Resveratrol enhances brown adipocyte formation and function by activating AMP-activated protein kinase (AMPK) α1 in mice fed high-fat diet

Molecular Nutrition and Food Research

Volumn 61, Issue 4, 2017, Pages

  Wang, Songbo ^a,b   Liang, Xingwei ^b,c   Yang, Qiyuan ^b   Fu, Xing ^b   Zhu, Meijun ^b   Rodgers, B D ^b   Jiang, Qingyan ^a   Dodson, Michael V ^b   Du, Min ^b  

^a SOUTH CHINA AGRICULTURAL UNIVERSITY   (China)

^b WASHINGTON STATE UNIVERSITY   (United States)

^c GUANGXI UNIVERSITY   (China)

Author keywords

AMP activated protein kinase (AMPK) 1; Brown adipocyte formation and function; Obesity resveratrol; Stromal vascular cells (SVCs); Uncoupling protein 1 (UCP1)

Indexed keywords

HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; ION CHANNEL; MITOCHONDRIAL PROTEIN; RESVERATROL; STILBENE DERIVATIVE; TRANSCRIPTION FACTOR;

ADIPOGENESIS; ANIMAL; BROWN ADIPOCYTE; BROWN ADIPOSE TISSUE; DRUG EFFECTS; GENETICS; LIPID DIET; METABOLISM; MOUSE; OBESITY; THERMOGENESIS;

ADIPOCYTES, BROWN; ADIPOGENESIS; ADIPOSE TISSUE, BROWN; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; DIET, HIGH-FAT; ION CHANNELS; MICE; MITOCHONDRIAL PROTEINS; OBESITY; STILBENES; THERMOGENESIS; TRANSCRIPTION FACTORS;

EID: 85017094113     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.201600746     Document Type: Article

References (53)

1. Seidell, J. C., Halberstadt, J., The global burden of obesity and the challenges of prevention. Ann. Nutr. Metab. 2015, 66(Suppl 2), 7–12.
2. Saito, M., Brown adipose tissue as a regulator of energy expenditure and body fat in humans. Diab. Metab. J. 2013, 37, 22–29.
3. Vosselman, M. J., van Marken Lichtenbelt, W. D., Schrauwen, P., Energy dissipation in brown adipose tissue: from mice to men. Mol. Cell. Endocrinol. 2013, 379, 43–50.
4. Cypess, A. M., Lehman, S., Williams, G., Tal, I. et al., Identification and importance of brown adipose tissue in adult humans. N. Engl. J. Med. 2009, 360, 1509–1517.
5. Virtanen, K. A., Lidell, M. E., Orava, J., Heglind, M. et al., Functional brown adipose tissue in healthy adults. N. Engl. J. Med. 2009, 360, 1518–1525.
6. Kim, S. H., Plutzky, J., Brown fat and browning for the treatment of obesity and related metabolic disorders. Diab. Metab. J. 2016, 40, 12–21.
7. Poher, A. L., Altirriba, J., Veyrat-Durebex, C., Rohner-Jeanrenaud, F., Brown adipose tissue activity as a target for the treatment of obesity/insulin resistance. Front. Physiol. 2015, 6, 4.
8. Poekes, L., Lanthier, N., Leclercq, I. A., Brown adipose tissue: a potential target in the fight against obesity and the metabolic syndrome. Clin. Sci. 2015, 129, 933–949.
9. Harms, M., Seale, P., Brown and beige fat: development, function and therapeutic potential. Nat. Med. 2013, 19, 1252–1263.
10. Wu, J., Jun, H., McDermott, J. R., Formation and activation of thermogenic fat. Trends Genet. 2015, 31, 232–238.
11. Wang, W., Seale, P., Control of brown and beige fat development. Nat Rev Mol Cell Biol 2016, 17, 691–702.
12. Villanueva, C. J., Vergnes, L., Wang, J., Drew, B. G. et al., Adipose subtype-selective recruitment of TLE3 or Prdm16 by PPARγ specifies lipid storage versus thermogenic gene programs. Cell Metab. 2013, 17, 423–435.
13. Seale, P., Kajimura, S., Yang, W., Chin, S. et al., Transcriptional control of brown fat determination by PRDM16. Cell Metab. 2007, 6, 38–54.
14. Seale, P., Transcriptional control of brown adipocyte development and thermogenesis. Int. J. Obes. 2010, 34, S17–S22.
15. Lee, Y. H., Jung, Y. S., Choi, D., Recent advance in brown adipose physiology and its therapeutic potential. Exp. Mol. Med. 2014, 46, e78.
16. Wang, S., Moustaid-Moussa, N., Chen, L., Mo, H. et al., Novel insights of dietary polyphenols and obesity. J. Nutr. Biochem. 2014, 25, 1–18.
17. Merlin, J., Evans, B. A., Dehvari, N., Sato, M. et al., Could burning fat start with a brite spark? Pharmacological and nutritional ways to promote thermogenesis. Mol. Nutr. Food Res. 2016, 60, 18–42.
18. Mohamed, S., Functional foods against metabolic syndrome (obesity, diabetes, hypertension and dyslipidemia) and cardiovasular disease. Trends Food Sci. Technol. 2014, 35, 114–128.
19. Wang, S., Zhu, M.-J., Du, M., Prevention of obesity by dietary resveratrol: how strong is the evidence? Exp. Rev. Endocrinol. Metab. 2015, 10, 561–564.
20. Lagouge, M., Argmann, C., Gerhart-Hines, Z., Meziane, H. et al., Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1alpha. Cell 2006, 127, 1109–1122.
21. Um, J. H., Park, S. J., Kang, H., Yang, S. et al., AMP-activated protein kinase-deficient mice are resistant to the metabolic effects of resveratrol. Diabetes 2010, 59, 554–563.
22. Zhang, C., Luo, J., Yu, B., Chen, J. et al., Effects of resveratrol on lipid metabolism in muscle and adipose tissues: A reevaluation in a pig model. J. Funct. Foods 2015, 14, 590–595.
23. Zhang, C., Luo, J., Yu, B., Zheng, P. et al., Dietary resveratrol supplementation improves meat quality of finishing pigs through changing muscle fiber characteristics and antioxidative status. Meat Sci. 2015, 102, 15–21.
24. Mendez-del Villar, M., Gonzalez-Ortiz, M., Martinez-Abundis, E., Perez-Rubio, K. G. et al., Effect of resveratrol administration on metabolic syndrome, insulin sensitivity, and insulin secretion. Metab. Syndr. Relat. Disord. 2014, 12, 497–501.
25. Konings, E., Timmers, S., Boekschoten, M. V., Goossens, G. H. et al., The effects of 30 days resveratrol supplementation on adipose tissue morphology and gene expression patterns in obese men. Int. J. Obes. (2005) 2014, 38, 470–473.
26. Mitterberger, M. C., Zwerschke, W., Mechanisms of resveratrol-induced inhibition of clonal expansion and terminal adipogenic differentiation in 3T3-L1 preadipocytes. J. Gerontol. A Biol. Sci. Med. Sci. 2013, 68, 1356–1376.
27. Lasa, A., Schweiger, M., Kotzbeck, P., Churruca, I. et al., Resveratrol regulates lipolysis via adipose triglyceride lipase. J. Nutr. Biochem. 2012, 23, 379–384.
28. Gomez-Zorita, S., Treguer, K., Mercader, J., Carpene, C., Resveratrol directly affects in vitro lipolysis and glucose transport in human fat cells. J. Physiol. Biochem. 2013, 69, 585–593.
29. Wang, S., Liang, X., Yang, Q., Fu, X. et al., Resveratrol induces brown-like adipocyte formation in white fat through activation of AMP-activated protein kinase (AMPK) alpha1. Int. J. Obes. (Lond.) 2015, 39, 967–976.
30. Alberdi, G., Rodriguez, V. M., Miranda, J., Macarulla, M. T. et al., Thermogenesis is involved in the body-fat lowering effects of resveratrol in rats. Food Chem. 2013, 141, 1530–1535.
31. Andrade, J. M., Frade, A. C., Guimaraes, J. B., Freitas, K. M. et al., 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. Eur. J. Nutr. 2014, 53, 1503–1510.
32. Lam, Y. Y., Peterson, C. M., Ravussin, E., Resveratrol vs. calorie restriction: data from rodents to humans. Exp. Gerontol. 2013, 48, 1018–1024.
33. Hardie, D. G., AMPK: positive and negative regulation, and its role in whole-body energy homeostasis. Curr. Opin. Cell Biol. 2015, 33, 1–7.
34. Bijland, S., Mancini, S. J., Salt, I. P., Role of AMP-activated protein kinase in adipose tissue metabolism and inflammation. Clin. Sci. (Lond) 2013, 124, 491–507.
35. Daval, M., Foufelle, F., Ferré, P., Functions of AMP-activated protein kinase in adipose tissue. J. Physiol. 2006, 574, 55–62.
36. Daval, M., Diot-Dupuy, F., Bazin, R., Hainault, I. et al., Anti-lipolytic action of AMP-activated protein kinase in rodent adipocytes. J. Biol. Chem. 2005, 280, 25250–25257.
37. Lihn, A. S., Jessen, N., Pedersen, S. B., Lund, S. et al., AICAR stimulates adiponectin and inhibits cytokines in adipose tissue. Biochem. Biophys. Res. Commun. 2004, 316, 853–858.
38. Gaidhu, M. P., Ceddia, R. B., The role of adenosine monophosphate kinase in remodeling white adipose tissue metabolism. Exerc. Sport. Sci. Rev. 2011, 39, 102–108.
39. Aune, U. L., Ruiz, L., Kajimura, S., Isolation and differentiation of stromal vascular cells to beige/brite cells. J. Visualized Exp. 2013, (73), e50191.
40. Yang, Q., Liang, X., Sun, X., Zhang, L. et al., AMPK/alpha-ketoglutarate axis dynamically mediates DNA demethylation in the Prdm16 promoter and brown adipogenesis. Cell Metab. 2016, 24, 1–13.
41. Wang, S., Zhou, G., Shu, G., Wang, L. et al., Glucose utilization, lipid metabolism and BMP-Smad signaling pathway of porcine intramuscular preadipocytes compared with subcutaneous preadipocytes. Cell. Physiol. Biochem. 2013, 31, 981–996.
42. Liang, X., Yang, Q., Fu, X., Rogers, C. J. et al., Maternal obesity epigenetically alters visceral fat progenitor cell properties in male offspring mice. J. Physiol. 2016, 594, 4453–4466.
43. Kissig, M., Shapira, S. N., Seale, P., SnapShot: brown and beige adipose thermogenesis. Cell 2016, 166, 258–258.e251.
44. Qian, S., Huang, H., Tang, Q., Brown and beige fat: the metabolic function, induction, and therapeutic potential. Front. Med. 2015, 9, 162–172.
45. Seale, P., Bjork, B., Yang, W., Kajimura, S. et al., PRDM16 controls a brown fat/skeletal muscle switch. Nature 2008, 454, 961–967.
46. Peirce, V., Carobbio, S., Vidal-Puig, A., The different shades of fat. Nature 2014, 510, 76–83.
47. Harms, M., Seale, P., Brown and beige fat: development, function and therapeutic potential. Nat. Med. 2013, 19, 1252–1263.
48. Higashida, K., Kim, S. H., Jung, S. R., Asaka, M. et al., Effects of resveratrol and SIRT1 on PGC-1alpha activity and mitochondrial biogenesis: a reevaluation. PLoS Biol. 2013, 11, e1001603.
49. 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. Biochem. Pharmacol. 2011, 81, 1343–1351.
50. Timmers, S., Konings, E., Bilet, L., Houtkooper, R. 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.
51. 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.
52. Rayalam, S., Yang, J. Y., Ambati, S., Della-Fera, M. A. et al., Resveratrol induces apoptosis and inhibits adipogenesis in 3T3-L1 adipocytes. Phytother. Res. 2008, 22, 1367–1371.
53. Price, N. L., Gomes, A. P., Ling, A. J., Duarte, F. V. et al., SIRT1 is required for AMPK activation and the beneficial effects of resveratrol on mitochondrial function. Cell Metab. 2012, 15, 675–690.