Prevalent mechanism of membrane bridging by synaptotagmin-1

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 34, 2013, Pages

  Seven, Alpay B ^a   Brewer, Kyle D ^a   Shi, Liang ^b   Jiang, Qiu Xing ^b   Rizo, Josep ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

Ca2+ sensing; Exocytosis; Membrane bending; Synaptic transmission

Indexed keywords

CALCIUM; NANODISC; NEUROTRANSMITTER; OLIGOMER; SNARE PROTEIN; SYNAPTOTAGMIN I;

ARTICLE; CALCIUM BINDING; CELL MEMBRANE; CONFORMATION; CONTROLLED STUDY; FLUORESCENCE SPECTROSCOPY; MEMBRANE BINDING; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN FUNCTION; SYNAPSE VESICLE;

CA2+ SENSING; EXOCYTOSIS; MEMBRANE BENDING; SYNAPTIC TRANSMISSION;

CARBON RADIOISOTOPES; CHROMATOGRAPHY, GEL; CHROMATOGRAPHY, ION EXCHANGE; CRYOELECTRON MICROSCOPY; ESCHERICHIA COLI; FLUORESCENCE; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; SPECTROPHOTOMETRY; SPIN LABELS; SYNAPTOTAGMIN I; TRITIUM;

EID: 84882767998     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1310327110     Document Type: Article

References (50)

1. Rizo J, Südhof TC (2012) The membrane fusion enigma: SNAREs, Sec1/Munc18 proteins, and their accomplices - guilty as charged? Annu Rev Cell Dev Biol 28: 279-308.
2. Jahn R, Fasshauer D (2012) Molecular machines governing exocytosis of synaptic vesicles. Nature 490(7419):201-207.
3. Brunger AT, Weninger K, Bowen M, Chu S (2009) Single-molecule studies of the neuronal SNARE fusion machinery. Annu Rev Biochem 78:903-928.
4. Chapman ER (2008) How does synaptotagmin trigger neurotransmitter release? Annu Rev Biochem 77:615-641.
5. Fernández-Chacón R, et al. (2001) Synaptotagmin I functions as a calcium regulator of release probability. Nature 410(6824):41-49.
6. Bhalla A, Chicka MC, Tucker WC, Chapman ER (2006) Ca(2+)-synaptotagmin directly regulates t-SNARE function during reconstituted membrane fusion. Nat Struct Mol Biol 13(4):323-330.
7. Xue M, Ma C, Craig TK, Rosenmund C, Rizo J (2008) The Janus-faced nature of the C(2)Bdomain is fundamental for synaptotagmin-1 function. Nat Struct Mol Biol 15(11):1160-1168.
8. Schaub JR, Lu X, Doneske B, Shin YK, McNew JA (2006) Hemifusion arrest by complexin is relieved by Ca2+-synaptotagmin I. Nat Struct Mol Biol 13(8):748-750.
9. Tang J, et al. (2006) A complexin/synaptotagmin 1 switch controls fast synaptic vesicle exocytosis. Cell 126(6):1175-1187.
10. Giraudo CG, Eng WS, Melia TJ, Rothman JE (2006) A clamping mechanism involved in SNARE-dependent exocytosis. Science 313(5787):676-680.
11. Parisotto D, Malsam J, Scheutzow A, Krause JM, Söllner TH (2012) SNAREpin assembly by Munc18-1 requires previous vesicle docking by synaptotagmin 1. J Biol Chem 287(37):31041-31049.
12. Ma C, Su L, Seven AB, Xu Y, Rizo J (2013) Reconstitution of the vital functions of Munc18 and Munc13 in neurotransmitter release. Science 339(6118):421-425.
13. Sutton RB, Davletov BA, Berghuis AM, Südhof TC, Sprang SR (1995) Structure of the first C2 domain of synaptotagmin I: A novel Ca2+/phospholipid-binding fold. Cell 80(6):929-938.
14. Ubach J, Zhang X, Shao X, Südhof TC, Rizo J (1998) Ca2+ binding to synaptotagmin: How many Ca2+ ions bind to the tip of a C2-domain? EMBO J 17(14):3921-3930.
15. Fernandez I, et al. (2001) Three-dimensional structure of the synaptotagmin 1 C2Bdomain: Synaptotagmin 1 as a phospholipid binding machine. Neuron 32(6): 1057-1069.
16. Chapman ER, Davis AF (1998) Direct interaction of a Ca2+-binding loop of synaptotagmin with lipid bilayers. J Biol Chem 273(22):13995-14001.
17. Zhang X, Rizo J, Südhof TC (1998) Mechanism of phospholipid binding by the C2Adomain of synaptotagmin I. Biochemistry 37(36):12395-12403.
18. Rhee JS, et al. (2005) Augmenting neurotransmitter release by enhancing the apparent Ca2+ affinity of synaptotagmin 1. Proc Natl Acad Sci USA 102(51): 18664-18669.
19. Damer CK, Creutz CE (1994) Synergistic membrane interactions of the two C2 domains of synaptotagmin. J Biol Chem 269(49):31115-31123.
20. Araç D, et al. (2006) Close membrane-membrane proximity induced by Ca(2+)-dependent multivalent binding of synaptotagmin-1 to phospholipids. Nat Struct Mol Biol 13(3):209-217.
21. Mackler JM, Drummond JA, Loewen CA, Robinson IM, Reist NE (2002) The C(2)B Ca(2+)-binding motif of synaptotagmin is required for synaptic transmission in vivo. Nature 418(6895):340-344.
22. Robinson IM, Ranjan R, Schwarz TL (2002) Synaptotagmins I and IV promote transmitter release independently of Ca(2+) binding in the C(2)A domain. Nature 418(6895):336-340.
23. Dai H, Shen N, Araç D, Rizo J (2007) A quaternary SNARE-synaptotagmin-Ca2+-phospholipid complex in neurotransmitter release. J Mol Biol 367(3):848-863.
24. Herrick DZ, et al. (2009) Solution and membrane-bound conformations of the tandem C2A and C2B domains of synaptotagmin 1: Evidence for bilayer bridging. J Mol Biol 390(5):913-923.
25. Connell E, et al. (2008) Cross-linking of phospholipid membranes is a conserved property of calcium-sensitive synaptotagmins. J Mol Biol 380(1):42-50.
26. van den Bogaart G, et al. (2011) Synaptotagmin-1 may be a distance regulator acting upstream of SNARE nucleation. Nat Struct Mol Biol 18(7):805-812.
27. Park Y, et al. (2012) Controlling synaptotagmin activity by electrostatic screening. Nat Struct Mol Biol 19(10):991-997.
28. Vennekate W, et al. (2012) Cis- and trans-membrane interactions of synaptotagmin-1. Proc Natl Acad Sci USA 109(27):11037-11042.
29. Hui E, et al. (2011) Mechanism and function of synaptotagmin-mediated membrane apposition. Nat Struct Mol Biol 18(7):813-821.
30. Diao J, Yoon TY, Su Z, Shin YK, Ha T (2009) C2AB: A molecular glue for lipid vesicles with a negatively charged surface. Langmuir 25(13):7177-7180.
31. Diao J, et al. (2012) Synaptic proteins promote calcium-triggered fast transition from point contact to full fusion. elife 1:e00109.
32. Ubach J, et al. (2001) The C2B domain of synaptotagmin I is a Ca2+-binding module. Biochemistry 40(20):5854-5860.
33. Zhou A, Brewer KD, Rizo J (2013) Analysis of SNARE complex/synaptotagmin- 1 interactions by one-dimensional NMR spectroscopy. Biochemistry 52(20):3446-3456.
34. Sun J, Li H (2010) How to operate a cryo-electron microscope. Methods Enzymol 481: 231-249.
35. Crowley KS, Reinhart GD, Johnson AE (1993) The signal sequence moves through a ribosomal tunnel into a noncytoplasmic aqueous environment at the ER membrane early in translocation. Cell 73(6):1101-1115.
36. Wu Y, et al. (2003) Visualization of synaptotagmin I oligomers assembled onto lipid monolayers. Proc Natl Acad Sci USA 100(4):2082-2087.
37. Denisov IG, Grinkova YV, Lazarides AA, Sligar SG (2004) Directed self-assembly of monodisperse phospholipid bilayer nanodiscs with controlled size. J Am Chem Soc 126(11):3477-3487.
38. Ruschak AM, Kay LE (2010) Methyl groups as probes of supra-molecular structure, dynamics and function. J Biomol NMR 46(1):75-87.
39. Clore GM, Iwahara J (2009) Theory, practice, and applications of paramagnetic relaxation enhancement for the characterization of transient low-population states of biological macromolecules and their complexes. Chem Rev 109(9):4108-4139.
40. Shao X, Fernandez I, Südhof TC, 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(46):16106-16115.
41. Choi UB, et al. (2010) Single-molecule FRET-derived model of the synaptotagmin 1-SNARE fusion complex. Nat Struct Mol Biol 17(3):318-324.
42. Vrljic M, et al. (2010) Molecular mechanism of the synaptotagmin-SNARE interaction in Ca2+-triggered vesicle fusion. Nat Struct Mol Biol 17(3):325-331.
43. Chicka MC, Hui E, Liu H, Chapman ER (2008) Synaptotagmin arrests the SNARE complex before triggering fast, efficient membrane fusion in response to Ca2+. Nat Struct Mol Biol 15(8):827-835.
44. Honigmann A, et al. (2013) Phosphatidylinositol 4,5-bisphosphate clusters act as molecular beacons for vesicle recruitment. Nat Struct Mol Biol 20(6): 679-686.
45. Wang P, Wang CT, Bai J, Jackson MB, Chapman ER (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(47):47030-47037.
46. Takamori S, et al. (2006) Molecular anatomy of a trafficking organelle. Cell 127(4): 831-846.
47. Banerjee S, Huber T, Sakmar TP (2008) Rapid incorporation of functional rhodopsin into nanoscale apolipoprotein bound bilayer (NABB) particles. J Mol Biol 377(4): 1067-1081.
48. Brewer KD, Li W, Horne BE, Rizo J (2011) Reluctance to membrane binding enables accessibility of the synaptobrevin SNARE motif for SNARE complex formation. Proc Natl Acad Sci USA 108(31):12723-12728.
49. Delaglio F, et al. (1995) NMRPipe: A multidimensional spectral processing system based on UNIX pipes. J Biomol NMR 6(3):277-293.
50. Johnson BA, Blevins RA (1994) NMR View: A computer program for the visualization and analysis of NMR data. J Biomol NMR 4(5):603-614.