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PMID: 25959063 Published · epublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

IL-10-producing intestinal macrophages prevent excessive antibacterial innate immunity by limiting IL-23 synthesis.

Nature communications ·Vol. 6 ·2015-05-11 ·Pages 7055

Krause P, Morris V, Greenbaum JA, Park Y, Bjoerheden U, Mikulski Z, Muffley T, Shui JW, Kim G, Cheroutre H, Liu YC, Peters B, Kronenberg M, Murai M

Abstract

Innate immune responses are regulated in the intestine to prevent excessive inflammation. Here we show that a subset of mouse colonic macrophages constitutively produce the anti-inflammatory cytokine IL-10. In mice infected with Citrobacter rodentium, a model for enteropathogenic Escherichia coli infection in humans, these macrophages are required to prevent intestinal pathology. IL-23 is significantly increased in infected mice with a myeloid cell-specific deletion of IL-10, and the addition of IL-10 reduces IL-23 production by intestinal macrophages. Furthermore, blockade of IL-23 leads to reduced mortality in the context of macrophage IL-10 deficiency. Transcriptome and other analyses indicate that IL-10-expressing macrophages receive an autocrine IL-10 signal. Interestingly, only transfer of the IL-10 positive macrophages could rescue IL-10-deficient infected mice. Therefore, these data indicate a pivotal role for intestinal macrophages that constitutively produce IL-10, in controlling excessive innate immune activation and preventing tissue damage after an acute bacterial infection.

MeSH Terms
Animals Bone Marrow Cells/physiology Caspase 1/genetics,metabolism Female Gene Expression Regulation/physiology Immunity, Innate/physiology Interleukin-10/genetics,metabolism Interleukin-1beta/genetics,metabolism Interleukin-23/genetics,metabolism Intestines/cytology Macrophages/metabolism Male Mice Mice, Inbred Strains Mice, Knockout Osmotic Pressure Sodium Chloride, Dietary/administration & dosage,toxicity Stress, Physiological Th17 Cells
Chemicals
IL10 protein, mouse Interleukin-1beta Interleukin-23 Sodium Chloride, Dietary Interleukin-10 Caspase 1
Authors & Affiliations
14 authors, click to expand affiliations / ORCID
Krause Petra
Division of Developmental Immunology, La Jolla Institute for Allergy and Immunology, 9420 Athena Circle, La Jolla, California 92037, USA.
Morris Venetia
Division of Developmental Immunology, La Jolla Institute for Allergy and Immunology, 9420 Athena Circle, La Jolla, California 92037, USA.
Greenbaum Jason A
Bioinformatics Core Facility, La Jolla Institute for Allergy and Immunology, 9420 Athena Circle, La Jolla, California 92037, USA.
Park Yoon
Division of Cell Biology, La Jolla Institute for Allergy and Immunology, 9420 Athena Circle, La Jolla, California 92037, USA.
Bjoerheden Unni
Division of Developmental Immunology, La Jolla Institute for Allergy and Immunology, 9420 Athena Circle, La Jolla, California 92037, USA.
Mikulski Zbigniew ORCID
Microscopy Core Facility, La Jolla Institute for Allergy and Immunology, 9420 Athena Circle, La Jolla, California 92037, USA.
Muffley Tracy
Division of Developmental Immunology, La Jolla Institute for Allergy and Immunology, 9420 Athena Circle, La Jolla, California 92037, USA.
Shui Jr-Wen
Division of Developmental Immunology, La Jolla Institute for Allergy and Immunology, 9420 Athena Circle, La Jolla, California 92037, USA.
Kim Gisen
Division of Developmental Immunology, La Jolla Institute for Allergy and Immunology, 9420 Athena Circle, La Jolla, California 92037, USA.
Cheroutre Hilde
Division of Developmental Immunology, La Jolla Institute for Allergy and Immunology, 9420 Athena Circle, La Jolla, California 92037, USA.
Liu Yun-Cai
Division of Cell Biology, La Jolla Institute for Allergy and Immunology, 9420 Athena Circle, La Jolla, California 92037, USA.
Peters Bjoern ORCID
Division of Vaccine Discovery, La Jolla Institute for Allergy and Immunology, 9420 Athena Circle, La Jolla, California 92037, USA.
Kronenberg Mitchell
Division of Developmental Immunology, La Jolla Institute for Allergy and Immunology, 9420 Athena Circle, La Jolla, California 92037, USA.
Murai Masako ORCID
Division of Developmental Immunology, La Jolla Institute for Allergy and Immunology, 9420 Athena Circle, La Jolla, California 92037, USA.
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Article Info
Journal
Nature communications
Abbr.
Nat Commun
ISSN
2041-1723
Published
2015-05-11
Epub
2015-00-11
Pages
7055
Language
English
Region
England
NLM ID
101528555
PMCID
PMC4428691
Subset
IM
Grants
NCRR NIH HHS · S10 RR027366 · United States
NIAID NIH HHS · R21 AI091911 · United States
NIAID NIH HHS · P01 AI089624 · United States
NIAID NIH HHS · R01 AI050265 · United States
NIDDK NIH HHS · P01 DK046763 · United States
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