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 |
---|---|
Main Authors: | , , , , , |
Other Authors: | , , , , , , , , , , , |
Format: | Article in Journal/Newspaper |
Language: | English |
Published: |
HAL CCSD
2020
|
Subjects: | |
Online Access: | https://doi.org/10.1111/febs.15500 https://hal.sorbonne-universite.fr/hal-02952460/file/Franc%20et%20al.%20-%20A%20functional%20m6A-RNA%20methylation%20pathway%20in%20the%20oy.pdf https://hal.sorbonne-universite.fr/hal-02952460 |
id |
fttriple:oai:gotriple.eu:10670/1.41ncot |
---|---|
record_format |
openpolar |
institution |
Open Polar |
collection |
Unknown |
op_collection_id |
fttriple |
language |
English |
topic |
methylation epitranscriptomics development oyster RNA acl stat archeo |
spellingShingle |
methylation epitranscriptomics development oyster RNA acl stat archeo 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 |
methylation epitranscriptomics development oyster RNA acl stat archeo |
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) Centre National de la Recherche Scientifique (CNRS)-Université des Antilles (UA)-Muséum national d'Histoire naturelle (MNHN)-Institut de Recherche pour le Développement (IRD)-Sorbonne Université (SU)-Université de Caen Normandie (UNICAEN) Normandie Université (NU)-Normandie Université (NU) Interactions Cellules Organismes Environnement (ICORE) CHU Caen Normandie Université (NU)-Tumorothèque de Caen Basse-Normandie (TCBN)-Normandie Université (NU)-Tumorothèque de Caen Basse-Normandie (TCBN)-Université de Caen Normandie (UNICAEN) Normandie Université (NU) 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 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 - Brest (IFREMER Centre de Bretagne) 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://doi.org/10.1111/febs.15500 https://hal.sorbonne-universite.fr/hal-02952460/file/Franc%20et%20al.%20-%20A%20functional%20m6A-RNA%20methylation%20pathway%20in%20the%20oy.pdf https://hal.sorbonne-universite.fr/hal-02952460 |
genre |
Crassostrea gigas |
genre_facet |
Crassostrea gigas |
op_source |
Hyper Article en Ligne - Sciences de l'Homme et de la Société ISSN: 1742-464X EISSN: 1742-4658 FEBS Journal FEBS Journal, Wiley, In press, ⟨10.1111/febs.15500⟩ |
op_relation |
hal-02952460 doi:10.1111/febs.15500 10670/1.41ncot https://hal.sorbonne-universite.fr/hal-02952460/file/Franc%20et%20al.%20-%20A%20functional%20m6A-RNA%20methylation%20pathway%20in%20the%20oy.pdf https://hal.sorbonne-universite.fr/hal-02952460 |
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_ |
1766394002625527808 |
spelling |
fttriple:oai:gotriple.eu:10670/1.41ncot 2023-05-15T15:58:16+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) Centre National de la Recherche Scientifique (CNRS)-Université des Antilles (UA)-Muséum national d'Histoire naturelle (MNHN)-Institut de Recherche pour le Développement (IRD)-Sorbonne Université (SU)-Université de Caen Normandie (UNICAEN) Normandie Université (NU)-Normandie Université (NU) Interactions Cellules Organismes Environnement (ICORE) CHU Caen Normandie Université (NU)-Tumorothèque de Caen Basse-Normandie (TCBN)-Normandie Université (NU)-Tumorothèque de Caen Basse-Normandie (TCBN)-Université de Caen Normandie (UNICAEN) Normandie Université (NU) 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 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 - Brest (IFREMER Centre de Bretagne) Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER) 2020-01-01 https://doi.org/10.1111/febs.15500 https://hal.sorbonne-universite.fr/hal-02952460/file/Franc%20et%20al.%20-%20A%20functional%20m6A-RNA%20methylation%20pathway%20in%20the%20oy.pdf https://hal.sorbonne-universite.fr/hal-02952460 en eng HAL CCSD Wiley hal-02952460 doi:10.1111/febs.15500 10670/1.41ncot https://hal.sorbonne-universite.fr/hal-02952460/file/Franc%20et%20al.%20-%20A%20functional%20m6A-RNA%20methylation%20pathway%20in%20the%20oy.pdf https://hal.sorbonne-universite.fr/hal-02952460 Hyper Article en Ligne - Sciences de l'Homme et de la Société ISSN: 1742-464X EISSN: 1742-4658 FEBS Journal FEBS Journal, Wiley, In press, ⟨10.1111/febs.15500⟩ methylation epitranscriptomics development oyster RNA acl stat archeo Journal Article https://vocabularies.coar-repositories.org/resource_types/c_6501/ 2020 fttriple https://doi.org/10.1111/febs.15500 2023-01-22T17:26:26Z 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 Unknown The FEBS Journal 288 5 1696 1711 |