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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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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