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Uncoupling of macrophage inflammation from self-renewal modulates host recovery from respiratory viral infection

Immunity (Cambridge, Mass.), 2021-06, Vol.54 (6), p.1200-1218.e9 [Peer Reviewed Journal]

2021 Elsevier Inc. ;Copyright © 2021 Elsevier Inc. All rights reserved. ;2021. Elsevier Inc. ;2021 Elsevier Inc. 2021 Elsevier Inc. ;ISSN: 1074-7613 ;EISSN: 1097-4180 ;DOI: 10.1016/j.immuni.2021.04.001 ;PMID: 33951416

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Title:
Uncoupling of macrophage inflammation from self-renewal modulates host recovery from respiratory viral infection
Author: Zhu, Bibo ; Wu, Yue ; Huang, Su ; Zhang, Ruixuan ; Son, Young Min ; Li, Chaofan ; Cheon, In Su ; Gao, Xiaochen ; Wang, Min ; Chen, Yao ; Zhou, Xian ; Nguyen, Quynh ; Phan, Anthony T. ; Behl, Supriya ; Taketo, M. Mark ; Mack, Matthias ; Shapiro, Virginia S. ; Zeng, Hu ; Ebihara, Hideki ; Mullon, John J. ; Edell, Eric S. ; Reisenauer, Janani S. ; Demirel, Nadir ; Kern, Ryan M. ; Chakraborty, Rana ; Cui, Weiguo ; Kaplan, Mark H. ; Zhou, Xiaobo ; Goldrath, Ananda W. ; Sun, Jie
Subjects: alveolar macrophages ; Alveoli ; Biomarkers ; Cancer ; Cell activation ; Cell growth ; Cell Self Renewal - immunology ; Chemokines ; COVID-19 ; COVID-19 - immunology ; COVID-19 - metabolism ; COVID-19 - virology ; Cytokines ; Cytokines - metabolism ; Disease Susceptibility - immunology ; Genes ; Glycolysis ; HIF-1α ; Homeostasis ; Host-Pathogen Interactions - immunology ; Humans ; Hypoxia-Inducible Factor 1, alpha Subunit - metabolism ; Hypoxia-inducible factor 1a ; Infections ; Inflammation ; Inflammation Mediators - metabolism ; Influenza ; influenza virus ; Ligands ; Lungs ; Macrophages ; Macrophages - cytology ; Macrophages - immunology ; Macrophages - metabolism ; Macrophages, Alveolar - immunology ; Macrophages, Alveolar - metabolism ; Medical treatment ; Metabolism ; Microorganisms ; Mitochondria ; Morbidity ; Neutrophils ; pulmonary inflammation ; Recovery ; Repopulation ; Respiratory diseases ; SARS-CoV-2 ; SARS-CoV-2 - immunology ; self-renewal ; Severe acute respiratory syndrome coronavirus 2 ; Signal Transduction ; Stem cells ; tissue macrophages ; tissue repair ; Tissues ; Tumor necrosis factor-TNF ; Viral infections ; Wnt protein ; Wound healing ; β-Catenin
Is Part Of: Immunity (Cambridge, Mass.), 2021-06, Vol.54 (6), p.1200-1218.e9
Description: Tissue macrophages self-renew during homeostasis and produce inflammatory mediators upon microbial infection. We examined the relationship between proliferative and inflammatory properties of tissue macrophages by defining the impact of the Wnt/β-catenin pathway, a central regulator of self-renewal, in alveolar macrophages (AMs). Activation of β-catenin by Wnt ligand inhibited AM proliferation and stemness, but promoted inflammatory activity. In a murine influenza viral pneumonia model, β-catenin-mediated AM inflammatory activity promoted acute host morbidity; in contrast, AM proliferation enabled repopulation of reparative AMs and tissue recovery following viral clearance. Mechanistically, Wnt treatment promoted β-catenin-HIF-1α interaction and glycolysis-dependent inflammation while suppressing mitochondrial metabolism and thereby, AM proliferation. Differential HIF-1α activities distinguished proliferative and inflammatory AMs in vivo. This β-catenin-HIF-1α axis was conserved in human AMs and enhanced HIF-1α expression associated with macrophage inflammation in COVID-19 patients. Thus, inflammatory and reparative activities of lung macrophages are regulated by β-catenin-HIF-1α signaling, with implications for the treatment of severe respiratory diseases. [Display omitted] •Wnt-β-catenin signaling modulates AM inflammation and self-renewal through HIF-1α•AM β-catenin and HIF-1α signaling promotes host diseases and inhibits lung recovery•HIF-1α activity separates AM inflammatory activity from proliferative potential in vivo•β-Catenin and HIF-1α signaling may contribute to severe disease development in COVID-19 Zhu et al. examine the relationship between proliferative and inflammatory properties of tissue macrophages by defining the impact of the Wnt-β-catenin pathway, a regulator of self-renewal, in alveolar macrophages (AMs). Their findings reveal a β-catenin-HIF-1α signaling axis that promotes inflammatory AMs at the expense of proliferation. This axis is conserved in human AMs, with implications for the treatment of severe respiratory diseases.
Publisher: United States: Elsevier Inc
Language: English
Identifier: ISSN: 1074-7613
EISSN: 1097-4180
DOI: 10.1016/j.immuni.2021.04.001
PMID: 33951416
Source: Cell Press Free Archives
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Uncoupling of macrophage inflammation from self-renewal modulates host recovery from respiratory viral infection

2021 Elsevier Inc. ;Copyright © 2021 Elsevier Inc. All rights reserved. ;2021. Elsevier Inc. ;2021 Elsevier Inc. 2021 Elsevier Inc. ;ISSN: 1074-7613 ;EISSN: 1097-4180 ;DOI: 10.1016/j.immuni.2021.04.001 ;PMID: 33951416

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