Resveratrol and diabetes: From animal to human studies

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1852, Issue 6, 2015, Pages 1145-1154

  Szkudelski, Tomasz ^a   Szkudelska, Katarzyna ^a  

^a POZNA UNIVERSITY OF LIFE SCIENCES   (Poland)

Author keywords

Diabetes; Insulin; Metabolism; Resveratrol

Indexed keywords

HYPOGLYCEMIC AGENTS; RESVERATROL; STILBENES;

ADIPOSE TISSUE; ANIMALS; DIABETES MELLITUS; DRUG EFFECTS; HUMANS; INSULIN-SECRETING CELLS; LIVER; METABOLISM; MUSCLE, SKELETAL; TRANSLATIONAL MEDICAL RESEARCH;

ADIPOSE TISSUE; ANIMALS; DIABETES MELLITUS; HUMANS; HYPOGLYCEMIC AGENTS; INSULIN-SECRETING CELLS; LIVER; MUSCLE, SKELETAL; STILBENES; TRANSLATIONAL MEDICAL RESEARCH;

EID: 84937532659     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2014.10.013     Document Type: Review

References (113)

1. International Diabetes Federation IDF Diabetes Atlas 2013, International Diabetes Federation, Brussels, Belgium. 6th edn.
2. American Diabetes Association Diagnosis and classification of diabetes mellitus. Diabetes Care 2006, 29:S43-S48.
3. Cheng A.Y., Fantus I.G. Oral antihyperglycemic therapy for type 2 diabetes mellitus. CMAJ 2005, 175:213-226.
4. Nicholson G., Hall G.M. Diabetes mellitus: new drugs for a new epidemic. Br. J. Anaesth. 2011, 107:65-73.
5. Verspohl E.J. Novel pharmacological approaches to the treatment of type 2 diabetes. Pharmacol. Rev. 2012, 64:188-237.
6. Frombaum M., Le Clanche S., Bonnefont-Rousselot D., Borderie D. Antioxidant effects of resveratrol and other stilbene derivatives on oxidative stress and NO bioavailability: Potential benefits to cardiovascular diseases. Biochimie 2012, 94:269-276.
7. Zordoky B.N.M., Robertson I.M., Dyck J.R.B. Preclinical and clinical evidence for the role of resveratrol in the treatment of cardiovascular diseases. Biochim. Biophys. Acta 2015, 1852:1155-1177.
8. Carter L.G., D'Orazio J.A., Pearson K.J. Resveratrol and cancer: focus on in vivo evidence. Endocr. Relat. Cancer 2014, 21:209-225.
9. Singh C.K., Ndiaye M.A., Ahmad N. Resveratrol and cancer: challenges for clinical translation. Biochim. Biophys. Acta 2015, 1852:1178-1185.
10. Poulsen M.M., Fjeldborg K., Ornstrup M.J., Kjær T.N., Nøhr M.K., Pedersen S.B. Resveratrol and inflammation. Biochim. Biophys. Acta 2015, 1852:1124-1136.
11. Pallàs M., Casadesús G., Smith M.A., Coto-Montes A., Pelegri C., Vilaplana J., Camins A. Resveratrol and neurodegenerative diseases: activation of SIRT1 as the potential pathway towards neuroprotection. Curr. Neurovasc. Res. 2009, 6:70-81.
12. Bastianetto S., Ménard C., Quirion R. Neuroprotective action of resveratrol. Biochim. Biophys. Acta 2015, 1852(6):1195-1201.
13. Szkudelska K., Szkudelski T. Resveratrol, obesity and diabetes. Eur. J. Pharmacol. 2010, 635:1-8.
14. De Ligt M., Timmers S., Schrauwen P. Resveratrol and obesity: can resveratrol relieve metabolic disturbances?. Biochim. Biophys. Acta 2015, 1852:1137-1144.
15. Szkudelski T., Szkudelska K. Anti-diabetic effects of resveratrol. Ann. N. Y. Acad. Sci. 2011, 1215:34-39.
16. Vang O., Ahmad N., Baile C.A., Baur J.A., Brown K., Csiszar A., Das D.K., Delmas D., Gottfried C., Lin H.Y., Ma Q.Y., Mukhopadhyay P., Nalini N., Pezzuto J.M., Richard T., Shukla Y., Surh Y.J., Szekeres T., Szkudelski T., Walle T., Wu J.M. What is new for an old molecule? Systematic review and recommendations on the use of resveratrol. PLoS ONE 2011, 6:e19881. (1-11).
17. Chi T.C., Chen W.P., Chi T.L., Kuo T.F., Lee S.S., Cheng J.T., Su M.J. Phosphatidylinositol-3-kinase is involved in the antihyperglycemic effect induced by resveratrol in streptozotocin-induced diabetic rats. Life Sci. 2007, 80:1713-1720.
18. Silan C. The effects of chronic resveratrol treatment on vascular responsiveness of streptozotocin-induced diabetic rats. Biol. Pharm. Bull. 2008, 31:897-902.
19. Shahi M.M., Haidari F., Shiri M.R. Comparison of effect of resveratrol and vanadium on diabetes related dyslipidemia and hyperglycemia in streptozotocin induced diabetic rats. Adv. Pharm. Bull. 2011, 1:81-86.
20. Chang C.C., Chang C.Y., Wu Y.T., Huang J.P., Yen T.H., Hung L.M. Resveratrol retards progression of diabetic nephropathy through modulations of oxidative stress, proinflammatory cytokines, and AMP-activated protein kinase. J. Biomed. Sci. 2011, 18:18-47.
21. Ku C.R., Lee H.J., Kim S.K., Lee E.Y., Lee M.K., Lee E.J. Resveratrol prevents streptozotocin-induced diabetes by inhibiting the apoptosis of pancreatic β-cell and the cleavage of poly (ADP-ribose) polymerase. Endocr. J. 2012, 59:103-109.
22. Chang C.C., Chang C.Y., Huang J.P., Hung L.M. Effect of resveratrol on oxidative and inflammatory stress in liver and spleen of streptozotocin-induced type 1 diabetic rats. Chin. J. Physiol. 2012, 55:192-201.
23. Jiang B., Guo L., Li B.Y., Zhen J.H., Song J., Peng T., Yang X.D., Hu Z., Gao H.Q. Resveratrol attenuates early diabetic nephropathy by down-regulating glutathione s-transferases Mu in diabetic rats. J. Med. Food 2013, 16:481-486.
24. Palsamy P., Subramanian S. Resveratrol, a natural phytoalexin, normalizes hyperglycemia in streptozotocin-nicotinamide induced experimental diabetic rats. Biomed. Pharmacother. 2008, 62:598-605.
25. Palsamy P., Subramanian S. Modulatory effects of resveratrol on attenuating the key enzymes activities of carbohydrate metabolism in streptozotocin-nicotinamide-induced diabetic rats. Chem. Biol. Interact. 2009, 179:356-362.
26. Palsamy P., Subramanian S. Ameliorative potential of resveratrol on proinflammatory cytokines, hyperglycemia mediated oxidative stress, and pancreatic beta-cell dysfunction in streptozotocin-nicotinamide-induced diabetic rats. J. Cell. Physiol. 2010, 224:423-432.
27. Soufi F.G., Vardyani M., Sheervalilou R., Mohammadi M., Somi M.H. Long-term treatment with resveratrol attenuates oxidative stress pro-inflammatory mediators and apoptosis in streptozotocin-nicotinamide-induced diabetic rats. Gen. Physiol. Biophys. 2012, 31:431-438.
28. Szkudelski T. The mechanism of alloxan and streptozotocin action in B cells of the rat pancreas. Physiol. Res. 2001, 50:537-546.
29. Szkudelski T. Streptozotocin-nicotinamide-induced diabetes in the rat. Characteristics of the experimental model. Exp. Biol. Med. (Maywood) 2012, 237:481-490.
30. Chang C.C., Yang M.H., Tung H.C., Chang C.Y., Tsai Y.L., Huang J.P., Yen T.H., Hung L.M. Resveratrol exhibits differential protective effects on fast- and slow-twitch muscles in streptozotocin-induced diabetic rats. J. Diabetes 2014, 6:60-67.
31. Lenzen S. Oxidative stress: the vulnerable beta-cell. Biochem. Soc. Trans. 2008, 36:343-347.
32. Lee S.M., Yang H., Tartar D.M., Gao B., Luo X., Ye S.Q., Zaghouani H., Fang D. Prevention and treatment of diabetes with resveratrol in a non-obese mouse model of type 1 diabetes. Diabetologia 2011, 54:1136-1146.
33. Chen K.H., Cheng M.L., Jing Y.H., Chiu D.T., Shiao M.S., Chen J.K. Resveratrol ameliorates metabolic disorders and muscle wasting in streptozotocin-induced diabetic rats. Am. J. Physiol. Endocrinol. Metab. 2011, 301:853-863.
34. D'Souza D.M., Al-Sajee D., Hawke T.J. Diabetic myopathy: impact of diabetes mellitus on skeletal muscle progenitor cells. Front. Physiol. 2013, 4:1-7.
35. Deng J.Y., Hsieh P.S., Huang J.P., Lu L.S., Hung L.M. Activation of estrogen receptor is crucial for resveratrol-stimulating muscular glucose uptake via both insulin-dependent and -independent pathways. Diabetes 2008, 57:1814-1823.
36. Hamadi N., Mansour A., Hassan M.H., Khalifi-Touhami F., Badary O. Ameliorative effects of resveratrol on liver injury in streptozotocin-induced diabetic rats. J. Biochem. Mol. Toxicol. 2012, 26:384-392.
37. Sadi G., Bozan D., Yildiz H.B. Redox regulation of antioxidant enzymes: post-translational modulation of catalase and glutathione peroxidase activity by resveratrol in diabetic rat liver. Mol. Cell. Biochem. 2014, 393:111-122.
38. Sattar N., Gill J.M. Type 2 diabetes as a disease of ectopic fat?. BMC Med. 2014, 26. 10.1186/s12916-014-0123-4.
39. Palermo A., Maggi D., Maurizi A.R., Pozzilli P., Buzzetti R. Prevention of type 2 diabetes mellitus: is it feasible?. Diabetes Metab. Res. Rev. 2014, 30:4-12.
40. Pedersen S.D. Metabolic complications of obesity. Best Pract. Res. Clin. Endocrinol. Metab. 2013, 27:179-193.
41. Han T.S., Wu F.C., Lean M.E. Obesity and weight management in the elderly: a focus on men. Best Pract. Res. Clin. Endocrinol. Metab. 2013, 27:509-525.
42. Weir G.C., Bonner-Weir S. Islet β cell mass in diabetes and how it relates to function, birth, and death. Ann. N. Y. Acad. Sci. 2013, 1281:92-105.
43. Björnholm M., Zierath J.R. Insulin signal transduction in human skeletal muscle: identifying the defects in type II diabetes. Biochem. Soc. Trans. 2005, 33:354-357.
44. Chen L.L., Zhang H.H., Zheng J., Hu X., Kong W., Hu D., Wang S.X., Zhang P. Resveratrol attenuates high-fat diet-induced insulin resistance by influencing skeletal muscle lipid transport and subsarcolemmal mitochondrial β-oxidation. Metab. Clin. Exp. 2011, 60:1598-1609.
45. Tan Z., Zhou L.J., Mu P.W., Liu S.P., Chen S.J., Fu X.D., Wang T.H. Caveolin-3 is involved in the protection of resveratrol against high-fat-diet-induced insulin resistance by promoting GLUT4 translocation to the plasma membrane in skeletal muscle of ovariectomized rats. J. Nutr. Biochem. 2012, 23:1716-1724.
46. 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.
47. Kang W., Hong H.J., Guan J., Kim D.G., Yang E.J., Koh G., Park D., Han C.H., Lee Y.J., Lee D.H. Resveratrol improves insulin signaling in a tissue-specific manner under insulin-resistant conditions only: in vitro and in vivo experiments in rodents. Metab. Clin. Exp. 2012, 61:424-433.
48. Zhang J., Chen L., Zheng J., Zeng T., Li H., Xiao H., Deng X., Hu X. The protective effect of resveratrol on islet insulin secretion and morphology in mice on a high-fat diet. Diabetes Res. Clin. Pract. 2012, 97:474-482.
49. Jeon B.T., Jeong E.A., Shin H.J., Lee Y., Lee D.H., Kim H.J., Kang S.S., Cho G.J., Choi W.S., Roh G.S. Resveratrol attenuates obesity-associated peripheral and central inflammation and improves memory deficit in mice fed a high-fat diet. Diabetes 2012, 61:1444-1454.
50. Yang S.J., Lim Y. Resveratrol ameliorates hepatic metaflammation and inhibits NLRP3 inflammasome activation. Metab. Clin. Exp. 2014, 63:693-701.
51. Zheng X., Zhu S., Chang S., Cao Y., Dong J., Li J., Long R., Zhou Y. Protective effects of chronic resveratrol treatment on vascular inflammatory injury in streptozotocin-induced type 2 diabetic rats: Role of NF-kappa B signaling. Eur. J. Pharmacol. 2013, 720:147-157.
52. Bagul P.K., Middela H., Matapally S., Padiya R., Bastia T., Madhusudana K., Reddy B.R., Chakravarty S., Banerjee S.K. Attenuation of insulin resistance, metabolic syndrome and hepatic oxidative stress by resveratrol in fructose-fed rats. Pharmacol. Res. 2012, 66:260-268.
53. Burgess T.A., Robich M.P., Chu L.M., Bianchi C., Sellke F.W. Improving glucose metabolism with resveratrol in a swine model of metabolic syndrome through alteration of signaling pathways in the liver and skeletal muscle. Arch. Surg. 2011, 146:556-564.
54. Rivera L., Morón R., Zarzuelo A., Galisteo M. Long-term resveratrol administration reduces metabolic disturbances and lowers blood pressure in obese Zucker rats. Biochem. Pharmacol. 2009, 77:1053-1063.
55. Beaudoin M.S., Snook L.A., Arkell A.M., Simpson J.A., Holloway G.P., Wright D.C. Resveratrol supplementation improves white adipose tissue function in a depot-specific manner in Zucker diabetic fatty rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2013, 305:542-551.
56. Chen S., Li J., Zhang Z., Li W., Sun Y., Zhang Q., Feng X., Zhu W. Effects of resveratrol on the amelioration of insulin resistance in KKAy mice. Can. J. Physiol. Pharmacol. 2012, 90:237-242.
57. Lee Y.E., Kim J.W., Lee E.M., Ahn Y.B., Song K.H., Yoon K.H., Kim H.W., Park C.W., Li G., Liu Z., Ko S.H. Chronic resveratrol treatment protects pancreatic islets against oxidative stress in db/db mice. PLoS ONE 2012, 7:e50412.
58. Guo R., Liu B., Wang K., Zhou S., Li W., Xu Y. Resveratrol ameliorates diabetic vascular inflammation and macrophage infiltration in db/db mice by inhibiting the NF-κB pathway. Diab. Vasc. Dis. Res. 2014, 11:92-102.
59. Marchal J., Blanc S., Epelbaum J., Aujard F., Pifferi F. Effects of chronic calorie restriction or dietary resveratrol supplementation on insulin sensitivity markers in a primate, Microcebus murinus. PLoS ONE 2012, 7:e34289.
60. 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., de Cabo R. Resveratrol improves adipose insulin signaling and reduces the inflammatory response in adipose tissue of rhesus monkeys on high-fat, high-sugar diet. Cell Metab. 2013, 18:533-545.
61. Fiori J.L., Shin Y.K., Kim W., Krzysik-Walker S.M., González-Mariscal I., Carlson O.D., Sanghvi M., Moaddel R., Farhang K., Gadkaree S.K., Doyle M.E., Pearson K.J., Mattison J.A., de Cabo R., Egan J.M. Resveratrol prevents β-cell dedifferentiation in nonhuman primates given a high-fat/high-sugar diet. Diabetes 2013, 62:3500-3513.
62. Do G.M., Jung U.J., Park H.J., Kwon E.Y., Jeon S.M., McGregor R.A., Choi M.S. Resveratrol ameliorates diabetes-related metabolic changes via activation of AMP-activated protein kinase and its downstream targets in db/db mice. Mol. Nutr. Food Res. 2012, 56:1282-1291.
63. Um J.H., Park S.J., Kang H., Yang S., Foretz M., McBurney M.W., Kim M.K., Viollet B., Chung J.H. AMP-activated protein kinase-deficient mice are resistant to the metabolic effects of resveratrol. Diabetes 2010, 59:554-563.
64. Coen P.M., Goodpaster B.H. Role of intramyocelluar lipids in human health. Trends Endocrinol. Metab. 2012, 23:391-398.
65. Hoeks J., Schrauwen P. Muscle mitochondria and insulin resistance: a human perspective. Trends Endocrinol. Metab. 2012, 23:444-450.
66. Kitada M., Koya D. SIRT1 in type 2 diabetes: Mechanisms and therapeutic potential. Diabetes Metab. J. 2013, 37:315-325.
67. Kitada M., Kume S., Kanasaki K., Takeda-Watanabe A., Koya D. Sirtuins as possible drug targets in type 2 diabetes. Curr. Drug Targets 2013, 14:622-636.
68. Baur J.A. Biochemical effects of SIRT1 activators. Biochim. Biophys. Acta 2010, 1804:1626-1634.
69. Ruderman N.B., Carling D., Prentki M., Cacicedo J.M. AMPK, insulin resistance, and the metabolic syndrome. J. Clin. Invest. 2013, 123:2764-2772.
70. Shang J., Chen L.L., Xiao F.X., Sun H., Ding H.C., Xiao H. Resveratrol improves non-alcoholic fatty liver disease by activating AMP-activated protein kinase. Acta Pharmacol. Sin. 2008, 29:698-706.
71. Hoehn K.L., Turner N., Swarbrick M.M., Wilks D., Preston E., Phua Y., Joshi H., Furler S.M., Larance M., Hegarty B.D., Leslie S.J., Pickford R., Hoy A.J., Kraegen E.W., James D.E., Cooney G.J. Acute or chronic upregulation of mitochondrial fatty acid oxidation has no net effect on whole-body energy expenditure or adiposity. Cell Metab. 2010, 11:70-76.
72. Poulsen M.M., Vestergaard P.F., Clasen B.F., Radko Y., Christensen L.P., Stødkilde-Jørgensen H., Møller N., Jessen N., Pedersen S.B., Jørgensen J.O. High-dose resveratrol supplementation in obese men: an investigator-initiated, randomized, placebo-controlled clinical trial of substrate metabolism, insulin sensitivity, and body composition. Diabetes 2013, 62:1186-1195.
73. Tauriainen E., Luostarinen M., Martonen E., Finckenberg P., Kovalainen M., Huotari A., Herzig K.H., Lecklin A., Mervaala E. Distinct effects of calorie restriction and resveratrol on diet-induced obesity and fatty liver formation. J. Nutr. Metab. 2011, 2011:525094.
74. Andrade J.M., Paraíso A.F., de Oliveira M.V., Martins A.M., Neto J.F., Guimarães A.L., de Paula A.M., Qureshi M., Santos S.H. Resveratrol attenuates hepatic steatosis in high-fat fed mice by decreasing lipogenesis and inflammation. Nutrition 2014, 30:915-919.
75. Gómez-Zorita S., Fernández-Quintela A., Lasa A., Hijona E., Bujanda L., Portillo M.P. Effects of resveratrol on obesity-related inflammation markers in adipose tissue of genetically obese rats. Nutrition 2013, 29:1374-1380.
76. Zhu W., Chen S., Li Z., Zhao X., Li W., Sun Y., Zhang Z., Ling W., Feng X. Effects and mechanisms of resveratrol on the amelioration of oxidative stress and hepatic steatosis in KKAy mice. Nutr. Metab. (Lond.) 2014, 12. 10.1186/1743-7075-11-35.
77. Alberdi G., Rodríguez V.M., Macarulla M.T., Miranda J., Churruca I., Portillo M.P. Hepatic lipid metabolic pathways modified by resveratrol in rats fed an obesogenic diet. Nutrition 2013, 29:562-567.
78. Hou X., Xu S., Maitland-Toolan K.A., Sato K., Jiang B., Ido Y., Lan F., Walsh K., Wierzbicki M., Verbeuren T.J., Cohen R.A., Zang M. SIRT1 regulates hepatocyte lipid metabolism through activating AMP-activated protein kinase. J. Biol. Chem. 2008, 283:20015-20026.
79. Hong H.J., Kang W., Kim D.G., Lee D.H., Lee Y., Han C.H. Effects of resveratrol on the insulin signaling pathway of obese mice. J. Vet. Sci. 2014, 15:179-185.
80. Boden G. Role of fatty acids in the pathogenesis of insulin resistance and NIDDM. Diabetes 1997, 46:3-10.
81. Rachek L.I. Free fatty acids and skeletal muscle insulin resistance. Prog. Mol. Biol. Transl. Sci. 2014, 121:267-292.
82. Jung U.J., Choi M.S. Obesity and its metabolic complications: the role of adipokines and the relationship between obesity, inflammation, insulin resistance, dyslipidemia and nonalcoholic fatty liver disease. Int. J. Mol. Sci. 2014, 15:6184-6223.
83. Lontchi-Yimagou E., Sobngwi E., Matsha T.E., Kengne A.P. Diabetes mellitus and inflammation. Curr. Diab. Rep. 2013, 13:435-444.
84. Mraz M., Haluzik M. The role of adipose tissue immune cells in obesity and low-grade inflammation. J. Endocrinol. 2014, 222:113-127.
85. Leiherer A., Mündlein A., Drexel H. Phytochemicals and their impact on adipose tissue inflammation and diabetes. Vascul. Pharmacol. 2013, 58:3-20.
86. Smith B.K., Perry C.G., Herbst E.A., Ritchie I.R., Beaudoin M.S., Smith J.C., Neufer P.D., Wright D.C., Holloway G.P. Submaximal ADP-stimulated respiration is impaired in ZDF rats and recovered by resveratrol. J. Physiol. 2013, 591:6089-6101.
87. Oliveira Andrade J.M., Paraíso A.F., Garcia Z.M., Ferreira A.V., Sinisterra R.D., Sousa F.B., Guimarães A.L., de Paula A.M., Campagnole-Santos M.J., dos Santos R.A., Santos S.H. Cross talk between angiotensin-(1-7)/Mas axis and sirtuins in adipose tissue and metabolism of high-fat feed mice. Peptides 2014, 55:158-165.
88. Brasnyó P., Molnár G.A., Mohás M., Markó L., Laczy B., Cseh J., Mikolás E., Szijártó I.A., Mérei A., Halmai R., Mészáros L.G., Sümegi B., Wittmann I. Resveratrol improves insulin sensitivity, reduces oxidative stress and activates the Akt pathway in type 2 diabetic patients. Br. J. Nutr. 2011, 106:383-938.
89. 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., Schrauwen P. Calorie restriction-like effects of 30days of resveratrol supplementation on energy metabolism and metabolic profile in obese humans. Cell Metab. 2011, 14:612-622.
90. Movahed A., Nabipour I., Lieben Louis X., Thandapilly S.J., Yu L., Kalantarhormozi M., Rekabpour S.J., Netticadan T. Antihyperglycemic effects of short term resveratrol supplementation in type 2 diabetic patients. Evid. Based Complement. Alternat. Med. 2013, 2013:851267.
91. Bhatt J.K., Thomas S., Nanjan M.J. Resveratrol supplementation improves glycemic control in type 2 diabetes mellitus. Nutr. Res. 2012, 32:537-541.
92. Crandall J.P., Oram V., Trandafirescu G., Reid M., Kishore P., Hawkins M., Cohen H.W., Barzilai N. Pilot study of resveratrol in older adults with impaired glucose tolerance. J. Gerontol. A Biol. Sci. Med. Sci. 2012, 67:1307-1312.
93. Méndez-Del Villar M., González-Ortiz M., Martínez-Abundis E., Pérez-Rubio K.G., Lizárraga-Valdez R. Effect of resveratrol administration on metabolic syndrome, insulin sensitivity, and insulin secretion. Metab. Syndr. Relat. Disord. 2014, 19. (Epub ahead of print).
94. Dash S., Xiao C., Morgantini C., Szeto L., Lewis G.F. High-dose resveratrol treatment for 2weeks inhibits intestinal and hepatic lipoprotein production in overweight/obese men. Arterioscler. Thromb. Vasc. Biol. 2013, 33:2895-2901.
95. Bashmakov Y.K., Assaad-Khalil S.H., Abou Seif M., Udumyan R., Megallaa M., Rohoma K.H., Zeitoun M., Petyaev I.M. Resveratrol promotes foot ulcer size reduction in type 2 diabetes patients. ISRN Endocrinol. 2014, 20. (816307).
96. Chachay V.S., Macdonald G.A., Martin J.H., Whitehead J.P., O'Moore-Sullivan T.M., Lee P., Franklin M., Klein K., Taylor P.J., Ferguson M., Coombes J.S., Thomas G.P., Cowin G.J., Kirkpatrick C.M., Prins J.B., Hickman I.J. Resveratrol does not benefit patients with nonalcoholic fatty liver disease. Clin. Gastroenterol. Hepatol. 2014, 25. 10.1016/j.cgh.2014.02.024.
97. Olesen J., Gliemann L., Biensø R., Schmidt J., Hellsten Y., Pilegaard H. Exercise training, but not resveratrol, improves metabolic and inflammatory status in skeletal muscle of aged men. J. Physiol. 2014, 592:1873-1886.
98. Yoshino J., Conte C., Fontana L., Mittendorfer B., Imai S., Schechtman K.B., Gu C., Kunz I., Rossi Fanelli F., Patterson B.W., Klein S. Resveratrol supplementation does not improve metabolic function in nonobese women with normal glucose tolerance. Cell Metab. 2012, 16:658-664.
99. Goh K.P., Lee H.Y., Lau D.P., Supaat W., Chan Y.H., Koh A.F.Y. Effects of resveratrol in patients with type 2 diabetes mellitus on skeletal muscle SIRT1 expression and energy expenditure. Int. J. Sport Nutr. Exerc. Metab. 2014, 24:2-13.
100. Hinke S.A., Hellemans K., Schuit F.C. Plasticity of the beta cell insulin secretory competence: preparing the pancreatic beta cell for the next meal. J. Physiol. 2004, 558:369-380.
101. Henquin J.C. The dual control of insulin secretion by glucose involves triggering and amplifying pathways in β-cells. Diabetes Res. Clin. Pract. 2011, 93:27-31.
102. Portha B., Giroix M.H., Tourrel-Cuzin C., Le-Stunff H., Movassat J. The GK rat: a prototype for the study of non-overweight type 2 diabetes. Methods Mol. Biol. 2012, 933:125-159.
103. Masiello P. Animal models of type 2 diabetes with reduced pancreatic beta-cell mass. Int. J. Biochem. Cell Biol. 2006, 38:873-893.
104. Bensellam M., Laybutt D.R., Jonas J.C. The molecular mechanisms of pancreatic β-cell glucotoxicity: recent findings and future research directions. Mol. Cell. Endocrinol. 2012, 364:1-27.
105. Marchetti P., Bugliani M., Boggi U., Masini M., Marselli L. The pancreatic beta cells in human type 2 diabetes. Adv. Exp. Med. Biol. 2012, 771:288-309.
106. Kong W., Chen L.L., Zheng J., Zhang H.H., Hu X., Zeng T.S., Hu D. Resveratrol supplementation restores high-fat diet-induced insulin secretion dysfunction by increasing mitochondrial function in islet. Exp. Biol. Med. (Maywood) 2014, 15. (Epub ahead of print).
107. Chan C.B., Saleh M.C., Koshkin V., Wheeler M.B. Uncoupling protein 2 and islet function. Diabetes 2004, 53:136-142.
108. Li N., Stojanovski S., Maechler P. Mitochondrial hormesis in pancreatic β cells: does uncoupling protein 2 play a role?. Oxid. Med. Cell. Longev. 2012, 10.1155/2012/740849.
109. Ježek P., Olejár T., Smolková K., Ježek J., Dlasková A., Plecitá-Hlavatá L., Zelenka J., Špaček T., Engstová H., Pajuelo Reguera D., Jabůrek M. Antioxidant and regulatory role of mitochondrial uncoupling protein UCP2 in pancreatic beta-cells. Physiol. Res. 2014, 63:73-91.
110. Knop F.K., Konings E., Timmers S., Schrauwen P., Holst J.J., Blaak E.E. Thirty days of resveratrol supplementation does not affect postprandial incretin hormone responses, but suppresses postprandial glucagon in obese subjects. Diabet. Med. 2013, 30:1214-1218.
111. 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., Sinclair D.A. SIRT1 is required for AMPK activation and the beneficial effects of resveratrol on mitochondrial function. Cell Metab. 2012, 15:675-690.
112. Ljubicic V., Burt M., Lunde J.A., Jasmin BJ B.J. Resveratrol induces expression of the slow, oxidative phenotype in mdx mouse muscle together with enhanced activity of the SIRT1-PGC-1α axis. Am. J. Physiol. Cell Physiol. 2014, 307:66-82.
113. Cottart C.H., Nivet-Antoine V., Beaudeux J.L. Reviev of recent data on the metabolism, biological effects, and toxicity of resveratrol in humans. Mol. Nutr. Food Res. 2014, 58:7-21.