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Macrophages (Mϕs) in the large intestine are crucial effectors of inflammatory bowel disease, but are also essential for homeostasis. It is unclear if these reflect separate populations of Mϕs or if resident Mϕs change during inflammation. In this study, we identify two subsets of colonic Mϕs in mice, whose proportions differ in healthy and inflamed intestine. Under resting conditions, most F4/80+ Mϕs are TLR− CCR2− CX3CR1 hi and do not produce TNF-α in response to stimulation. The lack of TLR expression is stable, affects all TLRs, and is determined both transcriptionally and posttranscriptionally. During experimental colitis, TLR2+ CCR2+ CX3CR1 int Ly6C hi Gr-1+, TNF-α–producing Mϕs come to dominate, and some of these are also present in the normal colon. The TLR2+ and TLR2− subsets are phenotypically distinct and have different turnover kinetics in vivo, and these properties are not influenced by the …