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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Main Authors: Livia V. Bayer, Samantha Milano, Stephen K. Formel, Harpreet Kaur, Rishi Ravichandran, Juan A. Cambeiro, Lizaveta Slinko, Irina E. Catrina, Diana P. Bratu
Format: Article
Language:English
Published: Taylor & Francis Group 2023-12-01
Series:RNA Biology
Subjects:
Online Access:http://dx.doi.org/10.1080/15476286.2023.2242650
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author Livia V. Bayer
Samantha Milano
Stephen K. Formel
Harpreet Kaur
Rishi Ravichandran
Juan A. Cambeiro
Lizaveta Slinko
Irina E. Catrina
Diana P. Bratu
author_facet Livia V. Bayer
Samantha Milano
Stephen K. Formel
Harpreet Kaur
Rishi Ravichandran
Juan A. Cambeiro
Lizaveta Slinko
Irina E. Catrina
Diana P. Bratu
author_sort Livia V. Bayer
collection DOAJ
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 doaj.art-5eee33f4725e4ca9a50e022f2d10c6292023-12-05T16:09:52ZengTaylor & Francis GroupRNA Biology1547-62861555-85842023-12-0120157358710.1080/15476286.2023.22426502242650Cup is essential for oskar mRNA translational repression during early Drosophila oogenesisLivia V. Bayer0Samantha Milano1Stephen K. Formel2Harpreet Kaur3Rishi Ravichandran4Juan A. Cambeiro5Lizaveta Slinko6Irina E. Catrina7Diana P. Bratu8City University of New YorkCity University of New YorkCity University of New YorkCity University of New YorkCity University of New YorkCity University of New YorkCity University of New YorkYeshiva UniversityCity University of New YorkStudy 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.http://dx.doi.org/10.1080/15476286.2023.2242650post transcriptional gene expression regulationoskar mrnaoskar mrnadrosophila oogenesiscupbruno 1p body
spellingShingle Livia V. Bayer
Samantha Milano
Stephen K. Formel
Harpreet Kaur
Rishi Ravichandran
Juan A. Cambeiro
Lizaveta Slinko
Irina E. Catrina
Diana P. Bratu
Cup is essential for oskar mRNA translational repression during early Drosophila oogenesis
RNA Biology
post transcriptional gene expression regulation
oskar mrna
oskar mrna
drosophila oogenesis
cup
bruno 1
p body
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 post transcriptional gene expression regulation
oskar mrna
oskar mrna
drosophila oogenesis
cup
bruno 1
p body
url http://dx.doi.org/10.1080/15476286.2023.2242650
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