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

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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Main Authors: Alexandre Fellous, Lorane Le Franc, Aude Jouaux, Didier Goux, Pascal Favrel, Guillaume Rivière
Format: Article
Language:English
Published: MDPI AG 2019-09-01
Series:Genes
Subjects:
Online Access:https://www.mdpi.com/2073-4425/10/9/695
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spelling doaj-3c21b383946c4ffebb1d3d9c47533bca2020-11-25T02:01:01ZengMDPI AGGenes2073-44252019-09-0110969510.3390/genes10090695genes10090695Histone Methylation Participates in Gene Expression Control during the Early Development of the Pacific Oyster <em>Crassostrea gigas</em>Alexandre Fellous0Lorane Le Franc1Aude Jouaux2Didier Goux3Pascal Favrel4Guillaume Rivière5Unité de Formation et de Recherches (UFR) des sciences, Université de Caen Normandie, 14032 Caen CEDEX, FranceUnité de Formation et de Recherches (UFR) des sciences, Université de Caen Normandie, 14032 Caen CEDEX, FranceUnité de Formation et de Recherches (UFR) des sciences, Université de Caen Normandie, 14032 Caen CEDEX, FranceUnité de Formation et de Recherches (UFR) des sciences, Université de Caen Normandie, 14032 Caen CEDEX, FranceUnité de Formation et de Recherches (UFR) des sciences, Université de Caen Normandie, 14032 Caen CEDEX, FranceUnité de Formation et de Recherches (UFR) des sciences, Université de Caen Normandie, 14032 Caen CEDEX, FranceHistone 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 <i>Crassostrea gigas</i> is under the strong epigenetic influence of DNA methylation, and <i>Jumonji</i> histone-demethylase orthologues are highly expressed during <i>C</i>. <i>gigas</i> 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.https://www.mdpi.com/2073-4425/10/9/695epigeneticshistone modificationsmethylstatembryosmolluskH3K4H3K9H3K27H3K36
collection DOAJ
language English
format Article
sources DOAJ
author Alexandre Fellous
Lorane Le Franc
Aude Jouaux
Didier Goux
Pascal Favrel
Guillaume Rivière
spellingShingle 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 <em>Crassostrea gigas</em>
Genes
epigenetics
histone modifications
methylstat
embryos
mollusk
H3K4
H3K9
H3K27
H3K36
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 <em>Crassostrea gigas</em>
title_short Histone Methylation Participates in Gene Expression Control during the Early Development of the Pacific Oyster <em>Crassostrea gigas</em>
title_full Histone Methylation Participates in Gene Expression Control during the Early Development of the Pacific Oyster <em>Crassostrea gigas</em>
title_fullStr Histone Methylation Participates in Gene Expression Control during the Early Development of the Pacific Oyster <em>Crassostrea gigas</em>
title_full_unstemmed Histone Methylation Participates in Gene Expression Control during the Early Development of the Pacific Oyster <em>Crassostrea gigas</em>
title_sort histone methylation participates in gene expression control during the early development of the pacific oyster <em>crassostrea gigas</em>
publisher MDPI AG
series Genes
issn 2073-4425
publishDate 2019-09-01
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 <i>Crassostrea gigas</i> is under the strong epigenetic influence of DNA methylation, and <i>Jumonji</i> histone-demethylase orthologues are highly expressed during <i>C</i>. <i>gigas</i> 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.
topic epigenetics
histone modifications
methylstat
embryos
mollusk
H3K4
H3K9
H3K27
H3K36
url https://www.mdpi.com/2073-4425/10/9/695
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