Curcumin attenuates diabetic nephropathy by inhibiting PKC-α and PKC-β1 activity in streptozotocin-induced type I diabetic rats

Molecular Nutrition and Food Research

Volumn 55, Issue 11, 2011, Pages 1655-1665

  Soetikno, Vivian ^a,b   Watanabe, Kenichi ^a   Sari, Flori R ^a   Harima, Meilei ^a   Thandavarayan, Rajarajan A ^a   Veeraveedu, Punniyakoti T ^a   Arozal, Wawaimuli ^a   Sukumaran, Vijayakumar ^a   Lakshmanan, Arun Prasath ^a   Arumugam, Somasundaram ^a   Suzuki, Kenji ^c  

^a NIIGATA UNIVERSITY OF PHARMACY AND APPLIED LIFE SCIENCES   (Japan)

^b UNIVERSITY OF INDONESIA   (Indonesia)

^c NIIGATA UNIVERSITY GRADUATE SCHOOL OF MEDICAL AND DENTAL SCIENCES   (Japan)

Author keywords

Curcumin; Diabetic nephropathy; Mitogen activated protein kinase; Oxidative stress; Protein kinase C

Indexed keywords

ANTIOXIDANT; CURCUMIN; ISOENZYME; MESSENGER RNA; NEUTROPHIL CYTOSOL FACTOR 67K; NOX4 PROTEIN, RAT; PHOSPHOPROTEIN; PROTEIN KINASE C; PROTEIN KINASE C ALPHA; PROTEIN KINASE C BETA; PROTEIN KINASE INHIBITOR; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SCLEROPROTEIN; STREPTOZOCIN;

ANIMAL; ARTICLE; DIABETIC NEPHROPATHY; DRUG ANTAGONISM; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; INSULIN DEPENDENT DIABETES MELLITUS; KIDNEY; MALE; METABOLISM; OXIDATIVE STRESS; PATHOLOGY; PATHOPHYSIOLOGY; RANDOMIZATION; RAT; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT;

ANIMALS; ANTIOXIDANTS; CURCUMIN; DIABETES MELLITUS, TYPE 1; DIABETIC NEPHROPATHIES; EXTRACELLULAR MATRIX PROTEINS; GENE EXPRESSION REGULATION; ISOENZYMES; KIDNEY; MALE; MAP KINASE SIGNALING SYSTEM; NADPH OXIDASE; OXIDATIVE STRESS; PHOSPHOPROTEINS; PROTEIN KINASE C; PROTEIN KINASE C-ALPHA; PROTEIN KINASE INHIBITORS; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; STREPTOZOCIN;

RATTUS;

EID: 80155194979     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.201100080     Document Type: Article

References (51)

1. Zelmanovitz, T., Gerchman, F., Balthazar, A. P. S., Thomazelli, F. C. S. et al., Diabetic nephropathy. Diabetol. Metab. Syndr. 2009, 21, 1-10.
2. Kanwar, Y. S., Wada, J., Sun, L., Xie, P. et al., Diabetic nephropathy: Mechanisms of renal disease progression. Exp. Biol. Med. 2008, 233, 4-11.
3. Sharma, K., Ziyadeh, F. N., Hyperglycemia and diabetic kidney disease. The case for transforming growth factor-beta as a key mediator. Diabetes 1995, 44, 1139-1146.
4. Riser, B. L., Denichilo, M., Cortes, P., Baker, C., Regulation of connective tissue growth factor activity in cultured rat mesangial cells and its expression in experimental diabetic glomerulosclerosis. J. Am. Soc. Nephrol. 2000, 11, 25-38.
5. Remuzzi, G., Benigni, A., Remuzzi, A., Mechanisms of progression and regression of renal lesions of chronic nephropathies and diabetes. J. Clin. Invest. 2006, 116, 288-296.
6. Mauer, S. M., Steffes, M. W., Ellis, E. N., Sutherland, D. E., Structural-functional relationships in diabetic nephropathy. J. Clin. Invest. 1984, 74, 1143-1155.
7. Ferrara, N., Vascular endothelial growth factor: basic science and clinical progress. Endocr. Rev. 2004, 25, 581-611.
8. Meier, M., King, G. L., Protein kinase C activation and its pharmacological inhibition in vascular disease. Vasc. Med. 2000, 5, 173-185.
9. Dempsey, E. C., Newton, A. C., Mochly-Rosen, D., Fields, A. P., Protein kinase C isozymes and the regulation of diverse cell responses. Am. J. Physiol. Lung. Cell. Mol. Physiol. 2000, 279, L429-L438.
10. Kikkawa, R., Haneda, M., Uzu, T., Koya, D. et al., Translocation of protein kinase C alpha and zeta in rat glomerular mesangial cells cultured under high glucose conditions. Diabetologia 1994, 37, 838-841.
11. Ayo, S. H., Radnik, R., Garoni, J. A., Troyer, D. A. et al., High glucose increases diacylglycerol mass and activates protein kinase C in mesangial cell cultures. Am. J. Physiol. 1991, 261, F571-F577.
12. Seger, R., Krebs, E. G., The MAPK signaling cascade. FASEB J. 1995, 9, 726-735.
13. Haneda, M., Koya, D., Isono, M., Kikkawa, R., Overview of glucose signaling in mesangial cells in diabetic nephropathy. J. Am. Soc. Nephrol. 2003, 14, 1374-1382.
14. Koya, D., Jirousek, M. R., Lin, Y. W., Ishii, H., Characterization of protein kinase C beta isoform activation on the gene expression of transforming growth factor-beta, extracellular matrix components, and prostanoids in the glomeruli of diabetic rats. J. Clin. Invest. 1997, 100, 115-126.
15. Inoguchi, T., Battan, R., Handler, E., Sportsman, J. R. et al., Preferential elevation of protein kinase C isoform beta II and diacylglycerol levels in the aorta and heart of diabetic rats: differential reversibility to glycemic control by islet cell transplantation. Proc. Natl. Acad. Sci. USA 1992, 89, 11059-11063.
16. Koya, D., Haneda, M., Nakagawa, H., Isshiki, K. et al., Amelioration of accelerated diabetic mesangial expansion by treatment with a PKC beta inhibitor in diabetic db/db mice, a rodent model for type 2 diabetes. FASEB J. 2000, 14, 439-447.
17. Menne, J., Park, J. K., Boehne, M., Elger, M. et al., Diminished loss of proteoglycans and lack of albuminuria in protein kinase C-alpha-deficient diabetic mice. Diabetes 2004, 53, 2101-2109.
18. Lin, J. K., Molecular targets of curcumin. Adv. Exp. Med. Biol. 2007, 595, 227-243.
19. Liu, J. Y., Lin, S. J., Lin, J. K., Inhibitory effects of curcumin on protein kinase C activity induced by TPA in NIH3T3 cells. Carcinogenesis 1993, 14, 857-861.
20. Jain, S. K., Rains, J., Croad, J., Larson, B. et al., Curcumin supplementation lowers TNF-α, IL-6, IL-8, MCP-1 secretion in high glucose-treated cultured monocytes and blood levels of TNF-α, IL-6, MCP-1, glucose, and glycosylated hemoglobin in diabetic rats. Antioxid. Redox. Signal. 2009, 11, 241-249.
21. Sharma, S., Kulkarni, S. K., Chopra, K., Curcumin, the active principle of turmeric (Curcuma longa), ameliorates diabetic nephropathy in rats. Clin. Exp. Pharmacol. Physiol. 2006, 33, 940-945.
22. Smith, P. K., Krohn, R. I., Hermanson, G. T., Mallia, A. K. et al., Measurement of protein using bicinchoninic acid. Anal. Biochem. 1985, 150, 76-85.
23. Thallas-Bonke, V., Thorpe, S. R., Coughlan, M. T., Fukami, K. et al., Inhibition of NADPH oxidase prevents advanced glycation end product-mediated damage in diabetic nephropathy through a protein kinase C-alpha-dependent pathway. Diabetes 2008, 57, 460-469.
24. Connelly, K. A., Kelly, D. J., Zhang, Y., Prior, D. L. et al., Inhibition of protein kinase C-beta by ruboxistaurin preserves cardiac function and reduces extracellular matrix production in diabetic cardiomyopathy. Circ. Heart Fail. 2009, 2, 129-137.
25. Wolf, G., Chen, S., Ziyadeh, F. N., From the periphery of the glomerular capillary wall toward the center of disease: podocyte injury comes of age in diabetic nephropathy. Diabetes 2005, 54, 1626-1634.
26. Babazono, T., Kapor-Drezgic, J., Dlugosz, J. A., Whiteside, C., Altered expression and subcellular localization of diacylglycerol-sensitive protein kinase C isoforms in diabetic rat glomerular cells. Diabetes 1998, 47, 668-676.
27. Haller, H., Baur, E., Quass, P., Behrend, M. et al., High glucose concentrations and protein kinase C isoforms in vascular smooth muscle cells. Kidney Int. 1995, 47, 1057-1067.
28. Whiteside, C. I., Dlugosz, J. A., Mesangial cell protein kinase C isozyme activation in the diabetic milieu. Am. J. Physiol. Renal Physiol. 2002, 282, F975-F980.
29. Ohshiro, Y., Ma, R. C., Yasuda, Y., Hiraoka-Yamamoto, J. et al., Reduction of diabetes-induced oxidative stress, fibrotic cytokine expression, and renal dysfunction in protein kinase C beta-null mice. Diabetes 2006, 55, 3112-3120.
30. Meier, M., Park, J. K., Overheu, D., Kirsch, T. et al., Deletion of protein kinase C-beta isoform in vivo reduces renal hypertrophy but not albuminuria in the streptozotocin-induced diabetic mouse model. Diabetes 2007, 56, 346-354.
31. Balasubramanyam, M., Koteswari, A. A., Kumar, R. S., Monickaraj, S. F. et al., Curcumin-induced inhibition of cellular reactive oxygen species generation: novel therapeutic implications. J. Biosci. 2003, 28, 715-721.
32. Mahmmoud, Y. A., Modulation of protein kinase C by curcumin; inhibition and activation switched by calcium ions. Br. J. Pharmacol. 2007, 150, 200-208.
33. Cooper, M. E., Vranes, D., Youssef, S., Stacker, S. A. et al., Increased renal expression of vascular endothelial growth factor (VEGF) and its receptor VEGFR-2 in experimental diabetes. Diabetes 1999, 48, 2229-2239.
34. Liu, E., Morimoto, M., Kitajima, S., Koike, T. et al., Increased expression of vascular endothelial growth factor in kidney leads to progressive impairment of glomerular functions. J. Am. Soc. Nephrol. 2007, 18, 2094-2104.
35. Kim, N. H., Oh, J. H., Seo, J. A., Lee, K. W. et al., Vascular endothelial growth factor (VEGF) and soluble VEGF receptor FLT-1 in diabetic nephropathy. Kidney Int. 2005, 67, 167-177.
36. de Vriese, A. S., Tilton, R. G., Elger, M., Stephan, C. C. et al., Antibodies against vascular endothelial growth factor improve early renal dysfunction in experimental diabetes. J. Am. Soc. Nephrol. 2001, 12, 993-1000.
37. Haneda, M., Araki, S., Togawa, M., Sugimoto, T. et al., Mitogen-activated protein kinase cascade is activated in glomeruli of diabetic rats and glomerular mesangial cells cultured under high glucose conditions. Diabetes 1997, 46, 847-853.
38. Toyoda, M., Suzuki, D., Honma, M., Uehara, G. et al., High expression of PKC-MAPK pathway mRNAs correlates with glomerular lesions in human diabetic nephropathy. Kidney Int. 2004, 66, 1107-1114.
39. Chen, S., Feng, B., George, B., Chakrabarti, R. et al., Transcriptional coactivator p300 regulates glucose-induced gene expression in endothelial cells. Am. J. Physiol. Endocrinol. Metab. 2010, 298, E127-E137.
40. Kaur, H., Chen, S., Xin, X., Chiu, J. et al., Diabetes-induced extracellular matrix protein expression is mediated by transcription coactivator p300. Diabetes 2006, 55, 3104-3111.
41. Morimoto, T., Sunagawa, Y., Kawamura, T., Takaya, T. et al., The dietary compound curcumin inhibits p300 histone acetyltransferase activity and prevents heart failure in rats. J. Clin. Invest. 2008, 118, 868-878.
42. Chiu, J., Khan, Z. A., Farhangkhoee, H., Chakrabarti, S., Curcumin prevents diabetes-associated abnormalities in the kidneys by inhibiting p300 and nuclear factor-kappaB. Nutrition 2009, 25, 964-972.
43. Lee, H. B., Yu, M. R., Yang, Y., Jiang, Z. et al., Reactive oxygen species-regulated signaling pathways in diabetic nephropathy. J. Am. Soc. Nephrol. 2003, 14, S241-S245.
44. Etoh, T., Inoguchi, T., Kakimoto, M., Sonoda, N. et al., 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 2003, 46, 1428-1437.
45. Satoh, M., Fujimoto, S., Haruna, Y., Arakawa, S. et al., 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. 2005, 288, F1144-F1152.
46. Inoguchi, T., Sonta, T., Tsubouchi, H., Etoh, T. et al., Protein kinase C-dependent increase in reactive oxygen species (ROS) production in vascular tissues of diabetes: role of vascular NAD(P)H oxidase. J. Am. Soc. Nephrol. 2003, 14, S227-S232.
47. Kitada, M., Koya, D., Sugimoto, T., Isono, M. et al., Translocation of glomerular p47phox and p67phox by protein kinase C-beta activation is required for oxidative stress in diabetic nephropathy. Diabetes 2003, 52, 2603-2614.
48. Gorin, Y., Block, K., Hernandez, J., Bhandari, B. et al., Nox4 NAD(P)H oxidase mediates hypertrophy and fibronectin expression in the diabetic kidney. J. Biol. Chem. 2005, 280, 16-26.
49. Kowluru, R. A., Kanwar, M., Effects of curcumin on retinal oxidative stress and inflammation in diabetes. Nutr. Metab. (Lond) 2007, 16, 4-8.
50. Anand, P., Kunnumakkara, A. B., Newman, R. A., Aggarwal, B. B., Bioavailability of curcumin: problems and promises. Mol. Pharm. 2007, 4, 807-818.
51. Cheng, A. L., Hsu, C. H., Lin, J. K., Hsu, M. M. et al., Phase I clinical trial of curcumin, a chemopreventive agent, in patients with high-risk or pre-malignant lesions. Anticancer Res. 2001, 21, 2895-2900.