IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v12y2021i1d10.1038_s41467-021-26402-9.html
   My bibliography  Save this article

Structural insights into RNA polymerase III-mediated transcription termination through trapping poly-deoxythymidine

Author

Listed:
  • Haifeng Hou

    (Fudan University Shanghai Cancer Center, Institutes of Biomedical Sciences, State Key Laboratory of Genetic Engineering, Shanghai Key Laboratory of Radiation Oncology, and Shanghai Key Laboratory of Medical Epigenetics, Shanghai Medical College of Fudan University)

  • Yan Li

    (Fudan University Shanghai Cancer Center, Institutes of Biomedical Sciences, State Key Laboratory of Genetic Engineering, Shanghai Key Laboratory of Radiation Oncology, and Shanghai Key Laboratory of Medical Epigenetics, Shanghai Medical College of Fudan University)

  • Mo Wang

    (Fudan University Shanghai Cancer Center, Institutes of Biomedical Sciences, State Key Laboratory of Genetic Engineering, Shanghai Key Laboratory of Radiation Oncology, and Shanghai Key Laboratory of Medical Epigenetics, Shanghai Medical College of Fudan University)

  • Aijun Liu

    (Fudan University Shanghai Cancer Center, Institutes of Biomedical Sciences, State Key Laboratory of Genetic Engineering, Shanghai Key Laboratory of Radiation Oncology, and Shanghai Key Laboratory of Medical Epigenetics, Shanghai Medical College of Fudan University)

  • Zishuo Yu

    (Fudan University Shanghai Cancer Center, Institutes of Biomedical Sciences, State Key Laboratory of Genetic Engineering, Shanghai Key Laboratory of Radiation Oncology, and Shanghai Key Laboratory of Medical Epigenetics, Shanghai Medical College of Fudan University)

  • Ke Chen

    (Fudan University Shanghai Cancer Center, Institutes of Biomedical Sciences, State Key Laboratory of Genetic Engineering, Shanghai Key Laboratory of Radiation Oncology, and Shanghai Key Laboratory of Medical Epigenetics, Shanghai Medical College of Fudan University)

  • Dan Zhao

    (Fudan University Shanghai Cancer Center, Institutes of Biomedical Sciences, State Key Laboratory of Genetic Engineering, Shanghai Key Laboratory of Radiation Oncology, and Shanghai Key Laboratory of Medical Epigenetics, Shanghai Medical College of Fudan University)

  • Yanhui Xu

    (Fudan University Shanghai Cancer Center, Institutes of Biomedical Sciences, State Key Laboratory of Genetic Engineering, Shanghai Key Laboratory of Radiation Oncology, and Shanghai Key Laboratory of Medical Epigenetics, Shanghai Medical College of Fudan University
    Shanghai Medical College of Fudan University
    Fudan University
    Inner Mongolia University)

Abstract

Termination of the RNA polymerase III (Pol III)-mediated transcription requires the conversion of an elongation complex (EC) to a pre-termination complex (PTC) on poly-deoxythymidine (dT)-containing non-template strand, a mechanism distinct from Pol I and Pol II. Here, our in vitro transcription elongation assay showed that 5-7 dT-containing DNA template led to transcription termination of Pol III, but not Pol I or Pol II. We assembled human Pol III PTC on a 7 dT-containing DNA template and determined the structure at 3.6 Å resolution. The structure reveals that poly-dT are trapped in a narrow exit tunnel formed by RPC2. A hydrophobic gate of the exit tunnel separates the bases of two connected deoxythymidines and may prevent translocation of the non-template strand. The fork loop 2 stabilizes both template and non-template strands around the transcription fork, and may further prevent strand translocation. Our study shows that the Pol III-specific exit tunnel and FL2 allow for efficient translocation of non-poly-dT sequence during transcription elongation but trap poly-dT to promote DNA retention of Pol III, revealing molecular mechanism of poly-dT-dependent transcription termination of Pol III.

Suggested Citation

  • Haifeng Hou & Yan Li & Mo Wang & Aijun Liu & Zishuo Yu & Ke Chen & Dan Zhao & Yanhui Xu, 2021. "Structural insights into RNA polymerase III-mediated transcription termination through trapping poly-deoxythymidine," Nature Communications, Nature, vol. 12(1), pages 1-11, December.
    • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-26402-9
    DOI: 10.1038/s41467-021-26402-9
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-021-26402-9
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-021-26402-9?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Guillermo Abascal-Palacios & Ewan Phillip Ramsay & Fabienne Beuron & Edward Morris & Alessandro Vannini, 2018. "Structural basis of RNA polymerase III transcription initiation," Nature, Nature, vol. 553(7688), pages 301-306, January.
    2. Carrie Bernecky & Franz Herzog & Wolfgang Baumeister & Jürgen M. Plitzko & Patrick Cramer, 2016. "Structure of transcribing mammalian RNA polymerase II," Nature, Nature, vol. 529(7587), pages 551-554, January.
    3. Niklas A. Hoffmann & Arjen J. Jakobi & María Moreno-Morcillo & Sebastian Glatt & Jan Kosinski & Wim J. H. Hagen & Carsten Sachse & Christoph W. Müller, 2015. "Molecular structures of unbound and transcribing RNA polymerase III," Nature, Nature, vol. 528(7581), pages 231-236, December.
    4. Matthias K. Vorländer & Heena Khatter & Rene Wetzel & Wim J. H. Hagen & Christoph W. Müller, 2018. "Molecular mechanism of promoter opening by RNA polymerase III," Nature, Nature, vol. 553(7688), pages 295-300, January.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Phong Quoc Nguyen & Sonia Huecas & Amna Asif-Laidin & Adrián Plaza-Pegueroles & Beatrice Capuzzi & Noé Palmic & Christine Conesa & Joël Acker & Juan Reguera & Pascale Lesage & Carlos Fernández-Tornero, 2023. "Structural basis of Ty1 integrase tethering to RNA polymerase III for targeted retrotransposon integration," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    2. Saurabh Mishra & Shaina H. Hasan & Rima M. Sakhawala & Shereen Chaudhry & Richard J. Maraia, 2021. "Mechanism of RNA polymerase III termination-associated reinitiation-recycling conferred by the essential function of the N terminal-and-linker domain of the C11 subunit," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    3. Kevin Van Bortle & David P. Marciano & Qing Liu & Tristan Chou & Andrew M. Lipchik & Sanjay Gollapudi & Benjamin S. Geller & Emma Monte & Rohinton T. Kamakaka & Michael P. Snyder, 2022. "A cancer-associated RNA polymerase III identity drives robust transcription and expression of snaR-A noncoding RNA," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    4. Guillermo Abascal-Palacios & Laura Jochem & Carlos Pla-Prats & Fabienne Beuron & Alessandro Vannini, 2021. "Structural basis of Ty3 retrotransposon integration at RNA Polymerase III-transcribed genes," Nature Communications, Nature, vol. 12(1), pages 1-11, December.
    5. Lisa-Marie Appel & Vedran Franke & Melania Bruno & Irina Grishkovskaya & Aiste Kasiliauskaite & Tanja Kaufmann & Ursula E. Schoeberl & Martin G. Puchinger & Sebastian Kostrhon & Carmen Ebenwaldner & M, 2021. "PHF3 regulates neuronal gene expression through the Pol II CTD reader domain SPOC," Nature Communications, Nature, vol. 12(1), pages 1-24, December.
    6. Vladyslava Gorbovytska & Seung-Kyoon Kim & Filiz Kuybu & Michael Götze & Dahun Um & Keunsoo Kang & Andreas Pittroff & Theresia Brennecke & Lisa-Marie Schneider & Alexander Leitner & Tae-Kyung Kim & Cl, 2022. "Enhancer RNAs stimulate Pol II pause release by harnessing multivalent interactions to NELF," Nature Communications, Nature, vol. 13(1), pages 1-22, December.
    7. Joseph G. Beton & Thomas Mulvaney & Tristan Cragnolini & Maya Topf, 2024. "Cryo-EM structure and B-factor refinement with ensemble representation," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    8. Johannes Benedum & Vedran Franke & Lisa-Marie Appel & Lena Walch & Melania Bruno & Rebecca Schneeweiss & Juliane Gruber & Helena Oberndorfer & Emma Frank & Xué Strobl & Anton Polyansky & Bojan Zagrovi, 2023. "The SPOC proteins DIDO3 and PHF3 co-regulate gene expression and neuronal differentiation," Nature Communications, Nature, vol. 14(1), pages 1-20, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-26402-9. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.