Cis-Resveratrol produces anti-inflammatory effects by inhibiting canonical and non-canonical inflammasomes in macrophages

Innate Immunity

Volumn 20, Issue 7, 2014, Pages 735-750

  Huang, Tsung Teng ^a,b   Lai, Hsin Chih ^a,b   Chen, Young Bin ^c   Chen, Lih Geeng ^d   Wu, Yi Hui ^e   Ko, Yun Fei ^f   Lu, Chia Chen ^g   Chang, Chih Jung ^b   Wu, Cheng Yeu ^a   Martel, Jan ^a   Ojcius, David M ^a,h   Chong, Kowit Yu ^b   Young, John D ^a,f  

^a CHANG GUNG UNIVERSITY   (Taiwan)

^b CHANG GUNG UNIVERSITY COLLEGE OF MEDICINE   (Taiwan)

^c NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^d NATIONAL CHIAYI UNIVERSITY   (Taiwan)

^e NATIONAL CHENG KUNG UNIVERSITY HOSPITAL   (Taiwan)

^f MING CHI UNIVERSITY OF TECHNOLOGY   (Taiwan)

^g FU JEN CATHOLIC UNIVERSITY   (Taiwan)

^h UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

caspase; inflammasome; interleukin 1 ; reactive oxygen species; Resveratrol

Indexed keywords

ADENOSINE TRIPHOSPHATE; CASPASE 4; CYCLOOXYGENASE 2; GLUCOSE REGULATED PROTEIN 78; INFLAMMASOME; INTERLEUKIN 18; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; MITOGEN ACTIVATED PROTEIN KINASE P38; PROSTAGLANDIN E2; PROTEIN C JUN; PURINERGIC P2X7 RECEPTOR; REACTIVE OXYGEN METABOLITE; RESVERATROL; ANTIOXIDANT; CYTOKINE; STILBENE DERIVATIVE;

ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; ARTICLE; CELL VIABILITY; CIS ISOMER; CONTROLLED STUDY; CYTOKINE RELEASE; DRUG MECHANISM; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; ENZYME RELEASE; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; MACROPHAGE; MACROPHAGE ACTIVATION; MEDIATOR RELEASE; PROSTAGLANDIN RELEASE; PROTEIN EXPRESSION; TOXICITY TESTING; TRANS ISOMER; BIOSYNTHESIS; CELL SURVIVAL; CHEMISTRY; DRUG EFFECTS; METABOLISM; STEREOISOMERISM; TUMOR CELL LINE;

ANTIOXIDANTS; CELL LINE, TUMOR; CELL SURVIVAL; CYCLOOXYGENASE 2; CYTOKINES; DINOPROSTONE; ENDOPLASMIC RETICULUM STRESS; HUMANS; INFLAMMASOMES; INTERLEUKIN-1BETA; MACROPHAGES; REACTIVE OXYGEN SPECIES; STEREOISOMERISM; STILBENES;

EID: 84901947130     PISSN: 17534259     EISSN: 17534267     Source Type: Journal    
DOI: 10.1177/1753425913507096     Document Type: Article

References (83)

1. Jang M, Cai L, Udeani GO, et al. Cancer chemopreventive activity of resveratrol, a natural product derived from grapes. Science. 1997 ; 275: 218-220
2. Frémont L. Biological effects of resveratrol. Life Sci. 2000 ; 66: 663-673
3. Goldberg DM, Tsang E, Karumanchiri A, et al. Method to assay the concentrations of phenolic constituents of biological interest in wines. Anal Chem. 1996 ; 68: 1688-1694
4. Chen X, He H, Wang G, et al. Stereospecific determination of cis- and trans-resveratrol in rat plasma by HPLC: application to pharmacokinetic studies. Biomed Chromatogr. 2007 ; 21: 257-265
5. de la Lastra CA, Villegas I. Resveratrol as an anti-inflammatory and anti-aging agent: mechanisms and clinical implications. Mol Nutr Food Res. 2005 ; 49: 405-430
6. de la Lastra CA, Villegas I. Resveratrol as an antioxidant and pro-oxidant agent: mechanisms and clinical implications. Biochem Soc Trans. 2007 ; 35: 1156-1160
7. Shakibaei M, Harikumar KB, Aggarwal BB. Resveratrol addiction: to die or not to die. Mol Nutr Food Res. 2009 ; 53: 115-128
8. Shen MY, Hsiao G, Liu CL, et al. Inhibitory mechanisms of resveratrol in platelet activation: pivotal roles of p38 MAPK and NO/cyclic GMP. Br J Haematol. 2007 ; 139: 475-485
9. Baur JA, Sinclair DA. Therapeutic potential of resveratrol: the in vivo evidence. Nat Rev Drug Discov. 2006 ; 5: 493-506
10. Bertelli AA, Giovannini L, Bernini W, et al. Antiplatelet activity of cis-resveratrol. Drugs Exp Clin Res. 1996 ; 22: 61-63
11. Pettit GR, Grealish MP, Jung MK, et al. Antineoplastic agents. 465. Structural modification of resveratrol: sodium resverastatin phosphate. J Med Chem. 2002 ; 45: 2534-2542
12. Kukri ZZ, Topali-Trivunovi LN. Antibacterial activity of cis- and trans-resveratrol isolated from Polygonum cuspidatum rhizome. Acta Period Technol. 2006 ; 37: 131-136
13. Dinarello CA. Interleukin-1beta, interleukin-18, and the interleukin-1 beta converting enzyme. Ann N Y Acad Sci. 1998 ; 856: 1-11
14. Gregory JL, Morand EF, McKeown SJ, et al. Macrophage migration inhibitory factor induces macrophage recruitment via CC chemokine ligand 2. J Immunol. 2006 ; 177: 8072-8079
15. Sims JE, Smith DE. The IL-1 family: regulators of immunity. Nat Rev Immunol. 2010 ; 10: 89-102
16. Dinarello CA. Immunological and inflammatory functions of the interleukin-1 family. Annu Rev Immunol. 2009 ; 27: 519-550
17. Davis BK, Wen H, Ting JP. The inflammasome NLRs in immunity, inflammation, and associated diseases. Annu Rev Immunol. 2011 ; 29: 707-735
18. Dinarello CA, Wolff SM. The role of interleukin-1 in disease. N Engl J Med. 1993 ; 328: 106-113
19. Dinarello CA. Biologic basis of interleukin-1 in disease. Blood. 1996 ; 87: 2095-2147
20. Church LD, Cook GP, McDermott M. Primer: inflammasomes and interleukin 1 beta in inflammatory disorders. Nat Clin Pract Rheumatol. 2008 ; 4: 34-42
21. Nakanishi K, Yoshimoto T, Tsutsui H, et al. Interleukin-18 regulates both Th1 and Th2 responses. Annu Rev Immunol. 2001 ; 19: 423-474
22. Arend WP, Palmer G, Gabay C. IL-1, IL-18, and IL-33 families of cytokines. Immunol Rev. 2008 ; 223: 20-38
23. Lee SH, Soyoola E, Chanmugam P, et al. Selective expression of mitogen-inducible cyclooxygenase in macrophages stimulated with lipopolysaccharide. J Biol Chem. 1992 ; 267: 25934-25938
24. Rocca B, FitzGerald GA. Cyclooxygenases and prostaglandins: shaping up the immune response. Int Immunopharmacol. 2002 ; 2: 603-630
25. Turini ME, DuBois RN. Cyclooxygenase-2: a therapeutic target. Annu Rev Med. 2002 ; 53: 35-57
26. Bianchi ME. DAMPs, PAMPs and alarmins: all we need to know about danger. J Leukoc Biol. 2007 ; 81: 1-5
27. Martinon F, Burns K, Tschopp J. The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-beta. Mol Cell. 2002 ; 10: 417-426
28. Pétrilli V, Dostert C, Muruve DA, et al. The inflammasome: a danger sensing complex triggering innate immunity. Curr Opin Immunol. 2007 ; 19: 615-622
29. Franchi L, Eigenbrod T, Muñoz-Planillo R, et al. The inflammasome: a caspase-1-activation platform that regulates immune responses and disease pathogenesis. Nat Immunol. 2009 ; 10: 241-247
30. von Moltke J, Trinidad NJ, Moayeri M, et al. Rapid induction of inflammatory lipid mediators by the inflammasome in vivo. Nature. 2012 ; 490: 107-111
31. Bours MJ, Swennen EL, Di Virgilio F, et al. Adenosine 5-triphosphate and adenosine as endogenous signaling molecules in immunity and inflammation. Pharmacol Ther. 2006 ; 112: 358-404
32. Di Virgilio F. Liaisons dangereuses: P2X7 and the inflammasome. Trends Pharmacol Sci. 2007 ; 28: 465-472
33. Yu HB, Finlay BB. The caspase-1 inflammasome: a pilot of innate immune response. Cell Host Microbe. 2008 ; 4: 198-208
34. 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
35. Duewell P, Kono H, Rayner KJ, et al. NLRP3 inflammasomes are required for atherogenesis and activated by cholesterol crystals. Nature. 2010 ; 464: 1357-1361
36. Feldmeyer L, Keller M, Niklaus G, et al. The inflammasome mediates UVB-induced activation and secretion of interleukin-1bata by keratinocytes. Curr Biol. 2007 ; 17: 1140-1145
37. Hise AG, Tomalka J, Ganesan S, et al. An essential role for the NLRP3 inflammasome in host defense against the human fungal pathogen Candida albicans. Cell Host Microbe. 2009 ; 5: 487-497
38. Hornung V, Bauernfeind F, Halle A, et al. Silica crystals and aluminum salts activate the NLRP3 inflammasome through phagosomal destabilization. Nat Immunol. 2008 ; 9: 847-856
39. Mariathasan S, Weiss DS, Newton K, et al. Cryopyrin activates the inflammasome in response to toxins and ATP. Nature. 2006 ; 440: 228-232
40. Martinon F, Pétrilli V, Mayor A, et al. Gout-associated uric acid crystals activate the NLRP3 inflammasome. Nature. 2006 ; 440: 237-241
41. Willingham SB, Bergstralh DT, O'Connor W, et al. Microbial pathogen-induced necrotic cell death mediated by the inflammasome component CIAS1/cryopyrin/NLRP3 and ASC. Cell Host Microbe. 2007 ; 2: 147-159
42. Bruey JM, Bruey-Sedano N, Luciano F, et al. Bcl-2 and Bcl-XL regulate proinflammatory caspase-1 activation with NALP1. Cell. 2007 ; 129: 45-56
43. Faustin B, Lartigue L, Bruey JM, et al. Reconstituted NALP1 inflammasome reveals two-step mechanism of caspase-1 activation. Mol Cell. 2007 ; 25: 713-724
44. Broz P, Ruby T, Belhocine K, et al. Caspase-11 increases susceptibility to Salmonella infection in the absence of caspase-1. Nature. 2012 ; 490: 288-291
45. Kayagaki N, Warming S, Lamkanfi M, et al. Non-canonical inflammasome activation targets caspase-11. Nature. 2011 ; 479: 117-121
46. Sollberger G, Strittmatter GE, Kistowska M, et al. Caspase-4 is required for activation of inflammasomes. J Immunol. 2012 ; 188: 1992-2000
47. Akhter A, Caution K, Abu Khweek A, et al. Caspase-11 promotes the fusion of phagosomes harboring pathogenic bacteria with lysosomes by modulating actin polymerization. Immunity. 2012 ; 37: 35-47
48. Schroder K, Tschopp J. The inflammasomes. Cell. 2010 ; 140: 821-832
49. Mehta VB, Hart J, Wewers MD. ATP stimulated release of IL-1β and IL-18 required priming by LPS and is independent of caspase-1 cleavage. J Biol Chem. 2001 ; 276: 3820-3826
50. Ferrari D, Pizzirani C, Adinolfi E, et al. The P2X7 receptor: a key player in IL-1 processing and release. J Immunol. 2006 ; 176: 3877-3883
51. Cruz CM, Rinna A, Forman HJ, et al. ATP activates a reactive oxygen species-dependent oxidative stress responses and secretion of proinflammatory cytokines in macrophages. J Biol Chem. 2007 ; 282: 2871-2879
52. Coutinho-Silva R, Corrêa G, Sater AA, et al. The P2X7 receptor and intracellular pathogens: a continuing struggle. Purinergic Signal. 2009 ; 5: 197-204
53. Liu H, Bowes RC, van de Water B, et al. Endoplasmic reticulum chaperones GRP78 and calreticulin prevent oxidative stress, Ca2+disturbances, and cell death in renal epithelial cells. J Biol Chem. 1997 ; 272: 21751-21759
54. Hayashi T, Saito A, Okuno S, et al. Damage to the endoplasmic reticulum and activation of apoptotic machinery by oxidative stress in ischemic neurons. J Cereb Blood Flow Metab. 2005 ; 25: 41-53
55. He S, Yaung J, Kim YH, et al. Endoplasmic reticulum stress induced by oxidative stress in retinal pigment epithelial cells. Graefes Arch Clin Exp Ophthalmol. 2008 ; 246: 677-683
56. Hitomi J, Katayama T, Eguchi Y, et al. Involvement of caspase-4 in endoplasmic reticulum stress-induced apoptosis and Aβ-induced cell death. J Cell Biol. 2004 ; 165: 347-356
57. Yoshida H, Haze K, Yanagi H, et al. Identification of the cis-acting endoplasmic reticulum stress response element responsible for transcriptional induction of mammalian Glc-regulated proteins. Involvement of basic leucine zipper transcription factors. J Biol Chem. 1998 ; 273: 33741-33749
58. Diez E, Balsinde J, Aracil M, et al. Ethanol induces release of arachidonic acid but not synthesis of eicosanoids in mouse peritoneal macrophages. Biochim Biophys Acta. 1987 ; 921: 82-89
59. Stancovski I, Baltimore D. NF-kappaB activation: the I kappaB kinase revealed?. Cell. 1997 ; 91: 299-302
60. Guha M, Mackman N. LPS induction of gene expression in human monocytes. Cell Signal. 2001 ; 13: 85-94
61. Rao KM. MAP kinase activation in macrophages. J Leukoc Biol. 2001 ; 69: 3-10
62. Angel P, Karin M. The role of Jun, Fos and the AP-1 complex in cell-proliferation and transformation. Biochim Biophys Acta. 1991 ; 1072: 129-157
63. Whitmarsh AJ, Davis RJ. Transcription factor AP-1 regulation by mitogen-activated protein kinase signal transduction pathways. J Mol Med. 1996 ; 74: 589-607
64. Medvedev AE, Kopydlowski KM, Vogel SN. Inhibition of lipopolysaccharide-induced signal transduction in endotoxin-tolerized mouse macrophages: dysregulation of cytokine, chemokine, and toll-like receptor 2 and 4 gene expression. J Immunol. 2000 ; 164: 5564-5574
65. Johansen C, Moeller K, Kragballe K, et al. The activity of caspase-1 is increased in lesional psoriatic epidermis. J Invest Dermatol. 2007 ; 127: 2857-2864
66. Ranganathan AC, Zhang L, Adam AP, et al. functional coupling of p38-induced up-regulation of Bip and activation of RNA-dependent protein kinase-like endoplasmic reticulum kinase to drug resistance of dormant carcinoma cells. Cancer Res. 2006 ; 66: 1702-1711
67. Schindler JF, Monahan JB, Smith WG. p38 pathway kinases as anti-inflammatory drug targets. J Dent Res. 2007 ; 86: 800-811
68. Ushio S, Namba M, Okura T, et al. Cloning of the cDNA for human IFN-gamma-inducing factor, expression in Escherichia coli, and studies on the biologic activities of the protein. J Immunol. 1996 ; 156: 4274-4279
69. Cheng J, Imanishi H, Morisaki H, et al. Recombinant HBsAg inhibits LPS-induced COX-2 expression and IL-18 production by interfering with the NFkappaB pathway in a human monocytic cell line, THP-1. J Hepatol. 2005 ; 43: 465-471
70. Bauernfeind F, 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 ; 187: 613-617
71. Liao PC, Chao LK, Chou JC, et al. Lipopolysaccharide/adenosine triphosphate-mediated signal transduction in the regulation of NLRP3 protein expression and caspase-1-mediated interleukin-1β secretion. Inflamm Res. 2013 ; 62: 89-96
72. Zhang R, Li S. COX-2 as a novel target of CRF family peptides' participating in inflammation. Biochem Biophys Res Commun. 2009 ; 382: 483-485
73. Park JY, Pillinger MH, Abramson SB. Prostaglandin E2 synthesis and secretion: the role of PGE2 synthases. Clin Immunol. 2006 ; 119: 229-240
74. Greenhough A, Smartt HJ, Moore AE, et al. The COX-2/PGE2 pathway: key roles in the hallmarks of cancer and adaptation to the tumour microenvironment. Carcinogenesis. 2009 ; 30: 377-386
75. Huang RY, Chen GG. Cigarette smoking, cyclooxygenase-2 pathway and cancer. Biochim Biophys Acta. 2011 ; 1815: 158-169
76. Leiro J, Alvarez E, Arranz JA, et al. Effects of cis-resveratrol on inflammatory murine macrophages: antioxidant activity and down-regulation of inflammatory genes. J Leukoc Biol. 2004 ; 75: 1156-1165
77. Barberà-Cremades M, Baroja-Mazo A, Gomez AI, et al. P2X7 receptor-stimulation causes fever via PGE2 and IL-1β release. FASEB J. 2012 ; 26: 2951-2962
78. Orallo F. Comparative studies of the antioxidant effects of cis-and trans-resveratrol. Curr Med Chem. 2006 ; 13: 87-98
79. Yokouchi M, Hiramatsu N, Hayakawa K, et al. Involvement of selective reactive oxygen species upstream of proapoptotic branches of unfolded protein response. J Biol Chem. 2008 ; 283: 4252-4260
80. Kuznetsov G, Bush KT, Zhang PL, et al. Perturbations in maturation of secretory proteins and their association with endoplasmic reticulum chaperones in a cell culture model for epithelial ischemia. Proc Natl Acad Sci U S A. 1996 ; 93: 8584-8589
81. Schmidt RL, Lenz LL. Distinct licensing of IL-18 and IL-1β secretion in response to NLRP3 inflammasome activation. PLoS One. 2012 ; 7: e45186 - e45186
82. Wenzel E, Somoza V. Metabolism and bioavailability of trans-resveratrol. Mol Nutr Food Res. 2005 ; 49: 472-481
83. Walle T, Hsieh F, DeLegge MH, et al. High absorption but very low bioavailability of oral resveratrol in humans. Drug Metab Dispos. 2004 ; 32: 1377-1382