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Heat-inactivated Bifidobacterium adolescentis ameliorates colon senescence through Paneth-like-cell-mediated stem cell activation

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Listed:
  • Yadong Qi

    (Zhejiang University School of Medicine
    Zhejiang University)

  • Jiamin He

    (Zhejiang University School of Medicine
    Zhejiang University)

  • Yawen Zhang

    (Zhejiang University School of Medicine
    Zhejiang University
    Zhejiang University School of Medicine)

  • Qiwei Ge

    (Zhejiang University
    Second Affiliated Hospital of Zhejiang University School of Medicine)

  • Qiwen Wang

    (Zhejiang University School of Medicine
    Zhejiang University)

  • Luyi Chen

    (Zhejiang University School of Medicine
    Zhejiang University School of Medicine)

  • Jilei Xu

    (Zhejiang University School of Medicine
    Zhejiang University)

  • Lan Wang

    (Zhejiang University School of Medicine
    Zhejiang University)

  • Xueqin Chen

    (Zhejiang University School of Medicine
    Zhejiang University)

  • Dingjiacheng Jia

    (Zhejiang University
    Second Affiliated Hospital of Zhejiang University School of Medicine)

  • Yifeng Lin

    (Zhejiang University
    Second Affiliated Hospital of Zhejiang University School of Medicine)

  • Chaochao Xu

    (Zhejiang University
    Second Affiliated Hospital of Zhejiang University School of Medicine)

  • Ying Zhang

    (Zhejiang University
    Second Affiliated Hospital of Zhejiang University School of Medicine)

  • Tongyao Hou

    (Zhejiang University School of Medicine
    Zhejiang University)

  • Jianmin Si

    (Zhejiang University School of Medicine
    Zhejiang University
    Zhejiang University School of Medicine)

  • Shujie Chen

    (Zhejiang University School of Medicine
    Zhejiang University
    Zhejiang University School of Medicine)

  • Liangjing Wang

    (Zhejiang University
    Zhejiang University School of Medicine
    Second Affiliated Hospital of Zhejiang University School of Medicine)

Abstract

Declined numbers and weakened functions of intestinal stem cells (ISCs) impair the integrity of the intestinal epithelium during aging. However, the impact of intestinal microbiota on ISCs in this process is unclear. Here, using premature aging mice (telomerase RNA component knockout, Terc−/−), natural aging mice, and in vitro colonoid models, we explore how heat-inactivated Bifidobacterium adolescentis (B. adolescentis) affects colon senescence. We find that B. adolescentis could mitigate colonic senescence-related changes by enhancing intestinal integrity and stimulating the regeneration of Lgr5+ ISCs via Wnt/β-catenin signaling. Furthermore, we uncover the involvement of Paneth-like cells (PLCs) within the colonic stem-cell-supporting niche in the B. adolescentis-induced ISC regeneration. In addition, we identify soluble polysaccharides (SPS) as potential effective components of B. adolescentis. Overall, our findings reveal the role of heat-inactivated B. adolescentis in maintaining the ISCs regeneration and intestinal barrier, and propose a microbiota target for ameliorating colon senescence.

Suggested Citation

  • Yadong Qi & Jiamin He & Yawen Zhang & Qiwei Ge & Qiwen Wang & Luyi Chen & Jilei Xu & Lan Wang & Xueqin Chen & Dingjiacheng Jia & Yifeng Lin & Chaochao Xu & Ying Zhang & Tongyao Hou & Jianmin Si & Shuj, 2023. "Heat-inactivated Bifidobacterium adolescentis ameliorates colon senescence through Paneth-like-cell-mediated stem cell activation," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-41827-0
    DOI: 10.1038/s41467-023-41827-0
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    1. Toshiro Sato & Johan H. van Es & Hugo J. Snippert & Daniel E. Stange & Robert G. Vries & Maaike van den Born & Nick Barker & Noah F. Shroyer & Marc van de Wetering & Hans Clevers, 2011. "Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts," Nature, Nature, vol. 469(7330), pages 415-418, January.
    2. Munhyung Bae & Chelsi D. Cassilly & Xiaoxi Liu & Sung-Moo Park & Betsabeh Khoramian Tusi & Xiangjun Chen & Jaeyoung Kwon & Pavel Filipčík & Andrew S. Bolze & Zehua Liu & Hera Vlamakis & Daniel B. Grah, 2022. "Akkermansia muciniphila phospholipid induces homeostatic immune responses," Nature, Nature, vol. 608(7921), pages 168-173, August.
    3. Imilce A. Rodriguez-Fernandez & Yanyan Qi & Heinrich Jasper, 2019. "Loss of a proteostatic checkpoint in intestinal stem cells contributes to age-related epithelial dysfunction," Nature Communications, Nature, vol. 10(1), pages 1-15, December.
    4. Tian Wang & Renjie Chai & Grace S. Kim & Nicole Pham & Lina Jansson & Duc-Huy Nguyen & Bryan Kuo & Lindsey A. May & Jian Zuo & Lisa L. Cunningham & Alan G. Cheng, 2015. "Lgr5+ cells regenerate hair cells via proliferation and direct transdifferentiation in damaged neonatal mouse utricle," Nature Communications, Nature, vol. 6(1), pages 1-15, May.
    5. Nick Barker & Johan H. van Es & Jeroen Kuipers & Pekka Kujala & Maaike van den Born & Miranda Cozijnsen & Andrea Haegebarth & Jeroen Korving & Harry Begthel & Peter J. Peters & Hans Clevers, 2007. "Identification of stem cells in small intestine and colon by marker gene Lgr5," Nature, Nature, vol. 449(7165), pages 1003-1007, October.
    6. Benoit Chassaing & Omry Koren & Julia K. Goodrich & Angela C. Poole & Shanthi Srinivasan & Ruth E. Ley & Andrew T. Gewirtz, 2015. "Dietary emulsifiers impact the mouse gut microbiota promoting colitis and metabolic syndrome," Nature, Nature, vol. 519(7541), pages 92-96, March.
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