Context‐specific anti‐inflammatory roles of type III interferon signaling in the lung in nonviral injuries

Abstract Type III interferons (λ1, λ2, and λ3) are potent antiviral cytokines in the lung. However, their roles in nonviral lung injuries are less well understood. This study investigates the activation of type III interferon signaling in three distinct models of lung injuries caused by diverse stim...

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Main Authors: Jingjing Feng, Jooyoung Kim, Victoria D. Wang, De Chang, Hongbo Liu, William G. Bain, Keven M. Robinson, Zhijun Jie, Sergei V. Kotenko, Charles S. Dela Cruz, Lokesh Sharma
Format: Article
Language:English
Published: Wiley 2024-10-01
Series:Physiological Reports
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Online Access:https://doi.org/10.14814/phy2.70104
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author Jingjing Feng
Jooyoung Kim
Victoria D. Wang
De Chang
Hongbo Liu
William G. Bain
Keven M. Robinson
Zhijun Jie
Sergei V. Kotenko
Charles S. Dela Cruz
Lokesh Sharma
author_facet Jingjing Feng
Jooyoung Kim
Victoria D. Wang
De Chang
Hongbo Liu
William G. Bain
Keven M. Robinson
Zhijun Jie
Sergei V. Kotenko
Charles S. Dela Cruz
Lokesh Sharma
author_sort Jingjing Feng
collection DOAJ
description Abstract Type III interferons (λ1, λ2, and λ3) are potent antiviral cytokines in the lung. However, their roles in nonviral lung injuries are less well understood. This study investigates the activation of type III interferon signaling in three distinct models of lung injuries caused by diverse stimuli: the bacterial pathogen Pseudomonas aeruginosa, bacterial endotoxin LPS, and the chemotherapeutic agent bleomycin. Our data show that, despite inducing a potent inflammatory response, Pseudomonas and LPS did not increase IFNλ secretion. In contrast, bleomycin instillation increased secretion of IFNλ in the airways at both early and late time points. Consistent with limited secretion, type III interferon signaling had a minimal role in the host response to both Pseudomonas and LPS, as measured by pathogen burden, inflammatory response, and lung injury. Conversely, a deficiency in type III interferon signaling led to increased inflammatory signaling and elevated acute lung injury in the bleomycin model on day 3. This elevated early injury resulted in impaired recovery in IFNLR1 knockout mice, as evidenced by their recovery from bleomycin‐induced weight loss. Taken together, these data suggest a context‐specific activation of type III interferon signaling, where it plays an anti‐inflammatory role in the lung.
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spelling doaj-art-f079971b4ef3452a86bee1efa3c2e9712025-08-20T02:12:03ZengWileyPhysiological Reports2051-817X2024-10-011220n/an/a10.14814/phy2.70104Context‐specific anti‐inflammatory roles of type III interferon signaling in the lung in nonviral injuriesJingjing Feng0Jooyoung Kim1Victoria D. Wang2De Chang3Hongbo Liu4William G. Bain5Keven M. Robinson6Zhijun Jie7Sergei V. Kotenko8Charles S. Dela Cruz9Lokesh Sharma10Department of Pulmonary and Critical Care Medicine, Shanghai Fifth People's Hospital, Center of Community‐Based Health Research Fudan University Shanghai ChinaSection of Pulmonary, Critical Care and Sleep Medicine Yale School of Medicine New Haven Connecticut USADivision of Pulmonary, Allergy, Critical Care, and Sleep Medicine, Department of Medicine University of Pittsburgh School of Medicine Pittsburgh Pennsylvania USASection of Pulmonary, Critical Care and Sleep Medicine Yale School of Medicine New Haven Connecticut USASection of Pulmonary, Critical Care and Sleep Medicine Yale School of Medicine New Haven Connecticut USADivision of Pulmonary, Allergy, Critical Care, and Sleep Medicine, Department of Medicine University of Pittsburgh School of Medicine Pittsburgh Pennsylvania USADivision of Pulmonary, Allergy, Critical Care, and Sleep Medicine, Department of Medicine University of Pittsburgh School of Medicine Pittsburgh Pennsylvania USADepartment of Pulmonary and Critical Care Medicine, Shanghai Fifth People's Hospital, Center of Community‐Based Health Research Fudan University Shanghai ChinaDepartment of Biochemistry and Molecular Biology Rutgers New Jersey Medical School New Brunswick New Jersey USASection of Pulmonary, Critical Care and Sleep Medicine Yale School of Medicine New Haven Connecticut USASection of Pulmonary, Critical Care and Sleep Medicine Yale School of Medicine New Haven Connecticut USAAbstract Type III interferons (λ1, λ2, and λ3) are potent antiviral cytokines in the lung. However, their roles in nonviral lung injuries are less well understood. This study investigates the activation of type III interferon signaling in three distinct models of lung injuries caused by diverse stimuli: the bacterial pathogen Pseudomonas aeruginosa, bacterial endotoxin LPS, and the chemotherapeutic agent bleomycin. Our data show that, despite inducing a potent inflammatory response, Pseudomonas and LPS did not increase IFNλ secretion. In contrast, bleomycin instillation increased secretion of IFNλ in the airways at both early and late time points. Consistent with limited secretion, type III interferon signaling had a minimal role in the host response to both Pseudomonas and LPS, as measured by pathogen burden, inflammatory response, and lung injury. Conversely, a deficiency in type III interferon signaling led to increased inflammatory signaling and elevated acute lung injury in the bleomycin model on day 3. This elevated early injury resulted in impaired recovery in IFNLR1 knockout mice, as evidenced by their recovery from bleomycin‐induced weight loss. Taken together, these data suggest a context‐specific activation of type III interferon signaling, where it plays an anti‐inflammatory role in the lung.https://doi.org/10.14814/phy2.70104bleomycinfibrosislung inflammationlung injurytype III interferons
spellingShingle Jingjing Feng
Jooyoung Kim
Victoria D. Wang
De Chang
Hongbo Liu
William G. Bain
Keven M. Robinson
Zhijun Jie
Sergei V. Kotenko
Charles S. Dela Cruz
Lokesh Sharma
Context‐specific anti‐inflammatory roles of type III interferon signaling in the lung in nonviral injuries
Physiological Reports
bleomycin
fibrosis
lung inflammation
lung injury
type III interferons
title Context‐specific anti‐inflammatory roles of type III interferon signaling in the lung in nonviral injuries
title_full Context‐specific anti‐inflammatory roles of type III interferon signaling in the lung in nonviral injuries
title_fullStr Context‐specific anti‐inflammatory roles of type III interferon signaling in the lung in nonviral injuries
title_full_unstemmed Context‐specific anti‐inflammatory roles of type III interferon signaling in the lung in nonviral injuries
title_short Context‐specific anti‐inflammatory roles of type III interferon signaling in the lung in nonviral injuries
title_sort context specific anti inflammatory roles of type iii interferon signaling in the lung in nonviral injuries
topic bleomycin
fibrosis
lung inflammation
lung injury
type III interferons
url https://doi.org/10.14814/phy2.70104
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