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Bone marrow-derived monocytes give rise to self-renewing and fully differentiated Kupffer cells

Author

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  • Charlotte L. Scott

    (Unit of Immunoregulation and Mucosal Immunology, VIB Inflammation Research Center
    Ghent University)

  • Fang Zheng

    (Myeloid Cell Immunology, VIB
    Cellular and Molecular Immunology Research Group, Vrije Universiteit Brussel
    Present Address: Department of Biochemistry and Molecular Biology, Health Science Center, Xi’an Jiaotong University, Xi’an 710049, China)

  • Patrick De Baetselier

    (Myeloid Cell Immunology, VIB
    Cellular and Molecular Immunology Research Group, Vrije Universiteit Brussel)

  • Liesbet Martens

    (Unit of Immunoregulation and Mucosal Immunology, VIB Inflammation Research Center
    Ghent University)

  • Yvan Saeys

    (Unit of Immunoregulation and Mucosal Immunology, VIB Inflammation Research Center
    Ghent University)

  • Sofie De Prijck

    (Unit of Immunoregulation and Mucosal Immunology, VIB Inflammation Research Center
    Ghent University)

  • Saskia Lippens

    (Ghent University
    VIB Bio Imaging Core
    Microscopy Core Facility, VIB, Inflammation Research Center)

  • Chloé Abels

    (Myeloid Cell Immunology, VIB
    Cellular and Molecular Immunology Research Group, Vrije Universiteit Brussel)

  • Steve Schoonooghe

    (Myeloid Cell Immunology, VIB
    Cellular and Molecular Immunology Research Group, Vrije Universiteit Brussel)

  • Geert Raes

    (Myeloid Cell Immunology, VIB
    Cellular and Molecular Immunology Research Group, Vrije Universiteit Brussel)

  • Nick Devoogdt

    (Cellular and Molecular Immunology Research Group, Vrije Universiteit Brussel
    In Vivo Cellular and Molecular Imaging Research Group, Vrije Universiteit Brussel)

  • Bart N. Lambrecht

    (Unit of Immunoregulation and Mucosal Immunology, VIB Inflammation Research Center
    Ghent University)

  • Alain Beschin

    (Myeloid Cell Immunology, VIB
    Cellular and Molecular Immunology Research Group, Vrije Universiteit Brussel)

  • Martin Guilliams

    (Unit of Immunoregulation and Mucosal Immunology, VIB Inflammation Research Center
    Ghent University)

Abstract

Self-renewing tissue-resident macrophages are thought to be exclusively derived from embryonic progenitors. However, whether circulating monocytes can also give rise to such macrophages has not been formally investigated. Here we use a new model of diphtheria toxin-mediated depletion of liver-resident Kupffer cells to generate niche availability and show that circulating monocytes engraft in the liver, gradually adopt the transcriptional profile of their depleted counterparts and become long-lived self-renewing cells. Underlining the physiological relevance of our findings, circulating monocytes also contribute to the expanding pool of macrophages in the liver shortly after birth, when macrophage niches become available during normal organ growth. Thus, like embryonic precursors, monocytes can and do give rise to self-renewing tissue-resident macrophages if the niche is available to them.

Suggested Citation

  • Charlotte L. Scott & Fang Zheng & Patrick De Baetselier & Liesbet Martens & Yvan Saeys & Sofie De Prijck & Saskia Lippens & Chloé Abels & Steve Schoonooghe & Geert Raes & Nick Devoogdt & Bart N. Lambr, 2016. "Bone marrow-derived monocytes give rise to self-renewing and fully differentiated Kupffer cells," Nature Communications, Nature, vol. 7(1), pages 1-10, April.
  • Handle: RePEc:nat:natcom:v:7:y:2016:i:1:d:10.1038_ncomms10321
    DOI: 10.1038/ncomms10321
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    Cited by:

    1. Stacy K. Thomas & Max M. Wattenberg & Shaanti Choi-Bose & Mark Uhlik & Ben Harrison & Heather Coho & Christopher R. Cassella & Meredith L. Stone & Dhruv Patel & Kelly Markowitz & Devora Delman & Micha, 2023. "Kupffer cells prevent pancreatic ductal adenocarcinoma metastasis to the liver in mice," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    2. Franziska Hildebrandt & Alma Andersson & Sami Saarenpää & Ludvig Larsson & Noémi Van Hul & Sachie Kanatani & Jan Masek & Ewa Ellis & Antonio Barragan & Annelie Mollbrink & Emma R. Andersson & Joakim L, 2021. "Spatial Transcriptomics to define transcriptional patterns of zonation and structural components in the mouse liver," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    3. Rebecca Fima & Sébastien Dussaud & Cheïma Benbida & Margault Blanchet & François Lanthiez & Lucie Poupel & Claudia Brambilla & Adélaïde Gélineau & Mattia Dessena & Marina Blanc & Cédric Lerévérend & M, 2024. "Loss of embryonically-derived Kupffer cells during hypercholesterolemia accelerates atherosclerosis development," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    4. Inhye Park & Michael E. Goddard & Jennifer E. Cole & Natacha Zanin & Leo-Pekka Lyytikäinen & Terho Lehtimäki & Evangelos Andreakos & Marc Feldmann & Irina Udalova & Ignat Drozdov & Claudia Monaco, 2022. "C-type lectin receptor CLEC4A2 promotes tissue adaptation of macrophages and protects against atherosclerosis," Nature Communications, Nature, vol. 13(1), pages 1-17, December.

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