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Science 337 (6097): 980-984

Copyright © 2012 by the American Association for the Advancement of Science

Neurexin and Neuroligin Mediate Retrograde Synaptic Inhibition in C. elegans

Zhitao Hu,1,2 Sabrina Hom,1,2,3 Tambudzai Kudze,1 Xia-Jing Tong,1,2 Seungwon Choi,1,2,3 Gayane Aramuni,4 Weiqi Zhang,5 Joshua M. Kaplan1,2,3,*

Abstract: The synaptic adhesion molecules neurexin and neuroligin alter the development and function of synapses and are linked to autism in humans. Here, we found that Caenorhabditis elegans neurexin (NRX-1) and neuroligin (NLG-1) mediated a retrograde synaptic signal that inhibited neurotransmitter release at neuromuscular junctions. Retrograde signaling was induced in mutants lacking a muscle microRNA (miR-1) and was blocked in mutants lacking NLG-1 or NRX-1. Release was rapid and abbreviated when the retrograde signal was on, whereas release was slow and prolonged when retrograde signaling was blocked. The retrograde signal adjusted release kinetics by inhibiting exocytosis of synaptic vesicles (SVs) that are distal to the site of calcium entry. Inhibition of release was mediated by increased presynaptic levels of tomosyn, an inhibitor of SV fusion.

1 Department of Molecular Biology, Massachusetts General Hospital, Boston, MA 02114, USA.
2 Department of Neurobiology, Harvard Medical School, Boston, MA 02115, USA.
3 Program in Neuroscience, Harvard Medical School, Boston, MA 02115, USA.
4 Max Planck Institute of Neurobiology, D-82152 Martinsried, Germany.
5 Department of Psychiatry, University of Münster, D-48149 Münster, Germany.

* To whom correspondence should be addressed. E-mail: kaplan{at}

UNC-13L, UNC-13S, and Tomosyn form a protein code for fast and slow neurotransmitter release in Caenorhabditis elegans.
Z. Hu, X.-J. Tong, and J. M. Kaplan (2013)
eLife Sci 2, e00967
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Neuroligins Provide Molecular Links Between Syndromic and Nonsyndromic Autism.
S. K. Singh and C. Eroglu (2013)
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