Inhibition of NADPH oxidase prevents advanced glycation end product-mediated damage in diabetic nephropathy through a protein kinase C-α-dependent pathway

Diabetes

Volumn 57, Issue 2, 2008, Pages 460-469

  Thallas Bonke, Vicki ^a   Thorpe, Suzanne R ^b   Coughlan, Melinda T ^a   Fukami, Kei ^a   Yap, Felicia Y T ^a   Sourris, Karly C ^a   Penfold, Sally A ^a   Bach, Leon A ^c   Cooper, Mark E ^a,c   Forbes, Josephine M ^a,c  

^a BAKER IDI HEART AND DIABETES INSTITUTE   (Australia)

^b UNIVERSITY OF SOUTH CAROLINA   (United States)

^c MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

3 [8 [(DIMETHYLAMINO)METHYL] 6,7,8,9 TETRAHYDROPYRIDO[1,2 A]INDOL 10 YL] 4 (1 METHYL 1H INDOL 3 YL) 1H PYRROLE 2,5 DIONE; ADVANCED GLYCATION END PRODUCT; ADVANCED GLYCATION END PRODUCT RECEPTOR; APOCYNIN; COLLAGEN; COLLAGEN TYPE 4; FIBRONECTIN; PROTEIN KINASE C ALPHA; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUPEROXIDE; VASCULOTROPIN; ACETOPHENONE DERIVATIVE; ADVANCED GLYCOSYLATION END PRODUCT RECEPTOR; ADVANCED GLYCOSYLATION END-PRODUCT RECEPTOR; DRUG DERIVATIVE; ENZYME INHIBITOR; IMMUNOGLOBULIN RECEPTOR; LYSINE; N(6) CARBOXYMETHYLLYSINE; N(6)-CARBOXYMETHYLLYSINE; UNCLASSIFIED DRUG;

ALBUMINURIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DIABETIC NEPHROPATHY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; EXTRACELLULAR MATRIX; FOLLOW UP; GLOMERULOSCLEROSIS; GLYCATION; MALE; MESANGIUM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN INTERACTION; PROTEIN LOCALIZATION; RAT; SPRAGUE DAWLEY RAT; STREPTOZOCIN DIABETES; ANIMAL; DRUG ANTAGONISM; DRUG EFFECT; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYMOLOGY; EXPERIMENTAL DIABETES MELLITUS; MESANGIUM; METABOLISM; PATHOLOGY; PHYSIOLOGY;

ACETOPHENONES; ANIMALS; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC NEPHROPATHIES; ENZYME INHIBITORS; ENZYME-LINKED IMMUNOSORBENT ASSAY; GLOMERULAR MESANGIUM; GLYCOSYLATION END PRODUCTS, ADVANCED; LYSINE; MALE; NADPH OXIDASE; PROTEIN KINASE C-ALPHA; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, IMMUNOLOGIC; SUPEROXIDES;

EID: 40749139536     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db07-1119     Document Type: Article

References (49)

1. Brownlee M: Biochemistry and molecular cell biology of diabetic complications. Nature 414:813-820, 2001
2. Hancock JT, Desikan R, Neill SJ: Role of reactive oxygen species in cell signalling pathways. Biochem Soc Trans 29:345-350, 2001
3. Gill PS, Wilcox CS: NADPH oxidases in the kidney. Antioxid Redox Signal 8:1597-1607, 2006
4. Fu MX, Wells-Knecht KJ, Blackledge JA, Lyons TJ, Thorpe SR, Baynes JW: Glycation, glycoxidation, and cross-linking of collagen by glucose: kinetics, mechanisms, and inhibition of late stages of the Maillard reaction. Diabetes 43:676-683, 1994
5. Soulis-Liparota T, Cooper M, Papazoglou D, Clarke B, Jerums G: Retardation by aminoguanidine of development of albuminuria, mesangial expansion, and tissue fluorescence in streptozocin-induced diabetic rat. Diabetes 40:1328-1334, 1991
6. Thallas-Bonke V, Lindschau C, Rizkalla B, Bach LA, Boner G, Meier M, Haller H, Cooper ME, Forbes JM: Attenuation of extracellular matrix accumulation in diabetic nephropathy by the advanced glycation end product cross-link breaker ALT-711 via a protein kinase C-α-dependent pathway. Diabetes 53:2921-2930, 2004
7. Vlassara H, Striker LJ, Teichberg S, Fuh H, Li YM, Steffes M: Advanced glycation end products induce glomerular sclerosis and albuminuria in normal rats. Proc Natl Acad SciU S A 91:11704-11708, 1994
8. Flyvbjerg A, Denner L, Schrijvers BF, Tilton RG, Mogensen TH, Paludan SR, Rasch R: Long-term renal effects of a neutralizing RAGE antibody in obese type 2 diabetic mice. Diabetes 53:166-172, 2004
9. Wendt TM, Tanji N, Guo J, Kislinger TR, Qu W, Lu Y, Bucciarelli LG, Rong LL, Moser B, Markowitz GS, Stein G, Bierhaus A, Liliensiek B, Arnold B, Nawroth PP, Stern DM, D'Agati VD, Schmidt AM: RAGE drives the development of glomerulosclerosis and implicates podocyte activation in the pathogenesis of diabetic nephropathy. Am J Pathol 162:1123-1137, 2003
10. Kislinger T, Fu C, Huber B, Qu W, Taguchi A, Du Yan S, Hofmann M, Yan SF, Pischetsrieder M, Stern D, Schmidt AM: N(epsilon)-(carboxymethyl)l- ysine adducts of proteins are ligands for receptor for advanced glycation end products that activate cell signaling pathways and modulate gene expression. J Biol Chem 274:31740-31749, 1999
11. Onozato ML, Tojo A, Goto A, Fujita T, Wilcox CS: Oxidative stress and nitric oxide synthase in rat diabetic nephropathy: effects of ACEI and ARB. Kidney Int 61:186-194, 2002
12. Li JM, Shah AM: ROS generation by nonphagocytic NADPH oxidase: potential relevance in diabetic nephropathy. J Am Soc Nephrol 14 (Suppl. 3):S221-S226, 2003
13. Matsunaga-Irie S, Maruyama T, Yamamoto Y, Motohashi Y, Hirose H, Shimada A, Murata M, Saruta T: Relation between development of ne-phropathy and the p22phox C242T and receptor for advanced glycation end product G1704T gene polymorphisms in type 2 diabetic patients. Diabetes Care 27:303-307, 2004
14. Hart BA, Simons JM: Metabolic activation of phenols by stimulated neutrophils: a concept for a selective type of anti-inflammatory drug. Biotechnol Ther 3:119-135, 1992
15. Meyer JW, Schmitt ME: A central role for the endothelial NADPH oxidase in atherosclerosis. FEBS Lett 472:1-4, 2000
16. Doublier S, Salvidio G, Lupia E, Ruotsalainen V, Verzola D, Deferrari G, Camussi G: Nephrin expression is reduced in human diabetic nephropathy: evidence for a distinct role for glycated albumin and angiotensin II. Diabetes 52:1023-1030, 2003
17. Lal MA, Brismar H, Eklof AC, Aperia A: Role of oxidative stress in advanced glycation end product-induced mesangial cell activation. Kidney Int 61:2006-2014, 2002
18. Abid MR, Tsai JC, Spokes KC, Deshpande SS, Irani K, Aird WC: Vascular endothelial growth factor induces manganese-superoxide dismutase expression in endothelial cells by a Rac1-regulated NADPH oxidase-dependent mechanism. Faseb J 15:2548-2550, 2001
19. Forbes JM, Thallas V, Thomas MC, Founds HW, Burns WC, Jerums G, Cooper ME: The breakdown of preexisting advanced glycation end products is associated with reduced renal fibrosis in experimental diabetes. Faseb J 17:1762-1764, 2003
20. Ido Y, Chang KC, Lejeune WS, Bjercke RJ, Reiser KM, Williamson JR, Tilton RG: Vascular dysfunction induced by AGE is mediated by VEGF via mechanisms involving reactive oxygen species, guanylate cyclase, and protein kinase C. Microcirculation 8:251-263, 2001
21. O'Brien RC, Allen TJ, Cooper ME, Bach L, Jerums G: Glomerular filtration rate in early experimental diabetes. J Diabet Complications 2:8-11, 1988
22. Cefalu WT, Wang ZQ, Bell-Farrow A, Kiger FD, Izlar C: Glycohemoglobin measured by automated affinity HPLC correlates with both short-term and long-term antecedent glycemia. Clin Chem 40:1317-1321, 1994
23. Fukami K, Ueda S, Yamagishi S, Kato S, Inagaki Y, Takeuchi M, Motomiya Y, Bucala R, Iida S, Tamaki K, Imaizumi T, Cooper ME, Okuda S: AGEs activate mesangial TGF-beta-Smad signaling via an angiotensin II type I receptor interaction. Kidney Int 66:2137-2147, 2004
24. Oldfield MD, Bach LA, Forbes JM, Nikolic-Paterson D, McRobert A, Thallas V, Atkins RC, Osicka T, Jerums G, Cooper ME: Advanced glycation end products cause epithelial-myofibroblast transdifferentiation via the receptor for advanced glycation end products (RAGE). J Clin Invest 108:1853-1863, 2001
25. Ji H, Pesce C, Zheng W, Kim J, Zhang Y, Menini S, Haywood JR, Sandberg K: Sex differences in renal injury and nitric oxide production in renal wrap hypertension. Am J Physiol Heart Circ Physiol 288:H43-H47, 2005
26. Forbes JM, Hewitson TD, Becker GJ, Jones CL: Ischemic acute renal failure: long-term histology of cell and matrix changes in the rat. Kidney Int 57:2375-2385, 2000
27. Coughlan MT, Thallas-Bonke V, Pete J, Long DM, Gasser A, Tong DC, Arnstein M, Thorpe SR, Cooper ME, Forbes JM: Combination therapy with the advanced glycation end product cross-link breaker, alagebrium, and angiotensin converting enzyme inhibitors in diabetes: synergy or redundancy? Endocrinology 148:886-895, 2007
28. Baines CP, Zhang J, Wang GW, Zheng YT, Xiu JX, Cardwell EM, Bolli R, Ping P: Mitochondrial PKCepsilon and MAPK form signaling modules in the murine heart: enhanced mitochondrial PKCepsilon-MAPK interactions and differential MAPK activation in PKCepsilon-induced cardioprotection. Circ Res 90:390-397, 2002
29. 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
30. 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
31. Heitzer T, Wenzel U, Hink U, Krollner D, Skatchkov M, Stahl RA, MacHarzina R, Brasen JH, Meinertz T, Munzel T: Increased NAD(P)H oxidase-mediated superoxide production in renovascular hypertension: evidence for an involvement of protein kinase C. Kidney Int 55:252-260, 1999
32. Bastian NR, Hibbs JB Jr.: Assembly and regulation ofNADPH oxidase and nitric oxide synthase. Curr Opin Immunol 6:131-139, 1994
33. Osicka TM, Yu Y, Lee V, Panagiotopoulos S, Kemp BE, Jerums G: Aminoguanidine and ramipril prevent diabetes-induced increases in protein kinase C activity in glomeruli, retina and mesenteric artery. Clin Sci (Lond) 100:249-257, 2001
34. Osicka TM, Yu Y, Panagiotopoulos S, Clavant SP, Kiriazis Z, Pike RN, Pratt LM, Russo LM, Kemp BE, Comper WD, Jerums G: Prevention of albumin-uria by aminoguanidine or ramipril in streptozotocin-induced diabetic rats is associated with the normalization of glomerular protein kinase C. Diabetes 49:87-93, 2000
35. Sheetz MJ, King GL: Molecular understanding of hyperglycemia's adverse effects for diabetic complications. JAMA 288:2579-2588, 2002
36. Meier M, Park JK, Boehne M, Elger M, Leitges M, Haller H, Menne J: Knockout of protein kinase C α protects against the development of albuminuria but not renal hypertrophy (Abstract). Diabetes 52:A50, 2003
37. Wu WS, Tsai RK, Chang CH, Wang S, Wu JR, Chang YX: Reactive oxygen species mediated sustained activation of protein kinase C alpha and extracellular signal-regulated kinase for migration of human hepatoma cell Hepg2. Mol Cancer Res 4:747-758, 2006
38. de Vriese AS, Tilton RG, Elger M, Stephan CC, Kriz W, Lameire NH: Antibodies against vascular endothelial growth factor improve early renal dysfunction in experimental diabetes. J Am, Soc Nephrol 12:993-1000, 2001
39. Sung SH, Ziyadeh FN, Wang A, Pyagay PE, Kanwar YS, Chen S: Blockade of vascular endothelial growth factor signaling ameliorates diabetic albu-minuria in mice. J Am Soc Nephrol 17:3093-3104, 2006
40. Lee BH, Park RW, Choi JY, Ryoo HM, Sohn KY, Kim IS: Stimulation of fibronectin synthesis through the protein kinase C signalling pathway in normal and transformed human lung fibroblasts. Biochem Mol Biol Int 39:895-904, 1996
41. Twigg SM, Joly AH, Chen MM, Tsubaki J, Kim HS, Hwa V, Oh Y, Rosenfeld RG: Connective tissue growth factor/IGF-binding protein-related protein-2 is a mediator in the induction of fibronectin by advanced glycosylation end-products in human dermal fibroblasts. Endocrinology 143:1260-1269, 2002
42. Pugliese G, Pricci F, Pugliese F, Mene P, Lenti L, Andreani D, Galli G, Casini A, Bianchi S, Rotella CM, et al.: Mechanisms of glucose-enhanced extracellular matrix accumulation in rat glomerular mesangial cells. Diabetes 43:478-490, 1994
43. Whiteside CI, Dlugosz JA: Mesangial cell protein kinase C isozyme activation in the diabetic milieu. Am J Physiol Renal Physiol 282:F975-F980, 2002
44. Lee HB, Yu MR, Yang Y, Jiang Z, Ha H: Reactive oxygen species-regulated signaling pathways in diabetic nephropathy. J Am Soc Nephrol 14 (Suppl. 3):S241-S245, 2003
45. Trachtman H, Futterweit S, Pine E, Mann J, Valderrama E: Chronic diabetic nephropathy: role of inducible nitric oxide synthase. Pediatr Nephrol 17:20-29, 2002
46. 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
47. Kelly DJ, Gilbert RE, Cox AJ, Soulis T, Jerums G, Cooper ME: Aminogua-nidine ameliorates overexpression of prosclerotic growth factors and collagen deposition in experimental diabetic nephropathy. J Am Soc Nephrol 12:2098-2107, 2001
48. Ha H, Lee HB: Oxidative stress in diabetic nephropathy: basic and clinical information. Curr Diab Rep 1:282-287, 2001
49. Rask-Madsen C, King GL: Mechanisms of disease: endothelial dysfunction in insulin resistance and diabetes. Nat Clin Pract Endocrinol Metab 3:46-56, 2007