Evolutionary Divergence of the C-terminal Domain of Complexin Accounts for Functional Disparities between Vertebrate and Invertebrate Complexins

Wragg, Rachel T.; Parisotto, Daniel A.; Li, Zhenlong; Terakawa, Mayu S.; Snead, David; Basu, Ishani; Weinstein, Harel; Eliezer, David; Dittman, Jeremy S.

doi:10.3389/fnmol.2017.00146

Title: Evolutionary Divergence of the C-terminal Domain of Complexin Accounts for Functional Disparities between Vertebrate and Invertebrate Complexins

Journal Article · Fri May 26 00:00:00 EDT 2017 · Frontiers in Molecular Neuroscience

DOI:https://doi.org/10.3389/fnmol.2017.00146· OSTI ID:1565628

Wragg, Rachel T. ^[1]; Parisotto, Daniel A. ^[1]; Li, Zhenlong ^[2]; Terakawa, Mayu S. ^[1]; Snead, David ^[1]; Basu, Ishani ^[1]; Weinstein, Harel ^[3]; Eliezer, David ^[1]; Dittman, Jeremy S. ^[1]

Weill Cornell Medical College, New York, NY (United States). Dept. of Biochemistry
Weill Cornell Medical College, New York, NY (United States). Dept. of Physiology and Biophysics
Weill Cornell Medical College, New York, NY (United States). Dept. of Physiology and Biophysics; Weill Cornell Medical College, New York, NY (United States). Inst. for Computational Biomedicine

Complexin is a critical presynaptic protein that regulates both spontaneous and calcium-triggered neurotransmitter release in all synapses. Although the SNARE-binding central helix of complexin is highly conserved and required for all known complexin functions, the remainder of the protein has profoundly diverged across the animal kingdom. Striking disparities in complexin inhibitory activity are observed between vertebrate and invertebrate complexins but little is known about the source of these differences or their relevance to the underlying mechanism of complexin regulation. We found that mouse complexin 1 (mCpx1) failed to inhibit neurotransmitter secretion in Caenorhabditis elegans neuromuscular junctions lacking the worm complexin 1 (CPX-1). This lack of inhibition stemmed from differences in the C-terminal domain (CTD) of mCpx1. Previous studies revealed that the CTD selectively binds to highly curved membranes and directs complexin to synaptic vesicles. Although mouse and worm complexin have similar lipid binding affinity, their last few amino acids differ in both hydrophobicity and in lipid binding conformation, and these differences strongly impacted CPX-1 inhibitory function. Moreover, function was not maintained if a critical amphipathic helix in the worm CPX-1 CTD was replaced with the corresponding mCpx1 amphipathic helix. Invertebrate complexins generally shared more C-terminal similarity with vertebrate complexin 3 and 4 isoforms, and the amphipathic region of mouse complexin 3 significantly restored inhibitory function to worm CPX-1. We hypothesize that the CTD of complexin is essential in conferring an inhibitory function to complexin, and that this inhibitory activity has been attenuated in the vertebrate complexin 1 and 2 isoforms. Thus, evolutionary changes in the complexin CTD differentially shape its synaptic role across phylogeny.

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Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States). Oak Ridge Leadership Computing Facility (OLCF)

Sponsoring Organization:: USDOE Office of Science (SC); National Institutes of Health (NIH); US Department of Defense

Grant/Contract Number:: AC05-00OR22725; R01-GM095674; R37-AG019391; R01-GM117518; P01-DA012408; CO6RR015495; P41GM066354

OSTI ID:: 1565628

Journal Information:: Frontiers in Molecular Neuroscience, Vol. 10; ISSN 1662-5099

Publisher:: Frontiers Media SACopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 16 works

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Title: Evolutionary Divergence of the C-terminal Domain of Complexin Accounts for Functional Disparities between Vertebrate and Invertebrate Complexins

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