The histone modification reader ZCWPW1 promotes double-strand break repair by regulating cross-talk of histone modifications and chromatin accessibility at meiotic hotspots
Abstract Background The PRDM9-dependent histone methylation H3K4me3 and H3K36me3 function in assuring accurate homologous recombination at recombination hotspots in mammals. Beyond histone methylation, H3 lysine 9 acetylation (H3K9ac) is also greatly enriched at recombination hotspots. Previous work...
| Main Authors: | , , , , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2022-09-01
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| Series: | Genome Biology |
| Online Access: | https://doi.org/10.1186/s13059-022-02758-z |
| _version_ | 1811273759734104064 |
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| author | Shenli Yuan Tao Huang Ziyou Bao Shiyu Wang Xinyue Wu Jiang Liu Hongbin Liu Zi-Jiang Chen |
| author_facet | Shenli Yuan Tao Huang Ziyou Bao Shiyu Wang Xinyue Wu Jiang Liu Hongbin Liu Zi-Jiang Chen |
| author_sort | Shenli Yuan |
| collection | DOAJ |
| description | Abstract Background The PRDM9-dependent histone methylation H3K4me3 and H3K36me3 function in assuring accurate homologous recombination at recombination hotspots in mammals. Beyond histone methylation, H3 lysine 9 acetylation (H3K9ac) is also greatly enriched at recombination hotspots. Previous work has indicated the potential cross-talk between H3K4me3 and H3K9ac at recombination hotspots, but it is still unknown what molecular mechanisms mediate the cross-talk between the two histone modifications at hotspots or how the cross-talk regulates homologous recombination in meiosis. Results Here, we find that the histone methylation reader ZCWPW1 is essential for maintaining H3K9ac by antagonizing HDAC proteins’ deacetylation activity and further promotes chromatin openness at recombination hotspots thus preparing the way for homologous recombination during meiotic double-strand break repair. Interestingly, ectopic expression of the germ-cell-specific protein ZCWPW1 in human somatic cells enhances double-strand break repair via homologous recombination. Conclusions Taken together, our findings provide new insights into how histone modifications and their associated regulatory proteins collectively regulate meiotic homologous recombination. |
| first_indexed | 2024-04-12T23:05:08Z |
| format | Article |
| id | doaj.art-d946e7a6e4704f61a0b5a4a5425736ff |
| institution | Directory Open Access Journal |
| issn | 1474-760X |
| language | English |
| last_indexed | 2024-04-12T23:05:08Z |
| publishDate | 2022-09-01 |
| publisher | BMC |
| record_format | Article |
| series | Genome Biology |
| spelling | doaj.art-d946e7a6e4704f61a0b5a4a5425736ff2022-12-22T03:12:56ZengBMCGenome Biology1474-760X2022-09-0123112610.1186/s13059-022-02758-zThe histone modification reader ZCWPW1 promotes double-strand break repair by regulating cross-talk of histone modifications and chromatin accessibility at meiotic hotspotsShenli Yuan0Tao Huang1Ziyou Bao2Shiyu Wang3Xinyue Wu4Jiang Liu5Hongbin Liu6Zi-Jiang Chen7Center for Reproductive Medicine, Shandong UniversityCenter for Reproductive Medicine, Shandong UniversityCenter for Reproductive Medicine, Shandong UniversityCenter for Reproductive Medicine, Shandong UniversityCenter for Reproductive Medicine, Shandong UniversityCAS Key Laboratory of Genome Sciences and Information, Collaborative Innovation Center of Genetics and Development, Beijing Institute of Genomics, China National Center for Bioinformation, and Chinese Academy of SciencesCenter for Reproductive Medicine, Shandong UniversityCenter for Reproductive Medicine, Shandong UniversityAbstract Background The PRDM9-dependent histone methylation H3K4me3 and H3K36me3 function in assuring accurate homologous recombination at recombination hotspots in mammals. Beyond histone methylation, H3 lysine 9 acetylation (H3K9ac) is also greatly enriched at recombination hotspots. Previous work has indicated the potential cross-talk between H3K4me3 and H3K9ac at recombination hotspots, but it is still unknown what molecular mechanisms mediate the cross-talk between the two histone modifications at hotspots or how the cross-talk regulates homologous recombination in meiosis. Results Here, we find that the histone methylation reader ZCWPW1 is essential for maintaining H3K9ac by antagonizing HDAC proteins’ deacetylation activity and further promotes chromatin openness at recombination hotspots thus preparing the way for homologous recombination during meiotic double-strand break repair. Interestingly, ectopic expression of the germ-cell-specific protein ZCWPW1 in human somatic cells enhances double-strand break repair via homologous recombination. Conclusions Taken together, our findings provide new insights into how histone modifications and their associated regulatory proteins collectively regulate meiotic homologous recombination.https://doi.org/10.1186/s13059-022-02758-z |
| spellingShingle | Shenli Yuan Tao Huang Ziyou Bao Shiyu Wang Xinyue Wu Jiang Liu Hongbin Liu Zi-Jiang Chen The histone modification reader ZCWPW1 promotes double-strand break repair by regulating cross-talk of histone modifications and chromatin accessibility at meiotic hotspots Genome Biology |
| title | The histone modification reader ZCWPW1 promotes double-strand break repair by regulating cross-talk of histone modifications and chromatin accessibility at meiotic hotspots |
| title_full | The histone modification reader ZCWPW1 promotes double-strand break repair by regulating cross-talk of histone modifications and chromatin accessibility at meiotic hotspots |
| title_fullStr | The histone modification reader ZCWPW1 promotes double-strand break repair by regulating cross-talk of histone modifications and chromatin accessibility at meiotic hotspots |
| title_full_unstemmed | The histone modification reader ZCWPW1 promotes double-strand break repair by regulating cross-talk of histone modifications and chromatin accessibility at meiotic hotspots |
| title_short | The histone modification reader ZCWPW1 promotes double-strand break repair by regulating cross-talk of histone modifications and chromatin accessibility at meiotic hotspots |
| title_sort | histone modification reader zcwpw1 promotes double strand break repair by regulating cross talk of histone modifications and chromatin accessibility at meiotic hotspots |
| url | https://doi.org/10.1186/s13059-022-02758-z |
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