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Discovery of an embryonically derived bipotent population of endothelial-macrophage progenitor cells in postnatal aorta

Author

Listed:
  • Anna E. Williamson

    (South Australian Health and Medical Research Institute
    The University of Adelaide)

  • Sanuri Liyanage

    (South Australian Health and Medical Research Institute
    The University of Adelaide)

  • Mohammadhossein Hassanshahi

    (South Australian Health and Medical Research Institute
    The University of Adelaide)

  • Malathi S. I. Dona

    (Baker Heart and Diabetes Institute)

  • Deborah Toledo-Flores

    (South Australian Health and Medical Research Institute)

  • Dang X. A. Tran

    (South Australian Health and Medical Research Institute)

  • Catherine Dimasi

    (South Australian Health and Medical Research Institute)

  • Nisha Schwarz

    (South Australian Health and Medical Research Institute)

  • Sanuja Fernando

    (South Australian Health and Medical Research Institute
    The University of Adelaide)

  • Thalia Salagaras

    (South Australian Health and Medical Research Institute)

  • Aaron Long

    (South Australian Health and Medical Research Institute
    Central Adelaide Local Health Network)

  • Jan Kazenwadel

    (University of South Australia and SA Pathology)

  • Natasha L. Harvey

    (The University of Adelaide
    University of South Australia and SA Pathology)

  • Grant R. Drummond

    (La Trobe University)

  • Antony Vinh

    (La Trobe University)

  • Vashe Chandrakanthan

    (The University of Adelaide
    University of New South Wales
    South Australian Health and Medical Research Institute)

  • Ashish Misra

    (University of Sydney and Heart Research Institute)

  • Zoltan Neufeld

    (The University of Queensland)

  • Joanne T. M. Tan

    (South Australian Health and Medical Research Institute
    The University of Adelaide)

  • Luciano Martelotto

    (The University of Adelaide)

  • Jose M. Polo

    (The University of Adelaide)

  • Claudine S. Bonder

    (University of South Australia and SA Pathology)

  • Alexander R. Pinto

    (Baker Heart and Diabetes Institute
    La Trobe University)

  • Shiwani Sharma

    (South Australian Health and Medical Research Institute
    Flinders University)

  • Stephen J. Nicholls

    (Monash University)

  • Christina A. Bursill

    (South Australian Health and Medical Research Institute
    The University of Adelaide)

  • Peter J. Psaltis

    (South Australian Health and Medical Research Institute
    The University of Adelaide
    Central Adelaide Local Health Network)

Abstract

Converging evidence indicates that extra-embryonic yolk sac is the source of both macrophages and endothelial cells in adult mouse tissues. Prevailing views are that these embryonically derived cells are maintained after birth by proliferative self-renewal in their differentiated states. Here we identify clonogenic endothelial-macrophage (EndoMac) progenitor cells in the adventitia of embryonic and postnatal mouse aorta, that are independent of Flt3-mediated bone marrow hematopoiesis and derive from an early embryonic CX3CR1+ and CSF1R+ source. These bipotent progenitors are proliferative and vasculogenic, contributing to adventitial neovascularization and formation of perfused blood vessels after transfer into ischemic tissue. We establish a regulatory role for angiotensin II, which enhances their clonogenic and differentiation properties and rapidly stimulates their proliferative expansion in vivo. Our findings demonstrate that embryonically derived EndoMac progenitors participate in local vasculogenic responses in the aortic wall by contributing to the expansion of endothelial cells and macrophages postnatally.

Suggested Citation

  • Anna E. Williamson & Sanuri Liyanage & Mohammadhossein Hassanshahi & Malathi S. I. Dona & Deborah Toledo-Flores & Dang X. A. Tran & Catherine Dimasi & Nisha Schwarz & Sanuja Fernando & Thalia Salagara, 2024. "Discovery of an embryonically derived bipotent population of endothelial-macrophage progenitor cells in postnatal aorta," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-51637-7
    DOI: 10.1038/s41467-024-51637-7
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    References listed on IDEAS

    as
    1. Alice Plein & Alessandro Fantin & Laura Denti & Jeffrey W. Pollard & Christiana Ruhrberg, 2018. "Erythro-myeloid progenitors contribute endothelial cells to blood vessels," Nature, Nature, vol. 562(7726), pages 223-228, October.
    2. Elisa Gomez Perdiguero & Kay Klapproth & Christian Schulz & Katrin Busch & Emanuele Azzoni & Lucile Crozet & Hannah Garner & Celine Trouillet & Marella F. de Bruijn & Frederic Geissmann & Hans-Reimer , 2015. "Tissue-resident macrophages originate from yolk-sac-derived erythro-myeloid progenitors," Nature, Nature, vol. 518(7540), pages 547-551, February.
    3. Igor M. Samokhvalov & Natalia I. Samokhvalova & Shin-ichi Nishikawa, 2007. "Cell tracing shows the contribution of the yolk sac to adult haematopoiesis," Nature, Nature, vol. 446(7139), pages 1056-1061, April.
    4. Jean-Charles Boisset & Wiggert van Cappellen & Charlotte Andrieu-Soler & Niels Galjart & Elaine Dzierzak & Catherine Robin, 2010. "In vivo imaging of haematopoietic cells emerging from the mouse aortic endothelium," Nature, Nature, vol. 464(7285), pages 116-120, March.
    Full references (including those not matched with items on IDEAS)

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