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Fosl2 facilitates chromatin accessibility to determine developmental events during follicular maturation

Author

Listed:
  • Hongyong Zhang

    (Guangdong Medical University)

  • Zechen Li

    (Guangdong Medical University)

  • Yanmei Zhu

    (Guangdong Medical University)

  • Wencong Lyu

    (Peking University)

  • Wenlu Wei

    (Guangdong Medical University)

  • Haochen Wang

    (Peking University)

  • Shuangjie Tian

    (Chinese Academy of Sciences)

  • Wei Yue

    (Shenyang Normal University)

  • Jiajing Zhong

    (Guangdong Medical University)

  • Qing-Yuan Sun

    (Guangdong Second Provincial General Hospital)

  • Yiting Guan

    (Guangdong Medical University)

Abstract

Granulosa cells (GCs) are the most dynamically responsive cell lineage to encourage continuous folliculogenesis; however, developmental dynamics and interplay with downstream transcription circuitry remain unclear. Here, we unravel the redistribution of genome-wide chromatin areas that drive broad developmental-related transcriptomic alterations during follicular maturation in murine and porcine GCs. Distinct GC-activated accessibility regions (GAAs) at the ovulatory phase are responsible for augmenting flanking GC-involved developmental gene (GDG) expression, which are essential for transcriptional responses to developmental cues. Mechanistically, the transcription factor Fosl2 is strongly recruited to GAAs, facilitating chromatin accessibility state transition. Elevated GAA signals driven by Fosl2 loading induce a significant upregulation of adjacent GDG expression. Additionally, GC-specific Fosl2 deletion in mice perturbs GC cellularity, leading to subfertility related to reproductive aging. Together, we highlight a dynamic chromatin accessibility landscape during follicular maturation, revealing the indispensable Fosl2 function not only controls transcriptional activation via a reconfigured chromatin state, but also orchestrates intricate signaling pathways that are fundamental for ovulation and reproduction.

Suggested Citation

  • Hongyong Zhang & Zechen Li & Yanmei Zhu & Wencong Lyu & Wenlu Wei & Haochen Wang & Shuangjie Tian & Wei Yue & Jiajing Zhong & Qing-Yuan Sun & Yiting Guan, 2025. "Fosl2 facilitates chromatin accessibility to determine developmental events during follicular maturation," Nature Communications, Nature, vol. 16(1), pages 1-19, December.
  • Handle: RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-025-64009-6
    DOI: 10.1038/s41467-025-64009-6
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    1. Michelle M. Halstead & Xin Ma & Chuan Zhou & Richard M. Schultz & Pablo J. Ross, 2020. "Chromatin remodeling in bovine embryos indicates species-specific regulation of genome activation," Nature Communications, Nature, vol. 11(1), pages 1-16, December.
    2. André F. Rendeiro & Christian Schmidl & Jonathan C. Strefford & Renata Walewska & Zadie Davis & Matthias Farlik & David Oscier & Christoph Bock, 2016. "Chromatin accessibility maps of chronic lymphocytic leukaemia identify subtype-specific epigenome signatures and transcription regulatory networks," Nature Communications, Nature, vol. 7(1), pages 1-12, September.
    3. Mette Bentsen & Philipp Goymann & Hendrik Schultheis & Kathrin Klee & Anastasiia Petrova & René Wiegandt & Annika Fust & Jens Preussner & Carsten Kuenne & Thomas Braun & Johnny Kim & Mario Looso, 2020. "ATAC-seq footprinting unravels kinetics of transcription factor binding during zygotic genome activation," Nature Communications, Nature, vol. 11(1), pages 1-11, December.
    4. Yan Zhang & Ye Wang & Xie’an Feng & Shuo Zhang & Xueqiang Xu & Lingyu Li & Shudong Niu & Yingnan Bo & Chao Wang & Zhen Li & Guoliang Xia & Hua Zhang, 2021. "Oocyte-derived microvilli control female fertility by optimizing ovarian follicle selection in mice," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    5. Jingyi Wu & Jiawei Xu & Bofeng Liu & Guidong Yao & Peizhe Wang & Zili Lin & Bo Huang & Xuepeng Wang & Tong Li & Senlin Shi & Nan Zhang & Fuyu Duan & Jia Ming & Xiangyang Zhang & Wenbin Niu & Wenyan So, 2018. "Publisher Correction: Chromatin analysis in human early development reveals epigenetic transition during ZGA," Nature, Nature, vol. 560(7718), pages 27-27, August.
    6. Jingyi Wu & Jiawei Xu & Bofeng Liu & Guidong Yao & Peizhe Wang & Zili Lin & Bo Huang & Xuepeng Wang & Tong Li & Senlin Shi & Nan Zhang & Fuyu Duan & Jia Ming & Xiangyang Zhang & Wenbin Niu & Wenyan So, 2018. "Chromatin analysis in human early development reveals epigenetic transition during ZGA," Nature, Nature, vol. 557(7704), pages 256-260, May.
    7. Huarong Wang & Han Cai & Xiao Wang & Meiling Zhang & Bingying Liu & Ziqi Chen & Tingting Yang & Junshun Fang & Yanhao Zhang & Wei Liu & Jun Han & Qirui Guo & Hua Zhang & Haibin Wang & Guoliang Xia & C, 2019. "HDAC3 maintains oocyte meiosis arrest by repressing amphiregulin expression before the LH surge," Nature Communications, Nature, vol. 10(1), pages 1-12, December.
    8. Jingyi Wu & Bo Huang & He Chen & Qiangzong Yin & Yang Liu & Yunlong Xiang & Bingjie Zhang & Bofeng Liu & Qiujun Wang & Weikun Xia & Wenzhi Li & Yuanyuan Li & Jing Ma & Xu Peng & Hui Zheng & Jia Ming &, 2016. "The landscape of accessible chromatin in mammalian preimplantation embryos," Nature, Nature, vol. 534(7609), pages 652-657, June.
    9. Franco Izzo & Robert M. Myers & Saravanan Ganesan & Levan Mekerishvili & Sanjay Kottapalli & Tamara Prieto & Elliot O. Eton & Theo Botella & Andrew J. Dunbar & Robert L. Bowman & Jesus Sotelo & Cather, 2024. "Mapping genotypes to chromatin accessibility profiles in single cells," Nature, Nature, vol. 629(8014), pages 1149-1157, May.
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