High Metal Concentrations Are Required for Self-Association of Synaptotagmin II

Biophysical Journal

Volumn 86, Issue 4, 2004, Pages 2455-2466

  García, Ricardo A ^a   Godwin, Hilary Arnold ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BARIUM; CALCIUM; LEAD; MAGNESIUM; METAL; METAL ION; NEUROTRANSMITTER; PROTEIN; STRONTIUM; SYNAPTOTAGMIN; SYNAPTOTAGMIN II; UNCLASSIFIED DRUG;

ARTICLE; DIMERIZATION; NEUROTRANSMISSION; PROTEIN CONFORMATION; PROTEIN DEGRADATION; SYNAPSE VESICLE;

EID: 1942423171     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(04)74302-7     Document Type: Article

References (73)

1. Bai, J., C. A. Earles, J. L. Lewis, and E. R. Chapman. 2000. Membrane-embedded synaptotagmin penetrates cis or trans target membranes and clusters via a novel mechanism. J. Biol. Chem. 275:25427-25435.
2. Bollmann, J. H., B. Sakmann, and J. G. Borst. 2000. Calcium sensitivity of glutamate release in a calyx-type terminal. Science. 289:953-957.
3. Bouton, C. M., L. P. Frelin, C. E. Forde, H. A. Godwin, and J. Pevsner. 2001. Synaptotagmin is a molecular target for lead. J. Neurochem. 76:1724-1735.
4. Brose, N., A. G. Petrenko, T. C. Sudhof, and R. Jahn. 1992. Synaptotagmin: a calcium sensor on the synaptic vesicle surface. Science. 256:1021-1025.
5. 2+-dependent exocytosis. Curr. Opin. Neurobiol. 10:293-302.
6. Chae, Y. K., F. Abildgaard, E. R. Chapman, and J. L. Markley. 1998. Lipid binding ridge on loops 2 and 3 of the C2A domain of synaptotagmin I as revealed by NMR spectroscopy. J. Biol. Chem. 273:25659-25663.
7. Chapman, E. R., S. An, J. M. Edwardson, and R. Jahn. 1996. A novel function for the second C2 domain of synaptotagmin. J. Biol. Chem. 271:5844-5849.
8. Chapman, E. R., R. C. Desai, A. F. Davis, and C. K. Tomehl. 1998. Delineation of the oligomerization, AP-2 binding, and synprint binding region of the C2B domain of synaptotagmin. J. Biol. Chem. 273:32966-32972.
9. 2+ regulates the interaction between synaptotagmin and syntaxin 1. J. Biol. Chem. 270:23667-23671.
10. Chapman, E. R., and R. Jahn. 1994. Calcium-dependent interaction of the cytoplasmic region of synaptotagmin with membranes. J. Biol. Chem. 269:5735-5741.
11. Damer, S. K., and C. E. Creutz. 1996. Calcium-dependent self-association of synaptotagmin I. J. Neurochem. 67:1661-1668.
12. Davis, A. F., J. Bai, D. Fasshauer, M. J. Wolowick, J. L. Lewis, and E. R. Chapman. 1999. Kinetics of synaptotagmin responses to Ca2+ and assembly with the core SNARE complex onto membranes. Neuron. 24:363-376. (Published erratum appears in Neuron 1999 24:1049).
13. Davis, A. F., J. Bai, D. Fasshauer, M. J. Wolowick, J. L. Lewis, and E. R. Chapman. 1999. Kinetics of synaptotagmin responses to Ca2+ and assembly with the core SNARE complex onto membranes. Neuron. 24:363-376. (Published erratum appears in Neuron 1999 24:1049).
14. Davletov, B., O. Perisic, and R. L. Williams. 1998. Calcium-dependent membrane penetration is a hallmark of the C2 domain of cytosolic phospholipase A2 whereas the C2A domain of synaptotagmin binds membranes electrostatically. J. Biol. Chem. 273:19093-19096.
15. Davletov, B., J. M. Sontag, Y. Hata, A. G. Petrenko, E. M. Fykse, R. Jahn, and T. C. Sudhof. 1993. Phosphorylation of synaptotagmin I by casein kinase II. J. Biol. Chem. 268:6816-6822.
16. 2+/phospholipid binding. J. Biol. Chem. 268:26386-26390.
17. 2+-dependent conformational change in synaptotagmin I. J. Biol. Chem. 269:28547-28550.
18. 2+-sensing module essential for exocytosis. J. Cell Biol. 150:1125-1135.
19. Edstrom, R. D., M. H. Meinke, X. Yang, R. Yang, V. Elings, and D. F. Evans. 1990. Direct visualization of phosphorylase-phosphorylase kinase complexes by scanning tunneling and atomic force microscopy. Biophys. J. 58:1437-1448.
20. Elferink, L. A., W. S. Trimble, and R. H. Scheller. 1989. Two vesicle-associated membrane protein genes are differentially expressed in the rat central nervous system. J. Biol. Chem. 264:11061-11064.
21. Felmy, F., E. Neher, and R. Schneggenburger. 2003. Probing the intracellular calcium sensitivity of transmitter release during synaptic facilitation. Neuron. 37:801-811.
22. Fernandez, I., D. Arac, J. Ubach, S. H. Gerber, O. Shin, Y. Gao, R. G. Anderson, T. C. Sudhof, and J. Rizo. 2001. Three-dimensional structure of the synaptotagmin 1 C2B-domain: synaptotagmin 1 as a phospholipid binding machine. Neuron. 32:1057-1069.
23. Fernandez-Chacon, R., A. Konigstorfer, S. H. Gerber, J. García, M. F. Matos, C. F. Stevens, N. Brose, J. Rizo, C. Rosenmund, and T. C. Sudhof. 2001. Synaptotagmin I functions as a calcium regulator of release probability. Nature. 410:41-49.
24. Fon, E. A., and R. H. Edwards. 2001. Molecular mechanisms of neurotransmitter release. Muscle Nerve. 24:581-601.
25. Fukuda, M. 2003a. Molecular cloning and characterization of human, rat, and mouse synaptotagmin XV. Biochem. Biophys. Res. Commun. 306:64-71.
26. Fukuda, M. 2003b. Molecular cloning, expression, and characterization of a novel class of synaptotagmin (Syt XIV) conserved from Drosophila to humans. J. Biochem. 133:641-649.
27. Fukuda, M., E. Kanno, and K. Mikoshiba. 1999. Conserved N-terminal cysteine motif is essential for homo- and heterodimer formation of synaptotagmins III, V, VI, and X. J. Biol. Chem. 274:31421-31427.
28. Fukuda, M., and K. Mikoshiba. 2000a. Calcium-dependent and -independent hetero-oligomerization in the synaptotagmin family. J. Biochem. 128:637-645.
29. Fukuda, M., and K. Mikoshiba. 2000b. Distinct self-oligomerization activities of synaptotagmin family. J. Biol. Chem. 275:28180-28185.
30. Fukuda, M., and K. Mikoshiba. 2000c. Genomic structures of synaptotagmin II protein: comparison of exon-intron organization of the synaptotagmin gene family. Biochem. Biophys. Res. Commun. 270:528-532.
31. Fukuda, M., and K. Mikoshiba. 2001. Mechanism of the calcium-dependent multimerization of synaptotagmin VII mediated by its first and second C2 domains. J. Biol. Chem. 276:27670-27676.
32. 6 DNA methyltransferases requires different deformations of DNA. Proc. Natl. Acad. Sci. USA. 93:7618-7622.
33. García, R. A., C. E. Forde, and H. A. Godwin. 2000. Calcium triggers an intramolecular association of the C2 domains in synaptotagmin. Proc. Natl. Acad. Sci. USA. 97:5883-5888.
34. 2+ sensor for transmitter release at a central synapse. Cell. 79:717-727.
35. 2+-dependent binding of synaptotagmin to SNARE complexes. J. Biol. Chem. 275:6328-6336.
36. Kee, Y., and R. H. Scheller. 1996. Localization of synaptotagmin-binding domains on syntaxin. J. Neurosci. 16:1975-1981.
37. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:680-685.
38. Leveque, C., J. A. Boudier, M. Takahashi, and M. Seagar. 2000. Calcium-dependent dissociation of synaptotagmin from synaptic SNARE complexes. J. Neurochem. 74:367-374.
39. 2+ binding properties of synaptotagmins. J. Biol. Chem. 270:24898-24902.
40. 2+-dependent and -independent activities of neural and non-neural synaptotagmins. Nature. 375:594-599.
41. Lin, R. C., and R. H. Scheller. 2000. Mechanisms of synaptic vesicle exocytosis. Ann. Rev. Cell Dev. Biol. 16:19-49.
42. 2+-triggered fusion and recycling of synaptic vesicles in vivo. J. Neurosci. 21:1421-1433.
43. Littleton, J. T., T. L. Serano, G. M. Rubin, B. Ganetzky, and E. R. Chapman. 1999. Synaptic function modulated by changes in the ratio of synaptotagmin I and IV. Nature. 400:757-760.
44. Manalis, R. S., G. P. Cooper, and S. L. Pomeroy. 1984. Effects of lead on neuromuscular transmission in the frog. Brain Res. 294:95-109.
45. Matos, M. F., J. Rizo, and T. C. Sudhof. 2000. The relation of protein binding to function: what is the significance of munc18 and synaptotagmin binding to syntaxin 1, and where are the corresponding binding sites? Eur. J. Cell Biol. 79:377-382.
46. Misura, K. M. S., A. P. May, and W. I. Wiess. 2000. Protein-protein interactions in intracellular membrane fusion. Curr. Opin. Struct. Biol. 10:662-671.
47. Mochida, S. 2000. Protein-protein interactions in neurotransmitter release. Neurosci. Res. 36:175-182.
48. Mochly-Rosen, D., K. G. Miller, R. H. Scheller, H. Khaner, J. Lopez, and B. Smith. 1992. p65 fragments, homologous to the C2 region of protein kinase C, bind to the intracellular receptors for protein kinase C. Biochemistry. 31:8120-8124.
49. Nalefski, E. A., and J. J. Falke. 1996. The C2 domain calcium-binding motif: structural and functional diversity. Protein Sci. 5:2375-2390.
50. Osborne, S. L., J. Herreros, P. I. Bastiaens, and G. Schiavo. 1999. Calcium-dependent oligomerization of synaptotagmins I and II. Synaptotagmins I and II are localized on the same synaptic vesicle and heterodimerize in the presence of calcium. J. Biol. Chem. 274:59-66.
51. Perin, M. S., V. A. Fried, G. A. Mignery, R. Jahn, and T. C. Sudhof. 1990. Phospholipid binding by a synaptic vesicle protein homologous to the regulatory region of protein kinase C. Nature. 345:260-263.
52. Reist, N. E., J. Buchanan, J. Li, A. DiAntonio, E. M. Buxton, and T. L. Schwarz. 1998. Morphologically docked synaptic vesicles are reduced in synaptotagmin mutants of Drosophila. J. Neurosci. 18:7662-7673.
53. 2+-binding domain. J. Biol. Chem. 273:15879-15882.
54. Schiavo, G., Q. M. Gu, G. D. Prestwich, T. H. Sollner, and J. E. Rothman. 1996. Calcium-dependent switching of the specificity of phosphoinositide binding to synaptotagmin. Proc. Natl. Acad. Sci. USA. 93:13327-13332.
55. Schiavo, G., S. L. Osborne, and J. G. Sgouros. 1998. Synaptotagmins: more isoforms than functions? Biochem. Biophys. Res. Commun. 248:1-8.
56. Schneggenburger, R., and E. Neher. 2000. Intracellular calcium dependence of transmitter release rates at a fast central synapse. Nature. 406:889-893.
57. Schneider, S. W., J. Larmer, R. M. Henderson, and H. Oberleithner. 1998. Molecular weights of individual proteins correlate with molecular volumes measured by atomic force microscopy. Pfluegers Arch. Eur. J. Physiol. 435:362-367.
58. Sehgal, B. U., R. Dunn, L. Hicke, and H. A. Godwin. 2000. High-yield expression and purification of recombinant proteins in bacteria: a versatile vector for glutathione S-transferase fusion proteins containing two protease cleavage sites. Anal. Biochem. 281:232-234.
59. 2+-dependent electrostatic switch. Neuron. 18:133-142.
60. Shin, O. H., J. Rizo, and T. C. Sudhof. 2002. Synaptotagmin function in dense core vesicle exocytosis studied in cracked PC12 cells. Nat. Neurosci. 5:649-656.
61. Smith, S. J., and G. J. Augustine. 1988. Calcium ions, active zones, and synaptic transmitter release. Trends Neurosci. 11:458-464.
62. Sudhof, T. C. 2002. Synaptotagmins: why so many? J. Biol. Chem. 277:7629-7632.
63. 2+-dependent properties of the first and second C2-domains of synaptotagmin I. J. Biol. Chem. 271:1262-1265.
64. 2+ affinities. EMBO J. 21:270-280.
65. 2+-dependent protein interactions mediated by the C(2)A domains of synaptotagmins. Biochemistry. 39:2940-2949.
66. 2+/phospholipid-binding fold. Cell. 80:929-938.
67. +2-independent snare complex interaction. J. Cell Biol. 147:589-598.
68. Trommershèauser, J., R. Schneggenburger, A. Zippelius, and E. Neher. 2003. Heterogeneous presynaptic release probabilities: functional relevance for short-term plasticity. Biophys. J. 84:1563-1579.
69. Verona, M., S. Zanotti, T. Schafer, G. Racagni, and M. Popoli, 2000. Changes of synaptotagmin interaction with t-SNARE proteins in vitro after calcium/calmodulin-dependent phosphorylation, J. Neurochem. 74:209-221.
70. von Poser, C., and T. C. Sudhof. 2001. Synaptotagmin 13: structure and expression of a novel synaptotagmin. Eur. J. Cell Biol. 80:41-47.
71. von Poser, C., J. Z. Zhang, C. Mineo, W. Ding, Y. Ying, T. C. Sudhof, and R. G. W. Anderson. 2000. Synaptotagmin regulation of coated pit assembly. J. Biol. Chem. 275:30916-30924.
72. Zhang, J. Z., B. A. Davletov, T. C. Sudhof, and R. G. Anderson. 1994. Synaptotagmin I is a high affinity receptor for clathrin AP-2: implications for membrane recycling. Cell. 78:751-760.
73. Zhang, X., J. Rizo, and T. C. Sudhof. 1998. Mechanism of phospholipid binding by the C2A-domain of synaptotagmin I. Biochemistry. 37:12395-12403.