A Two-Immunoglobulin-Domain Transmembrane Protein Mediates an Epidermal-Neuronal Interaction to Maintain Synapse Density

Neuron
Salvatore J Cherra, Yishi Jin

Abstract

Synaptic maintenance is essential for neural circuit function. In the C. elegans locomotor circuit, motor neurons are in direct contact with the epidermis. Here, we reveal a novel epidermal-neuronal interaction mediated by a two-immunoglobulin domain transmembrane protein, ZIG-10, that is necessary for maintaining cholinergic synapse density. ZIG-10 is localized at the cell surface of epidermis and cholinergic motor neurons, with high levels at areas adjacent to synapses. Loss of zig-10 increases the number of cholinergic excitatory synapses and exacerbates convulsion behavior in a seizure model. Mis-expression of zig-10 in GABAergic inhibitory neurons reduces GABAergic synapse number, dependent on the presence of ZIG-10 in the epidermis. Furthermore, ZIG-10 interacts with the tyrosine kinase SRC-2 to regulate the phagocytic activity of the epidermis to restrict cholinergic synapse number. Our studies demonstrate the highly specific roles of non-neuronal cells in modulating neural circuit function, through neuron-type-specific maintenance of synapse density.

References

Aug 10, 1976·Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences·J G WhiteS Brenner
Oct 2, 2003·Current Opinion in Cell Biology·Masahito YamagataJoshua A Weiner
Jun 2, 2004·Nature Reviews. Cancer·Timothy J Yeatman
Aug 25, 2005·The Journal of Biological Chemistry·Sentot SantosoTriantafyllos Chavakis
Jan 27, 2006·Journal of Cerebral Blood Flow and Metabolism : Official Journal of the International Society of Cerebral Blood Flow and Metabolism·Carl E Stafstrom
Mar 21, 2006·Nature·David Stellwagen, Robert C Malenka
Oct 13, 2006·Annual Review of Cell and Developmental Biology·Barry J Dickson, Giorgio F Gilestro
Nov 16, 2006·Glia·Alain BessisAnne Roumier
Dec 18, 2007·Cell·Beth StevensBen A Barres
Apr 14, 2009·Nature Methods·Daniel G GibsonHamilton O Smith
Apr 18, 2009·Cell Adhesion & Migration·Hideru TogashiYoshimi Takai
Nov 11, 2010·Nucleic Acids Research·Holger DinkelFrancesca Diella
May 10, 2011·Current Biology : CB·Tamara M StawickiYishi Jin
Jul 27, 2011·Proceedings of the National Academy of Sciences of the United States of America·Hakan KucukdereliCagla Eroglu
Nov 22, 2011·Current Biology : CB·Suhong Xu, Andrew D Chisholm
Nov 12, 1986·Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences·J G WhiteS Brenner
Jul 12, 2013·Annual Review of Neuroscience·S Lawrence Zipursky, Wesley B Grueber
Jul 23, 2013·Cell·Zhiyong ShaoDaniel A Colón-Ramos
Mar 22, 2014·The Journal of Neuroscience : the Official Journal of the Society for Neuroscience·Archana MishraRüdiger Klein
Sep 19, 2014·The Journal of Neuroscience : the Official Journal of the Society for Neuroscience·Sarah L RocheThomas H Gillingwater

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Citations

May 1, 2019·Cellular and Molecular Life Sciences : CMLS·Ardalan HendiKota Mizumoto
May 5, 2017·G3 : Genes - Genomes - Genetics·Katherine A McCullochSalvatore J Cherra
May 6, 2020·Journal of Neurogenetics·Salvatore J CherraYishi Jin
Mar 20, 2018·ELife·Florentina SotoDaniel Kerschensteiner
Jul 10, 2019·Annual Review of Neuroscience·Daniel K WiltonBeth Stevens
Jul 3, 2018·Frontiers in Molecular Neuroscience·Yanjun ShiZhiyong Shao
Jun 18, 2021·Frontiers in Cellular Neuroscience·Chang YinJay Z Parrish
Nov 23, 2021·Frontiers in Cellular Neuroscience·Brikha R ShresthaWesley B Grueber

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