Conformation and membrane position of the region linking the two C2 domains in synaptotagmin 1 by site-directed spin labeling

Biochemistry

Volumn 47, Issue 47, 2008, Pages 12380-12388

  Huang, Hao ^a   Cafiso, David S ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ASSOCIATION REACTIONS; CALCIUM; DIFFRACTIVE OPTICAL ELEMENTS; DYNAMICS; LABELING; LIPID BILAYERS; MEMBRANES; PARAMAGNETIC RESONANCE;

BILAYER SURFACES; C2 DOMAINS; DIRECT INTERACTIONS; INTEGRAL MEMBRANE PROTEINS; INTRAMOLECULAR ASSOCIATIONS; LINE SHAPES; MEASURING PARAMETERS; MEMBRANE INTERFACES; MEMBRANE SURFACES; NANO-SECONDS; SYNAPTIC VESICLES; SYNAPTOTAGMIN; TWO DOMAINS;

SPIN DYNAMICS;

CALCIUM; NICKEL COMPLEX; SNARE PROTEIN; SYNAPTOTAGMIN I;

ARTICLE; C2 A DOMAIN; C2 B DOMAIN; CONFORMATION; ELECTRON SPIN RESONANCE; LIPID BILAYER; MEMBRANE BINDING; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN LOCALIZATION; RAT; SITE DIRECTED SPIN LABELING; SPIN LABELING; SURFACE PROPERTY;

ANIMALS; CELL MEMBRANE; LIPID BILAYERS; MODELS, MOLECULAR; PHOSPHATES; PROTEIN STRUCTURE, TERTIARY; RATS; SNARE PROTEINS; SPIN LABELS; STAINING AND LABELING; SYNAPTOTAGMIN I; WATER;

EID: 56749117908     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi801470m     Document Type: Article

References (53)

1. Jahn, R., Lang, T., and Sudhof, T. C. (2003) Membrane Fusion. Cell 112, 519-533.
2. Rothman, J. E. (1994) Mechanisms of intracellular protein transport. Nature 372, 55-63.
3. Sudhof, T. C. (2004) The synaptic vesicle cycle. Annu. Rev. Neurosci. 27, 509-547.
4. 2+ sensor for neurotransmitter release. Trends Neurosci. 26, 413-422.
5. Rizo, J., Chen, X., and Arac, D. (2006) Unraveling the mechanisms of synaptotagmin and SNARE function in neurotransmitter release. Trends Cell Biol. 16, 339-350.
6. Chapman, E. R. (2008) How does synaptotagmin trigger neurotransmitter release? Annu. Rev. Biochem. 77, 615-641.
7. 2+-synaptotagmin directly regulates t-SNARE function during reconstituted membrane fusion. Nat. Struct. Mol. Biol. 13, 323-330.
8. Martens, S., Kozlov, M. M., and McMahon, H. T. (2007) How synaptotagmin promotes membrane fusion. Science 316, 1205-1208.
9. 2+-dependent multivalent binding of synaptotagmin-1 to phospholipids. Nat. Struct. Mol. Biol. 13, 209-217.
10. 2+- dependent trans interaction with phospholipids. Nat. Struct. Mol. Biol. 14, 904-911.
11. Herrick, D. Z., Sterbling, S., Rasch, K. A., Hinderliter, A., and Cafiso, D. S. (2006) Position of synaptotagmin I at the membrane interface: Cooperative interactions of tandem C2 domains. Biochemistry 45, 9668-9674.
12. 2+-phospholipid complex in neurotransmitter release. J. Mol. Biol. 367, 848-863.
13. Bowen, M. E., Weninger, K., Ernst, J., Chu, S., and Brunger, A. T. (2005) Single-molecule studies of synaptotagmin and complexin binding to the SNARE complex. Biophys. J. 89, 690-702.
14. 2+/phospholipid-binding fold. Cell 80, 929.
15. 2+ induce a conformational change? Biochemistry 37, 16106-16115.
16. 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.
17. 2+ coordination sites in synaptotagmin I C2B domain. Protein Sci. 13, 2665-2672.
18. 2+ reveals a novel domain association. Biochemistry 46, 13041-13048.
19. Garcia, R. A., Forde, C. E., and Godwin, H. A. (2000) Calcium triggers an intramolecular association of the C2 domains in synaptotagmin. Proc. Natl. Acad. Sci. U.S.A. 97, 5883-5888.
20. Hubbell, W. L., Gross, A., Langen, R., and Lietzow, M. A. (1998) Recent advances in site-directed spin labeling of proteins. Curr. Opin. Struct. Biol. 8, 649-656.
21. Hubbell, W. L., Cafiso, D. S., and Altenbach, C. (2000) Identifying conformational changes with site-directed spin labeling. Nat. Struct. Biol. 7, 735-739.
22. Columbus, L., and Hubbell, W. L. (2002) A new spin on protein dynamics. Trends Biochem. Sci. 27, 288-295.
23. Fanucci, G. E., and Cafiso, D. S. (2006) Recent advances and applications of site-directed spin labeling. Curr. Opin. Struct. Biol. 16, 644-653.
24. Klug, C. S., and Feix, J. B. (2008) Methods and applications of site-directed spin labeling EPR spectroscopy. Methods Cell Biol. 84, 617-658.
25. Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, Cold Spring Harbor Laboratory Press, Plainview, NY.
26. Rufener, E., Frazier, A. A., Wieser, C. M., Hinderliter, A., and Cafiso, D. S. (2005) Membrane-bound orientation and position of the synaptotagmin C2B domain determined by site-directed spin labeling. Biochemistry 44, 18-28.
27. Buser, C. A., Sigal, C. T., Resh, M. D., and McLaughlin, S. (1994) Membrane binding of myristylated peptides corresponding to the NH2 terminus of Src. Biochemistry 33, 13093-13101.
28. Frazier, A. A., Roller, C. R., Havelka, J. J., Hinderliter, A., and Cafiso, D. S. (2003) Membrane-bound orientation and position of the synaptotagmin I C2A domain by site-directed spin labeling. Biochemistry 42, 96-105.
29. Fasshauer, D., Eliason, W. K., Brunger, A. T., and Jahn, R. (1998) Identification of a minimal core of the synaptic SNARE complex sufficient for reversible assembly and disassembly. Biochemistry 37, 10354-10362.
30. Langen, R., Cai, K., Altenbach, C., Khorana, H. G., and Hubbell, W. L. (1999) Structural features of the C-terminal domain of bovine rhodopsin: A site-directed spin-labeling study. Biochemistry 38, 7918-7924.
31. Altenbach, C., Greenhalgh, D. A., Khorana, H. G., and Hubbell, W. L. (1994) A collision gradient-method to determine the immersion depth of nitroxides in lipid bilayers. Application to spinlabeled mutants of bacteriorhodopsin. Proc. Natl. Acad. Sci. U.S.A. 91, 1667-1671.
32. Victor, K., and Cafiso, D. S. (1998) Structure and position of the N-terminal binding domain of pp60src at the membrane interface. Biochemistry 37, 3402-3410.
33. Farahbakhsh, Z. T., Altenbach, C., and Hubbell, W. L. (1992) Spin-labeled cysteines as sensors for protein-lipid interaction and conformation in rhodopsin. Photochem. Photobiol. 56, 1019-1033.
34. Frazier, A. A., Wisner, M. A., Malmberg, N. J., Victor, K. G., Fanucci, G. E., Nalefski, E. A., Falke, J. J., and Cafiso, D. S. (2002) Membrane orientation and position of the C2 domain from cPLA2 by site-directed spin labeling. Biochemistry 41, 6282-6292.
35. Langen, R., Oh, K. J., Cascio, D., and Hubbell, W. L. (2000) Crystal structures of spin labeled T4 lysozyme mutants: Implications for the interpretation of EPR spectra in terms of structure. Biochemistry 39, 8396-8405.
36. Guo, Z., Cascio, D., Hideg, K., Kalai, T., and Hubbell, W. L. (2007) Structural determinants of nitroxide motion in spin-labeled proteins: Tertiary contact and solvent-inaccessible sites in helix G of T4 lysozyme. Protein Sci. 16, 1069-1086.
37. Guo, Z., Cascio, D., Hideg, K., and Hubbell, W. L. (2008) Structural determinants of nitroxide motion in spin-labeled proteins: Solvent-exposed sites in helix B of T4 lysozyme. Protein Sci. 17, 228-239.
38. Lietzow, M. A., and Hubbell, W. L. (2004) Motion of spin label side chains in cellular retinol-binding protein: Correlation with structure and nearest-neighbor interactions in an antiparallel β-sheet. Biochemistry 43, 3137-3151.
39. Columbus, L., and Hubbell, W. L. (2004) Mapping backbone dynamics in solution with site-directed spin labeling: GCN4-58 bZip free and bound to DNA. Biochemistry 43, 7273-7287.
40. Columbus, L., Kalai, T., Jeko, J., Hideg, K., and Hubbell, W. L. (2001) Molecular motion of spin labeled side chains in α-helices: Analysis by variation of side chain structure. Biochemistry 40, 3828-3846.
41. McHaourab, H. S., Lietzow, M. A., Hideg, K., and Hubbell, W. L. (1996) Motion of spin-labeled side chains in T4 lysozyme. Correlation with protein structure and dynamics. Biochemistry 35, 7692-7704.
42. Isas, J. M., Langen, R., Haigler, H. T., and Hubbell, W. L. (2002) Structure and dynamics of a helical hairpin and loop region in annexin 12: A site-directed spin labeling study. Biochemistry 41, 1464-1473.
43. Gross, A., and Hubbell, W. L. (2002) Identification of protein side chains near the membrane-aqueous interface: A site-directed spin labeling study of KcsA. Biochemistry 41, 1123-1128.
44. 2+ regulates the interaction between synaptotagmin and syntaxin 1. J. Biol. Chem. 270, 23667-23671.
45. Bai, J., and Chapman, E. R. (2004) The C2 domains of synaptotagmin: Partners in exocytosis. Trends Biochem. Sci. 29, 143-151.
46. Rickman, C., Archer, D. A., Meunier, F. A., Craxton, M., Fukuda, M., Burgoyne, R. D., and Davletov, B. (2004) Synaptotagmin Interaction with the Syntaxin/SNAP-25 Dimer Is Mediated by an Evolutionarily Conserved Motif and Is Sensitive to Inositol Hexakisphosphate. J. Biol. Chem. 279, 12574-12579.
47. Brunger, A. T. (2005) Structure and function of SNARE and SNARE-interacting proteins. Q. Rev. Biophys. 38, 1-47.
48. 2+- triggered vesicle exocytosis. Mol. Biol. Cell 18, 4957-4968.
49. Bai, J., Tucker, W. C., and Chapman, E. R. (2004) 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.
50. 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.
51. Tang, J., Maximov, A., Shin, O. H., Dai, H., Rizo, J., and Sudhof, T. C. (2006) A complexin/synaptotagmin 1 switch controls fast synaptic vesicle exocytosis. Cell 126, 1175-1187.
52. Lin, Y., Nielsen, R., Murray, D., Hubbell, W. L., Mailer, C., Robinson, B. H., and Gelb, M. H. (1998) Docking phospholipase A2 on membranes using electrostatic potential-modulated spin relaxation magnetic resonance. Science 279, 1925-1929.
53. Ball, A., Nielsen, R., Gelb, M. H., and Robinson, B. H. (1999) Interfacial membrane docking of cytosolic phospholipase A2 C2 domain using electrostatic potential-modulated spin relaxation magnetic resonance. Proc. Natl. Acad. Sci. U.S.A. 96, 6637-6642.