DNA Methylation Is Crucial for the Early Development in the Oyster C. gigas

International audience In vertebrates, epigenetic modifications influence gene transcription, and an appropriate DNA methylation is critical in development. Indeed, a precise temporal and spatial pattern of early gene expression is mandatory for a normal embryogenesis. However, such a regulation and...

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Published in:Marine Biotechnology
Main Authors: Riviere, Guillaume, Wu, Guan-Chung, Fellous, Alexandre, Goux, Didier, Sourdaine, Pascal, Favrel, Pascal
Other Authors: Biologie des mollusques marins et des écosystèmes associés (BioMEA), Université de Caen Normandie (UNICAEN), Normandie Université (NU)-Normandie Université (NU)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Centre National de la Recherche Scientifique (CNRS), National Taiwan Ocean University (NTOU), 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)
Format: Article in Journal/Newspaper
Language:English
Published: HAL CCSD 2013
Subjects:
Online Access:https://hal-normandie-univ.archives-ouvertes.fr/hal-02296498
https://doi.org/10.1007/s10126-013-9523-2
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spelling ftsorbonneuniv:oai:HAL:hal-02296498v1 2023-05-15T15:58:53+02:00 DNA Methylation Is Crucial for the Early Development in the Oyster C. gigas Riviere, Guillaume Wu, Guan-Chung Fellous, Alexandre Goux, Didier Sourdaine, Pascal Favrel, Pascal Biologie des mollusques marins et des écosystèmes associés (BioMEA) Université de Caen Normandie (UNICAEN) Normandie Université (NU)-Normandie Université (NU)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Centre National de la Recherche Scientifique (CNRS) National Taiwan Ocean University (NTOU) 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) 2013-12 https://hal-normandie-univ.archives-ouvertes.fr/hal-02296498 https://doi.org/10.1007/s10126-013-9523-2 en eng HAL CCSD Springer Verlag info:eu-repo/semantics/altIdentifier/doi/10.1007/s10126-013-9523-2 hal-02296498 https://hal-normandie-univ.archives-ouvertes.fr/hal-02296498 doi:10.1007/s10126-013-9523-2 ISSN: 1436-2228 EISSN: 1436-2236 Marine Biotechnology https://hal-normandie-univ.archives-ouvertes.fr/hal-02296498 Marine Biotechnology, Springer Verlag, 2013, 15 (6), pp.739-753. ⟨10.1007/s10126-013-9523-2⟩ Epigenetics Development Methylation Homeobox Evolution [SDV]Life Sciences [q-bio] info:eu-repo/semantics/article Journal articles 2013 ftsorbonneuniv https://doi.org/10.1007/s10126-013-9523-2 2022-03-22T23:54:11Z International audience In vertebrates, epigenetic modifications influence gene transcription, and an appropriate DNA methylation is critical in development. Indeed, a precise temporal and spatial pattern of early gene expression is mandatory for a normal embryogenesis. However, such a regulation and its underlying mechanisms remain poorly understood in more distant organisms such as Lophotrochozoa. Thus, despite DNA in the oyster genome being methylated, the role of DNA methylation in development is unknown. To clarify this point, oyster genomic DNA was examined during early embryogenesis and found differentially methylated. Reverse transcriptase quantitative polymerase chain reaction indicated stage-specific levels of transcripts encoding DNA-methyltransferase (DNMT) and methyl-binding domain proteins. In addition, as highlighted by electronic microscopy and immunohistochemistry, the DNMT inhibitor 5-aza-cytidine induced alterations in the quantity and the localisation of methylated DNA and severe dose-dependent development alterations and was lethal after zygotic genome reinitiation. Furthermore, methyl-DNA-immunoprecipitation–quantitative polymerase chain reaction revealed that the transcription level of most of the homeobox gene orthologues examined, but not of the other early genes investigated, was inversely correlated with their specific DNA methylation. Altogether, our results demonstrate that DNA methylation influences gene expression in Crassostrea gigas and is critical for oyster development, possibly by specifically controlling the transcription level of homeobox orthologues. These findings provide evidence for the importance of epigenetic regulation of development in Lophotrochozoans and bring new insights into the early life of C. gigas, one of the most important aquaculture resources worldwide. Article in Journal/Newspaper Crassostrea gigas HAL Sorbonne Université Marine Biotechnology 15 6 739 753
institution Open Polar
collection HAL Sorbonne Université
op_collection_id ftsorbonneuniv
language English
topic Epigenetics
Development
Methylation
Homeobox
Evolution
[SDV]Life Sciences [q-bio]
spellingShingle Epigenetics
Development
Methylation
Homeobox
Evolution
[SDV]Life Sciences [q-bio]
Riviere, Guillaume
Wu, Guan-Chung
Fellous, Alexandre
Goux, Didier
Sourdaine, Pascal
Favrel, Pascal
DNA Methylation Is Crucial for the Early Development in the Oyster C. gigas
topic_facet Epigenetics
Development
Methylation
Homeobox
Evolution
[SDV]Life Sciences [q-bio]
description International audience In vertebrates, epigenetic modifications influence gene transcription, and an appropriate DNA methylation is critical in development. Indeed, a precise temporal and spatial pattern of early gene expression is mandatory for a normal embryogenesis. However, such a regulation and its underlying mechanisms remain poorly understood in more distant organisms such as Lophotrochozoa. Thus, despite DNA in the oyster genome being methylated, the role of DNA methylation in development is unknown. To clarify this point, oyster genomic DNA was examined during early embryogenesis and found differentially methylated. Reverse transcriptase quantitative polymerase chain reaction indicated stage-specific levels of transcripts encoding DNA-methyltransferase (DNMT) and methyl-binding domain proteins. In addition, as highlighted by electronic microscopy and immunohistochemistry, the DNMT inhibitor 5-aza-cytidine induced alterations in the quantity and the localisation of methylated DNA and severe dose-dependent development alterations and was lethal after zygotic genome reinitiation. Furthermore, methyl-DNA-immunoprecipitation–quantitative polymerase chain reaction revealed that the transcription level of most of the homeobox gene orthologues examined, but not of the other early genes investigated, was inversely correlated with their specific DNA methylation. Altogether, our results demonstrate that DNA methylation influences gene expression in Crassostrea gigas and is critical for oyster development, possibly by specifically controlling the transcription level of homeobox orthologues. These findings provide evidence for the importance of epigenetic regulation of development in Lophotrochozoans and bring new insights into the early life of C. gigas, one of the most important aquaculture resources worldwide.
author2 Biologie des mollusques marins et des écosystèmes associés (BioMEA)
Université de Caen Normandie (UNICAEN)
Normandie Université (NU)-Normandie Université (NU)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Centre National de la Recherche Scientifique (CNRS)
National Taiwan Ocean University (NTOU)
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)
format Article in Journal/Newspaper
author Riviere, Guillaume
Wu, Guan-Chung
Fellous, Alexandre
Goux, Didier
Sourdaine, Pascal
Favrel, Pascal
author_facet Riviere, Guillaume
Wu, Guan-Chung
Fellous, Alexandre
Goux, Didier
Sourdaine, Pascal
Favrel, Pascal
author_sort Riviere, Guillaume
title DNA Methylation Is Crucial for the Early Development in the Oyster C. gigas
title_short DNA Methylation Is Crucial for the Early Development in the Oyster C. gigas
title_full DNA Methylation Is Crucial for the Early Development in the Oyster C. gigas
title_fullStr DNA Methylation Is Crucial for the Early Development in the Oyster C. gigas
title_full_unstemmed DNA Methylation Is Crucial for the Early Development in the Oyster C. gigas
title_sort dna methylation is crucial for the early development in the oyster c. gigas
publisher HAL CCSD
publishDate 2013
url https://hal-normandie-univ.archives-ouvertes.fr/hal-02296498
https://doi.org/10.1007/s10126-013-9523-2
genre Crassostrea gigas
genre_facet Crassostrea gigas
op_source ISSN: 1436-2228
EISSN: 1436-2236
Marine Biotechnology
https://hal-normandie-univ.archives-ouvertes.fr/hal-02296498
Marine Biotechnology, Springer Verlag, 2013, 15 (6), pp.739-753. ⟨10.1007/s10126-013-9523-2⟩
op_relation info:eu-repo/semantics/altIdentifier/doi/10.1007/s10126-013-9523-2
hal-02296498
https://hal-normandie-univ.archives-ouvertes.fr/hal-02296498
doi:10.1007/s10126-013-9523-2
op_doi https://doi.org/10.1007/s10126-013-9523-2
container_title Marine Biotechnology
container_volume 15
container_issue 6
container_start_page 739
op_container_end_page 753
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