The role of Resveratrol-induced mitophagy/autophagy in peritoneal mesothelial cells inflammatory injury via NLRP3 inflammasome activation triggered by mitochondrial ROS

Experimental Cell Research

Volumn 341, Issue 1, 2016, Pages 42-53

  Wu, Jun ^a   Li, Xiangyou ^a   Zhu, Geli ^a   Zhang, Yanxia ^a   He, Min ^b   Zhang, Jian ^b  

^a WUHAN UNIVERSITY   (China)

^b SHANTOU UNIVERSITY MEDICAL COLLEGE   (China)

Author keywords

Mitophagy autophagy; NLRP3; Peritoneal mesothelial cells; Resveratrol; ROS

Indexed keywords

ADENYLATE KINASE; AUTOPHAGY PROTEIN 5; BECLIN 1; CRYOPYRIN; GLUCOSE; INFLAMMASOME; INTERLEUKIN 1BETA; REACTIVE OXYGEN METABOLITE; RESVERATROL; SMALL INTERFERING RNA; CARRIER PROTEIN; NLRP3 PROTEIN, HUMAN; STILBENE DERIVATIVE;

ARTICLE; AUTOPHAGY; CONTROLLED STUDY; CYTOKINE RELEASE; DOWN REGULATION; ENZYME ACTIVATION; HUMAN; HUMAN CELL; INFLAMMATION; MITOCHONDRION; MITOPHAGY; PERITONEAL DIALYSIS; PERITONEAL MESOTHELIAL CELL; PERITONEUM CELL; PRIORITY JOURNAL; UPREGULATION; CELL CULTURE; CHEMICALLY INDUCED; DRUG EFFECTS; EPITHELIUM CELL; METABOLISM; PATHOLOGY;

AUTOPHAGY; CARRIER PROTEINS; CELLS, CULTURED; EPITHELIAL CELLS; HUMANS; INFLAMMASOMES; INFLAMMATION; MITOCHONDRIA; MITOCHONDRIAL DEGRADATION; REACTIVE OXYGEN SPECIES; STILBENES;

EID: 84958164990     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2016.01.014     Document Type: Article

References (41)

1. Yáñez-Mó M., Lara-Pezzi E., Selgas R., et al. Peritoneal dialysis and epithelial-to-mesenchymal transition of mesothelial cells. N. Engl. J. Med. 2003, 348:403-413.
2. Witowski J., Wisniewska J., Korybalska K., et al. Prolonged exposure to glucose degradation products impairs viability and function of human peritoneal mesothelial cells. J. Am. Soc. Nephrol. 2001, 12:2434-2441.
3. Schroder K., Tschopp J. The inflammasomes. Cell 2010, 140:821-832.
4. Kastner D.L., Aksentijevich I., Goldbach-Mansky R. Autoinflammatory disease reloaded: a clinical perspective. Cell 2010, 140:784-790.
5. Dostert C., Pétrilli V., Van Bruggen R., et al. Innate immune activation through Nalp3 inflammasome sensing of asbestos and silica. Science 2008, 320:674-677.
6. Raha S., Robinson B.H. Mitochondria, oxygen free radicals, and apoptosis. Am. J. Med. Genet. 2001, 106:62-70.
7. Green K., Brand M.D., Murphy M.P. Prevention of mitochondrial oxidative damage as a therapeutic strategy in diabetes. Diabetes 2004, 53(Suppl. 1):S110-S118.
8. Nakatogawa H., Suzuki K., Kamada Y., et al. Dynamics and diversity in autophagy mechanisms: lessons from yeast. Nat. Rev. Mol. Cell. Biol. 2009, 10:458-467.
9. Yang Z., Klionsky D.J. Eaten alive: a history of macroautophagy. Nat. Cell Biol. 2010, 12:814-822.
10. Kim I., Rodriguez-Enriquez S., Lemasters J.J. Selective degradation of mitochondria by mitophagy. Arch. Biochem. Biophys. 2007, 462:245-253.
11. Levine B., Mizushima N., Virgin H.W. Autophagy in immunity and inflammation. Nature 2011, 469:323-335.
12. Baur J.A., Sinclair D.A. Therapeutic potential of resveratrol: the in vivo evidence. Nat. Rev. Drug Discov. 2006, 5:493-506.
13. Aguirre L., Fernández-Quintela A., Arias N., et al. Resveratrol: anti-obesity mechanisms of action. Molecules 2014, 19:18632-18655.
14. Singh C.K., Ndiaye M.A., Ahmad N. Resveratrol and cancer: challenges for clinical translation. Biochim. Biophys. Acta 2015, 1852:1178-1185.
15. Poulsen M.M., Fjeldborg K., Ornstrup M.J., et al. Resveratrol and inflammation: challenges in translating pre-clinical findings to improved patient outcomes. Biochim. Biophys. Acta 2015, 1852:1124-1136.
16. Puissant A., Robert G., Fenouille N., et al. Resveratrol promotes autophagic cell death in chronic myelogenous leukemia cells via JNK-mediated p62/SQSTM1 expression and AMPK activation. Cancer Res. 2010, 70:1042-1052.
17. Vingtdeux V., Chandakkar P., Zhao H., et al. Novel synthetic small-molecule activators of AMPK as enhancers of autophagy and amyloid-β peptide degradation. FASEB J. 2011, 25:219-231.
18. Chang Y.P., Ka S.M., Hsu W.H., et al. Resveratrol inhibits NLRP3 inflammasome activation by preserving mitochondrial integrity and augmenting autophagy. J. Cell Physiol. 2015, 230:1567-1579.
19. Guo H., Chen Y., Liao L., et al. Resveratrol protects HUVECs from oxidized-LDL induced oxidative damage by autophagy upregulation via the AMPK/SIRT1 pathway. Cardiovasc. Drugs Ther. 2013, 27:189-198.
20. Chen M.L., Yi L., Jin X., et al. Resveratrol attenuates vascular endothelial inflammation by inducing autophagy through the cAMP signaling pathway. Autophagy 2013, 9:2033-2045.
21. Rougier J.P., Guia S., Hagège J., et al. PAI-secretion and matrix deposition in human peritoneal mesothelial cell cultures: transcriptional regulation by TGF-beta 1. Kidney Int. 1998, 54:87-98.
22. Wu J., Yang X., Zhang Y.F., et al. Glucose-based peritoneal dialysis fluids downregulates TLR and triggers hyporesponsiveness to pathogen-associated molecular patterns in human peritoneal mesothelial cells. Clin. Vaccine Immunol. 2010, 17:757-763.
23. Levine B., Kroemer G. Autophagy in the pathogenesis of disease. Cell 2008, 132:27-42.
24. Yung S., Chan T.M. Intrinsic cells: mesothelial cells -central players in regulating inflammation and resolution. Perit Dial Int. 2009, 29(Suppl. 2):S21-S27.
25. Lee H.B., Yu M.R., Song J.S., et al. Reactive oxygen species amplify protein kinase C signaling in high glucose-induced fibronectin expression by human peritoneal mesothelial cells. Kidney Int. 2004, 65:1170-1179.
26. Carrión B., Pérez-Martínez F.C., Monteagudo S., et al. Atorvastatin reduces high glucose toxicity in rat peritoneal mesothelial cells. Perit Dial Int. 2011, 31:325-331.
27. Zhang H., Wang J.W., Xu Y., et al. Effect of β-(3,4-dihydroxyphenyl)lactic acid on oxidative stress stimulated by high glucose levels in human peritoneal mesothelial cells. J. Int. Med. Res. 2012, 40:943-953.
28. Lu Y., Shen H., Shi X., et al. Hydrogen sulfide ameliorates high-glucose toxicity in rat peritoneal mesothelial cells by attenuating oxidative stress. Nephron Exp. Nephrol. 2014, 126:157-165.
29. Zhou R., Yazdi A.S., Menu P., et al. A role for mitochondria in NLRP3 inflammasome activation. Nature 2011, 469:221-225.
30. Dinarello C.A. A clinical perspective of IL-1beta as the gatekeeper of inflammation. Eur. J. Immunol. 2011, 41:1203-1217.
31. Leemans J.C., Cassel S.L., Sutterwala F.S. Sensing damage by the NLRP3 inflammasome. Immunol. Rev. 2011, 243:152-162.
32. Abderrazak A., Syrovets T., Couchie D., et al. NLRP3 inflammasome: from a danger signal sensor to a regulatory node of oxidative stress and inflammatory diseases. Redox Biol. 2015, 4:296-307.
33. Hayashi T., Hirshman M.F., Fujii N., et al. Metabolic stress and altered glucose transport: activation of AMP-activated protein kinase as a unifying coupling mechanism. Diabetes 2000, 49:527-531.
34. Baur J.A., Pearson K.J., Price N.L., et al. Resveratrol improves health and survival of mice on a high-calorie diet. Nature 2006, 444:337-342.
35. Dasgupta B., Milbrandt J. Resveratrol stimulates AMP kinase activity in neurons. Proc. Natl. Acad. Sci. USA 2007, 104:7217-7222.
36. Shin S.M., Cho I.J., Kim S.G. Resveratrol protects mitochondria against oxidative stress through AMP-activated protein kinase-mediated glycogen synthase kinase-3beta inhibition downstream of poly(ADP-ribose)polymerase-LKB1 pathway. Mol. Pharmacol. 2009, 76:884-895.
37. Donmez G., Guarente L. Aging and disease: connections to sirtuins. Aging Cell. 2010, 9:285-290.
38. Hou X., Xu S., Maitland-Toolan K.A., et al. SIRT1 regulates hepatocyte lipid metabolism through activating AMP-activated protein kinase. J. Biol. Chem. 2008, 283:20015-20026.
39. Lan F., Cacicedo J.M., Ruderman N., et al. SIRT1 modulation of the acetylation status, cytosolic localization, and activity of LKB1. Possible role in AMP-activated protein kinase activation. J. Biol. Chem. 2008, 283:27628-27635.
40. Price N.L., Gomes A.P., Ling A.J., et al. SIRT1 is required for AMPK activation and the beneficial effects of resveratrol on mitochondrial function. Cell Metab. 2012, 15:675-690.
41. Zhang Y., Chen M.L., Zhou Y., et al. Resveratrol improves hepatic steatosis by inducing autophagy through the cAMP signaling pathway. Mol. Nutr. Food Res. 2015, [Epub ahead of print]. 10.1002/mnfr.201500016.