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Mechanism of Rad26-assisted rescue of stalled RNA polymerase II in transcription-coupled repair

Author

Listed:
  • Chunli Yan

    (Georgia State University
    Georgia State University)

  • Thomas Dodd

    (Georgia State University
    Georgia State University)

  • Jina Yu

    (Georgia State University
    Georgia State University)

  • Bernice Leung

    (University of California San Diego)

  • Jun Xu

    (University of California San Diego)

  • Juntaek Oh

    (University of California San Diego)

  • Dong Wang

    (University of California San Diego
    University of California San Diego
    University of California San Diego)

  • Ivaylo Ivanov

    (Georgia State University
    Georgia State University)

Abstract

Transcription-coupled repair is essential for the removal of DNA lesions from the transcribed genome. The pathway is initiated by CSB protein binding to stalled RNA polymerase II. Mutations impairing CSB function cause severe genetic disease. Yet, the ATP-dependent mechanism by which CSB powers RNA polymerase to bypass certain lesions while triggering excision of others is incompletely understood. Here we build structural models of RNA polymerase II bound to the yeast CSB ortholog Rad26 in nucleotide-free and bound states. This enables simulations and graph-theoretical analyses to define partitioning of this complex into dynamic communities and delineate how its structural elements function together to remodel DNA. We identify an allosteric pathway coupling motions of the Rad26 ATPase modules to changes in RNA polymerase and DNA to unveil a structural mechanism for CSB-assisted progression past less bulky lesions. Our models allow functional interpretation of the effects of Cockayne syndrome disease mutations.

Suggested Citation

  • Chunli Yan & Thomas Dodd & Jina Yu & Bernice Leung & Jun Xu & Juntaek Oh & Dong Wang & Ivaylo Ivanov, 2021. "Mechanism of Rad26-assisted rescue of stalled RNA polymerase II in transcription-coupled repair," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-27295-4
    DOI: 10.1038/s41467-021-27295-4
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    References listed on IDEAS

    as
    1. Lijuan Yan & Li Wang & Yuanyuan Tian & Xian Xia & Zhucheng Chen, 2016. "Structure and regulation of the chromatin remodeller ISWI," Nature, Nature, vol. 540(7633), pages 466-469, 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. Yana van der Weegen & Hadar Golan-Berman & Tycho E. T. Mevissen & Katja Apelt & Román González-Prieto & Joachim Goedhart & Elisheva E. Heilbrun & Alfred C. O. Vertegaal & Diana van den Heuvel & Johann, 2020. "The cooperative action of CSB, CSA, and UVSSA target TFIIH to DNA damage-stalled RNA polymerase II," Nature Communications, Nature, vol. 11(1), pages 1-16, December.
    4. Meijing Li & Xian Xia & Yuanyuan Tian & Qi Jia & Xiaoyu Liu & Ying Lu & Ming Li & Xueming Li & Zhucheng Chen, 2019. "Mechanism of DNA translocation underlying chromatin remodelling by Snf2," Nature, Nature, vol. 567(7748), pages 409-413, March.
    5. Jun Xu & Indrajit Lahiri & Wei Wang & Adam Wier & Michael A. Cianfrocco & Jenny Chong & Alissa A. Hare & Peter B. Dervan & Frank DiMaio & Andres E. Leschziner & Dong Wang, 2017. "Structural basis for the initiation of eukaryotic transcription-coupled DNA repair," Nature, Nature, vol. 551(7682), pages 653-657, November.
    6. Yana Weegen & Hadar Golan-Berman & Tycho E. T. Mevissen & Katja Apelt & Román González-Prieto & Joachim Goedhart & Elisheva E. Heilbrun & Alfred C. O. Vertegaal & Diana Heuvel & Johannes C. Walter & S, 2020. "Publisher Correction: The cooperative action of CSB, CSA, and UVSSA target TFIIH to DNA damage-stalled RNA polymerase II," Nature Communications, Nature, vol. 11(1), pages 1-1, December.
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    Cited by:

    1. Jina Yu & Chunli Yan & Thomas Dodd & Chi-Lin Tsai & John A. Tainer & Susan E. Tsutakawa & Ivaylo Ivanov, 2023. "Dynamic conformational switching underlies TFIIH function in transcription and DNA repair and impacts genetic diseases," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    2. Xuan Zhang & Jun Xu & Jing Hu & Sitao Zhang & Yajing Hao & Dongyang Zhang & Hao Qian & Dong Wang & Xiang-Dong Fu, 2024. "Cockayne Syndrome Linked to Elevated R-Loops Induced by Stalled RNA Polymerase II during Transcription Elongation," Nature Communications, Nature, vol. 15(1), pages 1-16, December.

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