Inflammasome activation and function in liver disease (original) (raw)
Janeway, C. A., Jr Approaching the asymptote? Evolution and revolution in immunology. Cold Spring Harb. Symp. Quant. Biol.54, 1–13 (1989). ArticleCASPubMed Google Scholar
Matzinger, P. Tolerance, danger, and the extended family. Annu. Rev. Immunol.12, 991–1045 (1994). ArticleCASPubMed Google Scholar
Seki, E. & Brenner, D. A. Toll-like receptors and adaptor molecules in liver disease: update. Hepatology48, 322–335 (2008). ArticleCASPubMed Google Scholar
Chassaing, B., Etienne-Mesmin, L. & Gewirtz, A. T. Microbiota-liver axis in hepatic disease. Hepatology59, 328–339 (2014). ArticleCASPubMed Google Scholar
Schwabe, R. F., Seki, E. & Brenner, D. A. Toll-like receptor signaling in the liver. Gastroenterology130, 1886–1900 (2006). ArticleCASPubMed Google Scholar
Szabo, G., Dolganiuc, A. & Mandrekar, P. Pattern recognition receptors: a contemporary view on liver diseases. Hepatology44, 287–298 (2006). ArticleCASPubMed Google Scholar
Kubes, P. & Mehal, W. Z. Sterile inflammation in the liver. Gastroenterology143, 1158–1172 (2012). ArticleCASPubMed Google Scholar
Ogura, Y., Sutterwala, F. S. & Flavell, R. A. The inflammasome: first line of the immune response to cell stress. Cell126, 659–662 (2006). ArticleCASPubMed Google Scholar
Martinon, F., Burns, K. & Tschopp, J. The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-β. Mol. Cell10, 417–426 (2002). ArticleCASPubMed Google Scholar
Kumar, H., Kawai, T. & Akira, S. Pathogen recognition by the innate immune system. Int. Rev. Immunol.30, 16–34 (2011). ArticleCASPubMed Google Scholar
Mandrekar, P., Ambade, A., Lim, A., Szabo, G. & Catalano, D. An essential role for monocyte chemoattractant protein-1 in alcoholic liver injury: regulation of proinflammatory cytokines and hepatic steatosis in mice. Hepatology54, 2185–2197 (2011). ArticleCASPubMedPubMed Central Google Scholar
Petrasek, J. et al. IL-1 receptor antagonist ameliorates inflammasome-dependent alcoholic steatohepatitis in mice. J. Clin. Invest.122, 3476–3489 (2012). ArticleCASPubMedPubMed Central Google Scholar
Miura, K. et al. Toll-like receptor 9 promotes steatohepatitis by induction of interleukin-1β in mice. Gastroenterology139, 323–334 (2010). ArticleCASPubMedPubMed Central Google Scholar
Mariathasan, S. et al. Cryopyrin activates the inflammasome in response to toxins and ATP. Nature440, 228–232 (2006). ArticleCASPubMed Google Scholar
Rock, K. L., Kataoka, H. & Lai, J. J. Uric acid as a danger signal in gout and its comorbidities. Nat. Rev. Rheumatol.9, 13–23 (2013). ArticleCASPubMed Google Scholar
Csak, T. et al. Fatty acid and endotoxin activate inflammasomes in mouse hepatocytes that release danger signals to stimulate immune cells. Hepatology54, 133–144 (2011). ArticleCASPubMedPubMed Central Google Scholar
Matsuzaka, T. et al. Elovl6 promotes nonalcoholic steatohepatitis. Hepatology56, 2199–2208 (2012). ArticleCASPubMed Google Scholar
Wen, H. et al. Fatty acid-induced NLRP3-ASC inflammasome activation interferes with insulin signaling. Nat. Immunol.12, 408–415 (2011). ArticleCASPubMedPubMed Central Google Scholar
Vandanmagsar, B. et al. The NLRP3 inflammasome instigates obesity-induced inflammation and insulin resistance. Nat. Med.17, 179–188 (2011). ArticleCASPubMedPubMed Central Google Scholar
Shulga, N. & Pastorino, J. G. Hexokinase II binding to mitochondria is necessary for Kupffer cell activation and is potentiated by ethanol exposure. J. Biol. Chem.289, 26213–26225 (2014). ArticleCASPubMedPubMed Central Google Scholar
Petrasek, J., Dolganiuc, A., Csak, T., Kurt-Jones, E. A. & Szabo, G. Type I interferons protect from Toll-like receptor 9-associated liver injury and regulate IL-1 receptor antagonist in mice. Gastroenterology140, 697–708.e4 (2011). ArticleCASPubMed Google Scholar
Granowitz, E. V., Vannier, E., Poutsiaka, D. D. & Dinarello, C. A. Effect of interleukin-1 (IL-1) blockade on cytokine synthesis: II. IL-1 receptor antagonist inhibits lipopolysaccharide-induced cytokine synthesis by human monocytes. Blood79, 2364–2369 (1992). CASPubMed Google Scholar
Granowitz, E. V., Clark, B. D., Vannier, E., Callahan, M. V. & Dinarello, C. A. Effect of interleukin-1 (IL-1) blockade on cytokine synthesis: I. IL-1 receptor antagonist inhibits IL-1-induced cytokine synthesis and blocks the binding of IL-1 to its type II receptor on human monocytes. Blood79, 2356–2363 (1992). CASPubMed Google Scholar
Dinarello, C. A. Immunological and inflammatory functions of the interleukin-1 family. Annu. Rev. Immunol.27, 519–550 (2009). ArticleCASPubMed Google Scholar
Cosgrove, B. D. et al. An inducible autocrine cascade regulates rat hepatocyte proliferation and apoptosis responses to tumor necrosis factor-α. Hepatology48, 276–288 (2008). ArticleCASPubMedPubMed Central Google Scholar
Dinarello, C. A. The role of the interleukin-1-receptor antagonist in blocking inflammation mediated by interleukin-1. N. Engl. J. Med.343, 732–734 (2000). ArticleCASPubMed Google Scholar
Gross, O., Thomas, C. J., Guarda, G. & Tschopp, J. The inflammasome: an integrated view. Immunol. Rev.243, 136–151 (2011). ArticleCASPubMed Google Scholar
Davis, B. K., Wen, H. & Ting, J. P. The inflammasome NLRs in immunity, inflammation, and associated diseases. Annu. Rev. Immunol.29, 707–735 (2011). ArticleCASPubMedPubMed Central Google Scholar
Guma, M. et al. Caspase 1-independent activation of interleukin-1β in neutrophil-predominant inflammation. Arthritis Rheum.60, 3642–3650 (2009). ArticleCASPubMedPubMed Central Google Scholar
Joosten, L. A. et al. Inflammatory arthritis in caspase 1 gene-deficient mice: contribution of proteinase 3 to caspase 1-independent production of bioactive interleukin-1β. Arthritis Rheum.60, 3651–3662 (2009). ArticleCASPubMedPubMed Central Google Scholar
Greten, F. R. et al. NF-κB is a negative regulator of IL-1β secretion as revealed by genetic and pharmacological inhibition of IKKβ. Cell130, 918–931 (2007). ArticleCASPubMedPubMed Central Google Scholar
Mayer-Barber, K. D. et al. Caspase-1 independent IL-1β production is critical for host resistance to mycobacterium tuberculosis and does not require TLR signaling in vivo. J. Immunol.184, 3326–3330 (2010). ArticleCASPubMedPubMed Central Google Scholar
Fantuzzi, G. et al. Response to local inflammation of IL-1 beta-converting enzyme- deficient mice. J. Immunol.158, 1818–1824 (1997). CASPubMed Google Scholar
Coeshott, C. et al. Converting enzyme-independent release of tumor necrosis factor α and IL-1β from a stimulated human monocytic cell line in the presence of activated neutrophils or purified proteinase 3. Proc. Natl Acad. Sci. USA96, 6261–6266 (1999). ArticleCASPubMed Google Scholar
Kayagaki, N. et al. Noncanonical inflammasome activation by intracellular LPS independent of TLR4. Science341, 1246–1249 (2013). ArticleCASPubMed Google Scholar
Dinarello, C. A. Interleukin-18, a proinflammatory cytokine. Eur. Cytokine Netw.11, 483–486 (2000). CASPubMed Google Scholar
Imaeda, A. B. et al. Acetaminophen-induced hepatotoxicity in mice is dependent on Tlr9 and the Nalp3 inflammasome. J. Clin. Invest.119, 305–314 (2009). CASPubMedPubMed Central Google Scholar
Serti, E. et al. Monocytes activate natural killer cells via inflammasome-induced interleukin 18 in response to hepatitis C virus replication. Gastroenterology147, 209–220 (2014). ArticleCASPubMedPubMed Central Google Scholar
Arshad, M. I., Piquet-Pellorce, C. & Samson, M. IL-33 and HMGB1 alarmins: sensors of cellular death and their involvement in liver pathology. Liver Int.32, 1200–1210 (2012). ArticleCASPubMed Google Scholar
Carriere, V. et al. IL-33, the IL-1-like cytokine ligand for ST2 receptor, is a chromatin-associated nuclear factor in vivo. Proc. Natl Acad. Sci. USA104, 282–287 (2007). ArticleCASPubMed Google Scholar
Schmitz, J. et al. IL-33, an interleukin-1-like cytokine that signals via the IL-1 receptor-related protein ST2 and induces T helper type 2-associated cytokines. Immunity23, 479–490 (2005). ArticleCASPubMed Google Scholar
Cayrol, C. & Girard, J. P. The IL-1-like cytokine IL-33 is inactivated after maturation by caspase-1. Proc. Natl Acad. Sci. USA106, 9021–9026 (2009). ArticleCASPubMed Google Scholar
Luzina, I. G. et al. Full-length IL-33 promotes inflammation but not Th2 response in vivo in an ST2-independent fashion. J. Immunol.189, 403–410 (2012). ArticleCASPubMedPubMed Central Google Scholar
Volarevic, V. et al. Protective role of IL-33/ST2 axis in Con A-induced hepatitis. J. Hepatol.56, 26–33 (2012). ArticleCASPubMed Google Scholar
Marvie, P. et al. Interleukin-33 overexpression is associated with liver fibrosis in mice and humans. J. Cell. Mol. Med.14, 1726–1739 (2010). ArticleCASPubMed Google Scholar
Yin, H. et al. Pretreatment with soluble ST2 reduces warm hepatic ischemia/reperfusion injury. Biochem. Biophys. Res. Commun.351, 940–946 (2006). ArticleCASPubMed Google Scholar
Amatucci, A. et al. Recombinant ST2 boosts hepatic Th2 response in vivo. J. Leukoc. Biol.82, 124–132 (2007). ArticleCASPubMed Google Scholar
Oboki, K. et al. IL-33 is a crucial amplifier of innate rather than acquired immunity. Proc. Natl Acad. Sci. USA107, 18581–18586 (2010). ArticleCASPubMed Google Scholar
Schroder, K., Zhou, R. & Tschopp, J. The NLRP3 inflammasome: a sensor for metabolic danger? Science327, 296–300 (2010). ArticleCASPubMed Google Scholar
Csak, T. et al. Both bone marrow-derived and non-bone marrow-derived cells contribute to AIM2 and NLRP3 inflammasome activation in a MyD88-dependent manner in dietary steatohepatitis. Liver Int.34, 1402–1413 (2014). ArticleCASPubMedPubMed Central Google Scholar
Bauernfeind, F. G. et al. Cutting edge: NF-κB activating pattern recognition and cytokine receptors license NLRP3 inflammasome activation by regulating NLRP3 expression. J. Immunol.183, 787–791 (2009). ArticleCASPubMedPubMed Central Google Scholar
Martinon, F., Petrilli, V., Mayor, A., Tardivel, A. & Tschopp, J. Gout-associated uric acid crystals activate the NALP3 inflammasome. Nature440, 237–241 (2006). ArticleCASPubMed Google Scholar
Iyer, S. S. et al. Necrotic cells trigger a sterile inflammatory response through the Nlrp3 inflammasome. Proc. Natl Acad. Sci. USA106, 20388–20393 (2009). ArticleCASPubMed Google Scholar
Ioannou, G. N. et al. Cholesterol-lowering drugs cause dissolution of cholesterol crystals and disperse Kupffer cell crown-like structures during resolution of NASH. J. Lipid Res.56, 277–285 (2014). ArticleCASPubMed Google Scholar
Zhou, R., Yazdi, A. S., Menu, P. & Tschopp, J. A role for mitochondria in NLRP3 inflammasome activation. Nature469, 221–225 (2011). ArticleCAS Google Scholar
Kim, H. Y., Kim, S. J. & Lee, S. M. Activation of NLRP3 and AIM2 inflammasomes in Kupffer cells in hepatic ischemia/reperfusion. FEBS J.282, 259–270 (2014). ArticleCASPubMed Google Scholar
Muruve, D. A. et al. The inflammasome recognizes cytosolic microbial and host DNA and triggers an innate immune response. Nature452, 103–107 (2008). ArticleCAS Google Scholar
Nakahira, K. et al. Autophagy proteins regulate innate immune responses by inhibiting the release of mitochondrial DNA mediated by the NALP3 inflammasome. Nat. Immunol.12, 222–230 (2011). ArticleCASPubMed Google Scholar
Rathinam, V. A. et al. The AIM2 inflammasome is essential for host defense against cytosolic bacteria and DNA viruses. Nat. Immunol.11, 395–402 (2010). ArticleCASPubMedPubMed Central Google Scholar
Poeck, H. et al. Recognition of RNA virus by RIG-I results in activation of CARD9 and inflammasome signaling for interleukin 1 β production. Nat. Immunol.11, 63–69 (2010). ArticleCASPubMed Google Scholar
Lozano-Ruiz, B. et al. Absent in melanoma 2 triggers a heightened inflammasome response in ascitic fluid macrophages of patients with cirrhosis. J. Hepatol.62, 64–71 (2015). ArticleCASPubMed Google Scholar
Grenier, J. M. et al. Functional screening of five PYPAF family members identifies PYPAF5 as a novel regulator of NF-kappaB and caspase-1. FEBS Lett.530, 73–78 (2002). ArticleCASPubMed Google Scholar
Anand, P. K. et al. NLRP6 negatively regulates innate immunity and host defence against bacterial pathogens. Nature488, 389–393 (2012). ArticleCASPubMedPubMed Central Google Scholar
Chen, G. Y., Liu, M., Wang, F., Bertin, J. & Nunez, G. A functional role for Nlrp6 in intestinal inflammation and tumorigenesis. J. Immunol.186, 7187–7194 (2011). ArticleCASPubMedPubMed Central Google Scholar
Normand, S. et al. Nod-like receptor pyrin domain-containing protein 6 (NLRP6) controls epithelial self-renewal and colorectal carcinogenesis upon injury. Proc. Natl Acad. Sci. USA108, 9601–9606 (2011). ArticleCASPubMed Google Scholar
Wlodarska, M. et al. NLRP6 inflammasome orchestrates the colonic host-microbial interface by regulating goblet cell mucus secretion. Cell156, 1045–1059 (2014). ArticleCASPubMedPubMed Central Google Scholar
O'Shea, R. S., Dasarathy, S., McCullough, A. J., Practice Guideline Committee of the American Association for the Study of Liver, D. & Practice Parameters Committee of the American College of, G. Alcoholic liver disease. Hepatology51, 307–328 (2010). ArticlePubMed Google Scholar
Peng, Y., French, B. A., Tillman, B., Morgan, T. R. & French, S. W. The inflammasome in alcoholic hepatitis: Its relationship with Mallory-Denk body formation. Exp. Mol. Pathol.97, 305–313 (2014). ArticleCASPubMedPubMed Central Google Scholar
McClain, C. J. et al. Serum interleukin-1 (IL-1) activity in alcoholic hepatitis. Life Sci.39, 1479–1485 (1986). ArticleCASPubMed Google Scholar
Xiao, J. et al. Lycium barbarum polysaccharide attenuates alcoholic cellular injury through TXNIP-NLRP3 inflammasome pathway. Int. J. Biol. Macromol.69, 73–78 (2014). ArticleCASPubMed Google Scholar
Clemens, D. L. Use of cultured cells to study alcohol metabolism. Alcohol Res. Health29, 291–295 (2006). PubMedPubMed Central Google Scholar
Inokuchi, S. et al. Toll-like receptor 4 mediates alcohol-induced steatohepatitis through bone marrow-derived and endogenous liver cells in mice. Alcohol Clin. Exp. Res.35, 1509–1518 (2011). CASPubMedPubMed Central Google Scholar
Hoek, J. B., Cahill, A. & Pastorino, J. G. Alcohol and mitochondria: a dysfunctional relationship. Gastroenterology122, 2049–2063 (2002). ArticleCASPubMedPubMed Central Google Scholar
Lieber, C. S., Jones, D. P., Losowsky, M. S. & Davidson, C. S. Interrelation of uric acid and ethanol metabolism in man. J. Clin. Invest.41, 1863–1870 (1962). ArticleCASPubMedPubMed Central Google Scholar
Stiburkova, B., Pavlikova, M., Sokolova, J. & Kozich, V. Metabolic syndrome, alcohol consumption and genetic factors are associated with serum uric acid concentration. PLoS ONE9, e97646 (2014). ArticleCASPubMedPubMed Central Google Scholar
Petrasek J. et al. Metabolic danger signals, uric acid and ATP mediate inflammatory cross-talk between hepatocytes and immune cells in alcoholic liver disease. J. Leukoc. Biol.http://dx.doi.org/10.1189/jlb.3AB1214-590R.
Kono, H. et al. Allopurinol prevents early alcohol-induced liver injury in rats. J. Pharmacol. Exp. Ther.293, 296–303 (2000). CASPubMed Google Scholar
Ge, X. et al. High mobility group box-1 (HMGB1) participates in the pathogenesis of alcoholic liver disease (ALD). J. Biol. Chem.289, 22672–22691 (2014). ArticleCASPubMedPubMed Central Google Scholar
Yu, M. et al. HMGB1 signals through toll-like receptor (TLR) 4 and TLR2. Shock26, 174–179 (2006). ArticleCASPubMed Google Scholar
Esser, N., Legrand-Poels, S., Piette, J., Scheen, A. J. & Paquot, N. Inflammation as a link between obesity, metabolic syndrome and type 2 diabetes. Diabetes Res. Clin. Pract.105, 141–150 (2014). ArticleCASPubMed Google Scholar
Lee, H. M. et al. Upregulated NLRP3 inflammasome activation in patients with type 2 diabetes. Diabetes62, 194–204 (2013). ArticleCASPubMed Google Scholar
Masters, S. L. et al. Activation of the NLRP3 inflammasome by islet amyloid polypeptide provides a mechanism for enhanced IL-1β in type 2 diabetes. Nat. Immunol.11, 897–904 (2010). ArticleCASPubMedPubMed Central Google Scholar
Ganz, M., Csak, T. & Szabo, G. High fat diet feeding results in gender specific steatohepatitis and inflammasome activation. World J. Gastroenterol.20, 8525–8534 (2014). ArticleCASPubMedPubMed Central Google Scholar
Wree, A. et al. NLRP3 inflammasome activation results in hepatocyte pyroptosis, liver inflammation, and fibrosis in mice. Hepatology59, 898–910 (2014). ArticleCASPubMedPubMed Central Google Scholar
Wree, A. et al. NLRP3 inflammasome activation is required for fibrosis development in NAFLD. J. Mol. Med. (Berl.)92, 1069–1082 (2014). ArticleCAS Google Scholar
Mehal, W. Z. The Gordian Knot of dysbiosis, obesity and NAFLD. Nat. Rev. Gastroenterol. Hepatol.10, 637–644 (2013). ArticlePubMed Google Scholar
Pan, J. J. & Fallon, M. B. Gender and racial differences in nonalcoholic fatty liver disease. World J. Hepatol.6, 274–283 (2014). ArticlePubMedPubMed Central Google Scholar
Csak, T. et al. Deficiency in myeloid differentiation factor-2 and toll-like receptor 4 expression attenuates nonalcoholic steatohepatitis and fibrosis in mice. Am. J. Physiol. Gastrointest. Liver Physiol.300, G433–G441 (2011). ArticleCASPubMedPubMed Central Google Scholar
Petrasek, J., Csak, T., Ganz, M. & Szabo, G. Differences in innate immune signaling between alcoholic and non-alcoholic steatohepatitis. J. Gastroenterol. Hepatol.28, 93–98 (2013). ArticleCASPubMedPubMed Central Google Scholar
Messina, J. P. et al. Global distribution and prevalence of hepatitis C virus genotypes. Hepatology61, 77–87 (2015). ArticlePubMed Google Scholar
Dolganiuc, A. et al. Viral and host factors induce macrophage activation and loss of toll-like receptor tolerance in chronic HCV infection. Gastroenterology133, 1627–1636 (2007). ArticleCASPubMedPubMed Central Google Scholar
Chattergoon, M. A. et al. HIV and HCV activate the inflammasome in monocytes and macrophages via endosomal Toll-like receptors without induction of type 1 interferon. PLoS Pathog.10, e1004082 (2014). ArticleCASPubMedPubMed Central Google Scholar
Jaeschke, H., Williams, C. D., Ramachandran, A. & Bajt, M. L. Acetaminophen hepatotoxicity and repair: the role of sterile inflammation and innate immunity. Liver Int.32, 8–20 (2012). ArticleCASPubMed Google Scholar
McGill, M. R. et al. The mechanism underlying acetaminophen-induced hepatotoxicity in humans and mice involves mitochondrial damage and nuclear DNA fragmentation. J. Clin. Invest.122, 1574–1583 (2012). ArticleCASPubMedPubMed Central Google Scholar
McGill, M. R. et al. Serum mitochondrial biomarkers and damage-associated molecular patterns are higher in acetaminophen overdose patients with poor outcome. Hepatology60, 1336–1345 (2014). ArticleCASPubMedPubMed Central Google Scholar
Williams, C. D., Koerner, M. R., Lampe, J. N., Farhood, A. & Jaeschke, H. Mouse strain-dependent caspase activation during acetaminophen hepatotoxicity does not result in apoptosis or modulation of inflammation. Toxicol. Appl. Pharmacol.257, 449–458 (2011). ArticleCASPubMedPubMed Central Google Scholar
Jaeschke, H., Williams, C. D. & Farhood, A. No evidence for caspase-dependent apoptosis in acetaminophen hepatotoxicity. Hepatology53, 718–719 (2011). ArticlePubMed Google Scholar
Williams, C. D., Farhood, A. & Jaeschke, H. Role of caspase-1 and interleukin-1β in acetaminophen-induced hepatic inflammation and liver injury. Toxicol. Appl. Pharmacol.247, 169–178 (2010). ArticleCASPubMedPubMed Central Google Scholar
Sander, L. E. & Blander, J. M. Inflammasome and toll-like receptor 9: Partners in crime in toxic liver injury. Hepatology49, 2119–2121 (2009). ArticleCASPubMed Google Scholar
Chen, C. J. et al. Identification of a key pathway required for the sterile inflammatory response triggered by dying cells. Nat. Med.13, 851–856 (2007). ArticleCASPubMed Google Scholar
Hoque, R. et al. P2X7 receptor-mediated purinergic signaling promotes liver injury in acetaminophen hepatotoxicity in mice. Am. J. Physiol. Gastrointest. Liver Physiol.302, G1171–G1179 (2012). ArticleCASPubMedPubMed Central Google Scholar
Williams, C. D. et al. Role of the Nalp3 inflammasome in acetaminophen-induced sterile inflammation and liver injury. Toxicol. Appl. Pharmacol.252, 289–297 (2011). ArticleCASPubMedPubMed Central Google Scholar
Kataoka, H., Kono, H., Patel, Z. & Rock, K. L. Evaluation of the contribution of multiple DAMPs and DAMP receptors in cell death-induced sterile inflammatory responses. PLoS ONE9, e104741 (2014). ArticleCASPubMedPubMed Central Google Scholar
Kono, H., Chen, C. J., Ontiveros, F. & Rock, K. L. Uric acid promotes an acute inflammatory response to sterile cell death in mice. J. Clin. Invest.120, 1939–1949 (2010). ArticleCASPubMedPubMed Central Google Scholar
Antoniades, C. G. et al. Secretory leukocyte protease inhibitor: a pivotal mediator of anti-inflammatory responses in acetaminophen-induced acute liver failure. Hepatology59, 1564–1576 (2014). ArticleCASPubMed Google Scholar
Abu-Amara, M. et al. Liver ischemia/reperfusion injury: processes in inflammatory networks—a review. Liver Transpl.16, 1016–1032 (2010). ArticlePubMed Google Scholar
Weigand, K. et al. Ischemia/Reperfusion injury in liver surgery and transplantation: pathophysiology. HPB Surg.2012, 176723 (2012). ArticlePubMedPubMed Central Google Scholar
Zhai, Y., Petrowsky, H., Hong, J. C., Busuttil, R. W. & Kupiec-Weglinski, J. W. Ischaemia–reperfusion injury in liver transplantation—from bench to bedside. Nat. Rev. Gastroenterol. Hepatol.10, 79–89 (2013). ArticleCASPubMed Google Scholar
Jaeschke, H. Reactive oxygen and mechanisms of inflammatory liver injury: Present concepts. J. Gastroenterol. Hepatol.26, 173–179 (2011). ArticleCASPubMed Google Scholar
Gabrielli, M. et al. Steatotic livers. Can. we use them in OLTX? Outcome data from a prospective baseline liver biopsy study. Ann. Hepatol.11, 891–898 (2012). ArticlePubMed Google Scholar
Farrell, G. C., Teoh, N. C. & McCuskey, R. S. Hepatic microcirculation in fatty liver disease. Anat. Rec. (Hoboken)291, 684–692 (2008). Article Google Scholar
DuBray, B. J. Jr. et al. BH3-only proteins contribute to steatotic liver ischemia-reperfusion injury. J. Surg. Res.194, 653–658 (2014). ArticleCASPubMedPubMed Central Google Scholar
Zhu, P. et al. Gene silencing of NALP3 protects against liver ischemia-reperfusion injury in mice. Hum. Gene Ther.22, 853–864 (2011). ArticleCASPubMed Google Scholar
Huang, H. et al. Histones activate the NLRP3 inflammasome in Kupffer cells during sterile inflammatory liver injury. J. Immunol.191, 2665–2679 (2013). ArticleCASPubMedPubMed Central Google Scholar
Kamo, N. et al. ASC/caspase-1/IL-1β signaling triggers inflammatory responses by promoting HMGB1 induction in liver ischemia/reperfusion injury. Hepatology58, 351–362 (2013). ArticleCASPubMedPubMed Central Google Scholar
Shimizu, S. et al. Involvement of ICE family proteases in apoptosis induced by reoxygenation of hypoxic hepatocytes. Am. J. Physiol.271, G949–G958 (1996). CASPubMed Google Scholar
Shito, M. et al. Interleukin 1 receptor blockade reduces tumor necrosis factor production, tissue injury, and mortality after hepatic ischemia-reperfusion in the rat. Transplantation63, 143–148 (1997). ArticleCASPubMed Google Scholar
Harada, H. et al. Transfer of the interleukin-1 receptor antagonist gene into rat liver abrogates hepatic ischemia-reperfusion injury. Transplantation74, 1434–1441 (2002). ArticleCASPubMed Google Scholar
Takeuchi, D. et al. Interleukin 18 causes hepatic ischemia/reperfusion injury by suppressing anti-inflammatory cytokine expression in mice. Hepatology39, 699–710 (2004). ArticleCASPubMed Google Scholar
Inoue, Y. et al. NLRP3 regulates neutrophil functions and contributes to hepatic ischemia-reperfusion injury independently of inflammasomes. J. Immunol.192, 4342–4351 (2014). ArticleCASPubMed Google Scholar
Watanabe, A. et al. Inflammasome-mediated regulation of hepatic stellate cells. Am. J. Physiol. Gastrointest. Liver Physiol.296, G1248–G1257 (2009). ArticleCASPubMedPubMed Central Google Scholar
Ouyang, X., Ghani, A. & Mehal, W. Z. Inflammasome biology in fibrogenesis. Biochim. Biophys. Acta1832, 979–988 (2013). ArticleCASPubMed Google Scholar
Weiskirchen, R. & Tacke, F. Cellular and molecular functions of hepatic stellate cells in inflammatory responses and liver immunology. Hepatobiliary Surg. Nutr.3, 344–363 (2014). PubMedPubMed Central Google Scholar
Seki, E. et al. TLR4 enhances TGF-β signaling and hepatic fibrosis. Nat. Med.13, 1324–1332 (2007). ArticleCASPubMed Google Scholar
Khan, F., Peltekian, K. M. & Peterson, T. C. Effect of interferon-α, ribavirin, pentoxifylline, and interleukin-18 antibody on hepatitis C sera-stimulated hepatic stellate cell proliferation. J. Interferon Cytokine Res.28, 643–651 (2008). ArticleCASPubMed Google Scholar
Gieling, R. G., Wallace, K. & Han, Y. P. Interleukin-1 participates in the progression from liver injury to fibrosis. Am. J. Physiol. Gastrointest. Liver Physiol.296, G1324–G1331 (2009). ArticleCASPubMedPubMed Central Google Scholar
de Roos, B. et al. Attenuation of inflammation and cellular stress-related pathways maintains insulin sensitivity in obese type I interleukin-1 receptor knockout mice on a high-fat diet. Proteomics9, 3244–3256 (2009). ArticleCASPubMed Google Scholar
Kamari, Y. et al. Lack of interleukin-1α or interleukin-1β inhibits transformation of steatosis to steatohepatitis and liver fibrosis in hypercholesterolemic mice. J. Hepatol.55, 1086–1094 (2011). ArticleCASPubMedPubMed Central Google Scholar
Isoda, K. et al. Deficiency of interleukin-1 receptor antagonist deteriorates fatty liver and cholesterol metabolism in hypercholesterolemic mice. J. Biol. Chem.280, 7002–7009 (2005). ArticleCASPubMed Google Scholar
Dixon, L. J., Flask, C. A., Papouchado, B. G., Feldstein, A. E. & Nagy, L. E. Caspase-1 as a central regulator of high fat diet-induced non-alcoholic steatohepatitis. PLoS ONE8, e56100 (2013). ArticleCASPubMedPubMed Central Google Scholar
Samstad, E. O. et al. Cholesterol crystals induce complement-dependent inflammasome activation and cytokine release. J. Immunol.192, 2837–2845 (2014). ArticleCASPubMedPubMed Central Google Scholar
Wen, H., Ting, J. P. & O'Neill, L. A. A role for the NLRP3 inflammasome in metabolic diseases—did Warburg miss inflammation? Nat. Immunol.13, 352–357 (2012). ArticleCASPubMedPubMed Central Google Scholar
Ganz, M., Csak, T., Nath, B. & Szabo, G. Lipopolysaccharide induces and activates the Nalp3 inflammasome in the liver. World J. Gastroenterol.17, 4772–4778 (2011). ArticleCASPubMedPubMed Central Google Scholar
Tschopp, J. & Schroder, K. NLRP3 inflammasome activation: the convergence of multiple signalling pathways on ROS production? Nat. Rev. Immunol.10, 210–215 (2010). ArticleCASPubMed Google Scholar
Petrasek, J. et al. STING-IRF3 pathway links endoplasmic reticulum stress with hepatocyte apoptosis in early alcoholic liver disease. Proc. Natl Acad. Sci. USA110, 16544–16549 (2013). ArticleCASPubMed Google Scholar
Purohit, V. et al. Alcohol, intestinal bacterial growth, intestinal permeability to endotoxin, and medical consequences: summary of a symposium. Alcohol42, 349–361 (2008). ArticleCASPubMedPubMed Central Google Scholar
Neuman, M. G. et al. Mechanisms of alcoholic liver disease: cytokines. Alcohol Clin. Exp. Res.25, 251S–253S (2001). ArticleCASPubMed Google Scholar
Cohen, J. I., Roychowdhury, S., McMullen, M. R., Stavitsky, A. B. & Nagy, L. E. Complement and alcoholic liver disease: role of C1q in the pathogenesis of ethanol-induced liver injury in mice. Gastroenterology139, 664–674 (2010). ArticleCASPubMedPubMed Central Google Scholar
Roychowdhury, S. et al. An early complement-dependent and TLR-4-independent phase in the pathogenesis of ethanol-induced liver injury in mice. Hepatology49, 1326–1334 (2009). ArticleCASPubMedPubMed Central Google Scholar
Stranges, S. et al. Differential effects of alcohol drinking pattern on liver enzymes in men and women. Alcohol Clin. Exp. Res.28, 949–956 (2004). ArticleCASPubMed Google Scholar
Hatton, J. et al. Drinking patterns, dependency and life-time drinking history in alcohol-related liver disease. Addiction104, 587–592 (2009). ArticlePubMed Google Scholar
Askgaard, G. et al. Alcohol drinking pattern and risk of alcoholic liver cirrhosis: a prospective cohort study. J. Hepatol.62, 1061–1067 (2015). ArticlePubMed Google Scholar
Csak, T. et al. Mitochondrial antiviral signaling protein defect links impaired antiviral response and liver injury in steatohepatitis in mice. Hepatology53, 1917–1931 (2011). ArticleCASPubMedPubMed Central Google Scholar
Kohli, R. et al. High-fructose, medium chain trans fat diet induces liver fibrosis and elevates plasma coenzyme Q9 in a novel murine model of obesity and nonalcoholic steatohepatitis. Hepatology52, 934–944 (2010). ArticleCASPubMedPubMed Central Google Scholar
Day, C. P. & James, O. F. Steatohepatitis: a tale of two “hits”? Gastroenterology114, 842–845 (1998). ArticleCASPubMed Google Scholar
Tilg, H. & Moschen, A. R. Evolution of inflammation in nonalcoholic fatty liver disease: the multiple parallel hits hypothesis. Hepatology52, 1836–1846 (2010). ArticleCASPubMed Google Scholar
Linton, S. D. et al. First-in-class pan caspase inhibitor developed for the treatment of liver disease. J. Med. Chem.48, 6779–6782 (2005). ArticleCASPubMed Google Scholar
Shiffman, M. L. et al. Clinical trial: the efficacy and safety of oral PF-03491390, a pancaspase inhibitor—a randomized placebo-controlled study in patients with chronic hepatitis, C. Aliment. Pharmacol. Ther.31, 969–978 (2010). CASPubMed Google Scholar
Baskin-Bey, E. S. et al. Clinical trial of the pan-caspase inhibitor, IDN-6556, in human liver preservation injury. Am. J. Transplant7, 218–225 (2007). ArticleCASPubMed Google Scholar
Pockros, P. J. et al. Oral IDN-6556, an antiapoptotic caspase inhibitor, may lower aminotransferase activity in patients with chronic hepatitis, C. Hepatology46, 324–329 (2007). ArticleCASPubMed Google Scholar
MacKenzie, S. H., Schipper, J. L. & Clark, A. C. The potential for caspases in drug discovery. Curr. Opin. Drug Discov. Devel.13, 568–576 (2010). CASPubMedPubMed Central Google Scholar
Church, L. D. & McDermott, M. F. Canakinumab, a fully-human mAb against IL-1β for the potential treatment of inflammatory disorders. Curr. Opin. Mol. Ther.11, 81–89 (2009). CASPubMed Google Scholar
US National Library of Medicine. ClinicalTrials.gov[online], (2014).
Mandrup-Poulsen, T., Pickersgill, L. & Donath, M. Y. Blockade of interleukin 1 in type 1 diabetes mellitus. Nat. Rev. Endocrinol.6, 158–166 (2010). ArticleCASPubMed Google Scholar
Howard, C. et al. Safety and tolerability of canakinumab, an IL-1β inhibitor, in type 2 diabetes mellitus patients: a pooled analysis of three randomised double-blind studies. Cardiovasc. Diabetol.13, 94 (2014). ArticleCASPubMedPubMed Central Google Scholar
Callus, B. A. & Vaux, D. L. Caspase inhibitors: viral, cellular and chemical. Cell Death Differ.14, 73–78 (2007). ArticleCASPubMed Google Scholar
Bhaskaracharya, A. et al. Probenecid blocks human P2X7 receptor-induced dye uptake via a pannexin-1 independent mechanism. PLoS ONE9, e93058 (2014). ArticleCASPubMedPubMed Central Google Scholar
Yang, S. J. & Lim, Y. Resveratrol ameliorates hepatic metaflammation and inhibits NLRP3 inflammasome activation. Metabolism63, 693–701 (2014). ArticleCASPubMed Google Scholar
Ambade, A., Catalano, D., Lim, A. & Mandrekar, P. Inhibition of heat shock protein (molecular weight 90 kDa) attenuates proinflammatory cytokines and prevents lipopolysaccharide-induced liver injury in mice. Hepatology55, 1585–1595 (2012). ArticleCASPubMedPubMed Central Google Scholar
Kayagaki, N. et al. Non-canonical inflammasome activation targets caspase-11. Nature479, 117–121 (2011). ArticleCASPubMed Google Scholar
Staun-Olsen, P., Bjorneboe, M., Prytz, H., Thomsen, A. C. & Orskov, F. Escherichia coli antibodies in alcoholic liver disease. Correlation to alcohol consumption, alcoholic hepatitis, and serum IgA. Scand. J. Gastroenterol.18, 889–896 (1983). ArticleCASPubMed Google Scholar
Petrasek, J., Csak, T. & Szabo, G. Toll-like receptors in liver disease. Adv. Clin. Chem.59, 155–201 (2013). ArticleCASPubMed Google Scholar
Bala, S., Marcos, M., Gattu, A., Catalano, D. & Szabo, G. Acute binge drinking increases serum endotoxin and bacterial DNA levels in healthy individuals. PLoS ONE9, e96864 (2014). ArticlePubMedPubMed Central Google Scholar
Bode, C. et al. Antibiotics regulate the immune response in both presence and absence of lipopolysaccharide through modulation of Toll-like receptors, cytokine production and phagocytosis in vitro. Int. Immunopharmacol.18, 27–34 (2014). ArticleCASPubMed Google Scholar
Li, P. et al. Mice deficient in IL-1 β-converting enzyme are defective in production of mature IL-1 β and resistant to endotoxic shock. Cell80, 401–411 (1995). ArticleCASPubMed Google Scholar
Wang, S. et al. Murine caspase-11, an ICE-interacting protease, is essential for the activation of ICE. Cell92, 501–509 (1998). ArticleCASPubMed Google Scholar
McGill, M. R. et al. Argininosuccinate synthetase as a plasma biomarker of liver injury after acetaminophen overdose in rodents and humans. Biomarkers19, 222–230 (2014). ArticleCASPubMedPubMed Central Google Scholar
Williams, C. D. et al. Neutrophil activation during acetaminophen hepatotoxicity and repair in mice and humans. Toxicol. Appl. Pharmacol.275, 122–133 (2014). ArticleCASPubMedPubMed Central Google Scholar
McGill, M. R. et al. Circulating acylcarnitines as biomarkers of mitochondrial dysfunction after acetaminophen overdose in mice and humans. Arch. Toxicol.88, 391–401 (2014). ArticleCASPubMed Google Scholar