Resveratrol and SRT1720 elicit differential effects in metabolic organs and modulate systemic parameters independently of skeletal muscle peroxisome proliferator-activated receptor γ co-activator 1α (PGC-1α)

Journal of Biological Chemistry

Volumn 290, Issue 26, 2015, Pages 16059-16076

  Svensson, Kristoffer ^a   Schnyder, Svenia ^a   Albert, Verena ^a   Cardel, Bettina ^a   Quagliata, Luca ^b   Terracciano, Luigi M ^b   Handschin, Christoph ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

^b UNIVERSITY HOSPITAL BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOLOGY; GENES; MUSCLE; NUTRITION; RESVERATROL; TISSUE;

CALORIC RESTRICTION; DIFFERENTIAL EFFECT; ENERGY EXPENDITURE; GLUCOSE HOMEOSTASIS; MITOCHONDRIAL BIOGENESIS; MITOCHONDRIAL GENES; PEROXISOME PROLIFERATOR-ACTIVATED RECEPTOR; THERAPEUTIC INTERVENTION;

METABOLISM;

N [2 [3 (1 PIPERAZINYLMETHYL)IMIDAZO[2,1 B]THIAZOL 6 YL]PHENYL] 2 QUINOXALINECARBOXAMIDE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; RESVERATROL; FUSED HETEROCYCLIC RINGS; GLUCOSE; PPARGC1A PROTEIN, MOUSE; STILBENE DERIVATIVE; TRANSCRIPTION FACTOR;

ADIPOSE TISSUE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOGENESIS; CALORIC RESTRICTION; CONTROLLED STUDY; ENERGY EXPENDITURE; ENZYME ACTIVATION; GLUCOSE HOMEOSTASIS; IN VIVO STUDY; LIPID METABOLISM; LIVER; MALE; MITOCHONDRIAL GENE; MITOCHONDRION; MOUSE; NONHUMAN; OBESITY; PRIORITY JOURNAL; SKELETAL MUSCLE; TRANSCRIPTION REGULATION; ANIMAL; DRUG EFFECTS; ENERGY METABOLISM; FEMALE; GENETICS; KNOCKOUT MOUSE; METABOLISM;

ADIPOSE TISSUE; ANIMALS; ENERGY METABOLISM; FEMALE; GLUCOSE; HETEROCYCLIC COMPOUNDS WITH 4 OR MORE RINGS; LIPID METABOLISM; LIVER; MALE; MICE; MICE, KNOCKOUT; MUSCLE, SKELETAL; STILBENES; TRANSCRIPTION FACTORS;

EID: 84941299736     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.590653     Document Type: Article

References (48)

1. Speakman, J. R., and Mitchell, S. E. (2011) Caloric restriction. Mol. Aspects Med. 32, 159-221
2. Pearson, K. J., Baur, J. A., Lewis, K. N., Peshkin, L., Price, N. L., Labinskyy, N., Swindell, W. R., Kamara, D., Minor, R. K., Perez, E., Jamieson, H. A., Zhang, Y., Dunn, S. R., Sharma, K., Pleshko, N., Woollett, L. A., Csiszar, A., Ikeno, Y., Le Couteur, D., Elliott, P. J., Becker, K. G., Navas, P., Ingram, D. K., Wolf, N. S., Ungvari, Z., Sinclair, D. A., and De Cabo, R. (2008) Resveratrol delays age-related deterioration and mimics transcriptional aspects of dietary restriction without extending life span. Cell Metab. 8, 157-168
3. Smith, J. J., Kenney, R. D., Gagne, D. J., Frushour, B. P., Ladd, W., Galonek, H. L., Israelian, K., Song, J., Razvadauskaite, G., Lynch, A. V., Carney, D. P., Johnson, R. J., Lavu, S., Iffland, A., Elliott, P. J., Lambert, P. D., Elliston, K. O., Jirousek, M. R., Milne, J. C., and Boss, O. (2009) Small molecule activators of SIRT1 replicate signaling pathways triggered by calorie restriction in vivo. BMC Syst. Biol. 3, 31
4. Baur, J. A., Pearson, K. J., Price, N. L., Jamieson, H. A., Lerin, C., Kalra, A., Prabhu, V. V., Allard, J. S., Lopez-Lluch, G., Lewis, K., Pistell, P. J., Poosala, S., Becker, K. G., Boss, O., Gwinn, D., Wang, M., Ramaswamy, S., Fishbein, K. W., Spencer, R. G., Lakatta, E. G., Le Couteur, D., Shaw, R. J., Navas, P., Puigserver, P., Ingram, D. K., De Cabo, R., and Sinclair, D. A. (2006) Resveratrol improves health and survival of mice on a high-calorie diet. Nature 444, 337-342
5. 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., and Auwerx, J. (2006) Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1α. Cell 127, 1109-1122
6. Um, J. H., Park, S. J., Kang, H., Yang, S., Foretz, M., McBurney, M. W., Kim, M. K., Viollet, B., and Chung, J. H. (2010) AMP-activated protein kinasedeficient mice are resistant to the metabolic effects of resveratrol. Diabetes 59, 554-563
7. Price, N. L., Gomes, A. P., Ling, A. J., Duarte, F. V., Martin-Montalvo, A., North, B. J., Agarwal, B., Ye, L., Ramadori, G., Teodoro, J. S., Hubbard, B. P., Varela, A. T., Davis, J. G., Varamini, B., Hafner, A., Moaddel, R., Rolo, A. P., Coppari, R., Palmeira, C. M., De Cabo, R., Baur, J. A., and Sinclair, D. A. (2012) SIRT1 is required for AMPK activation and the beneficial effects of resveratrol on mitochondrial function. Cell Metab. 15, 675-690
8. Park, S. J., Ahmad, F., Philp, A., Baar, K., Williams, T., Luo, H., Ke, H., Rehmann, H., Taussig, R., Brown, A. L., Kim, M. K., Beaven, M. A., Burgin, A. B., Manganiello, V., and Chung, J. H. (2012) Resveratrol ameliorates aging-related metabolic phenotypes by inhibiting cAMP phosphodiesterases. Cell 148, 421-433
9. Baur, J. A. (2010) Biochemical effects of SIRT1 activators. Biochim. Biophys. Acta 1804, 1626-1634
10. Milne, J. C., Lambert, P. D., Schenk, S., Carney, D. P., Smith, J. J., Gagne, D. J., Jin, L., Boss, O., Perni, R. B., Vu, C. B., Bemis, J. E., Xie, R., Disch, J. S., Ng, P. Y., Nunes, J. J., Lynch, A. V., Yang, H., Galonek, H., Israelian, K., Choy, W., Iffland, A., Lavu, S., Medvedik, O., Sinclair, D. A., Olefsky, J. M., Jirousek, M. R., Elliott, P. J., and Westphal, C. H. (2007) Small molecule activators of SIRT1 as therapeutics for the treatment of type 2 diabetes. Nature 450, 712-716
11. Feige, J. N., Lagouge, M., Canto, C., Strehle, A., Houten, S. M., Milne, J. C., Lambert, P. D., Mataki, C., Elliott, P. J., and Auwerx, J. (2008) Specific SIRT1 activation mimics low energy levels and protects against diet-induced metabolic disorders by enhancing fat oxidation. Cell Metab. 8, 347-358
12. Minor, R. K., Baur, J. A., Gomes, A. P., Ward, T. M., Csiszar, A., Mercken, E. M., Abdelmohsen, K., Shin, Y. K., Canto, C., Scheibye-Knudsen, M., Krawczyk, M., Irusta, P. M., Martín-Montalvo, A., Hubbard, B. P., Zhang, Y., Lehrmann, E., White, A. A., Price, N. L., Swindell, W. R., Pearson, K. J., Becker, K. G., Bohr, V. A., Gorospe, M., Egan, J. M., Talan, M. I., Auwerx, J., Westphal, C. H., Ellis, J. L., Ungvari, Z., Vlasuk, G. P., Elliott, P. J., Sinclair, D. A., and De Cabo, R. (2011) SRT1720 improves survival and healthspan of obese mice. Sci. Rep. 1, 70
13. Pacholec, M., Bleasdale, J. E., Chrunyk, B., Cunningham, D., Flynn, D., Garofalo, R. S., Griffith, D., Griffor, M., Loulakis, P., Pabst, B., Qiu, X., Stockman, B., Thanabal, V., Varghese, A., Ward, J., Withka, J., and Ahn, K. (2010) SRT1720, SRT2183, SRT1460, and resveratrol are not direct activators of SIRT1. J. Biol. Chem. 285, 8340-8351
14. Martin-Montalvo, A., and De Cabo, R. (2013) Mitochondrial metabolic reprogramming induced by calorie restriction. Antioxid. Redox Signal. 19, 310-320
15. Herzig, S., Long, F., Jhala, U. S., Hedrick, S., Quinn, R., Bauer, A., Rudolph, D., Schutz, G., Yoon, C., Puigserver, P., Spiegelman, B., and Montminy, M. (2001) CREB regulates hepatic gluconeogenesis through the coactivator PGC-1. Nature 413, 179-183
16. Jäger, S., Handschin, C., St-Pierre, J., and Spiegelman, B. M. (2007) AMPactivated protein kinase (AMPK) action in skeletal muscle via direct phosphorylation of PGC-1α. Proc. Natl. Acad. Sci. U. S. A. 104, 12017-12022
17. Rodgers, J. T., Lerin, C., Haas, W., Gygi, S. P., Spiegelman, B. M., and Puigserver, P. (2005) Nutrient control of glucose homeostasis through a complex of PGC-1α and SIRT1. Nature 434, 113-118
18. Handschin, C. (2009) The biology of PGC-1α and its therapeutic potential. Trends Pharmacol. Sci. 30, 322-329
19. Pérez-Schindler, J., Summermatter, S., Santos, G., Zorzato, F., and Handschin, C. (2013) The transcriptional coactivator PGC-1α is dispensable for chronic overload-induced skeletal muscle hypertrophy and metabolic remodeling. Proc. Natl. Acad. Sci. U. S. A. 110, 20314-20319
20. Handschin, C., Choi, C. S., Chin, S., Kim, S., Kawamori, D., Kurpad, A. J., Neubauer, N., Hu, J., Mootha, V. K., Kim, Y. B., Kulkarni, R. N., Shulman, G. I., and Spiegelman, B. M. (2007) Abnormal glucose homeostasis in skeletal muscle-specific PGC-1α knockout mice reveals skeletal musclepancreatic beta cell cross-talk. J. Clin. Invest. 117, 3463-3474
21. Townsend, K. L., and Tseng, Y. H. (2014) Brown fat fuel utilization and thermogenesis. Trends Endocrinol. Metab. 25, 168-177
22. Jang, M. K., Son, Y., and Jung, M. H. (2013) ATF3 plays a role in adipocyte hypoxia-mediated mitochondria dysfunction in obesity. Biochem. Biophys. Res. Commun. 431, 421-427
23. Kim, H. B., Kong, M., Kim, T. M., Suh, Y. H., Kim, W. H., Lim, J. H., Song, J. H., and Jung, M. H. (2006) NFATc4 and ATF3 negatively regulate adiponectin gene expression in 3T3-L1 adipocytes. Diabetes 55, 1342-1352
24. Qi, L., Saberi, M., Zmuda, E., Wang, Y., Altarejos, J., Zhang, X., Dentin, R., Hedrick, S., Bandyopadhyay, G., Hai, T., Olefsky, J., and Montminy, M. (2009) Adipocyte CREB promotes insulin resistance in obesity. Cell Metab. 9, 277-286
25. Tilg, H., and Wolf, A. M. (2005) Adiponectin: a key fat-derived molecule regulating inflammation. Expert Opin. Ther. Targets 9, 245-251
26. Horton, J. D., Goldstein, J. L., and Brown, M. S. (2002) SREBPs: activators of the complete program of cholesterol and fatty acid synthesis in the liver. J. Clin. Invest. 109, 1125-1131
27. Ingram, D. K., Zhu, M., Mamczarz, J., Zou, S., Lane, M. A., Roth, G. S., and De Cabo, R. (2006) Calorie restriction mimetics: an emerging research field. Aging Cell 5, 97-108
28. Finley, L. W., Lee, J., Souza, A., Desquiret-Dumas, V., Bullock, K., Rowe, G. C., Procaccio, V., Clish, C. B., Arany, Z., and Haigis, M. C. (2012) Skeletal muscle transcriptional coactivator PGC-1α mediates mitochondrial, but not metabolic, changes during calorie restriction. Proc. Natl. Acad. Sci. U. S. A. 109, 2931-2936
29. Kelly, T. J., Lerin, C., Haas, W., Gygi, S. P., and Puigserver, P. (2009) GCN5-mediated transcriptional control of the metabolic coactivator PGC-1α through lysine acetylation. J. Biol. Chem. 284, 19945-19952
30. Gómez-Zorita, S., Fernández-Quintela, A., Macarulla, M. T., Aguirre, L., Hijona, E., Bujanda, L., Milagro, F., Martínez, J. A., and Portillo, M. P. (2012) Resveratrol attenuates steatosis in obese Zucker rats by decreasing fatty acid availability and reducing oxidative stress. Br. J. Nutr. 107, 202-210
31. Jin, S. H., Yang, J. H., Shin, B. Y., Seo, K., Shin, S. M., Cho, I. J., and Ki, S. H. (2013) Resveratrol inhibits LXRα-dependent hepatic lipogenesis through novel antioxidant Sestrin2 gene induction. Toxicol. Appl. Pharmacol. 271, 95-105
32. Yamazaki, Y., Usui, I., Kanatani, Y., Matsuya, Y., Tsuneyama, K., Fujisaka, S., Bukhari, A., Suzuki, H., Senda, S., Imanishi, S., Hirata, K., Ishiki, M., Hayashi, R., Urakaze, M., Nemoto, H., Kobayashi, M., and Tobe, K. (2009) Treatment with SRT1720, a SIRT1 activator, ameliorates fatty liver with reduced expression of lipogenic enzymes in MSG mice. Am. J. Physiol. Endocrinol. Metab. 297, E1179-E1186
33. Qiang, L., Lin, H. V., Kim-Muller, J. Y., Welch, C. L., Gu, W., and Accili, D. (2011) Proatherogenic abnormalities of lipid metabolism in SirT1 transgenic mice are mediated through Creb deacetylation. Cell Metab. 14, 758-767
34. Bhatt, J. K., Thomas, S., and Nanjan, M. J. (2012) Resveratrol supplementation improves glycemic control in type 2 diabetes mellitus. Nutr. Res. 32, 537-541
35. Timmers, S., Konings, E., Bilet, L., Houtkooper, R. H., Van De Weijer, T., Goossens, G. H., Hoeks, J., Van Der Krieken, S., Ryu, D., Kersten, S., Moonen-Kornips, E., Hesselink, M. K., Kunz, I., Schrauwen-Hinderling, V. B., Blaak, E. E., Auwerx, J., and Schrauwen, P. (2011) Calorie restrictionlike effects of 30 days of resveratrol supplementation on energy metabolism and metabolic profile in obese humans. Cell Metab. 14, 612-622
36. Tomé-Carneiro, J., Gonzálvez, M., Larrosa, M., Garcia-Almagro, F. J., Avilés-Plaza, F., Parra, S., Yáñez-Gascón, M. J., Ruiz-Ros, J. A., García-Conesa, M. T., Tomás-Barberán, F. A., and Espín, J. C. (2012) Consumption of a grape extract supplement containing resveratrol decreases oxidized LDL and ApoB in patients undergoing primary prevention of cardiovascular disease: a triple-blind, 6-month follow-up, placebo-controlled, randomized trial. Mol. Nutr. Food Res. 56, 810-821
37. Beaudoin, M. S., Snook, L. A., Arkell, A. M., Simpson, J. A., Holloway, G. P., and Wright, D. C. (2013) Resveratrol supplementation improves white adipose tissue function in a depot-specific manner in Zucker diabetic fatty rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 305, R542-R551
38. Gómez-Zorita, S., Fernández-Quintela, A., Lasa, A., Hijona, E., Bujanda, L., and Portillo, M. P. (2013) Effects of resveratrol on obesity-related inflammation markers in adipose tissue of genetically obese rats. Nutrition 29, 1374-1380
39. Rivera, L., Morón, R., Zarzuelo, A., and Galisteo, M. (2009) Long-term resveratrol administration reduces metabolic disturbances and lowers blood pressure in obese Zucker rats. Biochem. Pharmacol. 77, 1053-1063
40. Jimenez-Gomez, Y., Mattison, J. A., Pearson, K. J., Martin-Montalvo, A., Palacios, H. H., Sossong, A. M., Ward, T. M., Younts, C. M., Lewis, K., Allard, J. S., Longo, D. L., Belman, J. P., Malagon, M. M., Navas, P., Sanghvi, M., Moaddel, R., Tilmont, E. M., Herbert, R. L., Morrell, C. H., Egan, J. M., Baur, J. A., Ferrucci, L., Bogan, J. S., Bernier, M., and De Cabo, R. (2013) Resveratrol improves adipose insulin signaling and reduces the inflammatory response in adipose tissue of rhesus monkeys on high-fat, high-sugar diet. Cell Metab. 18, 533-545
41. Konings, E., Timmers, S., Boekschoten, M. V., Goossens, G. H., Jocken, J. W., Afman, L. A., Muller, M., Schrauwen, P., Mariman, E. C., and Blaak, E. E. (2013) The effects of 30 days resveratrol supplementation on adipose tissue morphology and gene expression patterns in obese men. Int. J. Obes. (Lond.) 38, 470-473
42. Hector, K. L., Lagisz, M., and Nakagawa, S. (2012) The effect of resveratrol on longevity across species: a meta-analysis. Biol. Lett. 8, 790-793
43. Miller, R. A., Harrison, D. E., Astle, C. M., Baur, J. A., Boyd, A. R., De Cabo, R., Fernandez, E., Flurkey, K., Javors, M. A., Nelson, J. F., Orihuela, C. J., Pletcher, S., Sharp, Z. D., Sinclair, D., Starnes, J. W., Wilkinson, J. E., Nadon, N. L., and Strong, R. (2011) Rapamycin, but not resveratrol or simvastatin, extends life span of genetically heterogeneous mice. J. Gerontol. A Biol. Sci. Med. Sci. 66, 191-201
44. Kulkarni, S. S., and Cantó, C. (2015) The molecular targets of resveratrol. Biochim. Biophys. Acta 1852, 1114-1123
45. Higashida, K., Kim, S. H., Jung, S. R., Asaka, M., Holloszy, J. O., and Han, D. H. (2013) Effects of resveratrol and SIRT1 on PGC-1α activity and mitochondrial biogenesis: a reevaluation. PLoS Biol. 11, e1001603
46. Ringholm, S., Olesen, J., Pedersen, J. T., Brandt, C. T., Halling, J. F., Hellsten, Y., Prats, C., and Pilegaard, H. (2013) Effect of lifelong resveratrol supplementation and exercise training on skeletal muscle oxidative capacity in aging mice; impact of PGC-1α. Exp. Gerontol. 48, 1311-1318
47. Montgomery, M. K., Osborne, B., Brown, S. H., Small, L., Mitchell, T. W., Cooney, G. J., and Turner, N. (2013) Contrasting metabolic effects of medium-versus long-chain fatty acids in skeletal muscle. J. Lipid Res. 54, 3322-3333
48. Turner, N., Hariharan, K., Tid Ang, J., Frangioudakis, G., Beale, S. M., Wright, L. E., Zeng, X. Y., Leslie, S. J., Li, J. Y., Kraegen, E. W., Cooney, G. J., and Ye, J. M. (2009) Enhancement of muscle mitochondrial oxidative capacity and alterations in insulin action are lipid species dependent: potent tissue-specific effects of medium-chain fatty acids. Diabetes 58, 2547-2554