NLRP3 inflammasome activation results in hepatocyte pyroptosis, liver inflammation, and fibrosis in mice
Open accessAbstract
Inflammasome activation plays a central role in the development of drug-induced and obesity-associated liver disease. However, the sources and mechanisms of inflammasome-mediated liver damage remain poorly understood. Our aim was to investigate the effect of NLRP3 inflammasome activation on the liver using novel mouse models. We generated global and myeloid cell-specific conditional mutant Nlrp3 knock-in mice expressing the D301N Nlrp3 mutation (ortholog of D303N in human NLRP3 ), resulting in a hyperactive NLRP3. To study the presence and significance of NLRP3-initiated pyroptotic cell death, we separated hepatocytes from nonparenchymal cells and developed a novel flow-cytometry–based (fluorescence-activated cell sorting; FACS) strategy to detect and quantify pyroptosis in vivo based on detection of active caspase 1 (Casp1)- and propidium iodide (PI)-positive cells. Liver inflammation was quantified histologically by FACS and gene expression analysis. Liver fibrosis was assessed by Sirius Red staining and quantitative polymerase chain reaction for markers of hepatic stellate cell (HSC) activation. NLRP3 activation resulted in shortened survival, poor growth, and severe liver inflammation; characterized by neutrophilic infiltration and HSC activation with collagen deposition in the liver. These changes were partially attenuated by treatment with anakinra, an interleukin-1 receptor antagonist. Notably, hepatocytes from global Nlrp3-mutant mice showed marked hepatocyte pyroptotic cell death, with more than a 5-fold increase in active Casp1/PI double-positive cells. Myeloid cell-restricted mutant NLRP3 activation resulted in a less-severe liver phenotype in the absence of detectable pyroptotic hepatocyte cell death. Conclusions : Our data demonstrate that global and, to a lesser extent, myeloid-specific NLRP3 inflammasome activation results in severe liver inflammation and fibrosis while identifying hepatocyte pyroptotic cell death as a novel mechanism of NLRP3-mediated liver damage. (HEPATOLOGY 2014;59:898–910)
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NLRP3 inflammasome activation is a key activator of liver inflammation in MASH.
“a key activator of liver inflammation in MASH (25, 26)”
From Lipid-associated macrophages' promotion of fibrosis resolution during MASH regression requires TREM2 (2024) · cites this paper as [26]
Hepatocyte death promotes fibrosis indirectly by activating inflammasomes and recruiting inflammatory cells, especially macrophages, which stimulate myofibroblasts and alter ECM turnover.
“Hepatocyte death promotes fibrosis indirectly through inflammasome activation and recruitment of inflammatory cells, especially macrophages, that stimulate myofibroblasts and alter extracellular matrix turnover (21, 22).”
From Found in translation—Fibrosis in metabolic dysfunction–associated steatohepatitis (MASH) (2023) · cites this paper as [22]
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- Authors
- Wree, A., Eguchi, A., McGeough, M. D., Pena, C. A., Johnson, C. D., Canbay, A., Hoffman, H. M., & Feldstein, A. E.
- Affiliations
- University of California San Diego (US)
- Essen University Hospital (DE)
- Corresponding author
- Feldstein, Ariel E.
- Venue
- Hepatology
- Published
- 2014-03
- Volume
- 59
- Issue
- 3
- Pages
- 898-910
- ISSN
- 0270-9139 (ISSN-L)
- PMC
- PMC4008151
- OpenAlex
- W2013907285
- Cited by
- 945
- References
- 41
- Citations by year
- 2026: 57 · 2025: 71 · 2024: 89 · 2023: 88 · 2022: 129 · 2021: 112 · 2020: 109 · 2019: 73 · 2018: 70 · 2017: 49 · 2016: 48 · 2015: 28 · 2014: 18 · 2013: 3 · 2012: 1
- FWCI
- 14.47
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Hepatology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- Deutsche Forschungsgemeinschaft
- National Institutes of Health
- National Institute of Allergy and Infectious Diseases (AI52430, R01AI052430)
- National Institute of Diabetes and Digestive and Kidney Diseases (R01DK082451, R01DK076852, DK082451, DK-076852)
- National Institute of Child Health and Human Development
- Eunice Kennedy Shriver National Institute of Child Health and Human Development
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Inflammasome and immune disorders
- Life Sciences › Pharmacology, Toxicology and Pharmaceutics › Pharmacology › Drug-Induced Hepatotoxicity and Protection
- Health Sciences › Medicine › Epidemiology › Liver Disease Diagnosis and Treatment
- Keywords
- NLRP3 inflammasome, pyroptosis, hepatocyte death, liver inflammation, liver fibrosis, caspase-1, hepatic stellate cells, myeloid cells, anakinra, interleukin-1 receptor antagonist, neutrophil infiltration, drug-induced liver injury
- MeSH terms
- NLR Family, Pyrin Domain-Containing 3 Protein, Animals, Carrier Proteins, Disease Models, Animal, Growth Disorders, Hepatitis, Humans, Liver Cirrhosis, Mice, Inbred C57BL, Mice, Mutant Strains, Neutrophils, Apoptosis, Point Mutation, Receptors, Interleukin-1, Antirheumatic Agents, Hepatocytes, Mice, Interleukin 1 Receptor Antagonist Protein, Hepatic Stellate Cells, Inflammasomes
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