IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-33483-7.html
   My bibliography  Save this article

Membrane-assisted assembly and selective secretory autophagy of enteroviruses

Author

Listed:
  • Selma Dahmane

    (Umeå University
    Umeå University
    Umeå University)

  • Adeline Kerviel

    (National Institutes of Health)

  • Dustin R. Morado

    (Stockholm University)

  • Kasturika Shankar

    (Umeå University
    Umeå University
    Umeå University)

  • Björn Ahlman

    (Umeå University
    Umeå University
    Umeå University)

  • Michael Lazarou

    (Monash University)

  • Nihal Altan-Bonnet

    (National Institutes of Health)

  • Lars-Anders Carlson

    (Umeå University
    Umeå University
    Umeå University)

Abstract

Enteroviruses are non-enveloped positive-sense RNA viruses that cause diverse diseases in humans. Their rapid multiplication depends on remodeling of cytoplasmic membranes for viral genome replication. It is unknown how virions assemble around these newly synthesized genomes and how they are then loaded into autophagic membranes for release through secretory autophagy. Here, we use cryo-electron tomography of infected cells to show that poliovirus assembles directly on replication membranes. Pharmacological untethering of capsids from membranes abrogates RNA encapsidation. Our data directly visualize a membrane-bound half-capsid as a prominent virion assembly intermediate. Assembly progression past this intermediate depends on the class III phosphatidylinositol 3-kinase VPS34, a key host-cell autophagy factor. On the other hand, the canonical autophagy initiator ULK1 is shown to restrict virion production since its inhibition leads to increased accumulation of virions in vast intracellular arrays, followed by an increased vesicular release at later time points. Finally, we identify multiple layers of selectivity in virus-induced autophagy, with a strong selection for RNA-loaded virions over empty capsids and the segregation of virions from other types of autophagosome contents. These findings provide an integrated structural framework for multiple stages of the poliovirus life cycle.

Suggested Citation

  • Selma Dahmane & Adeline Kerviel & Dustin R. Morado & Kasturika Shankar & Björn Ahlman & Michael Lazarou & Nihal Altan-Bonnet & Lars-Anders Carlson, 2022. "Membrane-assisted assembly and selective secretory autophagy of enteroviruses," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-33483-7
    DOI: 10.1038/s41467-022-33483-7
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-33483-7
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-022-33483-7?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. Zongdi Feng & Lucinda Hensley & Kevin L. McKnight & Fengyu Hu & Victoria Madden & LiFang Ping & Sook-Hyang Jeong & Christopher Walker & Robert E. Lanford & Stanley M. Lemon, 2013. "A pathogenic picornavirus acquires an envelope by hijacking cellular membranes," Nature, Nature, vol. 496(7445), pages 367-371, April.
    2. Ling Zhu & Yao Sun & Jinyan Fan & Bin Zhu & Lei Cao & Qiang Gao & Yanjun Zhang & Hongrong Liu & Zihe Rao & Xiangxi Wang, 2018. "Structures of Coxsackievirus A10 unveil the molecular mechanisms of receptor binding and viral uncoating," Nature Communications, Nature, vol. 9(1), pages 1-9, December.
    3. Steffen Klein & Mirko Cortese & Sophie L. Winter & Moritz Wachsmuth-Melm & Christopher J. Neufeldt & Berati Cerikan & Megan L. Stanifer & Steeve Boulant & Ralf Bartenschlager & Petr Chlanda, 2020. "SARS-CoV-2 structure and replication characterized by in situ cryo-electron tomography," Nature Communications, Nature, vol. 11(1), pages 1-10, December.
    4. William Wan & Larissa Kolesnikova & Mairi Clarke & Alexander Koehler & Takeshi Noda & Stephan Becker & John A. G. Briggs, 2017. "Structure and assembly of the Ebola virus nucleocapsid," Nature, Nature, vol. 551(7680), pages 394-397, November.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Liv Zimmermann & Xiaohan Zhao & Jana Makroczyova & Moritz Wachsmuth-Melm & Vibhu Prasad & Zach Hensel & Ralf Bartenschlager & Petr Chlanda, 2023. "SARS-CoV-2 nsp3 and nsp4 are minimal constituents of a pore spanning replication organelle," Nature Communications, Nature, vol. 14(1), pages 1-12, December.

    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. Scotland E. Farley & Jennifer E. Kyle & Hans C. Leier & Lisa M. Bramer & Jules B. Weinstein & Timothy A. Bates & Joon-Yong Lee & Thomas O. Metz & Carsten Schultz & Fikadu G. Tafesse, 2022. "A global lipid map reveals host dependency factors conserved across SARS-CoV-2 variants," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    2. Katelyn C. Cook & Elene Tsopurashvili & Jason M. Needham & Sunnie R. Thompson & Ileana M. Cristea, 2022. "Restructured membrane contacts rewire organelles for human cytomegalovirus infection," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    3. Lorène Gonnin & Ambroise Desfosses & Maria Bacia-Verloop & Didier Chevret & Marie Galloux & Jean-François Éléouët & Irina Gutsche, 2023. "Structural landscape of the respiratory syncytial virus nucleocapsids," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    4. Filip Mihalič & Leandro Simonetti & Girolamo Giudice & Marie Rubin Sander & Richard Lindqvist & Marie Berit Akpiroro Peters & Caroline Benz & Eszter Kassa & Dilip Badgujar & Raviteja Inturi & Muhammad, 2023. "Large-scale phage-based screening reveals extensive pan-viral mimicry of host short linear motifs," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    5. Patrick C. Hoffmann & Jan Philipp Kreysing & Iskander Khusainov & Maarten W. Tuijtel & Sonja Welsch & Martin Beck, 2022. "Structures of the eukaryotic ribosome and its translational states in situ," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    6. Susanne G. Grein & Kyra A. Y. Defourny & Huib H. Rabouw & Soenita S. Goerdayal & Martijn J. C. Herwijnen & Richard W. Wubbolts & Maarten Altelaar & Frank J. M. Kuppeveld & Esther N. M. Nolte-‘t Hoen, 2022. "The encephalomyocarditis virus Leader promotes the release of virions inside extracellular vesicles via the induction of secretory autophagy," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    7. Emilie Murigneux & Laurent Softic & Corentin Aubé & Carmen Grandi & Delphine Judith & Johanna Bruce & Morgane Le Gall & François Guillonneau & Alain Schmitt & Vincent Parissi & Clarisse Berlioz-Torren, 2024. "Proteomic analysis of SARS-CoV-2 particles unveils a key role of G3BP proteins in viral assembly," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    8. Liv Zimmermann & Xiaohan Zhao & Jana Makroczyova & Moritz Wachsmuth-Melm & Vibhu Prasad & Zach Hensel & Ralf Bartenschlager & Petr Chlanda, 2023. "SARS-CoV-2 nsp3 and nsp4 are minimal constituents of a pore spanning replication organelle," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    9. Keisuke Tabata & Vibhu Prasad & David Paul & Ji-Young Lee & Minh-Tu Pham & Woan-Ing Twu & Christopher J. Neufeldt & Mirko Cortese & Berati Cerikan & Yannick Stahl & Sebastian Joecks & Cong Si Tran & C, 2021. "Convergent use of phosphatidic acid for hepatitis C virus and SARS-CoV-2 replication organelle formation," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    10. Marion Jasnin & Jordan Hervy & Stéphanie Balor & Anaïs Bouissou & Amsha Proag & Raphaël Voituriez & Jonathan Schneider & Thomas Mangeat & Isabelle Maridonneau-Parini & Wolfgang Baumeister & Serge Dmit, 2022. "Elasticity of podosome actin networks produces nanonewton protrusive forces," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    11. Sara Pfister & Julius Rabl & Thomas Wiegand & Simone Mattei & Alexander A. Malär & Lauriane Lecoq & Stefan Seitz & Ralf Bartenschlager & Anja Böckmann & Michael Nassal & Daniel Boehringer & Beat H. Me, 2023. "Structural conservation of HBV-like capsid proteins over hundreds of millions of years despite the shift from non-enveloped to enveloped life-style," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    12. Andreia L. Pinto & Ranjit K. Rai & Jonathan C. Brown & Paul Griffin & James R. Edgar & Anand Shah & Aran Singanayagam & Claire Hogg & Wendy S. Barclay & Clare E. Futter & Thomas Burgoyne, 2022. "Ultrastructural insight into SARS-CoV-2 entry and budding in human airway epithelium," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    13. Francisco S. Mesquita & Laurence Abrami & Lucie Bracq & Nattawadee Panyain & Vincent Mercier & Béatrice Kunz & Audrey Chuat & Joana Carlevaro-Fita & Didier Trono & F. Gisou van der Goot, 2023. "SARS-CoV-2 hijacks a cell damage response, which induces transcription of a more efficient Spike S-acyltransferase," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    14. P. J. Schubert & R. Saxena & J. Kornfeld, 2024. "DeepFocus: fast focus and astigmatism correction for electron microscopy," Nature Communications, Nature, vol. 15(1), pages 1-10, December.
    15. Leonid Andronov & Mengting Han & Yanyu Zhu & Ashwin Balaji & Anish R. Roy & Andrew E. S. Barentine & Puja Patel & Jaishree Garhyan & Lei S. Qi & W. E. Moerner, 2024. "Nanoscale cellular organization of viral RNA and proteins in SARS-CoV-2 replication organelles," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    16. Yoko Fujita-Fujiharu & Yukihiko Sugita & Yuki Takamatsu & Kazuya Houri & Manabu Igarashi & Yukiko Muramoto & Masahiro Nakano & Yugo Tsunoda & Ichiro Taniguchi & Stephan Becker & Takeshi Noda, 2022. "Structural insight into Marburg virus nucleoprotein–RNA complex formation," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    17. Sergio Cruz-León & Tomáš Majtner & Patrick C. Hoffmann & Jan Philipp Kreysing & Sebastian Kehl & Maarten W. Tuijtel & Stefan L. Schaefer & Katharina Geißler & Martin Beck & Beata Turoňová & Gerhard Hu, 2024. "High-confidence 3D template matching for cryo-electron tomography," Nature Communications, Nature, vol. 15(1), pages 1-14, 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:13:y:2022:i:1:d:10.1038_s41467-022-33483-7. 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.