Cell Reports (Jan 2024)
The male pachynema-specific protein MAPS drives phase separation in vitro and regulates sex body formation and chromatin behaviors in vivo
- Zexiong Lin,
- Dongliang Li,
- Jiahuan Zheng,
- Chencheng Yao,
- Dongteng Liu,
- Hao Zhang,
- Haiwei Feng,
- Chunxu Chen,
- Peng Li,
- Yuxiang Zhang,
- Binjie Jiang,
- Zhe Hu,
- Yu Zhao,
- Fu Shi,
- Dandan Cao,
- Kenny A. Rodriguez-Wallberg,
- Zheng Li,
- William S.B. Yeung,
- Louise T. Chow,
- Hengbin Wang,
- Kui Liu
Affiliations
- Zexiong Lin
- Department of Obstetrics and Gynecology, Li Ka Shing Faculty of Medicine; Shenzhen Key Laboratory of Fertility Regulation, Center of Assisted Reproduction and Embryology, The University of Hong Kong-Shenzhen Hospital, The University of Hong Kong, Hong Kong, China
- Dongliang Li
- Department of Obstetrics and Gynecology, Li Ka Shing Faculty of Medicine; Shenzhen Key Laboratory of Fertility Regulation, Center of Assisted Reproduction and Embryology, The University of Hong Kong-Shenzhen Hospital, The University of Hong Kong, Hong Kong, China
- Jiahuan Zheng
- Department of Obstetrics and Gynecology, Li Ka Shing Faculty of Medicine; Shenzhen Key Laboratory of Fertility Regulation, Center of Assisted Reproduction and Embryology, The University of Hong Kong-Shenzhen Hospital, The University of Hong Kong, Hong Kong, China
- Chencheng Yao
- Department of Andrology, Center for Men’s Health, Department of ART, Institute of Urology, Urologic Medical Center, Shanghai Key Laboratory of Reproductive Medicine, Shanghai General Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200080, China
- Dongteng Liu
- Department of Obstetrics and Gynecology, Li Ka Shing Faculty of Medicine; Shenzhen Key Laboratory of Fertility Regulation, Center of Assisted Reproduction and Embryology, The University of Hong Kong-Shenzhen Hospital, The University of Hong Kong, Hong Kong, China
- Hao Zhang
- Department of Biochemistry and Molecular Genetics, University of Alabama at Birmingham, Birmingham, AL, USA
- Haiwei Feng
- Department of Obstetrics and Gynecology, Li Ka Shing Faculty of Medicine; Shenzhen Key Laboratory of Fertility Regulation, Center of Assisted Reproduction and Embryology, The University of Hong Kong-Shenzhen Hospital, The University of Hong Kong, Hong Kong, China
- Chunxu Chen
- Department of Biochemistry and Molecular Genetics, University of Alabama at Birmingham, Birmingham, AL, USA; Department of Internal Medicine, Division of Hematology, Oncology and Palliative Care, Massey Cancer Institute, Virginia Commonwealth University, Richmond, VA, USA
- Peng Li
- Department of Andrology, Center for Men’s Health, Department of ART, Institute of Urology, Urologic Medical Center, Shanghai Key Laboratory of Reproductive Medicine, Shanghai General Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200080, China
- Yuxiang Zhang
- Department of Andrology, Center for Men’s Health, Department of ART, Institute of Urology, Urologic Medical Center, Shanghai Key Laboratory of Reproductive Medicine, Shanghai General Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200080, China
- Binjie Jiang
- Department of Obstetrics and Gynecology, Li Ka Shing Faculty of Medicine; Shenzhen Key Laboratory of Fertility Regulation, Center of Assisted Reproduction and Embryology, The University of Hong Kong-Shenzhen Hospital, The University of Hong Kong, Hong Kong, China
- Zhe Hu
- Department of Obstetrics and Gynecology, Li Ka Shing Faculty of Medicine; Shenzhen Key Laboratory of Fertility Regulation, Center of Assisted Reproduction and Embryology, The University of Hong Kong-Shenzhen Hospital, The University of Hong Kong, Hong Kong, China
- Yu Zhao
- Department of Obstetrics and Gynecology, Li Ka Shing Faculty of Medicine; Shenzhen Key Laboratory of Fertility Regulation, Center of Assisted Reproduction and Embryology, The University of Hong Kong-Shenzhen Hospital, The University of Hong Kong, Hong Kong, China
- Fu Shi
- Department of Obstetrics and Gynecology, Li Ka Shing Faculty of Medicine; Shenzhen Key Laboratory of Fertility Regulation, Center of Assisted Reproduction and Embryology, The University of Hong Kong-Shenzhen Hospital, The University of Hong Kong, Hong Kong, China
- Dandan Cao
- Department of Obstetrics and Gynecology, Li Ka Shing Faculty of Medicine; Shenzhen Key Laboratory of Fertility Regulation, Center of Assisted Reproduction and Embryology, The University of Hong Kong-Shenzhen Hospital, The University of Hong Kong, Hong Kong, China
- Kenny A. Rodriguez-Wallberg
- Department of Oncology-Pathology, The Karolinska Institute, 14186 Stockholm, Sweden
- Zheng Li
- Department of Andrology, Center for Men’s Health, Department of ART, Institute of Urology, Urologic Medical Center, Shanghai Key Laboratory of Reproductive Medicine, Shanghai General Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200080, China
- William S.B. Yeung
- Department of Obstetrics and Gynecology, Li Ka Shing Faculty of Medicine; Shenzhen Key Laboratory of Fertility Regulation, Center of Assisted Reproduction and Embryology, The University of Hong Kong-Shenzhen Hospital, The University of Hong Kong, Hong Kong, China
- Louise T. Chow
- Department of Biochemistry and Molecular Genetics, University of Alabama at Birmingham, Birmingham, AL, USA; Corresponding author
- Hengbin Wang
- Department of Biochemistry and Molecular Genetics, University of Alabama at Birmingham, Birmingham, AL, USA; Department of Internal Medicine, Division of Hematology, Oncology and Palliative Care, Massey Cancer Institute, Virginia Commonwealth University, Richmond, VA, USA; Corresponding author
- Kui Liu
- Department of Obstetrics and Gynecology, Li Ka Shing Faculty of Medicine; Shenzhen Key Laboratory of Fertility Regulation, Center of Assisted Reproduction and Embryology, The University of Hong Kong-Shenzhen Hospital, The University of Hong Kong, Hong Kong, China; Corresponding author
- Journal volume & issue
-
Vol. 43,
no. 1
p. 113651
Abstract
Summary: Dynamic chromosome remodeling and nuclear compartmentalization take place during mammalian meiotic prophase I. We report here that the crucial roles of male pachynema-specific protein (MAPS) in pachynema progression might be mediated by its liquid-liquid phase separation in vitro and in cellulo. MAPS forms distinguishable liquid phases, and deletion or mutations of its N-terminal amino acids (aa) 2−9 disrupt its secondary structure and charge properties, impeding phase separation. Maps−/− pachytene spermatocytes exhibit defects in nucleus compartmentalization, including defects in forming sex bodies, altered nucleosome composition, and disordered chromatin accessibility. MapsΔ2–9/Δ2–9 male mice expressing MAPS protein lacking aa 2–9 phenocopy Maps−/− mice. Moreover, a frameshift mutation in C3orf62, the human counterpart of Maps, is correlated with nonobstructive azoospermia in a patient exhibiting pachynema arrest in spermatocyte development. Hence, the phase separation property of MAPS seems essential for pachynema progression in mouse and human spermatocytes.
