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Extended DNA threading through a dual-engine motor module of the activating signal co-integrator 1 complex

Author

Listed:
  • Junqiao Jia

    (Laboratory of Structural Biochemistry
    Harvard Medical School, Department of Cell Biology)

  • Tarek Hilal

    (Laboratory of Structural Biochemistry
    Research Center of Electron Microscopy)

  • Katherine E. Bohnsack

    (Universitätsmedizin Göttingen, Department of Molecular Biology)

  • Aleksandar Chernev

    (Bioanalytical Mass Spectrometry)

  • Ning Tsao

    (Washington University School of Medicine, Department of Pathology & Immunology and Center for Genome Integrity)

  • Juliane Bethmann

    (Bioanalytical Mass Spectrometry
    Universitätsmedizin Göttingen, Institut für Klinische Chemie, Bioanalytik)

  • Aruna Arumugam

    (Laboratory of Structural Biochemistry)

  • Lane Parmely

    (Washington University School of Medicine, Department of Pathology & Immunology and Center for Genome Integrity)

  • Nicole Holton

    (Laboratory of Structural Biochemistry)

  • Bernhard Loll

    (Laboratory of Structural Biochemistry)

  • Nima Mosammaparast

    (Washington University School of Medicine, Department of Pathology & Immunology and Center for Genome Integrity)

  • Markus T. Bohnsack

    (Universitätsmedizin Göttingen, Department of Molecular Biology
    Georg-August-Universität, Göttingen Center for Molecular Biosciences
    Max-Planck-Institut für Multidisziplinäre Naturwissenschaften)

  • Henning Urlaub

    (Bioanalytical Mass Spectrometry
    Universitätsmedizin Göttingen, Institut für Klinische Chemie, Bioanalytik)

  • Markus C. Wahl

    (Laboratory of Structural Biochemistry
    Macromolecular Crystallography)

Abstract

Activating signal co-integrator 1 complex (ASCC) subunit 3 (ASCC3) supports diverse genome maintenance and gene expression processes, and contains tandem Ski2-like NTPase/helicase cassettes crucial for these functions. Presently, the molecular mechanisms underlying ASCC3 helicase activity and regulation remain unresolved. We present cryogenic electron microscopy, DNA-protein cross-linking/mass spectrometry as well as in vitro and cellular functional analyses of the ASCC3-TRIP4 sub-module of ASCC. Unlike the related spliceosomal SNRNP200 RNA helicase, ASCC3 can thread substrates through both helicase cassettes. TRIP4 docks on ASCC3 via a zinc finger domain and stimulates the helicase by positioning an ASC-1 homology domain next to the C-terminal helicase cassette of ASCC3, likely supporting substrate engagement and assisting the DNA exit. TRIP4 binds ASCC3 mutually exclusively with the DNA/RNA dealkylase, ALKBH3, directing ASCC3 for specific processes. Our findings define ASCC3-TRIP4 as a tunable motor module of ASCC that encompasses two cooperating NTPase/helicase units functionally expanded by TRIP4.

Suggested Citation

  • Junqiao Jia & Tarek Hilal & Katherine E. Bohnsack & Aleksandar Chernev & Ning Tsao & Juliane Bethmann & Aruna Arumugam & Lane Parmely & Nicole Holton & Bernhard Loll & Nima Mosammaparast & Markus T. B, 2023. "Extended DNA threading through a dual-engine motor module of the activating signal co-integrator 1 complex," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-37528-3
    DOI: 10.1038/s41467-023-37528-3
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