Distinct fate, dynamics and niches of renal macrophages of bone marrow or embryonic origins

Fengming Liu; Shen Dai; Dechun Feng; Zhongnan Qin; Xiao Peng; Siva S.V.P. Sakamuri; Mi Ren; Li Huang; Min Cheng; Kabir E. Mohammad; Ping Qu; Yong Chen; Chunling Zhao; Faliang Zhu; Shujian Liang; Bertal H. Aktas; Xiaofeng Yang; Hong Wang; Prasad V.G. Katakam; David W. Busija; Tracy Fischer; Prasun K. Datta; Jay Rappaport; Bin Gao; Xuebin Qin

doi:10.1038/s41467-020-16158-z

Distinct fate, dynamics and niches of renal macrophages of bone marrow or embryonic origins

Fengming Liu, Shen Dai, Dechun Feng, Zhongnan Qin, Xiao Peng, Siva S.V.P. Sakamuri, Mi Ren, Li Huang, Min Cheng, Kabir E. Mohammad, Ping Qu, Yong Chen, Chunling Zhao, Faliang Zhu, Shujian Liang, Bertal H. Aktas, Xiaofeng Yang, Hong Wang, Prasad V.G. Katakam, David W. BusijaTracy Fischer, Prasun K. Datta, Jay Rappaport, Bin Gao, Xuebin Qin

Nuclear Dynamics and Cancer (NDC)

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

80 Scopus citations

Abstract

Renal macrophages (RMs) participate in tissue homeostasis, inflammation and repair. RMs consist of embryo-derived (EMRMs) and bone marrow-derived RMs (BMRMs), but the fate, dynamics, replenishment, functions and metabolic states of these two RM populations remain unclear. Here we investigate and characterize RMs at different ages by conditionally labeling and ablating RMs populations in several transgenic lines. We find that RMs expand and mature in parallel with renal growth after birth, and are mainly derived from fetal liver monocytes before birth, but self-maintain through adulthood with contribution from peripheral monocytes. Moreover, after the RMs niche is emptied, peripheral monocytes rapidly differentiate into BMRMs, with the CX3CR1/CX3CL1 signaling axis being essential for the maintenance and regeneration of both EMRMs and BMRMs. Lastly, we show that EMRMs have a higher capacity for scavenging immune complex, and are more sensitive to immune challenge than BMRMs, with this difference associated with their distinct glycolytic capacities.

Original language	English
Article number	2280
Pages (from-to)	2280
Journal	Nature Communications
Volume	11
Issue number	1
DOIs	https://doi.org/10.1038/s41467-020-16158-z
State	Published - Dec 1 2020

Keywords

Animals
Bone Marrow Cells/cytology
CX3C Chemokine Receptor 1/metabolism
Cell Lineage
Chemokine CX3CL1/blood
Female
Fetus/cytology
Kidney/embryology
Liver/embryology
Macrophages/cytology
Male
Mice
Monocytes/cytology

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Liu, F., Dai, S., Feng, D., Qin, Z., Peng, X., Sakamuri, S. S. V. P., Ren, M., Huang, L., Cheng, M., Mohammad, K. E., Qu, P., Chen, Y., Zhao, C., Zhu, F., Liang, S., Aktas, B. H., Yang, X., Wang, H., Katakam, P. V. G., ... Qin, X. (2020). Distinct fate, dynamics and niches of renal macrophages of bone marrow or embryonic origins. Nature Communications, 11(1), 2280. Article 2280. https://doi.org/10.1038/s41467-020-16158-z

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title = "Distinct fate, dynamics and niches of renal macrophages of bone marrow or embryonic origins",

abstract = "Renal macrophages (RMs) participate in tissue homeostasis, inflammation and repair. RMs consist of embryo-derived (EMRMs) and bone marrow-derived RMs (BMRMs), but the fate, dynamics, replenishment, functions and metabolic states of these two RM populations remain unclear. Here we investigate and characterize RMs at different ages by conditionally labeling and ablating RMs populations in several transgenic lines. We find that RMs expand and mature in parallel with renal growth after birth, and are mainly derived from fetal liver monocytes before birth, but self-maintain through adulthood with contribution from peripheral monocytes. Moreover, after the RMs niche is emptied, peripheral monocytes rapidly differentiate into BMRMs, with the CX3CR1/CX3CL1 signaling axis being essential for the maintenance and regeneration of both EMRMs and BMRMs. Lastly, we show that EMRMs have a higher capacity for scavenging immune complex, and are more sensitive to immune challenge than BMRMs, with this difference associated with their distinct glycolytic capacities.",

keywords = "Animals, Bone Marrow Cells/cytology, CX3C Chemokine Receptor 1/metabolism, Cell Lineage, Chemokine CX3CL1/blood, Female, Fetus/cytology, Kidney/embryology, Liver/embryology, Macrophages/cytology, Male, Mice, Monocytes/cytology",

author = "Fengming Liu and Shen Dai and Dechun Feng and Zhongnan Qin and Xiao Peng and Sakamuri, {Siva S.V.P.} and Mi Ren and Li Huang and Min Cheng and Mohammad, {Kabir E.} and Ping Qu and Yong Chen and Chunling Zhao and Faliang Zhu and Shujian Liang and Aktas, {Bertal H.} and Xiaofeng Yang and Hong Wang and Katakam, {Prasad V.G.} and Busija, {David W.} and Tracy Fischer and Datta, {Prasun K.} and Jay Rappaport and Bin Gao and Xuebin Qin",

note = "Publisher Copyright: {\textcopyright} 2020, The Author(s).",

year = "2020",

month = dec,

day = "1",

doi = "10.1038/s41467-020-16158-z",

language = "English",

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journal = "Nature Communications",

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Liu, F, Dai, S, Feng, D, Qin, Z, Peng, X, Sakamuri, SSVP, Ren, M, Huang, L, Cheng, M, Mohammad, KE, Qu, P, Chen, Y, Zhao, C, Zhu, F, Liang, S, Aktas, BH, Yang, X, Wang, H, Katakam, PVG, Busija, DW, Fischer, T, Datta, PK, Rappaport, J, Gao, B & Qin, X 2020, 'Distinct fate, dynamics and niches of renal macrophages of bone marrow or embryonic origins', Nature Communications, vol. 11, no. 1, 2280, pp. 2280. https://doi.org/10.1038/s41467-020-16158-z

TY - JOUR

T1 - Distinct fate, dynamics and niches of renal macrophages of bone marrow or embryonic origins

AU - Liu, Fengming

AU - Dai, Shen

AU - Feng, Dechun

AU - Qin, Zhongnan

AU - Peng, Xiao

AU - Sakamuri, Siva S.V.P.

AU - Ren, Mi

AU - Huang, Li

AU - Cheng, Min

AU - Mohammad, Kabir E.

AU - Qu, Ping

AU - Chen, Yong

AU - Zhao, Chunling

AU - Zhu, Faliang

AU - Liang, Shujian

AU - Aktas, Bertal H.

AU - Yang, Xiaofeng

AU - Wang, Hong

AU - Katakam, Prasad V.G.

AU - Busija, David W.

AU - Fischer, Tracy

AU - Datta, Prasun K.

AU - Rappaport, Jay

AU - Gao, Bin

AU - Qin, Xuebin

PY - 2020/12/1

Y1 - 2020/12/1

N2 - Renal macrophages (RMs) participate in tissue homeostasis, inflammation and repair. RMs consist of embryo-derived (EMRMs) and bone marrow-derived RMs (BMRMs), but the fate, dynamics, replenishment, functions and metabolic states of these two RM populations remain unclear. Here we investigate and characterize RMs at different ages by conditionally labeling and ablating RMs populations in several transgenic lines. We find that RMs expand and mature in parallel with renal growth after birth, and are mainly derived from fetal liver monocytes before birth, but self-maintain through adulthood with contribution from peripheral monocytes. Moreover, after the RMs niche is emptied, peripheral monocytes rapidly differentiate into BMRMs, with the CX3CR1/CX3CL1 signaling axis being essential for the maintenance and regeneration of both EMRMs and BMRMs. Lastly, we show that EMRMs have a higher capacity for scavenging immune complex, and are more sensitive to immune challenge than BMRMs, with this difference associated with their distinct glycolytic capacities.

AB - Renal macrophages (RMs) participate in tissue homeostasis, inflammation and repair. RMs consist of embryo-derived (EMRMs) and bone marrow-derived RMs (BMRMs), but the fate, dynamics, replenishment, functions and metabolic states of these two RM populations remain unclear. Here we investigate and characterize RMs at different ages by conditionally labeling and ablating RMs populations in several transgenic lines. We find that RMs expand and mature in parallel with renal growth after birth, and are mainly derived from fetal liver monocytes before birth, but self-maintain through adulthood with contribution from peripheral monocytes. Moreover, after the RMs niche is emptied, peripheral monocytes rapidly differentiate into BMRMs, with the CX3CR1/CX3CL1 signaling axis being essential for the maintenance and regeneration of both EMRMs and BMRMs. Lastly, we show that EMRMs have a higher capacity for scavenging immune complex, and are more sensitive to immune challenge than BMRMs, with this difference associated with their distinct glycolytic capacities.

KW - Animals

KW - Bone Marrow Cells/cytology

KW - CX3C Chemokine Receptor 1/metabolism

KW - Cell Lineage

KW - Chemokine CX3CL1/blood

KW - Female

KW - Fetus/cytology

KW - Kidney/embryology

KW - Liver/embryology

KW - Macrophages/cytology

KW - Male

KW - Mice

KW - Monocytes/cytology

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U2 - 10.1038/s41467-020-16158-z

DO - 10.1038/s41467-020-16158-z

M3 - Article

C2 - 32385245

AN - SCOPUS:85084253680

SN - 2041-1723

VL - 11

SP - 2280

JO - Nature Communications

JF - Nature Communications

IS - 1

M1 - 2280

ER -

Distinct fate, dynamics and niches of renal macrophages of bone marrow or embryonic origins

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Keywords

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