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Tracing the origin of adult intestinal stem cells

Author

Listed:
  • Jordi Guiu

    (University of Copenhagen)

  • Edouard Hannezo

    (University of Cambridge
    Institute of Science and Technology Austria)

  • Shiro Yui

    (University of Copenhagen
    Tokyo Medical and Dental University (TMDU))

  • Samuel Demharter

    (University of Copenhagen)

  • Svetlana Ulyanchenko

    (University of Copenhagen)

  • Martti Maimets

    (University of Copenhagen)

  • Anne Jørgensen

    (University of Copenhagen)

  • Signe Perlman

    (University of Copenhagen)

  • Lene Lundvall

    (University of Copenhagen)

  • Linn Salto Mamsen

    (University Hospital of Copenhagen, University of Copenhagen)

  • Agnete Larsen

    (Aarhus University)

  • Rasmus H. Olesen

    (Aarhus University)

  • Claus Yding Andersen

    (University Hospital of Copenhagen, University of Copenhagen)

  • Lea Langhoff Thuesen

    (Hvidovre University Hospital)

  • Kristine Juul Hare

    (Hvidovre University Hospital)

  • Tune H. Pers

    (University of Copenhagen)

  • Konstantin Khodosevich

    (University of Copenhagen)

  • Benjamin D. Simons

    (University of Cambridge
    University of Cambridge
    University of Cambridge)

  • Kim B. Jensen

    (University of Copenhagen
    University of Copenhagen)

Abstract

Adult intestinal stem cells are located at the bottom of crypts of Lieberkühn, where they express markers such as LGR51,2 and fuel the constant replenishment of the intestinal epithelium1. Although fetal LGR5-expressing cells can give rise to adult intestinal stem cells3,4, it remains unclear whether this population in the patterned epithelium represents unique intestinal stem-cell precursors. Here we show, using unbiased quantitative lineage-tracing approaches, biophysical modelling and intestinal transplantation, that all cells of the mouse intestinal epithelium—irrespective of their location and pattern of LGR5 expression in the fetal gut tube—contribute actively to the adult intestinal stem cell pool. Using 3D imaging, we find that during fetal development the villus undergoes gross remodelling and fission. This brings epithelial cells from the non-proliferative villus into the proliferative intervillus region, which enables them to contribute to the adult stem-cell niche. Our results demonstrate that large-scale remodelling of the intestinal wall and cell-fate specification are closely linked. Moreover, these findings provide a direct link between the observed plasticity and cellular reprogramming of differentiating cells in adult tissues following damage5–9, revealing that stem-cell identity is an induced rather than a hardwired property.

Suggested Citation

  • Jordi Guiu & Edouard Hannezo & Shiro Yui & Samuel Demharter & Svetlana Ulyanchenko & Martti Maimets & Anne Jørgensen & Signe Perlman & Lene Lundvall & Linn Salto Mamsen & Agnete Larsen & Rasmus H. Ole, 2019. "Tracing the origin of adult intestinal stem cells," Nature, Nature, vol. 570(7759), pages 107-111, June.
    • Handle: RePEc:nat:nature:v:570:y:2019:i:7759:d:10.1038_s41586-019-1212-5
    DOI: 10.1038/s41586-019-1212-5
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    Cited by:

    1. Feng Lin & Xia Li & Shiyu Sun & Zhongyi Li & Chenglin Lv & Jianbo Bai & Lin Song & Yizhao Han & Bo Li & Jianping Fu & Yue Shao, 2023. "Mechanically enhanced biogenesis of gut spheroids with instability-driven morphomechanics," Nature Communications, Nature, vol. 14(1), pages 1-15, 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. Martti Maimets & Marianne Terndrup Pedersen & Jordi Guiu & Jes Dreier & Malte Thodberg & Yasuko Antoku & Pawel J. Schweiger & Leonor Rib & Raul Bardini Bressan & Yi Miao & K. Christopher Garcia & Albi, 2022. "Mesenchymal-epithelial crosstalk shapes intestinal regionalisation via Wnt and Shh signalling," Nature Communications, Nature, vol. 13(1), pages 1-12, December.

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