IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-50162-x.html
   My bibliography  Save this article

Assembly of respiratory syncytial virus matrix protein lattice and its coordination with fusion glycoprotein trimers

Author

Listed:
  • Bryan S. Sibert

    (University of Wisconsin
    University of Wisconsin
    University of Wisconsin)

  • Joseph Y. Kim

    (University of Wisconsin
    University of Wisconsin)

  • Jie E. Yang

    (University of Wisconsin
    University of Wisconsin
    University of Wisconsin)

  • Zunlong Ke

    (University of Texas at Austin)

  • Christopher C. Stobart

    (Butler University)

  • Martin L. Moore

    (Inc.)

  • Elizabeth R. Wright

    (University of Wisconsin
    University of Wisconsin
    University of Wisconsin
    Morgridge Institute for Research)

Abstract

Respiratory syncytial virus (RSV) is an enveloped, filamentous, negative-strand RNA virus that causes significant respiratory illness worldwide. RSV vaccines are available, however there is still significant need for research to support the development of vaccines and therapeutics against RSV and related Mononegavirales viruses. Individual virions vary in size, with an average diameter of ~130 nm and ranging from ~500 nm to over 10 µm in length. Though the general arrangement of structural proteins in virions is known, we use cryo-electron tomography and sub-tomogram averaging to determine the molecular organization of RSV structural proteins. We show that the peripheral membrane-associated RSV matrix (M) protein is arranged in a packed helical-like lattice of M-dimers. We report that RSV F glycoprotein is frequently observed as pairs of trimers oriented in an anti-parallel conformation to support potential interactions between trimers. Our sub-tomogram averages indicate the positioning of F-trimer pairs is correlated with the underlying M lattice. These results provide insight into RSV virion organization and may aid in the development of RSV vaccines and anti-viral targets.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-50162-x
    DOI: 10.1038/s41467-024-50162-x
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-50162-x
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-50162-x?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. 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.
    2. 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.
    3. Vincent Rincheval & Mickael Lelek & Elyanne Gault & Camille Bouillier & Delphine Sitterlin & Sabine Blouquit-Laye & Marie Galloux & Christophe Zimmer & Jean-François Eleouet & Marie-Anne Rameix-Welti, 2017. "Functional organization of cytoplasmic inclusion bodies in cells infected by respiratory syncytial virus," Nature Communications, Nature, vol. 8(1), pages 1-11, December.
    4. Daiyin Tian & Michael B. Battles & Syed M. Moin & Man Chen & Kayvon Modjarrad & Azad Kumar & Masaru Kanekiyo & Kevin W. Graepel & Noor M. Taher & Anne L. Hotard & Martin L. Moore & Min Zhao & Zi-Zheng, 2017. "Structural basis of respiratory syncytial virus subtype-dependent neutralization by an antibody targeting the fusion glycoprotein," Nature Communications, Nature, vol. 8(1), pages 1-7, December.
    5. Zunlong Ke & Joaquin Oton & Kun Qu & Mirko Cortese & Vojtech Zila & Lesley McKeane & Takanori Nakane & Jasenko Zivanov & Christopher J. Neufeldt & Berati Cerikan & John M. Lu & Julia Peukes & Xiaoli X, 2020. "Structures and distributions of SARS-CoV-2 spike proteins on intact virions," Nature, Nature, vol. 588(7838), pages 498-502, December.
    6. Morgan S. A. Gilman & Polina Furmanova-Hollenstein & Gabriel Pascual & Angélique van ‘t Wout & Johannes P. M. Langedijk & Jason S. McLellan, 2019. "Transient opening of trimeric prefusion RSV F proteins," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    7. Zunlong Ke & Joshua D. Strauss & Cheri M. Hampton & Melinda A. Brindley & Rebecca S. Dillard & Fredrick Leon & Kristen M. Lamb & Richard K. Plemper & Elizabeth R. Wright, 2018. "Promotion of virus assembly and organization by the measles virus matrix protein," Nature Communications, Nature, vol. 9(1), pages 1-10, December.
    8. Christopher C. Stobart & Christina A. Rostad & Zunlong Ke & Rebecca S. Dillard & Cheri M. Hampton & Joshua D. Strauss & Hong Yi & Anne L. Hotard & Jia Meng & Raymond J. Pickles & Kaori Sakamoto & Suji, 2016. "A live RSV vaccine with engineered thermostability is immunogenic in cotton rats despite high attenuation," Nature Communications, Nature, vol. 7(1), pages 1-12, December.
    9. Sami Chaaban & Andrew P. Carter, 2022. "Structure of dynein–dynactin on microtubules shows tandem adaptor binding," Nature, Nature, vol. 610(7930), pages 212-216, October.
    10. Sami Chaaban & Andrew P. Carter, 2022. "Publisher Correction: Structure of dynein–dynactin on microtubules shows tandem adaptor binding," Nature, Nature, vol. 611(7935), pages 8-8, November.
    11. 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.
    12. Simon Jenni & Joshua A. Horwitz & Louis-Marie Bloyet & Sean P. J. Whelan & Stephen C. Harrison, 2022. "Visualizing molecular interactions that determine assembly of a bullet-shaped vesicular stomatitis virus particle," Nature Communications, Nature, vol. 13(1), pages 1-14, 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. 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.
    2. Jack D. Whitehead & Hortense Decool & Cédric Leyrat & Loic Carrique & Jenna Fix & Jean-François Eléouët & Marie Galloux & Max Renner, 2023. "Structure of the N-RNA/P interface indicates mode of L/P recruitment to the nucleocapsid of human metapneumovirus," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    3. Yuanchang Zhao & Sena Oten & Ahmet Yildiz, 2023. "Nde1 promotes Lis1-mediated activation of dynein," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    4. Kyoko Okada & Bharat R. Iyer & Lindsay G. Lammers & Pedro A. Gutierrez & Wenzhe Li & Steven M. Markus & Richard J. McKenney, 2023. "Conserved roles for the dynein intermediate chain and Ndel1 in assembly and activation of dynein," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    5. 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.
    6. Daníelsson, Jón & Macrae, Robert & Uthemann, Andreas, 2022. "Artificial intelligence and systemic risk," Journal of Banking & Finance, Elsevier, vol. 140(C).
    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. Rineke Jong & Norbert Stockhofe-Zurwieden & Judith Bonsing & Kai-Fen Wang & Sarah Vandepaer & Badiaa Bouzya & Jean-François Toussaint & Ilse Dieussaert & Haifeng Song & Ann-Muriel Steff, 2022. "ChAd155-RSV vaccine is immunogenic and efficacious against bovine RSV infection-induced disease in young calves," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    9. Tim Schulte & Antonio Chaves-Sanjuan & Valentina Speranzini & Kevin Sicking & Melissa Milazzo & Giulia Mazzini & Paola Rognoni & Serena Caminito & Paolo Milani & Chiara Marabelli & Alessandro Corbelli, 2024. "Helical superstructures between amyloid and collagen in cardiac fibrils from a patient with AL amyloidosis," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    10. Nikhil Kumar Tulsian & Raghuvamsi Venkata Palur & Xinlei Qian & Yue Gu & Bhuvaneshwari D/O Shunmuganathan & Firdaus Samsudin & Yee Hwa Wong & Jianqing Lin & Kiren Purushotorman & Mary McQueen Kozma & , 2023. "Defining neutralization and allostery by antibodies against COVID-19 variants," Nature Communications, Nature, vol. 14(1), pages 1-23, December.
    11. 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.
    12. Anna R. Mäkelä & Hasan Uğurlu & Liina Hannula & Ravi Kant & Petja Salminen & Riku Fagerlund & Sanna Mäki & Anu Haveri & Tomas Strandin & Lauri Kareinen & Jussi Hepojoki & Suvi Kuivanen & Lev Levanov &, 2023. "Intranasal trimeric sherpabody inhibits SARS-CoV-2 including recent immunoevasive Omicron subvariants," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    13. Xueming Meng & Cong Xu & Jiawei Li & Benhua Qiu & Jiajun Luo & Qin Hong & Yujie Tong & Chuyu Fang & Yanyan Feng & Rui Ma & Xiangyi Shi & Cheng Lin & Chen Pan & Xueliang Zhu & Xiumin Yan & Yao Cong, 2024. "Multi-scale structures of the mammalian radial spoke and divergence of axonemal complexes in ependymal cilia," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    14. Kemin Tan & Junjian Chen & Yu Kaku & Yi Wang & Luke Donius & Rafiq Ahmad Khan & Xiaolong Li & Hannah Richter & Michael S. Seaman & Thomas Walz & Wonmuk Hwang & Ellis L. Reinherz & Mikyung Kim, 2023. "Inadequate structural constraint on Fab approach rather than paratope elicitation limits HIV-1 MPER vaccine utility," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    15. Zhiqiang Li & Han Xia & Guibo Rao & Yan Fu & Tingting Chong & Kexing Tian & Zhiming Yuan & Sheng Cao, 2024. "Cryo-EM structures of Banna virus in multiple states reveal stepwise detachment of viral spikes," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    16. Rong Zhu & Daniel Canena & Mateusz Sikora & Miriam Klausberger & Hannah Seferovic & Ahmad Reza Mehdipour & Lisa Hain & Elisabeth Laurent & Vanessa Monteil & Gerald Wirnsberger & Ralph Wieneke & Robert, 2022. "Force-tuned avidity of spike variant-ACE2 interactions viewed on the single-molecule level," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    17. Oskar Staufer & Kapil Gupta & Jochen Estebano Hernandez Bücher & Fabian Kohler & Christian Sigl & Gunjita Singh & Kate Vasileiou & Ana Yagüe Relimpio & Meline Macher & Sebastian Fabritz & Hendrik Diet, 2022. "Synthetic virions reveal fatty acid-coupled adaptive immunogenicity of SARS-CoV-2 spike glycoprotein," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    18. Zhen Hou & Frank Nightingale & Yanan Zhu & Craig MacGregor-Chatwin & Peijun Zhang, 2023. "Structure of native chromatin fibres revealed by Cryo-ET in situ," Nature Communications, Nature, vol. 14(1), pages 1-7, December.
    19. Conny Leistner & Martin Wilkinson & Ailidh Burgess & Megan Lovatt & Stanley Goodbody & Yong Xu & Susan Deuchars & Sheena E. Radford & Neil A. Ranson & René A. W. Frank, 2023. "The in-tissue molecular architecture of β-amyloid pathology in the mammalian brain," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    20. 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.

    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_s41467-024-50162-x. 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.