Cited by 1,356Immune Response and InflammationRespiratory Support and MechanismsNeutrophil, Myeloperoxidase and Oxidative Mechanisms

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Identification of Oxidative Stress and Toll-like Receptor 4 Signaling as a Key Pathway of Acute Lung Injury

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Imai, Yumiko, Kuba, Keiji, Neely, G. Greg, Yaghubian-Malhami, Rubina, Perkmann, Thomas, van Loo, Geert, Ermolaeva, Maria, Veldhuizen, Ruud, Leung, Y.H. Connie, Wang, Hongliang, Liu, Haolin, Sun, Yang, Pasparakis, Manolis, Kopf, Manfred, Mech, Christin, Bavari, Sina, Peiris, J.S. Malik, Slutsky, Arthur S., Akira, Shizuo, Hultqvist, Malin, Holmdahl, Rikard, Nicholls, John, Jiang, Chengyu, Binder, Christoph J., Penninger, Josef M.·2008·Cell

DOI 10.1016/j.cell.2008.02.043PMC PMC7112336

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Abstract

Multiple lung pathogens such as chemical agents, H5N1 avian flu, or SARS cause high lethality due to acute respiratory distress syndrome. Here we report that Toll-like receptor 4 (TLR4) mutant mice display natural resistance to acid-induced acute lung injury (ALI). We show that TLR4-TRIF-TRAF6 signaling is a key disease pathway that controls the severity of ALI. The oxidized phospholipid (OxPL) OxPAPC was identified to induce lung injury and cytokine production by lung macrophages via TLR4-TRIF. We observed OxPL production in the lungs of humans and animals infected with SARS, Anthrax, or H5N1. Pulmonary challenge with an inactivated H5N1 avian influenza virus rapidly induces ALI and OxPL formation in mice. Loss of TLR4 or TRIF expression protects mice from H5N1-induced ALI. Moreover, deletion of ncf1, which controls ROS production, improves the severity of H5N1-mediated ALI. Our data identify oxidative stress and innate immunity as key lung injury pathways that control the severity of ALI.

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Authors: Imai, Y., Kuba, K., Neely, G. G., Yaghubian-Malhami, R., Perkmann, T., van Loo, G., Ermolaeva, M., Veldhuizen, R., Leung, Y. H. C., Wang, H., Liu, H., Sun, Y., Pasparakis, M., Kopf, M., Mech, C., Bavari, S., Peiris, J. S. M., Slutsky, A. S., Akira, S., Hultqvist, M., Holmdahl, R., Nicholls, J., Jiang, C., Binder, C. J., & Penninger, J. M.
Affiliations: Institute of Molecular Biotechnology (AT)
Austrian Academy of Sciences (AT)
University of Cologne (DE)
Western University (CA)
Chinese Academy of Medical Sciences & Peking Union Medical College (CN)
United States Army Medical Research Institute of Infectious Diseases (US)
St. Michael's Hospital (CA)
Research Institute for Microbial Diseases, The University of Osaka (JP)
Karolinska Institutet (SE)
University of Hong Kong (HK)
Corresponding author: Imai, Yumiko
Penninger, Josef M.
ORCID: Imai, Yumiko
Kuba, Keiji
Perkmann, Thomas
Ermolaeva, Maria
Veldhuizen, Ruud
Wang, Hongliang
Sun, Yang
Pasparakis, Manolis
Bavari, Sina
Slutsky, Arthur S.
Akira, Shizuo
Holmdahl, Rikard
Nicholls, John
Jiang, Chengyu
Binder, Christoph J.
Penninger, Josef M.
Venue: Cell
Publisher: Elsevier BV
Published: 2008-04
Volume: 133
Issue: 2
Pages: 235-249
ISSN: 0092-8674 (ISSN-L)
DOI: 10.1016/j.cell.2008.02.043
PMC: PMC7112336
OpenAlex: W2156613610
Cited by: 1,356
References: 60
Citations by year: 2026: 34 · 2025: 53 · 2024: 56 · 2023: 76 · 2022: 105 · 2021: 143 · 2020: 152 · 2019: 47 · 2018: 69 · 2017: 64 · 2016: 80 · 2015: 65 · 2014: 82 · 2013: 68 · 2012: 53
FWCI: 29.18
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 1933 d)
doi.org/10.15223/policy-017 (stm-asf)
doi.org/10.15223/policy-037 (stm-asf)
doi.org/10.15223/policy-012 (stm-asf)
doi.org/10.15223/policy-029 (stm-asf)
doi.org/10.15223/policy-004 (stm-asf)
Locations: Cell (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Ghent University Academic Bibliography (Ghent University) (submittedVersion)
The HKU Scholars Hub (University of Hong Kong) (submittedVersion)
Lund University Publications (Lund University) (submittedVersion)
Funders: University of Pittsburgh
European Commission
Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (100233)
Defense Threat Reduction Agency
Canadian Institutes of Health Research
Topics: Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Respiratory Support and Mechanisms
Life Sciences › Immunology and Microbiology › Immunology › Neutrophil, Myeloperoxidase and Oxidative Mechanisms
Keywords: acute lung injury, TLR4, TRIF, TRAF6, oxidized phospholipids, OxPAPC, oxidative stress, reactive oxygen species, NCF1, lung macrophages, H5N1 avian influenza, SARS, anthrax, innate immunity, respiratory distress syndrome
MeSH terms: Animals, Humans, Influenza, Human, Lung, Mice, Inbred C57BL, Orthomyxoviridae Infections, Phospholipids, Respiratory Distress Syndrome, Signal Transduction, Interleukin-6, NF-kappa B, Oxidative Stress, NADPH Oxidases, Adaptor Proteins, Vesicular Transport, Severe Acute Respiratory Syndrome, Toll-Like Receptor 4, Mice

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Identification of Oxidative Stress and Toll-like Receptor 4 Signaling as a Key Pathway of Acute Lung Injury

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