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CLIC and membrane wound repair pathways enable pandemic norovirus entry and infection

Author

Listed:
  • B. Vijayalakshmi Ayyar

    (Baylor College of Medicine)

  • Khalil Ettayebi

    (Baylor College of Medicine)

  • Wilhelm Salmen

    (Baylor College of Medicine)

  • Umesh C. Karandikar

    (Baylor College of Medicine)

  • Frederick H. Neill

    (Baylor College of Medicine)

  • Victoria R. Tenge

    (Baylor College of Medicine)

  • Sue E. Crawford

    (Baylor College of Medicine)

  • Erhard Bieberich

    (University of Kentucky, Lexington)

  • B. V. Venkataram Prasad

    (Baylor College of Medicine)

  • Robert L. Atmar

    (Baylor College of Medicine
    Baylor College of Medicine)

  • Mary K. Estes

    (Baylor College of Medicine
    Baylor College of Medicine)

Abstract

Globally, most cases of gastroenteritis are caused by pandemic GII.4 human norovirus (HuNoV) strains with no approved therapies or vaccines available. The cellular pathways that these strains exploit for cell entry and internalization are unknown. Here, using nontransformed human jejunal enteroids (HIEs) that recapitulate the physiology of the gastrointestinal tract, we show that infectious GII.4 virions and virus-like particles are endocytosed using a unique combination of endosomal acidification-dependent clathrin-independent carriers (CLIC), acid sphingomyelinase (ASM)-mediated lysosomal exocytosis, and membrane wound repair pathways. We found that besides the known interaction of the viral capsid Protruding (P) domain with host glycans, the Shell (S) domain interacts with both galectin-3 (gal-3) and apoptosis-linked gene 2-interacting protein X (ALIX), to orchestrate GII.4 cell entry. Recognition of the viral and cellular determinants regulating HuNoV entry provides insight into the infection process of a non-enveloped virus highlighting unique pathways and targets for developing effective therapeutics.

Suggested Citation

  • B. Vijayalakshmi Ayyar & Khalil Ettayebi & Wilhelm Salmen & Umesh C. Karandikar & Frederick H. Neill & Victoria R. Tenge & Sue E. Crawford & Erhard Bieberich & B. V. Venkataram Prasad & Robert L. Atma, 2023. "CLIC and membrane wound repair pathways enable pandemic norovirus entry and infection," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-36398-z
    DOI: 10.1038/s41467-023-36398-z
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    References listed on IDEAS

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    1. Yvan Campos & Xiaohui Qiu & Elida Gomero & Randall Wakefield & Linda Horner & Wojciech Brutkowski & Young-Goo Han & David Solecki & Sharon Frase & Antonella Bongiovanni & Alessandra d’Azzo, 2016. "Alix-mediated assembly of the actomyosin–tight junction polarity complex preserves epithelial polarity and epithelial barrier," Nature Communications, Nature, vol. 7(1), pages 1-15, September.
    2. Luana L. Scheffer & Sen Chandra Sreetama & Nimisha Sharma & Sushma Medikayala & Kristy J. Brown & Aurelia Defour & Jyoti K. Jaiswal, 2014. "Mechanism of Ca2+-triggered ESCRT assembly and regulation of cell membrane repair," Nature Communications, Nature, vol. 5(1), pages 1-12, December.
    3. Gabriela Alvarado & Wilhelm Salmen & Khalil Ettayebi & Liya Hu & Banumathi Sankaran & Mary K. Estes & B. V. Venkataram Prasad & James E. Crowe, 2021. "Author Correction: Broadly cross-reactive human antibodies that inhibit genogroup I and II noroviruses," Nature Communications, Nature, vol. 12(1), pages 1-1, December.
    4. Liya Hu & Wilhelm Salmen & Rong Chen & Yi Zhou & Frederick Neill & James E. Crowe & Robert L. Atmar & Mary K. Estes & B. V. Venkataram Prasad, 2022. "Atomic structure of the predominant GII.4 human norovirus capsid reveals novel stability and plasticity," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    5. Gabriela Alvarado & Wilhelm Salmen & Khalil Ettayebi & Liya Hu & Banumathi Sankaran & Mary K. Estes & B. V. Venkataram Prasad & James E. Crowe, 2021. "Broadly cross-reactive human antibodies that inhibit genogroup I and II noroviruses," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    6. Aurélie Bertin & Nicola Franceschi & Eugenio Mora & Sourav Maity & Maryam Alqabandi & Nolwen Miguet & Aurélie Cicco & Wouter H. Roos & Stéphanie Mangenot & Winfried Weissenhorn & Patricia Bassereau, 2020. "Author Correction: Human ESCRT-III polymers assemble on positively curved membranes and induce helical membrane tube formation," Nature Communications, Nature, vol. 11(1), pages 1-1, December.
    7. Aurélie Bertin & Nicola Franceschi & Eugenio Mora & Sourav Maity & Maryam Alqabandi & Nolwen Miguet & Aurélie Cicco & Wouter H. Roos & Stéphanie Mangenot & Winfried Weissenhorn & Patricia Bassereau, 2020. "Human ESCRT-III polymers assemble on positively curved membranes and induce helical membrane tube formation," Nature Communications, Nature, vol. 11(1), pages 1-13, December.
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    Cited by:

    1. Wilhelm Salmen & Liya Hu & Marina Bok & Natthawan Chaimongkol & Khalil Ettayebi & Stanislav V. Sosnovtsev & Kaundal Soni & B. Vijayalakshmi Ayyar & Sreejesh Shanker & Frederick H. Neill & Banumathi Sa, 2023. "A single nanobody neutralizes multiple epochally evolving human noroviruses by modulating capsid plasticity," Nature Communications, Nature, vol. 14(1), pages 1-11, December.

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