Effects of resveratrol on obesity-related inflammation markers in adipose tissue of genetically obese rats

Nutrition

Volumn 29, Issue 11-12, 2013, Pages 1374-1380

  Gómez Zorita, Saioa ^a,b   Fernández Quintela, Alfredo ^a,b   Lasa, Arrate ^a,b   Hijona, Elizabeth ^a,c   Bujanda, Luis ^a,c   Portillo, María P ^a,b  

^a UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

^b Instituto de Salud Carlos III   (Spain)

^c INSTITUTO DE SALUD CARLOS III   (Spain)

Author keywords

Adipose tissue; Inflammation; Lipases; Lipogenesis; Resveratrol; Zucker rat

Indexed keywords

ACETYL COENZYME A CARBOXYLASE; C REACTIVE PROTEIN; CYTOKINE; GLUCOSE 6 PHOSPHATE DEHYDROGENASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; LIPOPROTEIN LIPASE; MONOCYTE CHEMOTACTIC PROTEIN 1; RESVERATROL;

ADIPOSE TISSUE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BODY FAT; BODY WEIGHT; CELL INFILTRATION; CHRONIC INFLAMMATION; CONTROLLED STUDY; DRUG EFFICACY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME INHIBITION; FATTY ACID TRANSPORT; FOOD INTAKE; LIPOLYSIS; MACROPHAGE; MALE; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WEIGHT REDUCTION; WESTERN BLOTTING;

RATTUS; RICE STRIPE VIRUS;

ADIPOSE TISSUE; INFLAMMATION; LIPASES; LIPOGENESIS; RESVERATROL; ZUCKER RAT;

ACETYL-COA CARBOXYLASE; ADIPONECTIN; ADIPOSE TISSUE; ANIMALS; BODY WEIGHT; C-REACTIVE PROTEIN; CHEMOKINE CCL2; FATTY ACIDS; GLUCOSEPHOSPHATE DEHYDROGENASE; INFLAMMATION; INTERLEUKIN-6; LIPOLYSIS; MALE; NF-KAPPA B; OBESITY; RATS; RATS, ZUCKER; STILBENES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84884987767     PISSN: 08999007     EISSN: 18731244     Source Type: Journal    
DOI: 10.1016/j.nut.2013.04.014     Document Type: Article

References (52)

1. Kershaw E., Schupp M., Guan H.P., Grdner N.P., Lazar M.A., Flier J.S. PPARγ regulates adipose triglyceride lipase in adipocytes invitro and invivo. Am J Physiol Endocrinol Metab 2007, 293:E1736-E1745.
2. Rajala M.W., Obici S., Scherer P.E., Rossetti L. Adipose-derived resistin and gut-derived resistin-like molecule-β selectively impair insulin action on glucose production. J Clin Invest 2003, 111:225-230.
3. Bastard J.P., Maachi M., Lagathu C., Kim M.J., Caron M., Vidal H. Recent advancesin the relationship between obesity, inflammation, and insulin resistance. Eur Cytokine Netw 2006, 17:4-12.
4. Tilg H., Moschen A.R. Adipocytokines: mediators linking adipose tissue, inflammation and immunity. Nat Rev Immunol 2006, 6:772-783.
5. Xu H., Barnes G.T., Yang Q., Tan G., Yang D., Chou C.J., 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.
6. Schinler Y.H., Cardenas J., Prior J.O., Facta A.D., Kreissl M.C., Zhang X.L., et al. Relationship between increasing body weight, insulin resistance, inflammation, adipocyte leptin and coronary circulatory function. J Am Coll Cardiol 2006, 47:1188-1195.
7. Weisberg S.P., McCann D., Desai M., Rosenbaum M., Leibel R.L., Ferrante A.W. Obesity is associated with macrophage accumulation in adipose tissue. JCI 2003, 112:1796-1808.
8. Kang H.S., Okamoto K., Kim Y.S., Takeda Y., Bortner C.D., Dang H., et al. Nuclear orphan receptor TAK1/TR4-deficient mice are protected against obesity-linked inflammation, hepatic steatosis, and insulin resistance. Diabetes 2011, 60:177-188.
9. Langcake P., Pryce R.J. The production of resveratrol by Vitis Vinifera and other members of the Vitaceae as a response to infection or injury. Physiol Plant Phatol 1976, 9:77-86.
10. Frémont L. Biological effects of resveratrol. Life Sci 2000, 66:663-673.
11. Goswami S., Das D. Resveratrol and chemoprevention. Cancer Lett 2009, 284:1-6.
12. Das S., Das D.K. Anti-inflammatory responses of resveratrol. Inflamm Allergy Drug Targets 2007, 6:168-173.
13. González R., Ballester I., López-Posadas R., Suárez M.D., Zarzuelo A., Martínez-Augustin O., et al. Effects of flavonoids and other polyphenols on inflammation. Crit Rev Food Sci Nutr 2011, 51:331-362.
14. Kowalski J., Samojedni A., Paul M., Pietsz G., Wilczok T. Effect of apigenin, kaempferol and resveratrol on the expression of interleukin-1 beta and tumor necrosis factor-alpha genes in J774.2 macrophages. Pharmacol Rep 2005, 57:390-394.
15. Ma Z.H., Ma Q.Y., Wang L.C., Sha H.C., Wu S.L., Zhang M. Effect of resveratrol NF-kappaB activity in rat peritoneal macrophages. Am J Chin Med 2006, 34:623-630.
16. Lagouge M., Argmann C., Gerhart-Hines Z., Meziane H., Lerin C., Daussin F., et al. Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1 alpha. Cell 2006, 127:1109-1122.
17. Ahn J., Cho I., Kim S., Kwon D., Ha T. Dietary resveratrol alters lipid metabolism-related gene expression of mice on an atherogenic diet. J Hepatol 2008, 49:1019-1028.
18. Barger J.L., Kayo T., Vann J.M., Arias E.B., Wang J., Hacker T.A., et al. A Low Dose of Dietary Resveratrol Partially Mimics Caloric Restriction and Retards Aging Parameters in Mice. PLoS ONE 2008, 3:e2264.
19. Macarulla M.T., Alberdi G., Gómez S., Tueros I., Bald C., Rodríguez V.M., et al. Effects of different doses of resveratrol on body fat and serum parameters in rats fed a hypercaloric diet. J Physiol Biochem 2009, 65:369-376.
20. Rivera L., Morón R., Zarzuelo A., Galisteo M. Long-term resveratrol administration reduces metabolic disturbances and lowers blood pressure in obese Zucker rats. Biochem Pharmacol 2009, 77:1053-1063.
21. Szkudelska K., Szkudelski T. Resveratrol, obesity and diabetes. Eur J Pharmacol 2010, 635:1-8.
22. Alberdi G., Rodríguez V.M., Miranda J., Macarulla M.T., Arias N., Andrés-Lacueva C., et al. Changes in white adipose tissue metabolism induced by resveratrol in rats. Nutr Metab 2011, 8:29.
23. Dal-Pan A., Blanc S., Aujard F. Resveratrol suppresses body mass gain in a seasonal non-human primate model of obesity. BMC Physiology 2010, 10:11.
24. Timmers S., Konings E., Bilet L., Houtkooper R.H., van de Weijer T., Goossens G.H., et al. Calorie restriction-like effects of 30 days of resveratrol supplementation on energy metabolism and metabolic profile in obese humans. Cell Metab 2011, 14:612-622.
25. Zabala A., Churruca I., Macarulla M.T., Rodriguez V.M., Fernandez-Quintela A., Martinez J.A., et al. The trans-10, cis-12 isomer of conjugated linoleic acid reduces hepatic triacylglycerol content without affecting lipogenic enzymes in hamsters. Br J Nutr 2004, 92:383-389.
26. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25:402-408.
27. Gómez-Zorita S., Fernández-Quintela A., Macarulla M.T., Aguirre L., Hijona E., Bujanda L., et al. Resveratrol attenuates steatosis in obese Zucker rats by decreasing fatty acid availability and reducing oxidative stress. Br J Nutr 2012, 107:202-210.
28. Argilés J.M. The obese Zucker rat: a choice for fat metabolism 1968-1998: twenty years of research on the insights of the Zucker mutation. Prog Lipid Res 1989, 28:53-66.
29. Chakrabarti S.K., Wen Y., Dobrian A.D., Cole B.K., Ma Q., Pei H., et al. Evidence for activation of inflammatory lipoxygenase pathways in visceral adipose tissue of obese Zucker rats. Am J Physiol Endocrinol Metab 2010, 300:E175-E187.
30. Mercader J., Palou A., Bonet M.L. Resveratrol enhances fatty acid oxidation capacity and reduces resistin and Retinol-Binding Protein 4 expression in white adipocytes. J Nutr Biochem 2011, 22:828-834.
31. Wenzel E., Somoza V. Metabolism and bioavailability of trans-resveratrol. Mol Nutr Food Res 2005, 49:472-481.
32. Kapetanovic I.M., Muzzio M., Huang Z., Thompson T.N., McCormick D.L. Pharmacokinetics, oral bioavailability, and metabolic profile of resveratrol and its dimethylether analog, pterostilbene, in rats. Cancer Chemother Pharmacol 2011, 68:593-601.
33. Chuang C.C., Martinez K., Xie G., Kennedy A., Bumrungper A., Overman A., et al. Quercetin is equally or more effective than resveratrol in attenuating tumor necrosis factor-α-mediated inflammation and insulin resistance in primary human adipocytes. Am J Clin Nutr 2010, 92:1512-1521.
34. Kim S., Jin Y., Choi Y., Park T. Resveratrol exerts anti-obesity effects via mechanisms involving down-regulation of adipogenic and inflammatory processes in mice. Biocheml Pharmacol 2011, 81:1343-1351.
35. Olholm J., Paulsen S.K., Cullberg K.B., Richelsen B., Peersen S.B. Anti-inflammatory effect of resveratrol on adipokine expression and secretion in human adipose tissue explants. Int J Obes 2010, 34:1546-1553.
36. Chuang C.C., McIntosh M.K. Potential mechanisms by which polyphenol-rich grapes prevent obesity-mediated inflammation and metabolic diseases. Annu Rev Nutr 2011, 31:155-176.
37. Hogan S., Canning C., Sun S., Sun X., Kadouh H., Zhou K. Dietary supplementation of grape skin extract improves glycemia and inflammation in diet-induced obese mice fed a Western high fat diet. J Agric Food Chem 2011, 59:3035-3041.
38. Terra X., Montagut G., Bustos M., Llopiz N., Ardevol 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.
39. Terra X., Pallarés V., Ardevol A., Bladé C., Fernández-Larrea J., Pujadas G., et al. Modulatory effect of grape-seed procyanidins on local and systemic inflammation in diet-induced obesity rats. J Nutr Biochem 2011, 22:380-387.
40. Jeon B.T., Jeong E.A., Shin H.J., Lee Y., Lee D.H., Kim H.J., et al. Resveratrol attenuates obesity-associated peripheral and central inflammation and improves memory deficit in mice fed a high-fat diet. Diabetes 2012, 61:1444-1454.
41. Reagan-Shaw S., Nihal M., Ahmad N. Dose translation from animal to human studies revisited. FASEB J 2008, 22:659-661.
42. Brown V.A., Patel K.R., Viskaduraki M., Crowell J.A., Perloff M., Booth T.D., et al. Repeat dose study of the cancer chemopreventive agent resveratrol in healthy volunteers: safety, pharmacokinetics and effect on the insulin-like growth factor axis. Cancer Res 2010, 15:9003-9011.
43. Price S.R., Olivecrona T., Pekala P.H. Regulation of lipoprotein lipase synthesis by recombinant tumor necrosis factor-the primary regulatory role of the hormone in 3T3-L1 adipocytes. Arch Biochem Biophys 1986, 251:738-746.
44. Laurencikiene J., van Harmelen V., Arvidsson Nordstrom E., et al. NFkappaB is important for TNF-alpha-induced lipolysis in human adipocytes. J Lipid Res 2007, 48:1069-1077.
45. Hajer G.R., Van HAeften T.W., Visseren F.L.J. Adipose tissue dysfunction in obesity, diabetes, and vascular diseases. Eur Heart J 2008, 29:2959-2971.
46. Nam N.H. Naturally occurring NF-kappaB inhibitors. Mini Rev Med Chem 2006, 6:945-951.
47. Lin Q.Q., Yan C.F., Lin R., Zhang J.Y., Wang W.R., Yang L.N., et al. SIRT1 regulates TNF-α-induced expression of CD40 in 3T3-L1 adipocytes via NF-κB pathway. Cytokine 2012, 60:447-455.
48. Howitz K.T., Bitterman K.J., Cohen H.Y., Lamming D.W., Lavu S., Wood J.G., et al. Small molecule activators of sirtuins extend Saccharomyces cerevisiae lifespan. Nature 2003, 11:191-196.
49. Knutson M.D., Leeuwenburgh C. Resveratrol and novel potent activators of SIRT1: effects on aging and age-related diseases. Nutr Rev 2008, 66:591-596.
50. Alberdi G., Rodríguez V.M., Macarulla M.T., Miranda J., Churruca I., Portillo M.P. Hepatic lipid metabolic pathways modified by resveratrol in rats fed an obesogenic diet. Nutrition 2012, 29:562-567.
51. Fessler M.B., Rudel L.L., Brown J.M. Toll-like receptor signaling risks dietary fatty acids to the metabolic syndrome. Curr Opin Lipidol 2009, 20:379-385.
52. Fortis A., García-Macedo R., Maldonado-Bernal C., Alarcón-Aguilar F., Cruz M. El papel de la inmunidad innata en la obesidad. Salud pública de México 2012, 54:171-177.