Resveratrol decreases fructose-induced oxidative stress, mediated by NADPH oxidase via an AMPK-dependent mechanism

British Journal of Pharmacology

Volumn 171, Issue 11, 2014, Pages 2739-2750

  Cheng, Pei Wen ^a   Ho, Wen Yu ^b   Su, Yu Ting ^c   Lu, Pei Jung ^d   Chen, Bo Zone ^a   Cheng, Wen Han ^a,e   Lu, Wen Hsien ^e   Sun, Gwo Ching ^d,f   Yeh, Tung Chen ^a,c   Hsiao, Michael ^g   Tseng, Ching Jiunn ^a,c,e,h  

^a KAOHSIUNG VETERANS GENERAL HOSPITAL   (Taiwan)

^b KAOHSIUNG MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^c NATIONAL SUN YAT SEN UNIVERSITY   (Taiwan)

^d NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^e NATIONAL YANG MING UNIVERSITY   (Taiwan)

^f YULI VETERANS HOSPITAL   (Taiwan)

^g GENOMICS RESEARCH CENTER   (Taiwan)

^h NATIONAL DEFENSE MEDICAL CENTER   (Taiwan)

Author keywords

AMPK; hypertension; nitrogen oxides; nucleus tractus solitarii; resveratrol

Indexed keywords

HYDROETHIDINE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; NITRIC OXIDE; PROTEIN P22; PROTEIN P67; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; RESVERATROL; SUPEROXIDE DISMUTASE; ANTIOXIDANT; COPPER ZINC SUPEROXIDE DISMUTASE; FRUCTOSE; MANGANESE SUPEROXIDE DISMUTASE; NEURONAL NITRIC OXIDE SYNTHASE; NITROGEN OXIDE; PROTEIN KINASE B; STILBENE DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; CHEMOPROPHYLAXIS; CONTROLLED STUDY; HEART PROTECTION; HYPERTENSION; IMMUNOBLOTTING; IN VIVO STUDY; MALE; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; OXYGEN CONSUMPTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN RNA BINDING; RAT; REAL TIME POLYMERASE CHAIN REACTION; SOLITARY TRACT NUCLEUS; SYSTOLIC BLOOD PRESSURE; ANIMAL; BLOOD PRESSURE; CEREBELLUM; CHEMICALLY INDUCED; DRUG EFFECTS; METABOLISM; PATHOPHYSIOLOGY; WISTAR KYOTO RAT;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; ANTIOXIDANTS; BLOOD PRESSURE; CEREBELLUM; FRUCTOSE; HYPERTENSION; MALE; NADPH OXIDASE; NITRIC OXIDE SYNTHASE TYPE I; NITROGEN OXIDES; OXIDATIVE STRESS; PROTO-ONCOGENE PROTEINS C-AKT; RATS, INBRED WKY; REACTIVE OXYGEN SPECIES; SOLITARY NUCLEUS; STILBENES; SUPEROXIDE DISMUTASE;

EID: 84900546063     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/bph.12648     Document Type: Article

References (51)

1. Alexander SPH, Benson HE, Faccenda E, Pawson AJ, Sharman, JL, Spedding M, Peters JA, Harmar AJ, and CGTP Collaborators (2013a). The Concise Guide to PHARMACOLOGY 2013/14: G protein-coupled receptors. Br J Pharmacol 170: 1459-1581.
2. Alexander SPH, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Spedding M, Peters JA, Harmar AJ, and CGTP Collaborators (2013b). The Concise Guide to PHARMACOLOGY 2013/14: Enzymes. Br J Pharmacol 170: 1797-1867.
3. Aller EE, Abete I, Astrup A, Martinez JA, van Baak MA, (2011). Starches, sugars and obesity. Nutrients 3: 341-369.
4. Baur JA, Sinclair DA, (2006). Therapeutic potential of resveratrol: the in vivo evidence. Nat Rev Drug Discov 5: 493-506.
5. Bavithra S, Selvakumar K, Krishnamoorthy G, Venkataraman P, Arunakaran J, (2013). Melatonin attenuates polychlorinated biphenyls induced apoptosis in the neuronal cells of cerebral cortex and cerebellum of adult male rats-in vivo. Environ Toxicol Pharmacol 36: 152-163.
6. Bendall JK, Rinze R, Adlam D, Tatham AL, de Bono J, Wilson N, et al. (2007). Endothelial Nox2 overexpression potentiates vascular oxidative stress and hemodynamic response to angiotensin II: studies in endothelial-targeted Nox2 transgenic mice. Circ Res 100: 1016-1025.
7. Bhatt SR, Lokhandwala MF, Banday AA, (2011). Resveratrol prevents endothelial nitric oxide synthase uncoupling and attenuates development of hypertension in spontaneously hypertensive rats. Eur J Pharmacol 667: 258-264.
8. Campese VM, Sindhu RK, Ye S, Bai Y, Vaziri ND, Jabbari B, (2007). Regional expression of NO synthase, NAD(P)H oxidase and superoxide dismutase in the rat brain. Brain Res 1134: 27-32.
9. Chan SH, Wang LL, Tseng HL, Chan JY, (2007). Upregulation of AT1 receptor gene on activation of protein kinase Cbeta/nicotinamide adenine dinucleotide diphosphate oxidase/ERK1/2/c-fos signaling cascade mediates long-term pressor effect of angiotensin II in rostral ventrolateral medulla. J Hypertens 25: 1845-1861.
10. Chan SH, Wu CA, Wu KL, Ho YH, Chang AY, Chan JY, (2009). Transcriptional upregulation of mitochondrial uncoupling protein 2 protects against oxidative stress-associated neurogenic hypertension. Circ Res 105: 886-896.
11. Chen Z, Peng IC, Sun W, Su MI, Hsu PH, Fu Y, et al. (2009). AMP-activated protein kinase functionally phosphorylates endothelial nitric oxide synthase Ser633. Circ Res 104: 496-505.
12. Cheng TH, Liu JC, Lin H, Shih NL, Chen YL, Huang MT, et al. (2004). Inhibitory effect of resveratrol on angiotensin II-induced cardiomyocyte hypertrophy. Naunyn Schmiedebergs Arch Pharmacol 369: 239-244.
13. Cheng WH, Lu PJ, Ho WY, Tung CS, Cheng PW, Hsiao M, et al. (2010). Angiotensin II inhibits neuronal nitric oxide synthase activation through the ERK1/2-RSK signaling pathway to modulate central control of blood pressure. Circ Res 106: 788-795.
14. Chong ZZ, Wang S, Shang YC, Maiese K, (2012). Targeting cardiovascular disease with novel SIRT1 pathways. Future Cardiol 8: 89-100.
15. Colombo SL, Moncada S, (2009). AMPKalpha1 regulates the antioxidant status of vascular endothelial cells. Biochem J 421: 163-169.
16. Dasgupta B, Milbrandt J, (2007). Resveratrol stimulates AMP kinase activity in neurons. Proc Natl Acad Sci U S A 104: 7217-7222.
17. Dimo T, Rakotonirina SV, Tan PV, Azay J, Dongo E, Cros G, (2002). Leaf methanol extract of Bidens pilosa prevents and attenuates the hypertension induced by high-fructose diet in Wistar rats. J Ethnopharmacol 83: 183-191.
18. Dong Y, Zhang M, Liang B, Xie Z, Zhao Z, Asfa S, et al. (2010). Reduction of AMP-activated protein kinase alpha2 increases endoplasmic reticulum stress and atherosclerosis in vivo. Circulation 121: 792-803.
19. Farina JP, Garcia ME, Alzamendi A, Giovambattista A, Marra CA, Spinedi E, et al. (2013). Antioxidant treatment prevents the development of fructose-induced abdominal adipose tissue dysfunction. Clin Sci (Lond) 125: 87-97.
20. Fisslthaler B, Fleming I, (2009). Activation and signaling by the AMP-activated protein kinase in endothelial cells. Circ Res 105: 114-127.
21. Gao L, Wang W, Li YL, Schultz HD, Liu D, Cornish KG, et al. (2004). Superoxide mediates sympathoexcitation in heart failure: roles of angiotensin II and NAD(P)H oxidase. Circ Res 95: 937-944.
22. Guglielmotto M, Aragno M, Tamagno E, Vercellinatto I, Visentin S, Medana C, et al. (2012). AGEs/RAGE complex upregulates BACE1 via NF-kappaB pathway activation. Neurobiol Aging 33: 196, e113-127.
23. Hardie DG, Salt IP, Hawley SA, Davies SP, (1999). AMP-activated protein kinase: an ultrasensitive system for monitoring cellular energy charge. Biochem J 338 (Pt 3): 717-722.
24. Hecker PA, Galvao TF, O'Shea KM, Brown BH, Henderson R Jr, Riggle H, et al. (2012). High-sugar intake does not exacerbate metabolic abnormalities or cardiac dysfunction in genetic cardiomyopathy. Nutrition 28: 520-526.
25. Ho WY, Lu PJ, Hsiao M, Hwang HR, Tseng YC, Yen MH, et al. (2008). Adenosine modulates cardiovascular functions through activation of extracellular signal-regulated kinases 1 and 2 and endothelial nitric oxide synthase in the nucleus tractus solitarii of rats. Circulation 117: 773-780.
26. Hughes KJ, Meares GP, Hansen PA, Corbett JA, (2011). FoxO1 and SIRT1 regulate beta-cell responses to nitric oxide. J Biol Chem 286: 8338-8348.
27. Ilkun O, Boudina S, (2013). cardiac dysfunction and oxidative stress in the metabolic syndrome: an update on antioxidant therapies. Curr Pharm Des 19: 4806-4817.
28. Kantzides A, Badoer E, (2005). nNOS-containing neurons in the hypothalamus and medulla project to the RVLM. Brain Res 1037: 25-34.
29. Kilkenny C, Browne W, Cuthill IC, Emerson M, Altman DG, (2010). Animal research: reporting in vivo experiments: the ARRIVE guidelines. Br J Pharmacol 160: 1577-1579.
30. Levine YC, Li GK, Michel T, (2007). Agonist-modulated regulation of AMP-activated protein kinase (AMPK) in endothelial cells. Evidence for an AMPK → Rac1 → Akt → endothelial nitric-oxide synthase pathway. J Biol Chem 282: 20351-20364.
31. Li Y, Cao Z, Zhu H, (2006). Upregulation of endogenous antioxidants and phase 2 enzymes by the red wine polyphenol, resveratrol in cultured aortic smooth muscle cells leads to cytoprotection against oxidative and electrophilic stress. Pharmacol Res 53: 6-15.
32. McGrath J, Drummond G, McLachlan E, Kilkenny C, Wainwright C, (2010). Guidelines for reporting experiments involving animals: the ARRIVE guidelines. Br J Pharmacol 160: 1573-1576.
33. Miyazaki R, Ichiki T, Hashimoto T, Inanaga K, Imayama I, Sadoshima J, et al. (2008). SIRT1, a longevity gene, downregulates angiotensin II type 1 receptor expression in vascular smooth muscle cells. Arterioscler Thromb Vasc Biol 28: 1263-1269.
34. Nozoe M, Hirooka Y, Koga Y, Sagara Y, Kishi T, Engelhardt JF, et al. (2007). Inhibition of Rac1-derived reactive oxygen species in nucleus tractus solitarius decreases blood pressure and heart rate in stroke-prone spontaneously hypertensive rats. Hypertension 50: 62-68.
35. Paravicini TM, Touyz RM, (2006). Redox signaling in hypertension. Cardiovasc Res 71: 247-258.
36. Paxinos G, Watson C, (2006). The Rat Brain in Stereotaxic Coordinates, 6th edn. London: Elsevier.
37. Pfluger PT, Herranz D, Velasco-Miguel S, Serrano M, Tschop MH, (2008). Sirt1 protects against high-fat diet-induced metabolic damage. Proc Natl Acad Sci U S A 105: 9793-9798.
38. Qiu X, Brown K, Hirschey MD, Verdin E, Chen D, (2010). Calorie restriction reduces oxidative stress by SIRT3-mediated SOD2 activation. Cell Metab 12: 662-667.
39. Quincozes-Santos A, Gottfried C, (2011). Resveratrol modulates astroglial functions: neuroprotective hypothesis. Ann N Y Acad Sci 1215: 72-78.
40. Rebollo A, Roglans N, Alegret M, Laguna JC, (2012). Way back for fructose and liver metabolism: bench side to molecular insights. World J Gastroenterol 18: 6552-6559.
41. Robb EL, Page MM, Wiens BE, Stuart JA, (2008a). Molecular mechanisms of oxidative stress resistance induced by resveratrol: specific and progressive induction of MnSOD. Biochem Biophys Res Commun 367: 406-412.
42. Robb EL, Winkelmolen L, Visanji N, Brotchie J, Stuart JA, (2008b). Dietary resveratrol administration increases MnSOD expression and activity in mouse brain. Biochem Biophys Res Commun 372: 254-259.
43. Sartoretto JL, Kalwa H, Pluth MD, Lippard SJ, Michel T, (2011). Hydrogen peroxide differentially modulates cardiac myocyte nitric oxide synthesis. Proc Natl Acad Sci U S A 108: 15792-15797.
44. Siemann EH, Creasy LL, (1992). Concentration of the phytoalexin resveratrol in wine. Am J Enol Vitic 43: 49-52.
45. Stapleton D, Mitchelhill KI, Gao G, Widmer J, Michell BJ, Teh T, et al. (1996). Mammalian AMP-activated protein kinase subfamily. J Biol Chem 271: 611-614.
46. Thandapilly SJ, Louis XL, Yang T, Stringer DM, Yu L, Zhang S, et al. (2011). Resveratrol prevents norepinephrine induced hypertrophy in adult rat cardiomyocytes, by activating NO-AMPK pathway. Eur J Pharmacol 668: 217-224.
47. Tran LT, Yuen VG, McNeill JH, (2009). The fructose-fed rat: a review on the mechanisms of fructose-induced insulin resistance and hypertension. Mol Cell Biochem 332: 145-159.
48. Wang S, Zhang M, Liang B, Xu J, Xie Z, Liu C, et al. (2010). AMPKalpha2 deletion causes aberrant expression and activation of NAD(P)H oxidase and consequent endothelial dysfunction in vivo: role of 26S proteasomes. Circ Res 106: 1117-1128.
49. Wang X, Wang Q, Sun Z, (2012). Normal IgG downregulates the intracellular superoxide level and attenuates migration and permeability in human aortic endothelial cells isolated from a hypertensive patient. Hypertension 60: 818-826.
50. Wautier MP, Chappey O, Corda S, Stern DM, Schmidt AM, Wautier JL, (2001). Activation of NADPH oxidase by AGE links oxidant stress to altered gene expression via RAGE. Am J Physiol Endocrinol Metab 280: E685-E694.
51. Zhang Y, Croft KD, Mori TA, Schyvens CG, McKenzie KU, Whitworth JA, (2004). The antioxidant tempol prevents and partially reverses dexamethasone-induced hypertension in the rat. Am J Hypertens 17: 260-265.