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The AT-hook is an evolutionarily conserved auto-regulatory domain of SWI/SNF required for cell lineage priming

Author

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  • Dhurjhoti Saha

    (Univ. of Texas MD Anderson Cancer Center
    University of Texas MD Anderson Cancer Center, Center for Cancer Epigenetics)

  • Solomon Hailu

    (Univ. of Texas MD Anderson Cancer Center
    University of Texas MD Anderson Cancer Center, Center for Cancer Epigenetics
    Illumina, 5200 Illumina Way)

  • Arjan Hada

    (Univ. of Texas MD Anderson Cancer Center
    University of Texas MD Anderson Cancer Center, Center for Cancer Epigenetics)

  • Junwoo Lee

    (Univ. of Texas MD Anderson Cancer Center
    University of Texas MD Anderson Cancer Center, Center for Cancer Epigenetics)

  • Jie Luo

    (Institute for Systems Biology)

  • Jeff A. Ranish

    (Institute for Systems Biology)

  • Yuan-chi Lin

    (Univ. of Texas MD Anderson Cancer Center
    University of Texas MD Anderson Cancer Center, Center for Cancer Epigenetics
    BioAgilytix)

  • Kyle Feola

    (Univ. of Texas MD Anderson Cancer Center
    University of Texas Southwestern Medical Center)

  • Jim Persinger

    (Univ. of Texas MD Anderson Cancer Center
    University of Texas MD Anderson Cancer Center, Center for Cancer Epigenetics)

  • Abhinav Jain

    (Univ. of Texas MD Anderson Cancer Center
    University of Texas MD Anderson Cancer Center, Center for Cancer Epigenetics)

  • Bin Liu

    (Univ. of Texas MD Anderson Cancer Center)

  • Yue Lu

    (Univ. of Texas MD Anderson Cancer Center)

  • Payel Sen

    (National Institute on Aging)

  • Blaine Bartholomew

    (Univ. of Texas MD Anderson Cancer Center
    University of Texas MD Anderson Cancer Center, Center for Cancer Epigenetics)

Abstract

The SWI/SNF ATP-dependent chromatin remodeler is a master regulator of the epigenome, controlling pluripotency and differentiation. Towards the C-terminus of the catalytic subunit of SWI/SNF is a motif called the AT-hook that is evolutionary conserved. The AT-hook is present in many chromatin modifiers and generally thought to help anchor them to DNA. We observe however that the AT-hook regulates the intrinsic DNA-stimulated ATPase activity aside from promoting SWI/SNF recruitment to DNA or nucleosomes by increasing the reaction velocity a factor of 13 with no accompanying change in substrate affinity (KM). The changes in ATP hydrolysis causes an equivalent change in nucleosome movement, confirming they are tightly coupled. The catalytic subunit’s AT-hook is required in vivo for SWI/SNF remodeling activity in yeast and mouse embryonic stem cells. The AT-hook in SWI/SNF is required for transcription regulation and activation of stage-specific enhancers critical in cell lineage priming. Similarly, growth assays suggest the AT-hook is required in yeast SWI/SNF for activation of genes involved in amino acid biosynthesis and metabolizing ethanol. Our findings highlight the importance of studying SWI/SNF attenuation versus eliminating the catalytic subunit or completely shutting down its enzymatic activity.

Suggested Citation

  • Dhurjhoti Saha & Solomon Hailu & Arjan Hada & Junwoo Lee & Jie Luo & Jeff A. Ranish & Yuan-chi Lin & Kyle Feola & Jim Persinger & Abhinav Jain & Bin Liu & Yue Lu & Payel Sen & Blaine Bartholomew, 2023. "The AT-hook is an evolutionarily conserved auto-regulatory domain of SWI/SNF required for cell lineage priming," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-40386-8
    DOI: 10.1038/s41467-023-40386-8
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    1. Young-Kwon Park & Ji-Eun Lee & Zhijiang Yan & Kaitlin McKernan & Tommy O’Haren & Weidong Wang & Weiqun Peng & Kai Ge, 2021. "Interplay of BAF and MLL4 promotes cell type-specific enhancer activation," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    2. Xiaoyu Liu & Meijing Li & Xian Xia & Xueming Li & Zhucheng Chen, 2017. "Mechanism of chromatin remodelling revealed by the Snf2-nucleosome structure," Nature, Nature, vol. 544(7651), pages 440-445, April.
    3. 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.
    4. Cedric R. Clapier & Bradley R. Cairns, 2012. "Regulation of ISWI involves inhibitory modules antagonized by nucleosomal epitopes," Nature, Nature, vol. 492(7428), pages 280-284, December.
    5. 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.
    6. Emma A. Morrison & Julio C. Sanchez & Jehnna L. Ronan & Daniel P. Farrell & Katayoun Varzavand & Jenna K. Johnson & Brian X. Gu & Gerald R. Crabtree & Catherine A. Musselman, 2017. "DNA binding drives the association of BRG1/hBRM bromodomains with nucleosomes," Nature Communications, Nature, vol. 8(1), pages 1-14, December.
    7. Yan Han & Alexis A Reyes & Sara Malik & Yuan He, 2020. "Cryo-EM structure of SWI/SNF complex bound to a nucleosome," Nature, Nature, vol. 579(7799), pages 452-455, March.
    8. Darko Barisic & Michael B. Stadler & Mario Iurlaro & Dirk Schübeler, 2019. "Mammalian ISWI and SWI/SNF selectively mediate binding of distinct transcription factors," Nature, Nature, vol. 569(7754), pages 136-140, May.
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