IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-44958-0.html
   My bibliography  Save this article

Proteomic analysis of SARS-CoV-2 particles unveils a key role of G3BP proteins in viral assembly

Author

Listed:
  • Emilie Murigneux

    (Université Paris Cité, CNRS, Inserm, Institut Cochin)

  • Laurent Softic

    (Université Paris Cité, CNRS, Inserm, Institut Cochin)

  • Corentin Aubé

    (Université Paris Cité, CNRS, Inserm, Institut Cochin)

  • Carmen Grandi

    (Radboud University)

  • Delphine Judith

    (Université Paris Cité, CNRS, Inserm, Institut Cochin)

  • Johanna Bruce

    (Proteom’IC facility, Université Paris Cité, CNRS, Inserm, Institut Cochin)

  • Morgane Le Gall

    (Proteom’IC facility, Université Paris Cité, CNRS, Inserm, Institut Cochin)

  • François Guillonneau

    (Proteom’IC facility, Université Paris Cité, CNRS, Inserm, Institut Cochin
    Institut de Cancérologie de l’Ouest (ICO), CRCi2NA-Inserm UMR 1307, CNRS UMR 6075, Nantes Université)

  • Alain Schmitt

    (Université Paris Cité, CNRS, Inserm, Institut Cochin)

  • Vincent Parissi

    (Microbiologie Fondamentale et Pathogénicité Laboratory (MFP), UMR 5234, « Mobility of pathogenic genomes and chromatin dynamics » team (MobilVIR), CNRS-University of Bordeaux, DyNAVIR network)

  • Clarisse Berlioz-Torrent

    (Université Paris Cité, CNRS, Inserm, Institut Cochin)

  • Laurent Meertens

    (Université Paris Cité, Inserm U944, CNRS 7212, Institut de Recherche Saint-Louis, Hôpital Saint-Louis)

  • Maike M. K. Hansen

    (Radboud University)

  • Sarah Gallois-Montbrun

    (Université Paris Cité, CNRS, Inserm, Institut Cochin)

Abstract

Considerable progress has been made in understanding the molecular host-virus battlefield during SARS-CoV-2 infection. Nevertheless, the assembly and egress of newly formed virions are less understood. To identify host proteins involved in viral morphogenesis, we characterize the proteome of SARS-CoV-2 virions produced from A549-ACE2 and Calu-3 cells, isolated via ultracentrifugation on sucrose cushion or by ACE-2 affinity capture. Bioinformatic analysis unveils 92 SARS-CoV-2 virion-associated host factors, providing a valuable resource to better understand the molecular environment of virion production. We reveal that G3BP1 and G3BP2 (G3BP1/2), two major stress granule nucleators, are embedded within virions and unexpectedly favor virion production. Furthermore, we show that G3BP1/2 participate in the formation of cytoplasmic membrane vesicles, that are likely virion assembly sites, consistent with a proviral role of G3BP1/2 in SARS-CoV-2 dissemination. Altogether, these findings provide new insights into host factors required for SARS-CoV-2 assembly with potential implications for future therapeutic targeting.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-44958-0
    DOI: 10.1038/s41467-024-44958-0
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-44958-0
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-44958-0?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. David E. Gordon & Gwendolyn M. Jang & Mehdi Bouhaddou & Jiewei Xu & Kirsten Obernier & Kris M. White & Matthew J. O’Meara & Veronica V. Rezelj & Jeffrey Z. Guo & Danielle L. Swaney & Tia A. Tummino & , 2020. "A SARS-CoV-2 protein interaction map reveals targets for drug repurposing," Nature, Nature, vol. 583(7816), pages 459-468, July.
    2. Thomas Kruse & Caroline Benz & Dimitriya H. Garvanska & Richard Lindqvist & Filip Mihalic & Fabian Coscia & Raviteja Inturi & Ahmed Sayadi & Leandro Simonetti & Emma Nilsson & Muhammad Ali & Johanna K, 2021. "Large scale discovery of coronavirus-host factor protein interaction motifs reveals SARS-CoV-2 specific mechanisms and vulnerabilities," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    3. Shan Lu & Qiaozhen Ye & Digvijay Singh & Yong Cao & Jolene K. Diedrich & John R. Yates & Elizabeth Villa & Don W. Cleveland & Kevin D. Corbett, 2021. "The SARS-CoV-2 nucleocapsid phosphoprotein forms mutually exclusive condensates with RNA and the membrane-associated M protein," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    4. Doyeon Kim & Sukjun Kim & Joori Park & Hee Ryung Chang & Jeeyoon Chang & Junhak Ahn & Heedo Park & Junehee Park & Narae Son & Gihyeon Kang & Jeonghun Kim & Kisoon Kim & Man-Seong Park & Yoon Ki Kim & , 2021. "A high-resolution temporal atlas of the SARS-CoV-2 translatome and transcriptome," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    5. Alexey Stukalov & Virginie Girault & Vincent Grass & Ozge Karayel & Valter Bergant & Christian Urban & Darya A. Haas & Yiqi Huang & Lila Oubraham & Anqi Wang & M. Sabri Hamad & Antonio Piras & Fynn M., 2021. "Multilevel proteomics reveals host perturbations by SARS-CoV-2 and SARS-CoV," Nature, Nature, vol. 594(7862), pages 246-252, June.
    6. 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.
    7. Denisa Bojkova & Kevin Klann & Benjamin Koch & Marek Widera & David Krause & Sandra Ciesek & Jindrich Cinatl & Christian Münch, 2020. "Proteomics of SARS-CoV-2-infected host cells reveals therapy targets," Nature, Nature, vol. 583(7816), pages 469-472, July.
    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. Filip Mihalič & Caroline Benz & Eszter Kassa & Richard Lindqvist & Leandro Simonetti & Raviteja Inturi & Hanna Aronsson & Eva Andersson & Celestine N. Chi & Norman E. Davey & Anna K. Överby & Per Jemt, 2023. "Identification of motif-based interactions between SARS-CoV-2 protein domains and human peptide ligands pinpoint antiviral targets," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    2. Sara Sunshine & Andreas S. Puschnik & Joseph M. Replogle & Matthew T. Laurie & Jamin Liu & Beth Shoshana Zha & James K. Nuñez & Janie R. Byrum & Aidan H. McMorrow & Matthew B. Frieman & Juliane Winkle, 2023. "Systematic functional interrogation of SARS-CoV-2 host factors using Perturb-seq," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    3. Thomas Kruse & Caroline Benz & Dimitriya H. Garvanska & Richard Lindqvist & Filip Mihalic & Fabian Coscia & Raviteja Inturi & Ahmed Sayadi & Leandro Simonetti & Emma Nilsson & Muhammad Ali & Johanna K, 2021. "Large scale discovery of coronavirus-host factor protein interaction motifs reveals SARS-CoV-2 specific mechanisms and vulnerabilities," Nature Communications, Nature, vol. 12(1), pages 1-13, 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. Ma’ayan Israeli & Yaara Finkel & Yfat Yahalom-Ronen & Nir Paran & Theodor Chitlaru & Ofir Israeli & Inbar Cohen-Gihon & Moshe Aftalion & Reut Falach & Shahar Rotem & Uri Elia & Ital Nemet & Limor Klik, 2022. "Genome-wide CRISPR screens identify GATA6 as a proviral host factor for SARS-CoV-2 via modulation of ACE2," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    6. Kelsey M. Haas & Michael J. McGregor & Mehdi Bouhaddou & Benjamin J. Polacco & Eun-Young Kim & Thong T. Nguyen & Billy W. Newton & Matthew Urbanowski & Heejin Kim & Michael A. P. Williams & Veronica V, 2023. "Proteomic and genetic analyses of influenza A viruses identify pan-viral host targets," Nature Communications, Nature, vol. 14(1), pages 1-27, December.
    7. 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.
    8. Andrea Fossati & Deepto Mozumdar & Claire Kokontis & Melissa Mèndez-Moran & Eliza Nieweglowska & Adrian Pelin & Yuping Li & Baron Guo & Nevan J. Krogan & David A. Agard & Joseph Bondy-Denomy & Daniell, 2023. "Next-generation proteomics for quantitative Jumbophage-bacteria interaction mapping," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    9. Taha Y. Taha & Irene P. Chen & Jennifer M. Hayashi & Takako Tabata & Keith Walcott & Gabriella R. Kimmerly & Abdullah M. Syed & Alison Ciling & Rahul K. Suryawanshi & Hannah S. Martin & Bryan H. Bach , 2023. "Rapid assembly of SARS-CoV-2 genomes reveals attenuation of the Omicron BA.1 variant through NSP6," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    10. David Gomez-Zepeda & Danielle Arnold-Schild & Julian Beyrle & Arthur Declercq & Ralf Gabriels & Elena Kumm & Annica Preikschat & Mateusz Krzysztof Łącki & Aurélie Hirschler & Jeewan Babu Rijal & Chris, 2024. "Thunder-DDA-PASEF enables high-coverage immunopeptidomics and is boosted by MS2Rescore with MS2PIP timsTOF fragmentation prediction model," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    11. Christine E. Peters & Ursula Schulze-Gahmen & Manon Eckhardt & Gwendolyn M. Jang & Jiewei Xu & Ernst H. Pulido & Conner Bardine & Charles S. Craik & Melanie Ott & Or Gozani & Kliment A. Verba & Ruth H, 2022. "Structure-function analysis of enterovirus protease 2A in complex with its essential host factor SETD3," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    12. Gabriela Dias Noske & Yun Song & Rafaela Sachetto Fernandes & Rod Chalk & Haitem Elmassoudi & Lizbé Koekemoer & C. David Owen & Tarick J. El-Baba & Carol V. Robinson & Glaucius Oliva & Andre Schutzer , 2023. "An in-solution snapshot of SARS-COV-2 main protease maturation process and inhibition," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    13. 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.
    14. Haofeng Wang & Qi Yang & Xiaoce Liu & Zili Xu & Maolin Shao & Dongxu Li & Yinkai Duan & Jielin Tang & Xianqiang Yu & Yumin Zhang & Aihua Hao & Yajie Wang & Jie Chen & Chenghao Zhu & Luke Guddat & Hong, 2023. "Structure-based discovery of dual pathway inhibitors for SARS-CoV-2 entry," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    15. Xiaopan Gao & Huabin Tian & Kaixiang Zhu & Qing Li & Wei Hao & Linyue Wang & Bo Qin & Hongyu Deng & Sheng Cui, 2022. "Structural basis for Sarbecovirus ORF6 mediated blockage of nucleocytoplasmic transport," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    16. Pawel M. Wydorski & Jerzy Osipiuk & Benjamin T. Lanham & Christine Tesar & Michael Endres & Elizabeth Engle & Robert Jedrzejczak & Vishruth Mullapudi & Karolina Michalska & Krzysztof Fidelis & David F, 2023. "Dual domain recognition determines SARS-CoV-2 PLpro selectivity for human ISG15 and K48-linked di-ubiquitin," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    17. Valter Bergant & Daniel Schnepf & Niklas Andrade Krätzig & Philipp Hubel & Christian Urban & Thomas Engleitner & Ronald Dijkman & Bernhard Ryffel & Katja Steiger & Percy A. Knolle & Georg Kochs & Rola, 2023. "mRNA 3’UTR lengthening by alternative polyadenylation attenuates inflammatory responses and correlates with virulence of Influenza A virus," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    18. Hanbaek Lyu & Yacoub H. Kureh & Joshua Vendrow & Mason A. Porter, 2024. "Learning low-rank latent mesoscale structures in networks," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    19. Charulata Jindal & Sandeep Kumar & Sunil Sharma & Yuk Ming Choi & Jimmy T. Efird, 2020. "The Prevention and Management of COVID-19: Seeking a Practical and Timely Solution," IJERPH, MDPI, vol. 17(11), pages 1-11, June.
    20. Tabea M. Eser & Olga Baranov & Manuel Huth & Mohammed I. M. Ahmed & Flora Deák & Kathrin Held & Luming Lin & Kami Pekayvaz & Alexander Leunig & Leo Nicolai & Georgios Pollakis & Marcus Buggert & David, 2023. "Nucleocapsid-specific T cell responses associate with control of SARS-CoV-2 in the upper airways before seroconversion," Nature Communications, Nature, vol. 14(1), pages 1-13, 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_s41467-024-44958-0. 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.