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The histone modification reader ZCWPW1 links histone methylation to repair of PRDM9-induced meiotic double stand breaks

Tao Huang, Shenli Yuan, Mengjing Li, Xiaochen Yu, Jianhong Zhang, Yingying Yin, Chao Liu, Lei Gao, View ORCID ProfileWei Li, Jiang Liu, Zi-Jiang Chen, Hongbin Liu
doi: https://doi.org/10.1101/836023
Tao Huang
Center for Reproductive Medicine, Shandong Provincial Hospital Affiliated to Shandong UniversityNational Research Center for Assisted Reproductive Technology and Reproductive Genetics, ChinaThe Key laboratory of Reproductive Endocrinology (Shandong University), Ministry of EducationShandong Provincial Clinical Medicine Research Center for reproductive healthShandong Provincial Key Laboratory of Reproductive Medicine, No.157 Jingliu Road, Jinan, 250001, China
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Shenli Yuan
CAS Key Laboratory of Genome Sciences and Information, Beijing Institute of Genomics, Chinese Academy of Sciences, 100101 Beijing, China
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Mengjing Li
Center for Reproductive Medicine, Shandong Provincial Hospital Affiliated to Shandong UniversityNational Research Center for Assisted Reproductive Technology and Reproductive Genetics, ChinaThe Key laboratory of Reproductive Endocrinology (Shandong University), Ministry of EducationShandong Provincial Clinical Medicine Research Center for reproductive healthShandong Provincial Key Laboratory of Reproductive Medicine, No.157 Jingliu Road, Jinan, 250001, China
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Xiaochen Yu
Center for Reproductive Medicine, Shandong Provincial Hospital Affiliated to Shandong UniversityNational Research Center for Assisted Reproductive Technology and Reproductive Genetics, ChinaThe Key laboratory of Reproductive Endocrinology (Shandong University), Ministry of EducationShandong Provincial Clinical Medicine Research Center for reproductive healthShandong Provincial Key Laboratory of Reproductive Medicine, No.157 Jingliu Road, Jinan, 250001, China
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Jianhong Zhang
CAS Key Laboratory of Genome Sciences and Information, Beijing Institute of Genomics, Chinese Academy of Sciences, 100101 Beijing, China
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Yingying Yin
Center for Reproductive Medicine, Shandong Provincial Hospital Affiliated to Shandong UniversityNational Research Center for Assisted Reproductive Technology and Reproductive Genetics, ChinaThe Key laboratory of Reproductive Endocrinology (Shandong University), Ministry of EducationShandong Provincial Clinical Medicine Research Center for reproductive healthShandong Provincial Key Laboratory of Reproductive Medicine, No.157 Jingliu Road, Jinan, 250001, China
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Chao Liu
State Key Laboratory of Stem Cell and Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China
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Lei Gao
CAS Key Laboratory of Genome Sciences and Information, Beijing Institute of Genomics, Chinese Academy of Sciences, 100101 Beijing, China
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Wei Li
State Key Laboratory of Stem Cell and Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China
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  • ORCID record for Wei Li
Jiang Liu
CAS Key Laboratory of Genome Sciences and Information, Beijing Institute of Genomics, Chinese Academy of Sciences, 100101 Beijing, China
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  • For correspondence: liuj@big.ac.cn chenzijiang@hotmail.com hongbin_sduivf@aliyun.com
Zi-Jiang Chen
Center for Reproductive Medicine, Shandong Provincial Hospital Affiliated to Shandong UniversityNational Research Center for Assisted Reproductive Technology and Reproductive Genetics, ChinaThe Key laboratory of Reproductive Endocrinology (Shandong University), Ministry of EducationShandong Provincial Clinical Medicine Research Center for reproductive healthShandong Provincial Key Laboratory of Reproductive Medicine, No.157 Jingliu Road, Jinan, 250001, ChinaShanghai Key Laboratory for Assisted Reproduction and Reproductive Genetics, Shanghai, China
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  • For correspondence: liuj@big.ac.cn chenzijiang@hotmail.com hongbin_sduivf@aliyun.com
Hongbin Liu
Center for Reproductive Medicine, Shandong Provincial Hospital Affiliated to Shandong UniversityNational Research Center for Assisted Reproductive Technology and Reproductive Genetics, ChinaThe Key laboratory of Reproductive Endocrinology (Shandong University), Ministry of EducationShandong Provincial Clinical Medicine Research Center for reproductive healthShandong Provincial Key Laboratory of Reproductive Medicine, No.157 Jingliu Road, Jinan, 250001, ChinaCUHK-SDU Joint Laboratory on Reproductive Genetics, School of Biomedical Sciences, the Chinese University of Hong Kong, Hong Kong, China
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  • For correspondence: liuj@big.ac.cn chenzijiang@hotmail.com hongbin_sduivf@aliyun.com
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ABSTRACT

It is known that the histone modification writer PRDM9 deposits H3K4me3 and H3K36me3 marks at future DSB sites very early in meiosis, the nature of any proteins which can read such marks is unknown. Here, we demonstrate in vivo that ZCWPW1 is a H3K4me3 reader and show that its binding at chromatin promotes completion of DSB repair and synapsis in mouse testes. Based on multiple ChIP-seq and immunofluorescence analyses with mutants—including an H3K4me3-reader-dead variant of ZCWPW1 mice line—we establish that ZCWPW1's occupancy on chromatin is strongly but not exclusively promoted by the histone-modification activity of the PRDM9. ZCWPW1 localizes to DMC1-labelled DSB hotspots in a largely PRDM9-dependent manner, where it facilitates completion of synapsis by mediating the DSB repair process. In sum, our study demonstrates the function of a reader protein that carries out work resulting from an epigenetics-based recombination hotspot selection system in mammals.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted November 08, 2019.
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The histone modification reader ZCWPW1 links histone methylation to repair of PRDM9-induced meiotic double stand breaks
Tao Huang, Shenli Yuan, Mengjing Li, Xiaochen Yu, Jianhong Zhang, Yingying Yin, Chao Liu, Lei Gao, Wei Li, Jiang Liu, Zi-Jiang Chen, Hongbin Liu
bioRxiv 836023; doi: https://doi.org/10.1101/836023
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The histone modification reader ZCWPW1 links histone methylation to repair of PRDM9-induced meiotic double stand breaks
Tao Huang, Shenli Yuan, Mengjing Li, Xiaochen Yu, Jianhong Zhang, Yingying Yin, Chao Liu, Lei Gao, Wei Li, Jiang Liu, Zi-Jiang Chen, Hongbin Liu
bioRxiv 836023; doi: https://doi.org/10.1101/836023

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