Critical role of Nox4-based NADPH oxidase in glucose-induced oxidative stress in the kidney: Implications in type 2 diabetic nephropathy

American Journal of Physiology - Renal Physiology

Volumn 299, Issue 6, 2010, Pages

  Sedeek, M ^a   Callera, G ^a   Montezano, A ^a   Gutsol, A ^a   Heitz, F ^b   Szyndralewiez, C ^b   Page, P ^b   Kennedy, C R J ^a   Burns, K D ^a   Touyz, R M ^a   Hebert R L ^a  

^a OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^b GENKYOTEX SA   (Switzerland)

Author keywords

Diabetes; Hydrogen peroxide; Hyperglycemia; Nicotinamide adenine dinucleotide phosphate reduced form oxidase; Superoxide

Indexed keywords

2 (2 CHLOROPHENYL) 4 METHYL 5 (PYRIDIN 2 YLMETHYL) 1H PYRAZOLO[4,3 C]PYRIDINE 3,6(2H,5H) DIONE; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; ENZYME INHIBITOR; FIBRONECTIN; GK 136901; GLUCOSE; HYDROGEN PEROXIDE; LEVO GLUCOSE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN P22; PROTEIN P47; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 1; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; SMALL INTERFERING RNA; SUPEROXIDE; TRANSFORMING GROWTH FACTOR BETA1; TRANSFORMING GROWTH FACTOR BETA2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIABETIC NEPHROPATHY; ENZYME ACTIVATION; ENZYME INHIBITION; GENE EXPRESSION; KIDNEY CORTEX; KIDNEY FIBROSIS; KIDNEY MEDULLA; KIDNEY PROXIMAL TUBULE; MALE; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TISSUE CULTURE;

EID: 78649913769     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00028.2010     Document Type: Article

References (52)

1. Advani A, Gilbert RE, Thai K, Gow RM, Langham RG, Cox AJ, Connelly KA, Zhang Y, Herzenberg AM, Christensen PK, Pollock CA, Qi W, Tan SM, Parving HH, Kelly DJ. Expression, localization, and function of the thioredoxin system in diabetic nephropathy. J Am Soc Nephrol 20: 730-741, 2009.
2. Asaba K, Tojo A, Onozato ML, Goto A, Quinn MT, Fujita T, Wilcox CS. Effects of NADPH oxidase inhibitor in diabetic nephropathy. Kidney Int 67: 1890-1898, 2005.
3. Avogaro A, de Kreutzenberg SV, Fadini GP. Oxidative stress and vascular disease in diabetes: is the dichotomization of insulin signaling still valid? Free Radic Biol Med 44: 1209-1215, 2008.
4. Babior PH. NADPH oxidase. Curr Opin Immunol 16: 42-47, 2004.
5. Bedard K, Lardy B, Krause KH. NOX family NADPH oxidases: not just in mammals. Biochimie 89: 1107-1112, 2007.
6. Benter IF, Yousif MH, Dhaunsi GS, Kaur J, Chappell MC, Diz DI. Angiotensin-(1-7) prevents activation of NADPH oxidase and renal vascular dysfunction in diabetic hypertensive rats. Am J Nephrol 28: 25-33, 2008.
7. Block K, Gorin Y, Abboud HE. Subcellular localization of Nox4 and regulation in diabetes. Proc Natl Acad Sci USA 106: 14385-14390, 2009.
8. Brezniceanu ML, Liu F, Wei CC, Tran S, Sachetelli S, Zhang SL, Guo DF, Filep JG, Ingelfinger JR, Chan JS. Catalase overexpression attenuates angiotensinogen expression and apoptosis in diabetic mice. Kidney Int 71: 912-923, 2007.
9. Brosius 3rd FC. New insights into the mechanisms of fibrosis and sclerosis in diabetic nephropathy. Rev Endocr Metab Disord 9: 245-254, 2008.
10. Brosius 3rd FC, Alpers CE, Bottinger EP, Breyer MD, Coffman TM, Gurley SB, Harris RC, Kakoki M, Kretzler M, Leiter EH, Levi M, McIndoe RA, Sharma K, Smithies O, Susztak K, Takahashi N, Takahashi T. Mouse models of diabetic nephropathy. Animal Models of Diabetic Complications Consortium. J Am Soc Nephrol 20: 2503-2512, 2009.
11. Callera GE, Touyz RM, Tostes RC, Yogi A, He Y, Malkinson S, Schiffrin EL. Aldosterone activates vascular p38MAP kinase and NADPH oxidase via c-Src. Hypertension 45: 773-739, 2005.
12. Ding H, Hashem M, Triggle C. Increased oxidative stress in the streptozotocin-induced diabetic apoE-deficient mouse: changes in expression of NADPH oxidase subunits and eNOS. Eur J Pharmacol 561: 121-128, 2007.
13. Etoh T, Inoguchi T, Kakimoto M, Sonoda N, Kobayashi K, Kuroda J, Sumimoto H, Nawata H. Increased expression of NAD(P)H oxidase subunits, NOX4 and p22phox, in the kidney of streptozotocin-induced diabetic rats and its reversibility by interventive insulin treatment. Diabetologia 46: 1428-1437, 2003.
14. Forbes JM, Fukami K, Cooper ME. Diabetic nephropathy: where hemodynamics meets metabolism. Exp Clin Endocrinol Diabetes 115: 69-84, 2007.
15. Forbes JM, Coughlan MT, Cooper ME. Oxidative stress as a major culprit in kidney disease in diabetes. Diabetes 57: 1446-1454, 2008.
16. Fujii M, Inoguchi T, Maeda Y, Sasaki S, Sawada F, Saito R, Kobayashi K, Sumimoto H, Takayanagi R. Pitavastatin ameliorates albuminuria and renal mesangial expansion by downregulating NOX4 in db/db mice. Kidney Int 72: 473-480, 2007.
17. Geiszt M, Kopp JB, Várnai P, Leto TL. Identification of renox, an NAD(P)H oxidase in kidney. Proc Natl Acad Sci USA 97: 8010-8014, 2000.
18. Gill PS, Wilcox CS. NADPH oxidases in the kidney. Antioxid Redox Signal 8: 1597-1607, 2006.
19. Goettsch W, Muller G, Seebach J, Schnittler HJ, Morawietz H. Nox4 overexpression activates reactive oxygen species and p38MAPK in human endothelial cells. Biochem Biophys Res Commun 380: 355-360, 2009.
20. 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.
21. 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.
22. Gurley SB, Clare SE, Snow KP, Hu A, Meyer TW, Coffman TM. Impact of genetic background on nephropathy in diabetic mice. Am J Physiol Renal Physiol 290: F214-F222, 2006.
23. Hecker L, Vittal R, Jones T, Jagirdar R, Luckhardt TR, Horowitz JC, Pennathur S, Martinez FJ, Thannickal VJ. NADPH oxidase-4 mediates myofibroblast activation and fibrogenic responses to lung injury. Nat Med 15: 1077-1081, 2009.
24. Jerums G, Panagiotopoulos S, Premaratne E, MacIsaac RJ. Integrating albuminuria and GFR in the assessment of diabetic nephropathy. Nat Rev Nephrol 5: 397-406, 2009.
25. Kaneto H, Katakami N, Kawamori Miyatsuka T D, Sakamoto K, Matsuoka TA, Matsuhisa M, Yamasaki Y. Involvement of oxidative stress in the athogenesis of diabetes. Antioxid Redox Signal 9: 355-366, 2007.
26. Khavandi K, Greenstein AS, Sonoyama K, Withers S, Price A, Malik RA, Heagerty AM. Myogenic tone and small artery remodelling: insight into diabetic nephropathy. Nephrol Dial Transplant 24: 361-369, 2009.
27. Lassègue B, Clempus RE. Vascular NAD(P)H oxidases: specific features, expression, and regulation. Am J Physiol Regul Integr Comp Physiol 285: R277-R297, 2003.
28. Lee SJ, Kang JG, Ryu OH, Kim CS, Ihm SH, Choi MG, Yoo HJ, Kim DS, Kim TW. Effects of alpha-lipoic acid on transforming growth factor beta1-p38 mitogen-activated protein kinase-fibronectin pathway in diabetic nephropathy. Metabolism 58: 616-623, 2009.
29. Lena Serrander L, Cartier L, Bedard K, Banfi B, Lardy B, Plastre O, Sienkiewicz A, Fórró L, Schlegel W, Krause KH. NOX4 activity is determined by mRNA levels and reveals a unique pattern of ROS generation. Biochem J 406: 105-114, 2007.
30. Mahadev K, Motoshima H, Wu X, Ruddy JM, Arnold RS, Cheng G, Lambeth JD, Goldstein BJ. The NAD(P)H oxidase homolog Nox4 modulates insulin-stimulated generation of H2O2 and plays an integral role in insulin signal transduction. Mol Cell Biol 24: 1844-1854, 2004.
31. Maranchie JK, Zhan Y. Nox4 is critical for hypoxia-inducible factor 2-alpha transcriptional activity in von Hippel-Lindau-deficient renal cell carcinoma. Cancer Res 65: 9190-9193, 2005.
32. Orient A, Donkó A, Szabó A, Leto TL, Geiszt M. Novel sources of reactive oxygen species in the human body. Nephrol Dial Transplant 22: 1281-1288, 2007.
33. Page P, Orchard M, Fioraso-Cartier L, Mottironi B. Pyrazolo pyridine derivatives as NADPH oxidase inhibitors, Patent WO 2008/113856 A1. Genkyotex (Switzerland) 2008.
34. Palicz A, Foubert TR, Jesaitis AJ, Marodi L, McPhail LC. Phosphatidic acid and diacylglycerol directly activate NADPH oxidase by interacting with enzyme components. J Biol Chem 76: 3090-3097, 2001.
35. Quaggin SE, Coffman TM. Toward a mouse model of diabetic nephropathy: is endothelial nitric oxide synthase the missing link? J Am Soc Nephrol 18: 364-366, 2007.
36. Ritz E, Rychlik I, Locatelli F, Halimi S. End-stage renal failure in type 2 diabetes: a medical catastrophe of worldwide dimensions. Am J Kidney Dis 34: 795-808, 1999.
37. San Martín A, Griendling KK. Redox control of vascular smooth muscle migration. Antioxid Redox Signal 12: 625-640, 2010.
38. Sanchez AP, Sharma K. Transcription factors in the pathogenesis of diabetic nephropathy. Expert Rev Mol Med 11: e13, 2009.
39. Satoh M, Fujimoto S, Haruna Y, Arakawa S, Horike H, Komai N, Sasaki T, Tsujioka K, Makino H, Kashihara N. NAD(P)H oxidase and uncoupled nitric oxide synthase are major sources of glomerular superoxide in rats with experimental diabetic nephropathy. Am J Physiol Renal Physiol 288: F1144-F1152, 2005.
40. Sedeek M, Hébert RL, Kennedy CR, Burns KD, Touyz RM. Molecular mechanisms of hypertension: role of Nox family NADPH oxidases. Curr Opin Nephrol Hypertens 18: 122-127, 2009.
41. Shah SV, Baliga R, Rajapurkar M, Fonseca VA. Oxidants in chronic kidney disease. J Am Soc Nephrol 18: 16-28, 2007.
42. Shiose A, Kuroda J, Tsuruya K, Hirai M, Hirakata H, Naito S, Hattori M, Sakaki Y, Sumimoto H. A novel superoxide-producing NAD(P)H oxidase in kidney. J Biol Chem 276: 1417-1423, 2001.
43. Soldatos G, Cooper ME. Diabetic nephropathy: important pathophysiologic mechanisms. Diabetes Res Clin Pract 82: S75-S79, 2008.
44. Tabet F, Schiffrin EL, Callera GE, He Y, Yao G, Ostman A, Kappert K, Tonks NK, Touyz RM. Redox-sensitive signaling by angiotensin II involves oxidative inactivation and blunted phosphorylation of protein tyrosine phosphatase SHP-2 in vascular smooth muscle cells from SHR. Circ Res 103: 149-158, 2008.
45. Tan AL, Forbes JM, Cooper ME. AGE, RAGE, and ROS in diabetic nephropathy. Semin Nephrol 27: 130-143, 2007.
46. Thallas-Bonke V, Thorpe SR, Coughlan MT, Fukami K, Yap FY, Sourris KC, Penfold SA, Bach LA, Cooper ME, Forbes JM. Inhibition of NADPH oxidase prevents advanced glycation end product-mediated damage in diabetic nephropathy through a protein kinase C-alpha-dependent pathway. Diabetes 57: 460-469, 2008.
47. Tojo A, Asaba K, Onozato ML. Suppressing renal NADPH oxidase to treat diabetic nephropathy. Expert Opin Ther Targets 11: 1011-1018, 2007.
48. Touyz RM, Schiffrin EL. Ang II stimulated superoxide production is mediated via phospholipase D in human vascular smooth muscle cells. Hypertension 34: 976-982, 1999.
49. Xia L, Wang H, Goldberg HJ, Munk S, Fantus IG, Whiteside CI. Mesangial cell NADPH oxidase upregulation in high glucose is protein kinase C dependent and required for collagen IV expression. Am J Physiol Renal Physiol 290: F345-F356, 2006.
50. Yu L, Hébert MC, Zhang YE. TGF-beta receptor-activated p38 MAP kinase mediates Smad-independent TGF-beta responses. EMBO J 21: 3749-3759, 2002.
51. Yun MR, Im DS, Lee JS, Son SM, Sung SM, Bae SS, Kim CD. NAD(P)H oxidase-stimulating activity of serum from type 2 diabetic patients with retinopathy mediates enhanced endothelial expression of E-selectin. Life Sci 78: 2608-2614, 2006.
52. Zhang M, Fraser D, Phillips A. ERK, p38, and Smad signaling pathways differentially regulate transforming growth factor-beta1 autoinduction in proximal tubular epithelial cells. Am J Pathol 169: 1282-1293, 2006.