ArticleImmunity2021
Uncoupling of macrophage inflammation from self-renewal modulates host recovery from respiratory viral infection.
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Article in Immunity, 2021. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 104 papers.
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104citing papers in PubMed
7.8field-weighted citation impact, top 2% of its field
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Who cites it
104 citing papers in PubMed, 150 citations in OpenAlex.
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- Recent perspectives on macrophage memory: types, mechanisms, and characteristics in pulmonary diseases.Cell communication and signaling : CCS · 2026Review
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- Hypoxia: a critical pathophysiological driver in respiratory inflammatory diseases.Military Medical Research · 2026Review
44 more citing papers are in PubMed but not listed here.
Corrections and comments
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Authors and funding
30 authors at 8 institutions in 3 countries.
Bibo ZhuDivision of Pulmonary and Critical Care Medicine, Department of Medicine, Mayo Clinic College of Medicine and Science, Rochester, MN 55905, USA; Department of Immunology, Mayo Clinic College of Medicine and Science, Rochester, MN 55905, USA.
Yue WuDivision of Pulmonary and Critical Care Medicine, Department of Medicine, Mayo Clinic College of Medicine and Science, Rochester, MN 55905, USA; Department of Immunology, Mayo Clinic College of Medicine and Science, Rochester, MN 55905, USA.
Su HuangDivision of Pulmonary and Critical Care Medicine, Department of Medicine, Mayo Clinic College of Medicine and Science, Rochester, MN 55905, USA; Department of Immunology, Mayo Clinic College of Medicine and Science, Rochester, MN 55905, USA.
Ruixuan ZhangDivision of Pulmonary and Critical Care Medicine, Department of Medicine, Mayo Clinic College of Medicine and Science, Rochester, MN 55905, USA; Department of Immunology, Mayo Clinic College of Medicine and Science, Rochester, MN 55905, USA.
Young Min SonDivision of Pulmonary and Critical Care Medicine, Department of Medicine, Mayo Clinic College of Medicine and Science, Rochester, MN 55905, USA; Department of Immunology, Mayo Clinic College of Medicine and Science, Rochester, MN 55905, USA.
Chaofan LiDivision of Pulmonary and Critical Care Medicine, Department of Medicine, Mayo Clinic College of Medicine and Science, Rochester, MN 55905, USA; Department of Immunology, Mayo Clinic College of Medicine and Science, Rochester, MN 55905, USA.
In Su CheonDivision of Pulmonary and Critical Care Medicine, Department of Medicine, Mayo Clinic College of Medicine and Science, Rochester, MN 55905, USA; Department of Immunology, Mayo Clinic College of Medicine and Science, Rochester, MN 55905, USA.
Xiaochen GaoDivision of Pulmonary and Critical Care Medicine, Department of Medicine, Mayo Clinic College of Medicine and Science, Rochester, MN 55905, USA; Department of Immunology, Mayo Clinic College of Medicine and Science, Rochester, MN 55905, USA.
Min WangDivision of Pulmonary and Critical Care Medicine, Department of Medicine, Mayo Clinic College of Medicine and Science, Rochester, MN 55905, USA; Department of Immunology, Mayo Clinic College of Medicine and Science, Rochester, MN 55905, USA.
Yao ChenVersiti Blood Research Institute, Milwaukee, WI 53226, USA; Department of Microbiology and Immunology, Medical College of Wisconsin, Wauwatosa, WI 53226, USA.
Xian ZhouDepartment of Immunology, Mayo Clinic College of Medicine and Science, Rochester, MN 55905, USA; Division of Rheumatology, Department of Medicine, Mayo Clinic College of Medicine and Science, Rochester, MN 55905, USA.
Quynh NguyenDivision of Biological Sciences, Section of Molecular Biology, University of California, San Diego, La Jolla, CA 92093, USA.
Anthony T PhanDivision of Biological Sciences, Section of Molecular Biology, University of California, San Diego, La Jolla, CA 92093, USA.
Supriya BehlDepartment of Pediatric and Adolescent Medicine, Mayo Clinic, Rochester, MN 55905, USA.
M Mark TaketoDivision of Experimental Therapeutics, Graduate School of Medicine, Kyoto University, Kyoto, Japan.
Matthias MackDepartment of Nephrology, University Hospital Regensburg, 93053 Regensburg, Germany.
Virginia S ShapiroDepartment of Immunology, Mayo Clinic College of Medicine and Science, Rochester, MN 55905, USA.
Hu ZengDepartment of Immunology, Mayo Clinic College of Medicine and Science, Rochester, MN 55905, USA; Division of Rheumatology, Department of Medicine, Mayo Clinic College of Medicine and Science, Rochester, MN 55905, USA.
Hideki EbiharaDepartment of Molecular Medicine, Mayo Clinic College of Medicine and Science, Rochester, MN 55905, USA.
John J MullonDivision of Pulmonary and Critical Care Medicine, Department of Medicine, Mayo Clinic College of Medicine and Science, Rochester, MN 55905, USA.
Eric S EdellDivision of Pulmonary and Critical Care Medicine, Department of Medicine, Mayo Clinic College of Medicine and Science, Rochester, MN 55905, USA.
Janani S ReisenauerDivision of Pulmonary and Critical Care Medicine, Department of Medicine, Mayo Clinic College of Medicine and Science, Rochester, MN 55905, USA.
Nadir DemirelDepartment of Pediatric and Adolescent Medicine, Mayo Clinic, Rochester, MN 55905, USA.
Ryan M KernDivision of Pulmonary and Critical Care Medicine, Department of Medicine, Mayo Clinic College of Medicine and Science, Rochester, MN 55905, USA.
Rana ChakrabortyDepartment of Pediatric and Adolescent Medicine, Mayo Clinic, Rochester, MN 55905, USA.
Weiguo CuiVersiti Blood Research Institute, Milwaukee, WI 53226, USA; Department of Microbiology and Immunology, Medical College of Wisconsin, Wauwatosa, WI 53226, USA.
Mark H KaplanDepartment of Microbiology and Immunology, Indiana University School of Medicine, Indianapolis, IN 46202, USA.
Xiaobo ZhouChanning Division of Network Medicine, Department of Medicine, Brigham and Women's Hospital, Boston, MA 02115, USA.
Ananda W GoldrathDivision of Biological Sciences, Section of Molecular Biology, University of California, San Diego, La Jolla, CA 92093, USA.
Jie SunDivision of Pulmonary and Critical Care Medicine, Department of Medicine, Mayo Clinic College of Medicine and Science, Rochester, MN 55905, USA; Department of Immunology, Mayo Clinic College of Medicine and Science, Rochester, MN 55905, USA. Electronic address: sun.jie@mayo.edu.
Mayo Clinic · USMayo Clinic in Florida · USUniversity of California San Diego · USBrigham and Women's Hospital · USMedical College of Wisconsin · USIndiana University School of MedicineKyoto University · JPUniversity Hospital Regensburg · DE
Funding
T cell maintenance: molecular mediators of the TCR-derived survival signalR01AI067545 · NIAID · UNIVERSITY OF CALIFORNIA, SAN DIEGO · PI GOLDRATH, ANANDA W · 2006 to 2021
$6.1MRegulation of T cell immunity to viral infectionR01AI072117 · NIAID · UNIVERSITY OF CALIFORNIA, SAN DIEGO · PI GOLDRATH, ANANDA W · 2008 to 2022
$5.4MHost cellular network governing the development of post SARS-CoV-2 tissue sequelaeR01AI147394 · NIAID · UNIVERSITY OF VIRGINIA · PI Jie Sun · 2020 to 2026
$4.7MMolecular regulation of protective CD8 immunity against influenza infectionR01AI112844 · NIAID · UNIVERSITY OF VIRGINIA · PI SUN, JIE · 2015 to 2024
$4.5MElucidating the roles of alveolar macrophage inflammation and selfrenewal during influenza infectionR01AG069264 · NIA · UNIVERSITY OF VIRGINIA · PI Jie Sun · 2020 to 2026
$3.5MT cell maintenance: molecular mediators of T cell differentiation and survivalR37AI067545 · NIAID · UNIVERSITY OF CALIFORNIA, SAN DIEGO · PI Ananda W Goldrath · 2022 to 2026
$3.0MRoles of tissue-resident helper T cells in mucosal immunity against influenzainfectionR01AI154598 · NIAID · UNIVERSITY OF VIRGINIA · PI SUN, JIE · 2020 to 2024
$2.9MDetermining how macrophages regulate immunity to Zika virus infection at the maternal-fetal interfaceU01AI131566 · NIAID · EMORY UNIVERSITY · PI CHAKRABORTY, RANA, SUTHAR, MEHUL SHAMAL · 2017 to 2021
$2.3MTh9 cells in immediate hypersensitivityR01AI129241 · NIAID · INDIANA UNIVERSITY INDIANAPOLIS · PI KAPLAN, MARK H · 2017 to 2021
$2.0MSimultaneously boosting both humoral and cellular immunity following vaccinationR01AG047156 · NIA · MAYO CLINIC ROCHESTER · PI SUN, JIE · 2015 to 2019
$1.6MMechanisms of influenza viral pathogenesis in normal hosts and hosts with chronic diseasesR56AI150599 · NIAID · MAYO CLINIC ROCHESTER · PI SUN, JIE · 2020 to 2020
$494kIL-9-dependent interstitial macrophage function in the allergic lungR56AI129241 · NIAID · INDIANA UNIVERSITY INDIANAPOLIS · PI KAPLAN, MARK H · 2023 to 2023
$461kNIAID NIH HHS R01 AI067545NIAID NIH HHS R01 AI072117NIAID NIH HHS R01 AI112844NIAID NIH HHS R01 AI129241NIAID NIH HHS R01 AI147394NIAID NIH HHS R01 AI154598NIAID NIH HHS R37 AI067545NIAID NIH HHS R56 AI129241NIAID NIH HHS R56 AI150599NIAID NIH HHS U01 AI131566NIA NIH HHS R01 AG047156NIA NIH HHS R01 AG069264NICHD NIH HHS R21 HD103498
Abstract
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.
Indexed as
BiomarkersCell Self RenewalCOVID-19CytokinesDisease SusceptibilityHost-Pathogen InteractionsHumansHypoxia-Inducible Factor 1, alpha SubunitInflammation MediatorsMacrophagesMacrophages, AlveolarSARS-CoV-2Signal TransductionBiomarkersCytokinesHypoxia-Inducible Factor 1, alpha SubunitInflammation Mediatorsalveolar macrophagesHIF-1αinfluenza viruspulmonary inflammationSARS-CoV-2self-renewaltissue macrophagestissue repairβ-catenin
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