Role of NLRP3 inflammasome in liver disease.
Adaptive Immunity
/ genetics
Animals
Caspase 1
/ metabolism
Cell Death
/ genetics
Disease Progression
Humans
Inflammasomes
/ genetics
Interleukin-18
/ metabolism
Interleukin-1beta
/ metabolism
Liver
/ metabolism
Liver Diseases
/ genetics
NLR Family, Pyrin Domain-Containing 3 Protein
/ metabolism
Signal Transduction
/ genetics
NLRP3
caspase-1
gasdermin D
inflammasome
interleukin 1β
liver disease
Journal
Journal of digestive diseases
ISSN: 1751-2980
Titre abrégé: J Dig Dis
Pays: Australia
ID NLM: 101302699
Informations de publication
Date de publication:
Aug 2020
Aug 2020
Historique:
received:
14
12
2019
revised:
17
05
2020
accepted:
23
06
2020
pubmed:
26
6
2020
medline:
4
6
2021
entrez:
26
6
2020
Statut:
ppublish
Résumé
Inflammasomes have become an important natural sensor of host immunity, and can protect various organs against pathogenic infections, metabolic syndromes, cellular stress and cancer metastasis. Inflammasomes are intracellular multi-protein complexes found in both parenchymal and non-parenchymal cells, stimulating the initiation of caspase-1 and interleukin (IL)-1β and IL-18 in response to cell danger signals. Inflammasomes induce cell death mechanisms. The potential role of NOD-like receptor protein 3 (NLRP3) inflammasome in alcoholic and non-alcoholic steatohepatitis, hepatitis, nanoparticle-induced liver injury and other liver diseases has recently attracted widespread attention from clinicians and researchers. In this review we summarize the role played by the NLRP3 inflammasome in molecular and pathophysiological mechanisms in the pathogenesis and progression of liver disease. This article aims to establish that targeting the NLRP3 inflammasome and other inflammasome components may make a significant therapeutic approach to the treatment of liver disease.
Identifiants
pubmed: 32585073
doi: 10.1111/1751-2980.12918
doi:
Substances chimiques
Inflammasomes
0
Interleukin-18
0
Interleukin-1beta
0
NLR Family, Pyrin Domain-Containing 3 Protein
0
Caspase 1
EC 3.4.22.36
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
430-436Informations de copyright
© 2020 Chinese Medical Association Shanghai Branch, Chinese Society of Gastroenterology, Renji Hospital Affiliated to Shanghai Jiaotong University School of Medicine and John Wiley & Sons Australia, Ltd.
Références
Mogensen TH. Pathogen recognition and inflammatory signaling in innate immune defenses. Clin Microbiol Rev. 2009;22(2):240-273.
Szabo G, Mandrekar P, Dolganiuc A. Innate immune response and hepatic inflammation. Semin Liver Dis. 2007;27(4):339-350.
Latz E, Xiao TS, Stutz A. Activation and regulation of the inflammasomes. Nat Rev Immunol. 2013;13(6):397-411.
Sharma D, Kanneganti TD. The cell biology of inflammasomes: mechanisms of inflammasome activation and regulation. J Cell Biol. 2016;213(6):617-629.
Davis BK, Wen H, Ting JP. The inflammasome NLRs in immunity, inflammation, and associated diseases. Annu Rev Immunol. 2011;29:707-735.
Ringelhan M, McKeating JA, Protzer U. Viral hepatitis and liver cancer. Philos Trans R Soc Lond B Bio Sci. 2017;372(1732):20160274.
Wu XQ, Dong L, Lin XH, Li J. Relevance of the NLRP3 inflammasome in the pathogenesis of chronic liver disease. Front Immunol. 2017;8:1728.
Wang SG, Wang H, Ding WX. Pyroptosis, a novel player for alcoholic hepatitis? Hepatology. 2018;67(5):1660-1662.
Li JJ, Xue JC, Wang DP, et al. Regulation of gasdermin D by miR-379-5p is involved in arsenite-induced activation of hepatic stellate cells and in fibrosis via secretion of IL-1beta from human hepatic cells. Metallomics. 2019;11(2):483-495.
Heo MJ, Kim TH, You JS, Blaya D, Sancho-Bru P, Kim SG. Alcohol dysregulates miR-148a in hepatocytes through FoxO1, facilitating pyroptosis via TXNIP overexpression. Gut. 2019;68(4):708-720.
Ertunc ME, Hotamisligil GS. Lipid signaling and lipotoxicity in metaflammation: indications for metabolic disease pathogenesis and treatment. J lipid Res. 2016;57(12):2099-2114.
Kim KH, Lee MS. Pathogenesis of nonalcoholic steatohepatitis and hormone-based therapeutic approaches. Front Endocrinol (Lausanne). 2018;9:485.
Caligiuri A, Gentilini A, Marra F. Molecular pathogenesis of NASH. Int J Mol Sci. 2016;17(9):1575.
Wan XY, Xu CF, Yu CH, Li YM. Role of NLRP3 inflammasome in the progression of NAFLD to NASH. Can J Gastroenterol Hepatol. 2016;2016:6489012.
Mridha AR, Wree A, Robertson AAB, et al. NLRP3 inflammasome blockade reduces liver inflammation and fibrosis in experimental NASH in mice. J Hepatol. 2017;66(5):1037-1046.
Beier JI, Banales JM. Pyroptosis: an inflammatory link between NAFLD and NASH with potential therapeutic implications. J Hepatol. 2018;68(4):643-645.
Khanova E, Wu R, Wang W, et al. Pyroptosis by caspase11/4-gasdermin-D pathway in alcoholic hepatitis in mice and patients. Hepatology. 2018;67(5):1737-1753.
Yang G, Lee HE, Lee JY. A pharmacological inhibitor of NLRP3 inflammasome prevents non-alcoholic fatty liver disease in a mouse model induced by high fat diet. Sci Rep. 2016;6:24399.
Kim SH, Kim G, Han DH, et al. Ezetimibe ameliorates steatohepatitis via AMP activated protein kinase-TFEB-mediated activation of autophagy and NLRP3 inflammasome inhibition. Autophagy. 2017;13(10):1767-1781.
Pierantonelli I, Rychlicki C, Agostinelli L, et al. Lack of NLRP3-inflammasome leads to gut-liver axis derangement, gut dysbiosis and a worsened phenotype in a mouse model of NAFLD. Sci Rep. 2017;7(1):12200.
Zhen Y, Zhang H. NLRP3 Inflammasome and inflammatory bowel disease. Front Immunol. 2019;9(10):276. https://doi.org/10.3389/fimmu.2019.00276.
Petruzziello A. Epidemiology of hepatitis B virus (HBV) and hepatitis C virus (HCV) related hepatocellular carcinoma. Open Virol J. 2018;12:26-32.
Negash AA, Olson RM, Griffin S, Gale Jr M. Modulation of calcium signaling pathway by hepatitis C virus core protein stimulates NLRP3 inflammasome activation. PLoS Pathog. 2019;15(2):e1007593.
Yu X, Lan PX, Hou XB, et al. HBV inhibits LPS-induced NLRP3 inflammasome activation and IL-1β production via suppressing the NF-κB pathway and ROS production. J Hepatol. 2017;66(4):693-702.
Yang Y, Tu ZK, Liu XK, Zhang P. Mononuclear phagocyte system in hepatitis C virus infection. World J Gastroenterol. 2018;24(44):4962-4973.
Negash AA, Ramos HJ, Crochet N, et al. IL-1β production through the NLRP3 inflammasome by hepatic macrophages links hepatitis C virus infection with liver inflammation and disease. PLoS Pathog. 2013;9(4):e1003330.
Serti E, Werner JM, Chattergoon M, Cox AL, Lohmann V, Rehermann B. Monocytes activate natural killer cells via inflammasome-induced interleukin 18 in response to hepatitis C virus replication. Gastroenterology. 2014;147(1):209-220.e3.
Saha B, Szabo G. Innate immune cell networking in hepatitis C virus infection. J Leukoc Biol. 2014;96(5):757-766.
Luan JY, Zhang XY, Wang SF, et al. NOD-like receptor protein 3 inflammasome-dependent IL-1β accelerated ConA-induced hepatitis. Front Immunol. 2018;9:758.
Lan PX, Fan YH, Zhao Y, et al. TNF superfamily receptor OX40 triggers invariant NKT cell pyroptosis and liver injury. J Clin Invest. 2017;127(6):2222-2234.
Wells RG. Cellular sources of extracellular matrix in hepatic fibrosis. Clin Liver Dis. 2008;12(4):759-768.
Watanabe A, Sohail MA, Gomes DA, et al. Inflammasome-mediated regulation of hepatic stellate cells. Am J Pysiol Gastrointest Liver Physiol. 2009;296(6):G1248-G1257.
Robert S, Gicquel T, Victoni T, et al. Involvement of matrix metalloproteinases (MMPs) and inflammasome pathway in molecular mechanisms of fibrosis. Biosci Rep. 2016;36(4):e00360.
Zhang WJ, Fang ZM, Liu WQ. NLRP3 inflammasome activation from Kupffer cells is involved in liver fibrosis of Schistosoma japonicum-infected mice via NF-κB. Parasit Vectors. 2019;12(1):29.
Higashi T, Friedman SL, Hoshida Y. Hepatic stellate cells as key target in liver fibrosis. Adv Drug Deliv Rev. 2017;121:27-42.
Iannitti RG, Napolioni V, Oikonomou V, et al. IL-1 receptor antagonist ameliorates inflammasome-dependent inflammation in murine and human cystic fibrosis. Nat Commun. 2016;7:10791.
Wree A, Eguchi A, McGeough MD, et al. NLRP3 inflammasome activation results in hepatocyte pyroptosis, liver inflammation, and fibrosis in mice. Hepatology. 2014;59(3):898-910.
Martinez GJ, Nurieva RI, Yang XO, Dong C. Regulation and function of proinflammatory TH17 cells. Ann N Y Acad Sci. 2008;1143:188-211.
Kuwabara T, Ishikawa F, Kondo M, Kakiuchi T. The role of IL-17 and related cytokines in inflammatory autoimmune diseases. Mediators Inflamm. 2017;2017:3908061.
Del Campo JA, Gallego P, Grande L. Role of inflammatory response in liver diseases: therapeutic strategies. World J Hepatol. 2018;10(1):1-7.
Mirahadi M, Ghanbarzadeh S, Ghorbani M, Gholizadeh A, Hamishehkar H. A review on the role of lipid-based nanoparticles in medical diagnosis and imaging. Ther Deliv. 2018;9(8):557-569.
Zhang X, Luan J, Chen W, et al. Mesoporous silica nanoparticles induced hepatotoxicity via NLRP3 inflammasome activation and caspase-1-dependent pyroptosis. Nanoscale. 2018;10(19):9141-9152.
Wu TS, Liang X, He KY, et al. The role of NLRP3 inflammasome activation in the neuroinflammatory responses to Ag2Se quantum dots in microglia. Nanoscale. 2019;11(43):20820-20836.
Taabazuing CY, Okondo MC, Bachovchin DA. Pyroptosis and apoptosis pathways engage in bidirectional crosstalk in monocytes and macrophages. Cell Chem Biol. 2017;24(4):507-514. e4.
Yao H, Zhang YJ, Liu L, et al. Inhibition of lanthanide nanocrystal-induced inflammasome activation in macrophages by a surface coating peptide through abrogation of ROS production and TRPM2-mediated Ca(2+) influx. Biomaterials. 2016;108:143-156.
Lian DW, Lai JQ, Wu YJ, et al. Cathepsin B-mediated NLRP3 Inflammasome formation and activation in angiotensin II-induced hypertensive mice: role of macrophage digestion dysfunction. Cell Physiol Biochem. 2018;50(4):1585-1600.
Minasyan H. Sepsis: mechanisms of bacterial injury to the patient. Scand J Trauma Resusc Emerg Med. 2019;27(1):19.
Yan J, Li S, Li SL. The role of the liver in sepsis. Int Rev Immunol. 2014;33(6):498-510.
Bauernfeind FG, Horvath G, Stutz A, et al. Cutting edge: NF-kappaB activating pattern recognition and cytokine receptors license NLRP3 inflammasome activation by regulating NLRP3 expression. J Immunol. 2009;183(2):787-791.
Budai MM, Varga A, Milesz S, Tozser J, Benko S. Aloe vera downregulates LPS-induced inflammatory cytokine production and expression of NLRP3 inflammasome in human macrophages. Mol Immunol. 2013;56(4):471-479.
Jiang ZY, Meng Y, Bo LL, Wang CL, Bian JJ. Sophocarpine attenuates LPS-induced liver injury and improves survival of mice through suppressing oxidative stress, inflammation, and apoptosis. Mediators Inflamm. 2018;2018:5871431.
Joshi VD, Kalvakolanu DV, Hasday JD, Hebel RJ, Cross AS. IL-18 levels and the outcome of innate immune response to lipopolysaccharide: importance of a positive feedback loop with caspase-1 in IL-18 expression. J Immunol. 2002;169(5):2536-2544.
Tsuji H, Mukaida N, Harada A, et al. Alleviation of lipopolysaccharide-induced acute liver injury in Propionibacterium acnes-primed IFN-gamma-deficient mice by a concomitant reduction of TNF-alpha, IL-12, and IL-18 production. J Immunol. 1999;162(2):1049-1055.
Tsutsui H, Nishiguchi S. Importance of Kupffer cells in the development of acute liver injuries in mice. Int J Mol Sci. 2014;15(5):7711-7730.
Imamura M, Tsutsui H, Yasuda K, et al. Contribution of TIR domain-containing adapter inducing IFN-beta-mediated IL-18 release to LPS-induced liver injury in mice. J Hepatol 2009;51(2):333-341.
Weighardt H, Mages J, Jusek G, Kaiser-Moore S, Lang R, Holzmann B. Organ-specific role of MyD88 for gene regulation during polymicrobial peritonitis. Infect Immun. 2006;74(6):3618-3632.
Baker RG, Hayden MS, Ghosh S. NF-kappaB, inflammation, and metabolic disease. Cell Metab. 2011;13(1):11-22.
Tsutsui H, Imamura M, Fujimoto J, Nakanishi K. The TLR4/TRIF-mediated activation of NLRP3 Inflammasome underlies endotoxin-induced liver injury in mice. Gastroenterol Res Pract. 2010;2010:641865.
Gehrke N, Hovelmeyer N, Waisman A, et al. Hepatocyte-specific deletion of IL1-RI attenuates liver injury by blocking IL-1 driven autoinflammation. J Hepatol. 2018;68(5):986-995.
Barbier L, Ferhat M, Salamé E, et al. Interleukin-1 family cytokines: keystones in liver inflammatory diseases. Front Immunol. 2019;10:2014. https://doi.org/10.3389/fimmu.2019.02014.
Storek KM, Monack DM. Bacterial recognition pathways that lead to inflammasome activation. Immunol Rev. 2015;265(1):112-129.
Maltez VI, Tubbs AL, Cook KD, et al. Inflammasomes coordinate pyroptosis and natural killer cell cytotoxicity to clear infection by a ubiquitous environmental bacterium. Immunity. 2015;43(5):987-997.
David S, Hamilton JP. Drug-induced liver injury. US Gastroenterol Hepatol Rev. 2010;6:73-80.
Imaeda AB, Watanabe A, Sohail MA, et al. Acetaminophen-induced hepatotoxicity in mice is dependent on Tlr9 and the Nalp3 inflammasome. J Clin Invest. 2009;119(2):305-314.
Maher JJ. DAMPs ramp up drug toxicity. J Clin Invest. 2009;119(2):246-249.
Hinson JA, Roberts DW, James LP. Mechanisms of acetaminophen-induced liver necrosis. Handb Exp Pharmacol. 2010;196:369-405.
James LP, Farrar HC, Darville TL, et al. Elevation of serum interleukin 8 levels in acetaminophen overdose in children and adolescents. Clin Pharmacol Ther. 2001;70(3):280-286.
Sanz-Garcia C, Ferrer-Mayorga G, González-Rodríguez Á, et al. Sterile inflammation in acetaminophen-induced liver injury is mediated by Cot/tpl2. J Biol Chem. 2013;288(21):15342-15351.
Meier RPH, Meyer J, Montanari E, Lacotte S. Interleukin-1 receptor antagonist modulates liver inflammation and fibrosis in mice in a model-dependent manner. Int J Mol Sci. 2019;20(6):1295.
Barman PK, Mukherjee R, Prusty BK, Suklabaidya S, Senapati S, Ravindran B. Chitohexaose protects against acetaminophen-induced hepatotoxicity in mice. Cell Death Dis. 2016;7(5):e2224.
Neumann K, Schiller B, Tiegs G. NLRP3 inflammasome and IL-33: novel players in sterile liver inflammation. Int J Mol Sci. 2018;19(9):2732.
Bortolotti P, Faure E, Kipnis E. Inflammasomes in tissue damages and immune disorders after trauma. Front Immunol. 2018;9:1900.
Woolbright BL, Jaeschke H. Role of the inflammasome in acetaminophen-induced liver injury and acute liver failure. J Hepatol. 2017;66(4):836-848.
Liu B, Ma ZY, Wu G, Qian JM. Butyrate protects rats from hepatic ischemia/reperfusion injury. Int J Clin Exp Med. 2015;8(4):5406-5413.
Wu HH, Huang CC, Chang CP, Lin MT, Niu KC, Tian YF. Heat shock protein 70(HSP70) reduces hepatic inflammatory and oxidative damage in a rat model of liver ischemia/reperfusion injury with hyperbaric oxygen preconditioning. Med Sci Monit. 2018;24:8096-8104.
Koyama Y, Brenner DA. Liver inflammation and fibrosis. J Clin Invest. 2017;127(1):55-64.
Kim EJ, Park SY, Baek SE, et al. HMGB1 increases IL-1β production in vascular smooth muscle cells via NLRP3 Inflammasome. Front Physiol. 2018;9:313.
Fu S, Liu H, Xu L, et al. Baicalin modulates NF-κB and NLRP3 inflammasome signaling in porcine aortic vascular endothelial cells infected by Haemophilus parasuis causing Glässer's disease. Sci Rep. 2018;8(1):807.
Huang H, Chen HW, Evankovich J, et al. Histones activate the NLRP3 inflammasome in Kupffer cells during sterile inflammatory liver injury. J Immunol. 2013;191(5):2665-2679.
Guicciardi ME, Malhi H, Mott JL, Gores GJ. Apoptosis and necrosis in the liver. Compr Physiol. 2013;3(2):977-1010.
Cao L, Quan XB, Zeng WJ, Yang XO, Wang MJ. Mechanism of hepatocyte apoptosis. J Cell Death. 2016;9:19-29.
Sun Q, Gao W, Loughran P, et al. Caspase 1 activation is protective against hepatocyte cell death by up-regulating beclin 1 protein and mitochondrial autophagy in the setting of redox stress. J Biol Chem. 2013;288(22):15947-15958.
Takeuchi D, Yoshidome H, Kato A, et al. Interleukin 18 causes hepatic ischemia/reperfusion injury by suppressing anti-inflammatory cytokine expression in mice. Hepatology. 2004;39(3):699-710.
Wang J, Dong R, Zheng S. Roles of the inflammasome in the gut-liver axis (review). Mol Med Rep. 2019;19(1):3-14.
Jimenez-Castro MB, Cornide-Petronio ME, Gracia-Sancho J, Peralta C. Inflammasome-mediated inflammation in liver ischemia-reperfusion injury. Cells. 2019;8(10):1131.
Menzel CL, Sun Q, Loughran PA, Pape HC, Billiar TR, Scott MJ. Caspase-1 is hepatoprotective during trauma and hemorrhagic shock by reducing liver injury and inflammation. Mol Med. 2011;17(10):1031-1038.
Chu Q, Jiang Y, Zhang W, et al. Pyroptosis is involved in the pathogenesis of human hepatocellular carcinoma. Oncotarget. 2016;75(1):84658-84665.
Fan SH, Wang YY, Lu J, et al. Luteoloside suppresses proliferation and metastasis of hepatocellular carcinoma cells by inhibition of NLRP3 inflammasome. PLoS One. 2014;9(2):e89961.