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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
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    References listed on IDEAS

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    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. 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.
    3. 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.
    4. 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.
    5. 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.
    6. 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.
    7. 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.
    8. 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.
    9. 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.
    10. 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.
    11. 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.
    12. 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.
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