Resveratrol Metabolites Modify Adipokine Expression and Secretion in 3T3-L1 Pre-Adipocytes and Mature Adipocytes

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Eseberri, Itziar ^a,b   Lasa, Arrate ^a,b   Churruca, Itziar ^a,b   Portillo, María P ^a,b  

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

^b Instituto de Salud Carlos III   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPOCYTOKINE; ADIPONECTIN; APELIN; INSULIN; LEPTIN; MESSENGER RNA; NICOTINAMIDE PHOSPHORIBOSYLTRANSFERASE; POLYPHENOL DERIVATIVE; RESVERATROL; TRANSRESVERATROL 3 O GLUCURONIDE; TRANSRESVERATROL 4' O GLUCURONIDE; TRANSRESVERATROL 4' O SULFATE; UNCLASSIFIED DRUG;

ADIPOCYTE; ARTICLE; BIOAVAILABILITY; BODY FAT; CELL DIFFERENTIATION; CELL MATURATION; CELL STRAIN; CELL STRAIN 3T3 L1; CELLULAR SECRETION; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION; INSULIN SENSITIVITY; LIPID STORAGE; METABOLITE; PROADIPOCYTE; PROTEIN EXPRESSION; PROTEIN SECRETION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

3T3-L1 CELLS; ADIPOCYTES; ADIPONECTIN; ANIMALS; CELL DIFFERENTIATION; GENE EXPRESSION; GLUCURONIDES; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LEPTIN; MICE; NICOTINAMIDE PHOSPHORIBOSYLTRANSFERASE; RNA, MESSENGER; STILBENES;

EID: 84878061243     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0063918     Document Type: Article

References (54)

1. Frémont L, (2000) Biological effects of resveratrol. Life Sci. 66: 663-673.
2. Baarine M, Thandapilly SJ, Louis XL, Mazué F, Yu L, et al. (2011) Pro-apoptotic versus anti-apoptotic properties of dietary resveratrol on tumoral and normal cardiac cells. Genes Nutr. 6: 161-169.
3. Cucciolla V, Borriello A, Oliva A, Galletti P, Zappia V, et al. (2007) Resveratrol: from basic science to the clinic. Cell Cycle. 6: 2495-2510.
4. Lagouge M, Argmann C, Gerhart-Hines Z, Meziane H, Lerin C, et al. (2006) Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT-1 and PGC-1alpha. Cell. 27: 1109-1122.
5. Ahn J, Cho I, Kim S, Kwon D, Ha T, (2008) Dietary resveratrol alters lipid metabolism-related gene expression of mice on an atherogenic diet. J. Hepatol. 49: 1019-1028.
6. Shang J, Chen L, Xiao F, Sun H, Ding HC, et al. (2008) Resveratrol improves non-alcoholic fatty liver disease nyactivating AMP-activated protein kinase. Acta. Pharmacol. Sin. 29: 698-706.
7. Dal-Pan A, Blanc S, Aujard F, (2010) Resveratrol suppresses body mass gain in a seasonal non-human primate model of obesity. BMC. Physiology. 10: 11.
8. Baile CA, Yang JY, Rayalam S, Hartzell DL, Lai CY, et al. (2011) Effect of resveratrol on fat mobilization. Ann. N Y Acad. Sci. 1215: 40-47.
9. Macarulla M, Alberdi G, Gómez S, Tueros I, Bald C, et al. (2009) Effects of different doses of resveratrol on body fat and serum parameters in rats fed a hypercaloric diet. Physiol Biochem. 65: 369-376.
10. Alberdi G, Rodríguez VM, Miranda J, Macarulla MT, Arias N, et al. (2011) Changes in white adipose tissue metabolism induced by resveratrol in rats. Nutr Metab. 8: 29.
11. Kim S, Jin Y, Choi Y, Park T, (2011) Resveratrol exerts anti-obesity effects via mechanisms involving down-regulation of adipogenic and inflammatory processes in mice. Biochem Pharmacol. 81: 1343-1351.
12. Baur J, Pearson K, Price N, Jamieson H, Lerin C, et al. (2006) Resveratrol improves health and survival of mice on a high-calorie diet. Nature. 444: 337-342.
13. Chen S, Li J, Zhang Z, Li W, Sun Y, et al. (2012) Effects of resveratrol on the amelioration of insulin resistance in KKAy mice. Can. J. Physiol. Pharmacol. 90: 237-242.
14. Bagul PK, Middela H, Matapally S, Padiya R, Bastia T, et al. (2012) Attenuation of insulin resistance, metabolic syndrome and hepatic oxidative stress by resveratrol in fructose-fed rats. Pharmacol Res. 66: 260-268.
15. Brasnyo P, Molnar GA, Mohas M, Markó L, (2011) Resveratrol improves insulin sensitivity, reduces oxidative stress and activates the Akt pathway in type 2 diabetic patients. Br. J Nutr. 106: 383-389.
16. Bhatt JK, Thomas S, Nanjan MJ, (2012) Resveratrol supplementation improves glycemic control in type 2 diabetes mellitus. Nutr Res. 32: 537-541.
17. Ahima RS, Prabakaran D, Mantzoros C, Qu D, Lowell B, et al. (1996) Role of leptin in the neuroendocrine response to fasting. Nature. 382: 250-252.
18. Pelleymounter MA, Cullen MJ, Baker MB, Hecht R, Winters D, et al. (1995) Effects of the obese gene product on body weight regulation in ob/ob mice. Science. 269: 540-543.
19. Cases JA, Gabriely I, Ma XH, Yang XM, Michaeli t, et al. (2001) Physiological increase in plasma leptin markedly inhibits insulin secretion in vivo. Diabetes. 50: 348-352.
20. Sharma AM, Chetty VT, (2005) Obesity, hypertension and insulin resistance. Acta Diabetol. 42: S3-S8.
21. Yoon MJ, Lee GY, Chung JJ, Ahn YH, Hong SH, et al. (2006) Adiponectin increases fatty acid oxidation in skeletal muscle cells by sequential activation of AMP-activated protein kinase, p38 mitogen-activated protein kinase, and peroxisome proliferator-activated receptor alpha. Diabetes. 55: 2562-2570.
22. Szkudelska K, Nogowski L, Szkudelski T, (2009) The inhibitory effect of resveratrol on leptin secretion from rat adipocytes. Eur J Clin Invest. 39: 899-905.
23. Higuchi K, Masaki T, Gotoh K, Chiba S, Katsuragi I, et al. (2007) Apelin, an APJ receptor ligand, regulates body adiposity and favors the messenger ribonucleic acid expression of uncoupling proteins in mice. Endocrinology. 148: 2690-2697.
24. Revollo JR, Körner A, Mills KF, Satoh A, Wang T, et al. (2007) Nampt/PBEF/Visfatin regulates insulin secretion in beta cells as a systemic NAD biosynthetic enzyme. Cell. Metab. 6: 363-75.
25. Boucher J, Masri B, Daviaud D, Gesta S, Guigné C, et al. (2005) Apelin, a newly identified adipokine up-regulated by insulin and obesity. Endocrinology 146: 1764-1771.
26. Carpéné C, Dray C, Attané C, Valet P, Portillo M, et al. (2007) Expanding role for the apelin/APJ system in physiopathology. J Physiol Biochem 63: 359-373.
27. Dray C, Knauf C, Daviaud D, Waget A, Boucher J, et al. (2008) Apelin stimulates glucose utilization in normal and obese insulin-resistant mice. Cell Metab 8: 437-445.
28. Castan-laurell I, Dray C, Knauf C, Kunduzova O, Valet P, (2012) Apelin, a promising target for type 2 diabetes treatment?. Trends Endocrinol Metab. 23: 234-241.
29. Derdemezis CS, Kiortsis DN, Tsimihodimos V, Petraki MP, Veziraki P, et al. (2011) Effect of Plant Polyphenols on Adipokine Secretion from Human SGBS Adipocytes. Biochem. Res. Int. ID 285618, 5 pages.
30. Andres-Lacueva C, Macarulla MT, Rotches-Ribalta M, Boto-Ordóñez M, Urpi-Sarda M, et al. (2012) Distribution of resveratrol metabolites in liver, adipose tissue, and skeletal muscle in rats fed different doses of this polyphenol. J Agric Food Chem. 60: 4833-4840.
31. Bertelli AA, Giovannini L, Stradi R, Bertelli A, Tillement JP, (1996) Plasma, urine and tissue levels of trans- and cis-resveratrol (3,4′,5-trihydroxystilbene) after short-term or prolonged administration of red wine to rats. Int J Tissue React. 18: 67-71.
32. Walle T, Hsieh F, DeLegge MH, Oatis JE, Walle UK, (2004) High absorption but very low availability of oral resveratrol in humans. Drug. Metab. Dispos. 32: 1377-1382.
33. Asensi M, Medina I, Ortega A, Carretero J, Baño MC, et al. (2002) Inhibition of cancer growth by resveratrol is related to its low bioavailability. Free Radic. Biol. Med. 33: 387-398.
34. Andrés-Lacueva C, Urpí-Sardá M, Zamora-Ros R, Lamuela-Raventós RM. (2009) Bioavailability and metabolism of resveratrol. In: Fraga CG, Ed.; John Wiley & Sons. Plant Phenolics and Human Health: Biochemistry, Nutrition and Pharmacology. Hoboken, New Jersey. 265-299.
35. De Santi C, Pietrabissa A, Spisni R, Mosca F, Pacifici GM, (2000) Sulfation of resveratrol, a natural compound present in wine, and its inhibition by natural flavonoids. Xenobiotica. 30: 857-866.
36. Gatz SA, Weissmuller L, (2008) Take a break-resveratrol in action on DNA. Carcinogenesis. 29: 321-332.
37. Hoshino J, Park EJ, Kondratyuk TP, Marler L, Pezzuto JM, (2010) Selective synthesis and biological evaluation of sulfate-conjugated resveratrol metabolites. J. Med Chem. 53: 5033-5043.
38. Delmas D, Aires V, Limagne E, Dutartre P, Mazué F, et al. (2011) Transport, stability and biological activity of resveratrol. Ann. NY Acad. Sci. 1215: 48-59.
39. Calamini B, Ratia K, Malkowski M, Cuendet M, Pezzuto JM, et al. (2010) Pleiotropic mechanisms facilitated by resveratrol and its metabolites. Biochem J. 429: 273-282.
40. Lasa A, Churruca I, Eseberri I, Andrés-Lacueva C, Portillo MP, (2012) Delipidating effect of resveratrol metabolites in 3T3-L1 adipocytes. Mol. Nutr. Food Res. 00: 1-10.
41. Livak K, Schmittgen T, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 25: 402-408.
42. Walle T, (2011) Bioavailability of resveratrol. Ann. NY Acad. Sci. 1215: 9-15.
43. Delmas D, Solary E, Latruffe N, (2011) Resveratrol, a phytochemical inducer of multiple cell death pathways: apoptosis, autophagy and mitotic catastrophe. Curr Med Chem. 18: 1100-1121.
44. Park HJ, Yang JY, Ambati S, Della-Fera MA, Hausman DB, et al. (2008) Combined effects of genistein, quercetin and resveratrol in human and 3T3-L1 adipocytes. J Med Food. 11: 773-783.
45. Yang JY, Della-Fera MA, Rayalam S, Ambati S, Hartzel DL, et al. (2008) Enhanced inibition of apoptosis in 3t3-l1 adipocytes with combinations of resveratrol and quercetin. Life. Sci. 82: 1032-1039.
46. Rayalam S, Yang JY, Ambati S, Della-Fera MA, Baile CA, (2008) Resveratrol inuduces apoptosis and inhibits adipogenesis in 3T3-L1 adipocytes. Phytoter Res. 22: 1367-1371.
47. Wang A, Liu M, Liu X, Dong LQ, (2011) Up-regulation of adiponectin by resveratrol: the essential roles of the Akt/FOXO1 and AMP-activated protein kinase signaling pathways and DsbA-L. J. Biol. Chem. 286: 60-66.
48. Chen G, Gharib TG, Huang CC, Taylor JM, Misek DE,et al. Discordant protein and mRNA expression in lung adenocarcinomas. Mol. Cell. Proteomics. 1: 304-313.
49. Griffin TJ, Gygi SP, Ideker T, Rist B, Eng J, et al. (2002) Complementary profiling of gene expression at the transcriptome and proteome levels in Saccharomyces cerevisiae. Mol. Cell. Proteomics. 1: 323-333.
50. Hegde PS, White IR, Debouck C, (2003) Interplay of transcriptomics and proteomics. Curr. Opin. Biotechnol. 14: 647-651.
51. Lobo SM, Quinto BM, Oyama L, Nakamichi R, Ribeiro AB, (2012) TNF-α modulates statin effects on secretion and expression of MCP-1, PAI-1 and adiponectin in 3T3-L1 differentiated adipocytes. Cytokine. 60: 150-156.
52. Nickel W, Rabouille C, (2009) Mechanisms of regulated unconventional protein secretion. Nat Rev Mol Cell Biol. 10: 148-155.
53. Wang P, Keijer J, Bunschoten A, Bouwman F, (2006) Insulin modulates the secretion of proteins from mature 3T3-L1 adipocytes: a role for transcriptional regulation of processing. Diabetologia. 49: 2453-2462.
54. Mason MM, He Y, Chen H, Quon MJ, et al. (1998) Regulation of Leptin Promoter Function by Sp1, C/EBP, and a Novel Factor. Endocrinology. 139: 1013-1022.