Changes of synaptotagmin interaction with t-SNARE proteins in vitro after calcium/calmodulin-dependent phosphorylation

Journal of Neurochemistry

Volumn 74, Issue 1, 2000, Pages 209-221

  Verona, Marina ^a   Zanotti, Simona ^b   Schäfer, Theo ^d   Racagni, Giorgio ^a   Popoli, Maurizio ^a,c  

^a UNIVERSITY OF MILAN   (Italy)

^b IRCCS ISTITUTO CENTRO SAN GIOVANNI DI DIO FATEBENEFRATELLI   (Italy)

^c UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^d FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

Author keywords

Calcium; Neurotransmitter release; Protein phosphorylation; Synaptic plasticity; Synaptosome associated protein receptor; Synaptotagmin

Indexed keywords

SNARE PROTEIN; SYNAPTOBREVIN; SYNAPTOSOMAL ASSOCIATED PROTEIN 25; SYNAPTOTAGMIN; SYNTAXIN;

ANIMAL TISSUE; ARTICLE; DEPHOSPHORYLATION; IMMUNOPRECIPITATION; NERVE CELL PLASTICITY; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RAT; REACTION ANALYSIS; SYNAPSE VESICLE;

ANIMALS; ANTIGENS, SURFACE; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CALCIUM; CALCIUM-BINDING PROTEINS; DRUG INTERACTIONS; ENZYME INHIBITORS; GLUTATHIONE TRANSFERASE; MALE; MEMBRANE GLYCOPROTEINS; MEMBRANE PROTEINS; NERVE TISSUE PROTEINS; PHOSPHOPROTEIN PHOSPHATASE; PHOSPHORYLATION; RATS; RATS, SPRAGUE-DAWLEY; RECOMBINANT PROTEINS; SNARE PROTEINS; SYNAPTIC MEMBRANES; SYNAPTOSOMAL-ASSOCIATED PROTEIN 25; SYNAPTOSOMES; SYNAPTOTAGMINS; SYNTAXIN 1; VESICULAR TRANSPORT PROTEINS;

ANIMALIA;

EID: 0033981953     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.2000.0740209.x     Document Type: Article

References (52)

1. Barnes G. N., Slevin J. T., and Vanaman T. C. (1995) Rat brain protein phosphatase 2A: an enzyme that may regulate autophosphorylated protein kinases. J. Neurochem. 64, 340-353.
2. Bennett M. K., Miller K. G., and Scheller R. H. (1993) Casein kinase II phosphorylates the synaptic vesicle protein p65. J. Neurosci. 13, 1701-1707.
3. 2+ regulates the interaction between synaptotagmin and syntaxin I. J. Biol. Chem. 270, 23667-23671.
4. Charvin N., Leveque C., Walker D., Berton F., Raymond C., Kataoka M., Shoji-Kasai Y., Takahashi M., De Waard M., and Seagar M. J. (1997) Direct interaction of the calcium sensor protein synaptotagmin I with a cytoplasmic domain of the α1A subunit of the P/Q-type calcium channel. EMBO J. 16, 4591-4596.
5. Cheung H. S., Sallis J. D., and Struve J. A. (1996) Specific inhibition of basic calcium phosphate and calcium pyrophosphate crystal-induction of metalloproteinase synthesis by phosphocitrate. Biochim. Biophys. Acta 1315, 105-111.
6. 2+/phospholipid binding. J. Biol. Chem. 268, 26386-26390.
7. Davletov B. A., Sontag J.-M., Hata Y., Petrenko A. G., Fykse E. M., Jahn R., and Südhof T. C. (1993) Phosphorylation of synaptotagmin I by casein kinase II. J. Biol. Chem. 268, 6816-6822.
8. 2+/calmodulin-dependent protein kinase II and protein kinase C by glutamate in cultured rat hippocampal neurons. J. Biol. Chem. 267, 22527-22533.
9. Garcia E. P., McPherson P. S., Chilcote T. J., Takei K., and De Camilli P. (1995) rbSec1A and B colocalize with syntaxin 1 and SNAP-25 throughout the axon, but are not in a stable complex with syntaxin. J. Cell Biol. 129, 105-120.
10. 2+ sensor for transmitter release at a central synapse. Cell 79, 717-727.
11. 2+/calmodulin-dependent protein kinase II in intact nerve terminals. J. Biol. Chem. 263, 17209-17212.
12. Greengard P., Valtorta F., Czernik A. J., and Benfenati F. (1993) Synaptic vesicle phosphoproteins and regulation of synaptic function. Science 259, 780-785.
13. Hayashi T., Yamasaki S., Nauenburg S., Binz T., and Niemann H. (1995) Disassembly of the reconstituted synaptic vesicle membrane fusion complex in vitro. EMBO J. 14, 2317-2325.
14. Hirling H. and Scheller R. H. (1996) Phosphorylation of synaptic vesicle proteins: modulation of the αSNAP interaction with the core complex. Proc. Natl. Acad. Sci. USA 93, 11945-11949.
15. Huttner W. B., Schiebler W., Greengard P., and 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. J. Cell Biol. 96, 1373-1388.
16. 2+ and short term synaptic plasticity. Nature 371, 603-606.
17. Kee Y. and Scheller R. H. (1996) Localization of synaptotagmin-binding domains on syntaxin. J. Neurosci. 16, 1975-1981.
18. Komatsu M., McDermott A. M., and Sharp G. W. G. (1995) Sodium fluoride stimulates exocytosis at a late site of calcium interaction in stimulus-secretion coupling: studies with the RINm5f β cell line. Mol. Pharmacol. 47, 496-508.
19. 2+-dependent and -independent activities of neural and non-neural synaptotagmins. Nature 375, 594-599.
20. Lin J. W., Sugimori M., Llinas R., McGuinness T. L., and Greengard P. (1990) Effects of synapsin I and calcium/calmodulin-dependent protein kinase II on spontaneous neurotransmitter release in the squid giant synapse. Proc. Natl. Acad. Sci. USA 87, 8257-8261.
21. 2+-activated neurotransmitter release. Cell 74, 1125-1134.
22. Lonart G. and Südhof T. (1998) Region-specific phosphorylation of rabphilin in mossy fiber nerve terminals of the hippocampus. J. Neurosci. 15, 634-640.
23. 2+-dependent triggering of neurotransmitter exocytosis. Proc. Natl. Acad. Sci. USA 93, 10471-10476.
24. Murphy T. H., Blatter L. A., Bhat R. V., Fiore R. S., Wier W. G., and Baraban J. M. (1994) Differential regulation of calcium/calmodulin-dependent protein kinase II and p42 MAP kinase activity by synaptic transmission. J. Neurosci. 14, 1320-1331.
25. Nicholls D. G. (1978) Calcium transport and proton electrochemical potential gradient in mitochondria from guinea-pig cerebral cortex and rat heart. Biochem. J. 170, 511-522.
26. Nichols R. A., Haycock J. W., Wang J. K. T., and Greengard P. (1987) Phorbol ester enhancement of neurotransmitter release from rat brain synaptosomes. J. Neurochem. 48, 615-621.
27. Nichols R. A., Sihra T. S., Czernik A. J., Nairn A. C., and Greengard P. (1990) Calcium/calmodulin-dependent protein kinase II increases glutamate and noradrenaline release from synaptosomes. Nature 343, 647-651.
28. Nonet M. L., Grundahl K., Meyer B. J., and Rand J. B. (1993) Synaptic function is impaired but not eliminated in C. elegans mutants lacking synaptotagmin. Cell 73, 1291-1305.
29. O'Connor V. O., Heuss C., De Bello W. M., Dresbach T., Charlton M. P., Hunt J. H., Pellegrini L. L., Hodel A., Burger M. M., Betz H., Augustine G. J., and Schåfer T. (1997) Disruption of syntaxin-mediated protein interactions blocks neurotransmitter secretion. Proc. Natl. Acad. Sci. USA 94, 12186-12191.
30. Perin M. S. (1996) Mirror image motifs mediate the interaction of the COOH terminus of multiple synaptotagmins with the neurexins and calmodulin. Biochemistry 35, 13808-13816.
31. Perin M. S., Fried V. A., Mignery G. A., Jahn R., and Sudhof T. (1990) Phospholipid binding by a synaptic vesicle protein homologous to the regulatory region of protein kinase C. Nature 345, 260-263.
32. 2+/calmodulin protein kinase II in synaptic vesicles. FEBS Lett. 317, 85-88.
33. 2+/calmodulin-dependent protein kinase II: autophosphorylation and activity increase in the hippocampus after long-term blockade of serotonin reuptake. Mol. Pharmacol. 48, 623-629.
34. 2+/ phospholipid-binding and syntaxin-binding of native synaptotagmin I. Life Sci. 61, 711-721.
35. Popoli M., Venegoni A., Vocaturo C., Buffa L., Perez J., Smeraldi E., and Racagni G. (1997b) Synaptotagmin phosphorylation is affected by long-term blockade of 5-HT reuplake. Mol. Pharmacol. 51, 19-26.
36. Popoli M., Brunello N., Perez J., and Racagni G. (2000) Second messenger-regulated protein kinases in the brain: their functional role and the action of antidepressant drugs. J. Neurochem. 74, 21-33.
37. Risinger C. and Bennett M. K. (1999) Differential phosphorylation of syntaxin and synaptosome-associated protein of 25 kDa (SNAP-25) isoforms. J. Neurochem. 72, 614-624.
38. Rothman J. (1994) Mechanisms of intracellular protein transport. Nature 372, 99-163.
39. Scheller R. H. (1995) Membrane trafficking in the presynaptic terminal. Neuron 14, 893-897.
40. Schiavo G., Stenbeck G., Rothman J. E., and Sollner T. H. (1997) Binding of the synaptic vesicle v-SNARE, synaptotagmin, to the plasma membrane t-SNARE, SNAP-25, can explain docked vesicles at neurotoxin-treated synapses. Proc. Natl. Acad. Sci. USA 94, 997-1001.
41. Sesack S. R. and Snyder C. L. (1995) Cellular and subcellular localization of syntaxin-like immunoreactivity in the rat striatum and cortex. Neuroscience 67, 993-1007.
42. 2+ channels with the C2B domain of synaptotagmin I. Proc. Natl. Acad. Sci. USA 94, 5405-5410.
43. Shimazaki Y., Nishiki T., Omori A., Sekiguchi M., Kamata Y., Kozaki S., and Takahashi M. (1996) Phosphorylation of 25-kDa synaptosome-associated protein. Possible involvement in protein kinase C-mediated regulation of neurotransmitter release. J. Biol. Chem. 271, 14548-14553.
44. 2+ acts by two separate pathways to modulate the supply of release-competent vesicles in chromaffin cells. Neuron 20, 1243-1253.
45. Sollner T., Bennet M. K., Whiteheart S. W., Scheller R. H., and Rothman J. E. (1993) A protein assembly-disassembly pathway in vitro that may correspond to sequential steps of synaptic vesicle docking, activation and fusion. Cell 75, 409-418.
46. Stevens C. F. and Sullivan J. M. (1998) Regulation of the readily releasable vesicle pool by protein kinase C. Neuron 21, 885-893.
47. Südhof T. C. (1995) The synaptic vesicle cycle: a cascade of protein-protein interactions. Nature 375, 645-653.
48. 2+-stimulaied phosphorylation. Effects of protein phosphatases and phosphatase inhibitors. J. Biol. Chem. 265, 10352-10357.
49. Weber T., Zemelman B. V., McNew J. A., Westermann M. G., Parlati F., Sollner T. H., and Rothman J. E. (1998) SNAREpins; minimal machinery for membrane fusion. Cell 92, 759-772.
50. Wiser O., Tobi D., Trus M., and Atlas D. (1997) Synaptotagmin restores kinetic properties of a syntaxin-associated N-type voltage sensitive calcium channel. FEBS Lett. 404, 203-207.
51. Yokoyama C. T., Sheng Z.-H., and Catterall W. A. (1997) Phosphorylation of the synaptic protein interaction site on N-type calcium channels inhibits interactions with SNARE proteins. J. Neurosci. 17, 6929-6938.
52. Zucker R. S. (1996) Exocytosis: a molecular and physiological perspective. Neuron 17, 1049-1055.