Renoprotective effect of a novel selective PPARα modulator K-877 in db/db mice: A role of diacylglycerol-protein kinase C-NAD(P)H oxidase pathway

Metabolism: Clinical and Experimental

Volumn 71, Issue , 2017, Pages 33-45

  Maki, Toshinobu ^a   Maeda, Yasutaka ^a,b   Sonoda, Noriyuki ^a,b   Makimura, Hiroaki ^a   Kimura, Shinichiro ^a   Maeno, Sayaka ^a   Takayanagi, Ryoichi ^a   Inoguchi, Toyoshi ^a,b  

^a KYUSHU UNIVERSITY   (Japan)

^b KYUSHU UNIVERSITY   (Japan)

Author keywords

Diabetic nephropathy; NAD(P)H oxidase; Oxidative stress; Peroxisome proliferator activated receptor ; Protein kinase C

Indexed keywords

ACETYL COENZYME A CARBOXYLASE; ALBUMIN; DIACYLGLYCEROL; FATTY ACID; GLUCOSE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; PEMAFIBRATE; PROTEIN KINASE C; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; BENZOXAZOLE DERIVATIVE; BUTYRIC ACID DERIVATIVE; DIACYLGLYCEROL KINASE; K-877 COMPOUND; LIPID; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

ALBUMINURIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; DB/DB MOUSE; DIABETIC NEPHROPATHY; DRUG SELECTIVITY; FATTY ACID OXIDATION; GLUCOSE BLOOD LEVEL; GLYCEMIC CONTROL; KIDNEY HYPERTROPHY; LIPID BLOOD LEVEL; LONG TERM CARE; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RENAL PROTECTION; SHORT COURSE THERAPY; SIGNAL TRANSDUCTION; AGONISTS; ANIMAL; BLOOD; C57BL MOUSE; DIABETIC NEPHROPATHIES; DRUG EFFECTS; EXPERIMENTAL DIABETES MELLITUS; KIDNEY; METABOLISM;

ACETYL-COA CARBOXYLASE; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; BENZOXAZOLES; BUTYRATES; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC NEPHROPATHIES; DIACYLGLYCEROL KINASE; KIDNEY; LIPIDS; MALE; METABOLIC NETWORKS AND PATHWAYS; MICE; MICE, INBRED C57BL; NADPH OXIDASE; OXIDATIVE STRESS; PPAR ALPHA; PROTEIN KINASE C;

EID: 85015368396     PISSN: 00260495     EISSN: 15328600     Source Type: Journal    
DOI: 10.1016/j.metabol.2017.02.013     Document Type: Article

References (48)

1. [1] Brownlee, M., Cerami, A., Vlassara, H., Advanced glycosylation end products in tissue and the biochemical basis of diabetic complication. N Engl J Med 318 (1988), 1315–1321.
2. [2] Greene, D., Lattimer, S., Sima, A., Sorbitol, phosphoinositides, and sodium-potassium-ATPase in the pathogenesis of diabetic complications. N Engl J Med 316 (1987), 599–606.
3. [3] Baynes, J., Role of oxidative stress in development of complications in diabetes. Diabetes 40 (1991), 405–412.
4. [4] Sheetz, M., King, G., Molecular understanding of hyperglycemia's adverse effects for diabetic complications. JAMA 288 (2002), 2579–2588.
5. [5] Oberley, L., Free radicals and diabetes. Free Radic Biol Med 5 (1988), 113–124.
6. [6] Ha, H., Kim, C., Son, Y., Chung, M., Kim, K., DNA damage in the kidneys of diabetic rats exhibiting microalbuminuria. Free Radic Biol Med 16 (1994), 271–274.
7. [7] Kakimoto, M., Inoguchi, T., Sonta, T., Yu, H., Imamura, M., Etoh, T., et al. Accumulation of 8-hydroxy-2'-deoxyguanosine and mitochondrial DNA deletion in kidney of diabetic rats. Diabetes 51 (2002), 1588–1595.
8. [8] Koya, D., Hayashi, K., Kitada, M., Kashiwagi, A., Kikkawa, R., Haneda, M., Effects of antioxidants in diabetes-induced oxidative stress in the glomeruli of diabetic rats. J Am Soc Nephrol 14 (2003), 250S–2503.
9. [9] Inoguchi, T., Li, P., Umeda, F., Yu, H., Kakimoto, M., Imamura, M., et al. High glucose level and free fatty acid stimulate reactive oxygen species production through protein kinase. Diabetes 49 (2000), 1939–1945.
10. [10] Etoh, T., Inoguchi, T., Kakimoto, M., Sonoda, N., Kobayashi, K., Kuroda, J., et al. Increased expression of NAD(P)H oxidase subunits, NOX4 and p22phox, in the kidney of streptozotocin-induced diabetic rats and its reversibity by interventive insulin treatment. Diabetologia 46 (2003), 1428–1437.
11. [11] Inoguchi, T., 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 14 (2003), S227–S232.
12. [12] Inoguchi, T., Battan, R., Handler, E., Sportsman, J., Heath, W., King, G., 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 U S A 89 (1992), 11059–11063.
13. [13] Craven, P., Davidson, C., DeRubertis, F., Increase in diacylglycerol mass in isolated glomeruli by glucose from de novo synthesis of glycerolipids. Diabetes 39 (1990), 667–674.
14. [14] Inoguchi, T., Xia, P., Kunisaki, M., Higashi, S., Feener, E., King, G., Insulin's effect on protein kinase C and diacylglycerol induced by diabetes and glucose in vascular tissues. Am J Phys 267 (1994), E369–E379.
15. [15] Issemann, I., Green, S., Activation of a member of the steroid hormone receptor superfamily by peroxisome proliferators. Nature 347 (1990), 645–650.
16. [16] Yoon, M., The role of PPARalpha in lipid metabolism and obesity: focusing on the effects of estrogen on PPARalpha actions. Pharmacol Res 60 (2009), 151–159.
17. [17] Braissant, O., Foufelle, F., Scotto, C., Dauça, M., Wahli, W., Differential expression of peroxisome proliferator-activated receptors (PPARs): tissue distribution of PPAR-alpha, − beta, and -gamma in the adult rat. Endocrinology 137 (1996), 354–366.
18. [18] Ansquer, J., Foucher, C., Rattier, S., Taskinen, M., Steiner, G., Fenofibrate reduces progression to microalbuminuria over 3 years in a placebo-controlled study in type 2 diabetes: results from the diabetes atherosclerosis intervention study (DAIS). Am J Kidney Dis 45 (2005), 485–493.
19. [19] Davis, T., Ting, R., Best, J., Donoghoe, M., Drury, P., Sullivan, D., et al. Effects of fenofibrate on renal function in patients with type 2 diabetes mellitus: the fenofibrate intervention and event lowering in diabetes (FIELD) study. Diabetologia 54 (2011), 280–290.
20. [20] Ansquer, J.C., Foucher, C., Rattier, S., Taskinen, M.R., Steiner, G., Effect of fenofibrate on progression of coronary-artery disease in type 2 diabetes: the diabetes atherosclerosis intervention study, a randomised study. Lancet 357 (2001), 905–910.
21. [21] Keech, A., Simes, R., Barter, P., Best, J., Scott, R., Taskinen, M., et al. Effects of long-term fenofibrate therapy on cardiovascular events in 9795 people with type 2 diabetes mellitus (the FIELD study): randomised controlled trial. Lancet 366 (2005), 1849–1861.
22. [22] Park, C.W., Zhang, Y., Zhang, X., Wu, J., Chen, L., Cha, D.R., et al. PPARalpha agonist fenofibrate improves diabetic nephropathy in db/db mice. Kidney Int 69 (2006), 1511–1517.
23. [23] Hong, Y.A., Lim, J.H., Kim, M.Y., Kim, T.W., Kim, Y., Yang, K.S., et al. Fenofibrate improves renal lipotoxicity through activation of AMPK-PGC-1alpha in db/db mice. PLoS One, 9, 2014, e96147.
24. [24] Raza-Iqbal, S., Tanaka, T., Anai, M., Inagaki, T., Matsumura, Y., Ikeda, K., et al. Transcriptome analysis of K-877 (a novel selective PPARα modulator (SPPARMα))-regulated genes in primary human hepatocytes and the mouse liver. J Atheroscler Thromb 22 (2015), 754–772.
25. [25] Ishibashi, S., Yamashita, S., Arai, H., Araki, E., Yokote, K., Suganami, H., et al. Effects of K-877, a novel selective PPARalpha modulator (SPPARMalpha), in dyslipidaemic patients: a randomized, double blind, active- and placebo-controlled, phase 2 trial. Atherosclerosis 249 (2016), 36–43.
26. [26] Fujii, M., Inoguchi, T., Sasaki, S., Maeda, Y., Zheng, J., Kobayashi, K., et al. Bilirubin and biliverdin protect rodents against diabetic nephropathy by downregulating NAD(P)H oxidase. Kidney Int 78 (2010), 905–919.
27. [27] Takemoto, M., Asker, N., Gerhardt, H., Lundkvist, A., Johansson, B.R., Saito, Y., et al. A new method for large scale isolation of kidney glomeruli from mice. Am J Pathol 161 (2002), 799–805.
28. [28] Blachnio-Zabielska, A., Zabielski, P., Jensen, M., Intramyocellular diacylglycerol concentrations and [U-13C]palmitate isotopic enrichment measured by LC/MS/MS. J Lipid Res 54 (2013), 1705–1711.
29. [29] Ikeda, N., Inoguchi, T., Sonoda, N., Fujii, M., Takei, R., Hirata, E., et al. Biliverdin protects against the deterioration of glucose tolerance in db/db mice. Diabetologia 54 (2011), 2183–2191.
30. [30] Terami, N., Ogawa, D., Tachibana, H., Hatanaka, T., Wada, J., Nakatsuka, A., et al. Long-term treatment with the sodium glucose cotransporter 2 inhibitor, dapagliflozin, ameliorates glucose homeostasis and diabetic nephropathy in db/db mice. PLoS One, 9, 2014, e100777.
31. [31] Park, C., Kim, H., Ko, S., Chung, H., Lim, S., Yang, C., et al. Accelerated diabetic nephropathy in mice lacking the peroxisome proliferator-activated receptor alpha. Diabetes 55 (2006), 885–893.
32. [32] Fruchart, J., Selective peroxisome proliferator-activated receptor α modulators (SPPARMα) the next generation of peroxisome proliferator-activated receptor α-agonists. Cardiovasc Diabetol 12:82 (2013), 1–8.
33. [33] Ishii, H., Jirousek, M., Koya, D., Takagi, C., Xia, P., Clermont, A., et al. Amelioration of vascular dysfunctions in diabetic rats by an oral PKC beta inhibitor. Science 272 (1996), 728–731.
34. [34] Koya, D., Haneda, M., Nakagawa, H., Isshiki, K., Sato, H., Maeda, S., 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 14 (2000), 439–447.
35. [35] Gorin, Y., Block, K., Hernandez, J., Bhandari, B., Wagner, B., Barnes, J., et al. Nox4 NAD(P)H oxidase mediates hypertrophy and fibronectin expression in the diabetic kidney. J Biol Chem 280 (2005), 39616–39626.
36. [36] Geiszt, M., Leto, T., The Nox Family of NAD(P)H oxidases: host defense and beyond. J Biol Chem 279 (2004), 51715–51718.
37. [37] Jha, J., Gray, S., Barit, D., Okabe, J., El-Osta, A., Namikoshi, T., et al. Genetic targeting or pharmacologic inhibition of NADPH oxidase nox4 provides renoprotection in long-term diabetic nephropathy. J Am Soc Nephrol 25 (2014), 1237–1254.
38. [38] Yu, H., Inoguchi, T., Kakimoto, M., Nakashima, N., Imamura, M., Hashimoto, T., et al. Saturated non-esterified fatty acids stimulate de novo diacylglycerol synthesis and protein kinase c activity in cultured aortic smooth muscle cells. Diabetologia 44 (2001), 614–620.
39. [39] Wakil, S., Abu-Elheiga, L., Fatty acid metabolism: target for metabolic syndrome. J Lipid Res 50 (2009), S138–S143 [Suppl].
40. [40] Hardie, D., Pan, D., Regulation of fatty acid synthesis and oxidation by the AMP-activated protein kinase. Biochem Soc Trans 30 (2002), 1064–1670.
41. [41] Rakhshandehroo, M., Knoch, B., Muller, M., Kersten, S., Peroxisome proliferator-activated receptor alpha target genes. PPAR Res 2010 (2010), 1–20.
42. [42] Koh, E., Kim, M., Park, J., Kim, H., Youn, J., Park, H., et al. Peroxisome proliferator-activated receptor (PPAR)-α activation prevents diabetes in OLETF rats. Diabetes 52 (2003), 2331–2337.
43. [43] Idzior-Walus, B., Sieradzki, J., Rostworowski, W., Zdzienicka, A., Kawalec, E., Wójcik, J., et al. Effects of comicronised fenofibrate on lipid and insulin sensitivity in patients with polymetabolic syndrome X. Eur J Clin Invest 30 (2000), 871–878.
44. [44] Boden, G., Chen, X., Ruiz, J., White, J., Rossetti, L., Mechanisms of fatty acid-induced inhibition of glucose uptake. J Clin Investig 93:6 (1994), 2438–2446.
45. [45] Chalkley, S., Hettiarachchi, M., Chisholm, D., Kraegen, E., Five-hour fatty acid elevation increases muscle lipids and impairs glycogen synthesis in the rat. Metabolism 47 (1998), 1121–1126.
46. [46] Pineda, T.I., Gervois, P., Staels, B., Peroxisome proliferator-activated receptor alpha in metabolic disease, inflammation, atherosclerosis and aging. Curr Opin Lipidol 10 (1999), 151–159.
47. [47] Tsubouchi, H., Inoguchi, T., Inuo, M., Kakimoto, M., Sonta, T., Sonoda, N., et al. Sulfonylurea as well as elevated glucose levels stimulate reactive oxygen species production in the pancreatic beta-cell line, MIN6-a role of NAD(P)H oxidase in beta-cells. Biochem Biophys Res Commun 326 (2005), 60–65.
48. [48] Zawalich, W., Rasmussen, H., Control of insulin secretion: a model involving Ca2 +, cAMP and diacylglycerol. Mol Cell Endocrinol 70 (1990), 119–137.