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

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 Salagaras; Aaron Long; Jan Kazenwadel; Natasha L. Harvey; Grant R. Drummond; Antony Vinh; Vashe Chandrakanthan; Ashish Misra; Zoltan Neufeld; Joanne T.M. Tan; Luciano Martelotto; Jose M. Polo; Claudine S. Bonder; Alexander R. Pinto; Shiwani Sharma; Stephen J. Nicholls; Christina A. Bursill; Peter J. Psaltis

doi:10.1038/s41467-024-51637-7

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

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 Salagaras, Aaron Long, Jan Kazenwadel, Natasha L. Harvey, Grant R. Drummond, Antony Vinh, Vashe Chandrakanthan, Ashish Misra, Zoltan Neufeld, Joanne T.M. Tan, Luciano MartelottoJose M. Polo, Claudine S. Bonder, Alexander R. Pinto, Shiwani Sharma, Stephen J. Nicholls, Christina A. Bursill, Peter J. Psaltis

Research output: Contribution to journal › Article › peer-review

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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.

Original language	English
Article number	7097
Journal	Nature Communications
Volume	15
Issue number	1
DOIs	https://doi.org/10.1038/s41467-024-51637-7
Publication status	Published or Issued - 17 Aug 2024

ASJC Scopus subject areas

General Chemistry
General Biochemistry,Genetics and Molecular Biology
General Physics and Astronomy

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Williamson, A. E., Liyanage, S., Hassanshahi, M., Dona, M. S. I., Toledo-Flores, D., Tran, D. X. A., Dimasi, C., Schwarz, N., Fernando, S., Salagaras, T., Long, A., Kazenwadel, J., Harvey, N. L., Drummond, G. R., Vinh, A., Chandrakanthan, V., Misra, A., Neufeld, Z., Tan, J. T. M., ... Psaltis, P. J. (2024). Discovery of an embryonically derived bipotent population of endothelial-macrophage progenitor cells in postnatal aorta. Nature Communications, 15(1), Article 7097. https://doi.org/10.1038/s41467-024-51637-7

@article{271cf45d937e4bbb887f90a09f1ff6d8,

title = "Discovery of an embryonically derived bipotent population of endothelial-macrophage progenitor cells in postnatal aorta",

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.",

author = "Williamson, {Anna E.} and Sanuri Liyanage and Mohammadhossein Hassanshahi and Dona, {Malathi S.I.} and Deborah Toledo-Flores and Tran, {Dang X.A.} and Catherine Dimasi and Nisha Schwarz and Sanuja Fernando and Thalia Salagaras and Aaron Long and Jan Kazenwadel and Harvey, {Natasha L.} and Drummond, {Grant R.} and Antony Vinh and Vashe Chandrakanthan and Ashish Misra and Zoltan Neufeld and Tan, {Joanne T.M.} and Luciano Martelotto and Polo, {Jose M.} and Bonder, {Claudine S.} and Pinto, {Alexander R.} and Shiwani Sharma and Nicholls, {Stephen J.} and Bursill, {Christina A.} and Psaltis, {Peter J.}",

note = "Publisher Copyright: {\textcopyright} The Author(s) 2024.",

year = "2024",

month = aug,

day = "17",

doi = "10.1038/s41467-024-51637-7",

language = "English",

volume = "15",

journal = "Nature Communications",

issn = "2041-1723",

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Williamson, AE, Liyanage, S, Hassanshahi, M, Dona, MSI, Toledo-Flores, D, Tran, DXA, Dimasi, C, Schwarz, N, Fernando, S, Salagaras, T, Long, A, Kazenwadel, J, Harvey, NL, Drummond, GR, Vinh, A, Chandrakanthan, V, Misra, A, Neufeld, Z, Tan, JTM, Martelotto, L, Polo, JM, Bonder, CS, Pinto, AR, Sharma, S, Nicholls, SJ, Bursill, CA & Psaltis, PJ 2024, 'Discovery of an embryonically derived bipotent population of endothelial-macrophage progenitor cells in postnatal aorta', Nature Communications, vol. 15, no. 1, 7097. https://doi.org/10.1038/s41467-024-51637-7

TY - JOUR

T1 - Discovery of an embryonically derived bipotent population of endothelial-macrophage progenitor cells in postnatal aorta

AU - Williamson, Anna E.

AU - Liyanage, Sanuri

AU - Hassanshahi, Mohammadhossein

AU - Dona, Malathi S.I.

AU - Toledo-Flores, Deborah

AU - Tran, Dang X.A.

AU - Dimasi, Catherine

AU - Schwarz, Nisha

AU - Fernando, Sanuja

AU - Salagaras, Thalia

AU - Long, Aaron

AU - Kazenwadel, Jan

AU - Harvey, Natasha L.

AU - Drummond, Grant R.

AU - Vinh, Antony

AU - Chandrakanthan, Vashe

AU - Misra, Ashish

AU - Neufeld, Zoltan

AU - Tan, Joanne T.M.

AU - Martelotto, Luciano

AU - Polo, Jose M.

AU - Bonder, Claudine S.

AU - Pinto, Alexander R.

AU - Sharma, Shiwani

AU - Nicholls, Stephen J.

AU - Bursill, Christina A.

AU - Psaltis, Peter J.

PY - 2024/8/17

Y1 - 2024/8/17

N2 - 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.

AB - 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.

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U2 - 10.1038/s41467-024-51637-7

DO - 10.1038/s41467-024-51637-7

M3 - Article

AN - SCOPUS:85201424973

SN - 2041-1723

VL - 15

JO - Nature Communications

JF - Nature Communications

IS - 1

M1 - 7097

ER -

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

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