IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-40565-7.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-40565-7
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-40565-7?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. 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.
    2. 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.
    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.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Jia Li & Alan J. Simmons & Caroline V. Hawkins & Sophie Chiron & Marisol A. Ramirez-Solano & Naila Tasneem & Harsimran Kaur & Yanwen Xu & Frank Revetta & Paige N. Vega & Shunxing Bao & Can Cui & Regin, 2024. "Identification and multimodal characterization of a specialized epithelial cell type associated with Crohn’s disease," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    2. Alberto Díez-Sánchez & Håvard T. Lindholm & Pia M. Vornewald & Jenny Ostrop & Rouan Yao & Andrew B. Single & Anne Marstad & Naveen Parmar & Tovah N. Shaw & Mara Martín-Alonso & Menno J. Oudhoff, 2024. "LSD1 drives intestinal epithelial maturation and controls small intestinal immune cell composition independent of microbiota in a murine model," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    3. Xingxing Ren & Qiuyuan Liu & Peirong Zhou & Tingyue Zhou & Decai Wang & Qiao Mei & Richard A. Flavell & Zhanju Liu & Mingsong Li & Wen Pan & Shu Zhu, 2024. "DHX9 maintains epithelial homeostasis by restraining R-loop-mediated genomic instability in intestinal stem cells," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    4. Susanne Kessler & Bradly Burke & Geoffroy Andrieux & Jan Schinköthe & Lea Hamberger & Johannes Kacza & Shijun Zhan & Clara Reasoner & Taru S. Dutt & Maria Kaukab Osman & Marcela Henao-Tamayo & Julian , 2024. "Deciphering bat influenza H18N11 infection dynamics in male Jamaican fruit bats on a single-cell level," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    5. María A. Duque-Correa & David Goulding & Faye H. Rodgers & J. Andrew Gillis & Claire Cormie & Kate A. Rawlinson & Allison J. Bancroft & Hayley M. Bennett & Magda E. Lotkowska & Adam J. Reid & Annelies, 2022. "Defining the early stages of intestinal colonisation by whipworms," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    6. Jiarui Ding & John J. Garber & Amiko Uchida & Ariel Lefkovith & Grace T. Carter & Praveen Vimalathas & Lauren Canha & Michael Dougan & Kyle Staller & Joseph Yarze & Toni M. Delorey & Orit Rozenblatt-R, 2024. "An esophagus cell atlas reveals dynamic rewiring during active eosinophilic esophagitis and remission," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    7. Pietro Demela & Nicola Pirastu & Blagoje Soskic, 2023. "Cross-disorder genetic analysis of immune diseases reveals distinct gene associations that converge on common pathways," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    8. Wenjie Pan & Xuan Wang & Chunhua Ren & Xiao Jiang & Sanqiang Gong & Zhenyu Xie & Nai-Kei Wong & Xiaomin Li & Jiasheng Huang & Dingding Fan & Peng Luo & Yun Yang & Xinyue Ren & Suzhong Yu & Zhou Qin & , 2024. "Sea cucumbers and their symbiotic microbiome have evolved to feed on seabed sediments," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    9. Xiwen Xiong & Chenyan Yang & Wei-Qi He & Jiahui Yu & Yue Xin & Xinge Zhang & Rong Huang & Honghui Ma & Shaofang Xu & Zun Li & Jie Ma & Lin Xu & Qunyi Wang & Kaiqun Ren & Xiaoli S. Wu & Christopher R. , 2022. "Sirtuin 6 maintains epithelial STAT6 activity to support intestinal tuft cell development and type 2 immunity," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    10. Reza Mirzazadeh & Zaneta Andrusivova & Ludvig Larsson & Phillip T. Newton & Leire Alonso Galicia & Xesús M. Abalo & Mahtab Avijgan & Linda Kvastad & Alexandre Denadai-Souza & Nathalie Stakenborg & Ale, 2023. "Spatially resolved transcriptomic profiling of degraded and challenging fresh frozen samples," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    11. Sandor Spisak & David Chen & Pornlada Likasitwatanakul & Paul Doan & Zhixin Li & Pratyusha Bala & Laura Vizkeleti & Viktoria Tisza & Pushpamali Silva & Marios Giannakis & Brian Wolpin & Jun Qi & Nilay, 2024. "Identifying regulators of aberrant stem cell and differentiation activity in colorectal cancer using a dual endogenous reporter system," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    12. Lucia Taraborrelli & Yasin Şenbabaoğlu & Lifen Wang & Junghyun Lim & Kerrigan Blake & Noelyn Kljavin & Sarah Gierke & Alexis Scherl & James Ziai & Erin McNamara & Mark Owyong & Shilpa Rao & Aslihan Ka, 2023. "Tumor-intrinsic expression of the autophagy gene Atg16l1 suppresses anti-tumor immunity in colorectal cancer," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    13. Tianwei Yu, 2018. "A new dynamic correlation algorithm reveals novel functional aspects in single cell and bulk RNA-seq data," PLOS Computational Biology, Public Library of Science, vol. 14(8), pages 1-22, August.
    14. Greg Holmes & Ana S. Gonzalez-Reiche & Madrikha Saturne & Susan M. Motch Perrine & Xianxiao Zhou & Ana C. Borges & Bhavana Shewale & Joan T. Richtsmeier & Bin Zhang & Harm Bakel & Ethylin Wang Jabs, 2021. "Single-cell analysis identifies a key role for Hhip in murine coronal suture development," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    15. Akshaya Ramakrishnan & Aikaterini Symeonidi & Patrick Hanel & Katharina T. Schmid & Maria L. Richter & Michael Schubert & Maria Colomé-Tatché, 2023. "epiAneufinder identifies copy number alterations from single-cell ATAC-seq data," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    16. Jiacheng Wu & Xiaoqing Xu & Jiaqi Duan & Yangyang Chai & Jiaying Song & Dongsheng Gong & Bingjing Wang & Ye Hu & Taotao Han & Yuanyuan Ding & Yin Liu & Jingnan Li & Xuetao Cao, 2024. "EFHD2 suppresses intestinal inflammation by blocking intestinal epithelial cell TNFR1 internalization and cell death," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    17. Manqiang Lin & Kimberly Hartl & Julian Heuberger & Giulia Beccaceci & Hilmar Berger & Hao Li & Lichao Liu & Stefanie Müllerke & Thomas Conrad & Felix Heymann & Andrew Woehler & Frank Tacke & Nikolaus , 2023. "Establishment of gastrointestinal assembloids to study the interplay between epithelial crypts and their mesenchymal niche," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    18. Adam E. Hall & Sebastian Öther-Gee Pohl & Patrizia Cammareri & Stuart Aitken & Nicholas T. Younger & Michela Raponi & Caroline V. Billard & Alfonso Bolado Carrancio & Aslihan Bastem & Paz Freile & Fio, 2022. "RNA splicing is a key mediator of tumour cell plasticity and a therapeutic vulnerability in colorectal cancer," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    19. Egle Kvedaraite & Magda Lourda & Natalia Mouratidou & Tim Düking & Avinash Padhi & Kirsten Moll & Paulo Czarnewski & Indranil Sinha & Ioanna Xagoraris & Efthymia Kokkinou & Anastasios Damdimopoulos & , 2024. "Intestinal stroma guides monocyte differentiation to macrophages through GM-CSF," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    20. Jorge Mata-Garrido & Yao Xiang & Yunhua Chang-Marchand & Caroline Reisacher & Elisabeth Ageron & Ida Chiara Guerrera & Iñigo Casafont & Aurelia Bruneau & Claire Cherbuy & Xavier Treton & Anne Dumay & , 2022. "The Heterochromatin protein 1 is a regulator in RNA splicing precision deficient in ulcerative colitis," Nature Communications, Nature, vol. 13(1), pages 1-16, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-40565-7. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.