Resveratrol inhibits NLRP3 inflammasome activation by preserving mitochondrial integrity and augmenting autophagy

Journal of Cellular Physiology

Volumn 230, Issue 7, 2015, Pages 1567-1579

  Chang, Ya Ping ^a   Ka, Shuk Man ^b   Hsu, Wan Han ^b   Chen, Ann ^c   Chao, Louis Kuoping ^d   Lin, Chai Ching ^a   Hsieh, Cho Chen ^a   Chen, Ming Cheng ^a   Chiu, Huan Wen ^a   Ho, Chen Lung ^e   Chiu, Yi Chich ^a   Liu, May Lan ^f   Hua, Kuo Feng ^a  

^a NATIONAL ILAN UNIVERSITY   (Taiwan)

^b NATIONAL DEFENSE MEDICAL CENTER   (Taiwan)

^c TRI SERVICE GENERAL HOSPITAL   (Taiwan)

^d CHINA MEDICAL UNIVERSITY   (Taiwan)

^e TAIWAN FORESTRY RESEARCH INSTITUTE   (Taiwan)

^f TOKO UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; MITOGEN ACTIVATED PROTEIN KINASE; MULTIPROTEIN COMPLEX; NLRP3 INFLAMMASOME; PROTEIN P62; RESVERATROL; SUPEROXIDE; SYNAPTOPHYSIN; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATE; APOPTOSIS REGULATORY PROTEIN; CALCIUM BINDING PROTEIN; CARRIER PROTEIN; CIAS1 PROTEIN, MOUSE; IPAF PROTEIN, MOUSE; MITOGEN ACTIVATED PROTEIN KINASE KINASE; NALP1 PROTEIN, MOUSE; PROTEIN KINASE C; REACTIVE OXYGEN METABOLITE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; STILBENE DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPHAGY; CELL ACTIVATION; CELL DAMAGE; CELL INFILTRATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOKINE RELEASE; DRUG CYTOTOXICITY; DRUG INHIBITION; ENZYME ACTIVATION; GLOMERULAR INFLAMMATION; GLOMERULOPATHY; GLOMERULOSCLEROSIS; HISTOPATHOLOGY; IMMUNOGLOBULIN A NEPHROPATHY; MONONUCLEAR CELL; MOUSE; NONHUMAN; PERITONEUM MACROPHAGE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; ANIMAL; CELL CULTURE; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; INFLAMMATION; MACROPHAGE; METABOLISM; MITOCHONDRION; PHOSPHORYLATION; PHYSIOLOGY;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ADENOSINE TRIPHOSPHATE; ANIMALS; APOPTOSIS REGULATORY PROTEINS; AUTOPHAGY; CALCIUM-BINDING PROTEINS; CARRIER PROTEINS; CASPASE 1; CELLS, CULTURED; GENE EXPRESSION REGULATION; INFLAMMATION; INTERLEUKIN-1BETA; MACROPHAGES; MICE; MITOCHONDRIA; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; PHOSPHORYLATION; PROTEIN KINASE C; REACTIVE OXYGEN SPECIES; STILBENES;

EID: 84925584516     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.24903     Document Type: Article

References (60)

1. Alayev A, Sun Y, Snyder RB, Berger SM, Yu JJ, Holz MK. 2014. Resveratrol prevents rapamycin-induced upregulation of autophagy and selectively induces apoptosis in TSC2-deficient cells. Cell Cycle 13:371-382.
2. Andreadi C, Britton RG, Patel KR, Brown K. 2014. Resveratrol-sulfates provide an intracellular reservoir for generation of parent resveratrol, which induces autophagy in cancer cells. Autophagy 10:524-525.
3. Bauernfeind FG, Horvath G, Stutz A, Alnemri ES, MacDonald K, Speert D, Fernandes-Alnemri T, Wu J, Monks BG, Fitzgerald KA, Hornung V, Latz E. 2009. Cutting edge: NF-kappaB activating pattern recognition and cytokine receptors license NLRP3 inflammasome activation by regulating NLRP3 expression. J Immunol 183:787-791.
4. Bauernfeind F, Bartok E, Rieger A, Franchi L, Núñez G, Hornung V. 2011. Cutting edge: Reactive oxygen species inhibitors block priming, but not activation, of the NLRP3 inflammasome. J Immunol 187:613-617.
5. Bergsbaken T, Fink SL, Cookson BT. 2009. Pyroptosis: Host cell death and inflammation. Nat Rev Microbiol 7:99-109.
6. Bruchard M, Mignot G, Derangère V, Chalmin F, Chevriaux A, Végran F, Boireau W, Simon B, Ryffel B, Connat JL, Kanellopoulos J, Martin F, Rébé C, Apetoh L, Ghiringhelli F. 2013. Chemotherapy-triggered cathepsin B release in myeloid-derived suppressor cells activates the Nlrp3 inflammasome and promotes tumor growth. Nat Med 19:57-64.
7. Chao TK, Rifai A, Ka SM, Yang SM, Shui HA, Lin YF, Sytwu HK, Lee WH, Kung JT, Chen A. 2006. The endogenous immune response modulates the course of IgA-immune complex mediated nephropathy. Kidney Int 70:283-297.
8. Chen ML, Yi L, Jin X, Liang XY, Zhou Y, Zhang T, Xie Q, Zhou X, Chang H, Fu YJ, Zhu JD, Zhang QY, Mi MT. 2013. Resveratrol attenuates vascular endothelial inflammation by inducing autophagy through the cAMP signaling pathway. Autophagy 9:2033-2045.
9. Chen S, Sun B. 2013. Negative regulation of NLRP3 inflammasome signaling. Protein Cell 4:251-258.
10. Chow MT, Sceneay J, Paget C, Wong CS, Duret H, Tschopp J, Möller A, Smyth MJ. 2012. NLRP3 suppresses NK cell-mediated responses to carcinogen-induced tumors and metastases. Cancer Res 72:5721-5732.
11. Cruz CM, Rinna A, Forman HJ, Ventura AL, Persechini PM, Ojcius DM. 2007. ATP activates a reactive oxygen species-dependent oxidative stress response and secretion of proinflammatory cytokines in macrophages. J Biol Chem 282:2871-2879.
12. Danz ED, Skramsted J, Henry N, Bennett JA, Keller RS. 2009. Resveratrol prevents doxorubicin cardiotoxicity through mitochondrial stabilization and the Sirt1 pathway. Free Radic Biol Med 46:1589-1597.
13. Duewell P, Kono H, Rayner KJ, Sirois CM, Vladimer G, Bauernfeind FG, Abela GS, Franchi L, Nuñez G, Schnurr M, Espevik T, Lien E, Fitzgerald KA, Rock KL, Moore KJ, Wright SD, Hornung V, Latz E. 2010. NLRP3 inflammasomes are required for atherogenesis and activated by cholesterol crystals. Nature 464:1357-1361.
14. Feng X, Liang N, Zhu D, Gao Q, Peng L, Dong H, Yue Q, Liu H, Bao L, Zhang J, Hao J, Gao Y, Yu X, Sun J. 2013. Resveratrol inhibits β-amyloid-induced neuronal apoptosis through regulation of SIRT1-ROCK1 signaling pathway. PLoS ONE 8:e59888.
15. Fink SL, Cookson BT. 2006. Caspase-1-dependent pore formation during pyroptosis leads to osmotic lysis of infected host macrophages. Cell Microbiol 8:1812-1825.
16. Fu Y, Wang Y, Du L, Xu C, Cao J, Fan T, Liu J, Su X, Fan S, Liu Q, Fan F. 2013. Resveratrol inhibits ionising irradiation-induced inflammation in MSCs by activating SIRT1 and limiting NLRP-3 inflammasome activation. Int J Mol Sci 14:14105-14118.
17. Ge J, Liu Y, Li Q, Guo X, Gu L, Ma ZG, Zhu YP. 2013. Resveratrol Induces Apoptosis and Autophagy in T-cell Acute Lymphoblastic Leukemia Cells by Inhibiting Akt/mTOR and Activating p38-MAPK. Biomed Environ Sci 26:902-911.
18. Halle A, Hornung V, Petzold GC, Stewart CR, Monks BG, Reinheckel T, Fitzgerald KA, Latz E, Moore KJ, Golenbock DT. 2008. The NALP3 inflammasome is involved in the innate immune response to amyloid-beta. Nat Immunol 9:857-865.
19. Hao E, Lang F, Chen Y, Zhang H, Cong X, Shen X, Su G. 2013. Resveratrol alleviates endotoxin-induced myocardial toxicity via the Nrf2 transcription factor. PLoS ONE 8:e77794.
20. Harris J, Hartman M, Roche C, Zeng SG, O'Shea A, Sharp FA, Lambe EM, Creagh EM, Golenbock DT, Tschopp J, Kornfeld H, Fitzgerald KA, Lavelle EC. 2011. Autophagy controls IL-1beta secretion by targeting pro-IL-1beta for degradation. J Biol Chem 286:9587-9597.
21. He X, Andersson G, Lindgren U, Li Y. 2010. Resveratrol prevents RANKL-induced osteoclast differentiation of murine osteoclast progenitor RAW 264.7cells through inhibition of ROS production. Biochem Biophys Res Commun 401:356-362.
22. Hornung V, Bauernfeind F, Halle A, Samstad EO, Kono H, Rock KL, Fitzgerald KA, Latz E. 2008. Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nat Immunol 9:847-856.
23. Hua KF, Yang SM, Kao TY, Chang JM, Chen HL, Tsai YJ, Chen A, Yang SS, Chao LK, Ka SM. 2013. Osthole mitigates progressive IgA nephropathy by inhibiting reactive oxygen species generation and NF-κB/NLRP3 pathway. PLoS ONE 8:e77794.
24. Huang TT, Lai HC, Chen YB, Chen LG, Wu YH, Ko YF, Lu CC, Chang CJ, Wu CY, Martel J, Ojcius DM, Chong KY, Young JD. 2014. Cis-Resveratrol produces anti-inflammatory effects by inhibiting canonical and non-canonical inflammasomes in macrophages. Innate Immun 20:735-750.
25. Jimenez-Gomez Y, Mattison JA, Pearson KJ, Martin-Montalvo A, Palacios HH, Sossong AM, Ward TM, Younts CM, Lewis K, Allard JS, Longo DL, Belman JP, Malagon MM, Navas P, Sanghvi M, Moaddel R, Tilmont EM, Herbert RL, Morrell CH, Egan JM, Baur JA, Ferrucci L, Bogan JS, Bernier M, de Cabo R. 2013. Resveratrol improves adipose insulin signaling and reduces the inflammatory response in adipose tissue of rhesus monkeys on high-fat, high-sugar diet. Cell Metab 18:533-545.
26. Ka SM, Hsieh TT, Lin SH, Yang SS, Wu CC, Sytwu HK, Chen A. 2011. Decoy receptor 3 inhibits renal mononuclear leukocyte infiltration and apoptosis and prevents progression of IgA nephropathy in mice. Am J Physiol Renal Physiol 301:F1218-F1230.
27. Ka SM, Sytwu HK, Chang DM, Hsieh SL, Tsai PY, Chen A. 2007. Decoy receptor 3 ameliorates an autoimmune crescentic glomerulonephritis model in mice. J Am Soc Nephrol 18:2473-2485.
28. Kepp O, Galluzzi L, Kroemer G. 2011. Mitochondrial control of the NLRP3 inflammasome. Nat Immunol 12:199-200.
29. Kim HJ, Lee DW, Ravichandran K, Keys O, Akcay D, Nguyen A, He Q, Jani Z, Ljubanovic A, Edelstein D. 2013. NLRP3 inflammasome knockout mice are protected against ischemic but not cisplatin-induced acute kidney injury. J Pharmacol Exp Ther 346:465-472.
30. Kuballa P, Nolte WM, Castoreno AB, Xavier RJ. 2012. Autophagy and the immune system. Annu Rev Immunol 30:611-646.
31. Latz E, Xiao TS, Stutz A. 2013. Activation and regulation of the inflammasomes. Nat Rev Immunol 13:397-411.
32. Lee GS, Subramanian N, Kim AI, Aksentijevich I, Goldbach-Mansky R, Sacks DB, Germain RN, Kastner DL, Chae JJ. 2012. The calcium-sensing receptor regulates the NLRP3 inflammasome through Ca2+ and cAMP. Nature 492:123-127.
33. Leiro J, Alvarez E, Arranz JA, Laguna R, Uriarte E, Orallo F. 2004. Effects of cis-resveratrol on inflammatory murine macrophages: Antioxidant activity and down-regulation of inflammatory genes. J Leukoc Biol 75:1156-1165.
34. Levine B, Mizushima N, Virgin HW. 2011. Autophagy in immunity and inflammation. Nature 469:323-335.
35. Li XM, Zhou MT, Wang XM, Ji MH, Zhou ZQ, Yang JJ. 2014. Resveratrol pretreatment attenuates the isoflurane-induced cognitive impairment through its anti-inflammation and -apoptosis actions in aged mice. J Mol Neurosci 52:286-293.
36. Liao PC, Chao LK, Chou JC, Dong WC, Lin CN, Lin CY, Chen A, Ka SM, Ho CL, Hua KF. 2013. Lipopolysaccharide/adenosine triphosphate-mediated signal transduction in the regulation of NLRP3 protein expression and caspase-1-mediated interleukin-1β secretion. Inflamm Res 62:89-96.
37. Lin CJ, Lee CC, Shih YL, Lin TY, Wang SH, Lin YF, Shih CM. 2012. Resveratrol enhances the therapeutic effect of temozolomide against malignant glioma in vitro and in vivo by inhibiting autophagy. Free Radic Biol Med 52:377-391.
38. López-Castejón G, Pelegrín P. 2012. Current status of inflammasome blockers as anti-inflammatory drugs. Expert Opin Investig Drugs 21:995-1007.
39. Lv XC, Zhou HY. 2012. Resveratrol protects H9c2 embryonic rat heart derived cells from oxidative stress by inducing autophagy: Role of p38 mitogen-activated protein kinase. Can J Physiol Pharmacol 90:655-662.
40. Martinon F, Pétrilli V, Mayor A, Tardivel A, Tschopp J. 2006. Gout-associated uric acid crystals activate the NALP3 inflammasome. Nature 440:237-241.
41. Moore SF, MacKenzie AB. 2009. NADPH oxidase NOX2 mediates rapid cellular oxidation following ATP stimulation of endotoxin-primed macrophages. J Immunol 183:3302-3308.
42. Nakahira K, Haspel JA, Rathinam VA, Lee SJ, Dolinay T, Lam HC, Englert JA, Rabinovitch M, Cernadas M, Kim HP, Fitzgerald KA, Ryter SW, Choi AM. 2011. Autophagy proteins regulate innate immune responses by inhibiting the release of mitochondrial DNA mediated by the NALP3 inflammasome. Nat Immunol 12:222-230.
43. Park SJ, Ahmad F, Philp A, Baar K, Williams T, Luo H, Ke H, Rehmann H, Taussig R, Brown AL, Kim MK, Beaven MA, Burgin AB, Manganiello V, Chung JH. 2012. Resveratrol ameliorates aging-related metabolic phenotypes by inhibiting cAMP phosphodiesterases. Cell 148:421-433.
44. Peters-Golden M. 2009. Putting on the brakes: Cyclic AMP as a multipronged controller of macrophage function. Sci Signal 2:pe.
45. Puissant A, Fenouille N, Auberger P. 2012. When autophagy meets cancer through p62/SQSTM1. Am J Cancer Res 2:397-413.
46. Shi CS, Shenderov K, Huang NN, Kabat J, Abu-Asab M, Fitzgerald KA, Sher A, Kehrl JH. 2012a. Activation of autophagy by inflammatory signals limits IL-1β production by targeting ubiquitinated inflammasomes for destruction. Nat Immunol 13:255-263.
47. Shi YW, Wang CP, Liu L, Liu YL, Wang X, Hong Y, Li Z, Kong LD. 2012b. Antihyperuricemic and nephroprotective effects of resveratrol and its analogues in hyperuricemic mice. Mol Nutr Food Res 56:1433-1444.
48. Singh BN, Kumar D, Shankar S, Srivastava RK. 2012. Rottlerin induces autophagy which leads to apoptotic cell death through inhibition of PI3K/Akt/mTOR pathway in human pancreatic cancer stem cells. Biochem Pharmacol 84:1154-1163.
49. Tschopp J, Schroder K. 2010. NLRP3 inflammasome activation: The convergence of multiple signalling pathways on ROS production. Nat Rev Immunol 10:210-215.
50. Waltz P, Carchman EH, Young AC, Rao J, Rosengart MR, Kaczorowski D, Zuckerbraun BS. 2011. Lipopolysaccaride induces autophagic signaling in macrophages via a TLR4, heme oxygenase-1 dependent pathway. Autophagy 7:315-320.
51. Wen D, Huang X, Zhang M, Zhang L, Chen J, Gu Y, Hao CM. 2013. Resveratrol Attenuates Diabetic Nephropathy via Modulating Angiogenesis. PLoS ONE 8:e82336.
52. Wen H, Gris D, Lei Y, Jha S, Zhang L, Huang MT, Brickey WJ, Ting JP. 2011. Fatty acid-induced NLRP3-ASC inflammasome activation interferes with insulin signaling. Nat Immunol 12:408-415.
53. Xu X, Chen K, Kobayashi S, Timm D, Liang Q. 2012a. Resveratrol attenuates doxorubicin-induced cardiomyocyte death via inhibition of p70 S6 kinase 1-mediated autophagy. J Pharmacol Exp Ther 341:183-195.
54. Xu Y, Nie L, Yin YG, Tang JL, Zhou JY, Li DD, Zhou SW. 2012b. Resveratrol protects against hyperglycemia-induced oxidative damage to mitochondria by activating SIRT1 in rat mesangial cells. Toxicol Appl Pharmacol 259:395-401.
55. Yang SM, Ka SM, Hua KF, Wu TH, Chuang YP, Lin YW, Yang FL, Wu SH, Yang SS, Lin SH, Chang JM, Chen A. 2013a. Antroquinonol mitigates an accelerated and progressive IgA nephropathy model in mice by activating the Nrf2 pathway and inhibiting T cells and NLRP3 inflammasome. Free Radic Biol Med 61C:285-297.
56. Yang SJ, Lim Y. 2014. Resveratrol ameliorates hepatic metaflammation and inhibits NLRP3 inflammasome activation. Metabolism 63:693-701.
57. Yang Q, Wang B, Zang W, Wang X, Liu Z, Li W, Jia J. 2013b. Resveratrol inhibits the growth of gastric cancer by inducing g1 phase arrest and senescence in a sirt1-dependent manner. PLoS ONE 8:e70627.
58. Zhang L, Cardinal JS, Bahar R, Evankovich J, Huang H, Nace G, Billiar TR, Rosengart MR, Pan P, Tsung A. 2012. Interferon regulatory factor-1 regulates the autophagic response in LPS-stimulated macrophages through nitric oxide. Mol Med 18:201-208.
59. Zong Y, Sun L, Liu B, Deng YS, Zhan D, Chen YL, He Y, Liu J, Zhang ZJ, Sun J, Lu D. 2012. Resveratrol inhibits LPS-induced MAPKs activation via activation of the phosphatidylinositol 3-kinase pathway in murine RAW 264.7 macrophage cells. PLoS ONE 7:e44107.
60. Zhou R, Yazdi AS, Menu P, Tschopp J. 2011. A role for mitochondria in NLRP3 inflammasome activation. Nature 469:221-225.