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: Text
Language:English
Published: Multidisciplinary Digital Publishing Institute 2019
Subjects:
Online Access:https://doi.org/10.3390/genes10090695
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spelling ftmdpi:oai:mdpi.com:/2073-4425/10/9/695/ 2023-08-20T04:06:03+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 agris 2019-09-10 application/pdf https://doi.org/10.3390/genes10090695 EN eng Multidisciplinary Digital Publishing Institute Population and Evolutionary Genetics and Genomics https://dx.doi.org/10.3390/genes10090695 https://creativecommons.org/licenses/by/4.0/ Genes; Volume 10; Issue 9; Pages: 695 epigenetics histone modifications methylstat embryos mollusk H3K4 H3K9 H3K27 H3K36 Text 2019 ftmdpi https://doi.org/10.3390/genes10090695 2023-07-31T22:35:46Z 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. Text Crassostrea gigas Pacific oyster MDPI Open Access Publishing Pacific Genes 10 9 695
institution Open Polar
collection MDPI Open Access Publishing
op_collection_id ftmdpi
language English
topic epigenetics
histone modifications
methylstat
embryos
mollusk
H3K4
H3K9
H3K27
H3K36
spellingShingle epigenetics
histone modifications
methylstat
embryos
mollusk
H3K4
H3K9
H3K27
H3K36
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
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 Text
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 Multidisciplinary Digital Publishing Institute
publishDate 2019
url https://doi.org/10.3390/genes10090695
op_coverage agris
geographic Pacific
geographic_facet Pacific
genre Crassostrea gigas
Pacific oyster
genre_facet Crassostrea gigas
Pacific oyster
op_source Genes; Volume 10; Issue 9; Pages: 695
op_relation Population and Evolutionary Genetics and Genomics
https://dx.doi.org/10.3390/genes10090695
op_rights https://creativecommons.org/licenses/by/4.0/
op_doi https://doi.org/10.3390/genes10090695
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