Dietary intake of green tea polyphenols regulates insulin sensitivity with an increase in AMP-activated protein kinase α content and changes in mitochondrial respiratory complexes

Molecular Nutrition and Food Research

Volumn 57, Issue 3, 2013, Pages 459-470

  Serrano, José C E ^a   Gonzalo Benito, Hugo ^a   Jové, Mariona ^a   Fourcade, Stéphane ^b   Cassanyé, Anna ^a   Boada, Jordi ^a   Delgado, Marco A ^c   Espinel, Alberto E ^c   Pamplona, Reinald ^a   Portero Otín, Manuel ^a  

^a UNIVERSITY OF LLEIDA   (Spain)

^b BELLVITGE BIOMEDICAL RESEARCH INSTITUTE IDIBELL   (Spain)

^c Grupo Leche Pascual   (Spain)

Author keywords

AMPK ; Energy uptake; Insulin sensitivity; Mitochondria; Polyphenols

Indexed keywords

ANTIOXIDANT; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; LEPTIN; POLYPHENOL; PROTEIN;

ADIPOSE TISSUE; ANIMAL; ARTICLE; C57BL MOUSE; CALORIC INTAKE; CARBOHYDRATE METABOLISM; CELL STRAIN 3T3; CHEMISTRY; DRUG EFFECT; INSULIN RESISTANCE; LIPID METABOLISM; MALE; METABOLISM; MITOCHONDRION; MOUSE; OXIDATIVE STRESS; PROTEIN SUBUNIT; SECRETION (PROCESS); SKELETAL MUSCLE; TEA;

3T3-L1 CELLS; ADIPOSE TISSUE; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; ANTIOXIDANTS; CARBOHYDRATE METABOLISM; ENERGY INTAKE; INSULIN RESISTANCE; LEPTIN; LIPID METABOLISM; MALE; MICE; MICE, INBRED C57BL; MITOCHONDRIA; MUSCLE, SKELETAL; OXIDATIVE STRESS; POLYPHENOLS; PROTEIN SUBUNITS; PROTEINS; TEA;

MUS;

EID: 84875051800     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.201200513     Document Type: Article

References (43)

1. Manach, C., Williamson, G., Morand, C., Scalbert, A. et al., Bioavailability and bioefficacy of polyphenols in humans. I. Review of 97 bioavailability studies. Am. J. Clin. Nutr. 2005, 81, 230S-242S.
2. Williamson, G., Manach, C., Bioavailability and bioefficacy of polyphenols in humans. II. Review of 93 intervention studies. Am. J. Clin. Nutr. 2005, 81, 243S-255S.
3. Lotito, S. B., Frei, B., Consumption of flavonoid-rich foods and increased plasma antioxidant capacity in humans: cause, consequence, or epiphenomenon? Free Radic. Biol. Med. 2006, 41, 1727-1746.
4. Lambert, J. D., Sang, S., Lu, A. Y. H., Yang, C. S., Metabolism of dietary polyphenols and possible interactions with drugs. Curr. Drug Metab. 2007, 8, 499-507.
5. Pérez-Jiménez, J., Serrano, J., Tabernero, M., Arranz, S. et al., Effects of grape antioxidant dietary fiber in cardiovascular disease risk factors. Nutrition 2008, 24, 646-653.
6. Pérez-Jiménez, J., Serrano, J., Tabernero, M., Arranz, S. et al., Bioavailability of phenolic antioxidants associated with dietary fiber: plasma antioxidant capacity after acute and long-term intake in humans. Plant Foods Hum. Nutr. 2009, 64, 102-107.
7. Virgili, F., Marino, M., Regulation of cellular signals from nutritional molecules: a specific role for phytochemicals, beyond antioxidant activity. Free Radic. Biol. Med. 2008, 45, 1205-1216.
8. Larsen, C. A., Dashwood, R. H., Bisson, W. H., Tea catechins as inhibitors of receptor tyrosine kinases: mechanistic insights and human relevance. Pharmacol. Res. 2010, 62, 457-464.
9. Teillet, F., Boumendjel, A., Boutonnat, J., Ronot, X., Flavonoids as RTK inhibitors and potential anticancer agents. Med. Res. Rev. 2008, 28, 715-745.
10. Arner, P., Pollare, T., Lithell, H., Livingston, J. N., Defective insulin receptor tyrosine kinase in human skeletal muscle in obesity and type 2 (non-insulin-dependent) diabetes mellitus. Diabetologia 1987, 30, 437-440.
11. Klaus, S., Pültz, S., Thöne-Reineke, C., Wolfram, S., Epigallocatechin gallate attenuates diet-induced obesity in mice by decreasing energy absorption and increasing fat oxidation. Int. J. Obes. 2005, 29, 615-623.
12. Rains, T. M., Agarwal, S., Maki, K. C., Antiobesity effects of green tea catechins: a mechanistic review. J. Nutr. Biochem. 2011, 22, 1-7.
13. Englyst, H. N., Cummings, J. H., Improved method for measurement of dietary fiber as non-starch polysaccharides in plant foods. J. Assoc. Off. Anal. Chem. 1988, 71, 808-814.
14. Jové, M., Serrano, J. C. E., Ortega, N., Ayala, V. et al., Multicompartmental LC-Q-TOF-based metabonomics as an exploratory tool to identify novel pathways affected by polyphenol-rich diets in mice. J. Proteome Res. 2011, 10, 3501-3512.
15. Pamplona, R., Dalfó, E., Ayala, V., Bellmunt, M. J. et al., Proteins in human brain cortex are modified by oxidation, glycoxidation, and lipoxidation: effects of Alzheimer disease and identification of lipoxidation targets. J. Biol. Chem. 2005, 280, 21522-21530.
16. Brown, A. L., Lane, J., Holyoak, C., Nicol, B. et al., Health effects of green tea catechins in overweight and obese men: a randomised controlled cross-over trial. Br. J. Nutr. 2011, 106, 1880-1889.
17. Liao, S., Kao, Y., Hiipakka, R. A., Green tea: biochemical and biological basis for health benefits. Vit. Horm. 2001, 62, 1-94.
18. Dulloo, A. G., Duret, C., Rohrer, D., Girardier, L. et al., Efficacy of a green tea extract rich in catechin polyphenols and caffeine in increasing 24-h energy expenditure and fat oxidation in humans. Am. J. Clin. Nutr. 1999, 70, 1040-1045.
19. Finley, L. W. S., Lee, J., Souza, A., Desquiret-Dumas, V. et al., Skeletal muscle transcriptional coactivator PGC-1α mediates mitochondrial, but not metabolic, changes during calorie restriction. Proc. Natl. Acad. Sci. USA 2012, 109, 2931-2936.
20. Hardie, D. G., AMP-activated protein kinase-an energy sensor that regulates all aspects of cell function. Genes Dev. 2011, 25, 1895-1908.
21. Collins, Q. F., Liu, H., Pi, J., Liu, Z. et al., Epigallocatechin-3-gallate (EGCG), a green tea polyphenol, suppresses hepatic gluconeogenesis through 5′-AMP-activated protein kinase. J. Biol. Chem. 2007, 282, 30143-30149.
22. Echtay, K. S., Mitochondrial uncoupling proteins-what is their physiological role? Free Rad. Biol. Med. 2007, 43, 1351-1371.
23. Zhang, B. B., Zhou, G., Li, C., AMPK: an emerging drug target for diabetes and the metabolic syndrome. Cell Metab. 2009, 9, 407-416.
24. Lambert, J. D., Lee, M., Lu, H., Meng, X. et al., Epigallocatechin-3-gallate is absorbed but extensively glucuronidated following oral administration to mice. J. Nutr. 2003, 133, 4172-4177.
25. Chakrabarti, P., Anno, T., Manning, B. D., Luo, Z. et al., The mammalian target of rapamycin complex 1 regulates leptin biosynthesis in adipocytes at the level of translation: the role of the 5′-untranslated region in the expression of leptin messenger ribonucleic acid. Mol. Endocrinol. 2008, 22, 2260-2267.
26. Habinowski, S. A., Witters, L. A., The effects of AICAR on adipocyte differentiation of 3T3-L1 cells. Biochem. Biophys. Res. Commun. 2001, 286, 852-856.
27. Lin, J., Della-Fera, M. A., Baile, C. A., Green tea polyphenol epigallocatechin gallate inhibits adipogenesis and induces apoptosis in 3T3-L1 adipocytes. Obes. Res. 2005, 13, 982-990.
28. Meng, Q., Velalar, C. N., Ruan, R., Effects of epigallocatechin-3-gallate on mitochondrial integrity and antioxidative enzyme activity in the aging process of human fibroblast. Free Rad. Biol. Med. 2008, 44, 1032-1041.
29. Kobayashi, Y., Suzuki, M., Satsu, H., Arai, S. et al., Green tea polyphenols inhibit the sodium-dependent glucose transporter of intestinal epithelial cells by a competitive mechanism. J. Agric. Food Chem. 2000, 48, 5618-5623.
30. Shimizu, M., Kobayashi, Y., Suzuki, M., Satsu, H. et al., Regulation of intestinal glucose transport by tea catechins. Biofactors 2000, 13, 61-65.
31. Park, J. H., Jin, J. Y., Baek, W. K., Park, S. H. et al. Ambivalent role of gallated catechins in glucose tolerance in humans: a novel insight into non-absorbable gallated catechin-derived inhibitors of glucose absorption. J. Physiol. Pharmacol. 2009, 60, 101-109.
32. Nomura, M., Takahashi, T., Nagata, N., Tsutsumi, K. et al., Inhibitory mechanisms of flavonoids on insulin-stimulated glucose uptake in MC3T3-G2/PA6 adipose cells. Biol. Pharm. Bull. 2008, 31, 1403-1409.
33. Bazuine, M., Van Den Broek, P. J. A., Maassen, J. A., Genistein directly inhibits GLUT4-mediated glucose uptake in 3T3-L1 adipocytes. Biochem. Biophys. Res. Commun. 2005, 326, 511-514.
34. Strobel, P., Allard, C., Perez-Acle, T., Calderon, R. et al. Myricetin, quercetin and catechin-gallate inhibit glucose uptake in isolated rat adipocytes. Biochem. J. 2005, 386, 471-478.
35. Harmon, A. W., Patel, Y. M., Naringenin inhibits phosphoinositide 3-kinase activity and glucose uptake in 3T3-L1 adipocytes. Biochem. Biophys. Res. Commun. 2003, 305, 229-234.
36. Goldstein, B. J., Kalyankar, M., Wu, X., Redox paradox: insulin action is facilitated by insulin-stimulated reactive oxygen species with multiple potential signaling targets. Diabetes 2005, 54, 311-321.
37. Schroeder, E. K., Kelsey, N. A., Doyle, J., Breed, E. et al., Green tea epigallocatechin 3-gallate accumulates in mitochondria and displays a selective antiapoptotic effect against inducers of mitochondrial oxidative stress in neurons. Antioxid. Redox Signal 2009, 11, 469-480.
38. Bach, D., Naon, D., Pich, S., Soriano, F. X. et al., Expression of Mfn2, the Charcot-Marie-Tooth neuropathy type 2A gene, in human skeletal muscle: effects of type 2 diabetes, obesity, weight loss, and the regulatory role of tumor necrosis factor α and interleukin-6. Diabetes 2005, 54, 2685-2693.
39. Toledo, F. G. S., Watkins, S., Kelley, D. E., Changes induced by physical activity and weight loss in the morphology of intermyofibrillar mitochondria in obese men and women. J. Clin. Endocrinol. Metab. 2006, 91, 3224-3227.
40. Taub, P. R., Ramirez-Sanchez, I., Ciaraldi, T. P., Perkins, G. et al., Alterations in skeletal muscle indicators of mitochondrial structure and biogenesis in patients with type 2 diabetes and heart failure: effects of epicatechin rich cocoa. Clin. Transl. Sci. 2012, 5, 43-47.
41. Bach, D., Pich, S., Soriano, F. X., Vega, N. et al., Mitofusin-2 determines mitochondrial network architecture and mitochondrial metabolism: a novel regulatory mechanism altered in obesity. J. Biol. Chem. 2003, 278, 17190-17197.
42. Murase, T., Haramizu, S., Shimotoyodome, A., Tokimitsu, I. et al., Green tea extract improves running endurance in mice by stimulating lipid utilization during exercise. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2006, 290, R1550-R1556.
43. Okita, N., Hayashida, Y., Kojima, Y., Fukushima, M. et al., Differential responses of white adipose tissue and brown adipose tissue to caloric restriction in rats. Mech. Ageing Dev. 2012, 133, 255-266.