Memory consolidation in honey bees is enhanced by down-regulation of Down syndrome cell adhesion molecule and changes its alternative splicing

Down syndrome cell adhesion molecule (Dscam) gene encodes a cell adhesion molecule required for neuronal wiring. A remarkable feature of arthropod Dscam is massive alternative splicing generating thousands of different isoforms from three variable clusters of alternative exons. Dscam expression and...

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Main Authors: Pinar Ustaoglu, David W. J. McQuarrie, Anthony Rochet, Thomas C. Dix, Irmgard U. Haussmann, Roland Arnold, Jean-Marc Devaud, Matthias Soller
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-01-01
Series:Frontiers in Molecular Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fnmol.2023.1322808/full
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author Pinar Ustaoglu
Pinar Ustaoglu
David W. J. McQuarrie
David W. J. McQuarrie
Anthony Rochet
Thomas C. Dix
Thomas C. Dix
Irmgard U. Haussmann
Irmgard U. Haussmann
Roland Arnold
Roland Arnold
Jean-Marc Devaud
Jean-Marc Devaud
Matthias Soller
Matthias Soller
author_facet Pinar Ustaoglu
Pinar Ustaoglu
David W. J. McQuarrie
David W. J. McQuarrie
Anthony Rochet
Thomas C. Dix
Thomas C. Dix
Irmgard U. Haussmann
Irmgard U. Haussmann
Roland Arnold
Roland Arnold
Jean-Marc Devaud
Jean-Marc Devaud
Matthias Soller
Matthias Soller
author_sort Pinar Ustaoglu
collection DOAJ
description Down syndrome cell adhesion molecule (Dscam) gene encodes a cell adhesion molecule required for neuronal wiring. A remarkable feature of arthropod Dscam is massive alternative splicing generating thousands of different isoforms from three variable clusters of alternative exons. Dscam expression and diversity arising from alternative splicing have been studied during development, but whether they exert functions in adult brains has not been determined. Here, using honey bees, we find that Dscam expression is critically linked to memory retention as reducing expression by RNAi enhances memory after reward learning in adult worker honey bees. Moreover, alternative splicing of Dscam is altered in all three variable clusters after learning. Since identical Dscam isoforms engage in homophilic interactions, these results suggest a mechanism to alter inclusion of variable exons during memory consolidation to modify neuronal connections for memory retention.
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spelling doaj.art-fd81551ee6684cafa512de51b39b60952024-01-09T04:14:19ZengFrontiers Media S.A.Frontiers in Molecular Neuroscience1662-50992024-01-011610.3389/fnmol.2023.13228081322808Memory consolidation in honey bees is enhanced by down-regulation of Down syndrome cell adhesion molecule and changes its alternative splicingPinar Ustaoglu0Pinar Ustaoglu1David W. J. McQuarrie2David W. J. McQuarrie3Anthony Rochet4Thomas C. Dix5Thomas C. Dix6Irmgard U. Haussmann7Irmgard U. Haussmann8Roland Arnold9Roland Arnold10Jean-Marc Devaud11Jean-Marc Devaud12Matthias Soller13Matthias Soller14School of Biosciences, College of Life and Environmental Sciences, University of Birmingham, Birmingham, United KingdomBirmingham Centre for Genome Biology, University of Birmingham, Birmingham, United KingdomSchool of Biosciences, College of Life and Environmental Sciences, University of Birmingham, Birmingham, United KingdomBirmingham Centre for Genome Biology, University of Birmingham, Birmingham, United KingdomResearch Center on Animal Cognition (CRCA), Center for Integrative Biology (CBI), CNRS, UPS, Toulouse University, Toulouse, FranceSchool of Biosciences, College of Life and Environmental Sciences, University of Birmingham, Birmingham, United KingdomBirmingham Centre for Genome Biology, University of Birmingham, Birmingham, United KingdomSchool of Biosciences, College of Life and Environmental Sciences, University of Birmingham, Birmingham, United KingdomDepartment of Life Science, Faculty of Health, Education and Life Sciences, Birmingham City University, Birmingham, United KingdomBirmingham Centre for Genome Biology, University of Birmingham, Birmingham, United KingdomCollege of Medical and Dental Sciences, Institute of Cancer and Genomics Sciences, University of Birmingham, Birmingham, United KingdomResearch Center on Animal Cognition (CRCA), Center for Integrative Biology (CBI), CNRS, UPS, Toulouse University, Toulouse, FranceInstitut Universitaire de France (IUF), Paris, FranceSchool of Biosciences, College of Life and Environmental Sciences, University of Birmingham, Birmingham, United KingdomBirmingham Centre for Genome Biology, University of Birmingham, Birmingham, United KingdomDown syndrome cell adhesion molecule (Dscam) gene encodes a cell adhesion molecule required for neuronal wiring. A remarkable feature of arthropod Dscam is massive alternative splicing generating thousands of different isoforms from three variable clusters of alternative exons. Dscam expression and diversity arising from alternative splicing have been studied during development, but whether they exert functions in adult brains has not been determined. Here, using honey bees, we find that Dscam expression is critically linked to memory retention as reducing expression by RNAi enhances memory after reward learning in adult worker honey bees. Moreover, alternative splicing of Dscam is altered in all three variable clusters after learning. Since identical Dscam isoforms engage in homophilic interactions, these results suggest a mechanism to alter inclusion of variable exons during memory consolidation to modify neuronal connections for memory retention.https://www.frontiersin.org/articles/10.3389/fnmol.2023.1322808/fullDscamalternative splicinglearning and memoryhoney beeRNA interference (gene silencing)
spellingShingle Pinar Ustaoglu
Pinar Ustaoglu
David W. J. McQuarrie
David W. J. McQuarrie
Anthony Rochet
Thomas C. Dix
Thomas C. Dix
Irmgard U. Haussmann
Irmgard U. Haussmann
Roland Arnold
Roland Arnold
Jean-Marc Devaud
Jean-Marc Devaud
Matthias Soller
Matthias Soller
Memory consolidation in honey bees is enhanced by down-regulation of Down syndrome cell adhesion molecule and changes its alternative splicing
Frontiers in Molecular Neuroscience
Dscam
alternative splicing
learning and memory
honey bee
RNA interference (gene silencing)
title Memory consolidation in honey bees is enhanced by down-regulation of Down syndrome cell adhesion molecule and changes its alternative splicing
title_full Memory consolidation in honey bees is enhanced by down-regulation of Down syndrome cell adhesion molecule and changes its alternative splicing
title_fullStr Memory consolidation in honey bees is enhanced by down-regulation of Down syndrome cell adhesion molecule and changes its alternative splicing
title_full_unstemmed Memory consolidation in honey bees is enhanced by down-regulation of Down syndrome cell adhesion molecule and changes its alternative splicing
title_short Memory consolidation in honey bees is enhanced by down-regulation of Down syndrome cell adhesion molecule and changes its alternative splicing
title_sort memory consolidation in honey bees is enhanced by down regulation of down syndrome cell adhesion molecule and changes its alternative splicing
topic Dscam
alternative splicing
learning and memory
honey bee
RNA interference (gene silencing)
url https://www.frontiersin.org/articles/10.3389/fnmol.2023.1322808/full
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