Deficiency of autophagy protein Map1-LC3b mediates IL-17-dependent lung pathology during respiratory viral infection via ER stress-associated IL-1.

Reed, M; Morris, S H; Owczarczyk, A B; Lukacs, N W

doi:10.1038/mi.2015.3

Cited by 85Autophagy in Disease and TherapyEndoplasmic Reticulum Stress and DiseaseAsthma and respiratory diseases

Deficiency of autophagy protein Map1-LC3b mediates IL-17-dependent lung pathology during respiratory viral infection via ER stress-associated IL-1.

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Reed, M, Morris, S H, Owczarczyk, A B, Lukacs, N W·2015·Mucosal Immunology

DOI 10.1038/mi.2015.3PMC PMC4532659

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Abstract

While recent studies suggest that interleukin (IL)-1β production is modulated by macroautophagy or sensors of endoplasmic reticulum (ER) stress upon pro-inflammatory insult, autophagy and IL-1β production during viral infection has not been fully investigated. This was addressed using respiratory syncytial virus (RSV), which is associated with lung immunopathology, IL-1, and IL-17a secretion in severely infected patients. Mice deficient in the autophagy-associated protein Map1-LC3b (LC3b(-/-)) developed increased IL-17a-dependent lung pathology upon infection. RSV-infected LC3b(-/-) dendritic cells (DCs) fail to upregulate autophagosome formation, secrete IL-1β and IL-6, and elicit IL-17a production from CD4+ T cells. Bone marrow chimeras revealed that both structural and hematopoietic LC3b deficiency contribute to the development of IL-17a-dependent lung pathology in vivo. Further investigation revealed airway epithelium as the primary source of IL-1β during infection, whereas inhibition of the ER-stress sensor inositol-requiring protein-1 in primary airway epithelial cells reduced IL-1β production identifying a primary ER stress pathway. Finally, blockade of IL-1 receptor signaling in RSV-infected LC3b(-/-) mice abolished IL-17a-dependent lung pathology. These findings provide novel mechanistic insight into the contribution of autophagy- and ER stress-dependent cytokine production that initiate and maintain aberrant Th17 responses, while identifying IL-1 as a potential therapeutic target in the treatment of severe respiratory viral infections.

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LC3B plays a protective role in hypoxia, a pro-pathogenic role in cigarette smoke-induced emphysema, and increased susceptibility to lung pathology during respiratory viral infection.
“it has been shown to play a protective role in hypoxia; pro-pathogenic role in cigarette smoke induced emphysema; increased susceptibility to lung pathology during respiratory viral infection.”
From Microtubule-associated protein 1 light chain 3B, (LC3B) is necessary to maintain lipid-mediated homeostasis in the retinal pigment epithelium (2018) · cites this paper as Reed et al., 2015

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Requirement of Autophagy Proteins Beclin-1 and Map1-LC3b in the Induction of Innate and Adaptive Immune Responses to Respiratory Syncytial Virus Infection [electronic resource].
Reed, M. (2014) · University of Michigan Library Repository
Requirement of Autophagy Proteins Beclin-1 and Map1-LC3b in the Induction of Innate and Adaptive Immune Responses to Respiratory Syncytial Virus Infection.
Reed, M. (2014) · Deep Blue (University of Michigan)
Autophagy-Inducing Protein Beclin-1 in Dendritic Cells Regulates CD4 T Cell Responses and Disease Severity during Respiratory Syncytial Virus Infection
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IL-17–Induced Pulmonary Pathogenesis during Respiratory Viral Infection and Exacerbation of Allergic Disease
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Autophagy and TGF-β regulates innate immune response in human respiratory syncytial virus infected macrophages
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Authors: Reed, M., Morris, S. H., Owczarczyk, A. B., & Lukacs, N. W.
Affiliations: University of Michigan (US)
Corresponding author: Lukacs, N W
ORCID: Reed, M
Owczarczyk, A B
Lukacs, N W
Venue: Mucosal Immunology
Publisher: Elsevier BV
Published: 2015-09
Volume: 8
Issue: 5
Pages: 1118-1130
ISSN: 1933-0219 (ISSN-L)
DOI: 10.1038/mi.2015.3
PMC: PMC4532659
OpenAlex: W2096326560
Cited by: 85
References: 51
Citations by year: 2026: 3 · 2025: 4 · 2024: 5 · 2023: 7 · 2022: 8 · 2021: 11 · 2020: 11 · 2019: 3 · 2018: 10 · 2017: 11 · 2016: 6 · 2015: 5 · 2014: 1
FWCI: 8.36
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, 2340 d)
Locations: Mucosal Immunology (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: University of Michigan
National Institutes of Health (5t32ai007413-32)
National Heart, Lung, and Blood Institute (HL114858, R01HL114858)
National Institute of General Medical Sciences (T32GM007863)
National Institute of Allergy and Infectious Diseases (T32-AI-007413)
Topics: Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Endoplasmic Reticulum Stress and Disease
Health Sciences › Medicine › Physiology › Asthma and respiratory diseases
Keywords: autophagy, LC3B, endoplasmic reticulum stress, IL-1β, IL-17A, respiratory syncytial virus, respiratory viral infections, lung immunopathology, dendritic cells, airway epithelium, Th17 cells, IL-1 signaling, autophagosome formation, interleukin-6
MeSH terms: Animals, Dendritic Cells, Lung Diseases, Microtubule-Associated Proteins, Respiratory Syncytial Viruses, CD4-Positive T-Lymphocytes, Interleukin-6, Mice, Knockout, Respiratory Syncytial Virus Infections, Interleukin-17, Mice, Interleukin-1beta, Th17 Cells, Endoplasmic Reticulum Stress

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Deficiency of autophagy protein Map1-LC3b mediates IL-17-dependent lung pathology during respiratory viral infection via ER stress-associated IL-1.

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