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Functional and metabolic alterations of gut microbiota in children with new-onset type 1 diabetes

Author

Listed:
  • Xiaoxiao Yuan

    (Children’s Hospital of Fudan University)

  • Ruirui Wang

    (Shanghai University of Traditional Chinese Medicine)

  • Bing Han

    (Children’s Hospital of Fudan University
    Institutes of Biomedical Sciences, Fudan University)

  • ChengJun Sun

    (Children’s Hospital of Fudan University)

  • Ruimin Chen

    (Fuzhou Children’s Hospital of Fujian Medical University)

  • Haiyan Wei

    (Children’s Hospital Affiliated to Zhengzhou University)

  • Linqi Chen

    (Children’s Hospital of Soochow University)

  • Hongwei Du

    (The First Hospital of Jilin University)

  • Guimei Li

    (Shandong Provincial Hospital Affiliated to Shandong First Medical University)

  • Yu Yang

    (The Affiliated Children’s Hospital of Nanchang University)

  • Xiaojuan Chen

    (The Children’s Hospital of Shanxi Province)

  • Lanwei Cui

    (The First Affiliated Hospital of Harbin Medical University)

  • Zhenran Xu

    (Children’s Hospital of Fudan University)

  • Junfen Fu

    (Children’s Hospital, Zhejiang University School of Medicine)

  • Jin Wu

    (West China Second University Hospital, Sichuan University)

  • Wei Gu

    (Children’s Hospital of Nanjing Medical University)

  • Zhihong Chen

    (Affiliated Hospital of Qingdao University)

  • Xin Fang

    (Fujian Medical University Union Hospital)

  • Hongxiu Yang

    (Qingdao Women and Children’s Hospital)

  • Zhe Su

    (Shenzhen Children’s Hospital)

  • Jing Wu

    (Children’s Hospital of Fudan University)

  • Qiuyue Li

    (Children’s Hospital of Fudan University)

  • Miaoying Zhang

    (Children’s Hospital of Fudan University)

  • Yufeng Zhou

    (Children’s Hospital of Fudan University, and the Shanghai Key Laboratory of Medical Epigenetics, International Co-laboratory of Medical Epigenetics and Metabolism, Ministry of Science and Technology, Institutes of Biomedical Sciences, Fudan University
    Fudan University)

  • Lei Zhang

    (Shanghai University of Traditional Chinese Medicine)

  • Guang Ji

    (Shanghai University of Traditional Chinese Medicine)

  • Feihong Luo

    (Children’s Hospital of Fudan University)

Abstract

Gut dysbiosis has been linked to type 1 diabetes (T1D); however, microbial capacity in T1D remains unclear. Here, we integratively profiled gut microbial functional and metabolic alterations in children with new-onset T1D in independent cohorts and investigated the underlying mechanisms. In T1D, the microbiota was characterized by decreased butyrate production and bile acid metabolism and increased lipopolysaccharide biosynthesis at the species, gene, and metabolite levels. The combination of 18 bacterial species and fecal metabolites provided excellently discriminatory power for T1D. Gut microbiota from children with T1D induced elevated fasting glucose levels and declined insulin sensitivity in antibiotic-treated mice. In streptozotocin-induced T1D mice, butyrate and lipopolysaccharide exerted protective and destructive effects on islet structure and function, respectively. Lipopolysaccharide aggravated the pancreatic inflammatory response, while butyrate activated Insulin1 and Insulin2 gene expression. Our study revealed perturbed microbial functional and metabolic traits in T1D, providing potential avenues for microbiome-based prevention and intervention for T1D.

Suggested Citation

  • Xiaoxiao Yuan & Ruirui Wang & Bing Han & ChengJun Sun & Ruimin Chen & Haiyan Wei & Linqi Chen & Hongwei Du & Guimei Li & Yu Yang & Xiaojuan Chen & Lanwei Cui & Zhenran Xu & Junfen Fu & Jin Wu & Wei Gu, 2022. "Functional and metabolic alterations of gut microbiota in children with new-onset type 1 diabetes," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-33656-4
    DOI: 10.1038/s41467-022-33656-4
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    References listed on IDEAS

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    1. Tommi Vatanen & Eric A. Franzosa & Randall Schwager & Surya Tripathi & Timothy D. Arthur & Kendra Vehik & Åke Lernmark & William A. Hagopian & Marian J. Rewers & Jin-Xiong She & Jorma Toppari & Anette, 2018. "The human gut microbiome in early-onset type 1 diabetes from the TEDDY study," Nature, Nature, vol. 562(7728), pages 589-594, October.
    2. Fredrik H. Karlsson & Valentina Tremaroli & Intawat Nookaew & Göran Bergström & Carl Johan Behre & Björn Fagerberg & Jens Nielsen & Fredrik Bäckhed, 2013. "Gut metagenome in European women with normal, impaired and diabetic glucose control," Nature, Nature, vol. 498(7452), pages 99-103, June.
    3. Li Wen & Ruth E. Ley & Pavel Yu. Volchkov & Peter B. Stranges & Lia Avanesyan & Austin C. Stonebraker & Changyun Hu & F. Susan Wong & Gregory L. Szot & Jeffrey A. Bluestone & Jeffrey I. Gordon & Alexa, 2008. "Innate immunity and intestinal microbiota in the development of Type 1 diabetes," Nature, Nature, vol. 455(7216), pages 1109-1113, October.
    4. Junjie Qin & Yingrui Li & Zhiming Cai & Shenghui Li & Jianfeng Zhu & Fan Zhang & Suisha Liang & Wenwei Zhang & Yuanlin Guan & Dongqian Shen & Yangqing Peng & Dongya Zhang & Zhuye Jie & Wenxian Wu & Yo, 2012. "A metagenome-wide association study of gut microbiota in type 2 diabetes," Nature, Nature, vol. 490(7418), pages 55-60, October.
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