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Long-lived self-renewing bone marrow-derived macrophages displace embryo-derived cells to inhabit adult serous cavities

Author

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  • Calum C. Bain

    (The University of Edinburgh/MRC Centre for Inflammation Research, Queens Medical Research Institute)

  • Catherine A. Hawley

    (The University of Edinburgh/MRC Centre for Inflammation Research, Queens Medical Research Institute)

  • Hannah Garner

    (Centre for Molecular and Cellular Biology of Inflammation (CMCBI))

  • Charlotte L. Scott

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

  • Anika Schridde

    (Institute of Infection, Immunity and Inflammation, University of Glasgow
    Institute of Molecular Medicine, RWTH University)

  • Nicholas J. Steers

    (The University of Edinburgh/MRC Centre for Inflammation Research, Queens Medical Research Institute
    Present address: Department of Medicine, Columbia University, 630 West 168th Street, New York, New York 10032-3784, USA.)

  • Matthias Mack

    (Department of Internal Medicine - Nephrology University Hospital Regensburg)

  • Anagha Joshi

    (The Roslin Institute and Royal (Dick) School of Veterinary Studies, Easter Bush Campus, University of Edinburgh)

  • Martin Guilliams

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

  • Allan Mc I. Mowat

    (Institute of Infection, Immunity and Inflammation, University of Glasgow)

  • Frederic Geissmann

    (Centre for Molecular and Cellular Biology of Inflammation (CMCBI)
    Immunology Program, Memorial Sloan Kettering Cancer Center
    Weill Cornell Graduate School of Medical Sciences)

  • Stephen J. Jenkins

    (The University of Edinburgh/MRC Centre for Inflammation Research, Queens Medical Research Institute)

Abstract

Peritoneal macrophages are one of the most studied macrophage populations in the body, yet the composition, developmental origin and mechanisms governing the maintenance of this compartment are controversial. Here we show resident F4/80hiGATA6+ macrophages are long-lived, undergo non-stochastic self-renewal and retain cells of embryonic origin for at least 4 months in mice. However, Ly6C+ monocytes constitutively enter the peritoneal cavity in a CCR2-dependent manner, where they mature into short-lived F4/80loMHCII+ cells that act, in part, as precursors of F4/80hiGATA6+ macrophages. Notably, monocyte-derived F4/80hi macrophages eventually displace the embryonic population with age in a process that is highly gender dependent and not due to proliferative exhaustion of the incumbent embryonic population, despite the greater proliferative activity of newly recruited cells. Furthermore, although monocyte-derived cells acquire key characteristics of the embryonic population, expression of Tim4 was impaired, leading to cumulative changes in the population with age.

Suggested Citation

  • Calum C. Bain & Catherine A. Hawley & Hannah Garner & Charlotte L. Scott & Anika Schridde & Nicholas J. Steers & Matthias Mack & Anagha Joshi & Martin Guilliams & Allan Mc I. Mowat & Frederic Geissman, 2016. "Long-lived self-renewing bone marrow-derived macrophages displace embryo-derived cells to inhabit adult serous cavities," Nature Communications, Nature, vol. 7(1), pages 1-14, September.
    • Handle: RePEc:nat:natcom:v:7:y:2016:i:1:d:10.1038_ncomms11852
    DOI: 10.1038/ncomms11852
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    Cited by:

    1. Jeonghyeon Kwon & Haruya Kawase & Kenny Mattonet & Stefan Guenther & Lisa Hahnefeld & Jamal Shamsara & Jan Heering & Michael Kurz & Sina Kirchhofer & Cornelius Krasel & Michaela Ulrich & Margherita Pe, 2025. "Orphan G protein-coupled receptor GPRC5B controls macrophage function by facilitating prostaglandin E receptor 2 signaling," Nature Communications, Nature, vol. 16(1), pages 1-23, December.
    2. Norika Liu & Naofumi Kawahira & Yasuhiro Nakashima & Haruko Nakano & Akiyasu Iwase & Yasunobu Uchijima & Mei Wang & Sean M. Wu & Susumu Minamisawa & Hiroki Kurihara & Atsushi Nakano, 2023. "Notch and retinoic acid signals regulate macrophage formation from endocardium downstream of Nkx2-5," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    3. Jennifer Gherardini & Youhei Uchida & Jonathan A Hardman & Jérémy Chéret & Kimberly Mace & Marta Bertolini & Ralf Paus, 2020. "Tissue-resident macrophages can be generated de novo in adult human skin from resident progenitor cells during substance P-mediated neurogenic inflammation ex vivo," PLOS ONE, Public Library of Science, vol. 15(1), pages 1-16, January.
    4. Mingming Zhao & Dragana Jankovic & Verena M. Link & Camila Oliveira Silva Souza & Katherine M. Hornick & Oyebola Oyesola & Yasmine Belkaid & Justin Lack & Png Loke, 2025. "Genetic variation in IL-4 activated tissue resident macrophages determines strain-specific synergistic responses to LPS epigenetically," Nature Communications, Nature, vol. 16(1), pages 1-20, December.

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