Histone Methylation Participates in Gene Expression Control during the Early Development of the Pacific Oyster Crassostrea gigas

Histone methylation patterns are important epigenetic regulators of mammalian development, notably through stem cell identity maintenance by chromatin remodeling and transcriptional control of pluripotency genes. But, the implications of histone marks are poorly understood in distant groups outside...

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Published in:Genes
Main Authors: Alexandre Fellous, Lorane Le Franc, Aude Jouaux, Didier Goux, Pascal Favrel, Guillaume Rivière
Format: Article in Journal/Newspaper
Language:English
Published: MDPI AG 2019
Subjects:
Online Access:https://doi.org/10.3390/genes10090695
https://doaj.org/article/3c21b383946c4ffebb1d3d9c47533bca
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spelling ftdoajarticles:oai:doaj.org/article:3c21b383946c4ffebb1d3d9c47533bca 2023-05-15T15:58:21+02:00 Histone Methylation Participates in Gene Expression Control during the Early Development of the Pacific Oyster Crassostrea gigas Alexandre Fellous Lorane Le Franc Aude Jouaux Didier Goux Pascal Favrel Guillaume Rivière 2019-09-01T00:00:00Z https://doi.org/10.3390/genes10090695 https://doaj.org/article/3c21b383946c4ffebb1d3d9c47533bca EN eng MDPI AG https://www.mdpi.com/2073-4425/10/9/695 https://doaj.org/toc/2073-4425 2073-4425 doi:10.3390/genes10090695 https://doaj.org/article/3c21b383946c4ffebb1d3d9c47533bca Genes, Vol 10, Iss 9, p 695 (2019) epigenetics histone modifications methylstat embryos mollusk H3K4 H3K9 H3K27 H3K36 Genetics QH426-470 article 2019 ftdoajarticles https://doi.org/10.3390/genes10090695 2022-12-31T11:10:22Z Histone methylation patterns are important epigenetic regulators of mammalian development, notably through stem cell identity maintenance by chromatin remodeling and transcriptional control of pluripotency genes. But, the implications of histone marks are poorly understood in distant groups outside vertebrates and ecdysozoan models. However, the development of the Pacific oyster Crassostrea gigas is under the strong epigenetic influence of DNA methylation, and Jumonji histone-demethylase orthologues are highly expressed during C . gigas early life. This suggests a physiological relevance of histone methylation regulation in oyster development, raising the question of functional conservation of this epigenetic pathway in lophotrochozoan. Quantification of histone methylation using fluorescent ELISAs during oyster early life indicated significant variations in monomethyl histone H3 lysine 4 (H3K4me), an overall decrease in H3K9 mono- and tri-methylations, and in H3K36 methylations, respectively, whereas no significant modification could be detected in H3K27 methylation. Early in vivo treatment with the JmjC-specific inhibitor Methylstat induced hypermethylation of all the examined histone H3 lysines and developmental alterations as revealed by scanning electronic microscopy. Using microarrays, we identified 376 genes that were differentially expressed under methylstat treatment, which expression patterns could discriminate between samples as indicated by principal component analysis. Furthermore, Gene Ontology revealed that these genes were related to processes potentially important for embryonic stages such as binding, cell differentiation and development. These results suggest an important physiological significance of histone methylation in the oyster embryonic and larval life, providing, to our knowledge, the first insights into epigenetic regulation by histone methylation in lophotrochozoan development. Article in Journal/Newspaper Crassostrea gigas Pacific oyster Directory of Open Access Journals: DOAJ Articles Pacific Genes 10 9 695
institution Open Polar
collection Directory of Open Access Journals: DOAJ Articles
op_collection_id ftdoajarticles
language English
topic epigenetics
histone modifications
methylstat
embryos
mollusk
H3K4
H3K9
H3K27
H3K36
Genetics
QH426-470
spellingShingle epigenetics
histone modifications
methylstat
embryos
mollusk
H3K4
H3K9
H3K27
H3K36
Genetics
QH426-470
Alexandre Fellous
Lorane Le Franc
Aude Jouaux
Didier Goux
Pascal Favrel
Guillaume Rivière
Histone Methylation Participates in Gene Expression Control during the Early Development of the Pacific Oyster Crassostrea gigas
topic_facet epigenetics
histone modifications
methylstat
embryos
mollusk
H3K4
H3K9
H3K27
H3K36
Genetics
QH426-470
description Histone methylation patterns are important epigenetic regulators of mammalian development, notably through stem cell identity maintenance by chromatin remodeling and transcriptional control of pluripotency genes. But, the implications of histone marks are poorly understood in distant groups outside vertebrates and ecdysozoan models. However, the development of the Pacific oyster Crassostrea gigas is under the strong epigenetic influence of DNA methylation, and Jumonji histone-demethylase orthologues are highly expressed during C . gigas early life. This suggests a physiological relevance of histone methylation regulation in oyster development, raising the question of functional conservation of this epigenetic pathway in lophotrochozoan. Quantification of histone methylation using fluorescent ELISAs during oyster early life indicated significant variations in monomethyl histone H3 lysine 4 (H3K4me), an overall decrease in H3K9 mono- and tri-methylations, and in H3K36 methylations, respectively, whereas no significant modification could be detected in H3K27 methylation. Early in vivo treatment with the JmjC-specific inhibitor Methylstat induced hypermethylation of all the examined histone H3 lysines and developmental alterations as revealed by scanning electronic microscopy. Using microarrays, we identified 376 genes that were differentially expressed under methylstat treatment, which expression patterns could discriminate between samples as indicated by principal component analysis. Furthermore, Gene Ontology revealed that these genes were related to processes potentially important for embryonic stages such as binding, cell differentiation and development. These results suggest an important physiological significance of histone methylation in the oyster embryonic and larval life, providing, to our knowledge, the first insights into epigenetic regulation by histone methylation in lophotrochozoan development.
format Article in Journal/Newspaper
author Alexandre Fellous
Lorane Le Franc
Aude Jouaux
Didier Goux
Pascal Favrel
Guillaume Rivière
author_facet Alexandre Fellous
Lorane Le Franc
Aude Jouaux
Didier Goux
Pascal Favrel
Guillaume Rivière
author_sort Alexandre Fellous
title Histone Methylation Participates in Gene Expression Control during the Early Development of the Pacific Oyster Crassostrea gigas
title_short Histone Methylation Participates in Gene Expression Control during the Early Development of the Pacific Oyster Crassostrea gigas
title_full Histone Methylation Participates in Gene Expression Control during the Early Development of the Pacific Oyster Crassostrea gigas
title_fullStr Histone Methylation Participates in Gene Expression Control during the Early Development of the Pacific Oyster Crassostrea gigas
title_full_unstemmed Histone Methylation Participates in Gene Expression Control during the Early Development of the Pacific Oyster Crassostrea gigas
title_sort histone methylation participates in gene expression control during the early development of the pacific oyster crassostrea gigas
publisher MDPI AG
publishDate 2019
url https://doi.org/10.3390/genes10090695
https://doaj.org/article/3c21b383946c4ffebb1d3d9c47533bca
geographic Pacific
geographic_facet Pacific
genre Crassostrea gigas
Pacific oyster
genre_facet Crassostrea gigas
Pacific oyster
op_source Genes, Vol 10, Iss 9, p 695 (2019)
op_relation https://www.mdpi.com/2073-4425/10/9/695
https://doaj.org/toc/2073-4425
2073-4425
doi:10.3390/genes10090695
https://doaj.org/article/3c21b383946c4ffebb1d3d9c47533bca
op_doi https://doi.org/10.3390/genes10090695
container_title Genes
container_volume 10
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container_start_page 695
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