Glufosinate-Ammonium Induced Aberrant Histone Modifications in Mouse Sperm Are Concordant With Transcriptome in Preimplantation Embryos
Glufosinate-ammonium (GLA) is a widely used herbicide with emerging concern over its male reproductive toxicity. Abnormalities in sperm histone modification induced by GLA exposure observed in our previous study aroused our interest in whether such alterations could further affect embryonic gene exp...
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| Format: | Article |
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Frontiers Media S.A.
2022-01-01
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| Series: | Frontiers in Physiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fphys.2021.819856/full |
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| author | Xuan Ma Xuan Ma Yun Fan Yun Fan Yun Fan Wenwen Xiao Wenwen Xiao Xingwang Ding Xingwang Ding Weiyue Hu Weiyue Hu Yankai Xia Yankai Xia |
| author_facet | Xuan Ma Xuan Ma Yun Fan Yun Fan Yun Fan Wenwen Xiao Wenwen Xiao Xingwang Ding Xingwang Ding Weiyue Hu Weiyue Hu Yankai Xia Yankai Xia |
| author_sort | Xuan Ma |
| collection | DOAJ |
| description | Glufosinate-ammonium (GLA) is a widely used herbicide with emerging concern over its male reproductive toxicity. Abnormalities in sperm histone modification induced by GLA exposure observed in our previous study aroused our interest in whether such alterations could further affect embryonic gene expression. Here we administered adult male mice with 0.2 mg/kg⋅day of GLA for 5 weeks to collect their sperm or 4-cell embryos after copulation. Cleavage Under Targets and Tagmentation (CUT&Tag) sequencing showed alterations of sperm H3 lysine 4 trimethylation (H3K4me3) and histone H3 lysine 27 acetylation (H3K27ac), which are active histone modification marks involved in embryo development, while RNA sequencing identified differentially expressed genes in 4-cell embryos. Differentially H3K4me3 and H3K27ac occupied regions were mainly distributed at the gene promoters and putative enhancers, and were enriched in pathways related to the immune system and nervous system. Integrative analysis of these sequencing data showed that genes such as Mgl2 with increased H3K4me3 and H3K27ac in sperm were up-regulated in embryos, and vice versa for genes such as Dcn. Additionally, differentially occupied H3K4me3 and H3K27ac in sperm were linked to gene expression changes in both paternal and maternal alleles of 4-cell embryos. In conclusion, GLA-induced changes in sperm H3K4me3 and H3K27ac are concordant with gene expression in preimplantation embryos, which might further affect embryo development and offspring health. |
| first_indexed | 2024-04-11T18:28:38Z |
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| issn | 1664-042X |
| language | English |
| last_indexed | 2024-04-11T18:28:38Z |
| publishDate | 2022-01-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Physiology |
| spelling | doaj.art-571fe9ab0a694167919b0cb57251029a2022-12-22T04:09:32ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2022-01-011210.3389/fphys.2021.819856819856Glufosinate-Ammonium Induced Aberrant Histone Modifications in Mouse Sperm Are Concordant With Transcriptome in Preimplantation EmbryosXuan Ma0Xuan Ma1Yun Fan2Yun Fan3Yun Fan4Wenwen Xiao5Wenwen Xiao6Xingwang Ding7Xingwang Ding8Weiyue Hu9Weiyue Hu10Yankai Xia11Yankai Xia12State Key Laboratory of Reproductive Medicine, Center for Global Health, School of Public Health, Nanjing Medical University, Nanjing, ChinaKey Laboratory of Modern Toxicology of Ministry of Education, School of Public Health, Nanjing Medical University, Nanjing, ChinaState Key Laboratory of Reproductive Medicine, Center for Global Health, School of Public Health, Nanjing Medical University, Nanjing, ChinaKey Laboratory of Modern Toxicology of Ministry of Education, School of Public Health, Nanjing Medical University, Nanjing, ChinaDepartment of Microbes and Infection, School of Public Health, Nanjing Medical University, Nanjing, ChinaState Key Laboratory of Reproductive Medicine, Center for Global Health, School of Public Health, Nanjing Medical University, Nanjing, ChinaKey Laboratory of Modern Toxicology of Ministry of Education, School of Public Health, Nanjing Medical University, Nanjing, ChinaState Key Laboratory of Reproductive Medicine, Center for Global Health, School of Public Health, Nanjing Medical University, Nanjing, ChinaKey Laboratory of Modern Toxicology of Ministry of Education, School of Public Health, Nanjing Medical University, Nanjing, ChinaState Key Laboratory of Reproductive Medicine, Center for Global Health, School of Public Health, Nanjing Medical University, Nanjing, ChinaDepartment of Nutrition and Food Safety, School of Public Health, Nanjing Medical University, Nanjing, ChinaState Key Laboratory of Reproductive Medicine, Center for Global Health, School of Public Health, Nanjing Medical University, Nanjing, ChinaKey Laboratory of Modern Toxicology of Ministry of Education, School of Public Health, Nanjing Medical University, Nanjing, ChinaGlufosinate-ammonium (GLA) is a widely used herbicide with emerging concern over its male reproductive toxicity. Abnormalities in sperm histone modification induced by GLA exposure observed in our previous study aroused our interest in whether such alterations could further affect embryonic gene expression. Here we administered adult male mice with 0.2 mg/kg⋅day of GLA for 5 weeks to collect their sperm or 4-cell embryos after copulation. Cleavage Under Targets and Tagmentation (CUT&Tag) sequencing showed alterations of sperm H3 lysine 4 trimethylation (H3K4me3) and histone H3 lysine 27 acetylation (H3K27ac), which are active histone modification marks involved in embryo development, while RNA sequencing identified differentially expressed genes in 4-cell embryos. Differentially H3K4me3 and H3K27ac occupied regions were mainly distributed at the gene promoters and putative enhancers, and were enriched in pathways related to the immune system and nervous system. Integrative analysis of these sequencing data showed that genes such as Mgl2 with increased H3K4me3 and H3K27ac in sperm were up-regulated in embryos, and vice versa for genes such as Dcn. Additionally, differentially occupied H3K4me3 and H3K27ac in sperm were linked to gene expression changes in both paternal and maternal alleles of 4-cell embryos. In conclusion, GLA-induced changes in sperm H3K4me3 and H3K27ac are concordant with gene expression in preimplantation embryos, which might further affect embryo development and offspring health.https://www.frontiersin.org/articles/10.3389/fphys.2021.819856/fullglufosinate-ammoniumH3K4me3H3K27acspermembryo development |
| spellingShingle | Xuan Ma Xuan Ma Yun Fan Yun Fan Yun Fan Wenwen Xiao Wenwen Xiao Xingwang Ding Xingwang Ding Weiyue Hu Weiyue Hu Yankai Xia Yankai Xia Glufosinate-Ammonium Induced Aberrant Histone Modifications in Mouse Sperm Are Concordant With Transcriptome in Preimplantation Embryos Frontiers in Physiology glufosinate-ammonium H3K4me3 H3K27ac sperm embryo development |
| title | Glufosinate-Ammonium Induced Aberrant Histone Modifications in Mouse Sperm Are Concordant With Transcriptome in Preimplantation Embryos |
| title_full | Glufosinate-Ammonium Induced Aberrant Histone Modifications in Mouse Sperm Are Concordant With Transcriptome in Preimplantation Embryos |
| title_fullStr | Glufosinate-Ammonium Induced Aberrant Histone Modifications in Mouse Sperm Are Concordant With Transcriptome in Preimplantation Embryos |
| title_full_unstemmed | Glufosinate-Ammonium Induced Aberrant Histone Modifications in Mouse Sperm Are Concordant With Transcriptome in Preimplantation Embryos |
| title_short | Glufosinate-Ammonium Induced Aberrant Histone Modifications in Mouse Sperm Are Concordant With Transcriptome in Preimplantation Embryos |
| title_sort | glufosinate ammonium induced aberrant histone modifications in mouse sperm are concordant with transcriptome in preimplantation embryos |
| topic | glufosinate-ammonium H3K4me3 H3K27ac sperm embryo development |
| url | https://www.frontiersin.org/articles/10.3389/fphys.2021.819856/full |
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