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Cup is essential for oskar mRNA translational repression during early Drosophila oogenesis

Study of the timing and location for mRNA translation across model systems has begun to shed light on molecular events fundamental to such processes as intercellular communication, morphogenesis, and body pattern formation. In D. melanogaster, the posterior mRNA determinant, oskar, is transcribed ma...

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Autores principales: Bayer, Livia V., Milano, Samantha, Formel, Stephen K., Kaur, Harpreet, Ravichandran, Rishi, Cambeiro, Juan A., Slinko, Lizaveta, Catrina, Irina E., Bratu, Diana P.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Taylor & Francis 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10413924/
https://www.ncbi.nlm.nih.gov/pubmed/37553798
http://dx.doi.org/10.1080/15476286.2023.2242650
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author Bayer, Livia V.
Milano, Samantha
Formel, Stephen K.
Kaur, Harpreet
Ravichandran, Rishi
Cambeiro, Juan A.
Slinko, Lizaveta
Catrina, Irina E.
Bratu, Diana P.
author_facet Bayer, Livia V.
Milano, Samantha
Formel, Stephen K.
Kaur, Harpreet
Ravichandran, Rishi
Cambeiro, Juan A.
Slinko, Lizaveta
Catrina, Irina E.
Bratu, Diana P.
author_sort Bayer, Livia V.
collection PubMed
description Study of the timing and location for mRNA translation across model systems has begun to shed light on molecular events fundamental to such processes as intercellular communication, morphogenesis, and body pattern formation. In D. melanogaster, the posterior mRNA determinant, oskar, is transcribed maternally but translated only when properly localized at the oocyte’s posterior cortex. Two effector proteins, Bruno1 and Cup, mediate steps of oskar mRNA regulation. The current model in the field identifies Bruno1 as necessary for Cup’s recruitment to oskar mRNA and indispensable for oskar’s translational repression. We now report that this Bruno1-Cup interaction leads to precise oskar mRNA regulation during early oogenesis and, importantly, the two proteins mutually influence each other’s mRNA expression and protein distribution in the egg chamber. We show that these factors stably associate with oskar mRNA in vivo. Cup associates with oskar mRNA without Bruno1, while surprisingly Bruno1’s stable association with oskar mRNA depends on Cup. We demonstrate that the essential factor for oskar mRNA repression in early oogenesis is Cup, not Bruno1. Furthermore, we find that Cup is a key P-body component that maintains functional P-body morphology during oogenesis and is necessary for oskar mRNA’s association with P-bodies. Therefore, Cup drives the translational repression and stability of oskar mRNA. These experimental results point to a regulatory feedback loop between Bruno 1 and Cup in early oogenesis that appears crucial for oskar mRNA to reach the posterior pole and its expression in the egg chamber for accurate embryo development.
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spelling pubmed-104139242023-08-11 Cup is essential for oskar mRNA translational repression during early Drosophila oogenesis Bayer, Livia V. Milano, Samantha Formel, Stephen K. Kaur, Harpreet Ravichandran, Rishi Cambeiro, Juan A. Slinko, Lizaveta Catrina, Irina E. Bratu, Diana P. RNA Biol Research Paper Study of the timing and location for mRNA translation across model systems has begun to shed light on molecular events fundamental to such processes as intercellular communication, morphogenesis, and body pattern formation. In D. melanogaster, the posterior mRNA determinant, oskar, is transcribed maternally but translated only when properly localized at the oocyte’s posterior cortex. Two effector proteins, Bruno1 and Cup, mediate steps of oskar mRNA regulation. The current model in the field identifies Bruno1 as necessary for Cup’s recruitment to oskar mRNA and indispensable for oskar’s translational repression. We now report that this Bruno1-Cup interaction leads to precise oskar mRNA regulation during early oogenesis and, importantly, the two proteins mutually influence each other’s mRNA expression and protein distribution in the egg chamber. We show that these factors stably associate with oskar mRNA in vivo. Cup associates with oskar mRNA without Bruno1, while surprisingly Bruno1’s stable association with oskar mRNA depends on Cup. We demonstrate that the essential factor for oskar mRNA repression in early oogenesis is Cup, not Bruno1. Furthermore, we find that Cup is a key P-body component that maintains functional P-body morphology during oogenesis and is necessary for oskar mRNA’s association with P-bodies. Therefore, Cup drives the translational repression and stability of oskar mRNA. These experimental results point to a regulatory feedback loop between Bruno 1 and Cup in early oogenesis that appears crucial for oskar mRNA to reach the posterior pole and its expression in the egg chamber for accurate embryo development. Taylor & Francis 2023-08-08 /pmc/articles/PMC10413924/ /pubmed/37553798 http://dx.doi.org/10.1080/15476286.2023.2242650 Text en © 2023 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group. https://creativecommons.org/licenses/by-nc/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License (http://creativecommons.org/licenses/by-nc/4.0/ (https://creativecommons.org/licenses/by-nc/4.0/) ), which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. The terms on which this article has been published allow the posting of the Accepted Manuscript in a repository by the author(s) or with their consent.
spellingShingle Research Paper
Bayer, Livia V.
Milano, Samantha
Formel, Stephen K.
Kaur, Harpreet
Ravichandran, Rishi
Cambeiro, Juan A.
Slinko, Lizaveta
Catrina, Irina E.
Bratu, Diana P.
Cup is essential for oskar mRNA translational repression during early Drosophila oogenesis
title Cup is essential for oskar mRNA translational repression during early Drosophila oogenesis
title_full Cup is essential for oskar mRNA translational repression during early Drosophila oogenesis
title_fullStr Cup is essential for oskar mRNA translational repression during early Drosophila oogenesis
title_full_unstemmed Cup is essential for oskar mRNA translational repression during early Drosophila oogenesis
title_short Cup is essential for oskar mRNA translational repression during early Drosophila oogenesis
title_sort cup is essential for oskar mrna translational repression during early drosophila oogenesis
topic Research Paper
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10413924/
https://www.ncbi.nlm.nih.gov/pubmed/37553798
http://dx.doi.org/10.1080/15476286.2023.2242650
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