The antioxidant silybin prevents high glucose-induced oxidative stress and podocyte injury in vitro and in vivo

American Journal of Physiology - Renal Physiology

Volumn 305, Issue 5, 2013, Pages

  Khazim, Khaled ^b,c   Gorin, Yves ^b   Cavaglieri, Rita Cassia ^b   Abboud, Hanna E ^a,b   Fanti, Paolo ^a,b  

^a SOUTH TEXAS VETERANS HEALTH CARE SYSTEM   (United States)

^b Mays Cancer Center at UT Health San Antonio   (United States)

^c WESTERN GALILEE HOSPITAL   (Israel)

Author keywords

Albuminuria; Apoptosis; Diabetic nephropathy; NADPH oxidase; Phytochemicals

Indexed keywords

CELL DNA; GLUCOSE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; SILIBININ; SILYMARIN; SUPEROXIDE;

ALBUMINURIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DIABETIC NEPHROPATHY; GLUCOSE BLOOD LEVEL; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; INSULIN DEPENDENT DIABETES MELLITUS; MOUSE; NONHUMAN; OXIDATIVE STRESS; PODOCYTE; PODOCYTE INJURY; PRIORITY JOURNAL; PROTEIN EXPRESSION;

EID: 84883419205     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00028.2013     Document Type: Article

References (63)

1. Atkins RC, Briganti EM, Lewis JB, Hunsicker LG, Braden G, Champion de Crespigny PJ, DeFerrari G, Drury P, Locatelli F, Wiegmann TB, Lewis EJ. Proteinuria reduction and progression to renal failure in patients with type 2 diabetes mellitus and overt nephropathy. Am J Kidney Dis 45: 281-287, 2005.
2. Bannwart CF, Peracoli JC, Nakaira-Takahagi E, Peracoli MT. Inhibitory effect of silibinin on tumour necrosis factor-alpha and hydrogen peroxide production by human monocytes. Nat Prod Res 24: 1747-1757, 2010.
3. Berhane AM, Weil EJ, Knowler WC, Nelson RG, Hanson RL. Albuminuria and estimated glomerular filtration rate as predictors of diabetic end-stage renal disease and death. Clin J Am Soc Nephrol 6: 2444-2451, 2011.
4. Block K, Gorin Y. Aiding and abetting roles of NOX oxidases in cellular transformation. Nat Rev Cancer 12: 627-637, 2012.
5. Bokemeyer C, Fels LM, Dunn T, Voigt W, Gaedeke J, Schmoll HJ, Stolte H, Lentzen H. Silibinin protects against cisplatin-induced nephrotoxicity without compromising cisplatin or ifosfamide anti-tumour activity. Br J Cancer 74: 2036-2041, 1996.
6. Cosentino F, Hishikawa K, Katusic ZS, Luscher TF. High glucose increases nitric oxide synthase expression and superoxide anion generation in human aortic endothelial cells. Circulation 96: 25-28, 1997.
7. Cravedi P, Ruggenenti P, Remuzzi G. Proteinuria should be used as a surrogate in CKD. Nat Rev Nephrol 8: 301-306, 2012.
8. Das SK, Mukherjee S. Biochemical and immunological basis of silymarin effect, a milk thistle (Silybum marianum) against ethanol-induced oxidative damage. Toxicol Mech Methods 22: 409-413, 2012.
9. Dashti-Khavidaki S, Shahbazi F, Khalili H, Lessan-Pezeshki M. Potential renoprotective effects of silymarin against nephrotoxic drugs: a review of literature. J Pharm Pharm Sci 15: 112-123, 2012.
10. Day RT, Cavaglieri RC, Feliers D. Apelin retards the progression of diabetic nephropathy. Am J Physiol Renal Physiol 304: F788-F800, 2013.
11. de Zeeuw D, Ramjit D, Zhang Z, Ribeiro AB, Kurokawa K, Lash JP, Chan J, Remuzzi G, Brenner BM, Shahinfar S. Renal risk and renoprotection among ethnic groups with type 2 diabetic nephropathy: a post hoc analysis of RENAAL. Kidney Int 69: 1675-1682, 2006.
12. Deep G, Agarwal R. Chemopreventive efficacy of silymarin in skin and prostate cancer. Integr Cancer Ther 6: 130-145, 2007.
13. Dehmlow C, Erhard J, de Groot H. Inhibition of Kupffer cell functions as an explanation for the hepatoprotective properties of silibinin. Hepatology 23: 749-754, 1996.
14. Dehmlow C, Murawski N, de Groot H. Scavenging of reactive oxygen species and inhibition of arachidonic acid metabolism by silibinin in human cells. Life Sci 58: 1591-1600, 1996.
15. Eid AA, Ford BM, Block K, Kasinath BS, Gorin Y, Ghosh-Choudhury G, Barnes JL, Abboud HE. AMP-activated protein kinase (AMPK) negatively regulates Nox4-dependent activation of p53 and epithelial cell apoptosis in diabetes. J Biol Chem 285: 37503-37512, 2010.
16. Eid AA, Gorin Y, Fagg BM, Maalouf R, Barnes JL, Block K, Abboud HE. Mechanisms of podocyte injury in diabetes: role of cytochrome P450 and NADPH oxidases. Diabetes 58: 1201-1211, 2009.
17. Fallahzadeh MK, Dormanesh B, Sagheb MM, Roozbeh J, Vessal G, Pakfetrat M, Daneshbod Y, Kamali-Sarvestani E, Lankarani KB. Effect of addition of silymarin to renin-angiotensin system inhibitors on proteinuria in type 2 diabetic patients with overt nephropathy: a randomized, double-blind, placebo-controlled trial. Am J Kidney Dis 60: 896-903, 2012.
18. Forbes JM, Coughlan MT, Cooper ME. Oxidative stress as a major culprit in kidney disease in diabetes. Diabetes 57: 1446-1454, 2008.
19. Gaedeke J, Fels LM, Bokemeyer C, Mengs U, Stolte H, Lentzen H. Cisplatin nephrotoxicity and protection by silibinin. Nephrol Dial Transplant 11: 55-62, 1996.
20. Galluzzi L, Aaronson SA, Abrams J, Alnemri ES, Andrews DW, Baehrecke EH, Bazan NG, Blagosklonny MV, Blomgren K, Borner C, Bredesen DE, Brenner C, Castedo M, Cidlowski JA, Ciechanover A, Cohen GM, De Laurenzi V, De Maria R, Deshmukh M, Dynlacht BD, El-Deiry WS, Flavell RA, Fulda S, Garrido C, Golstein P, Gougeon ML, Green DR, Gronemeyer H, Hajnoczky G, Hardwick JM, Hengartner MO, Ichijo H, Jaattela M, Kepp O, Kimchi A, Klionsky DJ, Knight RA, Kornbluth S, Kumar S, Levine B, Lipton SA, Lugli E, Madeo F, Malomi W, Marine JC, Martin SJ, Medema JP, Mehlen P, Melino G, Moll UM, Morselli E, Nagata S, Nicholson DW, Nicotera P, Nunez G, Oren M, Penninger J, Pervaiz S, Peter ME, Piacentini M, Prehn JH, Puthalakath H, Rabinovich GA, Rizzuto R, Rodrigues CM, Rubinsztein DC, Rudel T, Scorrano L, Simon HU, Steller H, Tschopp J, Tsujimoto Y, Vandenabeele P, Vitale I, Vousden KH, Youle RJ, Yuan J, Zhivotovsky B, Kroemer G. Guidelines for the use and interpretation of assays for monitoring cell death in higher eukaryotes. Cell Death Differ 16: 1093-1107, 2009.
21. Gazak R, Walterova D, Kren V. Silybin and silymarin-new and emerging applications in medicine. Curr Med Chem 14: 315-338, 2007.
22. Gorin Y, Block K, Hernandez J, Bhandari B, Wagner B, Barnes JL, Abboud HE. Nox4 NAD(P)H oxidase mediates hypertrophy and fibronectin expression in the diabetic kidney. J Biol Chem 280: 39616-39626, 2005.
23. Gorin Y, Ricono JM, Kim NH, Bhandari B, Choudhury GG, Abboud HE. Nox4 mediates angiotensin II-induced activation of Akt/protein kinase B in mesangial cells. Am J Physiol Renal Physiol 285: F219-F229, 2003.
24. _ from p47phoxdependent NAD(P)H oxidases, leading to monocyte adhesion. J Biol Chem 278: 47291-47298, 2003.
25. Jeong DH, Lee GP, Jeong WI, Do SH, Yang HJ, Yuan DW, Park HY, Kim KJ, Jeong KS. Alterations of mast cells and TGF-beta1 on the silymarin treatment for CCl(4)-induced hepatic fibrosis. World J Gastroenterol 11: 1141-1148, 2005.
26. Jim B, Ghanta M, Qipo A, Fan Y, Chuang PY, Cohen HW, Abadi M, Thomas DB, He JC. Dysregulated nephrin in diabetic nephropathy of type 2 diabetes: a cross sectional study. PLoS One 7: e36041, 2012.
27. Kauntz H, Bousserouel S, Gosse F, Raul F. Silibinin triggers apoptotic signaling pathways and autophagic survival response in human colon adenocarcinoma cells and their derived metastatic cells. Apoptosis 16: 1042-1053, 2011.
28. Keane WF, Zhang Z, Lyle PA, Cooper ME, de Zeeuw D, Grunfeld JP, Lash JP, McGill JB, Mitch WE, Remuzzi G, Shahinfar S, Snapinn SM, Toto R, Brenner BM. Risk scores for predicting outcomes in patients with type 2 diabetes and nephropathy: the RENAAL study. Clin J Am Soc Nephrol 1: 761-767, 2006.
29. Laurindo FR, Fernandes DC, Santos CX. Assessment of superoxide production and NADPH oxidase activity by HPLC analysis of dihydroethidium oxidation products. Methods Enzymol 441: 237-260, 2008.
30. Li JJ, Kwak SJ, Jung DS, Kim JJ, Yoo TH, Ryu DR, Han SH, Choi HY, Lee JE, Moon SJ, Kim DK, Han DS, Kang SW. Podocyte biology in diabetic nephropathy. Kidney Int Suppl: S36-42, 2007.
31. Loguercio C, Festi D. Silybin and the liver: from basic research to clinical practice. World J Gastroenterol 17: 2288-2301, 2011.
32. Lu P, Mamiya T, Lu LL, Mouri A, Niwa M, Hiramatsu M, Zou LB, Nagai T, Ikejima T, Nabeshima T. Silibinin attenuates amyloid beta(25- 35) peptide-induced memory impairments: implication of inducible nitricoxide synthase and tumor necrosis factor-alpha in mice. J Pharmacol Exp Ther 331: 319-326, 2009.
33. Lu P, Mamiya T, Lu LL, Mouri A, Zou L, Nagai T, Hiramatsu M, Ikejima T, Nabeshima T. Silibinin prevents amyloid beta peptideinduced memory impairment and oxidative stress in mice. Br J Pharmacol 157: 1270-1277, 2009.
34. Menini S, Iacobini C, Oddi G, Ricci C, Simonelli P, Fallucca S, Grattarola M, Pugliese F, Pesce C, Pugliese G. Increased glomerular cell (podocyte) apoptosis in rats with streptozotocin-induced diabetes mellitus: role in the development of diabetic glomerular disease. Diabetologia 50: 2591-2599, 2007.
35. Meyer TW, Bennett PH, Nelson RG. Podocyte number predicts longterm urinary albumin excretion in Pima Indians with Type II diabetes and microalbuminuria. Diabetologia 42: 1341-1344, 1999.
36. Mochizuki T, Furuta S, Mitsushita J, Shang WH, Ito M, Yokoo Y, Yamaura M, Ishizone S, Nakayama J, Konagai A, Hirose K, Kiyosawa K, Kamata T. Inhibition of NADPH oxidase 4 activates apoptosis via the AKT/apoptosis signal-regulating kinase 1 pathway in pancreatic cancer PANC-1 cells. Oncogene 25: 3699-3707, 2006.
37. Mundlos S, Pelletier J, Darveau A, Bachmann M, Winterpacht A, Zabel B. Nuclear localization of the protein encoded by the Wilms' tumor gene WT1 in embryonic and adult tissues. Development 119: 1329-1341, 1993.
38. Muzes G, Deak G, Lang I, Nekam K, Gergely P, Feher J. Effect of the bioflavonoid silymarin on the in vitro activity and expression of superoxide dismutase (SOD) enzyme. Acta Physiol Hung 78: 3-9, 1991.
39. Navarro-Gonzalez JF, Mora-Fernandez C. The role of inflammatory cytokines in diabetic nephropathy. J Am Soc Nephrol 19: 433-442, 2008.
40. Nishikawa T, Edelstein D, Du XL, Yamagishi S, Matsumura T, Kaneda Y, Yorek MA, Beebe D, Oates PJ, Hammes HP, Giardino I, Brownlee M. Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature 404: 787-790, 2000.
41. Pagtalunan ME, Miller PL, Jumping-Eagle S, Nelson RG, Myers BD, Rennke HG, Coplon NS, Sun L, Meyer TW. Podocyte loss and progressive glomerular injury in type II diabetes. J Clin Invest 99: 342-348, 1997.
42. Prabu SM, Muthumani M. Silibinin ameliorates arsenic induced nephrotoxicity by abrogation of oxidative stress, inflammation and apoptosis in rats. Mol Biol Rep 39: 11201-11216, 2012.
43. Rasband WS. ImageJ. Bethesda, MD: National Institutes of Health, 1997-2012.
44. Rossing K, Christensen PK, Hovind P, Parving HH. Remission of nephrotic-range albuminuria reduces risk of end-stage renal disease and improves survival in type 2 diabetic patients. Diabetologia 48: 2241-2247, 2005.
45. Sedeek M, Callera G, Montezano A, Gutsol A, Heitz F, Szyndralewiez C, Page P, Kennedy CR, Burns KD, Touyz RM, Hebert RL. Critical role of Nox4-based NADPH oxidase in glucose-induced oxidative stress in the kidney: implications in type 2 diabetic nephropathy. Am J Physiol Renal Physiol 299: F1348-F1358, 2010.
46. Shankland SJ, Pippin JW, Reiser J, Mundel P. Podocytes in culture: past, present, and future. Kidney Int 72: 26-36, 2007.
47. Sharma K, McGowan TA. TGF-beta in diabetic kidney disease: role of novel signaling pathways. Cytokine Growth Factor Rev 11: 115-123, 2000.
48. Steffes MW, Schmidt D, McCrery R, Basgen JM. Glomerular cell number in normal subjects and in type 1 diabetic patients. Kidney Int 59: 2104-2113, 2001.
49. Su J, Li SJ, Chen ZH, Zeng CH, Zhou H, Li LS, Liu ZH. Evaluation of podocyte lesion in patients with diabetic nephropathy: Wilms' tumor-1 protein used as a podocyte marker. Diabetes Res Clin Pract 87: 167-175, 2010.
50. Susztak K, Raff AC, Schiffer M, Bottinger EP. Glucose-induced reactive oxygen species cause apoptosis of podocytes and podocyte depletion at the onset of diabetic nephropathy. Diabetes 55: 225-233, 2006.
51. Tiwari P, Kumar A, Balakrishnan S, Kushwaha HS, Mishra KP. Silibinin-induced apoptosis in MCF7 and T47D human breast carcinoma cells involves caspase-8 activation and mitochondrial pathway. Cancer Invest 29: 12-20, 2011.
52. Toklu HZ, Tunali Akbay T, Velioglu-Ogunc A, Ercan F, Gedik N, Keyer-Uysal M, Sener G. Silymarin, the antioxidant component of Silybum marianum, prevents sepsis-induced acute lung and brain injury. J Surg Res 145: 214-222, 2008.
53. Vaquero EC, Edderkaoui M, Pandol SJ, Gukovsky I, Gukovskaya AS. Reactive oxygen species produced by NAD(P)H oxidase inhibit apoptosis in pancreatic cancer cells. J Biol Chem 279: 34643-34654, 2004.
54. Varga Z, Ujhelyi L, Kiss A, Balla J, Czompa A, Antus S. Effect of silybin on phorbol myristate actetate-induced protein kinase C translocation, NADPH oxidase activity and apoptosis in human neutrophils. Phytomedicine 11: 206-212, 2004.
55. Vessal G, Akmali M, Najafi P, Moein MR, Sagheb MM. Silymarin and milk thistle extract may prevent the progression of diabetic nephropathy in streptozotocin-induced diabetic rats. Ren Fail 32: 733-739, 2010.
56. Wang YK, Hong YJ, Huang ZQ. Protective effects of silybin on human umbilical vein endothelial cell injury induced by H2O2 in vitro. Vascul Pharmacol 43: 198-206, 2005.
57. Wenzel S, Stolte H, Soose M. Effects of silibinin and antioxidants on high glucose-induced alterations of fibronectin turnover in human mesangial cell cultures. J Pharmacol Exp Therap 279: 1520-1526, 1996.
58. West IC. Radicals and oxidative stress in diabetes. Diabet Med 17: 171-180, 2000.
59. White KE, Bilous RW, Marshall SM, El Nahas M, Remuzzi G, Piras G, De Cosmo S, Viberti G. Podocyte number in normotensive type 1 diabetic patients with albuminuria. Diabetes 51: 3083-3089, 2002.
60. Wolf G, Chen S, Ziyadeh FN. From the periphery of the glomerular capillary wall toward the center of disease: podocyte injury comes of age in diabetic nephropathy. Diabetes 54: 1626-1634, 2005.
61. Wolf G, Ziyadeh FN. Cellular and molecular mechanisms of proteinuria in diabetic nephropathy. Nephron Physiol 106: p26-31, 2007.
62. Wu CH, Huang SM, Yen GC. Silymarin: a novel antioxidant with antiglycation and antiinflammatory properties in vitro and in vivo. Antioxid Redox Signal 14: 353-366, 2010.
63. Zheng S, Noonan WT, Metreveli NS, Coventry S, Kralik PM, Carlson EC, Epstein PN. Development of late-stage diabetic nephropathy in OVE26 diabetic mice. Diabetes 53: 3248-3257, 2004.