Acetylation at lysine 27 on maternal H3.3 regulates minor zygotic genome activation
Summary: Zygotic genome activation (ZGA) initiates transcription in early embryogenesis and requires extensive chromatin remodeling, including rapid incorporation of the histone variant H3.3. The distinct sources of H3.3 from paternal and maternal alleles (paH3.3 and maH3.3) complicate tracking thei...
Saved in:
| Main Authors: | , , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Elsevier
2025-01-01
|
| Series: | Cell Reports |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S2211124724014992 |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| _version_ | 1850057976408178688 |
|---|---|
| author | Jiaming Zhang Xuanwen Li Qi Zhao Jingzhang Ji Hongdi Cui Weibo Hou Xinyu Wang Entong Song Songling Xiao Shukuan Ling Shaorong Gao Xiaoyu Liu Duancheng Wen Qingran Kong |
| author_facet | Jiaming Zhang Xuanwen Li Qi Zhao Jingzhang Ji Hongdi Cui Weibo Hou Xinyu Wang Entong Song Songling Xiao Shukuan Ling Shaorong Gao Xiaoyu Liu Duancheng Wen Qingran Kong |
| author_sort | Jiaming Zhang |
| collection | DOAJ |
| description | Summary: Zygotic genome activation (ZGA) initiates transcription in early embryogenesis and requires extensive chromatin remodeling, including rapid incorporation of the histone variant H3.3. The distinct sources of H3.3 from paternal and maternal alleles (paH3.3 and maH3.3) complicate tracking their individual contributions. Here, using an H3.3B-hemagglutinin (HA)-tagged mouse model, we profile the temporal dynamics of paH3.3 and maH3.3, revealing a unique pattern of maH3.3 enrichment at the promoter regions from zygotes to 2-cell embryos, highlighting the crucial role of maternally stored H3.3 mRNAs and proteins (mH3.3) in pre-implantation development. Knockdown of mH3.3 compromises cleavage and minor ZGA. Mechanistically, mH3.3 facilitates minor ZGA through H3.3S31ph-dependent H3K27ac deposition. Profiling of H3.3 landscape in parthenogenetic (PG) and androgenetic (AG) embryos highlights the role of mH3.3 in remodeling the paternal genome by establishing H3K27ac. These findings demonstrate that mH3.3-mediated parental chromatin reprogramming is essential for orchestrating minor ZGA. |
| format | Article |
| id | doaj-art-9e7505f75d8b43888672ff11de07af3c |
| institution | DOAJ |
| issn | 2211-1247 |
| language | English |
| publishDate | 2025-01-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Cell Reports |
| spelling | doaj-art-9e7505f75d8b43888672ff11de07af3c2025-08-20T02:51:18ZengElsevierCell Reports2211-12472025-01-0144111514810.1016/j.celrep.2024.115148Acetylation at lysine 27 on maternal H3.3 regulates minor zygotic genome activationJiaming Zhang0Xuanwen Li1Qi Zhao2Jingzhang Ji3Hongdi Cui4Weibo Hou5Xinyu Wang6Entong Song7Songling Xiao8Shukuan Ling9Shaorong Gao10Xiaoyu Liu11Duancheng Wen12Qingran Kong13Oujiang Laboratory, Zhejiang Provincial Key Laboratory of Medical Genetics, Key Laboratory of Laboratory Medicine, Ministry of Education, School of Laboratory Medicine and Life Sciences, Wenzhou Medical University, Wenzhou, Zhejiang, China; Ronald O. Perelman and Claudia Cohen Center for Reproductive Medicine, Weill Cornell Medicine, New York, NY 10065, USA; Corresponding authorOujiang Laboratory, Zhejiang Provincial Key Laboratory of Medical Genetics, Key Laboratory of Laboratory Medicine, Ministry of Education, School of Laboratory Medicine and Life Sciences, Wenzhou Medical University, Wenzhou, Zhejiang, ChinaOujiang Laboratory, Zhejiang Provincial Key Laboratory of Medical Genetics, Key Laboratory of Laboratory Medicine, Ministry of Education, School of Laboratory Medicine and Life Sciences, Wenzhou Medical University, Wenzhou, Zhejiang, ChinaOujiang Laboratory, Zhejiang Provincial Key Laboratory of Medical Genetics, Key Laboratory of Laboratory Medicine, Ministry of Education, School of Laboratory Medicine and Life Sciences, Wenzhou Medical University, Wenzhou, Zhejiang, ChinaOujiang Laboratory, Zhejiang Provincial Key Laboratory of Medical Genetics, Key Laboratory of Laboratory Medicine, Ministry of Education, School of Laboratory Medicine and Life Sciences, Wenzhou Medical University, Wenzhou, Zhejiang, ChinaOujiang Laboratory, Zhejiang Provincial Key Laboratory of Medical Genetics, Key Laboratory of Laboratory Medicine, Ministry of Education, School of Laboratory Medicine and Life Sciences, Wenzhou Medical University, Wenzhou, Zhejiang, ChinaFrontier Science Center for Stem Cell Research, School of Life Sciences and Technology, Tongji University, Shanghai 200092, ChinaOujiang Laboratory, Zhejiang Provincial Key Laboratory of Medical Genetics, Key Laboratory of Laboratory Medicine, Ministry of Education, School of Laboratory Medicine and Life Sciences, Wenzhou Medical University, Wenzhou, Zhejiang, ChinaOujiang Laboratory, Zhejiang Provincial Key Laboratory of Medical Genetics, Key Laboratory of Laboratory Medicine, Ministry of Education, School of Laboratory Medicine and Life Sciences, Wenzhou Medical University, Wenzhou, Zhejiang, ChinaOujiang Laboratory, Zhejiang Provincial Key Laboratory of Medical Genetics, Key Laboratory of Laboratory Medicine, Ministry of Education, School of Laboratory Medicine and Life Sciences, Wenzhou Medical University, Wenzhou, Zhejiang, ChinaFrontier Science Center for Stem Cell Research, School of Life Sciences and Technology, Tongji University, Shanghai 200092, China; Corresponding authorFrontier Science Center for Stem Cell Research, School of Life Sciences and Technology, Tongji University, Shanghai 200092, China; Corresponding authorRonald O. Perelman and Claudia Cohen Center for Reproductive Medicine, Weill Cornell Medicine, New York, NY 10065, USA; Corresponding authorOujiang Laboratory, Zhejiang Provincial Key Laboratory of Medical Genetics, Key Laboratory of Laboratory Medicine, Ministry of Education, School of Laboratory Medicine and Life Sciences, Wenzhou Medical University, Wenzhou, Zhejiang, China; Corresponding authorSummary: Zygotic genome activation (ZGA) initiates transcription in early embryogenesis and requires extensive chromatin remodeling, including rapid incorporation of the histone variant H3.3. The distinct sources of H3.3 from paternal and maternal alleles (paH3.3 and maH3.3) complicate tracking their individual contributions. Here, using an H3.3B-hemagglutinin (HA)-tagged mouse model, we profile the temporal dynamics of paH3.3 and maH3.3, revealing a unique pattern of maH3.3 enrichment at the promoter regions from zygotes to 2-cell embryos, highlighting the crucial role of maternally stored H3.3 mRNAs and proteins (mH3.3) in pre-implantation development. Knockdown of mH3.3 compromises cleavage and minor ZGA. Mechanistically, mH3.3 facilitates minor ZGA through H3.3S31ph-dependent H3K27ac deposition. Profiling of H3.3 landscape in parthenogenetic (PG) and androgenetic (AG) embryos highlights the role of mH3.3 in remodeling the paternal genome by establishing H3K27ac. These findings demonstrate that mH3.3-mediated parental chromatin reprogramming is essential for orchestrating minor ZGA.http://www.sciencedirect.com/science/article/pii/S2211124724014992CP: Molecular biologyCP: Developmental biology |
| spellingShingle | Jiaming Zhang Xuanwen Li Qi Zhao Jingzhang Ji Hongdi Cui Weibo Hou Xinyu Wang Entong Song Songling Xiao Shukuan Ling Shaorong Gao Xiaoyu Liu Duancheng Wen Qingran Kong Acetylation at lysine 27 on maternal H3.3 regulates minor zygotic genome activation Cell Reports CP: Molecular biology CP: Developmental biology |
| title | Acetylation at lysine 27 on maternal H3.3 regulates minor zygotic genome activation |
| title_full | Acetylation at lysine 27 on maternal H3.3 regulates minor zygotic genome activation |
| title_fullStr | Acetylation at lysine 27 on maternal H3.3 regulates minor zygotic genome activation |
| title_full_unstemmed | Acetylation at lysine 27 on maternal H3.3 regulates minor zygotic genome activation |
| title_short | Acetylation at lysine 27 on maternal H3.3 regulates minor zygotic genome activation |
| title_sort | acetylation at lysine 27 on maternal h3 3 regulates minor zygotic genome activation |
| topic | CP: Molecular biology CP: Developmental biology |
| url | http://www.sciencedirect.com/science/article/pii/S2211124724014992 |
| work_keys_str_mv | AT jiamingzhang acetylationatlysine27onmaternalh33regulatesminorzygoticgenomeactivation AT xuanwenli acetylationatlysine27onmaternalh33regulatesminorzygoticgenomeactivation AT qizhao acetylationatlysine27onmaternalh33regulatesminorzygoticgenomeactivation AT jingzhangji acetylationatlysine27onmaternalh33regulatesminorzygoticgenomeactivation AT hongdicui acetylationatlysine27onmaternalh33regulatesminorzygoticgenomeactivation AT weibohou acetylationatlysine27onmaternalh33regulatesminorzygoticgenomeactivation AT xinyuwang acetylationatlysine27onmaternalh33regulatesminorzygoticgenomeactivation AT entongsong acetylationatlysine27onmaternalh33regulatesminorzygoticgenomeactivation AT songlingxiao acetylationatlysine27onmaternalh33regulatesminorzygoticgenomeactivation AT shukuanling acetylationatlysine27onmaternalh33regulatesminorzygoticgenomeactivation AT shaoronggao acetylationatlysine27onmaternalh33regulatesminorzygoticgenomeactivation AT xiaoyuliu acetylationatlysine27onmaternalh33regulatesminorzygoticgenomeactivation AT duanchengwen acetylationatlysine27onmaternalh33regulatesminorzygoticgenomeactivation AT qingrankong acetylationatlysine27onmaternalh33regulatesminorzygoticgenomeactivation |