IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-52891-5.html
   My bibliography  Save this article

Mycobacterial HelD connects RNA polymerase recycling with transcription initiation

Author

Listed:
  • Tomáš Kovaľ

    (Institute of Biotechnology of the Czech Academy of Sciences)

  • Nabajyoti Borah

    (Institute of Microbiology of the Czech Academy of Sciences
    Charles University)

  • Petra Sudzinová

    (Institute of Microbiology of the Czech Academy of Sciences)

  • Barbora Brezovská

    (Institute of Microbiology of the Czech Academy of Sciences)

  • Hana Šanderová

    (Institute of Microbiology of the Czech Academy of Sciences)

  • Viola Vaňková Hausnerová

    (Institute of Microbiology of the Czech Academy of Sciences
    Charles University)

  • Alena Křenková

    (Institute of Organic Chemistry and Biochemistry of the Czech Academy of Sciences)

  • Martin Hubálek

    (Institute of Organic Chemistry and Biochemistry of the Czech Academy of Sciences)

  • Mária Trundová

    (Institute of Biotechnology of the Czech Academy of Sciences)

  • Kristýna Adámková

    (Institute of Biotechnology of the Czech Academy of Sciences)

  • Jarmila Dušková

    (Institute of Biotechnology of the Czech Academy of Sciences)

  • Marek Schwarz

    (Institute of Microbiology of the Czech Academy of Sciences)

  • Jana Wiedermannová

    (Institute of Microbiology of the Czech Academy of Sciences)

  • Jan Dohnálek

    (Institute of Biotechnology of the Czech Academy of Sciences)

  • Libor Krásný

    (Institute of Microbiology of the Czech Academy of Sciences)

  • Tomáš Kouba

    (Institute of Organic Chemistry and Biochemistry of the Czech Academy of Sciences)

Abstract

Mycobacterial HelD is a transcription factor that recycles stalled RNAP by dissociating it from nucleic acids and, if present, from the antibiotic rifampicin. The rescued RNAP, however, must disengage from HelD to participate in subsequent rounds of transcription. The mechanism of release is unknown. We show that HelD from Mycobacterium smegmatis forms a complex with RNAP associated with the primary sigma factor σA and transcription factor RbpA but not CarD. We solve several structures of RNAP-σA-RbpA-HelD without and with promoter DNA. These snapshots capture HelD during transcription initiation, describing mechanistic aspects of HelD release from RNAP and its protective effect against rifampicin. Biochemical evidence supports these findings, defines the role of ATP binding and hydrolysis by HelD in the process, and confirms the rifampicin-protective effect of HelD. Collectively, these results show that when HelD is present during transcription initiation, the process is protected from rifampicin until the last possible moment.

Suggested Citation

  • Tomáš Kovaľ & Nabajyoti Borah & Petra Sudzinová & Barbora Brezovská & Hana Šanderová & Viola Vaňková Hausnerová & Alena Křenková & Martin Hubálek & Mária Trundová & Kristýna Adámková & Jarmila Dušková, 2024. "Mycobacterial HelD connects RNA polymerase recycling with transcription initiation," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-52891-5
    DOI: 10.1038/s41467-024-52891-5
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-52891-5
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-52891-5?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. Dingwei He & Linlin You & Xiaoxian Wu & Jing Shi & Aijia Wen & Zhi Yan & Wenhui Mu & Chengli Fang & Yu Feng & Yu Zhang, 2022. "Pseudomonas aeruginosa SutA wedges RNAP lobe domain open to facilitate promoter DNA unwinding," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    2. Elizabeth A. Hubin & Mirjana Lilic & Seth A. Darst & Elizabeth A. Campbell, 2017. "Structural insights into the mycobacteria transcription initiation complex from analysis of X-ray crystal structures," Nature Communications, Nature, vol. 8(1), pages 1-12, December.
    3. Katerina Naydenova & Christopher J. Russo, 2017. "Measuring the effects of particle orientation to improve the efficiency of electron cryomicroscopy," Nature Communications, Nature, vol. 8(1), pages 1-5, December.
    4. Timothy P. Newing & Aaron J. Oakley & Michael Miller & Catherine J. Dawson & Simon H. J. Brown & James C. Bouwer & Gökhan Tolun & Peter J. Lewis, 2020. "Molecular basis for RNA polymerase-dependent transcription complex recycling by the helicase-like motor protein HelD," Nature Communications, Nature, vol. 11(1), pages 1-11, December.
    5. Hande Boyaci & James Chen & Rolf Jansen & Seth A. Darst & Elizabeth A. Campbell, 2019. "Structures of an RNA polymerase promoter melting intermediate elucidate DNA unwinding," Nature, Nature, vol. 565(7739), pages 382-385, January.
    6. Tristan Bepler & Kotaro Kelley & Alex J. Noble & Bonnie Berger, 2020. "Topaz-Denoise: general deep denoising models for cryoEM and cryoET," Nature Communications, Nature, vol. 11(1), pages 1-12, December.
    7. Zakia Morichaud & Stefano Trapani & Rishi K. Vishwakarma & Laurent Chaloin & Corinne Lionne & Joséphine Lai-Kee-Him & Patrick Bron & Konstantin Brodolin, 2023. "Structural basis of the mycobacterial stress-response RNA polymerase auto-inhibition via oligomerization," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    8. Yeonoh Shin & M. Zuhaib Qayyum & Danil Pupov & Daria Esyunina & Andrey Kulbachinskiy & Katsuhiko S. Murakami, 2021. "Structural basis of ribosomal RNA transcription regulation," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    9. Tomáš Kouba & Tomáš Koval’ & Petra Sudzinová & Jiří Pospíšil & Barbora Brezovská & Jarmila Hnilicová & Hana Šanderová & Martina Janoušková & Michaela Šiková & Petr Halada & Michal Sýkora & Ivan Barvík, 2020. "Mycobacterial HelD is a nucleic acids-clearing factor for RNA polymerase," Nature Communications, Nature, vol. 11(1), pages 1-13, December.
    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. Linggang Yuan & Qingyang Liu & Liqiao Xu & Bing Wu & Yu Feng, 2024. "Structural basis of promoter recognition by Staphylococcus aureus RNA polymerase," Nature Communications, Nature, vol. 15(1), pages 1-9, December.
    2. Jie Li & Haonan Zhang & Dongyu Li & Ya-Jun Liu & Edward A. Bayer & Qiu Cui & Yingang Feng & Ping Zhu, 2023. "Structure of the transcription open complex of distinct σI factors," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    3. Dingwei He & Linlin You & Xiaoxian Wu & Jing Shi & Aijia Wen & Zhi Yan & Wenhui Mu & Chengli Fang & Yu Feng & Yu Zhang, 2022. "Pseudomonas aeruginosa SutA wedges RNAP lobe domain open to facilitate promoter DNA unwinding," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    4. Rhianna J. Rowland & Svitlana Korolchuk & Marco Salamina & Natalie J. Tatum & James R. Ault & Sam Hart & Johan P. Turkenburg & James N. Blaza & Martin E. M. Noble & Jane A. Endicott, 2024. "Cryo-EM structure of the CDK2-cyclin A-CDC25A complex," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    5. Hongcheng Fan & Bo Wang & Yan Zhang & Yun Zhu & Bo Song & Haijin Xu & Yujia Zhai & Mingqiang Qiao & Fei Sun, 2021. "A cryo-electron microscopy support film formed by 2D crystals of hydrophobin HFBI," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    6. Radostin Danev & Matthew Belousoff & Yi-Lynn Liang & Xin Zhang & Fabian Eisenstein & Denise Wootten & Patrick M. Sexton, 2021. "Routine sub-2.5 Å cryo-EM structure determination of GPCRs," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
    7. Yun-Tao Liu & Heng Zhang & Hui Wang & Chang-Lu Tao & Guo-Qiang Bi & Z. Hong Zhou, 2022. "Isotropic reconstruction for electron tomography with deep learning," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    8. Jin Qian & Bing Wang & Irina Artsimovitch & David Dunlap & Laura Finzi, 2024. "Force and the α-C-terminal domains bias RNA polymerase recycling," Nature Communications, Nature, vol. 15(1), pages 1-10, December.
    9. Xinyu Zhang & Tianfang Zhao & Jiansheng Chen & Yuan Shen & Xueming Li, 2022. "EPicker is an exemplar-based continual learning approach for knowledge accumulation in cryoEM particle picking," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    10. Tongtong Wang & Guang-Lei Wang & Ying Fang & Yi Zhang & Wenxin Peng & Yue Zhou & Aihong Zhang & Long-Jiang Yu & Congming Lu, 2024. "Architecture of the spinach plastid-encoded RNA polymerase," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    11. Erumbi S. Rangarajan & Julian L. Bois & Scott B. Hansen & Tina Izard, 2024. "High-resolution snapshots of the talin auto-inhibitory states suggest roles in cell adhesion and signaling," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    12. Fred E. Fregoso & Malgorzata Boczkowska & Grzegorz Rebowski & Peter J. Carman & Trevor Eeuwen & Roberto Dominguez, 2023. "Mechanism of synergistic activation of Arp2/3 complex by cortactin and WASP-family proteins," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    13. Simon Wiedemann & Reinhard Heckel, 2024. "A deep learning method for simultaneous denoising and missing wedge reconstruction in cryogenic electron tomography," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    14. Qiansheng Liang & Gamma Chi & Leonardo Cirqueira & Lianteng Zhi & Agostino Marasco & Nadia Pilati & Martin J. Gunthorpe & Giuseppe Alvaro & Charles H. Large & David B. Sauer & Werner Treptow & Manuel , 2024. "The binding and mechanism of a positive allosteric modulator of Kv3 channels," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    15. Anjie Li & Tingting You & Xiaojie Pang & Yidi Wang & Lijin Tian & Xiaobo Li & Zhenfeng Liu, 2024. "Structural basis for an early stage of the photosystem II repair cycle in Chlamydomonas reinhardtii," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    16. Luka Bacic & Guillaume Gaullier & Jugal Mohapatra & Guanzhong Mao & Klaus Brackmann & Mikhail Panfilov & Glen Liszczak & Anton Sabantsev & Sebastian Deindl, 2024. "Asymmetric nucleosome PARylation at DNA breaks mediates directional nucleosome sliding by ALC1," Nature Communications, Nature, vol. 15(1), pages 1-10, December.
    17. Yaejin Yun & Hyeongseop Jeong & Thibaut Laboute & Kirill A. Martemyanov & Hyung Ho Lee, 2024. "Cryo-EM structure of human class C orphan GPCR GPR179 involved in visual processing," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    18. Jianping Li & Yan Li & Akiko Koide & Huihui Kuang & Victor J. Torres & Shohei Koide & Da-Neng Wang & Nathaniel J. Traaseth, 2024. "Proton-coupled transport mechanism of the efflux pump NorA," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    19. Leishu Lin & Jiayuan Dong & Shun Xu & Jinman Xiao & Cong Yu & Fengfeng Niu & Zhiyi Wei, 2024. "Autoinhibition and relief mechanisms for MICAL monooxygenases in F-actin disassembly," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    20. Sriram Aiyer & Philip R. Baldwin & Shi Min Tan & Zelin Shan & Juntaek Oh & Atousa Mehrani & Marianne E. Bowman & Gordon Louie & Dario Oliveira Passos & Selena Đorđević-Marquardt & Mario Mietzsch & Jos, 2024. "Overcoming resolution attenuation during tilted cryo-EM data collection," Nature Communications, Nature, vol. 15(1), pages 1-19, 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:15:y:2024:i:1:d:10.1038_s41467-024-52891-5. 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.