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Bile acid-dependent transcription factors and chromatin accessibility determine regional heterogeneity of intestinal antimicrobial peptides

Author

Listed:
  • Yue Wang

    (Qilu Hospital of Shandong University)

  • Yanbo Yu

    (Qilu Hospital of Shandong University
    Qilu Hospital of Shandong University
    Shandong Provincial Clinical Research Center for digestive disease)

  • Lixiang Li

    (Qilu Hospital of Shandong University
    Qilu Hospital of Shandong University
    Shandong Provincial Clinical Research Center for digestive disease)

  • Mengqi Zheng

    (Qilu Hospital of Shandong University)

  • Jiawei Zhou

    (Qilu Hospital of Shandong University)

  • Haifan Gong

    (Sun Yat-sen University)

  • Bingcheng Feng

    (Qilu Hospital of Shandong University)

  • Xiao Wang

    (Qilu Hospital of Shandong University)

  • Xuanlin Meng

    (Shanghai Jiao Tong University)

  • Yanyan Cui

    (Shandong University)

  • Yanan Xia

    (Qilu Hospital of Shandong University)

  • Shuzheng Chu

    (Shandong University)

  • Lin Lin

    (Qilu Hospital of Shandong University)

  • Huijun Chang

    (Qilu Hospital of Shandong University)

  • Ruchen Zhou

    (Qilu Hospital of Shandong University)

  • Mingjun Ma

    (Qilu Hospital of Shandong University)

  • Zhen Li

    (Qilu Hospital of Shandong University
    Qilu Hospital of Shandong University
    Shandong Provincial Clinical Research Center for digestive disease)

  • Rui Ji

    (Qilu Hospital of Shandong University
    Qilu Hospital of Shandong University
    Shandong Provincial Clinical Research Center for digestive disease)

  • Ming Lu

    (Qilu Hospital of Shandong University)

  • Xiaoyun Yang

    (Qilu Hospital of Shandong University
    Qilu Hospital of Shandong University
    Shandong Provincial Clinical Research Center for digestive disease)

  • Xiuli Zuo

    (Qilu Hospital of Shandong University
    Qilu Hospital of Shandong University
    Shandong Provincial Clinical Research Center for digestive disease)

  • Shiyang Li

    (Qilu Hospital of Shandong University
    Shandong University
    Shandong University)

  • Yanqing Li

    (Qilu Hospital of Shandong University
    Qilu Hospital of Shandong University
    Shandong Provincial Clinical Research Center for digestive disease)

Abstract

Antimicrobial peptides (AMPs) are important mediators of intestinal immune surveillance. However, the regional heterogeneity of AMPs and its regulatory mechanisms remain obscure. Here, we clarified the regional heterogeneity of intestinal AMPs at the single-cell level, and revealed a cross-lineages AMP regulation mechanism that bile acid dependent transcription factors (BATFs), NR1H4, NR1H3 and VDR, regulate AMPs through a ligand-independent manner. Bile acids regulate AMPs by perturbing cell differentiation rather than activating BATFs signaling. Chromatin accessibility determines the potential of BATFs to regulate AMPs at the pre-transcriptional level, thus shaping the regional heterogeneity of AMPs. The BATFs-AMPs axis also participates in the establishment of intestinal antimicrobial barriers of fetuses and the defects of antibacterial ability during Crohn’s disease. Overall, BATFs and chromatin accessibility play essential roles in shaping the regional heterogeneity of AMPs at pre- and postnatal stages, as well as in maintenance of antimicrobial immunity during homeostasis and disease.

Suggested Citation

  • Yue Wang & Yanbo Yu & Lixiang Li & Mengqi Zheng & Jiawei Zhou & Haifan Gong & Bingcheng Feng & Xiao Wang & Xuanlin Meng & Yanyan Cui & Yanan Xia & Shuzheng Chu & Lin Lin & Huijun Chang & Ruchen Zhou &, 2023. "Bile acid-dependent transcription factors and chromatin accessibility determine regional heterogeneity of intestinal antimicrobial peptides," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-40565-7
    DOI: 10.1038/s41467-023-40565-7
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    1. Adam L. Haber & Moshe Biton & Noga Rogel & Rebecca H. Herbst & Karthik Shekhar & Christopher Smillie & Grace Burgin & Toni M. Delorey & Michael R. Howitt & Yarden Katz & Itay Tirosh & Semir Beyaz & Da, 2017. "A single-cell survey of the small intestinal epithelium," Nature, Nature, vol. 551(7680), pages 333-339, November.
    2. Rasa Elmentaite & Natsuhiko Kumasaka & Kenny Roberts & Aaron Fleming & Emma Dann & Hamish W. King & Vitalii Kleshchevnikov & Monika Dabrowska & Sophie Pritchard & Liam Bolt & Sara F. Vieira & Lira Mam, 2021. "Cells of the human intestinal tract mapped across space and time," Nature, Nature, vol. 597(7875), pages 250-255, September.
    3. Kaushal Parikh & Agne Antanaviciute & David Fawkner-Corbett & Marta Jagielowicz & Anna Aulicino & Christoffer Lagerholm & Simon Davis & James Kinchen & Hannah H. Chen & Nasullah Khalid Alham & Neil As, 2019. "Colonic epithelial cell diversity in health and inflammatory bowel disease," Nature, Nature, vol. 567(7746), pages 49-55, March.
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