Ozone-induced lung injury and inflammation: Pathways and therapeutic targets for pulmonary diseases caused by air pollutants

Exposure to ambient Ozone (O3) air pollution directly causes by its oxidative properties, respiratory epithelial cell injury, and cell death, which promote inflammation and hyperreactivity, posing a significant public health concern. Recent clinical and experimental studies have made strides in eluc...

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Main Authors: Remo C. Russo, Dieudonnée Togbe, Isabelle Couillin, Noria Segueni, Lianyong Han, Valérie F.J. Quesniaux, Tobias Stoeger, Bernhard Ryffel
Format: Article
Language:English
Published: Elsevier 2025-04-01
Series:Environment International
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Online Access:http://www.sciencedirect.com/science/article/pii/S0160412025001424
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author Remo C. Russo
Dieudonnée Togbe
Isabelle Couillin
Noria Segueni
Lianyong Han
Valérie F.J. Quesniaux
Tobias Stoeger
Bernhard Ryffel
author_facet Remo C. Russo
Dieudonnée Togbe
Isabelle Couillin
Noria Segueni
Lianyong Han
Valérie F.J. Quesniaux
Tobias Stoeger
Bernhard Ryffel
author_sort Remo C. Russo
collection DOAJ
description Exposure to ambient Ozone (O3) air pollution directly causes by its oxidative properties, respiratory epithelial cell injury, and cell death, which promote inflammation and hyperreactivity, posing a significant public health concern. Recent clinical and experimental studies have made strides in elucidating the mechanisms underlying O3-induced epithelial cell injury, inflammation, and airway hyperreactivity, which are discussed herein. The current data suggest that O3-induced oxidative stress is a central event-inducing oxeiptotic cell death pathway. O3-induced epithelial barrier damage and cell death, triggering the release of alarmins and damage-associated molecular patterns (DAMPs), with subsequent endogenous activation of Toll-like receptors (TLRs), DNA sensing pathways, and inflammasomes, activating interleukin-1-Myd88 inflammatory pathway with the production of a range of chemokines and cytokines. This cascade orchestrates lung tissue-resident cell activation in response to O3 in leukocyte and non-leukocyte populations, driving sterile innate immune response. Chronic inflammatory response to O3, by repeated exposures, supports a mixed phenotype combining asthma and emphysema, in which their exacerbation by other particulate pollutants potentially culminates in respiratory failure. We use data from lung single-cell transcriptomics to map genes of O3-damage sensing and signaling pathways to lung cells and thereby highlight potential hotspots of O3 responses. Deeper insights into these pathological pathways might be helpful for the identification of novel therapeutic targets and strategies.
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spelling doaj-art-b6c82412d9f349fda7be59576c0b279d2025-08-20T02:12:07ZengElsevierEnvironment International0160-41202025-04-0119810939110.1016/j.envint.2025.109391Ozone-induced lung injury and inflammation: Pathways and therapeutic targets for pulmonary diseases caused by air pollutantsRemo C. Russo0Dieudonnée Togbe1Isabelle Couillin2Noria Segueni3Lianyong Han4Valérie F.J. Quesniaux5Tobias Stoeger6Bernhard Ryffel7Laboratory of Pulmonary Immunology and Mechanics, Federal University of Minas Gerais, Belo Horizonte, Minas Gerais, Brazil; Corresponding authors at: Laboratory of Pulmonary Immunology and Mechanics, Federal University of Minas Gerais, Avenida Antonio Carlos 6627, 31270-901 Belo Horizonte, Minas Gerais, Brazil (Remo Castro Russo). Immuno-Neuro Modulation, INEM, UMR7355, 3B rue Ferollerie, 45071 Orleans, France (Bernhard Ryffel).Laboratory of Immuno-Neuro Modulation, INEM, UMR7355 CNRS and University of Orleans, Orleans, FranceLaboratory of Immuno-Neuro Modulation, INEM, UMR7355 CNRS and University of Orleans, Orleans, FranceArtImmune SAS, 13 Avenue Buffon, Orleans, FranceInstitute of Lung Health and Immunity (LHI), Comprehensive Pneumology Center, Helmholtz Zentrum München, German Research Center for Environmental Health, and Member of the German Center of Lung Research (DZL), GermanyLaboratory of Immuno-Neuro Modulation, INEM, UMR7355 CNRS and University of Orleans, Orleans, FranceInstitute of Lung Health and Immunity (LHI), Comprehensive Pneumology Center, Helmholtz Zentrum München, German Research Center for Environmental Health, and Member of the German Center of Lung Research (DZL), GermanyLaboratory of Immuno-Neuro Modulation, INEM, UMR7355 CNRS and University of Orleans, Orleans, France; ArtImmune SAS, 13 Avenue Buffon, Orleans, France; Corresponding authors at: Laboratory of Pulmonary Immunology and Mechanics, Federal University of Minas Gerais, Avenida Antonio Carlos 6627, 31270-901 Belo Horizonte, Minas Gerais, Brazil (Remo Castro Russo). Immuno-Neuro Modulation, INEM, UMR7355, 3B rue Ferollerie, 45071 Orleans, France (Bernhard Ryffel).Exposure to ambient Ozone (O3) air pollution directly causes by its oxidative properties, respiratory epithelial cell injury, and cell death, which promote inflammation and hyperreactivity, posing a significant public health concern. Recent clinical and experimental studies have made strides in elucidating the mechanisms underlying O3-induced epithelial cell injury, inflammation, and airway hyperreactivity, which are discussed herein. The current data suggest that O3-induced oxidative stress is a central event-inducing oxeiptotic cell death pathway. O3-induced epithelial barrier damage and cell death, triggering the release of alarmins and damage-associated molecular patterns (DAMPs), with subsequent endogenous activation of Toll-like receptors (TLRs), DNA sensing pathways, and inflammasomes, activating interleukin-1-Myd88 inflammatory pathway with the production of a range of chemokines and cytokines. This cascade orchestrates lung tissue-resident cell activation in response to O3 in leukocyte and non-leukocyte populations, driving sterile innate immune response. Chronic inflammatory response to O3, by repeated exposures, supports a mixed phenotype combining asthma and emphysema, in which their exacerbation by other particulate pollutants potentially culminates in respiratory failure. We use data from lung single-cell transcriptomics to map genes of O3-damage sensing and signaling pathways to lung cells and thereby highlight potential hotspots of O3 responses. Deeper insights into these pathological pathways might be helpful for the identification of novel therapeutic targets and strategies.http://www.sciencedirect.com/science/article/pii/S0160412025001424PollutionO3DAMPsInflammasomeAlarminsIL-33
spellingShingle Remo C. Russo
Dieudonnée Togbe
Isabelle Couillin
Noria Segueni
Lianyong Han
Valérie F.J. Quesniaux
Tobias Stoeger
Bernhard Ryffel
Ozone-induced lung injury and inflammation: Pathways and therapeutic targets for pulmonary diseases caused by air pollutants
Environment International
Pollution
O3
DAMPs
Inflammasome
Alarmins
IL-33
title Ozone-induced lung injury and inflammation: Pathways and therapeutic targets for pulmonary diseases caused by air pollutants
title_full Ozone-induced lung injury and inflammation: Pathways and therapeutic targets for pulmonary diseases caused by air pollutants
title_fullStr Ozone-induced lung injury and inflammation: Pathways and therapeutic targets for pulmonary diseases caused by air pollutants
title_full_unstemmed Ozone-induced lung injury and inflammation: Pathways and therapeutic targets for pulmonary diseases caused by air pollutants
title_short Ozone-induced lung injury and inflammation: Pathways and therapeutic targets for pulmonary diseases caused by air pollutants
title_sort ozone induced lung injury and inflammation pathways and therapeutic targets for pulmonary diseases caused by air pollutants
topic Pollution
O3
DAMPs
Inflammasome
Alarmins
IL-33
url http://www.sciencedirect.com/science/article/pii/S0160412025001424
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