Up-regulation of Nrf2 is involved in FGF21-mediated fenofibrate protection against type 1 diabetic nephropathy

Free Radical Biology and Medicine

Volumn 93, Issue , 2016, Pages 94-109

  Cheng, Yanli ^a,b,c   Zhang, Jingjing ^c,d,e   Guo, Weiying ^a   Li, Fengsheng ^f   Sun, Weixia ^a   Chen, Jing ^c   Zhang, Chi ^b,g   Lu, Xuemian ^g   Tan, Yi ^b,c,g   Feng, Wenke ^c   Fu, Yaowen ^a   Liu, Gilbert C ^h   Xu, Zhonggao ^a   Cai, Lu ^b,c,g  

^a THE FIRST HOSPITAL OF JILIN UNIVERSITY   (China)

^b WENZHOU MEDICAL UNIVERSITY   (China)

^c University of Louisville School of Medicine   (United States)

^d CHINA MEDICAL UNIVERSITY   (China)

^e People's Hospital of Liaoning Province   (China)

^f Second Artillery General Hospital   (China)

^g THE THIRD AFFILIATED HOSPITAL OF WENZHOU MEDICAL UNIVERSITY   (China)

^h UNIVERSITY OF LOUISVILLE   (United States)

Author keywords

Antioxidants; Diabetic nephropathy; FGF21; Nrf2; Oxidative stress; PPAR agonist; Type 1 diabetes

Indexed keywords

COLLAGEN; FENOFIBRATE; FIBROBLAST GROWTH FACTOR 21; GLYCOGEN SYNTHASE KINASE 3BETA; LIPID; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN KINASE FYN; STREPTOZOCIN; TRANSCRIPTION FACTOR NRF2; FIBROBLAST GROWTH FACTOR; NFE2L2 PROTEIN, MOUSE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL STIMULATION; CONTROLLED STUDY; DIABETIC NEPHROPATHY; DRUG MECHANISM; GENE DELETION; INFLAMMATION; INSULIN DEPENDENT DIABETES MELLITUS; KIDNEY DYSFUNCTION; KIDNEY FUNCTION; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RENAL PROTECTION; STREPTOZOTOCIN-INDUCED DIABETIC NEUROPATHY; UPREGULATION; AGONISTS; ANIMAL; BIOSYNTHESIS; DIABETES COMPLICATIONS; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC NEPHROPATHIES; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; HUMAN; PATHOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; DIABETES COMPLICATIONS; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC NEPHROPATHIES; FENOFIBRATE; FIBROBLAST GROWTH FACTORS; GENE EXPRESSION REGULATION; HUMANS; MICE; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; PPAR ALPHA; SIGNAL TRANSDUCTION;

EID: 84957536494     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2016.02.002     Document Type: Article

References (51)

1. K.R. Keshari, D.M. Wilson, V. Sai, R. Bok, K.Y. Jen, P. Larson, M. Van Criekinge, J. Kurhanewicz, and Z.J. Wang Noninvasive in vivo imaging of diabetes-induced renal oxidative stress and response to therapy using hyperpolarized 13C dehydroascorbate magnetic resonance Diabetes 64 2015 344 352
2. B. Li, S. Liu, L. Miao, and L. Cai Prevention of diabetic complications by activation of Nrf2: diabetic cardiomyopathy and nephropathy Exp. Diabetes Res. 2012 2012 216512
3. T. Miyata, N. Suzuki, and C. van Ypersele de Strihou Diabetic nephropathy: are there new and potentially promising therapies targeting oxygen biology? Kidney Int. 84 2013 693 702
4. J.B. de Haan Nrf2 activators as attractive therapeutics for diabetic nephropathy Diabetes 60 2011 2683 2684
5. H. Zheng, S.A. Whitman, W. Wu, G.T. Wondrak, P.K. Wong, D. Fang, and D.D. Zhang Therapeutic potential of Nrf2 activators in streptozotocin-induced diabetic nephropathy Diabetes 60 2011 3055 3066
6. T. Jiang, Z. Huang, Y. Lin, Z. Zhang, D. Fang, and D.D. Zhang The protective role of Nrf2 in streptozotocin-induced diabetic nephropathy Diabetes 59 2010 850 860
7. S.M. Strittmatter Overcoming drug development bottlenecks with repurposing: old drugs learn new tricks Nat. Med. 20 2014 590 591
8. M.J. Higgins, J. Thursby, and M. Thursby Bench-to-bench bottlenecks in translation Sci. Transl. Med. 6 2014 250fs232
9. J.C. Ansquer, C. Foucher, S. Rattier, M.R. Taskinen, G. Steiner, and D. Investigators 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
10. Y.A. Hong, J.H. Lim, M.Y. Kim, T.W. Kim, Y. Kim, K.S. Yang, H.S. Park, S.R. Choi, S. Chung, H.W. Kim, H.W. Kim, B.S. Choi, Y.S. Chang, and C.W. Park Fenofibrate improves renal lipotoxicity through activation of AMPK-PGC-1alpha in db/db mice PLoS One 9 2014 e96147
11. Y. Zhou, X. Kong, P. Zhao, H. Yang, L. Chen, J. Miao, X. Zhang, J. Yang, J. Ding, and Y. Guan Peroxisome proliferator-activated receptor-alpha is renoprotective in doxorubicin-induced glomerular injury Kidney Int. 79 2011 1302 1311
12. K. Mori, M. Mukoyama, and K. Nakao PPAR-alpha transcriptional activity is required to combat doxorubicin-induced podocyte injury in mice Kidney Int. 79 2011 1274 1276
13. L.L. Chen, J.Y. Zhang, and B.P. Wang Renoprotective effects of fenofibrate in diabetic rats are achieved by suppressing kidney plasminogen activator inhibitor-1 Vascul. Pharmacol. 44 2006 309 315
14. L. Chen, J. Zhang, Y. Zhang, Y. Wang, and B. Wang Improvement of inflammatory responses associated with NF-kappa B pathway in kidneys from diabetic rats Inflamm. Res. 57 2008 199 204
15. S. Kadian, N. Mahadevan, and P. Balakumar Differential effects of low-dose fenofibrate treatment in diabetic rats with early onset nephropathy and established nephropathy Eur. J. Pharmacol. 698 2013 388 396
16. D. Ye, Y. Wang, H. Li, W. Jia, K. Man, C.M. Lo, Y. Wang, K.S. Lam, and A. Xu Fibroblast growth factor 21 protects against acetaminophen-induced hepatotoxicity by potentiating peroxisome proliferator-activated receptor coactivator protein-1alpha-mediated antioxidant capacity in mice Hepatology 60 2014 977 989
17. Y. Yu, F. Bai, Y. Liu, Y. Yang, Q. Yuan, D. Zou, S. Qu, G. Tian, L. Song, T. Zhang, S. Li, Y. Liu, W. Wang, G. Ren, and D. Li Fibroblast growth factor (FGF21) protects mouse liver against d-galactose-induced oxidative stress and apoptosis via activating Nrf2 and PI3K/Akt pathways Mol. Cell. Biochem. 403 2015 287 299
18. X. Jiang, C. Zhang, Y. Xin, Z. Huang, Y. Tan, Y. Huang, Y. Wang, W. Feng, X. Li, W. Li, Y. Qu, and L. Cai Protective effect of FGF21 on type 1 diabetes-induced testicular apoptotic cell death probably via both mitochondrial- and endoplasmic reticulum stress-dependent pathways in the mouse model Toxicol. Lett. 219 2013 65 76
19. A. Planavila, I. Redondo-Angulo, F. Ribas, G. Garrabou, J. Casademont, M. Giralt, and F. Villarroya Fibroblast growth factor 21 protects the heart from oxidative stress Cardiovasc. Res. 106 2015 19 31
20. L. Cai, W. Li, G. Wang, L. Guo, Y. Jiang, and Y.J. Kang Hyperglycemia-induced apoptosis in mouse myocardium: mitochondrial cytochrome C-mediated caspase-3 activation pathway Diabetes 51 2002 1938 1948
21. L. Cai, J. Wang, Y. Li, X. Sun, L. Wang, Z. Zhou, and Y.J. Kang Inhibition of superoxide generation and associated nitrosative damage is involved in metallothionein prevention of diabetic cardiomyopathy Diabetes 54 2005 1829 1837
22. Y. Wang, Y. Wang, M. Luo, H. Wu, L. Kong, Y. Xin, W. Cui, Y. Zhao, J. Wang, G. Liang, L. Miao, and L. Cai Novel curcumin analog C66 prevents diabetic nephropathy via JNK pathway with the involvement of p300/CBP-mediated histone acetylation Biochim. Biophys. Acta 2015 1852 34 46
23. B.D. Whelton, D.P. Peterson, E.S. Moretti, R.W. Mauser, and M.H. Bhattacharyya Kidney changes in multiparous, nulliparous and ovariectomized mice fed either a nutrient-sufficient or -deficient diet containing cadmium Toxicology 119 1997 123 140
24. M. Jeansson, A.B. Granqvist, J.S. Nystrom, and B. Haraldsson Functional and molecular alterations of the glomerular barrier in long-term diabetes in mice Diabetologia 49 2006 2200 2209
25. W. Cui, Y. Bai, X. Miao, P. Luo, Q. Chen, Y. Tan, M.J. Rane, L. Miao, and L. Cai Prevention of diabetic nephropathy by sulforaphane: possible role of nrf2 upregulation and activation Oxid. Med. Cell Longev. 2012 2012 821936
26. L. Cai, Y. Wang, G. Zhou, T. Chen, Y. Song, X. Li, and Y.J. Kang Attenuation by metallothionein of early cardiac cell death via suppression of mitochondrial oxidative stress results in a prevention of diabetic cardiomyopathy J. Am. Coll. Cardiol. 48 2006 1688 1697
27. W. Sun, Y. Wang, X. Miao, Y. Wang, L. Zhang, Y. Xin, S. Zheng, P.N. Epstein, Y. Fu, and L. Cai Renal improvement by zinc in diabetic mice is associated with glucose metabolism signaling mediated by metallothionein and Akt, but not Akt2 Free Radic. Biol. Med. 68 2014 22 34
28. W. Cui, B. Li, Y. Bai, X. Miao, Q. Chen, W. Sun, Y. Tan, P. Luo, C. Zhang, S. Zheng, P.N. Epstein, L. Miao, and L. Cai Potential role for Nrf2 activation in the therapeutic effect of MG132 on diabetic nephropathy in OVE26 diabetic mice Am. J. Physiol. Endocrinol. Metab. 304 2013 E87 E99
29. L. Cai, S. Chen, T. Evans, D.X. Deng, K. Mukherjee, and S. Chakrabarti Apoptotic germ-cell death and testicular damage in experimental diabetes: prevention by endothelin antagonism Urol. Res. 28 2000 342 347
30. J.W. Baynes, and S.R. Thorpe Role of oxidative stress in diabetic complications: a new perspective on an old paradigm Diabetes 48 1999 1 9
31. M.K. Badman, P. Pissios, A.R. Kennedy, G. Koukos, J.S. Flier, and E. Maratos-Flier Hepatic fibroblast growth factor 21 is regulated by PPARalpha and is a key mediator of hepatic lipid metabolism in ketotic states Cell Metab. 5 2007 426 437
32. W. Wente, A.M. Efanov, M. Brenner, A. Kharitonenkov, A. Koster, G.E. Sandusky, S. Sewing, I. Treinies, H. Zitzer, and J. Gromada Fibroblast growth factor-21 improves pancreatic beta-cell function and survival by activation of extracellular signal-regulated kinase 1/2 and Akt signaling pathways Diabetes 55 2006 2470 2478
33. X. Jiang, J. Chen, C. Zhang, Z. Zhang, Y. Tan, W. Feng, M. Skibba, Y. Xin, and L. Cai The protective effect of FGF21 on diabetes-induced male germ cell apoptosis is associated with up-regulated testicular AKT and AMPK/Sirt1/PGC-1alpha signaling Endocrinology 156 2015 1156 1170
34. F. Rizvi, S. Shukla, and P. Kakkar Essential role of PH domain and leucine-rich repeat protein phosphatase 2 in Nrf2 suppression via modulation of Akt/GSK3beta/Fyn kinase axis during oxidative hepatocellular toxicity Cell Death Dis. 5 2014 e1153
35. B. Li, W. Cui, Y. Tan, P. Luo, Q. Chen, C. Zhang, W. Qu, L. Miao, and L. Cai Zinc is essential for the transcription function of Nrf2 in human renal tubule cells in vitro and mouse kidney in vivo under the diabetic condition J. Cell. Mol. Med. 18 2014 895 906
36. C.W. Park, H.W. Kim, S.H. Ko, H.W. Chung, S.W. Lim, C.W. Yang, Y.S. Chang, A. Sugawara, Y. Guan, and M.D. Breyer Accelerated diabetic nephropathy in mice lacking the peroxisome proliferator-activated receptor alpha Diabetes 55 2006 885 893
37. C. Galman, T. Lundasen, A. Kharitonenkov, H.A. Bina, M. Eriksson, I. Hafstrom, M. Dahlin, P. Amark, B. Angelin, and M. Rudling The circulating metabolic regulator FGF21 is induced by prolonged fasting and PPARalpha activation in man Cell Metab. 8 2008 169 174
38. K.L. Ong, K.A. Rye, R. O'Connell, A.J. Jenkins, C. Brown, A. Xu, D.R. Sullivan, P.J. Barter, A.C. Keech, and F.S. Investigators Long-term fenofibrate therapy increases fibroblast growth factor 21 and retinol-binding protein 4 in subjects with type 2 diabetes J. Clin. Endocrinol. Metab. 97 2012 4701 4708
39. H.W. Kim, J.E. Lee, J.J. Cha, Y.Y. Hyun, J.E. Kim, M.H. Lee, H.K. Song, D.H. Nam, J.Y. Han, S.Y. Han, K.H. Han, Y.S. Kang, and D.R. Cha Fibroblast growth factor 21 improves insulin resistance and ameliorates renal injury in db/db mice Endocrinology 154 2013 3366 3376
40. I. Loeffler, U. Hopfer, D. Koczan, and G. Wolf Type VIII collagen modulates TGF-beta1-induced proliferation of mesangial cells J. Am. Soc. Nephrol. 22 2011 649 663
41. M.K. Brahma, R.C. Adam, N.M. Pollak, D. Jaeger, K.A. Zierler, N. Pocher, R. Schreiber, M. Romauch, T. Moustafa, S. Eder, T. Ruelicke, K. Preiss-Landl, A. Lass, R. Zechner, and G. Haemmerle Fibroblast growth factor 21 is induced upon cardiac stress and alters cardiac lipid homeostasis J. Lipid Res. 55 2014 2229 2241
42. A. Planavila, I. Redondo, E. Hondares, M. Vinciguerra, C. Munts, R. Iglesias, L.A. Gabrielli, M. Sitges, M. Giralt, M. van Bilsen, and F. Villarroya Fibroblast growth factor 21 protects against cardiac hypertrophy in mice Nat. Commun. 4 2013 2019
43. W.T. Cong, J. Ling, H.S. Tian, R. Ling, Y. Wang, B.B. Huang, T. Zhao, Y.M. Duan, L.T. Jin, and X.K. Li Proteomic study on the protective mechanism of fibroblast growth factor 21 to ischemia-reperfusion injury Can. J. Physiol. Pharmacol. 91 2013 973 984
44. C. Zhang, M. Shao, H. Yang, L. Chen, L. Yu, W. Cong, H. Tian, F. Zhang, P. Cheng, L. Jin, Y. Tan, X. Li, L. Cai, and X. Lu Attenuation of hyperlipidemia- and diabetes-induced early-stage apoptosis and late-stage renal dysfunction via administration of fibroblast growth factor-21 is associated with suppression of renal inflammation PLoS One 8 2013 e82275
45. P.E. Pergola, M. Krauth, J.W. Huff, D.A. Ferguson, S. Ruiz, C.J. Meyer, and D.G. Warnock Effect of bardoxolone methyl on kidney function in patients with T2D and stage 3b-4 CKD Am. J. Nephrol. 33 2011 469 476
46. P.E. Pergola, P. Raskin, R.D. Toto, C.J. Meyer, J.W. Huff, E.B. Grossman, M. Krauth, S. Ruiz, P. Audhya, H. Christ-Schmidt, J. Wittes, D.G. Warnock, and B.S. Investigators Bardoxolone methyl and kidney function in CKD with type 2 diabetes N. Engl. J. Med. 365 2011 327 336
47. D. de Zeeuw, T. Akizawa, P. Audhya, G.L. Bakris, M. Chin, H. Christ-Schmidt, A. Goldsberry, M. Houser, M. Krauth, H.J. Lambers Heerspink, J.J. McMurray, C.J. Meyer, H.H. Parving, G. Remuzzi, R.D. Toto, N.D. Vaziri, C. Wanner, J. Wittes, D. Wrolstad, G.M. Chertow, and B.T. Investigators Bardoxolone methyl in type 2 diabetes and stage 4 chronic kidney disease N. Engl. J. Med. 369 2013 2492 2503
48. D.V. Chartoumpekis, P.G. Ziros, A.I. Psyrogiannis, A.G. Papavassiliou, V.E. Kyriazopoulou, G.P. Sykiotis, and I.G. Habeos Nrf2 represses FGF21 during long-term high-fat diet-induced obesity in mice Diabetes 60 2011 2465 2473
49. Y. Furusawa, A. Uruno, Y. Yagishita, C. Higashi, and M. Yamamoto Nrf2 induces fibroblast growth factor 21 in diabetic mice Genes Cells 19 2014 864 878
50. J.H. Koo, W.H. Lee, C.G. Lee, and S.G. Kim Fyn inhibition by cycloalkane-fused 1,2-dithiole-3-thiones enhances antioxidant capacity and protects mitochondria from oxidative injury Mol. Pharmacol. 82 2012 27 36
51. A.K. Jain, and A.K. Jaiswal GSK-3beta acts upstream of Fyn kinase in regulation of nuclear export and degradation of NF-E2 related factor 2 J. Biol. Chem. 282 2007 16502 16510