Genetic analysis of the complexin trans-clamping model for cross-linking SNARE complexes in vivo

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

Volumn 111, Issue 28, 2014, Pages 10317-10322

  Cho, Richard W ^a   Kümmel, Daniel ^b,c   Li, Feng ^b   Baguley, Stephanie Wood ^b   Coleman, Jeff ^b   Rothman, James E ^b   Littleton, J Troy ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF OSNABRÜCK   (Germany)

Author keywords

Exocytosis; Neurotransmitter release; Synapse

Indexed keywords

BINDING PROTEIN; COMPLEXIN; HYBRID PROTEIN; SNARE PROTEIN; UNCLASSIFIED DRUG;

ACTION POTENTIAL; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CROSS LINKING; DROSOPHILA MELANOGASTER; GENETIC ANALYSIS; GENETIC MANIPULATION; IN VIVO STUDY; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; SYNAPSE VESICLE;

EXOCYTOSIS; NEUROTRANSMITTER RELEASE; SYNAPSE;

ANIMALS; CALCIUM; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; MUTATION; NERVE TISSUE PROTEINS; SNARE PROTEINS;

EID: 84904284070     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1409311111     Document Type: Article

References (42)

1. Söllner T, et al. (1993) SNAP receptors implicated in vesicle targeting and fusion. Nature 362(6418):318-324. (Pubitemid 23101303)
2. Weber T, et al. (1998) SNAREpins:Minimal machinery for membrane fusion. Cell 92(6):759-772.
3. Sutton RB, Fasshauer D, Jahn R, Brunger AT (1998) Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 A resolution. Nature 395(6700):347-353. (Pubitemid 28450677)
4. Li F, et al. (2007) Energetics and dynamics of SNAREpin folding across lipid bilayers. Nat Struct Mol Biol 14(10):890-896. (Pubitemid 47525184)
5. Rizo J, Rosenmund C (2008) Synaptic vesicle fusion. Nat Struct Mol Biol 15(7):665-674. (Pubitemid 351932007)
6. Li F, et al. (2014) A half-zippered SNARE complex represents a functional intermediate in membrane fusion. J Am Chem Soc 136(9):3456-3464.
7. Südhof TC, Rothman JE (2009) Membrane fusion: Grappling with SNARE and SM proteins. Science 323(5913):474-477.
8. Südhof TC (2013) Neurotransmitter release: The last millisecond in the life of a synaptic vesicle. Neuron 80(3):675-690.
9. Littleton JT, Stern M, Schulze K, Perin M, Bellen HJ (1993) Mutational analysis of Drosophila synaptotagmin demonstrates its essential role in Ca(2+)-activated neurotransmitter release. Cell 74(6):1125-1134. (Pubitemid 23289468)
10. Geppert M, et al. (1994) Synaptotagmin I: A major Ca2+ sensor for transmitter release at a central synapse. Cell 79(4):717-727.
11. Malsam J, et al. (2012) Complexin arrests a pool of docked vesicles for fast Ca2+-dependent release. EMBO J 31(15):3270-3281.
12. Bharat TA, et al. (2014) SNARE and regulatory proteins induce local membrane protrusions to prime docked vesicles for fast calcium-triggered fusion. EMBO Rep 15(3):308-314.
13. McMahon HT, Missler M, Li C, Südhof TC (1995) Complexins: Cytosolic proteins that regulate SNAP receptor function. Cell 83(1):111-119.
14. Giraudo CG, Eng WS, Melia TJ, Rothman JE (2006) A clamping mechanism involved in SNARE-dependent exocytosis. Science 313(5787):676-680. (Pubitemid 44201147)
15. 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. (Pubitemid 44175169)
16. Huntwork S, Littleton JT (2007) A complexin fusion clamp regulates spontaneous neurotransmitter release and synaptic growth. Nat Neurosci 10(10):1235-1237. (Pubitemid 47480302)
17. Cho RW, Song Y, Littleton JT (2010) Comparative analysis of Drosophila and mammalian complexins as fusion clamps and facilitators of neurotransmitter release. Mol Cell Neurosci 45(4):389-397.
18. Maximov A, Tang J, Yang X, Pang ZP, Südhof TC (2009) Complexin controls the force transfer from SNARE complexes to membranes in fusion. Science 323(5913):516-521.
19. Hobson RJ, Liu Q, Watanabe S, Jorgensen EM (2011) Complexin maintains vesicles in the primed state in C. elegans. Curr Biol 21(2):106-113.
20. Martin JA, Hu Z, Fenz KM, Fernandez J, Dittman JS (2011) Complexin has opposite effects on two modes of synaptic vesicle fusion. Curr Biol 21(2):97-105.
21. Jorquera RA, Huntwork-Rodriguez S, Akbergenova Y, Cho RW, Littleton JT (2012) Complexin controls spontaneous and evoked neurotransmitter release by regulating the timing and properties of synaptotagmin activity. J Neurosci 32(50):18234-18245.
22. Xue M, et al. (2009) Tilting the balance between facilitatory and inhibitory functions of mammalian and Drosophila Complexins orchestrates synaptic vesicle exocytosis. Neuron 64(3):367-380.
23. Xue M, et al. (2010) Binding of the complexin N terminus to the SNARE complex potentiates synaptic-vesicle fusogenicity. Nat Struct Mol Biol 17(5):568-575.
24. Giraudo CG, et al. (2009) Alternative zippering as an on-off switch for SNARE-mediated fusion. Science 323(5913):512-516.
25. Krishnakumar SS, et al. (2011) A conformational switch in complexin is required for synaptotagmin to trigger synaptic fusion. Nat Struct Mol Biol 18(8):934-940.
26. Kümmel D, et al. (2011) Complexin cross-links prefusion SNAREs into a zigzag array. Nat Struct Mol Biol 18(8):927-933.
27. Li F, et al. (2011) Complexin activates and clamps SNAREpins by a common mechanism involving an intermediate energetic state. Nat Struct Mol Biol 18(8):941-946.
28. Chen X, et al. (2002) Three-dimensional structure of the complexin/SNARE complex. Neuron 33(3):397-409. (Pubitemid 34158843)
29. Reim K, et al. (2001) Complexins regulate a late step in Ca2+-dependent neurotransmitter release. Cell 104(1):71-81. (Pubitemid 32144973)
30. Xue M, et al. (2007) Distinct domains of complexin I differentially regulate neurotransmitter release. Nat Struct Mol Biol 14(10):949-958. (Pubitemid 47525173)
31. Iyer J, Wahlmark CJ, Kuser-Ahnert GA, Kawasaki F (2013) Molecular mechanisms of COMPLEXIN fusion clamp function in synaptic exocytosis revealed in a new Drosophila mutant. Mol Cell Neurosci 56:244-254.
32. Wragg RT, et al. (2013) Synaptic vesicles position complexin to block spontaneous fusion. Neuron 77(2):323-334.
33. Kaeser-Woo YJ, Yang X, Südhof TC (2012) C-terminal complexin sequence is selectively required for clamping and priming but not for Ca2+ triggering of synaptic exocytosis. J Neurosci 32(8):2877-2885.
34. Bykhovskaia M, Jagota A, Gonzalez A, Vasin A, Littleton JT (2013) Interaction of the complexin accessory helix with the C-terminus of the SNARE complex: Molecular-dynamics model of the fusion clamp. Biophys J 105(3):679-690.
35. Dhara M, et al. (2014) Complexin synchronizes primed vesicle exocytosis and regulates fusion pore dynamics. J Cell Biol 204(7):1123-1140.
36. Buhl LK, et al. (2013) Differential regulation of evoked and spontaneous neurotransmitter release by C-terminal modifications of complexin. Mol Cell Neurosci 52:161-172.
37. Ramirez DM, Kavalali ET (2012) The role of non-canonical SNAREs in synaptic vesicle recycling. Cell Logist 2(1):20-27.
38. Xu J, Brewer KD, Perez-Castillejos R, Rizo J (2013) Subtle interplay between synaptotagmin and complexin binding to the SNARE complex. J Mol Biol 425(18):3461-3475.
39. Kavalali ET, et al. (2011) Spontaneous neurotransmission: An independent pathway for neuronal signaling? Physiology (Bethesda) 26(1):45-53.
40. Melom JE, Akbergenova Y, Gavornik JP, Littleton JT (2013) Spontaneous and evoked release are independently regulated at individual active zones. J Neurosci 33(44):17253-17263.
41. Yang X, Kaeser-Woo YJ, Pang ZP, Xu W, Südhof TC (2010) Complexin clamps asynchronous release by blocking a secondary Ca(2+) sensor via its accessory α helix. Neuron 68(5):907-920.
42. Seiler F, Malsam J, Krause JM, Söllner TH (2009) A role of complexin-lipid interactions in membrane fusion. FEBS Lett 583(14):2343-2348.