Controlling synaptotagmin activity by electrostatic screening

Nature Structural and Molecular Biology

Volumn 19, Issue 10, 2012, Pages 991-999

  Park, Yongsoo ^a   Hernandez, Javier M ^a   Van Den Bogaart, Geert ^a   Ahmed, Saheeb ^a   Holt, Matthew ^a   Riedel, Dietmar ^a   Jahn, Reinhard ^a  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALCIUM ION; LIPOSOME; NUCLEOTIDE; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; PYROPHOSPHATE; SNARE PROTEIN; SYNAPTOTAGMIN; SYNAPTOTAGMIN I;

ARTICLE; CHROMAFFIN GRANULE; COW; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; STATIC ELECTRICITY;

ADENOSINE TRIPHOSPHATE; ANIMALS; CALCIUM; CATTLE; CHROMAFFIN GRANULES; EXOCYTOSIS; LIPOSOMES; MEMBRANE FUSION; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; PHOSPHOLIPIDS; POLYPHOSPHATES; RATS; SNARE PROTEINS; STATIC ELECTRICITY; SYNAPTOSOMAL-ASSOCIATED PROTEIN 25; SYNAPTOTAGMIN I; SYNTAXIN 1;

BOVINAE;

EID: 84867230114     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2375     Document Type: Article

References (53)

1. Augustine, G.J. How does calcium trigger neurotransmitter release? Curr. Opin. Neurobiol. 11, 320-326 (2001).
2. De Camilli, P. & Jahn, R. Pathways to regulated exocytosis in neurons. Annu. Rev. Physiol. 52, 625-645 (1990).
3. Park, Y. & Kim, K.T. Short-term plasticity of small synaptic vesicle (SSV) and large large dense-core vesicle (LDCV) exocytosis. Cell. Signal. 21, 1465-1470 (2009).
4. Neher, E. Vesicle pools and Ca2+ microdomains: new tools for understanding their roles in neurotransmitter release. Neuron 20, 389-399 (1998).
5. Neher, E. A comparison between exocytic control mechanisms in adrenal chromaffin cells and a glutamatergic synapse. Pflugers Arch. 453, 261-268 (2006).
6. Jahn, R. & Scheller, R.H. SNAREs-engines for membrane fusion. Nat. Rev. Mol. Cell Biol. 7, 631-643 (2006).
7. Martens, S. & McMahon, H.T. Mechanisms of membrane fusion: disparate players and common principles. Nat. Rev. Mol. Cell Biol. 9, 543-556 (2008).
8. Martin, T.F. The molecular machinery for fast and slow neurosecretion. Curr. Opin. Neurobiol. 4, 626-632 (1994).
9. Rizo, J. & Rosenmund, C. Synaptic vesicle fusion. Nat. Struct. Mol. Biol. 15, 665-674 (2008).
10. Malsam, J., Kreye, S. & Sollner, T.H. Membrane fusion: SNAREs and regulation. Cell. Mol. Life Sci. 65, 2814-2832 (2008).
11. Südhof, T.C. & Rothman, J.E. Membrane fusion: grappling with SNARE and SM proteins. Science 323, 474-477 (2009).
12. Stein, A., Weber, G., Wahl, M.C. & Jahn, R. Helical extension of the neuronal SNARE complex into the membrane. Nature 460, 525-528 (2009).
13. Wiederhold, K. & Fasshauer, D. Is assembly of the SNARE complex enough to fuel membrane fusion? J. Biol. Chem. 284, 13143-13152 (2009).
14. Fernandez, I. et al. Three-dimensional structure of the synaptotagmin 1 C2B-domain: synaptotagmin-1 as a phospholipid binding machine. Neuron 32, 1057-1069 (2001).
15. Chapman, E.R. How does synaptotagmin trigger neurotransmitter release? Annu. Rev. Biochem. 77, 615-641 (2008).
16. Stein, A., Radhakrishnan, A., Riedel, D., Fasshauer, D. & Jahn, R. Synaptotagmin activates membrane fusion through a Ca2+-dependent trans interaction with phospholipids. Nat. Struct. Mol. Biol. 14, 904-911 (2007).
17. Vennekate, W. et al. Cis-and trans-membrane interactions of synaptotagmin-1. Proc. Natl. Acad. Sci. USA 109, 11037-11042 (2012).
18. Takamori, S. et al. Molecular anatomy of a trafficking organelle. Cell 127, 831-846 (2006).
19. Holt, M., Riedel, D., Stein, A., Schuette, C. & Jahn, R. Synaptic vesicles are constitutively active fusion machines that function independently of Ca2+. Curr. Biol. 18, 715-722 (2008).
20. Mahal, L.K., Sequeira, S.M., Gureasko, J.M. & Sollner, T.H. Calcium-independent stimulation of membrane fusion and SNAREpin formation by synaptotagmin 1. J. Cell Biol. 158, 273-282 (2002).
21. Eaton, B.A., Haugwitz, M., Lau, D. & Moore, H.P. Biogenesis of regulated exocytotic carriers in neuroendocrine cells. J. Neurosci. 20, 7334-7344 (2000).
22. Grabner, C.P., Price, S.D., Lysakowski, A. & Fox, A.P. Mouse chromaffin cells have two populations of dense-core vesicles. J. Neurophysiol. 94, 2093-2104 (2005).
23. Plattner, H., Artalejo, A.R. & Neher, E. Ultrastructural organization of bovine chromaffin cell cortex-analysis by cryofixation and morphometry of aspects pertinent to exocytosis. J. Cell Biol. 139, 1709-1717 (1997).
24. Kim, T., Gondre-Lewis, M.C., Arnaoutova, I. & Loh, Y.P. Dense-core secretory granule biogenesis. Physiology (Bethesda) 21, 124-133 (2006).
25. Meldolesi, J., Chieregatti, E. & Luisa Malosio, M. Requirements for the identification of dense-core granules. Trends Cell Biol. 14, 13-19 (2004).
26. Pobbati, A.V., Stein, A. & Fasshauer, D. N-to C-terminal SNARE complex assembly promotes rapid membrane fusion. Science 313, 673-676 (2006).
27. Struck, D.K., Hoekstra, D. & Pagano, R.E. Use of resonance energy transfer to monitor membrane fusion. Biochemistry 20, 4093-4099 (1981).
28. Chernomordik, L.V. et al. Lysolipids reversibly inhibit Ca2+-, GTP-and pH-dependent fusion of biological membranes. FEBS Lett. 318, 71-76 (1993).
29. Lee, H.K. et al. Dynamic Ca2+-dependent stimulation of vesicle fusion by membrane-anchored synaptotagmin-1. Science 328, 760-763 (2010).
30. Davletov, B.A. & Sudhof, T.C. A single C2 domain from synaptotagmin-1 is sufficient for high-affinity Ca2+-phospholipid binding. J. Biol. Chem. 268, 26386-26390 (1993).
31. Zhang, X., Rizo, J. & Sudhof, T.C. Mechanism of phospholipid binding by the C2A-domain of synaptotagmin-1. Biochemistry 37, 12395-12403 (1998).
32. 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).
33. Di Paolo, G. & De Camilli, P. Phosphoinositides in cell regulation and membrane dynamics. Nature 443, 651-657 (2006).
34. Milosevic, I. et al. Plasmalemmal phosphatidylinositol-4,5-bisphosphate level regulates the releasable vesicle pool size in chromaffin cells. J. Neurosci. 25, 2557-2565 (2005).
35. Radhakrishnan, A., Stein, A., Jahn, R. & Fasshauer, D. The Ca2+ affinity of synaptotagmin-1 is markedly increased by a specific interaction of its C2B domain with phosphatidylinositol-4,5-bisphosphate. J. Biol. Chem. 284, 25749-25760 (2009).
36. van den Bogaart, G. et al. Membrane-protein sequestering by ionic protein-lipid interactions. Nature 479, 552-555 (2011).
37. Botelho, R.J., Scott, C.C. & Grinstein, S. Phosphoinositide involvement in phagocytosis and phagosome maturation. Curr. Top. Microbiol. Immunol. 282, 1-30 (2004).
38. Gillooly, D.J. et al. Localization of phosphatidylinositol-3-phosphate in yeast and mammalian cells. EMBO J. 19, 4577-4588 (2000).
39. Lai, Y. & Shin, Y.K. The importance of an asymmetric distribution of acidic lipids for synaptotagmin-1 function as a Ca2+ sensor. Biochem. J. 443, 223-229 (2012).
40. Bhalla, A., Chicka, M.C., Tucker, W.C. & Chapman, E.R. Ca2+-synaptotagmin directly regulates t-SNARE function during reconstituted membrane fusion. Nat. Struct. Mol. Biol. 13, 323-330 (2006).
41. Kyoung, M. et al. In vitro system capable of differentiating fast Ca2+-triggered content mixing from lipid exchange for mechanistic studies of neurotransmitter release. Proc. Natl. Acad. Sci. USA 108, E304-E313 (2011).
42. Wilson, J.E. & Chin, A. Chelation of divalent cations by ATP, studied by titration calorimetry. Anal. Biochem. 193, 16-19 (1991).
43. Kuo, W., Herrick, D.Z., Ellena, J.F. & Cafiso, D.S. The calcium-dependent and calcium-independent membrane binding of synaptotagmin-1: two modes of C2B binding. J. Mol. Biol. 387, 284-294 (2009).
44. Vrljic, M. et al. Post-translational modifications and lipid-binding profile of insect cell-expressed full-length mammalian synaptotagmin-1. Biochemistry 50, 9998-10012 (2011).
45. Li, L. et al. Phosphatidylinositol phosphates as co-activators of Ca2+ binding to C2 domains of synaptotagmin-1. J. Biol. Chem. 281, 15845-15852 (2006).
46. Baker, P.F. & Knight, D.E. Calcium-dependent exocytosis in bovine adrenal medullary cells with leaky plasma membranes. Nature 276, 620-622 (1978).
47. Barszczewski, M. et al. A novel site of action for α-SNAP in the SNARE conformational cycle controlling membrane fusion. Mol. Biol. Cell 19, 776-784 (2008).
48. van den Bogaart, G. et al. Synaptotagmin-1 may be a distance regulator acting upstream of SNARE nucleation. Nat. Struct. Mol. Biol. 18, 805-812 (2011).
49. Smith, A.D. & Winkler, H. A simple method for the isolation of adrenal chromaffin granules on a large scale. Biochem. J. 103, 480-482 (1967).
50. Li, Y. et al. A single mutation in the recombinant light chain of tetanus toxin abolishes its proteolytic activity and removes the toxicity seen after reconstitution with native heavy chain. Biochemistry 33, 7014-7020 (1994).
51. Weber, T. et al. SNAREpins: minimal machinery for membrane fusion. Cell 92, 759-772 (1998).
52. Cypionka, A. et al. Discrimination between docking and fusion of liposomes reconstituted with neuronal SNARE proteins using FCS. Proc. Natl. Acad. Sci. USA 106, 18575-18580 (2009).
53. Kendall, D.A. & MacDonald, R.C. Characterization of a fluorescence assay to monitor changes in the aqueous volume of lipid vesicles. Anal. Biochem. 134, 26-33 (1983).