Self-renewing resident arterial macrophages arise from embryonic CX3CR1 + precursors and circulating monocytes immediately after birth

Sherine Ensan; Angela Li; Rickvinder Besla; Norbert Degousee; Jake Cosme; Mark Roufaiel; Eric A. Shikatani; Mahmoud El-Maklizi; Jesse W. Williams; Lauren Robins; Cedric Li; Bonnie Lewis; Tae Jin Yun; Jun Seong Lee; Peter Wieghofer; Ramzi Khattar; Kaveh Farrokhi; John Byrne; Maral Ouzounian; Caleb C.J. Zavitz; Gary A. Levy; Carla M.T. Bauer; Peter Libby; Mansoor Husain; Filip K. Swirski; Cheolho Cheong; Marco Prinz; Ingo Hilgendorf; Gwendalyn J. Randolph; Slava Epelman; Anthony O. Gramolini; Myron I. Cybulsky; Barry B. Rubin; Clinton S. Robbins

doi:10.1038/ni.3343

Self-renewing resident arterial macrophages arise from embryonic CX3CR1 + precursors and circulating monocytes immediately after birth

Sherine Ensan, Angela Li, Rickvinder Besla, Norbert Degousee, Jake Cosme, Mark Roufaiel, Eric A. Shikatani, Mahmoud El-Maklizi, Jesse W. Williams, Lauren Robins, Cedric Li, Bonnie Lewis, Tae Jin Yun, Jun Seong Lee, Peter Wieghofer, Ramzi Khattar, Kaveh Farrokhi, John Byrne, Maral Ouzounian, Caleb C.J. ZavitzGary A. Levy, Carla M.T. Bauer, Peter Libby, Mansoor Husain, Filip K. Swirski, Cheolho Cheong, Marco Prinz, Ingo Hilgendorf, Gwendalyn J. Randolph, Slava Epelman, Anthony O. Gramolini, Myron I. Cybulsky, Barry B. Rubin, Clinton S. Robbins

Pediatric Genetics & Metabolism

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

266 Scopus citations

Abstract

Resident macrophages densely populate the normal arterial wall, yet their origins and the mechanisms that sustain them are poorly understood. Here we use gene-expression profiling to show that arterial macrophages constitute a distinct population among macrophages. Using multiple fate-mapping approaches, we show that arterial macrophages arise embryonically from CX3CR1 + precursors and postnatally from bone marrow-derived monocytes that colonize the tissue immediately after birth. In adulthood, proliferation (rather than monocyte recruitment) sustains arterial macrophages in the steady state and after severe depletion following sepsis. After infection, arterial macrophages return rapidly to functional homeostasis. Finally, survival of resident arterial macrophages depends on a CX3CR1-CX3CL1 axis within the vascular niche.

Original language	English (US)
Pages (from-to)	159-168
Number of pages	10
Journal	Nature immunology
Volume	17
Issue number	2
DOIs	https://doi.org/10.1038/ni.3343
State	Published - Feb 1 2016

Bibliographical note

Funding Information:
We acknowledge the administrative assistance of B. Bali. Supported by a Canadian Institutes of Health Research (CIHR) New Investigator Award (MSH136670), a CIHR operating grant (MOP133390), an Ontario Lung Association/Pfizer Award and the Peter Munk Chair in Aortic Disease Research (C.S.R.) and an Ontario Graduate Scholarship (S.E.).

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10.1038/ni.3343

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Ensan, S., Li, A., Besla, R., Degousee, N., Cosme, J., Roufaiel, M., Shikatani, E. A., El-Maklizi, M., Williams, J. W., Robins, L., Li, C., Lewis, B., Yun, T. J., Lee, J. S., Wieghofer, P., Khattar, R., Farrokhi, K., Byrne, J., Ouzounian, M., ... Robbins, C. S. (2016). Self-renewing resident arterial macrophages arise from embryonic CX3CR1 + precursors and circulating monocytes immediately after birth. Nature immunology, 17(2), 159-168. https://doi.org/10.1038/ni.3343

Ensan, S, Li, A, Besla, R, Degousee, N, Cosme, J, Roufaiel, M, Shikatani, EA, El-Maklizi, M, Williams, JW, Robins, L, Li, C, Lewis, B, Yun, TJ, Lee, JS, Wieghofer, P, Khattar, R, Farrokhi, K, Byrne, J, Ouzounian, M, Zavitz, CCJ, Levy, GA, Bauer, CMT, Libby, P, Husain, M, Swirski, FK, Cheong, C, Prinz, M, Hilgendorf, I, Randolph, GJ, Epelman, S, Gramolini, AO, Cybulsky, MI, Rubin, BB & Robbins, CS 2016, 'Self-renewing resident arterial macrophages arise from embryonic CX3CR1 + precursors and circulating monocytes immediately after birth', Nature immunology, vol. 17, no. 2, pp. 159-168. https://doi.org/10.1038/ni.3343

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title = "Self-renewing resident arterial macrophages arise from embryonic CX3CR1 + precursors and circulating monocytes immediately after birth",

abstract = "Resident macrophages densely populate the normal arterial wall, yet their origins and the mechanisms that sustain them are poorly understood. Here we use gene-expression profiling to show that arterial macrophages constitute a distinct population among macrophages. Using multiple fate-mapping approaches, we show that arterial macrophages arise embryonically from CX3CR1 + precursors and postnatally from bone marrow-derived monocytes that colonize the tissue immediately after birth. In adulthood, proliferation (rather than monocyte recruitment) sustains arterial macrophages in the steady state and after severe depletion following sepsis. After infection, arterial macrophages return rapidly to functional homeostasis. Finally, survival of resident arterial macrophages depends on a CX3CR1-CX3CL1 axis within the vascular niche.",

author = "Sherine Ensan and Angela Li and Rickvinder Besla and Norbert Degousee and Jake Cosme and Mark Roufaiel and Shikatani, {Eric A.} and Mahmoud El-Maklizi and Williams, {Jesse W.} and Lauren Robins and Cedric Li and Bonnie Lewis and Yun, {Tae Jin} and Lee, {Jun Seong} and Peter Wieghofer and Ramzi Khattar and Kaveh Farrokhi and John Byrne and Maral Ouzounian and Zavitz, {Caleb C.J.} and Levy, {Gary A.} and Bauer, {Carla M.T.} and Peter Libby and Mansoor Husain and Swirski, {Filip K.} and Cheolho Cheong and Marco Prinz and Ingo Hilgendorf and Randolph, {Gwendalyn J.} and Slava Epelman and Gramolini, {Anthony O.} and Cybulsky, {Myron I.} and Rubin, {Barry B.} and Robbins, {Clinton S.}",

note = "Funding Information: We acknowledge the administrative assistance of B. Bali. Supported by a Canadian Institutes of Health Research (CIHR) New Investigator Award (MSH136670), a CIHR operating grant (MOP133390), an Ontario Lung Association/Pfizer Award and the Peter Munk Chair in Aortic Disease Research (C.S.R.) and an Ontario Graduate Scholarship (S.E.).",

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AU - Cosme, Jake

AU - Roufaiel, Mark

AU - Shikatani, Eric A.

AU - El-Maklizi, Mahmoud

AU - Williams, Jesse W.

AU - Robins, Lauren

AU - Li, Cedric

AU - Lewis, Bonnie

AU - Yun, Tae Jin

AU - Lee, Jun Seong

AU - Wieghofer, Peter

AU - Khattar, Ramzi

AU - Farrokhi, Kaveh

AU - Byrne, John

AU - Ouzounian, Maral

AU - Zavitz, Caleb C.J.

AU - Levy, Gary A.

AU - Bauer, Carla M.T.

AU - Libby, Peter

AU - Husain, Mansoor

AU - Swirski, Filip K.

AU - Cheong, Cheolho

AU - Prinz, Marco

AU - Hilgendorf, Ingo

AU - Randolph, Gwendalyn J.

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AU - Gramolini, Anthony O.

AU - Cybulsky, Myron I.

AU - Rubin, Barry B.

AU - Robbins, Clinton S.

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Self-renewing resident arterial macrophages arise from embryonic CX3CR1 + precursors and circulating monocytes immediately after birth

Abstract

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