Regulation of exocytosis and fusion pores by synaptotagmin-effector interactions

Molecular Biology of the Cell

Volumn 21, Issue 16, 2010, Pages 2821-2831

  Zhang, Zhen ^a   Hui, Enfu ^b   Chapman, Edwin R ^c   Jackson, Meyer B ^c  

^a NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; ISOPROTEIN; LIPOSOME; PHOSPHATIDYLSERINE; SNARE PROTEIN; SYNAPTOTAGMIN I;

ARTICLE; CELL MEMBRANE; CELL STRAIN; EXOCYTOSIS; GENE OVEREXPRESSION; NORADRENALIN RELEASE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE;

AMINO ACID SUBSTITUTION; ANIMALS; BLOTTING, WESTERN; CALCIUM; ELECTROCHEMICAL TECHNIQUES; EXOCYTOSIS; KINETICS; LIPID BILAYERS; MEMBRANE FUSION; MUTATION; PC12 CELLS; PHOSPHATIDYLSERINES; PROTEIN BINDING; PROTEIN ISOFORMS; RATS; SNARE PROTEINS; SYNAPTOTAGMIN I; SYNAPTOTAGMINS;

EID: 77955638309     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E10-04-0285     Document Type: Article

References (42)

1. Ahras, M., Otto, G. P., and Tooze, S. A. (2006). Synaptotagmin IV is necessary for the maturation of secretory granules in PC12 cells. J. Cell Biol. 173, 242-251.
2. Augustine, G. J. (2001). How does calcium trigger neurotransmitter release? Curr. Opin. Neurobiol. 11, 320-326.
3. Bai, J., Wang, C. T., Richards, D. A., Jackson, M. B., and Chapman, E. R. (2004). Fusion pore dynamics are regulated by synaptotagmin*t-SNARE interactions. Neuron 41, 929-942. (Pubitemid 38429736)
4. Bennett, M. K., Calakos, N., and Scheller, R. H. (1992). Syntaxin: a synaptic protein implicated in docking of synaptic vesicles at presynaptic active zones. Science 257, 255-259.
5. Bhalla, A., Chicka, M. C., and Chapman, E. R. (2008). Analysis of the synaptotagmin family during reconstituted membrane fusion. Uncovering a class of inhibitory isoforms. J. Biol. Chem. 283, 21799-21807.
6. Bhalla, A., Chicka, M. C., Tucker, W. C., and Chapman, E. R. (2006). Ca(2+)-synaptotagmin directly regulates t-SNARE function during reconstituted membrane fusion. Nat. Struct. Mol. Biol. 13, 323-330.
7. Bhalla, A., Tucker, W. C., and Chapman, E. R. (2005). Synaptotagmin isoforms couple distinct ranges of Ca2+, Ba2+, and Sr2+ concentration to SNARE-mediated membrane fusion. Mol. Biol. Cell 16, 4755-4764.
8. Brose, N., Petrenko, A. G., Sudhof, T. C., and Jahn, R. (1992). Synaptotagmin: a calcium sensor on the synaptic vesicle surface. Science 256, 1021-1025.
9. Brunger, A. T. (2005). Structure and function of SNARE and SNARE-interacting proteins. Q. Rev. Biophys. 38, 1-47.
10. Chapman, E. R. (2008). How does synaptotagmin trigger neurotransmitter release? Annu. Rev. Biochem. 77, 615-641.
11. Chapman, E. R., and Jahn, R. (1994). Calcium-dependent interaction of the cytoplasmic region of synaptotagmin with membranes. Autonomous function of a single C2-homologous domain. J. Biol. Chem. 269, 5735-5741.
12. Chow, R. H., and von Rüden, L. (1995). Electrochemical detection of secretion from single cells. In: Single-Channel Recording, eds. B. Sakmann, Neher, E., New York: Plenum Press, 245-275.
13. Craxton, M. (2007). Evolutionary genomics of plant genes encoding N-terminal-TM-C2 domain proteins and the similar FAM62 genes and synaptotagmin genes of metazoans. BMC Genomics 8, 259.
14. Davletov, B. A., and Sudhof, T. C. (1993). A single C2 domain from synaptotagmin I is sufficient for high affinity Ca2+/phospholipid binding. J. Biol. Chem. 268, 26386-26390.
15. Fernandez-Chacon, R., Konigstorfer, A., Gerber, S. H., Garcia, J., Matos, M. F., Stevens, C. F., Brose, N., Rizo, J., Rosenmund, C., and Sudhof, T. C. (2001). Synaptotagmin I functions as a calcium regulator of release probability. Nature 410, 41-49. (Pubitemid 32225830)
16. Fernandez-Chacon, R., Shin, O. H., Konigstorfer, A., Matos, M. F., Meyer, A. C., Garcia, J., Gerber, S. H., Rizo, J., Sudhof, T. C., and Rosenmund, C. (2002). Structure/function analysis of Ca2+ binding to the C2A domain of synaptotagmin 1. J. Neurosci. 22, 8438-8446.
17. Fernandez, I., Arac, D., Ubach, J., Gerber, S. H., Shin, O., Gao, Y., Anderson, R. G., Sudhof, T. C., and Rizo, J. (2001). Three-dimensional structure of the synaptotagmin 1 C2B-domain: synaptotagmin 1 as a phospholipid binding machine. Neuron 32, 1057-1069.
18. Fukuda, M., Kanno, E., Satoh, M., Saegusa, C., and Yamamoto, A. (2004). Synaptotagmin VII is targeted to dense-core vesicles and regulates their Ca2+ -dependent exocytosis in PC12 cells. J. Biol. Chem. 279, 52677-52684.
19. Gaffaney, J. D., Dunning, F. M., Wang, Z., Hui, E., and Chapman, E. R. (2008). Synaptotagmin C2B domain regulates Ca2+-triggered fusion in vitro: critical residues revealed by scanning alanine mutagenesis. J. Biol. Chem. 283, 31763-31775.
20. Hui, E., Bai, J., Wang, P., Sugimori, M., Llinas, R. R., and Chapman, E. R. (2005). Three distinct kinetic groupings of the synaptotagmin family: candidate sensors for rapid and delayed exocytosis. Proc. Natl. Acad. Sci. USA. 102, 5210-5214.
21. Hui, E., Johnson, C. P., Yao, J., Dunning, F. M., and Chapman, E. R. (2009). Synaptotagmin-mediated bending of the target membrane is a critical step in Ca(2+)-regulated fusion. Cell 138, 709-721.
22. Koh, T. W., and Bellen, H. J. (2003). Synaptotagmin I, a Ca2+ sensor for neurotransmitter release. Trends Neurosci. 26, 413-422.
23. Lynch, K. L., Gerona, R. R., Kielar, D. M., Martens, S., McMahon, H. T., and Martin, T. F. (2008). Synaptotagmin-1 utilizes membrane bending and SNARE binding to drive fusion pore expansion. Mol. Biol. Cell 19, 5093-5103.
24. Mackler, J. M., Drummond, J. A., Loewen, C. A., Robinson, I. M., and Reist, N. E. (2002). The C(2)B Ca(2+)-binding motif of synaptotagmin is required for synaptic transmission in vivo. Nature 418, 340-344.
25. Martens, S., Kozlov, M. M., and McMahon, H. T. (2007). How synaptotagmin promotes membrane fusion. Science 316, 1205-1208.
26. Nagy, G., Kim, J. H., Pang, Z. P., Matti, U., Rettig, J., Sudhof, T. C., and Sorensen, J. B. (2006). Different effects on fast exocytosis induced by synaptotagmin 1 and 2 isoforms and abundance but not by phosphorylation. J. Neurosci. 26, 632-643.
27. Nishiki, T., and Augustine, G. J. (2004). Dual roles of the C2B domain of synaptotagmin I in synchronizing Ca2+-dependent neurotransmitter release. J. Neurosci. 24, 8542-8550.
28. Pang, Z. P., Shin, O. H., Meyer, A. C., Rosenmund, C., and Sudhof, T. C. (2006). A gain-of-function mutation in synaptotagmin-1 reveals a critical role of Ca2+-dependent soluble N-ethylmaleimide-sensitive factor attachment protein receptor complex binding in synaptic exocytosis. J. Neurosci. 26, 12556-12565.
29. Rhee, J. S., Li, L. Y., Shin, O. H., Rah, J. C., Rizo, J., Sudhof, T. C., and Rosenmund, C. (2005). Augmenting neurotransmitter release by enhancing the apparent Ca2+ affinity of synaptotagmin 1. Proc. Natl. Acad. Sci. USA. 102, 18664-18669.
30. Shao, X., Davletov, B. A., Sutton, R. B., Sudhof, T. C., and Rizo, J. (1996). Bipartite Ca2+-binding motif in C2 domains of synaptotagmin and protein kinase C. Science 273, 248-251.
31. Shao, X., Fernandez, I., Sudhof, T. C., and Rizo, J. (1998). Solution structures of the Ca2+-free and Ca2+-bound C2A domain of synaptotagmin I: does Ca2+ induce a conformational change? Biochemistry 37, 16106-16115.
32. Stevens, C. F., and Sullivan, J. M. (2003). The synaptotagmin C2A domain is part of the calcium sensor controlling fast synaptic transmission. Neuron 39, 299-308.
33. Travis, E. R., and Wightman, R. M. (1998). Spatio-temporal resolution of exocytosis from individual cells. Annu. Rev. Biophys. Biomol. Struct. 27, 77-103.
34. Tucker, W. C., Edwardson, J. M., Bai, J., Kim, H. J., Martin, T. F., and Chapman, E. R. (2003). Identification of synaptotagmin effectors via acute inhibition of secretion from cracked PC12 cells. J. Cell Biol. 162, 199-209.
35. 2+-regulated membrane fusion by synaptotagmin and SNAREs. Science 304, 435-438.
36. 2+ triggers two sequential steps in regulated exocytosis in rat PC12 cells: fusion pore opening and fusion pore dilation. J. Physiol. 570, 295-307.
37. Wang, C. T., Grishanin, R., Earles, C. A., Chang, P. Y., Martin, T. F., Chapman, E. R., and Jackson, M. B. (2001). Synaptotagmin modulation of fusion pore kinetics in regulated exocytosis of dense-core vesicles. Science 294, 1111-1115.
38. Wang, P., Wang, C. T., Bai, J., Jackson, M. B., and Chapman, E. R. (2003). Mutations in the effector binding loops in the C2A and C2B domains of synaptotagmin I disrupt exocytosis in a nonadditive manner. J. Biol. Chem. 278, 47030-47037.
39. 2+-triggered exocytosis and fusion pores in PC12 cells. Mol. Biol. Cell 20, 5086-5095.
40. Zhang, Z., and Jackson, M. B. (2008). Temperature dependence of fusion kinetics and fusion pores in Ca2+-triggered exocytosis from PC12 cells. J. Gen. Physiol. 131, 117-124.
41. Zhang, Z., and Jackson, M. B. (2010). Membrane bending energy and fusion pore kinetics in Ca2+-triggered exocytosis. Biophys. J. 98, 2524-2534.
42. Zhang, Z., Zhang, Z., and Jackson, M. B. (2010). Synaptotagmin IV modulation of vesicle size and fusion pores in PC12. Biophys. J. 98, 968-978.