Dietary (-)-epicatechin mitigates oxidative stress, NO metabolism alterations, and inflammation in renal cortex from fructose-fed rats

Free Radical Biology and Medicine

Volumn 90, Issue , 2016, Pages 35-46

  Prince, Paula D ^a   Lanzi, Cecilia Rodríguez ^b   Toblli, Jorge E ^c   Elesgaray, Rosana ^a   Oteiza, Patricia I ^d   Fraga, César G ^a,d   Galleano, Monica ^a  

^a UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^b UNIVERSIDAD NACIONAL DE CUYO   (Argentina)

^c HOSPITAL ALEMÁN   (Argentina)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

( ) Epicatechin; High fructose consumption; Inflammation; NADPH oxidase; Nitric oxide; Podocytes; Superoxide anion

Indexed keywords

3 NITROTYROSINE; AVIDIN; CREATININE; DRINKING WATER; ENDOTHELIAL NITRIC OXIDE SYNTHASE; EPICATECHIN; FRUCTOSE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 6; NEPHRIN; NITRIC OXIDE; SYNAPTOPODIN; THIOBARBITURIC ACID REACTIVE SUBSTANCE; TRIACYLGLYCEROL; TUMOR NECROSIS FACTOR ALPHA; URIC ACID; WT1 PROTEIN; CATECHIN; GLUTATHIONE PEROXIDASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DIET SUPPLEMENTATION; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; KIDNEY CORTEX; KIDNEY INJURY; MALE; NONHUMAN; OXIDATIVE STRESS; PODOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEINURIA; RAT; SYSTOLIC BLOOD PRESSURE; TRIACYLGLYCEROL BLOOD LEVEL; ANIMAL; DIETARY SUPPLEMENT; DRUG EFFECTS; INFLAMMATION; METABOLISM; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; CATECHIN; DIETARY SUPPLEMENTS; FRUCTOSE; GLUTATHIONE PEROXIDASE; INFLAMMATION; KIDNEY CORTEX; MALE; NF-KAPPA B; NITRIC OXIDE; OXIDATIVE STRESS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84947967500     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2015.11.009     Document Type: Article

References (57)

1. V. Jha, G. Garcia-Garcia, K. Iseki, Z. Li, S. Naicker, B. Plattner, and et al. Chronic kidney disease: global dimension and perspectives Lancet 382 2013 260 272 10.1016/S0140-6736(13)60687-X
2. J. Coresh, E. Selvin, L.A. Stevens, J. Manzi, J.W. Kusek, P. Eggers, and et al. Prevalence of chronic kidney disease in the United States J. Am. Med. Assoc. 298 2007 2038 2047 10.1001/jama.298.17.2038
3. R.C. Atkins The epidemiology of chronic kidney disease Kidney Int. Suppl. 2005 S14 S18 10.1111/j.1523-1755.2005.09403.x
4. L. Tappy, and K.-A. Lê Metabolic effects of fructose and the worldwide increase in obesity Physiol. Rev. 90 2010 23 46 10.1152/physrev.00019.2009
5. D.A. Shoham, R. Durazo-Arvizu, H. Kramer, A. Luke, S. Vupputuri, A. Kshirsagar, and et al. Sugary soda consumption and albuminuria: results from the National Health and Nutrition Examination Survey, 1999-2004 PLoS One 3 2008 e3431 10.1371/journal.pone.0003431
6. L.G. Sánchez-Lozada, E. Tapia, A. Jiménez, P. Bautista, M. Cristóbal, T. Nepomuceno, and et al. Fructose-induced metabolic syndrome is associated with glomerular hypertension and renal microvascular damage in rats Am. J. Physiol. Ren. Physiol. 292 2007 F423 F429 10.1152/ajprenal.00124.2006
7. C. Oudot, A.D. Lajoix, B. Jover, and C. Rugale Dietary sodium restriction prevents kidney damage in high fructose-fed rats Kidney Int. 83 2013 674 683 10.1038/ki.2012.478
8. C.G. Fraga, M.C. Litterio, P.D. Prince, V. Calabró, B. Piotrkowski, and M. Galleano Cocoa flavanols: effects on vascular nitric oxide and blood pressure J. Clin. Biochem. Nutr. 48 2011 63 67 10.3164/jcbn.11-010FR
9. C.G. Fraga Plant polyphenols: how to translate their in vitro antioxidant actions to in vivo conditions IUBMB Life 59 2007 308 315 10.1080/15216540701230529
10. P.J. Mink, C.G. Scrafford, L.M. Barraj, L. Harnack, C.-P. Hong, J.A. Nettleton, and et al. Flavonoid intake and cardiovascular disease mortality: a prospective study in postmenopausal women Am. J. Clin. Nutr. 85 2007 895 909
11. L. Hooper, P.A. Kroon, E.B. Rimm, J.S. Cohn, I. Harvey, K.A. Le Cornu, and et al. Flavonoids, flavonoid-rich foods, and cardiovascular risk: a meta-analysis of randomized controlled trials Am. J. Clin. Nutr. 88 2008 38 50
12. M. Galleano, V. Calabro, P.D. Prince, M.C. Litterio, B. Piotrkowski, M.A. Vazquez-Prieto, and et al. Flavonoids and metabolic syndrome Ann. NY Acad. Sci. 1259 2012 87 94 10.1111/j.1749-6632.2012.06511.x
13. H. Schroeter, C. Heiss, J.P.E. Spencer, C.L. Keen, J.R. Lupton, and H.H. Schmitz Recommending flavanols and procyanidins for cardiovascular health: current knowledge and future needs Mol. Asp. Med. 31 2010 546 557 10.1016/j.mam.2010.09.008
14. G. Williamson, and C. Manach Bioavailability and bioefficacy of polyphenols in humans. II. Review of 93 intervention studies Am. J. Clin. Nutr. 81 2005 243S 255S
15. M. Gómez-Guzmán, R. Jiménez, M. Sánchez, M. Romero, F. O'Valle, R. Lopez-Sepulveda, and et al. Chronic (-)-epicatechin improves vascular oxidative and inflammatory status but not hypertension in chronic nitric oxide-deficient rats Br. J. Nutr. 106 2011 1337 1348 10.1017/S0007114511004314
16. K. Tanabe, Y. Tamura, M.A. Lanaspa, M. Miyazaki, N. Suzuki, W. Sato, and et al. Epicatechin limits renal injury by mitochondrial protection in cisplatin nephropathy Am. J. Physiol. Ren. Physiol. 303 2012 F1264 F1274 10.1152/ajprenal.00227.2012
17. A. Bettaieb, M.A. Vazquez Prieto, C. Rodriguez Lanzi, R.M. Miatello, F.G. Haj, C.G. Fraga, and et al. (-)-Epicatechin mitigates high-fructose-associated insulin resistance by modulating redox signaling and endoplasmic reticulum stress Free. Radic. Biol. Med. 72 2014 247 256 10.1016/j.freeradbiomed.2014.04.011
18. A. Vogiatzoglou, A.A. Mulligan, M.A.H. Lentjes, R.N. Luben, J.P.E. Spencer, H. Schroeter, and et al. Flavonoid intake in European adults (18 to 64 years) PLoS One 10 2015 e0128132 10.1371/journal.pone.0128132
19. M.C. Litterio, M.A. Vazquez Prieto, A.M. Adamo, R. Elesgaray, P.I. Oteiza, M. Galleano, and et al. (-)-Epicatechin reduces blood pressure increase in high-fructose-fed rats: effects on the determinants of nitric oxide bioavailability J. Nutr. Biochem. 26 2015 745 751 10.1016/j.jnutbio.2015.02.004
20. L. Aimo, G.G. Mackenzie, A.H. Keenan, and P.I. Oteiza Gestational zinc deficiency affects the regulation of transcription factors AP-1, NF-κB and NFAT in fetal brain J. Nutr. Biochem. 21 2010 1069 1075 10.1016/j.jnutbio.2009.09.003
21. O.H. Lowry, N.J. Rosebrough, A.L. Farr, and R.J. Randall Protein measurement with the Folin phenol reagent J. Biol. Chem. 193 1951 265 275
22. C.G. Fraga, B.E. Leibovitz, and A.L. Tappel Halogenated compounds as inducers of lipid peroxidation in tissue slices Free. Radic. Biol. Med. 3 1987 119 123
23. J.-M. Li, S. Wheatcroft, L.M. Fan, M.T. Kearney, and A.M. Shah Opposing roles of p47phox in basal versus angiotensin II-stimulated alterations in vascular O2- production, vascular tone, and mitogen-activated protein kinase activation Circulation 109 2004 1307 1313 10.1161/01.CIR.0000118463.23388.B9
24. H. Aebi Catalase in vitro Methods Enzymol. 105 1984 121 126
25. B. Chance, H. Sies, and A. Boveris Hydroperoxide metabolism in mammalian organs Physiol. Rev. 59 1979 527 605
26. L. Flohé, and W.A. Günzler Assays of glutathione peroxidase Methods Enzymol. 105 1984 114 121
27. A. Boveris, C.G. Fraga, A.I. Varsavsky, and O.R. Koch Increased chemiluminescence and superoxide production in the liver of chronically ethanol-treated rats Arch. Biochem. Biophys. 227 1983 534 541
28. M.A. Costa, A. Loria, R. Elesgaray, A.M. Balaszczuk, and C. Arranz Role of nitric oxide pathway in hypotensive and renal effects of furosemide during extracellular volume expansion J. Hypertens. 22 2004 1561 1569
29. M.L. Schuman, M.S. Landa, J.E. Toblli, L.S. Peres Diaz, A.L. Alvarez, S. Finkielman, and et al. Cardiac thyrotropin-releasing hormone mediates left ventricular hypertrophy in spontaneously hypertensive rats Hypertension 57 2011 103 109 10.1161/HYPERTENSIONAHA.110.161265
30. J.E. Toblli, G. Cao, C. Rivas, and H. Kulaksiz Heart and iron deficiency anaemia in rats with renal insufficiency: the role of hepcidin Nephrol. Carlton Vic. 13 2008 636 645 10.1111/j.1440-1797.2008.01019.x
31. C. Zhao, P. Wang, X. Xiao, J. Chao, L. Chao, D.W. Wang, and et al. Gene therapy with human tissue kallikrein reduces hypertension and hyperinsulinemia in fructose-induced hypertensive rats Hypertension 42 2003 1026 1033 10.1161/01.HYP.0000097603.55404.35
32. T. Kizhner, and M.J. Werman Long-term fructose intake: biochemical consequences and altered renal histology in the male rat Metabolism 51 2002 1538 1547 10.1053/meta.2002.36306
33. C.-Y. Fan, M.-X. Wang, C.-X. Ge, X. Wang, J.-M. Li, and L.-D. Kong Betaine supplementation protects against high-fructose-induced renal injury in rats J. Nutr. Biochem. 25 2014 353 362 10.1016/j.jnutbio.2013.11.010
34. X.-Q. Ding, T.-T. Gu, W. Wang, L. Song, T.-Y. Chen, Q.-C. Xue, and et al. Curcumin protects against fructose-induced podocyte insulin signaling impairment through up-regulation of miR-206 Mol. Nutr. Food Res. 2015 10.1002/mnfr.201500370
35. Z. Hu, L. Ren, C. Wang, B. Liu, and G. Song Effect of chenodeoxycholic acid on fibrosis, inflammation and oxidative stress in kidney in high-fructose-fed Wistar rats Kidney Blood Press. Res. 36 2012 85 97 10.1159/000341485
36. P.-W. Cheng, W.-Y. Ho, Y.-T. Su, P.-J. Lu, B.-Z. Chen, W.-H. Cheng, and et al. Resveratrol decreases fructose-induced oxidative stress, mediated by NADPH oxidase via an AMPK-dependent mechanism Br. J. Pharmacol. 171 2014 2739 2750 10.1111/bph.12648
37. K.M. Yoo, I.-K. Hwang, and B. Moon Comparative flavonoids contents of selected herbs and associations of their radical scavenging activity with antiproliferative actions in V79-4 cells J. Food Sci. 74 2009 C419 C425 10.1111/j.1750-3841.2009.01191.x
38. B. Yang, A. Kotani, K. Arai, and F. Kusu Relationship of electrochemical oxidation of catechins on their antioxidant activity in microsomal lipid peroxidation Chem. Pharm. Bull. (Tokyo) 49 2001 747 751
39. M. Yoshikawa, K. Ninomiya, H. Shimoda, N. Nishida, and H. Matsuda Hepatoprotective and antioxidative properties of Salacia reticulata: preventive effects of phenolic constituents on CCl4-induced liver injury in mice Biol. Pharm. Bull. 25 2002 72 76
40. J.I. Ottaviani, T.Y. Momma, G.K. Kuhnle, C.L. Keen, and H. Schroeter Structurally related (-)-epicatechin metabolites in humans: assessment using de novo chemically synthesized authentic standards Free Radic. Biol. Med. 52 2012 1403 1412 10.1016/j.freeradbiomed.2011.12.010
41. L. Actis-Goretta, A. Lévèques, F. Giuffrida, F. Romanov-Michailidis, F. Viton, D. Barron, and et al. Elucidation of (-)-epicatechin metabolites after ingestion of chocolate by healthy humans Free Radic. Biol. Med. 53 2012 787 795 10.1016/j.freeradbiomed.2012.05.023
42. M. Galleano, S.V. Verstraeten, P.I. Oteiza, and C.G. Fraga Antioxidant actions of flavonoids: thermodynamic and kinetic analysis Arch. Biochem. Biophys. 501 2010 23 30 10.1016/j.abb.2010.04.005
43. S.V. Verstraeten, G.G. Mackenzie, P.I. Oteiza, and C.G. Fraga (-)-Epicatechin and related procyanidins modulate intracellular calcium and prevent oxidation in Jurkat T cells Free Radic. Res. 42 2008 864 872 10.1080/10715760802471452
44. M.A. Vazquez-Prieto, A. Bettaieb, F.G. Haj, C.G. Fraga, and P.I. Oteiza (-)-Epicatechin prevents TNFα-induced activation of signaling cascades involved in inflammation and insulin sensitivity in 3T3-L1 adipocytes Arch. Biochem. Biophys. 527 2012 113 118 10.1016/j.abb.2012.02.019
45. P.S. Gill, and C.S. Wilcox NADPH oxidases in the kidney Antioxid. Redox Signal. 8 2006 1597 1607 10.1089/ars.2006.8.1597
46. T.M. Buetler, A. Krauskopf, and U.T. Ruegg Role of superoxide as a signaling molecule News Physiol. Sci. Int. J. Physiol. Prod. Jointly Int. Union Physiol. Sci. Am. Physiol. Soc. 19 2004 120 123
47. C. Cao, Y. Leng, W. Huang, X. Liu, and D. Kufe Glutathione peroxidase 1 is regulated by the c-Abl and Arg tyrosine kinases J. Biol. Chem. 278 2003 39609 39614 10.1074/jbc.M305770200
48. J.S. Beckman, and W.H. Koppenol Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and ugly Am. J. Physiol. 271 1996 C1424 C1437
49. R. Radi Peroxynitrite, a stealthy biological oxidant J. Biol. Chem. 288 2013 26464 26472 10.1074/jbc.R113.472936
50. I. Ramirez-Sanchez, L. Maya, G. Ceballos, and F. Villarreal (-)-Epicatechin activation of endothelial cell endothelial nitric oxide synthase, nitric oxide, and related signaling pathways Hypertension 55 2010 1398 1405 10.1161/HYPERTENSIONAHA.109.147892
51. B. Piotrkowski, V. Calabró, M. Galleano, and C.G. Fraga (-)-Epicatechin prevents alterations in the metabolism of superoxide anion and nitric oxide in the hearts of l-NAME-treated rats Food Funct. 6 2015 155 161 10.1039/c4fo00554f
52. A. Sachse, and G. Wolf Angiotensin II-induced reactive oxygen species and the kidney J. Am. Soc. Nephrol. JASN 18 2007 2439 2446 10.1681/ASN.2007020149
53. M. Morrison, R. van der Heijden, P. Heeringa, E. Kaijzel, L. Verschuren, R. Blomhoff, and et al. Epicatechin attenuates atherosclerosis and exerts anti-inflammatory effects on diet-induced human-CRP and NFκB in vivo Atherosclerosis 233 2014 149 156 10.1016/j.atherosclerosis.2013.12.027
54. G.G. Mackenzie, F. Carrasquedo, J.M. Delfino, C.L. Keen, C.G. Fraga, and P.I. Oteiza Epicatechin, catechin, and dimeric procyanidins inhibit PMA-induced NF-kappaB activation at multiple steps in Jurkat T cells FASEB J. Off. Publ. Fed. Am. Soc. Exp. Biol. 18 2004 167 169 10.1096/fj.03-0402fje
55. G.G. Mackenzie, and P.I. Oteiza Modulation of transcription factor NF-kappaB in Hodgkin's lymphoma cell lines: effect of (-)-epicatechin Free Radic. Res. 40 2006 1086 1094 10.1080/10715760600788396
56. Y. Steffen, T. Schewe, and H. Sies (-)-Epicatechin elevates nitric oxide in endothelial cells via inhibition of NADPH oxidase Biochem. Biophys. Res. Commun. 359 2007 828 833 10.1016/j.bbrc.2007.05.200
57. W. Wang, X.-Q. Ding, T.-T. Gu, L. Song, J.-M. Li, Q.-C. Xue, and et al. Pterostilbene and allopurinol reduce fructose-induced podocyte oxidative stress and inflammation via microRNA-377 Free. Radic. Biol. Med. 83 2015 214 226 10.1016/j.freeradbiomed.2015.02.029