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Macrophage autophagy protects against liver fibrosis in mice
Open accessAbstract
Autophagy is a lysosomal degradation pathway of cellular components that displays antiinflammatory properties in macrophages. Macrophages are critically involved in chronic liver injury by releasing mediators that promote hepatocyte apoptosis, contribute to inflammatory cell recruitment and activation of hepatic fibrogenic cells. Here, we investigated whether macrophage autophagy may protect against chronic liver injury. Experiments were performed in mice with mutations in the autophagy gene Atg5 in the myeloid lineage (Atg5(fl/fl) LysM-Cre mice, referred to as atg5(-/-)) and their wild-type (Atg5(fl/fl), referred to as WT) littermates. Liver fibrosis was induced by repeated intraperitoneal injection of carbon tetrachloride. In vitro studies were performed in cultures or co-cultures of peritoneal macrophages with hepatic myofibroblasts. As compared to WT littermates, atg5(-/-) mice exposed to chronic carbon tetrachloride administration displayed higher hepatic levels of IL1A and IL1B and enhanced inflammatory cell recruitment associated with exacerbated liver injury. In addition, atg5(-/-) mice were more susceptible to liver fibrosis, as shown by enhanced matrix and fibrogenic cell accumulation. Macrophages from atg5(-/-) mice secreted higher levels of reactive oxygen species (ROS)-induced IL1A and IL1B. Moreover, hepatic myofibroblasts exposed to the conditioned medium of macrophages from atg5(-/-) mice showed increased profibrogenic gene expression; this effect was blunted when neutralizing IL1A and IL1B in the conditioned medium of atg5(-/-) macrophages. Finally, administration of recombinant IL1RN (interleukin 1 receptor antagonist) to carbon tetrachloride-exposed atg5(-/-) mice blunted liver injury and fibrosis, identifying IL1A/B as central mediators in the deleterious effects of macrophage autophagy invalidation. These results uncover macrophage autophagy as a novel antiinflammatory pathway regulating liver fibrosis.
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“In particular, atg5 deletion (Lodder et al, 2015; Habib et al, 2019) and genetic inhibition of LAP components (Wan et al, 2020) in the myeloid compartment exacerbate hepatic inflammation in mice with chronic liver injury, thus enhancing liver fibrosis.”
From Autophagy in major human diseases (2021) · cites this paper as Lodder et al, 2015
In the citing paper
“activation of a noncanonical form of autophagy (LC3-associated phagocytosis) shifts the macrophage phenotype toward an anti-inflammatory stage with resulting antifibrogenic effects (133, 134)”
From Immunoregulation of Liver Fibrosis: New Opportunities for Antifibrotic Therapy (2024) · cites this paper as [133]
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“Besides its anti-inflammatory effects, activation of autophagy protects against hepatocyte injury, improves endothelial dysfunction, and decreases the release of profibrogenic extracellular vesicles from HSCs (133, 135–138).”
From Immunoregulation of Liver Fibrosis: New Opportunities for Antifibrotic Therapy (2024) · cites this paper as [133]
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“and (ii) autophagy as a limiting factor to a pro‐inflammatory phenotype in macrophages.”
From Autophagy in major human diseases (2021) · cites this paper as Lodder et al, 2015
In the citing paper
“| Cirrhosis | Myeloid cell‐specific deletion of Atg5 | Exacerbated CCl4‐induced liver fibrosis linked to enhanced inflammatory infiltrate | Lodder et al (2015), Habib et al (2019) |”
From Autophagy in major human diseases (2021) · cites this paper as Lodder et al, 2015
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Metadata
- Authors
- Lodder, J., Denaës, T., Chobert, M.-N., Wan, J., El-Benna, J., Pawlotsky, J.-M., Lotersztajn, S., & Teixeira-Clerc, F.
- Affiliations
- Inserm (FR)
- INSERM UMR-1149; Centre de Recherche sur l'Inflammation; Paris; France
- Corresponding author
- Lotersztajn, Sophie
- Teixeira-Clerc, Fatima
- Venue
- Autophagy
- Publisher
- Informa UK Limited
- Published
- 2015-08-03
- Volume
- 11
- Issue
- 8
- Pages
- 1280-1292
- ISSN
- 1554-8627 (ISSN-L)
- 1554-8635
- PMC
- PMC4590651
- OpenAlex
- W1807054663
- Cited by
- 266
- References
- 43
- Citations by year
- 2026: 14 · 2025: 22 · 2024: 21 · 2023: 31 · 2022: 23 · 2021: 34 · 2020: 25 · 2019: 25 · 2018: 28 · 2017: 19 · 2016: 17 · 2015: 5
- FWCI
- 13.63
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Autophagy (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Agence Nationale de la Recherche (ANR-11-IDEX-0005)
- Institut National de la Santé et de la Recherche Médicale (ANR-11-Idex-005-02)
- Topics
- Health Sciences › Medicine › Hepatology › Liver physiology and pathology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Autophagy in Disease and Therapy
- Health Sciences › Medicine › Hepatology › Liver Diseases and Immunity
- Keywords
- macrophage autophagy, liver fibrosis, ATG5, carbon tetrachloride-induced liver injury, interleukin-1 alpha, IL-1β, interleukin-1 receptor antagonist, hepatic myofibroblasts, reactive oxygen species, chronic inflammation, anti-inflammatory pathways
- MeSH terms
- Autophagy-Related Protein 5, Animals, Autophagy, Carbon Tetrachloride, Disease Models, Animal, Inflammation, Kupffer Cells, Liver, Liver Cirrhosis, Lysosomes, Macrophages, Microtubule-Associated Proteins, Mutation, Neutrophils, Recombinant Proteins, Culture Media, Conditioned, Reactive Oxygen Species, Macrophages, Peritoneal, Mice, Knockout, Cell Lineage, Mice, Interleukin-1alpha, Interleukin-1beta, Myofibroblasts
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