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

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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
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

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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

@article{dbe1fd7056c24bb5a413de9c188a99ed,

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.).",

year = "2016",

month = feb,

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doi = "10.1038/ni.3343",

language = "English",

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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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T1 - Self-renewing resident arterial macrophages arise from embryonic CX3CR1 + precursors and circulating monocytes immediately after birth

AU - Ensan, Sherine

AU - Li, Angela

AU - Besla, Rickvinder

AU - Degousee, Norbert

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.

AU - Epelman, Slava

AU - Gramolini, Anthony O.

AU - Cybulsky, Myron I.

AU - Rubin, Barry B.

AU - Robbins, Clinton S.

N1 - 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.).

PY - 2016/2/1

Y1 - 2016/2/1

N2 - 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.

AB - 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.

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U2 - 10.1038/ni.3343

DO - 10.1038/ni.3343

M3 - Article

C2 - 26642357

AN - SCOPUS:84955129407

SN - 1529-2908

VL - 17

SP - 159

EP - 168

JO - Nature immunology

JF - Nature immunology

IS - 2

ER -

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

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