Melatonin Suppresses NLRP3 Inflammasome Activation via TLR4/NF-κB and P2X7R Signaling in High-Fat Diet-Induced Murine NASH Model

References

• Grundy SM, Brewer HB, Cleeman JI, Smith SC, Lenfant C. Definition of metabolic syndrome: report of the national heart, lung, and serum institute/American Heart Association conference on scientific issues related to definition. Circulation. 2004;109(3):433–438. doi:10.1161/01.CIR.0000111245.75752.C6
   PubMed Web of Science ®Google Scholar
• Neuschwander-Tetri BA, Caldwell SH. Nonalcoholic steatohepatitis: summary of an AASLD single topic conference. Hepatology. 2003;37(5):1202–1219. doi:10.1053/jhep.2003.50193
   PubMed Web of Science ®Google Scholar
• Sayiner M, Koenig A, Henry L, Younossi ZM. Epidemiology of nonalcoholic fatty liver disease and nonalcoholic steatohepatitis in the United States and the rest of the world. Clin Liver Dis. 2016;20(2):205–214. doi:10.1016/j.cld.2015.10.001
   PubMed Web of Science ®Google Scholar
• Negro F. Natural history of NASH and HCC. Liver Int. 2020;40(S1):72–76. doi:10.1111/liv.14362
   PubMed Web of Science ®Google Scholar
• Lazo M, Hernaez R, Eberhardt MS, et al. Prevalence of nonalcoholic fatty liver disease in the United States: the third national health and nutrition examination survey, 1988–1994. Am J Epidemiol. 2013;178(1):38–45. doi:10.1093/aje/kws448
   PubMed Web of Science ®Google Scholar
• Fan JG. Impact of non-alcoholic fatty liver disease on accelerated metabolic complications. J Dig Dis. 2008;9(2):63–67. doi:10.1111/j.1751-2980.2008.00323.x
   PubMed Web of Science ®Google Scholar
• Boppidi H, Daram SR. Nonalcoholic fatty liver disease: hepatic manifestation of obesity and the metabolic syndrome. Postgrad Med. 2008;120(2):1–3. doi:10.3810/pgm.2008.07.1800
   PubMedGoogle Scholar
• Satapati S, Kucejova B, Shawn C, et al. Mitochondrial metabolism mediates oxidative stress and inflammation in fatty liver. J Clin Invest. 2016;125:4447–4462. doi:10.1172/JCI82204
   Web of Science ®Google Scholar
• Lebeaupin C, Vallée D, Hazari Y, Hetz C, Chevet E, Bailly-Maitre B. Endoplasmic reticulum stress signalling and the pathogenesis of non-alcoholic fatty liver disease. J Hepatol. 2018;69(4):927–947. doi:10.1016/j.jhep.2018.06.008
   PubMed Web of Science ®Google Scholar
• Chen Z, Tian R, She Z, Cai J, Li H. Corrigendum to “Role of oxidative stress in the pathogenesis of nonalcoholic fatty liver disease”. Free Radic Biol Med. 2020;152:116–141. doi:10.1016/j.freeradbiomed.2020.06.011
   PubMed Web of Science ®Google Scholar
• Buzzetti E, Pinzani M, Tsochatzis EA. The multiple-hit pathogenesis of non-alcoholic fatty liver disease (NAFLD). Metabolism. 2016;65(8):1038–1048. doi:10.1016/j.metabol.2015.12.012
   PubMed Web of Science ®Google Scholar
• Fang YL, Chen H, Wang CL, Liang L. Pathogenesis of non-alcoholic fatty liver disease in children and adolescence: from “two hit theory” to “multiple hit model”. World J Gastroenterol. 2018;24(27):2974–2983. doi:10.3748/wjg.v24.i27.2974
   PubMed Web of Science ®Google Scholar
• Softic S, Cohen DE, Kahn CR. Role of dietary fructose and hepatic de novo lipogenesis in fatty liver disease. Dig Dis Sci. 2016;61(5):1282–1293. doi:10.1007/s10620-016-4054-0
   PubMed Web of Science ®Google Scholar
• Franchi L, Eigenbrod T, Muñoz-Planillo R, Nuñez G. The inflammasome: a caspase-1-activation platform that regulates immune responses and disease pathogenesis. Nat Immunol. 2009;10(3):241–247. doi:10.1038/ni.1703
   PubMed Web of Science ®Google Scholar
• Bawa M, Saraswat VA. Gut-liver axis: role of inflammasomes. J Clin Exp Hepatol. 2013;3(2):141–149. doi:10.1016/j.jceh.2013.03.225
   PubMedGoogle Scholar
• Juliana C, Fernandes-Alnemri T, Kang S, Farias A, Qin F, Alnemri ES. Non-transcriptional priming and deubiquitination regulate NLRP3 inflammasome activation. J Biol Chem. 2012;287(43):36617–36622. doi:10.1074/jbc.M112.407130
   PubMed Web of Science ®Google Scholar
• Weber K, Schilling JD. Lysosomes integrate metabolic-inflammatory cross-talk in primary macrophage inflammasome activation. J Biol Chem. 2014;289(13):9158–9171. doi:10.1074/jbc.M113.531202
   PubMed Web of Science ®Google Scholar
• Franceschini A, Capece M, Chiozzi P, et al. The P2X7 receptor directly interacts with the NLRP3 inflammasome scaffold protein. FASEB J. 2015;29(6):2450–2461. doi:10.1096/fj.14-268714
   PubMed Web of Science ®Google Scholar
• Csak T, Ganz M, Pespisa J, Kodys K, Dolganiuc A, Szabo G. Fatty acid and endotoxin activate inflammasomes in mouse hepatocytes that release danger signals to stimulate immune cells. Hepatology. 2011;54(1):133–144. doi:10.1002/hep.24341
   PubMed Web of Science ®Google Scholar
• Wree A, McGeough MD, Peña CA, et al. NLRP3 inflammasome activation is required for fibrosis development in NAFLD. J Mol Med. 2014;92(10):1069–1082. doi:10.1007/s00109-014-1170-1
   PubMed Web of Science ®Google Scholar
• 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. doi:10.1016/j.jhep.2017.01.022
   PubMed Web of Science ®Google Scholar
• Thomas H. NAFLD: a critical role for the NLRP3 inflammasome in NASH. Nat Rev Gastroenterol Hepatol. 2017;14(4):197. doi:10.1038/nrgastro.2017.21
   Google Scholar
• Zhao D, Yu Y, Shen Y, et al. Melatonin synthesis and function: evolutionary history in animals and plants. Front Endocrinol (Lausanne). 2019;10:1–16. doi:10.3389/fendo.2019.00249
   PubMed Web of Science ®Google Scholar
• Tan D-X, Hardeland R, Manchester LC, et al. The changing biological roles of melatonin during evolution: from an antioxidant to signals of darkness, sexual selection and fitness. Biol Rev. 2010;85(3):607–623. doi:10.1111/j.1469-185X.2009.00118.x
   PubMed Web of Science ®Google Scholar
• Lochner A, Marais E, Huisamen B. Melatonin and cardioprotection against ischaemia/reperfusion injury: what’s new? A review. J Pineal Res. 2018;65(1):1–22. doi:10.1111/jpi.12490
   Web of Science ®Google Scholar
• Sun H, Wang X, Chen J, et al. Melatonin improves non-alcoholic fatty liver disease via MAPK-JNK/P38 signaling in high-fat-diet-induced obese mice. Lipids Health Dis. 2016;15(1):1–8. doi:10.1186/s12944-016-0370-9
   PubMed Web of Science ®Google Scholar
• Hatzis G, Ziakas P, Kavantzas N, et al. Melatonin attenuates high fat diet-induced fatty liver disease in rats. World J Hepatol. 2013;5(4):160–169. doi:10.4254/wjh.v5.i4.160
   PubMedGoogle Scholar
• Tahan V, Atug O, Akin H, et al. Melatonin ameliorates methionine- and choline-deficient diet-induced nonalcoholic steatohepatitis in rats. J Pineal Res. 2009;46(4):401–407. doi:10.1111/j.1600-079X.2009.00676.x
   PubMed Web of Science ®Google Scholar
• Gómez-Lechón MJ, Donato MT, Martínez-Romero A, Jiménez N, Castell JV, O’Connor JE. A human hepatocellular in vitro model to investigate steatosis. Chem Biol Interact. 2007;165(2):106–116. doi:10.1016/j.cbi.2006.11.004
   PubMed Web of Science ®Google Scholar
• Bort A, Sánchez BG, Spínola E, Mateos-Gómez PA, Rodríguez-Henche N, Díaz-Laviada I. The red pepper’s spicy ingredient capsaicin activates AMPK in HepG2 cells through CaMKKβ. PLoS One. 2019;14(1):1–15. doi:10.1371/journal.pone.0211420
   Web of Science ®Google Scholar
• Jiang LH, Mackenzie AB, North RA, Surprenant A. Brilliant blue G selectively blocks ATP-gated rat P2X7 receptors. Mol Pharmacol. 2000;58(1):82–88. doi:10.1124/mol.58.1.82
   PubMed Web of Science ®Google Scholar
• Pandey NR, Renwick J, Rabaa S, et al. An induction in hepatic HDL secretion associated with reduced ATPase expression. Am J Pathol. 2009;175(4):1777–1787. doi:10.2353/ajpath.2009.090082
   PubMed Web of Science ®Google Scholar
• Dobashi H, Seki S, Habu Y, et al. Activation of mouse liver natural killer cells and NK1.1+ T cells by bacterial superantigen-primed Kupffer cells. Hepatology. 1999;30(2):430–436. doi:10.1002/hep.510300209
   PubMed Web of Science ®Google Scholar
• Jackson M, Taylor H, Jones E, Forrester LM. Mouse Cell Culture. Methods Mol Biol. 2010;633(1):29–56. doi:10.1007/978-1-59745-019-5
   PubMedGoogle Scholar
• Aly FZ, Kleiner DE. Update on fatty liver disease and steatohepatitis. Adv Anat Pathol. 2011;18(4):294–300. doi:10.1097/PAP.0b013e318220f59b
   PubMed Web of Science ®Google Scholar
• Lanthier N. Targeting Kupffer cells in non-alcoholic fatty liver disease/ non-alcoholic steatohepatitis: why and how? World J Hepatol. 2015;7(19):2184–2188. doi:10.4254/wjh.v7.i19.2184
   PubMedGoogle Scholar
• Wan X, Xu C, Yu C, Li Y. Role of NLRP3 inflammasome in the progression of NAFLD to NASH. Can J Gastroenterol Hepatol. 2016;2016:1–7. doi:10.1155/2016/6489012
   Web of Science ®Google Scholar
• Friedman SL, Neuschwander-Tetri BA, Rinella M, Sanyal AJ. Mechanisms of NAFLD Development and Therapeutic Strategies. Nat Med. 2018;24(7):908-922. doi:10.1038/s41591-018-0104-9
   Google Scholar
• Rogero MM, Calder PC. Obesity, inflammation, toll-like receptor 4 and fatty acids. Nutrients. 2018;10(4):1–19. doi:10.3390/nu10040432
   Web of Science ®Google Scholar
• Shi H, Yin H, Flier JS, et al. TLR4 links innate immunity and fatty acid – induced insulin resistance. J Clin Invest. 2006;116(11):3015–3025. doi:10.1172/JCI28898
   PubMed Web of Science ®Google Scholar
• Velázquez-Miranda E, Díaz-Muñoz M, Vázquez-Cuevas FG. Purinergic signaling in hepatic disease. Purinergic Signalling. 2019;15(4):477–489. doi:10.1007/s11302-019-09680-3
   PubMed Web of Science ®Google Scholar
• Rossato M, Di Vincenzo A, Pagano C, El Hadi H, Vettor R. The P2X7 receptor and NLRP3 axis in non-alcoholic fatty liver disease: a brief review. Cells. 2020;9(4):1–12. doi:10.3390/cells9041047
   Web of Science ®Google Scholar
• Chatterjee S, Das S. P2X7 receptor as a key player in oxidative stress-driven cell fate in nonalcoholic steatohepatitis. Oxid Med Cell Longev. 2015;2015:1–7. doi:10.1155/2015/172493
   Web of Science ®Google Scholar
• Masarone M, Rosato V, Dallio M, et al. Role of oxidative stress in pathophysiology of nonalcoholic fatty liver disease. Oxid Med Cell Longev. 2018;2018:9547613. doi:10.1155/2018/9547613
   PubMed Web of Science ®Google Scholar
• Besse-Patin A, Estall JL. An intimate relationship between ros and insulin signalling: implications for antioxidant treatment of fatty liver disease. Int J Cell Biol. 2014;2014:519153. doi:10.1155/2014/519153
   PubMedGoogle Scholar
• Delli Bovi AP, Marciano F, Mandato C, et al. Oxidative stress in non-alcoholic fatty liver disease. An updated mini review. Front Med. 2021;8:595371. doi:10.3389/fmed.2021.595371
   Web of Science ®Google Scholar
• Wang D, Wang H, Gao H, et al. P2X7 receptor mediates NLRP3 inflammasome activation in depression and diabetes. Cell Biosci. 2020;10(1):1–9. doi:10.1186/s13578-020-00388-1
   PubMed Web of Science ®Google Scholar
• Marchesini G, Day CP, Dufour JF, et al. EASL-EASD-EASO clinical practice guidelines for the management of non-alcoholic fatty liver disease. J Hepatol. 2016;64(6):1388–1402. doi:10.1016/j.jhep.2015.11.004
   PubMed Web of Science ®Google Scholar
• Zhang JJ, Meng X, Li Y, et al. Effects of melatonin on liver injuries and diseases. Int J Mol Sci. 2017;18(4):1–27. doi:10.3390/ijms18040673
   Web of Science ®Google Scholar
• García JA, Volt H, Venegas C, et al. Disruption of the NF-κB/NLRP3 connection by melatonin requires retinoid-related orphan receptor-a and blocks the septic response in mice. FASEB J. 2015;29(9):3863–3875. doi:10.1096/fj.15-273656
   PubMed Web of Science ®Google Scholar
• Farias da de SMT, Paixao da RI, MM Cruz, et al. Melatonin supplementation attenuates the pro-inflammatory adipokines expression in visceral fat from obese mice induced by a high-fat diet. Cells. 2019;8(9). doi:10.3390/cells8091041
   Web of Science ®Google Scholar
• Karolczak K, Watala C. The mystery behind the pineal gland: melatonin affects the metabolism of cholesterol. Oxid Med Cell Longev. 2019;2019:4531865. doi:10.1155/2019/4531865
   PubMed Web of Science ®Google Scholar
• Yu GM, Kubota H, Okita M, Maeda T. The anti-inflammatory and antioxidant effects of melatonin on LPS-stimulated bovine mammary epithelial cells. PLoS One. 2017;12(5):1–17. doi:10.1371/journal.pone.0178525
   Web of Science ®Google Scholar
• Seok JK, Kang HC, Cho YY, Lee HS, Lee JY. Therapeutic regulation of the NLRP3 inflammasome in chronic inflammatory diseases. Arch Pharm Res. 2021;44(1):16–35. doi:10.1007/s12272-021-01307-9
   PubMed Web of Science ®Google Scholar
• Xia MZ, Liang YL, Wang H, et al. Melatonin modulates TLR4-mediated inflammatory genes through MyD88- and TRIF-dependent signaling pathways in lipopolysaccharide-stimulated RAW264.7 cells. J Pineal Res. 2012;53(4):325–334. doi:10.1111/j.1600-079X.2012.01002.x
   PubMed Web of Science ®Google Scholar
• Chuffa GGA, Fioruci-Fontanelli BA, Mendes LO, et al. Melatonin attenuates the TLR4-mediated inflammatory response through MyD88- and TRIF-dependent signaling pathways in an in vivo model of ovarian cancer. BMC Cancer. 2015;15(1):1–13. doi:10.1186/s12885-015-1032-4
   PubMed Web of Science ®Google Scholar
• Bonomini F, Dos Santos M, Veronese FV, Rezzani R. NLRP3 inflammasome modulation by melatonin supplementation in chronic pristane-induced lupus nephritis. Int J Mol Sci. 2019;20(14):14. doi:10.3390/ijms20143466
   Web of Science ®Google Scholar
• Liu Y, Li C, Yin H, Zhang X, Li Y. NLRP3 inflammasome: a potential alternative therapy target for atherosclerosis. Evidence-Based Complement Altern Med. 2020;2020. doi:10.1155/2020/1561342.
   Web of Science ®Google Scholar
• Osier N, McGreevy E, Pham L, et al. Melatonin as a Therapy for Traumatic Brain Injury: A Review of Published Evidence. Int J Mol Sci.2018;19(5):1539. doi:10.3390/ijms19051539
   Google Scholar
• Friedman SL. Mechanisms of hepatic fibrogenesis. Gastroenterology. 2008;134(6):1655–1669. doi:10.1053/j.gastro.2008.03.003
   PubMed Web of Science ®Google Scholar
• Naim A, Pan Q, Baig MS. Matrix Metalloproteinases (MMPs) in liver diseases. J Clin Exp Hepatol. 2017;7(4):367–372. doi:10.1016/j.jceh.2017.09.004
   PubMed Web of Science ®Google Scholar
• Roeb E. Matrix metalloproteinases and liver fibrosis (translational aspects). Matrix Biol. 2018;68–69:463–473. doi:10.1016/j.matbio.2017.12.012
   PubMed Web of Science ®Google Scholar
• Hu W, Ma Z, Jiang S, et al. Melatonin: the dawning of a treatment for fibrosis? J Pineal Res. 2016;60(2):121–131. doi:10.1111/jpi.12302
   PubMed Web of Science ®Google Scholar
• Wu X, Dong L, Lin X, Li J. Relevance of the NLRP3 inflammasome in the pathogenesis of chronic liver disease. Front Immunol. 2017;8. doi:10.3389/fimmu.2017.01728.
   Web of Science ®Google Scholar
• Kong F, Ye B, Cao J, et al. Curcumin represses NLRP3 inflammasome activation via TLR4/MyD88/NF-κB and P2X7R signaling in PMA-induced macrophages. Front Pharmacol. 2016;7:1–10. doi:10.3389/fphar.2016.00369
   PubMed Web of Science ®Google Scholar