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Regulation of NSL by TAF4A is critical for genome stability and quiescence of muscle stem cells

Author

Listed:
  • Angelina M. Georgieva

    (Max Planck Institute for Heart and Lung Research)

  • Krishna Sreenivasan

    (Max Planck Institute for Heart and Lung Research)

  • Dong Ding

    (Max Planck Institute for Heart and Lung Research)

  • Clementine Villeneuve

    (Max Planck Institute for Molecular Biomedicine)

  • Sara A. Wickström

    (Max Planck Institute for Molecular Biomedicine)

  • Stefan Günther

    (Max Planck Institute for Heart and Lung Research)

  • Carsten Kuenne

    (Max Planck Institute for Heart and Lung Research)

  • Ulrich Gärtner

    (University of Giessen)

  • Xinyue Guo

    (Max Planck Institute for Heart and Lung Research)

  • Yonggang Zhou

    (Max Planck Institute for Heart and Lung Research)

  • Xuejun Yuan

    (Max Planck Institute for Heart and Lung Research)

  • Thomas Braun

    (Max Planck Institute for Heart and Lung Research
    The Hong Kong University of Science and Technology)

Abstract

Acetylation of lamin A/C by the non-specific lethal complex, containing MOF and KANSL2, is instrumental for maintaining nuclear architecture and genome stability, but the mechanisms controlling expression of its components in different cell types are poorly characterized. Here, we show that TAF4A, primarily known as a subunit of TFIID, forms a complex with the heterotrimeric transcription factor NF-Y and is critical for cell type-specific regulation of Kansl2 in muscle stem cells. Inactivation of Taf4a reduces expression of Kansl2 and alters post-translational modification of lamin A/C, thereby decreasing nuclear stiffness, which disrupts the nuclear architecture and results in severe genomic instability. Reduced expression of Kansl2 in Taf4a-mutant muscle stem cells changes expression of numerous genes involved in chromatin regulation. The subsequent loss of heterochromatin, in combination with pronounced genomic instability, activates muscle stem cells but impairs their proliferation, which depletes the stem cell pool and abolishes skeletal muscle regeneration. We conclude that TAF4A-NF-Y-dependent transcription regulation safeguards heterochromatin and genome stability of muscle stem cells via the non-specific lethal complex.

Suggested Citation

  • Angelina M. Georgieva & Krishna Sreenivasan & Dong Ding & Clementine Villeneuve & Sara A. Wickström & Stefan Günther & Carsten Kuenne & Ulrich Gärtner & Xinyue Guo & Yonggang Zhou & Xuejun Yuan & Thom, 2025. "Regulation of NSL by TAF4A is critical for genome stability and quiescence of muscle stem cells," Nature Communications, Nature, vol. 16(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-025-64402-1
    DOI: 10.1038/s41467-025-64402-1
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    as
    1. Angelina M. Georgieva & Xinyue Guo & Marek Bartkuhn & Stefan Günther & Carsten Künne & Christian Smolka & Ann Atzberger & Ulrich Gärtner & Kamel Mamchaoui & Eva Bober & Yonggang Zhou & Xuejun Yuan & T, 2022. "Inactivation of Sirt6 ameliorates muscular dystrophy in mdx mice by releasing suppression of utrophin expression," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    2. Suyang Zhang & Feng Yang & Yile Huang & Liangqiang He & Yuying Li & Yi Ching Esther Wan & Yingzhe Ding & Kui Ming Chan & Ting Xie & Hao Sun & Huating Wang, 2023. "ATF3 induction prevents precocious activation of skeletal muscle stem cell by regulating H2B expression," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    3. Suyang Zhang & Feng Yang & Yile Huang & Liangqiang He & Yuying Li & Yi Ching Esther Wan & Yingzhe Ding & Kui Ming Chan & Ting Xie & Hao Sun & Huating Wang, 2023. "Author Correction: ATF3 induction prevents precocious activation of skeletal muscle stem cell by regulating H2B expression," Nature Communications, Nature, vol. 14(1), pages 1-1, December.
    4. F. Relaix & M. Bencze & M. J. Borok & A. Vartanian & F. Gattazzo & D. Mademtzoglou & S. Perez-Diaz & A. Prola & P. C. Reyes-Fernandez & A. Rotini & Taglietti, 2021. "Perspectives on skeletal muscle stem cells," Nature Communications, Nature, vol. 12(1), pages 1-11, December.
    5. Diana Langer & Igor Martianov & Daniel Alpern & Muriel Rhinn & Céline Keime & Pascal Dollé & Gabrielle Mengus & Irwin Davidson, 2016. "Essential role of the TFIID subunit TAF4 in murine embryogenesis and embryonic stem cell differentiation," Nature Communications, Nature, vol. 7(1), pages 1-16, April.
    6. Cheng-Zhong Zhang & Alexander Spektor & Hauke Cornils & Joshua M. Francis & Emily K. Jackson & Shiwei Liu & Matthew Meyerson & David Pellman, 2015. "Chromothripsis from DNA damage in micronuclei," Nature, Nature, vol. 522(7555), pages 179-184, June.
    7. Ting Zhang & Carsten Künne & Dong Ding & Stefan Günther & Xinyue Guo & Yonggang Zhou & Xuejun Yuan & Thomas Braun, 2022. "Replication collisions induced by de-repressed S-phase transcription are connected with malignant transformation of adult stem cells," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
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