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Single-molecule reconstruction of eukaryotic factor-dependent transcription termination

Author

Listed:
  • Ying Xiong

    (Chinese Academy of Sciences
    Songshan Lake Materials Laboratory
    University of Chinese Academy of Sciences)

  • Weijing Han

    (Songshan Lake Materials Laboratory)

  • Chunhua Xu

    (Chinese Academy of Sciences)

  • Jing Shi

    (Nanjing University of Chinese Medicine
    Zhejiang University School of Medicine)

  • Lisha Wang

    (Songshan Lake Materials Laboratory)

  • Taoli Jin

    (Songshan Lake Materials Laboratory)

  • Qi Jia

    (Songshan Lake Materials Laboratory)

  • Ying Lu

    (Chinese Academy of Sciences)

  • Shuxin Hu

    (Chinese Academy of Sciences)

  • Shuo-Xing Dou

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Wei Lin

    (Nanjing University of Chinese Medicine
    Jiangsu Collaborative Innovation Center of Chinese Medicinal Resources Industrialization
    China Pharmaceutical University
    Chinese Academy of Sciences)

  • Terence R. Strick

    (CNRS
    Equipe Labellisée de la Ligue Nationale Contre le Cancer)

  • Shuang Wang

    (Chinese Academy of Sciences
    Songshan Lake Materials Laboratory)

  • Ming Li

    (Chinese Academy of Sciences
    Songshan Lake Materials Laboratory)

Abstract

Factor-dependent termination uses molecular motors to remodel transcription machineries, but the associated mechanisms, especially in eukaryotes, are poorly understood. Here we use single-molecule fluorescence assays to characterize in real time the composition and the catalytic states of Saccharomyces cerevisiae transcription termination complexes remodeled by Sen1 helicase. We confirm that Sen1 takes the RNA transcript as its substrate and translocates along it by hydrolyzing multiple ATPs to form an intermediate with a stalled RNA polymerase II (Pol II) transcription elongation complex (TEC). We show that this intermediate dissociates upon hydrolysis of a single ATP leading to dissociation of Sen1 and RNA, after which Sen1 remains bound to the RNA. We find that Pol II ends up in a variety of states: dissociating from the DNA substrate, which is facilitated by transcription bubble rewinding, being retained to the DNA substrate, or diffusing along the DNA substrate. Our results provide a complete quantitative framework for understanding the mechanism of Sen1-dependent transcription termination in eukaryotes.

Suggested Citation

  • Ying Xiong & Weijing Han & Chunhua Xu & Jing Shi & Lisha Wang & Taoli Jin & Qi Jia & Ying Lu & Shuxin Hu & Shuo-Xing Dou & Wei Lin & Terence R. Strick & Shuang Wang & Ming Li, 2024. "Single-molecule reconstruction of eukaryotic factor-dependent transcription termination," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-49527-z
    DOI: 10.1038/s41467-024-49527-z
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    References listed on IDEAS

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    1. Helen Neil & Christophe Malabat & Yves d’Aubenton-Carafa & Zhenyu Xu & Lars M. Steinmetz & Alain Jacquier, 2009. "Widespread bidirectional promoters are the major source of cryptic transcripts in yeast," Nature, Nature, vol. 457(7232), pages 1038-1042, February.
    2. Timothy T. Harden & Karina S. Herlambang & Mathew Chamberlain & Jean-Benoît Lalanne & Christopher D. Wells & Gene-Wei Li & Robert Landick & Ann Hochschild & Jane Kondev & Jeff Gelles, 2020. "Alternative transcription cycle for bacterial RNA polymerase," Nature Communications, Nature, vol. 11(1), pages 1-11, December.
    3. Jun Fan & Mathieu Leroux-Coyau & Nigel J. Savery & Terence R. Strick, 2016. "Reconstruction of bacterial transcription-coupled repair at single-molecule resolution," Nature, Nature, vol. 536(7615), pages 234-237, August.
    4. Eric A. Galburt & Stephan W. Grill & Anna Wiedmann & Lucyna Lubkowska & Jason Choy & Eva Nogales & Mikhail Kashlev & Carlos Bustamante, 2007. "Backtracking determines the force sensitivity of RNAP II in a factor-dependent manner," Nature, Nature, vol. 446(7137), pages 820-823, April.
    5. S. Wang & Z. Han & D. Libri & O. Porrua & T. R. Strick, 2019. "Single-molecule characterization of extrinsic transcription termination by Sen1 helicase," Nature Communications, Nature, vol. 10(1), pages 1-11, December.
    6. Minkyu Kim & Nevan J. Krogan & Lidia Vasiljeva & Oliver J. Rando & Eduard Nedea & Jack F. Greenblatt & Stephen Buratowski, 2004. "The yeast Rat1 exonuclease promotes transcription termination by RNA polymerase II," Nature, Nature, vol. 432(7016), pages 517-522, November.
    7. Joseph N. Forkey & Margot E. Quinlan & M. Alexander Shaw & John E. T. Corrie & Yale E. Goldman, 2003. "Three-dimensional structural dynamics of myosin V by single-molecule fluorescence polarization," Nature, Nature, vol. 422(6930), pages 399-404, March.
    8. Zhenyu Xu & Wu Wei & Julien Gagneur & Fabiana Perocchi & Sandra Clauder-Münster & Jurgi Camblong & Elisa Guffanti & Françoise Stutz & Wolfgang Huber & Lars M. Steinmetz, 2009. "Bidirectional promoters generate pervasive transcription in yeast," Nature, Nature, vol. 457(7232), pages 1033-1037, February.
    9. Furqan M. Fazal & Cong A. Meng & Kenji Murakami & Roger D. Kornberg & Steven M. Block, 2015. "Real-time observation of the initiation of RNA polymerase II transcription," Nature, Nature, vol. 525(7568), pages 274-277, September.
    10. Sina Ghaemmaghami & Won-Ki Huh & Kiowa Bower & Russell W. Howson & Archana Belle & Noah Dephoure & Erin K. O'Shea & Jonathan S. Weissman, 2003. "Global analysis of protein expression in yeast," Nature, Nature, vol. 425(6959), pages 737-741, October.
    11. Wooyoung Kang & Kook Sun Ha & Heesoo Uhm & Kyuhyong Park & Ja Yil Lee & Sungchul Hohng & Changwon Kang, 2020. "Transcription reinitiation by recycling RNA polymerase that diffuses on DNA after releasing terminated RNA," Nature Communications, Nature, vol. 11(1), pages 1-9, December.
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