Differential regulation of evoked and spontaneous neurotransmitter release by C-terminal modifications of complexin

Molecular and Cellular Neuroscience

Volumn 52, Issue , 2013, Pages 161-172

  Buhl, Lauren K ^a   Jorquera, Ramon A ^a,b   Akbergenova, Yulia ^a   Huntwork Rodriguez, Sarah ^a   Volfson, Dina ^a   Littleton, J Troy ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b UNIVERSIDAD CENTRAL DEL CARIBE   (United States)

Author keywords

Exocytosis; Neurotransmitter release; SNARE complex; Synapse; Synaptic vesicle

Indexed keywords

COMPLEXIN DERIVATIVE; INSECT PROTEIN; MESSENGER RNA; SNARE PROTEIN; UNCLASSIFIED DRUG;

ALLELE; ALPHA HELIX; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DROSOPHILA; GENE LOCUS; MUTAGENESIS; NEUROMUSCULAR SYNAPSE; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PRENYLATION; PROTEIN STABILITY; RNA EDITING; SYNAPSE VESICLE;

ALTERNATIVE SPLICING; AMINO ACID SEQUENCE; ANIMALS; BLOTTING, WESTERN; DROSOPHILA; DROSOPHILA PROTEINS; EXOCYTOSIS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MOLECULAR SEQUENCE DATA; NERVE TISSUE PROTEINS; NEUROMUSCULAR JUNCTION; NEUROTRANSMITTER AGENTS; PROTEIN ISOFORMS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SNARE PROTEINS; SYNAPTIC VESICLES;

EID: 84870829393     PISSN: 10447431     EISSN: 10959327     Source Type: Journal    
DOI: 10.1016/j.mcn.2012.11.009     Document Type: Article

References (44)

1. An S.J., Grabner C.P., Zenisek D. Real-time visualization of complexin during single exocytic events. Nat. Neurosci. 2010, 13:577-583.
2. Bracher A., Kadlec J., Betz H., Weissenhorn W. X-ray structure of a neuronal complexin-SNARE complex from squid. J. Biol. Chem. 2002, 277:26517-26523.
3. Brand A.H., Perrimon N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 1993, 118:401-415.
4. 2+-triggered exocytosis by facilitating vesicle priming. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:19538-19543.
5. Chen X., Tomchick D.R., Kovrigin E., A.c, D., Machius M., Südhof T.C., Rizo J. Three-dimensional structure of the complexin/SNARE complex. Neuron 2002, 33:397-409.
6. Cho R.W., Song Y., Littleton J.T. Comparative analysis of Drosophila and mammalian complexins as fusion clamps and facilitators of neurotransmitter release. Mol. Cell. Neurosci. 2010, 45:389-397.
7. 2+ sensor for transmitter release at a central synapse. Cell 1994, 79:717-727.
8. Giraudo C.G., Eng W.S., Melia T.J., Rothman J.E. A clamping mechanism involved in SNARE-dependent exocytosis. Science 2006, 313:676-680.
9. Giraudo C.G., Garcia-Diaz A., Eng W.S., Yamamoto A., Melia T.J., Rothman J.E. Distinct domains of complexins bind SNARE complexes and clamp fusion in vitro. J. Biol. Chem. 2008, 283:21211-21219.
10. Giraudo C.G., Garcia-Diaz A., Eng W.S., Chen Y., Hendrickson W.A., Melia T.J., Rothman J.E. Alternative zippering as an on-off switch for SNARE-mediated fusion. Science 2009, 323:512-516.
11. Guan Z., Saraswati S., Adolfsen B., Littleton J.T. Genome-wide transcriptional changes associated with enhanced activity in the Drosophila nervous system. Neuron 2005, 48:91-107.
12. Higuchi M., Single F.N., Köhler M., Sommer B., Sprengel R., Seeburg P.H. RNA editing of AMPA receptor subunit GluR-B: a base-paired intron-exon structure determines position and efficiency. Cell 1993, 75:1361-1370.
13. Hobson R.J., Liu Q., Watanabe S., Jorgensen E.M. Complexin maintains vesicles in the primed state in C. elegans. Curr. Biol. 2011, 21:106-113.
14. Hoopengardner B., Bhalla T., Staber C., Reenan R. Nervous system targets of RNA editing identified by comparative genomics. Science 2003, 301:832-836.
15. Huntwork S., Littleton J.T. A complexin fusion clamp regulates spontaneous neurotransmitter release and synaptic growth. Nat. Neurosci. 2007, 10:1235-1237.
16. 2+ triggering of synaptic exocytosis. J. Neurosci. 2012, 32:2877-2885.
17. Karatekin E., Giovanni J.D., Iborra C., Coleman J., O'Shaughnessy B., Seagar M., Rothman J.E. A fast, single-vesicle fusion assay mimics physiological SNARE requirements. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:3517-3521.
18. Littleton J.T., Bellen H.J., Perin M.S. Expression of synaptotagmin in Drosophila reveals transport and localization of synaptic vesicles to the synapse. Development 1993, 118:1077-1088.
19. Malsam J., Seiler F., Schollmeier Y., Rusu P., Krause J., Söllner T. The carboxy-terminal domain of complexin I stimulates liposome fusion. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:2001-2006.
20. Martin J.A., Hu Z., Fenz K.M., Fernandez J., Dittman J.S. Complexin has opposite effects on two modes of synaptic vesicle fusion. Curr. Biol. 2011, 21:97-105.
21. Maximov A., Tang J., Yang X., Pang Z.P., Südhof T.C. Complexin controls the force transfer from SNARE complexes to membranes in fusion. Science 2009, 323:516-521.
22. McMahon H.T., Missler M., Li C., Südhof T.C. Complexins: cytosolic proteins that regulate SNAP receptor function. Cell 1995, 83:111-119.
23. Mohrmann R., de Wit H., Verhage M., Neher E., Sorensen J.B. Fast vesicle fusion in living cells requires at least three SNARE complexes. Science 2010, 330:502-505.
24. Ni J.Q., Markstein M., Binari R., Pfeiffer B., Liu L.P., Villalta C., Booker M., Perkins L., Perrimon N. Vector and parameters for targeted transgenic RNA interference in Drosophila melanogaster. Nat. Methods 2008, 5:49-51.
25. Pabst S., Hazzard J.W., Antonin W., Südhof T.C., Jahn R., Rizo J., Fasshauer D. Selective interaction of complexin with the neuronal SNARE complex. Determination of the binding regions. J. Biol. Chem. 2000, 275:19808-19818.
26. Pickering B.M., Willis A.E. The implications of structured 5' untranslated regions on translation and disease. Semin. Cell Dev. Biol. 2005, 16:39-47.
27. 2+-dependent neurotransmitter release. Cell 2001, 104:71-81.
28. Reim K., Wegmeyer H., Brandstätter J.H., Xue M., Rosenmund C., Dresbach T., Hofmann K., Brose N. Structurally and functionally unique complexins at retinal ribbon synapses. J. Cell Biol. 2005, 169:669-680.
29. Rieckhof G.E., Yoshihara M., Guan Z., Littleton J.T. Presynaptic N-type calcium channels regulate synaptic growth. J. Biol. Chem. 2003, 278:41099-41108.
30. 2+-synaptotagmin I. Nat. Struct. Mol. Biol. 2006, 13:748-750.
31. Seiler F., Malsam J., Krause J.M., Söllner T.H. A role of complexin-lipid interactions in membrane fusion. FEBS Lett. 2009, 583:2343-2348.
32. Strenzke N., Chanda S., Kopp-Scheinpflug C., Khimich D., Reim K., Bulankina A.V., Neef A., Wolf F., Brose N., Xu-Friedman M.A., et al. Complexin-I is required for high-fidelity transmission at the endbulb of Held auditory synapse. J. Neurosci. 2009, 29:7991-8004.
33. Südhof T.C., Rothman J.E. Membrane fusion: grappling with SNARE and SM proteins. Science 2009, 323:474-477.
34. Tautz D., Pfeifle C. A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback. Chromosoma 1989, 98:81-85.
35. Tweedie S., Ashburner M., Falls K., Leyland P., McQuilton P., Marygold S., Millburn G., Osumi-Sutherland D., Schroeder A., Seal R., Zhang H., FlyBase Consortium Flybase: enhancing Drosophila gene ontology annotations. Nucleic Acids Res. 2009, 37:D555-D559.
36. Van Den Bogaart J., Holt M.G., Bunt G., Riedel D., Wouters F.S., Jahn R. One SNARE complex is sufficient for membrane fusion. Nat. Struct. Mol. Biol. 2010, 17:358-364.
37. 2+ sensors for fast release that specify distinct presynaptic properties in subsets of neurons. Neuron 2007, 54:567-581.
38. Xue M., Reim K., Chen X., Chao H.-T., Deng H., Rizo J., Brose N., Rosenmund C. Distinct domains of complexin I differentially regulate neurotransmitter release. Nat. Struct. Mol. Biol. 2007, 14:949-958.
39. Xue M., Stradomska A., Chen H., Brose N., Zhang W., Rosenmund C., Reim K. Complexins facilitate neurotransmitter release at excitatory and inhibitory synapses in mammalian central nervous system. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:7875-7880.
40. Xue M., Lin Y.Q., Pan H., Reim K., Deng H., Bellen H.J., Rosenmund C. Tilting the balance between facilitatory and inhibitory functions of mammalian and Drosophila Complexins orchestrates synaptic vesicle exocytosis. Neuron 2009, 64:367-380.
41. Xue M., Craig T.K., Xu J., Chao H.-T., Rizo J., Rosenmund C. Binding of the complexin N terminus to the SNARE complex potentiates synaptic-vesicle fusogenicity. Nat. Struct. Mol. Biol. 2010, 17:568-575.
42. Yoshihara M., Littleton J.T. Synaptotagmin I functions as a calcium sensor to synchronize neurotransmitter release. Neuron 2002, 36:897-908.
43. Zhang F.L., Casey P.J. Protein prenylation: molecular mechanisms and functional consequences. Annu. Rev. Biochem. 1996, 65:241-269.
44. Zuker M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 2003, 31:3406-3415.