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ARID1A safeguards the canalization of the cell fate decision during osteoclastogenesis

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  • Jiahui Du

    (Shanghai Jiao Tong University School of Medicine
    Shanghai Jiao Tong University
    Shanghai Engineering Research Center of Advanced Dental Technology and Materials)

  • Yili Liu

    (Shanghai Jiao Tong University School of Medicine
    Shanghai Jiao Tong University
    Shanghai Engineering Research Center of Advanced Dental Technology and Materials)

  • Jinrui Sun

    (Shanghai Jiao Tong University School of Medicine
    Shanghai Jiao Tong University
    Shanghai Engineering Research Center of Advanced Dental Technology and Materials)

  • Enhui Yao

    (Shanghai Jiao Tong University School of Medicine
    Shanghai Jiao Tong University
    Shanghai Engineering Research Center of Advanced Dental Technology and Materials)

  • Jingyi Xu

    (Shanghai Jiao Tong University School of Medicine
    Shanghai Jiao Tong University
    Shanghai Engineering Research Center of Advanced Dental Technology and Materials)

  • Xiaolin Wu

    (Shanghai Jiao Tong University School of Medicine
    Shanghai Jiao Tong University
    Shanghai Engineering Research Center of Advanced Dental Technology and Materials)

  • Ling Xu

    (Shanghai Jiao Tong University School of Medicine
    Shanghai Jiao Tong University
    Shanghai Engineering Research Center of Advanced Dental Technology and Materials)

  • Mingliang Zhou

    (Shanghai Jiao Tong University School of Medicine
    Shanghai Jiao Tong University
    Shanghai Engineering Research Center of Advanced Dental Technology and Materials)

  • Guangzheng Yang

    (Shanghai Jiao Tong University School of Medicine
    Shanghai Jiao Tong University
    Shanghai Engineering Research Center of Advanced Dental Technology and Materials)

  • Xinquan Jiang

    (Shanghai Jiao Tong University School of Medicine
    Shanghai Jiao Tong University
    Shanghai Engineering Research Center of Advanced Dental Technology and Materials)

Abstract

Chromatin remodeler ARID1A regulates gene transcription by modulating nucleosome positioning and chromatin accessibility. While ARID1A-mediated stage and lineage-restricted gene regulation during cell fate canalization remains unresolved. Using osteoclastogenesis as a model, we show that ARID1A transcriptionally safeguards the osteoclast (OC) fate canalization during proliferation-differentiation switching at single-cell resolution. Notably, ARID1A is indispensable for the transcriptional apparatus condensates formation with coactivator BRD4/lineage-specifying transcription factor (TF) PU.1 at Nfatc1 super-enhancer during safeguarding the OC fate canalization. Besides, the antagonist function between ARID1A-cBAF and BRD9-ncBAF complex during osteoclastogenesis has been validated with in vitro assay and compound mutant mouse model. Furthermore, the antagonistic function of ARID1A-“accelerator” and BRD9-“brake” both depend on coactivator BRD4-“clutch” during osteoclastogenesis. Overall, these results uncover sophisticated cooperation between chromatin remodeler ARID1A, coactivator, and lineage-specifying TF at super-enhancer of lineage master TF in a condensate manner, and antagonist between distinct BAF complexes in the proper and balanced cell fate canalization.

Suggested Citation

  • Jiahui Du & Yili Liu & Jinrui Sun & Enhui Yao & Jingyi Xu & Xiaolin Wu & Ling Xu & Mingliang Zhou & Guangzheng Yang & Xinquan Jiang, 2024. "ARID1A safeguards the canalization of the cell fate decision during osteoclastogenesis," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-50225-z
    DOI: 10.1038/s41467-024-50225-z
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    1. Ji-Eun Lee & Young-Kwon Park & Sarah Park & Younghoon Jang & Nicholas Waring & Anup Dey & Keiko Ozato & Binbin Lai & Weiqun Peng & Kai Ge, 2017. "Brd4 binds to active enhancers to control cell identity gene induction in adipogenesis and myogenesis," Nature Communications, Nature, vol. 8(1), pages 1-12, December.
    2. Jovylyn Gatchalian & Shivani Malik & Josephine Ho & Dong-Sung Lee & Timothy W. R. Kelso & Maxim N. Shokhirev & Jesse R. Dixon & Diana C. Hargreaves, 2018. "A non-canonical BRD9-containing BAF chromatin remodeling complex regulates naive pluripotency in mouse embryonic stem cells," Nature Communications, Nature, vol. 9(1), pages 1-16, December.
    3. Jesse R. Dixon & Siddarth Selvaraj & Feng Yue & Audrey Kim & Yan Li & Yin Shen & Ming Hu & Jun S. Liu & Bing Ren, 2012. "Topological domains in mammalian genomes identified by analysis of chromatin interactions," Nature, Nature, vol. 485(7398), pages 376-380, May.
    4. Wei Wang & Jiang-Jiang Qin & Sukesh Voruganti & Kalkunte S. Srivenugopal & Subhasree Nag & Shivaputra Patil & Horrick Sharma & Ming-Hai Wang & Hui Wang & John K Buolamwini & Ruiwen Zhang, 2014. "The pyrido[b]indole MDM2 inhibitor SP-141 exerts potent therapeutic effects in breast cancer models," Nature Communications, Nature, vol. 5(1), pages 1-12, December.
    5. Jiahui Du & Yili Liu & Xiaolin Wu & Jinrui Sun & Junfeng Shi & Hongming Zhang & Ao Zheng & Mingliang Zhou & Xinquan Jiang, 2023. "BRD9-mediated chromatin remodeling suppresses osteoclastogenesis through negative feedback mechanism," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    6. Mark A. Dawson & Rab K. Prinjha & Antje Dittmann & George Giotopoulos & Marcus Bantscheff & Wai-In Chan & Samuel C. Robson & Chun-wa Chung & Carsten Hopf & Mikhail M. Savitski & Carola Huthmacher & Em, 2011. "Inhibition of BET recruitment to chromatin as an effective treatment for MLL-fusion leukaemia," Nature, Nature, vol. 478(7370), pages 529-533, October.
    7. Lena Ho & Gerald R. Crabtree, 2010. "Chromatin remodelling during development," Nature, Nature, vol. 463(7280), pages 474-484, January.
    8. William J. Boyle & W. Scott Simonet & David L. Lacey, 2003. "Osteoclast differentiation and activation," Nature, Nature, vol. 423(6937), pages 337-342, May.
    9. Yohei Abe & Royhan Rozqie & Yoshihiro Matsumura & Takeshi Kawamura & Ryo Nakaki & Yuya Tsurutani & Kyoko Tanimura-Inagaki & Akira Shiono & Kenta Magoori & Kanako Nakamura & Shotaro Ogi & Shingo Kajimu, 2015. "JMJD1A is a signal-sensing scaffold that regulates acute chromatin dynamics via SWI/SNF association for thermogenesis," Nature Communications, Nature, vol. 6(1), pages 1-14, November.
    10. Heiko Lickert & Jun K. Takeuchi & Ingo von Both & Johnathon R. Walls & Fionnuala McAuliffe & S. Lee Adamson & R. Mark Henkelman & Jeffrey L. Wrana & Janet Rossant & Benoit G. Bruneau, 2004. "Baf60c is essential for function of BAF chromatin remodelling complexes in heart development," Nature, Nature, vol. 432(7013), pages 107-112, November.
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