Renoprotective effects of a novel Nox1/4 inhibitor in a mouse model of type 2 diabetes

Clinical Science

Volumn 124, Issue 3, 2013, Pages 191-202

  Sedeek, Mona ^a   Gutsol, Alex ^a   Montezano, Augusto C ^a   Burger, Dylan ^a   Nguyen Dinh Cat, Aurelie ^a   Kennedy, Chris R J ^a   Burns, Kevin D ^a   Cooper, Mark E ^b   Jandeleit Dahm, Karin ^b   Page, Patrick ^c   Szyndralewiez, Cedric ^c   Heitz, Freddy ^c   Hebert, Richard L ^a   Touyz, Rhian M ^a,d  

^a OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^b BAKER IDI HEART AND DIABETES INSTITUTE   (Australia)

^c GENKYOTEX SA   (Switzerland)

^d UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

db db mouse; Diabetes; Kidney; NADPH oxidase; NOX inhibitor; Oxidative stress

Indexed keywords

BIOLOGICAL MARKER; COPPER ZINC SUPEROXIDE DISMUTASE; FIBRONECTIN; GKT 136901; GLUCOSE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; OXIDOREDUCTASE INHIBITOR; PROCOLLAGEN; PROTECTIVE AGENT; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 1; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; STRESS ACTIVATED PROTEIN KINASE; THIOBARBITURIC ACID REACTIVE SUBSTANCE; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; VASCULAR CELL ADHESION MOLECULE 1; 2 (2 CHLOROPHENYL) 4 METHYL 5 (PYRIDIN 2 YLMETHYL) 1H PYRAZOLO(4,3 C)PYRIDINE 3,6(2H,5H) DIONE; 2-(2-CHLOROPHENYL)-4-METHYL-5-(PYRIDIN-2-YLMETHYL)-1H-PYRAZOLO(4,3-C)PYRIDINE-3,6(2H,5H)-DIONE; NOX4 PROTEIN, MOUSE; OXIDOREDUCTASE; PYRAZOLE DERIVATIVE; PYRIDONE DERIVATIVE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUPEROXIDE DISMUTASE;

ALBUMINURIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; CONTROLLED STUDY; DIABETIC NEPHROPATHY; GENE EXPRESSION; GLUCOSE BLOOD LEVEL; GLYCEMIC CONTROL; HISTOPATHOLOGY; HYPERGLYCEMIA; KIDNEY INJURY; MALE; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RENAL PROTECTION; ANIMAL; BLOOD; BLOOD PRESSURE; BODY WEIGHT; C57BL MOUSE; DISEASE MODEL; DRUG ANTAGONISM; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; KIDNEY; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; URINE; WESTERN BLOTTING;

ALBUMINURIA; ANIMALS; BLOOD GLUCOSE; BLOOD PRESSURE; BLOTTING, WESTERN; BODY WEIGHT; DIABETES MELLITUS, TYPE 2; DIABETIC NEPHROPATHIES; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; KIDNEY; MALE; MICE; MICE, INBRED C57BL; MITOGEN-ACTIVATED PROTEIN KINASES; NADH, NADPH OXIDOREDUCTASES; NADPH OXIDASE; PYRAZOLES; PYRIDONES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SUPEROXIDE DISMUTASE; THIOBARBITURIC ACID REACTIVE SUBSTANCES; TRANSFORMING GROWTH FACTOR BETA; VASCULAR CELL ADHESION MOLECULE-1;

EID: 84871819023     PISSN: 01435221     EISSN: None     Source Type: Journal    
DOI: 10.1042/CS20120330     Document Type: Article

References (54)

1. Ritz, E., Rychlik, I., Locatelli, F. and Halimi, S. (1999) End-stage renal failure in type 2 diabetes: a medical catastrophe of worldwide dimensions. Am. J. Kidney Dis. 34, 795-808
2. Morales, A. (2009) A better future for children with type 1 diabetes: Review of the conclusions from the diabetes control and complications trial and the epidemiology of diabetes interventions and complications study. J. Ark. Med. Soc. 106, 90-93
3. Macisaac, R. J. and Jerums, G. (2011) Diabetic kidney disease with and without albuminuria. Curr. Opin. Nephrol. Hypertens. 20, 246-257
4. Fornoni, A., Ijaz, A., Tejada, T. and Lenz, O. (2008) Role of inflammation in diabetic nephropathy. Curr. Diabetes Rev. 4, 10-07
5. Vallon, V. (2011) The proximal tubule in the pathophysiology of the diabetic kidney. Am. J. Physiol. Regul. Integr. Comp. Physiol. 300, R1009-R1022
6. Soldatos, G. and Cooper, M. E. (2008) Diabetic nephropathy: important pathophysiologic mechanisms. Diabetes Res. Clin. Pract. 82, S75-S79
7. Ramasamy, R., Yan, S. F. and Schmidt, A. M. (2011) Receptor for AGE (RAGE): signaling mechanisms in the pathogenesis of diabetes and its complications. Ann. N.Y. Acad. Sci. 1243, 88-102
8. Forbes, J. M., Coughlan, M. T. and Cooper, M. E. (2008) Oxidative stress as a major culprit in kidney disease in diabetes. Diabetes 57, 1446-1454
9. Wei, W., Liu, Q., Tan, Y., Liu, L., Li, X. and Cai, L. (2009) Oxidative stress, diabetes, and diabetic complications. Hemoglobin 33, 370-377
10. Tan, A. L., Forbes, J. M. and Cooper, M. E. (2007) AGE, RAGE, and ROS in diabetic nephropathy. Semin. Nephrol. 27, 130-143
11. Shah, S. V., Baliga, R., Rajapurkar, M. and Fonseca, V. A. (2007) Oxidants in chronic kidney disease. J. Am. Soc. Nephrol. 18, 16-28
12. de Haan, J. B. (2011) Nrf2 activators as attractive therapeutics for diabetic nephropathy. Diabetes 60, 2683-2684
13. Takayanagi, R., Inoguchi, T. and Ohnaka, K. (2011) Clinical and experimental evidence for oxidative stress as an exacerbating factor of diabetes mellitus. J. Clin. Biochem. Nutr. 48, 72-77
14. Cvetkovíc, T., Mitíc, B., Lazarevíc, G., Vlahovíc, P., Antíc, S. and Stefanovíc, V. (2009) Oxidative stress parameters as possible urine markers in patients with diabetic nephropathy. J. Diabetes Complications 23, 337-342
15. Pergola, P. E., Raskin, P., Toto, R. D., Meyer, C. J., Huff, J. W., Grossman, E. B., Krauth, M., Ruiz, S., Audhya, P., Christ-Schmidt, H. et al. (2011) BEAM study investigators. Bardoxolone methyl and kidney function in CKD with type 2 diabetes. N. Engl. J. Med. 365, 327-336
16. Thannickal, V. J. and Fanburg, B. L. (2000) Reactive oxygen species in cell signalling. Am. J. Physiol. Lung Cell Mol. Physiol. 279, L1005-L1028
17. Al Ghouleh, I., Khoo, N. K., Knaus, U. G., Griendling, K. K., Touyz, R. M., Thannickal, V. J., Barchowsky, A., Nauseef, W. M., Kelley, E. E., Bauer, P. M. et al. (2011) Oxidases and peroxidases in cardiovascular and lung disease: new concepts in reactive oxygen species signaling. Free Radical Biol. Med. 51, 1271-1288
18. Jay, D., Hitomi, H. and Griendling, K. K (2006) Oxidative stress and diabetic cardiovascular complications. Free Radical Biol. Med. 40, 183-192
19. Asaba, K., Tojo, A., Onozato, M. L., Goto, A., Quinn, M. T., Fujita, T. and Wilcox, C. S. (2005) Effects of NADPH oxidase inhibitor in diabetic nephropathy. Kidney Int. 67, 1890-1898
20. Bedard, K. and Krause, K. H. (2007) The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol. Rev. 87, 245-313
21. Touyz, R. M. and Briones, A. M. (2011) Reactive oxygen species and vascular biology: implications in human hypertension. Hypertens. Res. 34, 5-14
22. Gill, P. S. and Wilcox, C. S. (2006) NADPH oxidases in the kidney. Antioxid Redox Signaling 8, 1597-1607
23. Shiose, A., Kuroda, J., Tsuruya, K., Hirai, M., Hirakata, H., Naito, S., Hattori, M., Sakaki, Y. and Sumimoto, H. (2001) A novel superoxide-producing) NAD(P)H oxidase in kidney. J. Biol. Chem. 276, 1417-1423
24. Sedeek, M., Callera, G., Montezano, A., Gutsol, A., Heitz, F., Szyndralewiez, C., Page, P., Kennedy, C. R., Burns, K. D., Touyz, R. M. et al. (2010) 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
25. Touyz, R. M., Deschepper, C., Park, J. B., He, G., Chen, X., Neves, M. F., Virdis, A. and Schiffrin, E. L. (2002) Inhibition of mitogen-activated protein/extracellular-signal-regulated kinase improves endothelial function and attenuates Ang II-induced contractility of mesenteric resistance arteries from spontaneously hypertensive rats. J. Hypertens. 20, 1127-1134
26. Callera, G. E., Tostes, R. C., Yogi, A., Montezano, A. C. and Touyz, R. M. (2006) Endothelin-1-induced oxidative stress in DOCA-salt hypertension involves NADPH-oxidase-independent mechanisms. Clin. Sci. 110, 243-253
27. Tervaert, T. W., Mooyaart, A. L., Amann, K., Cohen, A. H., Cook, H. T., Drachenberg, C. B., Ferrario, F., Fogo, A. B., Haas, M., de Heer, E. et al. (2010) Pathologic classification of diabetic nephropathy. J. Am. Soc. Nephrol. 21, 556-563
28. Dikalov, S., Griendling, K. K. and Harrison, D. G. (2007) Measurement of reactive oxygen species in cardiovascular studies. Hypertension 49, 717-727
29. Laurindo, F. R., Fernandes, D. C. and Santos, C. X. (2008) Assessment of superoxide production and NADPH oxidase activity by HPLC analysis of dihydroethidium oxidation products. Methods Enzymol. 441, 237-260
30. Xu, M., Dai, D. Z. and Dai, Y. (2009) Normalizing NADPH oxidase contributes to attenuating diabetic nephropathy by the dual endothelin receptor antagonist CPU0213 in rats. Am. J. Nephrol. 29, 252-256
31. Tojo, A., Asaba, K. and Onozato, M. L. (2007) Suppressing renal NADPH oxidase to treat diabetic nephropathy. Expert Opin. Ther. Targets. 11, 1011-1018
32. Nam, S. M., Lee, M. Y., Koh, J. H., Park, J. H., Shin, J. Y., Shin, Y. G., Koh, S. B., Lee, E. Y. and Chung, C. H. (2009) Effects of NADPH oxidase inhibitor on diabetic nephropathy in OLETF rats: the role of reducing oxidative stress in its protective property. Diabetes Res. Clin. Pract. 83, 176-182
33. Ahmad, A., Mondello, S., Di Paola, R., Mazzon, E., Esposito, E., Catania, M. A., Italiano, D., Mondello, P., Aloisi, C. and Cuzzocrea, S. (2011) Protective effect of apocynin, a NADPH-oxidase inhibitor, against contrast-induced nephropathy in the diabetic rats: a comparison with n-acetylcysteine. Chem.-Biol. Interact. 189, 119-126
34. Alpers, C. E. and Hudkins, K. L. (2011) Mouse models of diabetic nephropathy. Curr. Opin. Nephrol. Hypertens. 20, 278-284
35. Brosius, III, F. C., Alpers, C. E., Bottinger, E. P., Breyer, M. D., Coffman, T. M., Gurley, S. B., Harris, R. C., Kakoki, M., Kretzler, M., Leiter, E. H. et al. (2009) Animal models of diabetic complications consortium. Mouse models of diabetic nephropathy. J. Am. Soc. Nephrol. 20, 2503-2512
36. Ninichuk, V., Kulkarni, O., Clauss, S. and Anders, H. J. (2007) Tubular atrophy, interstitial fibrosis, and inflammation in type 2 diabetic db/db mice. An accelerated model of advanced diabetic nephropathy. Eur. J. Med. Res. 12, 351-355
37. Fu, Y., Zhang, Y., Wang, Z., Wang, L., Wei, X., Zhang, B., Wen, Z., Fang, H., Pang, Q. and Yi, F. (2010) Regulation of NADPH oxidase activity is associated with miRNA-25-mediated NOX4 expression in experimental diabetic nephropathy. Am. J. Nephrol. 32, 581-589
38. Kantharidis, P., Wang, B., Carew, R. M. and Lan, H. Y. (2011) Diabetes complications: the microRNA perspective. Diabetes 60, 1832-1837
39. Aronson, D. (2008) Hyperglycemia and the pathobiology of diabetic complications. Adv. Cardiol. 45, 1-16
40. Maalouf, R. M., Eid, A. A., Gorin, Y. C., Block, K., Escobar, G. P., Bailey, S. and Abboud, H. E. (2012) Nox4-derived reactive oxygen species mediate cardiomyocyte injury in early type 1 diabetes. Am. J. Physiol. Cell Physiol. 302, C597-C604
41. Block, K., Gorin, Y. and Abboud, H. E. (2009) Subcellular localization of Nox4 and regulation in diabetes. Proc. Natl. Acad. Sci. U.S.A. 106, 14385-14390
42. phox homologues nox1 and nox4. Free Radical Biol. Med. 39, 381-391
43. phox (CYBA) and glutamate cysteine ligase catalytic subunit (GCLC) and renal disease in patients with type 1 diabetes mellitus. BMC Med. Genet. 12, 129
44. Souza-Smith, F. M., Katz, P. S., Trask, A. J., Stewart, J. A. Jr., Lord, K. C., Varner, K. J., Vassallo, D. V. and Lucchesi, P. A. (2011) Mesenteric resistance arteries in type 2 diabetic db/db mice undergo outward remodeling. PLoS ONE 6, e23337
45. Thallas-Bonke, V., Coughlan, M. T., Bach, L. A., Cooper, M. E. and Forbes, J. M. (2010) Preserv-ation of kidney function with combined inhibition of NADPH oxidase and angiotensin-converting enzyme in diabetic nephropathy. Am. J. Nephrol. 32, 73-82
46. Winiarska, K., Grabowski, M. and Rogacki, M. K. (2011) Inhibition of renal gluconeogenesis contributes to hypoglycaemic action of NADPH oxidase inhibitor, apocynin. Chem.-Biol. Interact. 189, 119-126
47. Guichard, C., Moreau, R., Pessayre, D., Epperson, T. K. and Krause, K. H. (2008) NOX family NADPH oxidases in liver and in pancreatic islets: a role in the metabolic syndrome and diabetes? Biochem. Soc. Trans. 36, 920-929
48. Sedeek, M., Hebert, R. L., Kennedy, C. R., Burns, K. D. and Touyz, R. M. (2009) Molecular mechanisms of hypertension: role of Nox family NADPH oxidases. Curr. Opin. Nephrol. Hypertens. 18, 122-127
49. Lambeth J.D. (2007) Nox enzymes, ROS, and chronic disease: an example of antagonistic pleiotropy. Free Radical Biol. Med. 43, 332-347
50. DeRubertis, F. R., Craven, P. A., Melhem, M. F. and Salah, E. M. (2004) Attenuation of renal injury in db/db mice overexpressing superoxide dismutase: evidence for reduced superoxide-nitric oxide interaction. Diabetes 53, 762-768
51. DeRubertis F.R., Craven, P. A. and Melhem, M. F. (2007) Acceleration of diabetic renal injury in the superoxide dismutase knockout mouse: effects of tempol. Metabolism 56, 1256-1264
52. Piwkowska A. Rogacka, D., Audzeyenka, I., Jankowski, M. and Angielski, S. (2011) High glucose concentration affects the oxidant-antioxidant balance in cultured mouse podocytes. J. Cell Biochem. 112, 1661-1672
53. Pettersson, U. S., Christoffersson, G., Massena, S., Ahl, D., Jansson, L., Henriksnas, J. and Phillipson, M. (2011) Increased recruitment but impaired function of leukocytes during inflammation in mouse models of type 1 and type 2 diabetes. PLoS ONE 6, e22480
54. Ma, F. Y., Sachchithananthan, M., Flanc, R. S. and Nikolic-Paterson, D. J. (2009) Mitogen activated protein kinases in renal fibrosis. Front. Biosci. 1, 171-187