Nutrition Research and Practice

The Korean Nutrition Society (한국영양학회)
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Resveratrol blunts tumor necrosis factor-${\alpha}$-induced monocyte adhesion and transmigration

  • Kim, Dong-Shoo (Department of Food and Nutrition and Korean Institute of Nutrition, Hallym University) ;
  • Kwon, Hyang-Mi (Department of Food and Nutrition and Korean Institute of Nutrition, Hallym University) ;
  • Choi, Jung-Suk (Department of Food and Nutrition and Korean Institute of Nutrition, Hallym University) ;
  • Kang, Sang-Wook (Department of Food and Nutrition and Korean Institute of Nutrition, Hallym University) ;
  • Ji, Geun-Eog (Department of Food and Nutrition, Seoul National University) ;
  • Kang, Young-Hee (Department of Food and Nutrition and Korean Institute of Nutrition, Hallym University)
  • Published : 2007.12.31
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Abstract

The leukocyte recruitment and transmigration across the endothelial barrier into the vessel wall are crucial steps in atherosclerosis. Leukocyte trafficking on the endothelium is elicited by induction of endothelial adhesion molecules, and its transmigration is mediated by degradation of basement membrane proteins through enzymatic activity of matrix metalloproteinases (MMP). The current study investigated whether resveratrol, a polyphenol present in grapes and red wine, was capable of inhibiting leukocyte adhesion to tumor necrosis factor (TNF)-${\alpha}$-activated endothelium. It was found that resveratrol inhibited the TNF-${\alpha}$-activated endothelial expression of vascular cell adhesion molecule-1 in a dose-dependent manner. In addition, resveratrol hampered THP-1 monocyte adhesion to activated endothelial cells. This study further examined whether resveratrol interfered with transendothelial migration of leukocytes. The MMP-2 gelatinolytic activity of endothelial cells was enhanced by TNF-${\alpha}$, which was attenuated by an addition of ${\geq}25{\mu}M$ resveratrol. In addition, 25 ${\mu}M$ resveratrol mitigated the MMP-9 activity of THP-1 cells, followed by a marked inhibition of transendothelial migration. These results demonstrated that resveratrol suppressed monocyte adhesion and migration induced by TNF-${\alpha}$ through modulating expression of adhesion molecules and gelatinolytic activity of MMP. These findings suggest that dietary resveratrol may be therapeutic agent for inhibiting leukocyte recruitment into the subendothelium during inflammatory atherosclerosis.

Keywords

References

  1. Ahn J, Lee H, Kim S & Ha T (2007). Resveratrol inhibits TNF-${\alpha}$-induced changes of adipokines in 3T3-L1 adipocytes. Biochem Biophys Res Commun 364:972-977 https://doi.org/10.1016/j.bbrc.2007.10.109
  2. Aviram M & Fuhrman B (2002). Wine flavonoids protect against LDLoxidation and atherosclerosis. Ann NY Acad Sci 957:146-161 https://doi.org/10.1111/j.1749-6632.2002.tb02913.x
  3. Baur JA & Sinclair DA (2006). Therapeutic potential of resveratrol: the in vivo evidence. Nat Rev Drug Discov 5:493-506 https://doi.org/10.1038/nrd2060
  4. Belleville J (2002). The French paradox: possible involvement of ethanol in the protective effect against cardiovascular diseases. Nutrition 18:173-177 https://doi.org/10.1016/S0899-9007(01)00721-3
  5. Berk BC, Abe JI, Min W, Surapisitchat H & Yan C (2001). Endothelial atheroprotective and anti-inflammatory mechanisms. Ann N Y Acad Dci 947:93-111
  6. Bertelli AA, Giovannini L, Giannessi D, Migliori M, Bernini W, Fregoni M & Bertelli A (1995). Antiplatelet activity of synthetic and natural resveratrol in red wine. Int J Tissue React 17:1-3
  7. Bradamante S, Barenghi L & Villa A (2004). Cardiovascular protective effects of resveratrol. Cardiovasc Drug Rev 22:169-188 https://doi.org/10.1111/j.1527-3466.2004.tb00139.x
  8. Choi YJ, Jeong YJ, Lee YJ, Kwon HM & Kang YH (2005). (-) Epigallocatechin gallate and quercetin enhance survival signaling in response to oxidant-induced human endothelial apoptosis. J Nutr 135:707-713
  9. Chow SE, Hshu YC, Wang JS & Chen JK (2007). Resveratrol attenuates oxLDL-stimulated NADPH oxidase activity and protects endothelial cells from oxidative functional damages. J Appl Physiol 102:1520-1527 https://doi.org/10.1152/japplphysiol.00881.2006
  10. Cullen JP, Morrow D, Jin Y, von Offenberg Sweeney N, Sitzmann JV, Cahill PA & Redmond EM (2007). Resveratrol inhibits expression and binding activity of the monocyte chemotactic protein-1 receptor, CCR2, on THP-1 monocytes. Atherosclerosis 195:e125-e133 https://doi.org/10.1016/j.atherosclerosis.2007.03.039
  11. de Lange DW, Verhoef S, Gorter G, Kraaijenhagen RJ, van de Wiel A & Akkerman JW. (2007) Polyphenolic grape extract inhibits platelet activation through PECAM-1: an explanation for the French paradox. Alcohol Clin Exp Res 31:1308-1314 https://doi.org/10.1111/j.1530-0277.2007.00439.x
  12. Fukuhara K, Nagakawa M, Nakanishi I, Ohkubo K, Imai K, Urano S, Fukuzumi S, Ozawa T, Ikota N, Mochizuki M, Miyata N & Okuda H (2006). Structural basis for DNA-cleaving activity of resveratrol in the presence of $Cu^{2+}$. Bioorg Med Chem 14: 1437-1443 https://doi.org/10.1016/j.bmc.2005.09.070
  13. Gagliano N, Moscheni C, Torri C, Magnani I, Bertelli AA & Gioia M (2005). Effect of resveratrol on matrix metalloproteinase-2 (MMP-2) and Secreted Protein Acidic and Rich in Cysteine (SPARC) on human cultured glioblastoma cells. Biomed Pharmacother 59:359-364 https://doi.org/10.1016/j.biopha.2005.06.001
  14. Galis ZS, Sukhova GK, Lark MW & Libby P (1994). Increased expression of matrix metalloproteinases and matrix degrading activity in vulnerable regions of human atherosclerotic plaques. J Clin Invest 94:2493-2503 https://doi.org/10.1172/JCI117619
  15. Hao HD & He LR (2004). Mechanisms of cardiovascular protection by resveratrol. J Med Food 7:290-298 https://doi.org/10.1089/jmf.2004.7.290
  16. Hu J, Huang Y, Xiong M, Luo S, Chen Y & Li Y (2006). The effects of natural flavonoids on lipoxygenase-mediated oxidation of compounds with a benzene ring structure-a new possible mechanism of flavonoid anti-chemical carcinogenesis and other toxicities. Int J Toxicol 25:295-301 https://doi.org/10.1080/10915810600746122
  17. Katiyar SK (2006). Matrix metalloproteinases in cancer metastasis: molecular targets for prostate cancer prevention by green tea polyphenols and grape seed proanthocyanidins. Endocr Metab Immune Disord Drug Targets 6:17-24 https://doi.org/10.2174/187153006776056648
  18. Krasinski K, Spyridopoulos I, Kearney M & Losordo DW (2000). In vivo blockade of tumor necrosis factor-alpha accelerates functional endothelial recovery after balloon angioplasty. Circulation 104:1754-1756 https://doi.org/10.1161/hc4001.098046
  19. Middleton E. Jr, Kandaswami C & Theoharides TC (2000). The effects of plant flavonoids on mammalian cells: implications for inflammation heart disease and cancer. Pharmacol Rev 52:673-751
  20. Nagaoka I & Hirota S (2000). Increased expression of matrix metalloproteinase-9 in neutrophils in glycogen-induced peritoneal inflammation of guinea pigs. Inflamm Res 49:55-62
  21. Nakashima Y, Raines EW, Plump AS, Breslow JL & Ross R (1998). Upregulation of VCAM-1 and ICAM-1 at atherosclerosis-prone sites on the endothelium in the Apo-E-deficient mouse. Arterioscler Thromb Vasc Biol 18:842-851 https://doi.org/10.1161/01.ATV.18.5.842
  22. Nijveldt RJ, van Nood E, van Hoorn DE, Boelens PG, van Norren K & van Leeuwen PA (2001). Flavonoids: a review of probable mechanisms of action and potential applications. Am J Clin Nutr 74:418-425 https://doi.org/10.1093/ajcn/74.4.418
  23. Pober JS & Cotran RS (1990). The role of endothelial cells in inflammation. Transplantation 50:537-533 https://doi.org/10.1097/00007890-199010000-00001
  24. Ross R (1993). The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature 362:801-809 https://doi.org/10.1038/362801a0
  25. Saarialho-Kere UK, Welgus HG & Parks WC (1993). Distinct mechanisms regulate interstitial collagenase and 92-kDa gelatinase expression in human monocytic-like cells exposed to bacterial endotoxin. J Biol Chem 268:7354-7361
  26. Schonbeck U, Mach F & Libby P (2000). CD154 (CD40 ligand). Int J Biochem Cell Biol 32:687-693 https://doi.org/10.1016/S1357-2725(00)00016-9
  27. Shankar S, Singh G & Srivastava RK (2007). Chemoprevention by resveratrol: molecular mechanisms and therapeutic potential. Front Biosci 12:4839-4854 https://doi.org/10.2741/2432
  28. Stoclet JC, Chataigneau T, Ndiaye M, Oak MH, El Bedoui J, Chataigneau M & Schini-Kerth VB (2004). Vascular protection by dietary polyphenols. Eur J Pharmacol 500:299-313 https://doi.org/10.1016/j.ejphar.2004.07.034
  29. Teixeira S, Siquet C, Alves C, Boal I, Marques MP, Borges F, Lima JL & Reis S (2005). Structure-property studies on the antioxidant activity of flavonoids present in diet. Free Radic Biol Med 39:1099-108 https://doi.org/10.1016/j.freeradbiomed.2005.05.028
  30. Woo JH, Lim JH, Kim YH, Suh SI, Min DS, Chang JS, Lee YH, Park JW & Kwon TK (2004). Resveratrol inhibits phorbol myristate acetate-induced matrix metalloproteinase-9 expression by inhibiting JNK and PKC delta signal transduction. Oncogene 23:1845-1853 https://doi.org/10.1038/sj.onc.1207307
  31. Wung BS, Hsu MC, Wu CC & Hsieh CW (2005). Resveratrol suppresses IL-6-induced ICAM-1 gene expression in endothelial cells: effects on the inhibition of STAT3 phosphorylation. Life Sci 78:389-397 https://doi.org/10.1016/j.lfs.2005.04.052
  32. Zhu Z, Klironomos G, Vachereau A, Neirinck L & Goodman DW (1999). Determination of trans-resveratrol in human plasma by high-performance liquid chromatography. J Chromatogr B 724: 389-392 https://doi.org/10.1016/S0378-4347(98)00586-6