IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v16y2025i1d10.1038_s41467-025-65117-z.html
   My bibliography  Save this article

Visualizing influenza A virus assembly by in situ cryo-electron tomography

Author

Listed:
  • Moritz Wachsmuth-Melm

    (Heidelberg University
    Heidelberg University)

  • Sarah Peterl

    (Heidelberg University
    Heidelberg University)

  • Aidan O’Riain

    (Católica Medical School — Universidade Católica Portuguesa)

  • Jana Makroczyová

    (Heidelberg University
    Heidelberg University)

  • Konstantin Fischer

    (Heidelberg University
    Heidelberg University)

  • Tim Krischuns

    (Heidelberg University
    Heidelberg University)

  • Sílvia Vale-Costa

    (Universidade do Porto)

  • Maria João Amorim

    (Católica Medical School — Universidade Católica Portuguesa)

  • Petr Chlanda

    (Heidelberg University
    Heidelberg University)

Abstract

Influenza A virus (IAV) forms pleomorphic particles that package eight ribonucleoprotein complexes (vRNPs), each carrying a distinct RNA genome segment. vRNPs assemble in the nucleus and undergo selective sorting during Rab11a-mediated trafficking to the plasma membrane. Virion assembly is orchestrated by matrix protein 1 (M1), which forms a layer beneath the viral envelope containing hemagglutinin (HA) and neuraminidase (NA). However, molecular details of vRNP distribution, cytosolic trafficking, and coordination of IAV assembly remains unclear. Using in situ cryo-ET, we reveal that HA-containing membranes provide Rab11a-dependent platforms for membrane-assisted vRNP clustering, reducing inter-vRNP distances. In the absence of HA, vRNPs cluster on NA-containing membranes and virus assembly remains intact, indicating that vRNP clustering and trafficking is membrane-assisted but HA independent. The characteristic 7 + 1 vRNP bundle forms concomitantly with budding and is orchestrated by M1 layer assembly that precedes plasma membrane attachment. We further reveal that intracellular M1 forms multilayered helical assemblies of antiparallel dimers, structurally distinct from the M1 layer in virions. These assemblies are compact in the nucleus but partially dissociate in the cytoplasm, likely serving as a reservoir for budding. Together, our findings uncover membrane-assisted vRNP clustering and molecular details of M1 coordinated influenza virus assembly.

Suggested Citation

  • Moritz Wachsmuth-Melm & Sarah Peterl & Aidan O’Riain & Jana Makroczyová & Konstantin Fischer & Tim Krischuns & Sílvia Vale-Costa & Maria João Amorim & Petr Chlanda, 2025. "Visualizing influenza A virus assembly by in situ cryo-electron tomography," Nature Communications, Nature, vol. 16(1), pages 1-15, December.
  • Handle: RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-025-65117-z
    DOI: 10.1038/s41467-025-65117-z
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-025-65117-z
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-025-65117-z?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. Marta Alenquer & Sílvia Vale-Costa & Temitope Akhigbe Etibor & Filipe Ferreira & Ana Laura Sousa & Maria João Amorim, 2019. "Influenza A virus ribonucleoproteins form liquid organelles at endoplasmic reticulum exit sites," Nature Communications, Nature, vol. 10(1), pages 1-19, December.
    2. Amar R. Bhagwat & Valerie Le Sage & Eric Nturibi & Katarzyna Kulej & Jennifer Jones & Min Guo & Eui Tae Kim & Benjamin A. Garcia & Matthew D. Weitzman & Hari Shroff & Seema S. Lakdawala, 2020. "Quantitative live cell imaging reveals influenza virus manipulation of Rab11A transport through reduced dynein association," Nature Communications, Nature, vol. 11(1), pages 1-14, December.
    3. 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.
    4. Julia Peukes & Xiaoli Xiong & Simon Erlendsson & Kun Qu & William Wan & Leslie J. Calder & Oliver Schraidt & Susann Kummer & Stefan M. V. Freund & Hans-Georg Kräusslich & John A. G. Briggs, 2020. "The native structure of the assembled matrix protein 1 of influenza A virus," Nature, Nature, vol. 587(7834), pages 495-498, November.
    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. Lu Xue & Tiancai Chang & Zimu Li & Chenchen Wang & Heyu Zhao & Mei Li & Peng Tang & Xin Wen & Mengmeng Yu & Jiqin Wu & Xichen Bao & Xiaojun Wang & Peng Gong & Jun He & Xinwen Chen & Xiaoli Xiong, 2024. "Cryo-EM structures of Thogoto virus polymerase reveal unique RNA transcription and replication mechanisms among orthomyxoviruses," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    2. Xiaofeng Yan & Shudong Li & Weilin Huang & Hao Wang & Tianfang Zhao & Mingtao Huang & Niyun Zhou & Yuan Shen & Xueming Li, 2025. "MPicker: visualizing and picking membrane proteins for cryo-electron tomography," Nature Communications, Nature, vol. 16(1), pages 1-13, December.
    3. Kang Zhou & Zhu Si & Peng Ge & Jun Tsao & Ming Luo & Z. Hong Zhou, 2022. "Atomic model of vesicular stomatitis virus and mechanism of assembly," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    4. Bryan S. Sibert & Joseph Y. Kim & Jie E. Yang & Zunlong Ke & Christopher C. Stobart & Martin L. Moore & Elizabeth R. Wright, 2024. "Assembly of respiratory syncytial virus matrix protein lattice and its coordination with fusion glycoprotein trimers," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    5. 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.
    6. 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.
    7. Yuen-Yan Chang & Camila Valenzuela & Arthur Lensen & Noelia Lopez-Montero & Saima Sidik & John Salogiannis & Jost Enninga & John Rohde, 2024. "Microtubules provide force to promote membrane uncoating in vacuolar escape for a cyto-invasive bacterial pathogen," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    8. 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.
    9. 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.
    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. 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.

    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:16:y:2025:i:1:d:10.1038_s41467-025-65117-z. 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.