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Bridging the Synaptic Gap: Neuroligins and Neurexin I in Apis mellifera

Vertebrate studies show neuroligins and neurexins are binding partners in a trans-synaptic cell adhesion complex, implicated in human autism and mental retardation disorders. Here we report a genetic analysis of homologous proteins in the honey bee. As in humans, the honeybee has five large (31–246...

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Autores principales: Biswas, Sunita, Russell, Robyn J., Jackson, Colin J., Vidovic, Maria, Ganeshina, Olga, Oakeshott, John G., Claudianos, Charles
Formato: Texto
Lenguaje:English
Publicado: Public Library of Science 2008
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2570956/
https://www.ncbi.nlm.nih.gov/pubmed/18974885
http://dx.doi.org/10.1371/journal.pone.0003542
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author Biswas, Sunita
Russell, Robyn J.
Jackson, Colin J.
Vidovic, Maria
Ganeshina, Olga
Oakeshott, John G.
Claudianos, Charles
author_facet Biswas, Sunita
Russell, Robyn J.
Jackson, Colin J.
Vidovic, Maria
Ganeshina, Olga
Oakeshott, John G.
Claudianos, Charles
author_sort Biswas, Sunita
collection PubMed
description Vertebrate studies show neuroligins and neurexins are binding partners in a trans-synaptic cell adhesion complex, implicated in human autism and mental retardation disorders. Here we report a genetic analysis of homologous proteins in the honey bee. As in humans, the honeybee has five large (31–246 kb, up to 12 exons each) neuroligin genes, three of which are tightly clustered. RNA analysis of the neuroligin-3 gene reveals five alternatively spliced transcripts, generated through alternative use of exons encoding the cholinesterase-like domain. Whereas vertebrates have three neurexins the bee has just one gene named neurexin I (400 kb, 28 exons). However alternative isoforms of bee neurexin I are generated by differential use of 12 splice sites, mostly located in regions encoding LNS subdomains. Some of the splice variants of bee neurexin I resemble the vertebrate α- and β-neurexins, albeit in vertebrates these forms are generated by alternative promoters. Novel splicing variations in the 3′ region generate transcripts encoding alternative trans-membrane and PDZ domains. Another 3′ splicing variation predicts soluble neurexin I isoforms. Neurexin I and neuroligin expression was found in brain tissue, with expression present throughout development, and in most cases significantly up-regulated in adults. Transcripts of neurexin I and one neuroligin tested were abundant in mushroom bodies, a higher order processing centre in the bee brain. We show neuroligins and neurexins comprise a highly conserved molecular system with likely similar functional roles in insects as vertebrates, and with scope in the honeybee to generate substantial functional diversity through alternative splicing. Our study provides important prerequisite data for using the bee as a model for vertebrate synaptic development.
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spelling pubmed-25709562008-10-31 Bridging the Synaptic Gap: Neuroligins and Neurexin I in Apis mellifera Biswas, Sunita Russell, Robyn J. Jackson, Colin J. Vidovic, Maria Ganeshina, Olga Oakeshott, John G. Claudianos, Charles PLoS One Research Article Vertebrate studies show neuroligins and neurexins are binding partners in a trans-synaptic cell adhesion complex, implicated in human autism and mental retardation disorders. Here we report a genetic analysis of homologous proteins in the honey bee. As in humans, the honeybee has five large (31–246 kb, up to 12 exons each) neuroligin genes, three of which are tightly clustered. RNA analysis of the neuroligin-3 gene reveals five alternatively spliced transcripts, generated through alternative use of exons encoding the cholinesterase-like domain. Whereas vertebrates have three neurexins the bee has just one gene named neurexin I (400 kb, 28 exons). However alternative isoforms of bee neurexin I are generated by differential use of 12 splice sites, mostly located in regions encoding LNS subdomains. Some of the splice variants of bee neurexin I resemble the vertebrate α- and β-neurexins, albeit in vertebrates these forms are generated by alternative promoters. Novel splicing variations in the 3′ region generate transcripts encoding alternative trans-membrane and PDZ domains. Another 3′ splicing variation predicts soluble neurexin I isoforms. Neurexin I and neuroligin expression was found in brain tissue, with expression present throughout development, and in most cases significantly up-regulated in adults. Transcripts of neurexin I and one neuroligin tested were abundant in mushroom bodies, a higher order processing centre in the bee brain. We show neuroligins and neurexins comprise a highly conserved molecular system with likely similar functional roles in insects as vertebrates, and with scope in the honeybee to generate substantial functional diversity through alternative splicing. Our study provides important prerequisite data for using the bee as a model for vertebrate synaptic development. Public Library of Science 2008-10-31 /pmc/articles/PMC2570956/ /pubmed/18974885 http://dx.doi.org/10.1371/journal.pone.0003542 Text en Biswas et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Biswas, Sunita
Russell, Robyn J.
Jackson, Colin J.
Vidovic, Maria
Ganeshina, Olga
Oakeshott, John G.
Claudianos, Charles
Bridging the Synaptic Gap: Neuroligins and Neurexin I in Apis mellifera
title Bridging the Synaptic Gap: Neuroligins and Neurexin I in Apis mellifera
title_full Bridging the Synaptic Gap: Neuroligins and Neurexin I in Apis mellifera
title_fullStr Bridging the Synaptic Gap: Neuroligins and Neurexin I in Apis mellifera
title_full_unstemmed Bridging the Synaptic Gap: Neuroligins and Neurexin I in Apis mellifera
title_short Bridging the Synaptic Gap: Neuroligins and Neurexin I in Apis mellifera
title_sort bridging the synaptic gap: neuroligins and neurexin i in apis mellifera
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2570956/
https://www.ncbi.nlm.nih.gov/pubmed/18974885
http://dx.doi.org/10.1371/journal.pone.0003542
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