Resveratrol protects against methylglyoxal-induced hyperglycemia and pancreatic damage in vivo

Nutrients

Volumn 7, Issue 4, 2015, Pages 2850-2865

  Cheng, An Sheng ^a   Cheng, Yu Hsiang ^b   Lee, Chi Ying ^a   Chung, Chin Yuan ^a   Chang, Wen Chang ^a  

^a Department of Medicinal Plant Development   (Taiwan)

^b UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

Diabetes; Methylglyoxal; Nuclear factor erythroid 2 related factor 2; Resveratrol; Retinoic acid

Indexed keywords

INSULIN RECEPTOR SUBSTRATE 1; INTERLEUKIN 1BETA; METHYLGLYOXAL; PIOGLITAZONE; RESVERATROL; RETINOIC ACID; TRANSCRIPTION FACTOR NRF2; TUMOR NECROSIS FACTOR ALPHA; TYROSINE; ANTIDIABETIC AGENT; ANTIINFLAMMATORY AGENT; GLUCOSE BLOOD LEVEL; INSULIN; INSULIN RECEPTOR SUBSTRATE; IRS1 PROTEIN, MOUSE; NFE2L2 PROTEIN, MOUSE; STILBENE DERIVATIVE;

ANIMAL MODEL; ANIMAL TISSUE; ANTIDIABETIC ACTIVITY; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BLOOD ANALYSIS; CONTROLLED STUDY; DIABETES MELLITUS; DRUG INDUCED DISEASE; ENZYME LINKED IMMUNOSORBENT ASSAY; GLUCOSE BLOOD LEVEL; GLYCOSYLATION; HOMEOSTASIS; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; INSULIN RESISTANCE; INSULIN TOLERANCE TEST; MALE; METHYLGLYOXAL INDUCED HYPERGLYCEMIA; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; ORAL GLUCOSE TOLERANCE TEST; PANCREAS DISEASE; PROTEIN EXPRESSION ASSAY; PROTEIN PHOSPHORYLATION; RISK ASSESSMENT; ANIMAL; BAGG ALBINO MOUSE; BLOOD; CHEMICALLY INDUCED; CYTOLOGY; DISEASE MODEL; DRUG EFFECTS; GENETICS; GLUCOSE TOLERANCE TEST; HYPERGLYCEMIA; INFLAMMATION; LIVER; METABOLISM; PANCREAS; PANCREATIC DISEASES; PHOSPHORYLATION;

MUS;

ANIMALS; ANTI-INFLAMMATORY AGENTS; BLOOD GLUCOSE; DISEASE MODELS, ANIMAL; GLUCOSE TOLERANCE TEST; HYPERGLYCEMIA; HYPOGLYCEMIC AGENTS; INFLAMMATION; INSULIN; INSULIN RECEPTOR SUBSTRATE PROTEINS; INSULIN RESISTANCE; LIVER; MALE; MICE; MICE, INBRED BALB C; NF-E2-RELATED FACTOR 2; PANCREAS; PANCREATIC DISEASES; PHOSPHORYLATION; PYRUVALDEHYDE; STILBENES;

EID: 84927915781     PISSN: None     EISSN: 20726643     Source Type: Journal    
DOI: 10.3390/nu7042850     Document Type: Article

References (60)

1. Negre-Salvayre, A.; Halvayre, R.; Auge, N.; Pamplona, R.; Portero-Otin, M. Hyperglycemia and glycation in diabetic complications. Antioxid. Redox Signal. 2009, 11, 3071-3109.
2. Schiekofer, S.; Andrassy, M.; Chen, J.; Rudofsky, G.; Schneider, J.; Wendt, T.; Stefan, N.; Humpert, P.; Fritsche, A.; Stumvoll, M.; et al. Acute hyperglycemia causes intracellular formation of CML and activation of ras p42/44 MAPK and nuclear factor kappaB in PBMCs. Diabetes 2003, 52, 621-633.
3. Bonnefont-Rousselot, D. Glucose and reactive oxygen species. Curr. Opin. Clin. Nutr. Metab. Care 2002, 5, 561-568.
4. Wu, C.H.; Huang, S.M.; Lin, J.A.; Yen, G.C. Inhibition of advanced glycationend product formation by foodstuffs. Food Funct. 2011, 2, 224-234.
5. Dhar, A.; Desai, K.M.; Wu, L. Alagebrium attenuates acute methylglyoxal induced glucose intolerance in Sprague-Dawley rats. Br. J. Pharmacol. 2010, 159, 166-175.
6. Dhar, A.; Dhar, I.; Jiang, B.; Desai, K.M.; Wu, L. Chronic methylglyoxal injection by minipump causes pancreatic beta-cell dysfunction and induces type 2 diabetes in Sprague-Dawley rats. Diabetes 2011, 60, 899-908.
7. Keum, Y.S.; Owuor, E.D.; Kim, B.R.; Hu, R.; Kong, A.N. Involvement of Nrf2 and JNK1 in the activation of antioxidant responsive element (ARE) by chemopreventive agent phenethylisothiocyanate (PEITC). Pharm. Res.2003, 20, 1351-1356.
8. Kobayashi, M.; Yamamoto, M. Molecular mechanisms activating the Nrf2-Keap1 pathway of antioxidant gene regulation. Antioxid. Redox Signal. 2005, 7, 385-394.
9. Vander-Jagt, D.; Hunsaker, L. Methylglyoxal metabolism and diabetic complications: Roles of aldose reductase, glyxalase-I, betaine aldehyde dehydrogenase and oxoaldehyde dehydrogenase. Chem. Biol. Int. 2003, 143, 341-351.
10. Romero-Sarmiento, Y.; Soto-Rodriguez, I.; Arzaba-Villalba, A.; Garcia, H.S.; Alexander-Aguilera, A. Effects of conjugated linoleic acid on oxidative stress in rats with sucrose-induced non-alcoholic fatty liver disease. J. Funct. Foods 2012, 4, 219-225.
11. Khuhawar, M.Y.; Kandhro, A.J.; Khand, F.D. Liquid chromatographic determination of glyoxal and methylglyoxal from serum of diabetic patients using meso-stilbenediamine as derivatizing agent. Anal. Lett. 2006, 39, 2205-2215.
12. Wang, J.; Chang, T. Methylglyoxal content in drinking coffee as a cytotoxic factor. J. Food Sci. 2010, 75, H167-H171.
13. Adams, C.J.; Manley-Harris, M.; Molan, P.C. The origin of methylglyoxal in New Zealand manuka (Leptospermum scoparium) honey. Carbohydr. Res. 2009, 344, 1050-1053.
14. Arrbias-Lorenzo, G.; Morales, F.J. Analysis, distribution, and dietary exposure of glyoxal and methylglyoxal in cookies and their relationship with other heat-induced contaminants. J. Agric. Food Chem. 2010, 58, 2966-2972.
15. De Revel, G.; Bertrand, A. A method for the detection of carbonyl compounds in wine: Glyoxal and methylglyoxal. J. Sci. Food Agric. 1993, 61, 267-272.
16. Barros, A.; Rodrigues, J.A.; Almeida, P.J.; Oliva-Teles, M.T. Determination of glyoxal, methylglyoxal and diacetyl in selected beer and wine by HPLC with UV spectrophotometric detection after derivatization with O-phenylendiamine. J. Liq. Chromatogr. Relat. Technol. 1999, 22, 2061-2069.
17. Espín, J.C.; García-Conesa, M.T.; Tomás-Barberán, F.A. Nutraceuticals: Facts and fiction. Phytochemistry 2007, 68, 2986-3008.
18. Murakamim, A. Modulation of protein quality control systems by food phytochemicals. J. Clin. Biochem. Nutr. 2013, 52, 215-227.
19. Aggarwal, B.B.; Bhardwaj, A.; Aggarwal, R.S.; Seeram, N.P.; Shishodia, S.; Takada, Y. Role of resveratrol in prevention and therapy of cancer: Preclinical and clinical studies. Anticancer Res. 2004, 24, 2783-2840.
20. Fernández-Mar, M.I.; Mateos, R.; García-Parrilla, M.C.; Puertas, B.; Cantos-Villar, E. Bioactive compounds in wine: Resveratrol, hydroxytyrosol and melatonin: A review. Food Chem. 2012, 130, 797-813.
21. Xu, Y.; Nie, L.; Yin, Y.G.; Tang, J.L.; Zhou, J.Y.; Li, D.D.; Zhou, S.W. Resveratrol protects against hyperglycemia-induced oxidative damage to mitochondria by activating SIRT1 in rat mesangial cells. Toxicol. Appl. Pharmacol. 2012, 259, 395-401.
22. Yu, W.; Fu, Y.C.; Wang, W. Cellular and molecular effects of resveratrol in health and disease. J. Cell Biochem. 2012, 113, 752-759.
23. 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.; et al. Resveratrol prevents β-cell dedifferentiation in nonhuman primates given a high-fat/high-sugar diet. Diabetes 2013, 62, 3500-3513.
24. Do, G.M.; Jung, U.J.; Park, H.J.; Kwon, E.Y.; Jeon, S.M.; McGregor, R.A.; Choi, M.S. Resveratrol ameliorates diabetesrelated 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.
25. Wu, L.; Zhou, L.; Lu, Y.; Zhang, J.; Jian, F.; Liu, Y.; Li, F.; Li, W.; Wang, X.; Li, G. Activation of SIRT1 protects pancreatic β cells against palmitate-induced dysfunction. Biochim. Biophys. Acta 2012, 1822, 1815-1825.
26. 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.
27. 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.; et al. Small molecule activators of SIRT1 as therapeutics for the treatment of type 2 diabetes. Nature 2007, 450, 712-716.
28. Cheng, A.S.; Cheng, Y.H.; Chang, T.L. Resveratrol protects RINm5F pancreatic cells from methylglyoxal-induced apoptosis. J. Funct. Foods 2013, 5, 1774-1783.
29. 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.
30. Rouse, M.; Younès, A.; Egan, J.M. Resveratrol and curcumin enhance pancreatic β-cell function by inhibiting phosphodiesterase activity. J. Endocrinol. 2014, 223, 107-117.
31. Szkudelski, T.; Szkudelska, K. Resveratrol and diabetes: From animal to human studies. Biochim. Biophys. Acta 2014, doi:10.1016/j.bbadis.2014.10.013.
32. Movahed, A.; Nabipour, I.; Louis, X.L.; Thandapilly, S.J.; Yu, L.; Kalantarhormozi, M.; Rekabpour, S.J.; Netticadan, T. Antihyperglycemic effects of short term resveratrol supplementation in type 2 diabetic patients. eCAM 2013, 2013, 851267-851278.
33. Rotches-Ribalta, M.; Andres-Lacueva, C.; Estruch, R.; Escribano, E.; Urpi-Sarda, M. Pharmocokinetics of resveratrol metabolic profile in healthy humans after moderate consumption of red wine and grape extract tablets. J. Pharm. Res. 2012, 66, 375-382.
34. Smoliga, J.M.; Blanchard, O. Enhancing the delivery of resveratrol in humans: If low bioavailability is the problem, what is the solution? Molecules 2014, 19, 17154-17172.
35. 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.; et al. SIRT1 is required for AMPK activation and the beneficial effects of resveratrol on mitochondrial function. Cell Metab. 2012, 15, 675-690.
36. Furimsky, A.; Green, C.; Sharp, E.; Cats, P.; Adjeu, A.; Parman, T.; Kapetanovic, I.; Weinshilboum, R.; Lyver, L. Effect of resveratrol on 17beta-estradiol sulfation by human hepatic and jejunal S9 and recombinant sulfotransferase 1E1. Drug Metab. Dispos. 2008, 36, 129-136.
37. Bahadoran, Z.; Mirmiran, P.; Azizi, F. Dietary polyphenols as potential nutraceuticals in management of diabetes: A review. J. Diabetes Metab. Disord. 2013, 12, 43.
38. Wang, X.J.; Hayes, J.D.; Henderson, C.J.; Wolf, C.R. Identification of retinoic acid as an inhibitor of transcription factor Nrf2 through activation of retinoic acid receptor α. Proc. Natl. Acad. Sci. USA 2007, 104, 19589-19594.
39. Cheng, A.S.; Cheng, Y.H.; Chiou, C.H.; Chang, T.L. Resveratrol upregulates Nrf2 expression to attenuate methylglyoxal-induced insulin resistance in Hep G2 cells. J. Agric. Food Chem. 2012, 60, 9180-9187.
40. Matthews, D.R.; Hosker, J.R.; Rudenski, A.S.; Naylor, B.A.; Treacher, D.F.; Turner, R.C. Homeostasis model assessment: Insulin resistance and β-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 1985, 28, 412-419.
41. Hsieh, M.J.; Lan, K.P.; Liu, H.Y.; Zhang, X.Z.; Lin, Y.F.; Chen, T.Y.; Chiou, H.L. Hepatitis C virus E2 protein involve in insulin resistance through an impairment of Akt/PKB and GSK3ß signaling in hepatocytes. BMC Gastroenterol. 2012, 12, doi:10.1186/1471-230X-12-74.
42. Kim, S.P.; Ellmerer, M.; Can Citters, G.W.; Bergman, R.N. Primacy of hepatic insulin resistance in the development of the metabolic syndrome induced by an isocaloric moderate-fat diet in the dog. Diabetes 2003, 52, 2453-2460.
43. Wang, N.; Zhang, D.L.; Mao, X.Q.; Zou, F.; Jin, H.; Ouyang, I.P. Astragalus polysaccharides decreased the expression of PTP1B through relieving ER stress induced activation of ATF6 in a rat model of type 2 diabetes. Mol. Cell Endocrinol. 2009, 307, 89-98.
44. Cheung, A.T.; Wang, J.; Ree, D.; Koll, J.K.; Bryer-Ash, M. Tumor necrosis factor-α induces hepatic insulin resistance in obese zucker (fa/fa) rats via interaction of leukocyte antigen-related tyrosine phosphatase with focal adhesion kinase. Diabetes 2000, 49, 810-819.
45. Lee, B.H.; Hsu, W.H.; Pan, T.M. Inhibitory effects of dioscorea polysaccharide on TNF-alpha-induced insulin resistance in mouse FL83B cells. J. Agric. Food Chem. 2011, 59, 5279-5285.
46. 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.
47. Kitada, M.; Koya, D. SIRT1 in type 2 diabetes: Mechanisms and therapeutic potential. Diabetes Metab. J. 2013, 37, 315-325.
48. Wu, C.C.; Hsu, M.C.; Hsieh, C.W.; Lin, J.B.; Lai, P.H.; Wung, B.S. Upregulation of heme oxygenase-1 by epigallocatechin-3-gallate via the phosphatidylinositol 3-kinase/Akt and ERK pathways. Life Sci. 2006, 78, 2889-2897.
49. Wu, C.H.; Huang, S.M.; Yen, G.C. Silymarin: A novel antioxidant with antiglycation and antiinflammatory properties in vitro and in vivo. Antioxid. Redox Signal. 2011, 14, 353-366.
50. Ankrah, N.A.; Appiah-Opong, R. Toxicity of low levels ofmethylglyoxal: Depletion of blood glutathione and adverse effect onglucose tolerance in mice. Toxicol. Lett. 1999, 109, 61-67.
51. Chartoumpekis, D.V.; Ziros, P.G.; Psyrogiannis, A.I.; Papavassiliou, A.G.; Kyriazopoulou, V.E.; Sykiotis, G.P.; Habeos, I.G. Nrf2 represses FGF21 during long-term high-fat diet-induced obesity in mice. Diabetes 2011, 60, 2465-2473.
52. Zheng, H.T.; Whitman, S.A.; Wu, W.; Wondrak, G.T.; Wong, P.K.; Fang, D. Therapeutic potential of Nrf2 activators in streptozotocin-induced diabetic nephropathy. Diabetes 2011, 60, 3055-3066.
53. Hsu, W.H.; Lee, B.H.; Chang, Y.Y.; Hsu, Y.W.; Pan, T.M. A novel natural Nrf2 activator with PPARgamma-agonist (monascin) attenuates the toxicity of methylglyoxal and hyperglycemia. Toxicol. Appl. Pharmacol. 2013, 272, 842-851.
54. Hsu, W.H.; Lee, B.H.; Li, C.H.; Hsu, Y.W.; Pan, T.M. Monascin and AITC attenuate methylglyoxal-induced PPARgamma phosphorylation and degradation through inhibition of the oxidative stress/PKC pathway depending on Nrf2 activation. J. Agric. Food Chem. 2013, 61, 5996-6006.
55. Lee, B.H.; Hsu, W.H.; Huang, T.; Chang, Y.Y.; Hsu, Y.W.; Pan, T.M. Effects of monascin on anti-inflammation mediated by Nrf2 activation in advanced glycation end product-treated THP-1 monocytes and methylglyoxal-treated Wistar rats. J. Agric. Food Chem. 2013, 61, 1288-1298.
56. Lee, B.H.; Hsu, W.H.; Hsu, Y.W.; Pan, T.M. Dimerumic acid attenuates receptor for advanced glycationend products signal to inhibit inflammation and diabetes mediated by Nrf2 activation and promotes methylglyoxal metabolism into D-lactic acid. Free Radic. Biol. Med. 2013, 60, 7-16.
57. Hsu, W.H.; Huang, Y.C.; Lee, B.H.; Hsu, Y.W.; Pan, T.M. The improvements of ankaflavin isolated from Monascus-fermented products on dyslipidemia in high-fat diet-induced hamster. J. Funct. Foods 2013, 5, 434-443.
58. Hsu, W.H.; Lee, B.H.; Chang, Y.Y.; Hsu, Y.W.; Pan, T.M. Ankaflavin, a novel Nrf2 activator for attenuating allergic airway inflammation. Free Radic. Biol. Med. 2012, 53, 1643-1651.
59. He, X.; Wang, L.; Szklarz, G.; Bi, Y.; Ma, Q. Resveratrol inhibits paraquat-induced oxidative stress and fibrogenic response by activating the nuclear factor erythroid 2-related factor 2 pathway. J. Pharmacol. Exp. Ther. 2012, 342, 81-90.
60. Palsamy, P.; Subramanian, S. Resveratrol protects diabetic kidney by attenuating hyperglycemia-mediated oxidative stress and renal inflammatory cytokines via Nrf2-Keap1 signaling. Biochim. Biophys. Acta 2011, 1812, 719-731.