Polycomb Group Proteins Regulate Chromatin Architecture in Mouse Oocytes and Early Embryos

Zhenhai Du; Hui Zheng; Yumiko K. Kawamura; Ke Zhang; Johanna Gassler; Sean Powell; Qianhua Xu; Zili Lin; Kai Xu; Qian Zhou; Evgeniy A. Ozonov; Nathalie Véron; Bo Huang; Lijia Li; Guang Yu; Ling Liu; Wan Kin Au Yeung; Peizhe Wang; Lei Chang; Qiujun Wang; Aibin He; Yujie Sun; Jie Na; Qingyuan Sun; Hiroyuki Sasaki; Kikuë Tachibana; Antoine H.F.M. Peters; Wei Xie

doi:10.1016/j.molcel.2019.11.011

Polycomb Group Proteins Regulate Chromatin Architecture in Mouse Oocytes and Early Embryos

Zhenhai Du, Hui Zheng, Yumiko K. Kawamura, Ke Zhang, Johanna Gassler, Sean Powell, Qianhua Xu, Zili Lin, Kai Xu, Qian Zhou, Evgeniy A. Ozonov, Nathalie Véron, Bo Huang, Lijia Li, Guang Yu, Ling Liu, Wan Kin Au Yeung, Peizhe Wang, Lei Chang, Qiujun WangAibin He, Yujie Sun, Jie Na, Qingyuan Sun, Hiroyuki Sasaki, Kikuë Tachibana, Antoine H.F.M. Peters, Wei Xie

Department of Molecular and Structural Biology

Research output: Contribution to journal › Article › peer-review

13 Citations (Scopus)

Abstract

In mammals, germ cells undergo a series of events to give rise to haploid gametes. The dynamics of meiotic chromatin architecture still remain poorly understood. By applying Hi-C to mouse oocytes, Du et al. reveal a unique Polycomb-regulated chromatin architecture, which adds a new perspective to the non-canonical oocyte epigenomes.

Original language	English
Pages (from-to)	825-839.e7
Journal	Molecular Cell
Volume	77
Issue number	4
DOIs	https://doi.org/10.1016/j.molcel.2019.11.011
Publication status	Published - Feb 20 2020

All Science Journal Classification (ASJC) codes

Molecular Biology
Cell Biology

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10.1016/j.molcel.2019.11.011

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Du, Z., Zheng, H., Kawamura, Y. K., Zhang, K., Gassler, J., Powell, S., Xu, Q., Lin, Z., Xu, K., Zhou, Q., Ozonov, E. A., Véron, N., Huang, B., Li, L., Yu, G., Liu, L., Au Yeung, W. K., Wang, P., Chang, L., ... Xie, W. (2020). Polycomb Group Proteins Regulate Chromatin Architecture in Mouse Oocytes and Early Embryos. Molecular Cell, 77(4), 825-839.e7. https://doi.org/10.1016/j.molcel.2019.11.011

Polycomb Group Proteins Regulate Chromatin Architecture in Mouse Oocytes and Early Embryos. / Du, Zhenhai; Zheng, Hui; Kawamura, Yumiko K.; Zhang, Ke; Gassler, Johanna; Powell, Sean; Xu, Qianhua; Lin, Zili; Xu, Kai; Zhou, Qian; Ozonov, Evgeniy A.; Véron, Nathalie; Huang, Bo; Li, Lijia; Yu, Guang; Liu, Ling; Au Yeung, Wan Kin; Wang, Peizhe; Chang, Lei; Wang, Qiujun; He, Aibin; Sun, Yujie; Na, Jie; Sun, Qingyuan; Sasaki, Hiroyuki; Tachibana, Kikuë; Peters, Antoine H.F.M.; Xie, Wei.

In: Molecular Cell, Vol. 77, No. 4, 20.02.2020, p. 825-839.e7.

Research output: Contribution to journal › Article › peer-review

Du, Z, Zheng, H, Kawamura, YK, Zhang, K, Gassler, J, Powell, S, Xu, Q, Lin, Z, Xu, K, Zhou, Q, Ozonov, EA, Véron, N, Huang, B, Li, L, Yu, G, Liu, L, Au Yeung, WK, Wang, P, Chang, L, Wang, Q, He, A, Sun, Y, Na, J, Sun, Q, Sasaki, H, Tachibana, K, Peters, AHFM & Xie, W 2020, 'Polycomb Group Proteins Regulate Chromatin Architecture in Mouse Oocytes and Early Embryos', Molecular Cell, vol. 77, no. 4, pp. 825-839.e7. https://doi.org/10.1016/j.molcel.2019.11.011

Du, Zhenhai ; Zheng, Hui ; Kawamura, Yumiko K. ; Zhang, Ke ; Gassler, Johanna ; Powell, Sean ; Xu, Qianhua ; Lin, Zili ; Xu, Kai ; Zhou, Qian ; Ozonov, Evgeniy A. ; Véron, Nathalie ; Huang, Bo ; Li, Lijia ; Yu, Guang ; Liu, Ling ; Au Yeung, Wan Kin ; Wang, Peizhe ; Chang, Lei ; Wang, Qiujun ; He, Aibin ; Sun, Yujie ; Na, Jie ; Sun, Qingyuan ; Sasaki, Hiroyuki ; Tachibana, Kikuë ; Peters, Antoine H.F.M. ; Xie, Wei. / Polycomb Group Proteins Regulate Chromatin Architecture in Mouse Oocytes and Early Embryos. In: Molecular Cell. 2020 ; Vol. 77, No. 4. pp. 825-839.e7.

@article{b70d5d258a9f4a048aa3923da83675c1,

title = "Polycomb Group Proteins Regulate Chromatin Architecture in Mouse Oocytes and Early Embryos",

abstract = "In mammals, germ cells undergo a series of events to give rise to haploid gametes. The dynamics of meiotic chromatin architecture still remain poorly understood. By applying Hi-C to mouse oocytes, Du et al. reveal a unique Polycomb-regulated chromatin architecture, which adds a new perspective to the non-canonical oocyte epigenomes.",

author = "Zhenhai Du and Hui Zheng and Kawamura, {Yumiko K.} and Ke Zhang and Johanna Gassler and Sean Powell and Qianhua Xu and Zili Lin and Kai Xu and Qian Zhou and Ozonov, {Evgeniy A.} and Nathalie V{\'e}ron and Bo Huang and Lijia Li and Guang Yu and Ling Liu and {Au Yeung}, {Wan Kin} and Peizhe Wang and Lei Chang and Qiujun Wang and Aibin He and Yujie Sun and Jie Na and Qingyuan Sun and Hiroyuki Sasaki and Kiku{\"e} Tachibana and Peters, {Antoine H.F.M.} and Wei Xie",

note = "Funding Information: We thank Prof. Fei Gao (IOZ, Beijing, China) for providing Gdf9-Cre mice, Dr. Miguel Vidal (CSIC, Madrid, Spain) for Ring1 deficient mice, Prof. Maarten van Lohuizen (NKI, Amsterdam, the Netherlands) for Rnf2fl/fl mice, and Prof. Barbara Knowles (JAX, Bar Harbor, ME, USA) for Zp3-Cre transgenic mice. We are grateful to Rui Ma, Hui Quan, Xianglin Zhang, Zhaofeng Ye, Yuanyuan Li, Wenhao Zhang, Xiaowo Wang, Jianyang Zeng, Yiqin Gao, and Juntao Gao for discussions. We thank Drs. Haruhiko Koseki, Yi Zhang, and Inoue Azusa for sharing reagents or protocols. We appreciate members of the Xie laboratory for comments during preparation of the manuscript. This work is supported by funding provided by the National Natural Science Foundation of China (grants 31422031 and 31725018 to W.X.); the National Basic Research Program of China (grant 2015CB856201 to W.X.); the Beijing Municipal Science & Technology Commission (grant Z181100001318006 to W.X.); the THU-PKU Center for Life Sciences (W.X.); the Novartis Research Foundation (N.V. and A.H.F.M.P.); the European Research Council (grant ERC 695288?Totipotency to Y.K.K. E.A.O. and A.H.F.M.P.); and the JSPS (KAKENHI JP18H05214 to H.S.). Research in the laboratory of K.T. is supported by the Austrian Academy of Sciences, the FWF and Herzfelder foundation (P30613-B21), a European Research Council grant (ERC-StG-336460 ChromHeritance), and an HFSP project grant (PGP0057-2018). Z.D. H.Z. and Q.X. are supported by THU-PKU Center for Life Sciences postdoctoral fellowships. W.X. is an HHMI international research scholar. J.G. is supported by the European Research Council and the L'Or?al Austria Fellowship for Women in Science and is an associated student of the DK Chromosome Dynamics (W1238-B20) supported by the Austrian Science Fund (FWF). Z.D. H.Z. and W.X. conceived the project. Z.D. conducted the sisHi-C experiments. Z.L. Q.X. B.H. K.X. Z.D. Y.K.K. J.G. and K.Z. performed the mouse PGCs, oocytes, and embryo experiments. H.Z. and Z.D. performed bioinformatics analysis. L. Li and G.Y. performed the CUT&RUN experiments. J.G. performed the single-nucleus Hi-C experiments. S.P. processed the single-nucleus Hi-C data. L.C. P.W. L. Liu, E.A.O. N.V. Q.Z. and W.K.A.Y. helped with various experiments or analyses. Q.W. performed next-generation sequencing (NGS). A.H. Y.S. J.N. Q.S. H.S. K.T. A.H.F.M.P. and W.X. supervised the project or related experiments. Z.D. H.Z. K.Z. A.H.F.M.P. and W.X. wrote the manuscript, with help from other authors. The authors declare no competing interests. Funding Information: We thank Prof. Fei Gao (IOZ, Beijing, China) for providing Gdf9-Cre mice, Dr. Miguel Vidal (CSIC, Madrid, Spain) for Ring1 deficient mice, Prof. Maarten van Lohuizen (NKI, Amsterdam, the Netherlands) for Rnf2 fl/fl mice, and Prof. Barbara Knowles (JAX, Bar Harbor, ME, USA) for Zp3-Cre transgenic mice. We are grateful to Rui Ma, Hui Quan, Xianglin Zhang, Zhaofeng Ye, Yuanyuan Li, Wenhao Zhang, Xiaowo Wang, Jianyang Zeng, Yiqin Gao, and Juntao Gao for discussions. We thank Drs. Haruhiko Koseki, Yi Zhang, and Inoue Azusa for sharing reagents or protocols. We appreciate members of the Xie laboratory for comments during preparation of the manuscript. This work is supported by funding provided by the National Natural Science Foundation of China (grants 31422031 and 31725018 to W.X.); the National Basic Research Program of China (grant 2 015CB856201 to W.X.); the Beijing Municipal Science & Technology Commission (grant Z181100001318006 to W.X.); the THU-PKU Center for Life Sciences (W.X.); the Novartis Research Foundation (N.V. and A.H.F.M.P.); the European Research Council (grant ERC 695288–Totipotency to Y.K.K., E.A.O., and A.H.F.M.P.); and the JSPS ( KAKENHI JP18H05214 to H.S.). Research in the laboratory of K.T. is supported by the Austrian Academy of Sciences , the FWF and Herzfelder foundation ( P30613-B21 ), a European Research Council grant ( ERC-StG-336460 ChromHeritance), and an HFSP project grant ( PGP0057-2018 ). Z.D., H.Z., and Q.X. are supported by THU-PKU Center for Life Sciences postdoctoral fellowships. W.X. is an HHMI international research scholar. J.G. is supported by the European Research Council and the L'Or{\'e}al Austria Fellowship for Women in Science and is an associated student of the DK Chromosome Dynamics ( W1238-B20 ) supported by the Austrian Science Fund (FWF) . ",

year = "2020",

month = feb,

day = "20",

doi = "10.1016/j.molcel.2019.11.011",

language = "English",

volume = "77",

pages = "825--839.e7",

journal = "Molecular Cell",

issn = "1097-2765",

publisher = "Cell Press",

number = "4",

}

TY - JOUR

T1 - Polycomb Group Proteins Regulate Chromatin Architecture in Mouse Oocytes and Early Embryos

AU - Du, Zhenhai

AU - Zheng, Hui

AU - Kawamura, Yumiko K.

AU - Zhang, Ke

AU - Gassler, Johanna

AU - Powell, Sean

AU - Xu, Qianhua

AU - Lin, Zili

AU - Xu, Kai

AU - Zhou, Qian

AU - Ozonov, Evgeniy A.

AU - Véron, Nathalie

AU - Huang, Bo

AU - Li, Lijia

AU - Yu, Guang

AU - Liu, Ling

AU - Au Yeung, Wan Kin

AU - Wang, Peizhe

AU - Chang, Lei

AU - Wang, Qiujun

AU - He, Aibin

AU - Sun, Yujie

AU - Na, Jie

AU - Sun, Qingyuan

AU - Sasaki, Hiroyuki

AU - Tachibana, Kikuë

AU - Peters, Antoine H.F.M.

AU - Xie, Wei

N1 - Funding Information: We thank Prof. Fei Gao (IOZ, Beijing, China) for providing Gdf9-Cre mice, Dr. Miguel Vidal (CSIC, Madrid, Spain) for Ring1 deficient mice, Prof. Maarten van Lohuizen (NKI, Amsterdam, the Netherlands) for Rnf2fl/fl mice, and Prof. Barbara Knowles (JAX, Bar Harbor, ME, USA) for Zp3-Cre transgenic mice. We are grateful to Rui Ma, Hui Quan, Xianglin Zhang, Zhaofeng Ye, Yuanyuan Li, Wenhao Zhang, Xiaowo Wang, Jianyang Zeng, Yiqin Gao, and Juntao Gao for discussions. We thank Drs. Haruhiko Koseki, Yi Zhang, and Inoue Azusa for sharing reagents or protocols. We appreciate members of the Xie laboratory for comments during preparation of the manuscript. This work is supported by funding provided by the National Natural Science Foundation of China (grants 31422031 and 31725018 to W.X.); the National Basic Research Program of China (grant 2015CB856201 to W.X.); the Beijing Municipal Science & Technology Commission (grant Z181100001318006 to W.X.); the THU-PKU Center for Life Sciences (W.X.); the Novartis Research Foundation (N.V. and A.H.F.M.P.); the European Research Council (grant ERC 695288?Totipotency to Y.K.K. E.A.O. and A.H.F.M.P.); and the JSPS (KAKENHI JP18H05214 to H.S.). Research in the laboratory of K.T. is supported by the Austrian Academy of Sciences, the FWF and Herzfelder foundation (P30613-B21), a European Research Council grant (ERC-StG-336460 ChromHeritance), and an HFSP project grant (PGP0057-2018). Z.D. H.Z. and Q.X. are supported by THU-PKU Center for Life Sciences postdoctoral fellowships. W.X. is an HHMI international research scholar. J.G. is supported by the European Research Council and the L'Or?al Austria Fellowship for Women in Science and is an associated student of the DK Chromosome Dynamics (W1238-B20) supported by the Austrian Science Fund (FWF). Z.D. H.Z. and W.X. conceived the project. Z.D. conducted the sisHi-C experiments. Z.L. Q.X. B.H. K.X. Z.D. Y.K.K. J.G. and K.Z. performed the mouse PGCs, oocytes, and embryo experiments. H.Z. and Z.D. performed bioinformatics analysis. L. Li and G.Y. performed the CUT&RUN experiments. J.G. performed the single-nucleus Hi-C experiments. S.P. processed the single-nucleus Hi-C data. L.C. P.W. L. Liu, E.A.O. N.V. Q.Z. and W.K.A.Y. helped with various experiments or analyses. Q.W. performed next-generation sequencing (NGS). A.H. Y.S. J.N. Q.S. H.S. K.T. A.H.F.M.P. and W.X. supervised the project or related experiments. Z.D. H.Z. K.Z. A.H.F.M.P. and W.X. wrote the manuscript, with help from other authors. The authors declare no competing interests. Funding Information: We thank Prof. Fei Gao (IOZ, Beijing, China) for providing Gdf9-Cre mice, Dr. Miguel Vidal (CSIC, Madrid, Spain) for Ring1 deficient mice, Prof. Maarten van Lohuizen (NKI, Amsterdam, the Netherlands) for Rnf2 fl/fl mice, and Prof. Barbara Knowles (JAX, Bar Harbor, ME, USA) for Zp3-Cre transgenic mice. We are grateful to Rui Ma, Hui Quan, Xianglin Zhang, Zhaofeng Ye, Yuanyuan Li, Wenhao Zhang, Xiaowo Wang, Jianyang Zeng, Yiqin Gao, and Juntao Gao for discussions. We thank Drs. Haruhiko Koseki, Yi Zhang, and Inoue Azusa for sharing reagents or protocols. We appreciate members of the Xie laboratory for comments during preparation of the manuscript. This work is supported by funding provided by the National Natural Science Foundation of China (grants 31422031 and 31725018 to W.X.); the National Basic Research Program of China (grant 2 015CB856201 to W.X.); the Beijing Municipal Science & Technology Commission (grant Z181100001318006 to W.X.); the THU-PKU Center for Life Sciences (W.X.); the Novartis Research Foundation (N.V. and A.H.F.M.P.); the European Research Council (grant ERC 695288–Totipotency to Y.K.K., E.A.O., and A.H.F.M.P.); and the JSPS ( KAKENHI JP18H05214 to H.S.). Research in the laboratory of K.T. is supported by the Austrian Academy of Sciences , the FWF and Herzfelder foundation ( P30613-B21 ), a European Research Council grant ( ERC-StG-336460 ChromHeritance), and an HFSP project grant ( PGP0057-2018 ). Z.D., H.Z., and Q.X. are supported by THU-PKU Center for Life Sciences postdoctoral fellowships. W.X. is an HHMI international research scholar. J.G. is supported by the European Research Council and the L'Oréal Austria Fellowship for Women in Science and is an associated student of the DK Chromosome Dynamics ( W1238-B20 ) supported by the Austrian Science Fund (FWF) .

PY - 2020/2/20

Y1 - 2020/2/20

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AB - In mammals, germ cells undergo a series of events to give rise to haploid gametes. The dynamics of meiotic chromatin architecture still remain poorly understood. By applying Hi-C to mouse oocytes, Du et al. reveal a unique Polycomb-regulated chromatin architecture, which adds a new perspective to the non-canonical oocyte epigenomes.

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