Polyphenol-rich grape powder extract (GPE) attenuates inflammation in human macrophages and in human adipocytes exposed to macrophage-conditioned media

International Journal of Obesity

Volumn 34, Issue 5, 2010, Pages 800-808

  Overman, A ^a   Bumrungpert, A ^b   Kennedy, A ^a   Martinez, K ^a   Chuang, C C ^a   West, T ^a   Dawson, B ^a   Jia, W ^a   McIntosh, M ^a  

^a UNIVERSITY OF NORTH CAROLINA AT GREENSBORO   (United States)

^b MAHIDOL UNIVERSITY   (Thailand)

Author keywords

Adipocytes; Grape powder extract; Inflammation; Insulin resistance; Macrophages

Indexed keywords

CYCLOOXYGENASE 2; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GRAPE POWDER EXTRACT; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; LIPOPOLYSACCHARIDE; MITOGEN ACTIVATED PROTEIN KINASE; PLANT EXTRACT; POLYPHENOL; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR ELK 1; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; CULTURE MEDIUM; CYTOKINE; FLAVONOID; PHENOL DERIVATIVE;

ADIPOCYTE; ARTICLE; CELL STIMULATION; CELL STRAIN U937; CONTROLLED STUDY; CULTURE MEDIUM; CYTOKINE PRODUCTION; ENZYME ACTIVATION; GENE; GENE EXPRESSION; GLUCOSE TRANSPORT; HUMAN; HUMAN CELL; INCUBATION TIME; INFLAMMATION; INSULIN RESISTANCE; MACROPHAGE; PHOSPHORYLATION; PRIORITY JOURNAL; REPORTER GENE; CHEMISTRY; DRUG EFFECTS; IMMUNOLOGY; METABOLISM; PHARMACOLOGY; PHYSIOLOGY; VITIS;

ADIPOCYTES; CULTURE MEDIA, CONDITIONED; CYTOKINES; FLAVONOIDS; HUMANS; INFLAMMATION; INSULIN RESISTANCE; LIPOPOLYSACCHARIDES; MACROPHAGES; PHENOLS; PLANT EXTRACTS; VITIS; POLYPHENOLS;

VITACEAE;

EID: 77952289381     PISSN: 03070565     EISSN: 14765497     Source Type: Journal    
DOI: 10.1038/ijo.2009.296     Document Type: Article

References (66)

1. Tilg H, Moschen AR. Adipocytokines: mediators linking adipose tissue, inflammation and immunity. Nat Rev Immunol 2006; 6: 772-783.
2. Poirier P, Giles TD, Bray GA, Hong Y, Stern JS, Pi-Sunyer FX et al. Obesity and cardiovascular disease: pathophysiology, evaluation, and effect of weight loss: an update of the 1997 American Heart Association Scientific Statement on Obesity and Heart Disease from the Obesity Committee of the Council on Nutrition, Physical Activity, and Metabolism. Circulation 2006; 113: 898-918.
3. Cottam DR, Mattar SG, Barinas-Mitchell E, Eid G, Kuller L, Kelley DE et al. The chronic inflammatory hypothesis for the morbidity associated with morbid obesity: implications and effects of weight loss. Obes Surg 2004; 14: 589-600.
4. Trayhurn P, Wood IS. Adipokines: inflammation and the pleio-tropic role of white adipose tissue. Br J Nutr 2004; 92: 347-355.
5. Laine PS, Schwartz EA, Wang Y, Zhang WY, Karnik SK, Musi N et al. Palmitic acid induces IP-10 expression in human macro-phages via NF-kappaB activation. Biochem Biophys Res Commun 2007; 358: 150-155.
6. Wellen KE, Hotamisligil GS. Inflammation, stress, and diabetes. J Clin Invest 2005; 115: 1111-1119.
7. Fantuzzi G. Adipose tissue, adipokines, and inflammation. J Allergy Clin Immunol 2004; 115: 911-919.
8. Fain JN, Madan AK, Hiler ML, Cheema P, Bahouth SW. Comparison of the release of adipokines by adipose tissue, adipose tissue matrix, and adipocytes from visceral and subcutaneous abdominal adipose tissue of obese humans. Endocrinology 2004; 145: 2273-2282.
9. Clément K, Viguerie N, Poitou C, Carette C, Pelloux V, Curat CA et al. Weight loss regulates inflammation-related genes in white adipose tissue of obese subjects. FASEB J 2004; 18: 1657-1669.
10. Curat CA, Wegner V, Sengenes C, Miranville A, Tonus C, Busse R et al. Macrophages in human visceral adipose tissue: increased accumulation in obesity and a source of resistin and visfatin. Diabetologia 2006; 49: 744-747.
11. Kanda H, Tateya S, Tamori Y, Kotani K, Hiasa K, Kitazawa R. MCP-1 contributes to macrophage infiltration into adipose tissue, insulin resistance, and hepatic steatosis in obesity. J Clin Invest 2006; 116: 1494-1505.
12. Skurk T, Herder C, Kraft I, Muller-Scholze S, Hauner H, Kolb H. Production and release of macrophage migration inhibitory factor from human adipocytes. Endocrinology 2005; 146: 1006-1011.
13. Lumeng C, Deyoung S, Saltiel A. Macrophages block insulin action in adipcytes by altering expression of signaling and glucose transport proteins. Am J Physiol 2007; 292: E166-E174.
14. Arkan MC, Hevener AL, Greten FR, Maeda S, Li ZW, Long JM et al. IKK-beta links inflammation to obesity-induced insulin resistance. Nat Med 2005; 11: 191-198.
15. Weisberg SP, Hunter D, Huber R, Lemieux J, Slaymaker S, Vaddi K et al. CCR2 modulates inflammatory and metabolic effects of high-fat feeding. J Clin Invest 2005; 116: 115-124.
16. Cani PD, Bibiloni R, Knauf C, Waget A, Neyrinck AM, Delzenne NM et al. Changes in gut microbiota control metabolic endo-toxemia-induced inflammation in high-fat fed mice-induced obesity and diabetes. Diabetes 2008; 57: 1470-1481.
17. Sakurai T, Kitadateb K, Nishiokab H, Fujiib H, Kizakia T, Kondohc Y et al. Oligomerized grape seed polyphenols attenuate inflammatory changes due to antioxidative properties in coculture of adipocytes and macrophages. J Nutr Biochem 2010; 21: 47-54.
18. Terra X, Valls J, Vitrac X, Mérrillon JM, Arola L, Ardèvol A et al. Grape-seed procyanidins act as antiinflammatory agents in endotoxin-stimulated RAW 264.7 macrophages by inhibiting NFkB signaling pathway. J Agric Food Chem 2007; 55: 4357-4365.
19. Brown JM, Sandberg-Boysen M, Chung S, Fabiyi O, Morrision R, Mandrup S et al. Conjugated linoleic acid (CLA) induces human adipocyte delipidation: autocrine/paracrine regulation of MEK/ERK signaling by adipocytokines. J Biol Chem 2004; 279: 26735-26747.
20. Chung S, Lapoint K, Martinez K, Kennedy A, Boysen Sandberg M, McIntosh MK. Preadipocytes mediate lipopolysaccharide-induced inflammation and insulin resistance in primary cultures of newly differentiated human adipocytes. Endocrinology 2006; 147: 5340-5351.
21. Seymour EM, Singer AA, Bennink MR, Parikh RV, Kirakosyan A, Kaufman PB et al. Chronic intake of phytochemical-enriched diet reduces cardiac fibrosis and diastolic dysfunction caused by prolonged salt-sensitive hypertension. J Gerontol A Biol Sci Med Sci 2008; 63: 1034-1042.
22. Xie G, Zhao A, Li P, Li L, Jia W. Fingerprint analysis of Rhizoma chuanxiong by pressurized capillary electrochromatography and high-performance liquid chromatography. Biomed Chromatogr 2007; 21: 867-875.
23. Suganami T, Nishida H, Ogawa Y. A paracrine loop between adipocytes and macrophages aggravates inflammatory changes: Role of free fatty acids and TNFa. Arterioscler Throm Vasc Biol 2005; 25: 2062-2068.
24. Jang S, Kelley KW, Johnson RW. Luteolin reduces IL-6 production in microglia by inhibiting JNK phosphorylation and activation of AP-1. Proc Natl Acad Sci USA 2008; 105: 7534-7539.
25. Chen CY, Peng WH, Tsai KD, Hsu SL. Luteolin suppresses inflammation-associated gene expression by blocking NF-kappaB and AP-1 activation pathway in mouse alveolar macrophages. Life Sci 2007; 81: 1602-1614.
26. Xu H, Barnes GT, Yang Q, Tan G, Yang D, Chou CJ et al. Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J Clin Invest 2003; 112: 1821-1830.
27. Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, Ferrante Jr AW. Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 2003; 112: 1796-1808.
28. Permana PA, Menge C, Reaven PD. Macrophage-secreted factors induce adipocyte inflammation and insulin resistance. Biochem Biophys Res Commun 2006; 341: 507-514.
29. Leifert W, Abeywardena M. Cardioprotective actions of grape polyphenols. Nutr Res 2008; 28: 729-737.
30. Perez-Jimenez J, Saurea-Calixto F. Grape products and cardiovascular disease risk factors. Nutr Res Rev 2008; 21: 158-173.
31. Castilla P, Dávalos A, Teruel JL, Cerrato F, Fernández- Lucas M, Merino JL et al. Comparative effects of dietary supplementation with red grape juice and vitamin E on production of superoxide by circulating neutrophil NADPH oxidase in hemodialysis patients. Am J Clin Nutr 2008; 87: 1053-1061.
32. O'Bryne DJ, Devaraj S, Grundy SM, Jialal I. Comparison of the antioxidant effects of Concord grape juice flavonoids a-tocopherol on markers of oxidative stress in healthy adults. Am J Clin Nutr 2002; 76: 1367-1374.
33. Zern TL, Wood RJ, Greene C, West KL, Liu Y, Aggarwal D et al. Grape polyphenols exert a cardioprotective effect in pre-and postmenopausal women by lowering plasma lipids and reducing oxidative stress. J Nutr 2005; 135: 1911-1917.
34. Pignatelli P, Ghiselli A, Buchetti B, Carnevale R, Natella F, Germanó G et al. Polyphenols synergestically inhibit oxidative stress in subjects given red and white wine. Atherosclerosis 2006; 188: 77-83.
35. Terra X, Montagut G, Bustos M, Llopiz N, Ardèvol A, Bladé C et al. Grape-seed procyanidins prevent low-grade inflammation by modulating cytokine expression in rats fed a high-fat diet. J Nutr Biochem 2009; 20: 210-218.
36. Fuhrman B, Volkova N, Coleman R, Aviram M. Grape powder polyphenols attenuate atherosclerosis development in apolipo-protein E deficient (E0) mice and reduce macrophage athero-genicity. J Nutr 2005; 135: 722-728.
37. Vinson JA, Mandarano MA, Shuta DL, Bagchi M, Bagchi D. Beneficial effects of novel IH636 grape seed proanthocyanidin extract and niacin-bound chromium in a hamster atherosclerosis model. Mol Cell Biochem 2002; 240: 99-103. (Pubitemid 35385824)
38. Terra X, Fernández-Larrea J, Pujadas G, Ardèvol A, Bladé C, Salvadó J et al. Inhibitory effects of grape seed procyanidins on foam cell formation in vitro. J Agric Food Chem 2009; 57: 2588-2594.
39. Chacón MR, Ceperuelo-Mallafré V, Maymó-Masip E, Mateo-Sanz JM, Arola L, Guitiérrez C et al. Grape-seed procyanidins modulate inflammation on human differentiated adipocytes in vitro. Cytokine 2009; 47: 137-142.
40. Iyori M, Kataoka H, Shamsul HM, Kiura K, Yasuda M, Nakata T et al. Resveratrol modulates phagocytosis of bacteria through an NF-kappaB-dependent gene program. Antimicrob Agents Chemother 2008; 52: 121-127.
41. Moon SO, Kim W, Sung MJ, Lee S, Kang KP, Kim DH et al. Resveratrol suppresses tumor necrosis factor-alpha-induced frac-talkine expression in endothelial cells. Mol Pharmacol 2006; 70: 112-119.
42. Okoko T, Oruambo IF. Inhibitory activity of quercetin and its metabolite on lipopolysaccharide-induced activation of macro-phage U937 cells. Food Chem Toxicol 2009; 47: 809-812.
43. Kaneko M, Takimoto H, Sugiyama T, Seki Y, Kawaguchi K, Kumazawa Y. Suppressive effects of the flavonoids quercetin and luteolin on the accumulation of lipid rafts after signal transduc-tion via receptors. Immunopharmacol Immunotoxicol 2008; 30: 867-882.
44. Necela BM, Su W, Thompson EA. Toll-like receptor 4 mediates cross-talk between peroxisome proliferator-activated receptor g and nuclear factor-kB in macrophages. Immunology 2008; 125: 344-358.
45. Su CG, Wen X, Bailey ST, Jiang W, Rangwala SM, Keilbaugh SA et al. A novel therapy for colitis utilizing PPAR-gamma ligands to inhibit the epithelial inflammatory response. J Clin Invest 1999; 104: 383-389.
46. Desreumaux P, Dubuquoy L, Nutten S, Peuchmaur M, Englaro W, Schoonjans K et al. Attenuation of colon inflammation through activators of the retinoid X receptor(RXR)/peroxisome prolifera-tor-activated receptor gamma(PPARgamma) heterodimer. A basis for new therapeutic strategies. J Exp Med 2001; 193: 827-838.
47. Saubermann LJ, Nakajima A, Wada K, Zhao S, Terauchi Y, Kadowaki T et al. Peroxisome proliferator-activated receptor gamma agonist ligands stimulate a Th2 cytokine response and prevent acute colitis. Inflamm Bowel Dis 2002; 8: 330-339.
48. Katayama K, Wada K, Nakajima A, Mizuguchi H, Hayakawa T, Nakagawa S et al. A novel PPAR gamma gene therapy to control inflammation associated with inflammatory bowel disease in a murine model. Gastroenterology 2003; 124: 1315-1324.
49. Lytle C, Tod TJ, Vo KT, Lee JW, Atkinson RD, Straus DS. The peroxisome proliferator-activated receptor gamma ligand rosigli-tazone delays the onset of inflammatory bowel disease in mice with interleukin 10 deficiency. Inflamm Bowel Dis 2005; 11: 231-243.
50. Schaefer KL, Denevich S, Ma C, Cooley SR, Nakajima A, Wada K et al. Intestinal anti-inflammatory effects of thiazolidenedione peroxisome proliferator-activated receptor-gamma ligands on T helper type 1 chemokine regulation include nontranscriptional control mechanisms. Inflamm Bowel Dis 2005; 11: 244-252.
51. Nagy L, Tontonoz P, Alvarez JG, Chen H, Evans RM. Oxidized LDL regulates macrophage gene expression through ligand activation of PPARgamma. Cell 1998; 93: 229-240.
52. Tontonoz P, Nagy L, Alvarez JG, Thomazy VA, Evans RM. PPARgamma promotes monocyte/macrophage differentiation and uptake of oxidized LDL. Cell 1998; 93: 241-252.
53. Li AC, Brown KK, Silvestre MJ, Willson TM, Palinski W, Glass CK. Peroxisome proliferator-activated receptor gamma ligands inhibit development of atherosclerosis in LDL receptor-deficient mice. J Clin Invest 2000; 106: 523-531.
54. Zhang L, Chawla A. Role of PPARgamma in macrophage biology and atherosclerosis. Trends Endocrinol Metab 2004; 15: 500-505.
55. Hammad H, de Heer HJ, Soullie T, Angeli V, Trottein F, Hoogsteden HC et al. Activation of peroxisome proliferator activated receptor-gamma in dendritic cells inhibits the development of eosinophilic airway inflammation in a mouse model of asthma. Am J Pathol 2004; 164: 263-271.
56. Woerly G, Honda K, Loyens M, Papin JP, Auwerx J, Staels B et al. Peroxisome proliferator-activated receptors alpha and gamma down-regulate allergic inflammation and eosinophil activation. J Exp Med 2003; 198: 411-421.
57. Trifilieff A, Bench A, Hanley M, Bayley D, Campbell E, Whittaker P. PPAR-alpha and-gamma but not-delta agonists inhibit airway inflammation in a murine model of asthma: in vitro evidence for an NF-kappaB-independent effect. Br J Pharmacol 2003; 139: 163-171.
58. Demerjian M, Man MQ, Choi EH, Brown BE, Crumrine D, Chang S et al. Topical treatment with thiazolidinediones, activators of peroxisome proliferator-activated receptor-gamma, normalizes epidermal homeostasis in a murine hyperproliferative disease model. Exp Dermatol 2006; 15: 154-160.
59. Hasegawa H, Takano H, Zou Y, Qin Y, Hizukuri K, Odaka K et al. Pioglitazone, a peroxisome proliferator activated receptor gamma activator, ameliorates experimental autoimmune myocarditis by modulating Th1/Th2 balance. J Mol Cell Cardiol 2005; 38: 257-265.
60. Yuan ZY, Liu Y, Liu Y, Zhang JJ, Kishimoto C, Wang YN et al. PPAR-gamma ligands inhibit the expression of inflammatory cytokines and attenuate autoimmune myocarditis. Chin Med J (Engl) 2004; 117: 1253-1255. (Pubitemid 39199936)
61. Natarajan C, Bright JJ. Peroxisome proliferator-activated receptor-gamma agonists inhibit experimental allergic encephalomyelitis by blocking IL-12 production, IL-12 signaling and Th1differen-tiation. Genes Immun 2002; 3: 59-70.
62. Diab A, Deng C, Smith JD, Hussain RZ, Phanavanh B, Lovett-Racke AE et al. Peroxisome proliferator-activated receptor-gamma agonist 15-deoxy-Delta(12,14)- prostaglandinJ(2) ameliorates experimental autoimmune encephalomyelitis. J Immunol 2002; 168: 2508-2515.
63. Wang Q, Xia M, Liu C, Guo H, Ye Q, Hu Y et al. Cyanidin-3-O-beta- glucoside inhibits iNOS and COX-2 expression by inducing liver X receptor alpha activation in THP-1 macrophages. Life Sci 2008; 83: 176-184.
64. Xia M, Hou M, Zhu H, Ma J, Tang Z, Wang Q et al. Anthocyanins induce cholesterol efflux from mouse peritoneal macrophages: the role of the peroxisome proliferator-activated receptor {gamma}-liver X receptor {alpha}-ABCA1 pathway. J Biol Chem 2005; 280: 36792-36801.
65. Szanto A, Rõszer T. Nuclear receptors in macrophages: A link between metabolism and inflammation. FEBS Lett 2008; 582: 106-116.
66. Varga T, Nagy L. Nuclear receptors, transcription factors linking lipid metabolism and immunity: the case of peroxisome proliferator-activated receptor gamma. Eur J Clin Invest 2008; 38: 695-707.