Resveratrol increases brown adipose tissue thermogenesis markers by increasing SIRT1 and energy expenditure and decreasing fat accumulation in adipose tissue of mice fed a standard diet

European Journal of Nutrition

Volumn 53, Issue 7, 2014, Pages 1503-1510

  Andrade, João Marcus Oliveira ^b   Frade, Alessandra Caroline Montes ^a   Guimarães, Juliana Bohnen ^a   Freitas, Kátia Michelle ^a   Lopes, Miriam Teresa Paz ^a   Guimarães, André Luiz Sena ^b   de Paula, Alfredo Maurício Batista ^b   Coimbra, Cândido Celso ^a   Santos, Sérgio Henrique Sousa ^a,b  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^b STATE UNIVERSITY OF MONTES CLAROS   (Brazil)

Author keywords

Adipose tissue; PTEN; SIRT1; Thermogenesis; UCP1

Indexed keywords

ADIPONECTIN; CHOLESTEROL; GLUCOSE; HIGH DENSITY LIPOPROTEIN; OSTEOGENIC PROTEIN 1; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; RESVERATROL; SIRTUIN 1; TRIACYLGLYCEROL; UNCOUPLING PROTEIN 1; UNCOUPLING PROTEIN 3; BMP7 PROTEIN, MOUSE; ION CHANNEL; MITOCHONDRIAL PROTEIN; MITOCHONDRIAL UNCOUPLING PROTEIN; PTEN PROTEIN, MOUSE; SIRT1 PROTEIN, MOUSE; STILBENE DERIVATIVE;

ANIMAL EXPERIMENT; ARTICLE; BROWN ADIPOSE TISSUE; BROWN ADIPOSE TISSUE THERMOGENESIS; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; DIET; ENERGY BALANCE; ENERGY EXPENDITURE; FOOD INTAKE; GENE EXPRESSION; GLUCOSE BLOOD LEVEL; LIPID STORAGE; LOCOMOTION; MALE; MOUSE; MUSCLE MASS; NONHUMAN; OXYGEN CONSUMPTION; SKELETAL MUSCLE; THERMOGENESIS; ANIMAL; DRUG EFFECTS; ENERGY METABOLISM; GENETICS; METABOLISM; WHITE ADIPOSE TISSUE;

MAMMALIA; MUS; RICE STRIPE VIRUS;

ADIPOSE TISSUE, BROWN; ADIPOSE TISSUE, WHITE; ANIMALS; BONE MORPHOGENETIC PROTEIN 7; DIET; ENERGY METABOLISM; ION CHANNELS; MALE; MICE; MITOCHONDRIAL PROTEINS; PTEN PHOSPHOHYDROLASE; SIRTUIN 1; STILBENES; THERMOGENESIS;

EID: 84914678932     PISSN: 14366207     EISSN: 14366215     Source Type: Journal    
DOI: 10.1007/s00394-014-0655-6     Document Type: Article

References (42)

1. Gesta S, Tseng YH, Kahn CR (2007) Developmental origin of fat: tracking obesity to its source. Cell 131(2):242–256. doi:10.1016/j.cell.2007.10.004
2. Del Gonzalez-BarrosoM M, Ricquier D, Cassard-Doulcier AM (2000) The human uncoupling protein-1 gene (UCP1): present status and perspectives in obesity research. Obes Rev 1(2):61–72
3. Alberdi G, Rodriguez VM, Miranda J, Macarulla MT, Churruca I, Portillo MP (2013) Thermogenesis is involved in the body-fat lowering effects of resveratrol in rats. Food Chem 141(2):1530–1535. doi:10.1016/j.foodchem.2013.03.085
4. Baur JA, Pearson KJ, Price NL, Jamieson HA, Lerin C, Kalra A, Prabhu VV, Allard JS, Lopez-Lluch G, Lewis K, Pistell PJ, Poosala S, Becker KG, Boss O, Gwinn D, Wang M, Ramaswamy S, Fishbein KW, Spencer RG, Lakatta EG, Le Couteur D, Shaw RJ, Navas P, Puigserver P, Ingram DK, de Cabo R, Sinclair DA (2006) Resveratrol improves health and survival of mice on a high-calorie diet. Nature 444(7117):337–342. doi:10.1038/nature05354
5. Baur JA, Sinclair DA (2006) Therapeutic potential of resveratrol: the in vivo evidence. Nat Rev Drug Discov 5(6):493–506. doi:10.1038/nrd2060
6. Carafa V, Nebbioso A, Altucci L (2012) Sirtuins and disease: the road ahead. Front Pharmacol 3:4. doi:10.3389/fphar.2012.00004
7. Lavu S, Boss O, Elliott PJ, Lambert PD (2008) Sirtuins–novel therapeutic targets to treat age-associated diseases. Nat Rev Drug Discov 7(10):841–853. doi:10.1038/nrd2665
8. Alberdi G, Rodriguez VM, Miranda J, Macarulla MT, Arias N, Andres-Lacueva C, Portillo MP (2011) Changes in white adipose tissue metabolism induced by resveratrol in rats. Nutr Metab (Lond) 8(1):29. doi:10.1186/1743-7075-8-29
9. 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(11):1343–1351. doi:10.1016/j.bcp.2011.03.012
10. Qiang L, Wang L, Kon N, Zhao W, Lee S, Zhang Y, Rosenbaum M, Zhao Y, Gu W, Farmer SR, Accili D (2012) Brown remodeling of white adipose tissue by SirT1-dependent deacetylation of Ppargamma. Cell 150(3):620–632. doi:10.1016/j.cell.2012.06.027
11. Canto C, Gerhart-Hines Z, Feige JN, Lagouge M, Noriega L, Milne JC, Elliott PJ, Puigserver P, Auwerx J (2009) AMPK regulates energy expenditure by modulating NAD+ metabolism and SIRT1 activity. Nature 458(7241):1056–1060. doi:10.1038/nature07813
12. Milne JC, Lambert PD, Schenk S, Carney DP, Smith JJ, Gagne DJ, Jin L, Boss O, Perni RB, Vu CB, Bemis JE, Xie R, Disch JS, Ng PY, Nunes JJ, Lynch AV, Yang H, Galonek H, Israelian K, Choy W, Iffland A, Lavu S, Medvedik O, Sinclair DA, Olefsky JM, Jirousek MR, Elliott PJ, Westphal CH (2007) Small molecule activators of SIRT1 as therapeutics for the treatment of type 2 diabetes. Nature 450(7170):712–716. doi:10.1038/nature06261
13. Lagouge M, Argmann C, Gerhart-Hines Z, Meziane H, Lerin C, Daussin F, Messadeq N, Milne J, Lambert P, Elliott P, Geny B, Laakso M, Puigserver P, Auwerx J (2006) Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1alpha. Cell 127(6):1109–1122. doi:10.1016/j.cell.2006.11.013
14. de Pinho L, Andrade JM, Paraiso A, Filho AB, Feltenberger JD, Guimaraes AL, de Paula AM, Caldeira AP, Botelho AC, Campagnole-Santos MJ, Santos SH (2013) Diet composition modulate expression of sirtuins and renin-angiotensin system components in adipose tissue. Obesity. doi:10.1002/oby.20305
15. Feltenberger JD, Andrade JM, Paraiso A, Barros LO, Filho AB, Sinisterra RD, Sousa FB, Guimaraes AL, de Paula AM, Campagnole-Santos MJ, Qureshi M, Dos Santos RA, Santos SH (2013) Oral formulation of angiotensin-(1–7) improves lipid metabolism and prevents high-fat diet-induced hepatic steatosis and inflammation in mice. Hypertension. doi:10.1161/HYPERTENSIONAHA.111.00919
16. Leite LH, Lacerda AC, Balthazar CH, Marubayashi U, Coimbra CC (2007) Central AT(1) receptor blockade increases metabolic cost during exercise reducing mechanical efficiency and running performance in rats. Neuropeptides 41(3):189–194. doi:10.1016/j.npep.2007.01.002
17. Guimaraes JB, Wanner SP, Machado SC, Lima MR, Cordeiro LM, Pires W, La Guardia RB, Silami-Garcia E, Rodrigues LO, Lima NR (2013) Fatigue is mediated by cholinoceptors within the ventromedial hypothalamus independent of changes in core temperature. Scand J Med Sci Sports 23(1):46–56. doi:10.1111/j.1600-0838.2011.01350.x
18. de Queiroz KB, Rodovalho GV, Guimaraes JB, de Lima DC, Coimbra CC, Evangelista EA, Guerra-Sa R (2012) Endurance training blocks uncoupling protein 1 up-regulation in brown adipose tissue while increasing uncoupling protein 3 in the muscle tissue of rats fed with a high-sugar diet. Nutr Res 32(9):709–717. doi:10.1016/j.nutres.2012.06.020
19. Saely CH, Geiger K, Drexel H (2012) Brown versus white adipose tissue: a mini-review. Gerontology 58(1):15–23. doi:10.1159/000321319
20. Bjorndal B, Burri L, Staalesen V, Skorve J, Berge RK (2011) Different adipose depots: their role in the development of metabolic syndrome and mitochondrial response to hypolipidemic agents. J Obes 2011:490650. doi:10.1155/2011/490650
21. Caesar R, Manieri M, Kelder T, Boekschoten M, Evelo C, Muller M, Kooistra T, Cinti S, Kleemann R, Drevon CA (2010) A combined transcriptomics and lipidomics analysis of subcutaneous, epididymal and mesenteric adipose tissue reveals marked functional differences. PLoS ONE 5(7):e11525. doi:10.1371/journal.pone.0011525
22. DiGirolamo M, Fine JB, Tagra K, Rossmanith R (1998) Qualitative regional differences in adipose tissue growth and cellularity in male Wistar rats fed ad libitum. Am J Physiol 274(5 Pt 2):R1460–R1467
23. Norheim F, Langleite TM, Hjorth M, Holen T, Kielland A, Stadheim HK, Gulseth HL, Birkeland KI, Jensen J, Drevon CA (2013) The effects of acute and chronic exercise on PGC-1alpha, irisin and browning of subcutaneous adipose tissue in humans. FEBS J. doi:10.1111/febs.12619
24. Bartelt A, Heeren J (2014) Adipose tissue browning and metabolic health. Nat Rev Endocrinol 10(1):24–36. doi:10.1038/nrendo.2013.204
25. Giralt M, Villarroya F (2013) White, brown, beige/brite: different adipose cells for different functions? Endocrinology 154(9):2992–3000. doi:10.1210/en.2013-1403
26. Liu X, Rossmeisl M, McClaine J, Riachi M, Harper ME, Kozak LP (2003) Paradoxical resistance to diet-induced obesity in UCP1-deficient mice. J Clin Investig 111(3):399–407. doi:10.1172/JCI15737
27. Hamann A, Flier JS, Lowell BB (1996) Decreased brown fat markedly enhances susceptibility to diet-induced obesity, diabetes, and hyperlipidemia. Endocrinology 137(1):21–29
28. Okamatsu-Ogura Y, Nio-Kobayashi J, Iwanaga T, Terao A, Kimura K, Saito M (2011) Possible involvement of uncoupling protein 1 in appetite control by leptin. Exp Biol Med 236(11):1274–1281. doi:10.1258/ebm.2011.011143
29. Oh HH, Kim KS, Choi SM, Yang HS, Yoon Y (2004) The effects of uncoupling protein-1 genotype on lipoprotein cholesterol level in Korean obese subjects. Metab Clin Exp 53(8):1054–1059
30. Sale MM, Hsu FC, Palmer ND, Gordon CJ, Keene KL, Borgerink HM, Sharma AJ, Bergman RN, Taylor KD, Saad MF, Norris JM (2007) The uncoupling protein 1 gene, UCP1, is expressed in mammalian islet cells and associated with acute insulin response to glucose in African American families from the IRAS Family Study. BMC Endocr Disord 7:1. doi:10.1186/1472-6823-7-1
31. Proenza AM, Poissonnet CM, Ozata M, Ozen S, Guran S, Palou A, Strosberg AD (2000) Association of sets of alleles of genes encoding beta3-adrenoreceptor, uncoupling protein 1 and lipoprotein lipase with increased risk of metabolic complications in obesity. Int J Obes Relat Metab Disord J Int Assoc Study Obes 24(1):93–100
32. Shin HD, Kim KS, Cha MH, Yoon Y (2005) The effects of UCP-1 polymorphisms on obesity phenotypes among Korean female subjects. Biochem Biophys Res Commun 335(2):624–630. doi:10.1016/j.bbrc.2005.07.096
33. Jia JJ, Tian YB, Cao ZH, Tao LL, Zhang X, Gao SZ, Ge CR, Lin QY, Jois M (2010) The polymorphisms of UCP1 genes associated with fat metabolism, obesity and diabetes. Mol Biol Rep 37(3):1513–1522. doi:10.1007/s11033-009-9550-2
34. Kozak LP, Harper ME (2000) Mitochondrial uncoupling proteins in energy expenditure. Annu Rev Nutr 20:339–363. doi:10.1146/annurev.nutr.20.1.339
35. Lanouette CM, Giacobino JP, Perusse L, Lacaille M, Yvon C, Chagnon M, Kuhne F, Bouchard C, Muzzin P, Chagnon YC (2001) Association between uncoupling protein 3 gene and obesity-related phenotypes in the Quebec Family Study. Mol Med 7(7):433–441
36. Wu Z, Puigserver P, Andersson U, Zhang C, Adelmant G, Mootha V, Troy A, Cinti S, Lowell B, Scarpulla RC, Spiegelman BM (1999) Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98(1):115–124. doi:10.1016/S0092-8674(00)80611-X
37. Rodgers JT, Lerin C, Haas W, Gygi SP, Spiegelman BM, Puigserver P (2005) Nutrient control of glucose homeostasis through a complex of PGC-1alpha and SIRT1. Nature 434(7029):113–118. doi:10.1038/nature03354
38. Ortega-Molina A, Efeyan A, Lopez-Guadamillas E, Munoz-Martin M, Gomez-Lopez G, Canamero M, Mulero F, Pastor J, Martinez S, Romanos E, Mar Gonzalez-Barroso M, Rial E, Valverde AM, Bischoff JR, Serrano M (2012) Pten positively regulates brown adipose function, energy expenditure, and longevity. Cell Metab 15(3):382–394. doi:10.1016/j.cmet.2012.02.001
39. Tseng YH, Kokkotou E, Schulz TJ, Huang TL, Winnay JN, Taniguchi CM, Tran TT, Suzuki R, Espinoza DO, Yamamoto Y, Ahrens MJ, Dudley AT, Norris AW, Kulkarni RN, Kahn CR (2008) New role of bone morphogenetic protein 7 in brown adipogenesis and energy expenditure. Nature 454(7207):1000–1004. doi:10.1038/nature07221
40. Seale P, Kajimura S, Yang W, Chin S, Rohas LM, Uldry M, Tavernier G, Langin D, Spiegelman BM (2007) Transcriptional control of brown fat determination by PRDM16. Cell Metab 6(1):38–54. doi:10.1016/j.cmet.2007.06.001
41. Puigserver P, Wu Z, Park CW, Graves R, Wright M, Spiegelman BM (1998) A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 92(6):829–839
42. Schulz TJ, Huang P, Huang TL, Xue R, McDougall LE, Townsend KL, Cypess AM, Mishina Y, Gussoni E, Tseng YH (2013) Brown-fat paucity due to impaired BMP signalling induces compensatory browning of white fat. Nature 495(7441):379–383. doi:10.1038/nature11943