Farnesoid X receptor protects against kidney injury in uninephrectomized obese mice

Journal of Biological Chemistry

Volumn 291, Issue 5, 2016, Pages 2397-2411

  Gai, Zhibo ^a   Gui, Ting ^b   Hiller, Christian ^a   Kullak Ublick, Gerd A ^a  

^a UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^b UNIVERSITY OF BERN   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CELL DEATH; CELL MEMBRANES; CHEMICAL ACTIVATION; MAMMALS; MEDICAL PROBLEMS; METABOLISM; NUTRITION; PEPTIDES; PROTEINS;

ENDOPLASMIC RETICULUM STRESS; FARNESOID X RECEPTORS; GLUTATHIONE METABOLISM; MITOCHONDRIAL FUNCTION; MITOCHONDRIAL RESPIRATORY CHAIN; REACTIVE OXYGEN SPECIES; RENAL PROXIMAL TUBULAR CELLS; THERAPEUTIC POTENTIALS;

FATTY ACIDS;

4 HYDROXYNONENAL; FARNESOID X RECEPTOR; GLUCOSE REGULATED PROTEIN 78; GLUTATHIONE; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; REACTIVE OXYGEN METABOLITE; 4-HYDROXY-2-NONENAL; ALDEHYDE; BILE ACID; CCAAT ENHANCER BINDING PROTEIN; CEBPA PROTEIN, MOUSE; CELL RECEPTOR; CHENODEOXYCHOLIC ACID; FARNESOID X-ACTIVATED RECEPTOR; FATTY ACID; HEAT SHOCK PROTEIN; LIPID; MOLECULAR CHAPERONE GRP78; OBETICHOLIC ACID;

ADULT; ALBUMINURIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; FATTY ACID OXIDATION; FATTY LIVER; FEMALE; GLOMERULOSCLEROSIS; HUMAN; HUMAN TISSUE; HYPERLIPIDEMIA; IMMUNOHISTOCHEMISTRY; KIDNEY FIBROSIS; KIDNEY FUNCTION; KIDNEY INJURY; KIDNEY PROXIMAL TUBULE; LIPID PEROXIDATION; LIPID STORAGE; MALE; MIDDLE AGED; MOUSE; NONHUMAN; OBESITY; OXIDATIVE STRESS; PRIORITY JOURNAL; RENAL PROTECTION; RESPIRATORY CHAIN; ANALOGS AND DERIVATIVES; ANIMAL; C57BL MOUSE; CHEMISTRY; GENETICS; INJURIES; KIDNEY; KIDNEY DISEASE; KIDNEY TUBULE; LIPID DIET; LIPID METABOLISM; METABOLISM; MOUSE MUTANT; NEPHRECTOMY; NONALCOHOLIC FATTY LIVER; PATHOLOGY; PATHOPHYSIOLOGY;

ALDEHYDES; ANIMALS; BILE ACIDS AND SALTS; CCAAT-ENHANCER-BINDING PROTEINS; CHENODEOXYCHOLIC ACID; DIET, HIGH-FAT; ENDOPLASMIC RETICULUM STRESS; FATTY ACIDS, NONESTERIFIED; FEMALE; GLUTATHIONE; HEAT-SHOCK PROTEINS; HUMANS; KIDNEY; KIDNEY DISEASES; KIDNEY TUBULES; LIPID METABOLISM; LIPID PEROXIDATION; LIPIDS; MALE; MICE; MICE, INBRED C57BL; MICE, OBESE; MIDDLE AGED; NEPHRECTOMY; NON-ALCOHOLIC FATTY LIVER DISEASE; OBESITY; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; RECEPTORS, CYTOPLASMIC AND NUCLEAR;

EID: 84956970185     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.694323     Document Type: Article

References (53)

1. Wang, Y., Chen, X., Song, Y., Caballero, B., and Cheskin, L. J. (2008) Association between obesity and kidney disease: a systematic review and meta-analysis. Kidney Int. 73, 19-33
2. Kambham, N., Markowitz, G. S., Valeri, A. M., Lin, J., and D'Agati, V. D. (2001) Obesity-related glomerulopathy: an emerging epidemic. Kidney Int. 59, 1498-1509
3. de Vries, A. P., Ruggenenti, P., Ruan, X. Z., Praga, M., Cruzado, J. M., Bajema, I. M., D'Agati, V. D., Lamb, H. J., Pongrac Barlovic, D., Hojs, R., Abbate, M., Rodriquez, R., Mogensen, C. E., Porrini, E., and ERA-EDTA Working Group Diabesity (2014) Fatty kidney: emerging role of ectopic lipid in obesity-related renal disease. Lancet Diabetes Endocrinol. 2, 417-426
4. Abrass, C. K. (2004) Overview: obesity: what does it have to do with kidney disease? J. Am. Soc. Nephrol. 15, 2768-2772
5. Bagby, S. P. (2004) Obesity-initiated metabolic syndrome and the kidney: a recipe for chronic kidney disease? J. Am. Soc. Nephrol. 15, 2775-2791
6. Gin, H., Rigalleau, V., and Aparicio, M. (2000) Lipids, protein intake, and diabetic nephropathy. Diabetes Metab. 26, Suppl. 4, 45-53
7. Bonnet, F., and Cooper, M. E. (2000) Potential influence of lipids in diabetic nephropathy: insights from experimental data and clinical studies. Diabetes Metab. 26, 254-264
8. Wang, Z., Jiang, T., Li, J., Proctor, G., McManaman, J. L., Lucia, S., Chua, S., and Levi, M. (2005) Regulation of renal lipid metabolism, lipid accumulation, and glomerulosclerosis in FVBdb/db mice with type 2 diabetes. Diabetes 54, 2328-2335
9. Brookheart, R. T., Michel, C. I., and Schaffer, J. E. (2009) As a matter of fat. Cell Metab. 10, 9-12
10. Neuschwander-Tetri, B. A. (2010) Hepatic lipotoxicity and the pathogenesis of nonalcoholic steatohepatitis: the central role of nontriglyceride fatty acid metabolites. Hepatology 52, 774-788
11. Weinberg, J. M. (2006) Lipotoxicity. Kidney Int. 70, 1560-1566
12. Jaimes, E. A., Hua, P., Tian, R. X., and Raij, L. (2010) Human glomerular endothelium: interplay among glucose, free fatty acids, angiotensin II, and oxidative stress. Am. J. Physiol. Renal. Physiol. 298, F125-F132
13. Fujii, H., Kono, K., Nakai, K., Goto, S., Komaba, H., Hamada, Y., Shinohara, M., Kitazawa, R., Kitazawa, S., and Fukagawa, M. (2010) Oxidative and nitrosative stress and progression of diabetic nephropathy in type 2 diabetes. Am. J. Nephrol. 31, 342-352
14. Oberg, B. P., McMenamin, E., Lucas, F. L., McMonagle, E., Morrow, J., Ikizler, T. A., and Himmelfarb, J. (2004) Increased prevalence of oxidant stress and inflammation in patients with moderate to severe chronic kidney disease. Kidney Int. 65, 1009-1016
15. Habibi, J., Hayden, M. R., Sowers, J. R., Pulakat, L., Tilmon, R. D., Manrique, C., Lastra, G., Demarco, V. G., and Whaley-Connell, A. (2011) Nebivolol attenuates redox-sensitive glomerular and tubular mediated proteinuria in obese rats. Endocrinology 152, 659-668
16. Tang, J., Yan, H., and Zhuang, S. (2012) Inflammation and oxidative stress in obesity-related glomerulopathy. Int. J. Nephrol. 2012, 608397
17. Cho, E. J., Yoon, J. H., Kwak, M. S., Jang, E. S., Lee, J. H., Yu, S. J., Kim, Y. J., Kim, C. Y., and Lee, H. S. (2014) Tauroursodeoxycholic acid attenuates progression of steatohepatitis in mice fed a methionine-choline-deficient diet. Dig. Dis. Sci. 59, 1461-1474
18. Hu, Z., Ren, L., Wang, C., Liu, B., and Song, G. (2012) Effect of chenodeoxycholic acid on fibrosis, inflammation and oxidative stress in kidney in high-fructose-fed Wistar rats. Kidney Blood Press. Res. 36, 85-97
19. Fiorucci, S., Rizzo, G., Antonelli, E., Renga, B., Mencarelli, A., Riccardi, L., Orlandi, S., Pruzanski, M., Morelli, A., and Pellicciari, R. (2005) A farnesoid X receptor-small heterodimer partner regulatory cascade modulates tissue metalloproteinase inhibitor-1 and matrix metalloprotease expression in hepatic stellate cells and promotes resolution of liver fibrosis. J. Pharmacol. Exp. Ther. 314, 584-595
20. Jiang, T., Wang, X. X., Scherzer, P., Wilson, P., Tallman, J., Takahashi, H., Li, J., Iwahashi, M., Sutherland, E., Arend, L., and Levi, M. (2007) Farnesoid X receptor modulates renal lipid metabolism, fibrosis, and diabetic nephropathy. Diabetes 56, 2485-2493
21. Wang, X. X., Jiang, T., Shen, Y., Adorini, L., Pruzanski, M., Gonzalez, F. J., Scherzer, P., Lewis, L., Miyazaki-Anzai, S., and Levi, M. (2009) The farnesoid X receptor modulates renal lipid metabolism and diet-induced renal inflammation, fibrosis, and proteinuria. Am. J. Physiol. Renal. Physiol. 297, F1587-F1596
22. Pellicciari, R., Fiorucci, S., Camaioni, E., Clerici, C., Costantino, G., Maloney, P. R., Morelli, A., Parks, D. J., and Willson, T. M. (2002) 6alpha-ethylchenodeoxycholic acid (6-ECDCA), a potent and selective FXR agonist endowed with anticholestatic activity. J. Med. Chem. 45, 3569-3572
23. Gai, Z., Hiller, C., Chin, S. H., Hofstetter, L., Stieger, B., Konrad, D., and Kullak-Ublick, G. A. (2014) Uninephrectomy augments the effects of high fat diet induced obesity on gene expression in mouse kidney. Biochim. Biophys. Acta 1842, 1870-1878
24. González, E., Gutiérrez, E., Morales, E., Hernández, E., Andres, A., Bello, I., Díaz-González, R., Leiva, O., and Praga, M. (2005) Factors influencing the progression of renal damage in patients with unilateral renal agenesis and remnant kidney. Kidney Int. 68, 263-270
25. Gai, Z., Zhou, G., Gui, T., Itoh, S., Oikawa, K., Uetani, K., and Muragaki, Y. (2010) Trps1 haploinsufficiency promotes renal fibrosis by increasing Arkadia expression. J. Am. Soc. Nephrol. 21, 1468-1476
26. Soumura, M., Kume, S., Isshiki, K., Takeda, N., Araki, S., Tanaka, Y., Sugimoto, T., Chin-Kanasaki, M., Nishio, Y., Haneda, M., Koya, D., Kashiwagi, A., Maegawa, H., and Uzu, T. (2010) Oleate and eicosapentaenoic acid attenuate palmitate-induced inflammation and apoptosis in renal proximal tubular cell. Biochem. Biophys. Res. Commun. 402, 265-271
27. Tanaka, Y., Kume, S., Araki, S., Isshiki, K., Chin-Kanasaki, M., Sakaguchi, M., Sugimoto, T., Koya, D., Haneda, M., Kashiwagi, A., Maegawa, H., and Uzu, T. (2011) Fenofibrate, a PPARα agonist, has renoprotective effects in mice by enhancing renal lipolysis. Kidney Int. 79, 871-882
28. Kume, S., Uzu, T., Araki, S., Sugimoto, T., Isshiki, K., Chin-Kanasaki, M., Sakaguchi, M., Kubota, N., Terauchi, Y., Kadowaki, T., Haneda, M., Kashiwagi, A., and Koya, D. (2007) Role of altered renal lipid metabolism in the development of renal injury induced by a high-fat diet. J. Am. Soc. Nephrol. 18, 2715-2723
29. -/- mice with chronic kidney disease. Circ. Res. 106, 1807-1817
30. Ozcan, U., Yilmaz, E., Ozcan, L., Furuhashi, M., Vaillancourt, E., Smith, R. O., Görgün, C. Z., and Hotamisligil, G. S. (2006) Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science 313, 1137-1140
31. Fang, L., Zhou, Y., Cao, H., Wen, P., Jiang, L., He, W., Dai, C., and Yang, J. (2013) Autophagy attenuates diabetic glomerular damage through protection of hyperglycemia-induced podocyte injury. PloS One 8, e60546
32. Yamahara, K., Kume, S., Koya, D., Tanaka, Y., Morita, Y., Chin-Kanasaki, M., Araki, H., Isshiki, K., Araki, S., Haneda, M., Matsusaka, T., Kashiwagi, A., Maegawa, H., and Uzu, T. (2013) Obesity-mediated autophagy insufficiency exacerbates proteinuria-induced tubulointerstitial lesions. J. Am. Soc. Nephrol. 24, 1769-1781
33. Ozcan, U., Cao, Q., Yilmaz, E., Lee, A. H., Iwakoshi, N. N., Ozdelen, E., Tuncman, G., Görgün, C., Glimcher, L. H., and Hotamisligil, G. S. (2004) Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science 306, 457-461
34. Zhan, L., Liu, H. X., Fang, Y., Kong, B., He, Y., Zhong, X. B., Fang, J., Wan, Y. J., and Guo, G. L. Genome-wide binding and transcriptome analysis of human farnesoid X receptor in primary human hepatocytes. PloS One 9, e105930
35. Wang, X. X., Jiang, T., Shen, Y., Caldas, Y., Miyazaki-Anzai, S., Santamaria, H., Urbanek, C., Solis, N., Scherzer, P., Lewis, L., Gonzalez, F. J., Adorini, L., Pruzanski, M., Kopp, J. B., Verlander, J. W., and Levi, M. (2010) Diabetic nephropathy is accelerated by farnesoid X receptor deficiency and inhibited by farnesoidXreceptor activation in a type 1 diabetes model. Diabetes 59, 2916-2927
36. Sun, L., Halaihel, N., Zhang, W., Rogers, T., and Levi, M. (2002) Role of sterol regulatory element-binding protein 1 in regulation of renal lipid metabolism and glomerulosclerosis in diabetes mellitus. J. Biol. Chem. 277, 18919-18927
37. Deji, N., Kume, S., Araki, S., Soumura, M., Sugimoto, T., Isshiki, K., Chin-Kanasaki, M., Sakaguchi, M., Koya, D., Haneda, M., Kashiwagi, A., and Uzu, T. (2009) Structural and functional changes in the kidneys of high-fat diet-induced obese mice. Am. J. Physiol. Renal. Physiol. 296, F118-F126
38. Halliwell, B. (1991) Reactive oxygen species in living systems: source, biochemistry, and role in human disease. Am. J. Med. 91, 14S-22S
39. Declèves, A. E., Zolkipli, Z., Satriano, J., Wang, L., Nakayama, T., Rogac, M., Le, T. P., Nortier, J. L., Farquhar, M. G., Naviaux, R. K., and Sharma, K. (2014) Regulation of lipid accumulation by AMP-activated kinase [corrected] in high fat diet-induced kidney injury. Kidney Int. 85, 611-623
40. Che, R., Yuan, Y., Huang, S., and Zhang, A. (2014) Mitochondrial dysfunction in the pathophysiology of renal diseases. Am. J. Physiol. Renal. Physiol. 306, F367-F378
41. Sharma, K., Karl, B., Mathew, A. V., Gangoiti, J. A., Wassel, C. L., Saito, R., Pu, M., Sharma, S., You, Y. H., Wang, L., Diamond-Stanic, M., Lindenmeyer, M. T., Forsblom, C., Wu, W., Ix, J. H., Ideker, T., Kopp, J. B., Nigam, S. K., Cohen, C. D., Groop, P. H., Barshop, B. A., Natarajan, L., Nyhan, W. L., and Naviaux, R. K. (2013) Metabolomics reveals signature of mitochondrial dysfunction in diabetic kidney disease. J. Am. Soc. Nephrol. 24, 1901-1912
42. Kang, H. M., Ahn, S. H., Choi, P., Ko, Y. A., Han, S. H., Chinga, F., Park, A. S., Tao, J., Sharma, K., Pullman, J., Bottinger, E. P., Goldberg, I. J., and Susztak, K. (2015) Defective fatty acid oxidation in renal tubular epithelial cells has a key role in kidney fibrosis development. Nat. Med. 21, 37-46
43. Dugan, L. L., You, Y. H., Ali, S. S., Diamond-Stanic, M., Miyamoto, S., DeCleves, A. E., Andreyev, A., Quach, T., Ly, S., Shekhtman, G., Nguyen, W., Chepetan, A., Le, T. P., Wang, L., Xu, M., Paik, K. P., Fogo, A., Viollet, B., Murphy, A., Brosius, F., Naviaux, R. K., and Sharma, K. (2013) AMPK dysregulation promotes diabetes-related reduction of superoxide and mitochondrial function. J. Clin. Invest. 123, 4888-4899
44. Buchberger, A., Bukau, B., and Sommer, T. (2010) Protein quality control in the cytosol and the endoplasmic reticulum: brothers in arms. Mol. Cell 40, 238-252
45. Nelson, D. and Cox, M. (2005) Lehninger Principles of Biochemistry, 4th Ed., pp. 647-650, W. H. Freeman and Co., New York
46. Sieber, J., Lindenmeyer, M. T., Kampe, K., Campbell, K. N., Cohen, C. D., Hopfer, H., Mundel, P., and Jehle, A. W. (2010) Regulation of podocyte survival and endoplasmic reticulum stress by fatty acids. Am. J. Physiol. Renal. Physiol. 299, F821-F829
47. Cao, Y., Hao, Y., Li, H., Liu, Q., Gao, F., Liu, W., and Duan, H. (2014) Role of endoplasmic reticulum stress in apoptosis of differentiated mouse podocytes induced by high glucose. Int. J. Mol. Med. 33, 809-816
48. Bernales, S., Schuck, S., and Walter, P. (2007) ER-phagy: selective autophagy of the endoplasmic reticulum. Autophagy 3, 285-287
49. Choi, B. H., Kang, K. S., and Kwak, M. K. (2014) Effect of redox modulating NRF2 activators on chronic kidney disease. Molecules 19, 12727-12759
50. Tan, S. M., Sharma, A., Stefanovic, N., Yuen, D. Y., Karagiannis, T. C., Meyer, C., Ward, K. W., Cooper, M. E., and de Haan, J. B. (2014) Derivative of bardoxolone methyl, dh404, in an inverse dose-dependent manner lessens diabetes-associated atherosclerosis and improves diabetic kidney disease. Diabetes 63, 3091-3103
51. Cipriani, S., Mencarelli, A., Palladino, G., and Fiorucci, S. (2010) FXR activation reverses insulin resistance and lipid abnormalities and protects against liver steatosis in Zucker (fa/fa) obese rats. J. Lipid Res. 51, 771-784
52. Dröse, S., and Brandt, U. (2012) Molecular mechanisms of superoxide production by the mitochondrial respiratory chain. Adv. Exp. Med. Biol. 748, 145-169
53. Praga, M., and Morales, E. (2006) Obesity, proteinuria and progression of renal failure. Curr. Opin. Nephrol. Hypertens. 15, 481-486