Micronutrient supplementation affects DNA methylation in male gonads with potential intergenerational epigenetic inheritance involving the embryonic development through glutamate receptor-associated genes
18 pages, 5 figures, 6 tables, supplementary information https://doi.org/10.1186/s12864-022-08348-4
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Format: | artículo biblioteca |
Language: | English |
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BioMed Central
2022-02
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Subjects: | Atlantic salmon, Micronutrient, Epigenetics, DNA methylation, Intergenerational inheritance, Male germline, Gonad, Glutamate receptor, GRIN3A, HDAC2, Conserve and sustainably use the oceans, seas and marine resources for sustainable development, |
Online Access: | http://hdl.handle.net/10261/357682 http://dx.doi.org/10.13039/501100000780 |
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dig-icm-es-10261-3576822024-05-21T07:53:48Z Micronutrient supplementation affects DNA methylation in male gonads with potential intergenerational epigenetic inheritance involving the embryonic development through glutamate receptor-associated genes Saito, Takaya Whatmore, Paul Taylor, John F. Fernandes, Jorge M. O. Adam, Anne‑Catrin Tocher, Douglas R. Espe, Marit Skjærven, Kaja H. European Commission Atlantic salmon Micronutrient Epigenetics DNA methylation Intergenerational inheritance Male germline Gonad Glutamate receptor GRIN3A HDAC2 Conserve and sustainably use the oceans, seas and marine resources for sustainable development 18 pages, 5 figures, 6 tables, supplementary information https://doi.org/10.1186/s12864-022-08348-4 Background: DNA methylation has an important role in intergenerational inheritance. An increasing number of studies have reported evidence of germline inheritance of DNA methylation induced by nutritional signals in mammals. Vitamins and minerals as micronutrients contribute to growth performance in vertebrates, including Atlantic salmon (Salmo salar), and also have a role in epigenetics as environmental factors that alter DNA methylation status. It is important to understand whether micronutrients in the paternal diet can influence the offspring through alterations of DNA methylation signatures in male germ cells. Results: Here, we show the effect of micronutrient supplementation on DNA methylation profiles in the male gonad through a whole life cycle feeding trial of Atlantic salmon fed three graded levels of micronutrient components. Our results strongly indicate that micronutrient supplementation affects the DNA methylation status of genes associated with cell signalling, synaptic signalling, and embryonic development. In particular, it substantially affects DNA methylation status in the promoter region of a glutamate receptor gene, glutamate receptor ionotropic, NMDA 3A-like (grin3a-like), when the fish are fed both medium and high doses of micronutrients. Furthermore, two transcription factors, histone deacetylase 2 (hdac2) and a zinc finger protein, bind to the hyper-methylated site in the grin3a-like promoter. An estimated function of hdac2 together with a zinc finger indicates that grin3a-like has a potential role in intergenerational epigenetic inheritance and the regulation of embryonic development affected by paternal diet. Conclusions: The present study demonstrates alterations of gene expression patterns and DNA methylation signatures in the male gonad when Atlantic salmon are fed different levels of micronutrients. Alterations of gene expression patterns are of great interest because the gonads are supposed to have limited metabolic activities compared to other organs, whereas alterations of DNA methylation signatures are of great importance in the field of nutritional epigenetics because the signatures affected by nutrition could be transferred to the next generation. We provide extensive data resources for future work in the context of potential intergenerational inheritance through the male germline This study was funded by the European Commission FP7 Integrated Project No. 288925, Advanced Research Initiatives for Nutrition & Aquaculture (ARRAINA) for the feeding trial, sampling and the analysis of growth measurement. The study was also funded by the Norwegian Research Council, project no: 267787 (NutrEpi) for RNA-seq and RRBS sequencing, data analyses, and writing the manuscript Peer reviewed 2024-05-21T07:53:47Z 2024-05-21T07:53:47Z 2022-02 artículo http://purl.org/coar/resource_type/c_6501 BMC Genomics 23: 115 (2022) http://hdl.handle.net/10261/357682 10.1186/s12864-022-08348-4 1471-2164 http://dx.doi.org/10.13039/501100000780 en #PLACEHOLDER_PARENT_METADATA_VALUE# info:eu-repo/grantAgreement/EC/FP7/288925 Publisher's version https://doi.org/10.1186/s12864-022-08348-4 No open BioMed Central |
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Atlantic salmon Micronutrient Epigenetics DNA methylation Intergenerational inheritance Male germline Gonad Glutamate receptor GRIN3A HDAC2 Conserve and sustainably use the oceans, seas and marine resources for sustainable development Atlantic salmon Micronutrient Epigenetics DNA methylation Intergenerational inheritance Male germline Gonad Glutamate receptor GRIN3A HDAC2 Conserve and sustainably use the oceans, seas and marine resources for sustainable development |
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Atlantic salmon Micronutrient Epigenetics DNA methylation Intergenerational inheritance Male germline Gonad Glutamate receptor GRIN3A HDAC2 Conserve and sustainably use the oceans, seas and marine resources for sustainable development Atlantic salmon Micronutrient Epigenetics DNA methylation Intergenerational inheritance Male germline Gonad Glutamate receptor GRIN3A HDAC2 Conserve and sustainably use the oceans, seas and marine resources for sustainable development Saito, Takaya Whatmore, Paul Taylor, John F. Fernandes, Jorge M. O. Adam, Anne‑Catrin Tocher, Douglas R. Espe, Marit Skjærven, Kaja H. Micronutrient supplementation affects DNA methylation in male gonads with potential intergenerational epigenetic inheritance involving the embryonic development through glutamate receptor-associated genes |
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18 pages, 5 figures, 6 tables, supplementary information https://doi.org/10.1186/s12864-022-08348-4 |
author2 |
European Commission |
author_facet |
European Commission Saito, Takaya Whatmore, Paul Taylor, John F. Fernandes, Jorge M. O. Adam, Anne‑Catrin Tocher, Douglas R. Espe, Marit Skjærven, Kaja H. |
format |
artículo |
topic_facet |
Atlantic salmon Micronutrient Epigenetics DNA methylation Intergenerational inheritance Male germline Gonad Glutamate receptor GRIN3A HDAC2 Conserve and sustainably use the oceans, seas and marine resources for sustainable development |
author |
Saito, Takaya Whatmore, Paul Taylor, John F. Fernandes, Jorge M. O. Adam, Anne‑Catrin Tocher, Douglas R. Espe, Marit Skjærven, Kaja H. |
author_sort |
Saito, Takaya |
title |
Micronutrient supplementation affects DNA methylation in male gonads with potential intergenerational epigenetic inheritance involving the embryonic development through glutamate receptor-associated genes |
title_short |
Micronutrient supplementation affects DNA methylation in male gonads with potential intergenerational epigenetic inheritance involving the embryonic development through glutamate receptor-associated genes |
title_full |
Micronutrient supplementation affects DNA methylation in male gonads with potential intergenerational epigenetic inheritance involving the embryonic development through glutamate receptor-associated genes |
title_fullStr |
Micronutrient supplementation affects DNA methylation in male gonads with potential intergenerational epigenetic inheritance involving the embryonic development through glutamate receptor-associated genes |
title_full_unstemmed |
Micronutrient supplementation affects DNA methylation in male gonads with potential intergenerational epigenetic inheritance involving the embryonic development through glutamate receptor-associated genes |
title_sort |
micronutrient supplementation affects dna methylation in male gonads with potential intergenerational epigenetic inheritance involving the embryonic development through glutamate receptor-associated genes |
publisher |
BioMed Central |
publishDate |
2022-02 |
url |
http://hdl.handle.net/10261/357682 http://dx.doi.org/10.13039/501100000780 |
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