proc. Natl. Acad. Sci. USA. 83:1986;4253-4257.
34. 2+ / calmodulin-independence. Proc. Natl. Acad. Sci. USA. 84:1987;5710-5714.
35. 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. 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.
36. 2+ / calmodulin-dependent protein kinase II of transmitter release in squid giant synapse. J. Physiol. 436:1991;257-282.
37. 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. USA. 82:1985;3035-3039.
38. 2+ / calmodulin-dependent protein kinase. J. Neurosci. 9:1989;2020-2032.
39. Mayford M., Wang J., Kandel E.R., O'Dell T.J. CaMKII regulates the frequency-response function of hippocampal synapses for the production of both LTD and LTP. Cell. 81:1995;891-904.
40. McGlade-McCulloh E., Yamamoto H., Tan S.-E., Brickey D.A., Soderling T.R. Phosphorylation and regulation of glutamate receptors by calcium/calmodulin-dependent protein kinase II. Nature. 362:1993;640-642.
41. 2+/calmodulin-dependent protein kinase II isozymic forms from rat forebrain and cerebellum. J. Biol. Chem. 260:1985;1696-1704.
42. Meyer T., Hanson P.I., Stryer L., Schulman H. Calmodulin trapping by calcium-calmodulin-dependent protein kinase. Science. 256:1992;1199-1202.
43. 2+-triggered molecular switch. Cell. 44:1986;861-870.
44. 2+-independent activity. Neuron. 1:1988;593-604.
45. Munson P.J., Rodboard D. LIGAND: A versatile computerized approach for characterization of ligand-binding systems. Anal. Biochem. 107:1980;220-239.
46. Nichols R.A., Sihra T.S., Czernik A.J., Nairn A.C., Greengard P. Calcium/calmodulin-dependent protein kinase II increases glutamate and noradrenaline release from synaptosomes. Nature. 343:1990;647-651.
47. Nichols R.A., Chilcote T.J., Czernik A.J., Greengard P. Synapsin I regulates glutamate release from rat brain synaptosomes. J. Neurochem. 58:1992;783-785.
48. Nielander H.B., Onofri F., Valtorta F., Schiavo G., Montecucco C., Greengard P., Benfenati F. Phosphorylation of VAMP/synaptobrevin in synaptic vesicles by endogenous protein kinases. J. Neurochem. 65:1995;1712-1720.
49. O'Farrell P.Z., Goodman H.M., O'Farrell P.H. High resolution two-dimensional electrophoresis of basic as well as acidic proteins. Cell. 12:1977;1133-1142.
50. Quimet C.C., McGuinness T.L., Greengard P. Immunocytochemical localization of calcium/calmodulin-dependent protein kinase II in rat brain. Proc. Natl. Acad. Sci. USA. 81:1984;5604-5608.
51. Payne M.E., Fong Y.-L., Ono T., Colbran R.J., Kemp B.E., Soderling T.S., Means A.R. Calcium/calmodulin-dependent protein kinase II characterization of distinct calmodulin binding and inhibitory domains. J. Biol. Chem. 263:1988;7190-7195.
52. Pieribone V.A., Shupliakov O., Brodin L., Hilfiker-Rothenfluh S., Czernik A.J., Greengard P. Distinct pools of synaptic vesicles in neurotransmitter release. Nature. 375:1995;493-497.
53. 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. 75:1993;861-870.
54. 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. 375:1995;488-493.
55. Rubenstein J.L., Greengard P., Czernik A.J. Calcium-dependent serine phosphorylation of synaptophysin. Synapse. 13:1993;161-172.
56. 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.
57. 2+/calmodulin-dependent protein kinase II: identification of a regulatory autophosphorylation site adjacent to the inhibitory and calmodulin-binding domains. J. Biol. Chem. 263:1988;13486-13489.
58. Schulman H., Hanson P.I., Mayer T. Decoding calcium signals by multifunctional CaM kinasse. Cell Calcium. 13:1992;401-411.
59. Shields S.M., Vernon P.J., Kelly P.T. Autophosphorylation of calmodulin-kinase II in synaptic junctions modulates endogenous kinase activity. J. Neurochem. 43:1984;1599-1609.
60. Silva A.J., Stevens C.F., Tonegawa S., Wang Y. Deficient hippocampal long-term potentiation in α-calcium-calmodulin kinase II mutant mice. Science. 257:1992;201-206.
61. Silva A.J., Paylor R., Wehner J.M., Tonegawa S. Impaired spatial learning in α-calcium-calmodulin kinase II mutant mice. Science. 257:1992;206-211.
62. Sriniavasan M., Edman C.F., Schulman H. Alternative splicing introduces a nuclear localization signal that targets multifunctional CaM kinase to the nucleus. J. Cell Biol. 126:1994;839-852.
63. 2+-independent activity. Proc. Natl. Acad. Sci. USA. 85:1988;6337-6341.
64. Tobimatsu T., Fujisawa H. Tissue-specific expression of four types of rat calmodulin-dependent protein kinase II mRNAs. J. Biol. Chem. 264:1989;17907-17912.
65. Towbin L., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA. 76:1979;4350-4354.
66. Walaas S.I., Gorelick F.S., Greengard P. Presence of calcium/calmodulin-dependent protein kinase II in nerve terminals of rat brain. Synapse. 3:1989;356-362.
67. Wollenweber H.W., Morrison D.C. Synthesis and biochemical characterization of a photoactivatable, iodinatable, cleavable lipopolysaccharide derivative. J. Biol. Chem. 260:1985;15068-15074.
68. Wu K., Huang Y., Adler J., Black I.B. On the identity of the major postsynaptic density protein. Proc. Natl. Acad. Sci. USA. 89:1992;3015-3019.