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Dietary protein increases T-cell-independent sIgA production through changes in gut microbiota-derived extracellular vesicles

Author

Listed:
  • Jian Tan

    (The University of Sydney
    University of Sydney)

  • Duan Ni

    (The University of Sydney
    University of Sydney)

  • Jemma Taitz

    (The University of Sydney
    University of Sydney)

  • Gabriela Veronica Pinget

    (The University of Sydney
    University of Sydney)

  • Mark Read

    (The University of Sydney
    University of Sydney)

  • Alistair Senior

    (The University of Sydney
    University of Sydney)

  • Jibran Abdul Wali

    (The University of Sydney
    University of Sydney)

  • Reem Elnour

    (The University of Sydney
    University of Sydney)

  • Erin Shanahan

    (The University of Sydney
    University of Sydney)

  • Huiling Wu

    (The University of Sydney
    University of Sydney
    Royal Prince Alfred Hospital)

  • Steven J. Chadban

    (The University of Sydney
    University of Sydney
    Royal Prince Alfred Hospital)

  • Ralph Nanan

    (The University of Sydney
    University of Sydney)

  • Nicholas Jonathan Cole King

    (The University of Sydney
    University of Sydney
    The University of Sydney and The Centenary Institute)

  • Georges Emile Grau

    (University of Sydney
    The University of Sydney)

  • Stephen J. Simpson

    (The University of Sydney
    University of Sydney)

  • Laurence Macia

    (The University of Sydney
    University of Sydney
    The University of Sydney and The Centenary Institute)

Abstract

Secretory IgA is a key mucosal component ensuring host-microbiota mutualism. Here we use nutritional geometry modelling in mice fed 10 different macronutrient-defined, isocaloric diets, and identify dietary protein as the major driver of secretory IgA production. Protein-driven secretory IgA induction is not mediated by T-cell-dependent pathways or changes in gut microbiota composition. Instead, the microbiota of high protein fed mice produces significantly higher quantities of extracellular vesicles, compared to those of mice fed high-carbohydrate or high-fat diets. These extracellular vesicles activate Toll-like receptor 4 to increase the epithelial expression of IgA-inducing cytokine, APRIL, B cell chemokine, CCL28, and the IgA transporter, PIGR. We show that succinate, produced in high concentrations by microbiota of high protein fed animals, increases generation of reactive oxygen species by bacteria, which in turn promotes extracellular vesicles production. Here we establish a link between dietary macronutrient composition, gut microbial extracellular vesicles release and host secretory IgA response.

Suggested Citation

  • Jian Tan & Duan Ni & Jemma Taitz & Gabriela Veronica Pinget & Mark Read & Alistair Senior & Jibran Abdul Wali & Reem Elnour & Erin Shanahan & Huiling Wu & Steven J. Chadban & Ralph Nanan & Nicholas Jo, 2022. "Dietary protein increases T-cell-independent sIgA production through changes in gut microbiota-derived extracellular vesicles," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-31761-y
    DOI: 10.1038/s41467-022-31761-y
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    References listed on IDEAS

    as
    1. Helia N. Sanchez & Justin B. Moroney & Huoqun Gan & Tian Shen & John L. Im & Tianbao Li & Julia R. Taylor & Hong Zan & Paolo Casali, 2020. "B cell-intrinsic epigenetic modulation of antibody responses by dietary fiber-derived short-chain fatty acids," Nature Communications, Nature, vol. 11(1), pages 1-19, December.
    2. Lawson, John & Willden, Cameron, 2016. "Mixture Experiments in R Using mixexp," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 72(c02).
    Full references (including those not matched with items on IDEAS)

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