IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-45205-2.html
   My bibliography  Save this article

The host RNA polymerase II C-terminal domain is the anchor for replication of the influenza virus genome

Author

Listed:
  • Tim Krischuns

    (Université Paris Cité, CNRS UMR 3569, RNA Biology of Influenza Virus)

  • Benoît Arragain

    (European Molecular Biology Laboratory)

  • Catherine Isel

    (Université Paris Cité, CNRS UMR 3569, RNA Biology of Influenza Virus)

  • Sylvain Paisant

    (Université Paris Cité, CNRS UMR 3569, RNA Biology of Influenza Virus)

  • Matthias Budt

    (Robert Koch Institut)

  • Thorsten Wolff

    (Robert Koch Institut)

  • Stephen Cusack

    (European Molecular Biology Laboratory)

  • Nadia Naffakh

    (Université Paris Cité, CNRS UMR 3569, RNA Biology of Influenza Virus)

Abstract

The current model is that the influenza virus polymerase (FluPol) binds either to host RNA polymerase II (RNAP II) or to the acidic nuclear phosphoprotein 32 (ANP32), which drives its conformation and activity towards transcription or replication of the viral genome, respectively. Here, we provide evidence that the FluPol-RNAP II binding interface, beyond its well-acknowledged function in cap-snatching during transcription initiation, has also a pivotal role in replication of the viral genome. Using a combination of cell-based and in vitro approaches, we show that the RNAP II C-terminal-domain, jointly with ANP32, enhances FluPol replication activity. We observe successive conformational changes to switch from a transcriptase to a replicase conformation in the presence of the bound RNPAII C-terminal domain and propose a model in which the host RNAP II is the anchor for transcription and replication of the viral genome. Our data open new perspectives on the spatial coupling of viral transcription and replication and the coordinated balance between these two activities.

Suggested Citation

  • Tim Krischuns & Benoît Arragain & Catherine Isel & Sylvain Paisant & Matthias Budt & Thorsten Wolff & Stephen Cusack & Nadia Naffakh, 2024. "The host RNA polymerase II C-terminal domain is the anchor for replication of the influenza virus genome," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-45205-2
    DOI: 10.1038/s41467-024-45205-2
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-45205-2
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-45205-2?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. Carol M. Sheppard & Daniel H. Goldhill & Olivia C. Swann & Ecco Staller & Rebecca Penn & Olivia K. Platt & Ksenia Sukhova & Laury Baillon & Rebecca Frise & Thomas P. Peacock & Ervin Fodor & Wendy S. B, 2023. "An Influenza A virus can evolve to use human ANP32E through altering polymerase dimerization," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    2. Haitian Fan & Alexander P. Walker & Loïc Carrique & Jeremy R. Keown & Itziar Serna Martin & Dimple Karia & Jane Sharps & Narin Hengrung & Els Pardon & Jan Steyaert & Jonathan M. Grimes & Ervin Fodor, 2019. "Structures of influenza A virus RNA polymerase offer insight into viral genome replication," Nature, Nature, vol. 573(7773), pages 287-290, September.
    3. Jeremy R. Keown & Zihan Zhu & Loïc Carrique & Haitian Fan & Alexander P. Walker & Itziar Serna Martin & Els Pardon & Jan Steyaert & Ervin Fodor & Jonathan M. Grimes, 2022. "Mapping inhibitory sites on the RNA polymerase of the 1918 pandemic influenza virus using nanobodies," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    4. Patrick Cramer, 2019. "Organization and regulation of gene transcription," Nature, Nature, vol. 573(7772), pages 45-54, September.
    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. Baolei Yuan & Xuan Zhou & Keiichiro Suzuki & Gerardo Ramos-Mandujano & Mengge Wang & Muhammad Tehseen & Lorena V. Cortés-Medina & James J. Moresco & Sarah Dunn & Reyna Hernandez-Benitez & Tomoaki Hish, 2022. "Wiskott-Aldrich syndrome protein forms nuclear condensates and regulates alternative splicing," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    2. Mitsuaki Fujimoto & Ryosuke Takii & Masaki Matsumoto & Mariko Okada & Keiich I. Nakayama & Ryuichiro Nakato & Katsunori Fujiki & Katsuhiko Shirahige & Akira Nakai, 2022. "HSF1 phosphorylation establishes an active chromatin state via the TRRAP–TIP60 complex and promotes tumorigenesis," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    3. Hiroaki Ohishi & Seiru Shimada & Satoshi Uchino & Jieru Li & Yuko Sato & Manabu Shintani & Hitoshi Owada & Yasuyuki Ohkawa & Alexandros Pertsinidis & Takashi Yamamoto & Hiroshi Kimura & Hiroshi Ochiai, 2022. "STREAMING-tag system reveals spatiotemporal relationships between transcriptional regulatory factors and transcriptional activity," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    4. Marta Vicioso-Mantis & Raquel Fueyo & Claudia Navarro & Sara Cruz-Molina & Wilfred F. J. Ijcken & Elena Rebollo & Álvaro Rada-Iglesias & Marian A. Martínez-Balbás, 2022. "JMJD3 intrinsically disordered region links the 3D-genome structure to TGFβ-dependent transcription activation," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    5. Carol M. Sheppard & Daniel H. Goldhill & Olivia C. Swann & Ecco Staller & Rebecca Penn & Olivia K. Platt & Ksenia Sukhova & Laury Baillon & Rebecca Frise & Thomas P. Peacock & Ervin Fodor & Wendy S. B, 2023. "An Influenza A virus can evolve to use human ANP32E through altering polymerase dimerization," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    6. Claire Marchal & Nivedita Singh & Zachary Batz & Jayshree Advani & Catherine Jaeger & Ximena Corso-Díaz & Anand Swaroop, 2022. "High-resolution genome topology of human retina uncovers super enhancer-promoter interactions at tissue-specific and multifactorial disease loci," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    7. David Flores-Solis & Irina P. Lushpinskaia & Anton A. Polyansky & Arya Changiarath & Marc Boehning & Milana Mirkovic & James Walshe & Lisa M. Pietrek & Patrick Cramer & Lukas S. Stelzl & Bojan Zagrovi, 2023. "Driving forces behind phase separation of the carboxy-terminal domain of RNA polymerase II," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    8. Tomas Kouba & Dominik Vogel & Sigurdur R. Thorkelsson & Emmanuelle R. J. Quemin & Harry M. Williams & Morlin Milewski & Carola Busch & Stephan Günther & Kay Grünewald & Maria Rosenthal & Stephen Cusac, 2021. "Conformational changes in Lassa virus L protein associated with promoter binding and RNA synthesis activity," Nature Communications, Nature, vol. 12(1), pages 1-18, December.
    9. 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.
    10. Ecco Staller & Loïc Carrique & Olivia C. Swann & Haitian Fan & Jeremy R. Keown & Carol M. Sheppard & Wendy S. Barclay & Jonathan M. Grimes & Ervin Fodor, 2024. "Structures of H5N1 influenza polymerase with ANP32B reveal mechanisms of genome replication and host adaptation," Nature Communications, Nature, vol. 15(1), pages 1-10, December.
    11. Chun-Yi Cho & Patrick H. O’Farrell, 2023. "Stepwise modifications of transcriptional hubs link pioneer factor activity to a burst of transcription," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    12. Alewo Idoko-Akoh & Daniel H. Goldhill & Carol M. Sheppard & Dagmara Bialy & Jessica L. Quantrill & Ksenia Sukhova & Jonathan C. Brown & Samuel Richardson & Ciara Campbell & Lorna Taylor & Adrian Sherm, 2023. "Creating resistance to avian influenza infection through genome editing of the ANP32 gene family," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    13. Jin Xie & Mohamed Ouizougun-Oubari & Li Wang & Guanglei Zhai & Daitze Wu & Zhaohu Lin & Manfu Wang & Barbara Ludeke & Xiaodong Yan & Tobias Nilsson & Lu Gao & Xinyi Huang & Rachel Fearns & Shuai Chen, 2024. "Structural basis for dimerization of a paramyxovirus polymerase complex," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    14. Michael DeBerardine & Gregory T. Booth & Philip P. Versluis & John T. Lis, 2023. "The NELF pausing checkpoint mediates the functional divergence of Cdk9," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    15. Shurong Liu & Junhong Huang & Jie Zhou & Siyan Chen & Wujian Zheng & Chang Liu & Qiao Lin & Ping Zhang & Di Wu & Simeng He & Jiayi Ye & Shun Liu & Keren Zhou & Bin Li & Lianghu Qu & Jianhua Yang, 2024. "NAP-seq reveals multiple classes of structured noncoding RNAs with regulatory functions," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    16. Qiaoqiao Zhang & Kai Deng & Mengyou Liu & Shengye Yang & Wei Xu & Tong Feng & Minwen Jie & Zhiming Liu & Xiao Sheng & Haiyang Chen & Hao Jiang, 2023. "Phase separation of BuGZ regulates gut regeneration and aging through interaction with m6A regulators," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    17. Lijing Yang & Lei Tu & Shilpa Bisht & Yiqing Mao & Daniel Petkovich & Sara-Jayne Thursby & Jinxiao Liang & Nibedita Patel & Ray-Whay Chiu Yen & Tina Largent & Cynthia Zahnow & Malcolm Brock & Kathy Ga, 2024. "Tissue-location-specific transcription programs drive tumor dependencies in colon cancer," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    18. Tuan Nguyen & Sai Li & Jeremy T-H Chang & John W. Watters & Htet Ng & Adewola Osunsade & Yael David & Shixin Liu, 2022. "Chromatin sequesters pioneer transcription factor Sox2 from exerting force on DNA," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    19. Nathaniel G. Jones & Vincent Geoghegan & Gareth Moore & Juliana B. T. Carnielli & Katherine Newling & Félix Calderón & Raquel Gabarró & Julio Martín & Rab K. Prinjha & Inmaculada Rioja & Anthony J. Wi, 2022. "Bromodomain factor 5 is an essential regulator of transcription in Leishmania," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    20. Hui Wang & Boyuan Li & Linyu Zuo & Bo Wang & Yan Yan & Kai Tian & Rong Zhou & Chenlu Wang & Xizi Chen & Yongpeng Jiang & Haonan Zheng & Fangfei Qin & Bin Zhang & Yang Yu & Chao-Pei Liu & Yanhui Xu & J, 2022. "The transcriptional coactivator RUVBL2 regulates Pol II clustering with diverse transcription factors," Nature Communications, Nature, vol. 13(1), pages 1-26, 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_s41467-024-45205-2. 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.