A functional m 6 A‐RNA methylation pathway in the oyster Crassostrea gigas assumes epitranscriptomic regulation of lophotrochozoan development
International audience N6‐methyladenosine (m6A) is a prevalent epitranscriptomic mark in eukaryotic RNA, with crucial roles for mammalian and ecdysozoan development. Indeed, m6A‐RNA and the related protein machinery are important for splicing, translation, maternal‐to‐zygotic transition and cell dif...
Published in: | The FEBS Journal |
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Main Authors: | , , , , , |
Other Authors: | , , , , , , , , , |
Format: | Article in Journal/Newspaper |
Language: | English |
Published: |
HAL CCSD
2020
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Subjects: | |
Online Access: | https://hal.sorbonne-universite.fr/hal-02952460 https://hal.sorbonne-universite.fr/hal-02952460/document https://hal.sorbonne-universite.fr/hal-02952460/file/Franc%20et%20al.%20-%20A%20functional%20m6A-RNA%20methylation%20pathway%20in%20the%20oy.pdf https://doi.org/10.1111/febs.15500 |
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ftunivnantes:oai:HAL:hal-02952460v1 |
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record_format |
openpolar |
institution |
Open Polar |
collection |
Université de Nantes: HAL-UNIV-NANTES |
op_collection_id |
ftunivnantes |
language |
English |
topic |
development epitranscriptomics methylation oyster RNA acl [SDV.BA.ZI]Life Sciences [q-bio]/Animal biology/Invertebrate Zoology [SDV.BDD]Life Sciences [q-bio]/Development Biology [SDV.BBM.GTP]Life Sciences [q-bio]/Biochemistry Molecular Biology/Genomics [q-bio.GN] [SDE.BE]Environmental Sciences/Biodiversity and Ecology |
spellingShingle |
development epitranscriptomics methylation oyster RNA acl [SDV.BA.ZI]Life Sciences [q-bio]/Animal biology/Invertebrate Zoology [SDV.BDD]Life Sciences [q-bio]/Development Biology [SDV.BBM.GTP]Life Sciences [q-bio]/Biochemistry Molecular Biology/Genomics [q-bio.GN] [SDE.BE]Environmental Sciences/Biodiversity and Ecology Le Franc, Lorane Bernay, Benoit Petton, Bruno Since, Marc Favrel, Pascal Rivière, Guillaume A functional m 6 A‐RNA methylation pathway in the oyster Crassostrea gigas assumes epitranscriptomic regulation of lophotrochozoan development |
topic_facet |
development epitranscriptomics methylation oyster RNA acl [SDV.BA.ZI]Life Sciences [q-bio]/Animal biology/Invertebrate Zoology [SDV.BDD]Life Sciences [q-bio]/Development Biology [SDV.BBM.GTP]Life Sciences [q-bio]/Biochemistry Molecular Biology/Genomics [q-bio.GN] [SDE.BE]Environmental Sciences/Biodiversity and Ecology |
description |
International audience N6‐methyladenosine (m6A) is a prevalent epitranscriptomic mark in eukaryotic RNA, with crucial roles for mammalian and ecdysozoan development. Indeed, m6A‐RNA and the related protein machinery are important for splicing, translation, maternal‐to‐zygotic transition and cell differentiation. However, to date, the presence of an m6A‐RNA pathway remains unknown in more distant animals, questioning the evolution and significance of the epitranscriptomic regulation. Therefore, we investigated the m6A‐RNA pathway in the oyster Crassostrea gigas, a lophotrochozoan model whose development was demonstrated under strong epigenetic influence. Using mass spectrometry and dot blot assays, we demonstrated that m6A‐RNA is actually present in the oyster and displays variations throughout early oyster development, with the lowest levels at the end of cleavage. In parallel, by in silico analyses, we were able to characterize at the molecular level a complete and conserved putative m6A machinery. The expression levels of the identified putative m6A writers, erasers and readers were strongly regulated across oyster development. Finally, RNA pull‐down coupled to LC‐MS/MS allowed us to prove the actual presence of readers able to bind m6A‐RNA and exhibiting specific developmental patterns. Altogether, our results demonstrate the conservation of a complete m6A‐RNA pathway in the oyster and strongly suggest its implication in early developmental processes including MZT. This first demonstration and characterization of an epitranscriptomic regulation in a lophotrochozoan model, potentially involved in the embryogenesis, bring new insights into our understanding of developmental epigenetic processes and their evolution. |
author2 |
Biologie des Organismes et Ecosystèmes Aquatiques (BOREA) Université de Caen Normandie (UNICAEN) Normandie Université (NU)-Normandie Université (NU)-Muséum national d'Histoire naturelle (MNHN)-Institut de Recherche pour le Développement (IRD)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Université des Antilles (UA) Interactions Cellules Organismes Environnement (ICORE) Normandie Université (NU)-Normandie Université (NU)-CHU Caen Normandie Université (NU)-Tumorothèque de Caen Basse-Normandie (TCBN)-Tumorothèque de Caen Basse-Normandie (TCBN) Laboratoire des Sciences de l'Environnement Marin (LEMAR) (LEMAR) Institut de Recherche pour le Développement (IRD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Université de Brest (UBO)-Institut Universitaire Européen de la Mer (IUEM) Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS) Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER) |
format |
Article in Journal/Newspaper |
author |
Le Franc, Lorane Bernay, Benoit Petton, Bruno Since, Marc Favrel, Pascal Rivière, Guillaume |
author_facet |
Le Franc, Lorane Bernay, Benoit Petton, Bruno Since, Marc Favrel, Pascal Rivière, Guillaume |
author_sort |
Le Franc, Lorane |
title |
A functional m 6 A‐RNA methylation pathway in the oyster Crassostrea gigas assumes epitranscriptomic regulation of lophotrochozoan development |
title_short |
A functional m 6 A‐RNA methylation pathway in the oyster Crassostrea gigas assumes epitranscriptomic regulation of lophotrochozoan development |
title_full |
A functional m 6 A‐RNA methylation pathway in the oyster Crassostrea gigas assumes epitranscriptomic regulation of lophotrochozoan development |
title_fullStr |
A functional m 6 A‐RNA methylation pathway in the oyster Crassostrea gigas assumes epitranscriptomic regulation of lophotrochozoan development |
title_full_unstemmed |
A functional m 6 A‐RNA methylation pathway in the oyster Crassostrea gigas assumes epitranscriptomic regulation of lophotrochozoan development |
title_sort |
functional m 6 a‐rna methylation pathway in the oyster crassostrea gigas assumes epitranscriptomic regulation of lophotrochozoan development |
publisher |
HAL CCSD |
publishDate |
2020 |
url |
https://hal.sorbonne-universite.fr/hal-02952460 https://hal.sorbonne-universite.fr/hal-02952460/document https://hal.sorbonne-universite.fr/hal-02952460/file/Franc%20et%20al.%20-%20A%20functional%20m6A-RNA%20methylation%20pathway%20in%20the%20oy.pdf https://doi.org/10.1111/febs.15500 |
genre |
Crassostrea gigas |
genre_facet |
Crassostrea gigas |
op_source |
ISSN: 1742-464X EISSN: 1742-4658 FEBS Journal https://hal.sorbonne-universite.fr/hal-02952460 FEBS Journal, Wiley, In press, ⟨10.1111/febs.15500⟩ |
op_relation |
info:eu-repo/semantics/altIdentifier/doi/10.1111/febs.15500 hal-02952460 https://hal.sorbonne-universite.fr/hal-02952460 https://hal.sorbonne-universite.fr/hal-02952460/document https://hal.sorbonne-universite.fr/hal-02952460/file/Franc%20et%20al.%20-%20A%20functional%20m6A-RNA%20methylation%20pathway%20in%20the%20oy.pdf doi:10.1111/febs.15500 |
op_rights |
info:eu-repo/semantics/OpenAccess |
op_doi |
https://doi.org/10.1111/febs.15500 |
container_title |
The FEBS Journal |
container_volume |
288 |
container_issue |
5 |
container_start_page |
1696 |
op_container_end_page |
1711 |
_version_ |
1766394041119801344 |
spelling |
ftunivnantes:oai:HAL:hal-02952460v1 2023-05-15T15:58:19+02:00 A functional m 6 A‐RNA methylation pathway in the oyster Crassostrea gigas assumes epitranscriptomic regulation of lophotrochozoan development Le Franc, Lorane Bernay, Benoit Petton, Bruno Since, Marc Favrel, Pascal Rivière, Guillaume Biologie des Organismes et Ecosystèmes Aquatiques (BOREA) Université de Caen Normandie (UNICAEN) Normandie Université (NU)-Normandie Université (NU)-Muséum national d'Histoire naturelle (MNHN)-Institut de Recherche pour le Développement (IRD)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Université des Antilles (UA) Interactions Cellules Organismes Environnement (ICORE) Normandie Université (NU)-Normandie Université (NU)-CHU Caen Normandie Université (NU)-Tumorothèque de Caen Basse-Normandie (TCBN)-Tumorothèque de Caen Basse-Normandie (TCBN) Laboratoire des Sciences de l'Environnement Marin (LEMAR) (LEMAR) Institut de Recherche pour le Développement (IRD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Université de Brest (UBO)-Institut Universitaire Européen de la Mer (IUEM) Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS) Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER) 2020 https://hal.sorbonne-universite.fr/hal-02952460 https://hal.sorbonne-universite.fr/hal-02952460/document https://hal.sorbonne-universite.fr/hal-02952460/file/Franc%20et%20al.%20-%20A%20functional%20m6A-RNA%20methylation%20pathway%20in%20the%20oy.pdf https://doi.org/10.1111/febs.15500 en eng HAL CCSD Wiley info:eu-repo/semantics/altIdentifier/doi/10.1111/febs.15500 hal-02952460 https://hal.sorbonne-universite.fr/hal-02952460 https://hal.sorbonne-universite.fr/hal-02952460/document https://hal.sorbonne-universite.fr/hal-02952460/file/Franc%20et%20al.%20-%20A%20functional%20m6A-RNA%20methylation%20pathway%20in%20the%20oy.pdf doi:10.1111/febs.15500 info:eu-repo/semantics/OpenAccess ISSN: 1742-464X EISSN: 1742-4658 FEBS Journal https://hal.sorbonne-universite.fr/hal-02952460 FEBS Journal, Wiley, In press, ⟨10.1111/febs.15500⟩ development epitranscriptomics methylation oyster RNA acl [SDV.BA.ZI]Life Sciences [q-bio]/Animal biology/Invertebrate Zoology [SDV.BDD]Life Sciences [q-bio]/Development Biology [SDV.BBM.GTP]Life Sciences [q-bio]/Biochemistry Molecular Biology/Genomics [q-bio.GN] [SDE.BE]Environmental Sciences/Biodiversity and Ecology info:eu-repo/semantics/article Journal articles 2020 ftunivnantes https://doi.org/10.1111/febs.15500 2022-07-12T23:40:55Z International audience N6‐methyladenosine (m6A) is a prevalent epitranscriptomic mark in eukaryotic RNA, with crucial roles for mammalian and ecdysozoan development. Indeed, m6A‐RNA and the related protein machinery are important for splicing, translation, maternal‐to‐zygotic transition and cell differentiation. However, to date, the presence of an m6A‐RNA pathway remains unknown in more distant animals, questioning the evolution and significance of the epitranscriptomic regulation. Therefore, we investigated the m6A‐RNA pathway in the oyster Crassostrea gigas, a lophotrochozoan model whose development was demonstrated under strong epigenetic influence. Using mass spectrometry and dot blot assays, we demonstrated that m6A‐RNA is actually present in the oyster and displays variations throughout early oyster development, with the lowest levels at the end of cleavage. In parallel, by in silico analyses, we were able to characterize at the molecular level a complete and conserved putative m6A machinery. The expression levels of the identified putative m6A writers, erasers and readers were strongly regulated across oyster development. Finally, RNA pull‐down coupled to LC‐MS/MS allowed us to prove the actual presence of readers able to bind m6A‐RNA and exhibiting specific developmental patterns. Altogether, our results demonstrate the conservation of a complete m6A‐RNA pathway in the oyster and strongly suggest its implication in early developmental processes including MZT. This first demonstration and characterization of an epitranscriptomic regulation in a lophotrochozoan model, potentially involved in the embryogenesis, bring new insights into our understanding of developmental epigenetic processes and their evolution. Article in Journal/Newspaper Crassostrea gigas Université de Nantes: HAL-UNIV-NANTES The FEBS Journal 288 5 1696 1711 |