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B cell-intrinsic epigenetic modulation of antibody responses by dietary fiber-derived short-chain fatty acids

Author

Listed:
  • Helia N. Sanchez

    (University of Texas Long School of Medicine, UT Health Science Center)

  • Justin B. Moroney

    (University of Texas Long School of Medicine, UT Health Science Center)

  • Huoqun Gan

    (University of Texas Long School of Medicine, UT Health Science Center
    Central South University)

  • Tian Shen

    (University of Texas Long School of Medicine, UT Health Science Center
    Central South University)

  • John L. Im

    (University of Texas Long School of Medicine, UT Health Science Center)

  • Tianbao Li

    (University of Texas Long School of Medicine, UT Health Science Center)

  • Julia R. Taylor

    (University of Texas Long School of Medicine, UT Health Science Center)

  • Hong Zan

    (University of Texas Long School of Medicine, UT Health Science Center)

  • Paolo Casali

    (University of Texas Long School of Medicine, UT Health Science Center)

Abstract

Short-chain fatty acids (SCFAs) butyrate and propionate are metabolites from dietary fiber's fermentation by gut microbiota that can affect differentiation or functions of T cells, macrophages and dendritic cells. We show here that at low doses these SCFAs directly impact B cell intrinsic functions to moderately enhance class-switch DNA recombination (CSR), while decreasing at higher doses over a broad physiological range, AID and Blimp1 expression, CSR, somatic hypermutation and plasma cell differentiation. In human and mouse B cells, butyrate and propionate decrease B cell Aicda and Prdm1 by upregulating select miRNAs that target Aicda and Prdm1 mRNA-3′UTRs through inhibition of histone deacetylation (HDAC) of those miRNA host genes. By acting as HDAC inhibitors, not as energy substrates or through GPR-engagement signaling in these B cell-intrinsic processes, these SCFAs impair intestinal and systemic T-dependent and T-independent antibody responses. Their epigenetic impact on B cells extends to inhibition of autoantibody production and autoimmunity in mouse lupus models.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:11:y:2020:i:1:d:10.1038_s41467-019-13603-6
    DOI: 10.1038/s41467-019-13603-6
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    Cited by:

    1. Wenna Chi & Na Kang & Linlin Sheng & Sichen Liu & Lei Tao & Xizhi Cao & Ye Liu & Can Zhu & Yuming Zhang & Bolong Wu & Ruiqun Chen & Lili Cheng & Jing Wang & Xiaolin Sun & Xiaohui Liu & Haiteng Deng & , 2024. "MCT1-governed pyruvate metabolism is essential for antibody class-switch recombination through H3K27 acetylation," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    2. 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.
    3. Yijiang Xu & Hang Zhou & Ginell Post & Hong Zan & Paolo Casali, 2022. "Rad52 mediates class-switch DNA recombination to IgD," Nature Communications, Nature, vol. 13(1), pages 1-18, December.

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