Ca2+–synaptotagmin directly regulates t-SNARE function during reconstituted membrane fusion
10.1038/nsmb1076
Crossref journal-article
Springer Science and Business Media LLC
Nature Structural & Molecular Biology (297)
Bibliography

Bhalla, A., Chicka, M. C., Tucker, W. C., & Chapman, E. R. (2006). Ca2+–synaptotagmin directly regulates t-SNARE function during reconstituted membrane fusion. Nature Structural & Molecular Biology, 13(4), 323–330.

Authors 4
  1. Akhil Bhalla (first)
  2. Michael C Chicka (additional)
  3. Ward C Tucker (additional)
  4. Edwin R Chapman (additional)
References 60 Referenced 157
  1. Rothman, J.E. Mechanisms of intracellular protein transport. Nature 372, 55–63 (1994). (10.1038/372055a0) / Nature by JE Rothman (1994)
  2. Chen, Y.A. & Scheller, R.H. SNARE-mediated membrane fusion. Nat. Rev. Mol. Cell Biol. 2, 98–106 (2001). (10.1038/35052017) / Nat. Rev. Mol. Cell Biol. by YA Chen (2001)
  3. Jahn, R. & Sudhof, T.C. Membrane fusion and exocytosis. Annu. Rev. Biochem. 68, 863–911 (1999). (10.1146/annurev.biochem.68.1.863) / Annu. Rev. Biochem. by R Jahn (1999)
  4. Sutton, R.B., Fasshauer, D., Jahn, R. & Brunger, A.T. Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 A resolution. Nature 395, 347–353 (1998). (10.1038/26412) / Nature by RB Sutton (1998)
  5. Poirier, M.A. et al. The synaptic SNARE complex is a parallel four-stranded helical bundle. Nat. Struct. Biol. 5, 765–769 (1998). (10.1038/1799) / Nat. Struct. Biol. by MA Poirier (1998)
  6. Lin, R.C. & Scheller, R.H. Structural organization of the synaptic exocytosis core complex. Neuron 19, 1087–1094 (1997). (10.1016/S0896-6273(00)80399-2) / Neuron by RC Lin (1997)
  7. Hanson, P.I., Roth, R., Morisaki, H., Jahn, R. & Heuser, J.E. Structure and conformational changes in NSF and its membrane receptor complexes visualized by quick-freeze/deep-etch electron microscopy. Cell 90, 523–535 (1997). (10.1016/S0092-8674(00)80512-7) / Cell by PI Hanson (1997)
  8. Weber, T. et al. SNAREpins: minimal machinery for membrane fusion. Cell 92, 759–772 (1998). (10.1016/S0092-8674(00)81404-X) / Cell by T Weber (1998)
  9. McNew, J.A., Weber, T., Engelman, D.M., Sollner, T.H. & Rothman, J.E. The length of the flexible SNAREpin juxtamembrane region is a critical determinant of SNARE-dependent fusion. Mol. Cell 4, 415–421 (1999). (10.1016/S1097-2765(00)80343-3) / Mol. Cell by JA McNew (1999)
  10. Fiebig, K.M., Rice, L.M., Pollock, E. & Brunger, A.T. Folding intermediates of SNARE complex assembly. Nat. Struct. Biol. 6, 117–123 (1999). (10.1038/5803) / Nat. Struct. Biol. by KM Fiebig (1999)
  11. Chen, Y.A., Scales, S.J. & Scheller, R.H. Sequential SNARE assembly underlies priming and triggering of exocytosis. Neuron 30, 161–170 (2001). (10.1016/S0896-6273(01)00270-7) / Neuron by YA Chen (2001)
  12. Melia, T.J. et al. Regulation of membrane fusion by the membrane-proximal coil of the t-SNARE during zippering of SNAREpins. J. Cell Biol. 158, 929–940 (2002). (10.1083/jcb.200112081) / J. Cell Biol. by TJ Melia (2002)
  13. Zhang, F., Chen, Y., Su, Z. & Shin, Y.K. SNARE assembly and membrane fusion, a kinetic analysis. J. Biol. Chem. 279, 38668–38672 (2004). (10.1074/jbc.M404904200) / J. Biol. Chem. by F Zhang (2004)
  14. McNew, J.A. et al. Compartmental specificity of cellular membrane fusion encoded in SNARE proteins. Nature 407, 153–159 (2000). (10.1038/35025000) / Nature by JA McNew (2000)
  15. Chen, Y.A., Scales, S.J., Patel, S.M., Doung, Y.C. & Scheller, R.H. SNARE complex formation is triggered by Ca2+ and drives membrane fusion. Cell 97, 165–174 (1999). (10.1016/S0092-8674(00)80727-8) / Cell by YA Chen (1999)
  16. Koh, T.W. & Bellen, H.J. Synaptotagmin I, a Ca2+ sensor for neurotransmitter release. Trends Neurosci. 26, 413–422 (2003). (10.1016/S0166-2236(03)00195-4) / Trends Neurosci. by TW Koh (2003)
  17. Chapman, E.R. Synaptotagmin: a Ca2+ sensor that triggers exocytosis? Nat. Rev. Mol. Cell Biol. 3, 498–508 (2002). (10.1038/nrm855) / Nat. Rev. Mol. Cell Biol. by ER Chapman (2002)
  18. Matthew, W.D., Tsavaler, L. & Reichardt, L.F. Identification of a synaptic vesicle-specific membrane protein with a wide distribution in neuronal and neurosecretory tissue. J. Cell Biol. 91, 257–269 (1981). (10.1083/jcb.91.1.257) / J. Cell Biol. by WD Matthew (1981)
  19. Perin, M.S., Fried, V.A., Mignery, G.A., Jahn, R. & Sudhof, T.C. Phospholipid binding by a synaptic vesicle protein homologous to the regulatory region of protein kinase C. Nature 345, 260–263 (1990). (10.1038/345260a0) / Nature by MS Perin (1990)
  20. Chapman, E.R. & Jahn, R. 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 (1994). (10.1016/S0021-9258(17)37523-3) / J. Biol. Chem. by ER Chapman (1994)
  21. Bennett, M.K., Calakos, N. & Scheller, R.H. Syntaxin: a synaptic protein implicated in docking of synaptic vesicles at presynaptic active zones. Science 257, 255–259 (1992). (10.1126/science.1321498) / Science by MK Bennett (1992)
  22. Sollner, T., Bennett, M.K., Whiteheart, S.W., Scheller, R.H. & Rothman, J.E. A protein assembly-disassembly pathway in vitro that may correspond to sequential steps of synaptic vesicle docking, activation, and fusion. Cell 75, 409–418 (1993). (10.1016/0092-8674(93)90376-2) / Cell by T Sollner (1993)
  23. Bai, J., Wang, C.T., Richards, D.A., Jackson, M.B. & Chapman, E.R. Fusion pore dynamics are regulated by synaptotagmin*t-SNARE interactions. Neuron 41, 929–942 (2004). (10.1016/S0896-6273(04)00117-5) / Neuron by J Bai (2004)
  24. Chapman, E.R., Hanson, P.I., An, S. & Jahn, R. Ca2+ regulates the interaction between synaptotagmin and syntaxin 1. J. Biol. Chem. 270, 23667–23671 (1995). (10.1074/jbc.270.40.23667) / J. Biol. Chem. by ER Chapman (1995)
  25. Schiavo, G., Stenbeck, G., Rothman, J.E. & Sollner, T.H. 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 (1997). (10.1073/pnas.94.3.997) / Proc. Natl. Acad. Sci. USA by G Schiavo (1997)
  26. Brose, N., Petrenko, A.G., Sudhof, T.C. & Jahn, R. Synaptotagmin: a calcium sensor on the synaptic vesicle surface. Science 256, 1021–1025 (1992). (10.1126/science.1589771) / Science by N Brose (1992)
  27. Bai, J., Tucker, W.C. & Chapman, E.R. PIP2 increases the speed-of-response of synaptotagmin and steers its membrane penetration activity toward the plasma membrane. Nat. Struct. Mol. Biol. 11, 36–44 (2004). (10.1038/nsmb709) / Nat. Struct. Mol. Biol. by J Bai (2004)
  28. Fernandez-Chacon, R. et al. Synaptotagmin I functions as a calcium regulator of release probability. Nature 410, 41–49 (2001). (10.1038/35065004) / Nature by R Fernandez-Chacon (2001)
  29. Sorensen, J.B., Fernandez-Chacon, R., Sudhof, T.C. & Neher, E. Examining synaptotagmin 1 function in dense core vesicle exocytosis under direct control of Ca2+. J. Gen. Physiol. 122, 265–276 (2003). (10.1085/jgp.200308855) / J. Gen. Physiol. by JB Sorensen (2003)
  30. Wang, P., Wang, C.T., Bai, J., Jackson, M.B. & Chapman, E.R. Mutations in the effector binding loops in the C2A and C2B domains of synaptotagmin I disrupt exocytosis in a non-additive manner. J. Biol. Chem. 278, 47030–47037 (2003). (10.1074/jbc.M306728200) / J. Biol. Chem. by P Wang (2003)
  31. Tucker, W.C., Weber, T. & Chapman, E.R. Reconstitution of Ca2+-regulated membrane fusion by synaptotagmin and SNAREs. Science 304, 435–438 (2004). (10.1126/science.1097196) / Science by WC Tucker (2004)
  32. Bhalla, A., Tucker, W.C. & Chapman, E.R. Synaptotagmin isoforms couple distinct ranges of Ca2+, Ba2+, and Sr2+ concentration to SNARE-mediated membrane fusion. Mol. Biol. Cell 16, 4755–4764 (2005). (10.1091/mbc.e05-04-0277) / Mol. Biol. Cell by A Bhalla (2005)
  33. Davis, A.F. et al. Kinetics of synaptotagmin responses to Ca2+ and assembly with the core SNARE complex onto membranes. Neuron 24, 363–376 (1999). (10.1016/S0896-6273(00)80850-8) / Neuron by AF Davis (1999)
  34. Bai, J., Wang, P. & Chapman, E.R. C2A activates a cryptic Ca2+-triggered membrane penetration activity within the C2B domain of synaptotagmin I. Proc. Natl. Acad. Sci. USA 99, 1665–1670 (2002). (10.1073/pnas.032541099) / Proc. Natl. Acad. Sci. USA by J Bai (2002)
  35. Wu, Y. et al. Visualization of synaptotagmin I oligomers assembled onto lipid monolayers. Proc. Natl. Acad. Sci. USA 100, 2082–2087 (2003). (10.1073/pnas.0435872100) / Proc. Natl. Acad. Sci. USA by Y Wu (2003)
  36. Brennwald, P. et al. Sec9 is a SNAP-25-like component of a yeast SNARE complex that may be the effector of Sec4 function in exocytosis. Cell 79, 245–258 (1994). (10.1016/0092-8674(94)90194-5) / Cell by P Brennwald (1994)
  37. Littleton, J.T. et al. synaptotagmin mutants reveal essential functions for the C2B domain in Ca2+-triggered fusion and recycling of synaptic vesicles in vivo. J. Neurosci. 21, 1421–1433 (2001). (10.1523/JNEUROSCI.21-05-01421.2001) / J. Neurosci. by JT Littleton (2001)
  38. Liu, T., Tucker, W.C., Bhalla, A., Chapman, E.R. & Weisshaar, J.C. SNARE-driven, 25-millisecond vesicle fusion in vitro. Biophys. J. 89, 2458–2472 (2005). (10.1529/biophysj.105.062539) / Biophys. J. by T Liu (2005)
  39. Quetglas, S. et al. Calmodulin and lipid binding to synaptobrevin regulates calcium-dependent exocytosis. EMBO J. 21, 3970–3979 (2002). (10.1093/emboj/cdf404) / EMBO J. by S Quetglas (2002)
  40. Hayashi, T. et al. Synaptic vesicle membrane fusion complex: action of clostridial neurotoxins on assembly. EMBO J. 13, 5051–5061 (1994). (10.1002/j.1460-2075.1994.tb06834.x) / EMBO J. by T Hayashi (1994)
  41. Fasshauer, D., Antonin, W., Subramaniam, V. & Jahn, R. SNARE assembly and disassembly exhibit a pronounced hysteresis. Nat. Struct. Biol. 9, 144–151 (2002). (10.1038/nsb750) / Nat. Struct. Biol. by D Fasshauer (2002)
  42. McIntyre, J.C. & Sleight, R.G. Fluorescence assay for phospholipid membrane asymmetry. Biochemistry 30, 11819–11827 (1991). (10.1021/bi00115a012) / Biochemistry by JC McIntyre (1991)
  43. Xu, Y., Zhang, F., Su, Z., McNew, J.A. & Shin, Y.K. Hemifusion in SNARE-mediated membrane fusion. Nat. Struct. Mol. Biol. 12, 417–422 (2005). (10.1038/nsmb921) / Nat. Struct. Mol. Biol. by Y Xu (2005)
  44. Boon, J.M., Shukla, R., Smith, B.D., Licini, G. & Scrimin, P. Selective phosphatidylethanolamine translocation across vesicle membranes using synthetic translocases. Chem. Commun. (Camb.) 260–261 (2002). (10.1039/b110357c)
  45. Matsuzaki, K., Yoneyama, S. & Miyajima, K. Pore formation and translocation of melittin. Biophys. J. 73, 831–838 (1997). (10.1016/S0006-3495(97)78115-3) / Biophys. J. by K Matsuzaki (1997)
  46. Katz, B. The release of neural transmitter substances (Thomas, Springfield, Illinois, USA, 1969). / The release of neural transmitter substances by B Katz (1969)
  47. Zhang, X., Kim-Miller, M.J., Fukuda, M., Kowalchyk, J.A. & Martin, T.F. Ca2+-dependent synaptotagmin binding to SNAP-25 is essential for Ca2+-triggered exocytosis. Neuron 34, 599–611 (2002). (10.1016/S0896-6273(02)00671-2) / Neuron by X Zhang (2002)
  48. Shin, O.H., Maximov, A., Lim, B.K., Rizo, J. & Sudhof, T.C. Unexpected Ca2+-binding properties of synaptotagmin 9. Proc. Natl. Acad. Sci. USA 101, 2554–2559 (2004). (10.1073/pnas.0308477100) / Proc. Natl. Acad. Sci. USA by OH Shin (2004)
  49. Shin, O.H. et al. Sr2+ binding to the Ca2+ binding site of the synaptotagmin 1 C2B domain triggers fast exocytosis without stimulating SNARE interactions. Neuron 37, 99–108 (2003). (10.1016/S0896-6273(02)01145-5) / Neuron by OH Shin (2003)
  50. Lu, X., Zhang, F., McNew, J.A. & Shin, Y.K. Membrane fusion induced by neuronal SNAREs transits through hemifusion. J. Biol. Chem. 280, 30538–30541 (2005). (10.1074/jbc.M506862200) / J. Biol. Chem. by X Lu (2005)
  51. Giraudo, C.G. et al. SNAREs can promote complete fusion and hemifusion as alternative outcomes. J. Cell Biol. 170, 249–260 (2005). (10.1083/jcb.200501093) / J. Cell Biol. by CG Giraudo (2005)
  52. Reese, C., Heise, F. & Mayer, A. Trans-SNARE pairing can precede a hemifusion intermediate in intracellular membrane fusion. Nature 436, 410–414 (2005). (10.1038/nature03722) / Nature by C Reese (2005)
  53. Pevsner, J. et al. Specificity and regulation of a synaptic vesicle docking complex. Neuron 13, 353–361 (1994). (10.1016/0896-6273(94)90352-2) / Neuron by J Pevsner (1994)
  54. Wang, C.T., Bai, J., Chang, P.Y., Chapman, E.R. & Jackson, M.B. Synaptotagmin-Ca2+ triggers two sequential steps in regulated exocytosis in rat PC12 cells: fusion pore opening and fusion pore dilation. J. Physiol. (Lond.) 570, 295–307 (2006). (10.1113/jphysiol.2005.097378) / J. Physiol. (Lond.) by CT Wang (2006)
  55. Wang, C.T. et al. Different domains of synaptotagmin control the choice between kiss-and-run and full fusion. Nature 424, 943–947 (2003). (10.1038/nature01857) / Nature by CT Wang (2003)
  56. Wang, C.T. et al. Synaptotagmin modulation of fusion pore kinetics in regulated exocytosis of dense-core vesicles. Science 294, 1111–1115 (2001). (10.1126/science.1064002) / Science by CT Wang (2001)
  57. Han, X., Wang, C.T., Bai, J., Chapman, E.R. & Jackson, M.B. Transmembrane segments of syntaxin line the fusion pore of Ca2+-triggered exocytosis. Science 304, 289–292 (2004). (10.1126/science.1095801) / Science by X Han (2004)
  58. Desai, R.C. et al. The C2B domain of synaptotagmin is a Ca2+-sensing module essential for exocytosis. J. Cell Biol. 150, 1125–1136 (2000). (10.1083/jcb.150.5.1125) / J. Cell Biol. by RC Desai (2000)
  59. Chapman, E.R., An, S., Edwardson, J.M. & Jahn, R. A novel function for the second C2 domain of synaptotagmin. Ca2+-triggered dimerization. J. Biol. Chem. 271, 5844–5849 (1996). (10.1074/jbc.271.10.5844) / J. Biol. Chem. by ER Chapman (1996)
  60. Bark, I.C. & Wilson, M.C. Human cDNA clones encoding two different isoforms of the nerve terminal protein SNAP-25. Gene 139, 291–292 (1994). (10.1016/0378-1119(94)90773-0) / Gene by IC Bark (1994)
Dates
Type When
Created 19 years, 5 months ago (March 26, 2006, 2:14 p.m.)
Deposited 2 years, 3 months ago (May 19, 2023, 12:48 a.m.)
Indexed 2 months, 3 weeks ago (June 12, 2025, 4:04 p.m.)
Issued 19 years, 5 months ago (March 26, 2006)
Published 19 years, 5 months ago (March 26, 2006)
Published Online 19 years, 5 months ago (March 26, 2006)
Published Print 19 years, 5 months ago (April 1, 2006)
Funders 0

None

@article{Bhalla_2006, title={Ca2+–synaptotagmin directly regulates t-SNARE function during reconstituted membrane fusion}, volume={13}, ISSN={1545-9985}, url={http://dx.doi.org/10.1038/nsmb1076}, DOI={10.1038/nsmb1076}, number={4}, journal={Nature Structural & Molecular Biology}, publisher={Springer Science and Business Media LLC}, author={Bhalla, Akhil and Chicka, Michael C and Tucker, Ward C and Chapman, Edwin R}, year={2006}, month=mar, pages={323–330} }