Constant replenishment from circulating monocytes maintains the macrophage pool in the intestine of adult mice

Calum C Bain; Alberto Bravo-Blas; Charlotte L Scott; Elisa Gomez Perdiguero; Frederic Geissmann; Sandrine Henri; Bernard Malissen; Lisa C Osborne; David Artis; Allan McI Mowat

doi:10.1038/ni.2967

Constant replenishment from circulating monocytes maintains the macrophage pool in the intestine of adult mice

Calum C Bain, Alberto Bravo-Blas, Charlotte L Scott, Elisa Gomez Perdiguero, Frederic Geissmann, Sandrine Henri, Bernard Malissen, Lisa C Osborne, David Artis, Allan McI Mowat

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

Abstract / Description of output

The paradigm that macrophages that reside in steady-state tissues are derived from embryonic precursors has never been investigated in the intestine, which contains the largest pool of macrophages. Using fate-mapping models and monocytopenic mice, together with bone marrow chimera and parabiotic models, we found that embryonic precursor cells seeded the intestinal mucosa and demonstrated extensive in situ proliferation during the neonatal period. However, these cells did not persist in the intestine of adult mice. Instead, they were replaced around the time of weaning by the chemokine receptor CCR2–dependent influx of Ly6C^hi monocytes that differentiated locally into mature, anti-inflammatory macrophages. This process was driven largely by the microbiota and had to be continued throughout adult life to maintain a normal intestinal macrophage pool.

Original language	English
Pages (from-to)	929-937
Number of pages	9
Journal	Nature Immunology
Volume	15
Issue number	10
Early online date	24 Aug 2014
DOIs	https://doi.org/10.1038/ni.2967
Publication status	Published - Oct 2014

Keywords / Materials (for Non-textual outputs)

Animals
Animals, Newborn
Antigens, CD11b
Antigens, Differentiation
Antigens, Ly
Bone Marrow Transplantation
Cell Differentiation
Cell Proliferation
Flow Cytometry
Gene Expression
Intestinal Mucosa
Intestines
Macrophages
Mice, Inbred C57BL
Mice, Knockout
Mice, Transgenic
Models, Immunological
Monocytes
Parabiosis
Receptors, CCR2
Receptors, Chemokine
Reverse Transcriptase Polymerase Chain Reaction
Time Factors

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10.1038/ni.2967

Calum Bain
- Deanery of Clinical Sciences - Senior Lecturer
- Centre for Inflammation Research
Person: Academic: Research Active

Cite this

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title = "Constant replenishment from circulating monocytes maintains the macrophage pool in the intestine of adult mice",

abstract = "The paradigm that macrophages that reside in steady-state tissues are derived from embryonic precursors has never been investigated in the intestine, which contains the largest pool of macrophages. Using fate-mapping models and monocytopenic mice, together with bone marrow chimera and parabiotic models, we found that embryonic precursor cells seeded the intestinal mucosa and demonstrated extensive in situ proliferation during the neonatal period. However, these cells did not persist in the intestine of adult mice. Instead, they were replaced around the time of weaning by the chemokine receptor CCR2–dependent influx of Ly6Chi monocytes that differentiated locally into mature, anti-inflammatory macrophages. This process was driven largely by the microbiota and had to be continued throughout adult life to maintain a normal intestinal macrophage pool.",

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author = "Bain, {Calum C} and Alberto Bravo-Blas and Scott, {Charlotte L} and {Gomez Perdiguero}, Elisa and Frederic Geissmann and Sandrine Henri and Bernard Malissen and Osborne, {Lisa C} and David Artis and Mowat, {Allan McI}",

year = "2014",

month = oct,

doi = "10.1038/ni.2967",

language = "English",

volume = "15",

pages = "929--937",

journal = "Nature Immunology",

issn = "1529-2908",

publisher = "Nature Publishing Group",

number = "10",

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TY - JOUR

T1 - Constant replenishment from circulating monocytes maintains the macrophage pool in the intestine of adult mice

AU - Bain, Calum C

AU - Bravo-Blas, Alberto

AU - Scott, Charlotte L

AU - Gomez Perdiguero, Elisa

AU - Geissmann, Frederic

AU - Henri, Sandrine

AU - Malissen, Bernard

AU - Osborne, Lisa C

AU - Artis, David

AU - Mowat, Allan McI

PY - 2014/10

Y1 - 2014/10

N2 - The paradigm that macrophages that reside in steady-state tissues are derived from embryonic precursors has never been investigated in the intestine, which contains the largest pool of macrophages. Using fate-mapping models and monocytopenic mice, together with bone marrow chimera and parabiotic models, we found that embryonic precursor cells seeded the intestinal mucosa and demonstrated extensive in situ proliferation during the neonatal period. However, these cells did not persist in the intestine of adult mice. Instead, they were replaced around the time of weaning by the chemokine receptor CCR2–dependent influx of Ly6Chi monocytes that differentiated locally into mature, anti-inflammatory macrophages. This process was driven largely by the microbiota and had to be continued throughout adult life to maintain a normal intestinal macrophage pool.

AB - The paradigm that macrophages that reside in steady-state tissues are derived from embryonic precursors has never been investigated in the intestine, which contains the largest pool of macrophages. Using fate-mapping models and monocytopenic mice, together with bone marrow chimera and parabiotic models, we found that embryonic precursor cells seeded the intestinal mucosa and demonstrated extensive in situ proliferation during the neonatal period. However, these cells did not persist in the intestine of adult mice. Instead, they were replaced around the time of weaning by the chemokine receptor CCR2–dependent influx of Ly6Chi monocytes that differentiated locally into mature, anti-inflammatory macrophages. This process was driven largely by the microbiota and had to be continued throughout adult life to maintain a normal intestinal macrophage pool.

KW - Animals

KW - Animals, Newborn

KW - Antigens, CD11b

KW - Antigens, Differentiation

KW - Antigens, Ly

KW - Bone Marrow Transplantation

KW - Cell Differentiation

KW - Cell Proliferation

KW - Flow Cytometry

KW - Gene Expression

KW - Intestinal Mucosa

KW - Intestines

KW - Macrophages

KW - Mice, Inbred C57BL

KW - Mice, Knockout

KW - Mice, Transgenic

KW - Models, Immunological

KW - Monocytes

KW - Parabiosis

KW - Receptors, CCR2

KW - Receptors, Chemokine

KW - Reverse Transcriptase Polymerase Chain Reaction

KW - Time Factors

U2 - 10.1038/ni.2967

DO - 10.1038/ni.2967

M3 - Article

C2 - 25151491

SN - 1529-2908

VL - 15

SP - 929

EP - 937

JO - Nature Immunology

JF - Nature Immunology

IS - 10

ER -

Constant replenishment from circulating monocytes maintains the macrophage pool in the intestine of adult mice

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Keywords / Materials (for Non-textual outputs)

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Calum Bain

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