Protective effects of resveratrol against streptozotocin-induced diabetes in rats by modulation of visfatin/sirtuin-1 pathway and glucose transporters

International Journal of Food Sciences and Nutrition

Volumn 66, Issue 3, 2015, Pages 314-320

  Gencoglu, Hasan ^a   Tuzcu, Mehmet ^a   Hayirli, Armagan ^b   Sahin, Kazim ^c  

^a FIRAT UNIVERSITY   (Turkey)

^b ATATÜRK UNIVERSITY   (Turkey)

^c FIRAT UNIVERSITY   (Turkey)

Author keywords

Oxidative stress; Polyphenols; Preventive medicine; Systemic diseases

Indexed keywords

RATTUS;

ANTIDIABETIC AGENT; ANTIOXIDANT; GLUCOSE BLOOD LEVEL; GLUCOSE TRANSPORTER; MALONALDEHYDE; NICOTINAMIDE PHOSPHORIBOSYLTRANSFERASE; PLANT EXTRACT; POLYPHENOL; RESVERATROL; SIRTUIN 1; STILBENE DERIVATIVE;

ANIMAL; BLOOD; DIABETES MELLITUS, EXPERIMENTAL; DIET SUPPLEMENTATION; DRUG EFFECTS; GLUCOSE BLOOD LEVEL; HYPERGLYCEMIA; MALE; METABOLISM; OXIDATIVE STRESS; PANCREAS; PHYTOTHERAPY; SKELETAL MUSCLE; WEIGHT REDUCTION; WISTAR RAT;

ANIMALS; ANTIOXIDANTS; BLOOD GLUCOSE; DIABETES MELLITUS, EXPERIMENTAL; DIETARY SUPPLEMENTS; GLUCOSE TRANSPORT PROTEINS, FACILITATIVE; HYPERGLYCEMIA; HYPOGLYCEMIC AGENTS; MALE; MALONDIALDEHYDE; MUSCLE, SKELETAL; NICOTINAMIDE PHOSPHORIBOSYLTRANSFERASE; OXIDATIVE STRESS; PANCREAS; PHYTOTHERAPY; PLANT EXTRACTS; POLYPHENOLS; RATS, WISTAR; SIRTUIN 1; STILBENES; WEIGHT LOSS;

EID: 84929915831     PISSN: 09637486     EISSN: 14653478     Source Type: Journal    
DOI: 10.3109/09637486.2014.1003534     Document Type: Article

References (69)

1. Acquaviva R, Russo A, Campisi A, Sorrenti V, di Giacomo C, Barcellona ML, Avitabile M, Vanella A. 2002. Antioxidant activity and protective effect on DNA cleavage of resveratrol. J Food Sci 67:137-141.
2. Adeghate E. 2008. Visfatin: structure, function and relation to diabetes mellitus and other dysfunctions. Curr Med Chem 15:1851-1862.
3. Aggarwal BB, Bhardwaj A, Aggarwal RS, Seeram NP, Shishodia S, Takada Y. 2004. Role of resveratrol in prevention and therapy of cancer: preclinical and clinical studies. Anticancer Res 24:2783-2840.
4. Akar F, Pektas MB, Tufan C, Soylemez S, Sepici A, Ulus AT, Gokalp B, et al. 2011. Resveratrol shows vasoprotective effect reducing oxidative stress without affecting metabolic disturbances in insulin-dependent diabetes of rabbits. Cardiovasc Drugs Ther 25:119-131.
5. Akar F, Uludag O, Aydn A, Aytekin YA, Elbeg S, Tuzcu M, Sahin K. 2012. High-fructose corn syrup causes vascular dysfunction associated with metabolic disturbance in rats: protective effect of resveratrol. Food Chem Toxicol 50:2135-2141.
6. Akiyama S, Katsumata SI, Suzuki K, Ishimi Y, Wu J, Uehara M. 2010. Dietary hesperidin exerts hypoglycemic and hypolipidemic effects in streptozotocin-induced marginal type 1 diabetic rats. J Clin Biochem Nutr 46:87-92.
7. Ates O, Cayli SR, Yucel N, Altinoz E, Kocak A, Durak MA, Turkoz Y, et al. 2007. Central nervous system protection by resveratrol in streptozotocin-induced diabetic rats. J Clin Neurosci 14:256-260.
8. Bagul PK, Middela H, Matapally S, Padiya R, Bastia T, Madhusudana K, Reddy BR, et al. 2012. Attenuation of insulin resistance: metabolic syndrome and hepatic oxidative stress by resveratrol in fructose-fed rats. Pharmacol Res 66:260-268.
9. Baur JA, Sinclair DA. 2006. Therapeutic potential of resveratrol: the in vivo evidence. Nat Rev Drug Discov 6:493-506.
10. Bayramoglu A, Bayramoglu G, Senturk H. 2013. Lycopene partially reverses symptoms of diabetes in rats with streptozotocin-induced diabetes. J Med Food 16:128-132.
11. Bishnoi M, Bosgraaf CA, Abooj M, Zhong L, Premkumar LS. 2011. Streptozotocin-induced early thermal hyperalgesia is independent of glycemic state of rats: role of transient receptor potential vanilloid 1(TRPV1) and inflammatory mediators. Mol Pain 7:52-63.
12. Bonnefont-Rousselot D. 2004. The role of antioxidant micronutrients in the prevention of diabetic complications. Treat Endocrinol 3:41-52.
13. Chang CC, Chang CY, Huang JP, Hung LM. 2012. Effect of resveratrol on oxidative and inflammatory stress in liver and spleen of streptozotocin-induced type 1 diabetic rats. Chin J Physiol 55:192-201.
14. Chen H, Liu X, Chen H, Cao J, Zhang L, Hu X, Wang J. 2013. Role of SIRT1 and AMPK in mesenchymal stem cells differentiation. Ageing Res Rev 13:55-64.
15. Chi TC, Chen WP, Chi TL, Kuo TF, Lee SS, Cheng JT, Su MJ. 2007. Phosphatidylinositol-3-kinase is involved in the antihyperglycemic effect induced by resveratrol in streptozotocin-induced diabetic rats. Life Sci 80:1713-1720.
16. Cline GW, Petersen KF, Krssak M, Shen J, Hundal RS, Trajanoski Z, Inzucchi S, et al. 1999. Impaired glucose transport as a cause of decreased insulin-stimulated muscle glycogen synthesis in type 2 diabetes. N Engl J Med 341:240-246.
17. Crandall JP, Oram V, Trandafirescu G, Reid M, Kishore P, Hawkins M, Cohen HW, et al. 2012. Pilot study of resveratrol in older adults with impaired glucose tolerance. J Gerontol A Biol Sci Med Sci 12: 1307-1312.
18. Cushman SW, Wardzala LJ. 1980. Potential mechanism of insulin action on glucose transport in the isolated rat adipose cell. Apparent translocation of intracellular transport systems to the plasma membrane. J Biol Chem 255:4758-4762.
19. Deng JY, Hsieh PS, Huang JP, Lu LS, Hung LM. 2008. Activation of estrogen receptor is crucial for resveratrol-stimulating muscular glucose uptake via both insulin-dependent and-independent pathways. Diabetes 57:1814-1823.
20. Ding SY, Shen ZF, Chen YT, Sun SJ, Liu Q, Xie MZ. 2005. Pioglitazone can ameliorate insulin resistance in low-dose streptozotocin and high sucrose-fat diet induced obese rats. Acta Pharmacol Sin 26:575-580.
21. Do GM, Jung UJ, Park HJ, Kwon EY, Jeon SM, McGregor RA, Choi MS. 2012. 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 56:1282-1291.
22. Eseberri I, Lasa A, Churruca I, Portillo MP. 2013. Resveratrol metabolites modify apdipokine expression and secretion in 3T3-L1 pre-adipocytes and manure adipocytes. PLoS One 8:e63918.
23. Farombi EO, Shrotriya S, Na HK, Kim SH, Surh YJ. 2008. Curcumin attenuates dimethylnitrosamine-induced liver injury in rats through Nrf2-mediated induction of heme oxygenase-1. Food Chem Toxicol 46:1279-1287.
24. Fukuhara A, Matsuda M, Nishizawa M, Segawa K, Tanaka M, Kishimoto K, Matsuki Y, et al. 2005. Visfatin: a protein secreted by visceral fat that mimics the effects of insulin. Science 307:426-430.
25. Hirotani Y, Ikeda T, Yamamoto K, Kurokawa N. 2007. Effects of hachimi-jio-gan (ba-wei-di-huang-wan) on hyperglycemia in streptozotocin-induced diabetic rats. Biol Pharm Bull 30:1015-1020.
26. Imai S, Kiess W. 2009. Therapeutic potential of SIRT1 and NAMPTmediated NAD biosynthesis in type 2 diabetes. Front Biosci 14: 2983-2995.
27. Jang M, Cai L, Udeani GO, Slowing KV, Thomas CF, Beecher CW, Fong HH, et al. 1997. Cancer chemopreventive activity of resveratrol. A natural product derived from grapes. Science 275:218-220.
28. Karatepe M. 2004. Simultaneous determination of ascorbic acid and free malondialdehyde in human serum by HPLC-UV. LC GC N Am 22: 362-365.
29. Kitada M, Kume S, Imaizumi N, Koya D. 2011. Resveratrol improves oxidative stress and protects against diabetic nephropathy through normalization of Mn-SOD dysfunction in AMPK/SIRT1-independent pathway. Diabetes 60:634-643.
30. Knight CM, Gutierrez-Juarez R, Lam TK, Arrieta-Cruz I, Huang L, Schwartz G, Barzilai N, et al. 2011. Mediobasal hypothalamic SIRT1 is essential for resveratrol's effects on insulin action in rats. Diabetes 60: 2691-2700.
31. Ku CR, Lee HJ, Kim SK, Lee EY, Lee MK, Lee EJ. 2012. Resveratrol prevents streptozotocin-induced diabetes by inhibiting the apoptosis of pancreatic b-cell and the cleavage of poly (ADP-ribose) polymerase. Endocrinol J 59:103-109.
32. Lagouge M, Argmann C, Gerhart-Hines Z, Meziane H, Lerin C, Daussin F, Messadeq N, et al. 2006. Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1 alpha. Cell 127:1109-1122.
33. Martinez J, Moreno JJ. 2000. Effect of resveratrol, a natural polyphenolic compound, on reactive oxygen species and prostaglandin production. Biochem Pharmacol 59:865-870.
34. Marty N, Dallaporta M, Thorens B. 2007. Brain glucose sensing. counter regulation, and energy homeostasis. Physiology (Bethesda) 22: 241-251.
35. Melloul D, Marshak S, Cerasi E. 2002. Regulation of insulin gene transcription. Diabetologia 45:309-326.
36. Milne JC, Lambert PD, Schenk S, Carney DP, Smith JJ, Gagne DJ, Jin L, et al. 2007. Small molecule activators of SIRT1 as therapeutics for the treatment of type 2 diabetes. Nature 450:712-716.
37. Mulakayala C, Babajan B, Madhusudana P, Anuradha CM, Rao RM, Nune RP, Manna SK, et al. 2013. Synthesis and evaluation of resveratrol derivatives as new chemical entities for cancer. J Mol Graph Model 4:43-54.
38. Negi G, Kumar A, Sharma SS. 2011. Melatonin modulates neuroinflammation and oxidative stress in experimental diabetic neuropathy: effects on NF-kappaB and Nrf2 cascades. J Pineal Res 50:124-131.
39. Opara EC. 2002. Oxidative stress. micronutrients. diabetes mellitus and its complications. J R Soc Promot Health 122:28-34.
40. Orimo M, Minamino T, Miyauchi H, Tateno K, Okada S, Moriya J, Komuro I. 2009. Protective role of SIRT1 in diabetic vascular dysfunction. Arterioscler Thromb Vasc Biol 29:889-894.
41. Oyedemi S, Koekemoer T, Bradley G, van de Venter M, Afolayan A. 2013. In vitro anti-hyperglycemia properties of the aqueous stem bark extract from Strychnos henningsii (Gilg). Int J Diabetes Dev Ctries 33: 120-127.
42. Palsamy P, Subramanian S. 2008. Resveratrol, a natural phytoalexin, normalizes hyperglycemia in streptozotocin-nicotinamide induced experimental diabetic rats. Biomed Pharmacother 62:598-605.
43. Palsamy P, Subramanian S. 2011. Resveratrol protects diabetic kidney by attenuating hyperglycemia-mediated oxidative stress and renal inflammatory cytokines via Nrf2-Keap1 signaling. Biochim Biophys Acta 1812:719-731.
44. Price NL, Gomes AP, Ling AJ, Duarte FV, Martin-Montalvo A, North BJ, Agarwal B, et al. 2012. SIRT1 is required for AMPK activation and the beneficial effects of resveratrol on mitochondrial function. Cell Metab 15:675-690.
45. Revollo JR, Körner A, Mills KF, Satoh A, Wang T, Garten A, Dasgupta B, et al. 2007. Nampt/PBEF/Visfatin regulates insulin secretion in beta cells as a systemic NAD biosynthetic enzyme. Cell Metab 6: 363-375.
46. Roghani M, Baluchnejadmojarad T. 2010. Mechanisms underlying vascular effect of chronic resveratrol in streptozotocin-diabetic rats. Phytother Res 2:148-154.
47. Saddi-Rosa P, Viana de Oliveira CS, Crispim F, Giuffrida FM, de Lima VC, Vieira JG, Doria A, et al. 2013. Association of circulating levels of nicotinamide phosphoribosyltransferase (NAMPT/Visfatin) and of a frequent polymorphism in the promoter of the NAMPT gene with coronary artery disease in diabetic and non-diabetic subjects. Cardiovasc Diabetol 12:119-126.
48. Sahin K, Tuzcu M, Orhan C, Gencoglu H, Ulas M, Atalay M, Sahin N, et al. 2012. The effects of chromium picolinate and chromium histidinate administration on Nf-kb and Nrf2/HO-1 pathway in the brain of diabetic rats. Biol Trace Elem Res 150:291-296.
49. Schmatz R, Mazzanti CM, Spanevello R, Stefanello N, Gutierres J, Maldonado PA, Correâ M, et al. 2009a. Ectonucleotidase and acetylcholinesterase activities in synaptosomes from the cerebral cortex of streptozotocin-induced diabetic rats and treated with resveratrol. Brain Res Bull 80:371-376.
50. Schmatz R, Schetinger MR, Spanevello RM, Mazzanti CM, Stefanello N, Maldonado PA, Gutierres J, Correâ Mde C, et al. 2009b. Effects of resveratrol on nucleotide degrading enzymes in streptozotocin-induced diabetic rats. Life Sci 84:345-350.
51. Sellamuthu PS, Muniappan BP, Perumal SM, Kandasamy M. 2009. Antihyperglycemic effect of mangiferin in streptozotocin induced diabetic rats. J Health Sci 55:206-214.
52. Sgambato A, Ardito R, Faraglia B, Boninsegna A, Wolf FI, Cittadini A. 2001. Resveratrol, a natural phenolic compound, inhibits cell proliferation and prevents oxidative DNA damage. Mutat Res 496:171-180.
53. Sharma M, Gupta YK. 2002. Chronic treatment with transresveratrol prevents intracerebroventricular streptozotocin induced cognitive impairment and oxidative stress in rats. Life Sci 71:2489-2498.
54. Sharma S, Anjaneyulu M, Kulkarni SK, Chopra K. 2006. Resveratrol, a polyphenolic phytoalexin, attenuates diabetic nephropathy in rats. Pharmacology 76:69-75.
55. Sies H. 1997. Oxidative stress: oxidants and antioxidants. Exp Physiol 82: 291-295.
56. Silan C. 2008. The effects of chronic resveratrol treatment on vascular responsiveness of streptozotocin-induced diabetic rats. Biol Pharm Bull 31:897-902.
57. Statistical Analysis System (SAS). 2002. User's guide statistics, version 9.Cary (NC): SAS Inst. Inc.
58. Stenbit AE, Tsao TS, Li J, Burcelin R, Geenen DL, Factor SM, Houseknecht K, et al. 1997. GLUT4 heterozygous knockout mice develop muscle insulin resistance and diabetes. Nat Med 3:1096-1101.
59. Su HC, Hung LM, Chen JK. 2006. Resveratrol, a red wine antioxidant, possesses an insulin-like effect in streptozotocin-induced diabetic rats. Am J Physiol Endocrinol Metab 290:1339-1346.
60. Suzuki I, Kono T. 1980. Evidence that insulin causes translocation of glucose transport activity to the plasma membrane from an intracellular storage site. Proc Natl Acad Sci USA 77:2542-2545.
61. Tanaka T, Nabeshima Y. 2007. Nampt/PBEF/Visfatin: a new player in beta cell physiology and in metabolic diseases Cell Metab 6:341-343.
62. Turan B, Tuncay E, Vassort G. 2012. Resveratrol and diabetic cardiac function: focus on recent in vitro and in vivo studies. J Bioenerg Biomembr 44:281-296.
63. Vetterli L, Brun T, Giovannoni L, Bosco D, Maechler P. 2011. Resveratrol potentiates glucose-stimulated insulin secretion in INS-1E beta-cells and human islets through a SIRT1-dependent mechanism. J Biol Chem 286:6049-6060.
64. Visioli F, Borsani L, Gali C. 2000. Diet and prevention of coronary heart disease: the potential role of phytochemicals. Cardiovasc Res 47: 419-425.
65. Wenzel E, Somoza V. 2005. Metabolism and bioavailability of transresveratrol. Mol Nutr Food Res 49:472-481.
66. Wild S, Roglic G, Green A, Sicree R, King H. 2004. Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care 27:1047-1053.
67. Yar AS, Menevse S, Alp E. 2011. The effects of resveratrol on cyclooxygenase-1 and-2, nuclear factor kappa beta, matrix metalloproteinase-9, and sirtuin 1 mRNA expression in hearts of streptozotocin-induced diabetic rats. Genet Mol Res 10:2962-2975.
68. Yoh K, Hirayama A, Ishizaki K, Yamada A, Takeuchi M, Yamagishi S, Morito N, et al. 2008. Hyperglycemia induces oxidative and nitrosative stress and increases renal functional impairment in Nrf2-deficient mice. Genes Cells 13:1159-1170.
69. Zhu W, Chen S, Li Z, Zhao X, Li W, Sun Y, Zhang Z, et al. 2014. Effects and mechanisms of resveratrol on the amelioration of oxidative stress and hepatic steatosis in KKAy mice. Nutr Metab (Lond) 12:11-35.