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A structural dynamics model for how CPEB3 binding to SUMO2 can regulate translational control in dendritic spines

A prion-like RNA-binding protein, CPEB3, can regulate local translation in dendritic spines. CPEB3 monomers repress translation, whereas CPEB3 aggregates activate translation of its target mRNAs. However, the CPEB3 aggregates, as long-lasting prions, may raise the problem of unregulated translationa...

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Autores principales: Gu, Xinyu, Schafer, Nicholas P., Bueno, Carlos, Lu, Wei, Wolynes, Peter G.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9674179/
https://www.ncbi.nlm.nih.gov/pubmed/36346822
http://dx.doi.org/10.1371/journal.pcbi.1010657
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author Gu, Xinyu
Schafer, Nicholas P.
Bueno, Carlos
Lu, Wei
Wolynes, Peter G.
author_facet Gu, Xinyu
Schafer, Nicholas P.
Bueno, Carlos
Lu, Wei
Wolynes, Peter G.
author_sort Gu, Xinyu
collection PubMed
description A prion-like RNA-binding protein, CPEB3, can regulate local translation in dendritic spines. CPEB3 monomers repress translation, whereas CPEB3 aggregates activate translation of its target mRNAs. However, the CPEB3 aggregates, as long-lasting prions, may raise the problem of unregulated translational activation. Here, we propose a computational model of the complex structure between CPEB3 RNA-binding domain (CPEB3-RBD) and small ubiquitin-like modifier protein 2 (SUMO2). Free energy calculations suggest that the allosteric effect of CPEB3-RBD/SUMO2 interaction can amplify the RNA-binding affinity of CPEB3. Combining with previous experimental observations on the SUMOylation mode of CPEB3, this model suggests an equilibrium shift of mRNA from binding to deSUMOylated CPEB3 aggregates to binding to SUMOylated CPEB3 monomers in basal synapses. This work shows how a burst of local translation in synapses can be silenced following a stimulation pulse, and explores the CPEB3/SUMO2 interplay underlying the structural change of synapses and the formation of long-term memories.
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spelling pubmed-96741792022-11-19 A structural dynamics model for how CPEB3 binding to SUMO2 can regulate translational control in dendritic spines Gu, Xinyu Schafer, Nicholas P. Bueno, Carlos Lu, Wei Wolynes, Peter G. PLoS Comput Biol Research Article A prion-like RNA-binding protein, CPEB3, can regulate local translation in dendritic spines. CPEB3 monomers repress translation, whereas CPEB3 aggregates activate translation of its target mRNAs. However, the CPEB3 aggregates, as long-lasting prions, may raise the problem of unregulated translational activation. Here, we propose a computational model of the complex structure between CPEB3 RNA-binding domain (CPEB3-RBD) and small ubiquitin-like modifier protein 2 (SUMO2). Free energy calculations suggest that the allosteric effect of CPEB3-RBD/SUMO2 interaction can amplify the RNA-binding affinity of CPEB3. Combining with previous experimental observations on the SUMOylation mode of CPEB3, this model suggests an equilibrium shift of mRNA from binding to deSUMOylated CPEB3 aggregates to binding to SUMOylated CPEB3 monomers in basal synapses. This work shows how a burst of local translation in synapses can be silenced following a stimulation pulse, and explores the CPEB3/SUMO2 interplay underlying the structural change of synapses and the formation of long-term memories. Public Library of Science 2022-11-08 /pmc/articles/PMC9674179/ /pubmed/36346822 http://dx.doi.org/10.1371/journal.pcbi.1010657 Text en © 2022 Gu et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Gu, Xinyu
Schafer, Nicholas P.
Bueno, Carlos
Lu, Wei
Wolynes, Peter G.
A structural dynamics model for how CPEB3 binding to SUMO2 can regulate translational control in dendritic spines
title A structural dynamics model for how CPEB3 binding to SUMO2 can regulate translational control in dendritic spines
title_full A structural dynamics model for how CPEB3 binding to SUMO2 can regulate translational control in dendritic spines
title_fullStr A structural dynamics model for how CPEB3 binding to SUMO2 can regulate translational control in dendritic spines
title_full_unstemmed A structural dynamics model for how CPEB3 binding to SUMO2 can regulate translational control in dendritic spines
title_short A structural dynamics model for how CPEB3 binding to SUMO2 can regulate translational control in dendritic spines
title_sort structural dynamics model for how cpeb3 binding to sumo2 can regulate translational control in dendritic spines
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9674179/
https://www.ncbi.nlm.nih.gov/pubmed/36346822
http://dx.doi.org/10.1371/journal.pcbi.1010657
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