Diabetic nephropathy is accelerated by farnesoid X receptor deficiency and inhibited by farnesoid X receptor activation in a type 1 diabetes model

Diabetes

Volumn 59, Issue 11, 2010, Pages 2916-2927

  Wang, Xiaoxin X ^a   Jiang, Tao ^a   Shen, Yan ^a   Caldas, Yupanqui ^a   Miyazaki Anzai, Shinobu ^a   Santamaria, Hannah ^a   Urbanek, Cydney ^a   Solis, Nathaniel ^a   Scherzer, Pnina ^b   Lewis, Linda ^a   Gonzalez, Frank J ^c   Adorini, Luciano ^d   Pruzanski, Mark ^d   Kopp, Jeffrey B ^e   Verlander, Jill W ^f   Levi, Moshe ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

^c NATIONAL CANCER INSTITUTE   (United States)

^d INTERCEPT PHARMACEUTICALS   (United States)

^e NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^f UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

6ALPHA ETHYLCHENODEOXYCHOLIC ACID; CHENODEOXYCHOLIC ACID DERIVATIVE; FARNESOID X RECEPTOR; INT 747; STEROL REGULATORY ELEMENT BINDING PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIABETIC NEPHROPATHY; GLOMERULOSCLEROSIS; HYPERGLYCEMIA; INSULIN DEFICIENCY; INSULIN DEPENDENT DIABETES MELLITUS; KIDNEY FIBROSIS; KIDNEY INJURY; LIPID METABOLISM; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEINURIA; STREPTOZOCIN DIABETES;

ANIMALS; CROSSES, GENETIC; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 1; DIABETIC NEPHROPATHIES; DNA PRIMERS; FEMALE; FOAM CELLS; KIDNEY; KIDNEY GLOMERULUS; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED DBA; MICE, KNOCKOUT; POLYMERASE CHAIN REACTION; RECEPTORS, CYTOPLASMIC AND NUCLEAR;

EID: 78049299629     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db10-0019     Document Type: Article

References (51)

1. United States Renal Data System. Atlas of end-stage renal disease in the United States. In USRDS 2009 Annual Data Report. Bethesda, MD, 2009. Available from http://www.usrds.org/adr.htm. Accessed 24 August 2010
2. Brownlee M. The pathobiology of diabetic complications: a unifying mechanism. Diabetes 2005;54:1615-1625 (Pubitemid 40770750)
3. Qian Y, Feldman E, Pennathur S, Kretzler M, Brosius FC 3rd. From fibrosis to sclerosis: mechanisms of glomerulosclerosis in diabetic nephropathy. Diabetes 2008;57:1439-1445
4. Sun L, Halaihel N, Zhang W, Rogers T, Levi M. Role of sterol regulatory element-binding protein 1 in regulation of renal lipid metabolism and glomerulosclerosis in diabetes mellitus. J Biol Chem 2002;277:18919-18927
5. Wang Z, Jiang T, Li J, Proctor G, McManaman JL, Lucia S, Chua S, Levi M. Regulation of renal lipid metabolism, lipid accumulation, and glomerulosclerosis in FVB db/db mice with type 2 diabetes. Diabetes 2005;54:2328-2335 (Pubitemid 41134259)
6. Proctor G, Jiang T, Iwahashi M, Wang Z, Li J, Levi M. Regulation of renal fatty acid and cholesterol metabolism, inflammation, and fibrosis in Akita and OVE26 mice with type 1 diabetes. Diabetes 2006;55:2502-2509 (Pubitemid 44871150)
7. Jiang T, Wang XX, Scherzer P, Wilson P, Tallman J, Takahashi H, Li J, Iwahashi M, Sutherland E, Arend L, Levi M. Farnesoid X receptor modulates renal lipid metabolism, fibrosis, and diabetic nephropathy. Diabetes 2007;56:2485-2493 (Pubitemid 47523255)
8. Ishigaki N, Yamamoto T, Shimizu Y, Kobayashi K, Yatoh S, Sone H, Takahashi A, Suzuki H, Yamagata K, Yamada N, Shimano H. Involvement of glomerular SREBP-1c in diabetic nephropathy. Biochem Biophys Res Commun 2007;364:502-508 (Pubitemid 350026495)
9. Jiang T, Wang Z, Proctor G, Moskowitz S, Liebman SE, Rogers T, Lucia MS, Li J, Levi M. Diet-induced obesity in C57BL/6J mice causes increased renal lipid accumulation and glomerulosclerosis via a sterol regulatory element-binding protein-1c-dependent pathway. J Biol Chem 2005;280:32317-32325
10. Watanabe M, Houten SM, Wang L, Moschetta A, Mangelsdorf DJ, Heyman RA, Moore DD, Auwerx J. Bile acids lower triglyceride levels via a pathway involving FXR, SHP, and SREBP-1c. J Clin Invest 2004;113:1408-1418
11. Zhang Y, Castellani LW, Sinal CJ, Gonzalez FJ, Edwards PA. Peroxisome proliferator-activated receptor-gamma coactivator 1α (PGC-1α) regulates triglyceride metabolism by activation of the nuclear receptor FXR. Genes Dev 2004;18:157-169
12. Wang XX, Jiang T, Shen Y, Adorini L, Pruzanski M, Gonzalez FJ, Scherzer P, Lewis L, Miyazaki-Anzai S, Levi M. The farnesoid X receptor modulates renal lipid metabolism and diet-induced renal inflammation, fibrosis, and proteinuria. Am J Physiol Renal Physiol 2009;297:F1587-F1596
13. Sinal CJ, Tohkin M, Miyata M, Ward JM, Lambert G, Gonzalez FJ. Targeted disruption of the nuclear receptor FXR/BAR impairs bile acid and lipid homeostasis. Cell 2000;102:731-744
14. Pellicciari R, Fiorucci S, Camaioni E, Clerici C, Costantino G, Maloney PR, Morelli A, Parks DJ, Willson TM. 6α-ethyl-chenodeoxycholic acid (6-ECDCA), a potent and selective FXR agonist endowed with anticholestatic activity. J Med Chem 2002;45:3569-3572
15. Qi Z, Fujita H, Jin J, Davis LS, Wang Y, Fogo AB, Breyer MD. Characterization of susceptibility of inbred mouse strains to diabetic nephropathy. Diabetes 2005;54:2628-2637 (Pubitemid 41233584)
16. Jefferson JA, Shankland SJ, Pichler RH. Proteinuria in diabetic kidney disease: a mechanistic viewpoint. Kidney Int 2008;74:22-36 (Pubitemid 351841893)
17. Ly J, Alexander M, Quaggin SE. A podocentric view of nephrology. Curr Opin Nephrol Hypertens 2004;13:299-305
18. Mundel P, Heid HW, Mundel TM, Kruger M, Reiser J, Kriz W. Synaptopodin: an actin-associated protein in telencephalic dendrites and renal podocytes. J Cell Biol 1997;139:193-204 (Pubitemid 27444091)
19. Strutz F, Zeisberg M. Renal fibroblasts and myofibroblasts in chronic kidney disease. J Am Soc Nephrol 2006;17:2992-2998
20. Bottinger EP. TGF-β in renal injury and disease. Semin Nephrol 2007;27: 309-320
21. Kato M, Zhang J, Wang M, Lanting L, Yuan H, Rossi JJ, Natarajan R. MicroRNA-192 in diabetic kidney glomeruli and its function in TGF-β-induced collagen expression via inhibition of E-box repressors. Proc Natl Acad Sci U S A 2007;104:3432-3437
22. van Rooij E, Sutherland LB, Thatcher JE, DiMaio JM, Naseem RH, Marshall WS, Hill JA, Olson EN. Dysregulation of microRNAs after myocardial infarction reveals a role of miR-29 in cardiac fibrosis. Proc Natl Acad Sci U S A 2008;105:13027-13032
23. Niranjan T, Bielesz B, Gruenwald A, Ponda MP, Kopp JB, Thomas DB, Susztak K. The Notch pathway in podocytes plays a role in the development of glomerular disease. Nat Med 2008;14:290-298
24. Hirano T. Lipoprotein abnormalities in diabetic nephropathy. Kidney Int 1999;71(Suppl.):S22-S24
25. Krolewski AS, Warram JH, Christlieb AR. Hypercholesterolemia-a determinant of renal function loss and deaths in IDDM patients with nephropathy. Kidney Int 1994;45 (Suppl.):S125-S131
26. Zhang Y, Lee FY, Barrera G, Lee H, Vales C, Gonzalez FJ, Willson TM, Edwards PA. Activation of the nuclear receptor FXR improves hyperglycemia and hyperlipidemia in diabetic mice. Proc Natl Acad Sci U S A 2006;103:1006-1011
27. Lambert G, Amar MJ, Guo G, Brewer HB, Jr, Gonzalez FJ, Sinal CJ. The farnesoid X-receptor is an essential regulator of cholesterol homeostasis. J Biol Chem 2003;278:2563-2570
28. Raghow R, Yellaturu C, Deng X, Park EA, Elam MB. SREBPs: the crossroads of physiological and pathological lipid homeostasis. Trends Endocrinol Metab 2008;19:65-73 (Pubitemid 351317897)
29. 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, Koya D. Role of altered renal lipid metabolism in the development of renal injury induced by a high-fat diet. J Am Soc Nephrol 2007;18:2715-2723 (Pubitemid 47531198)
30. Bookout AL, Jeong Y, Downes M, Yu RT, Evans RM, Mangelsdorf DJ. Anatomical profiling of nuclear receptor expression reveals a hierarchical transcriptional network. Cell 2006;126:789-799 (Pubitemid 44233630)
31. Abrass CK. Cellular lipid metabolism and the role of lipids in progressive renal disease. Am J Nephrol 2004;24:46-53
32. Weinberg JM. Lipotoxicity. Kidney Int 2006;70:1560-1566
33. Prieur X, Roszer T, Ricote M: Lipotoxicity in macrophages: evidence from diseases associated with the metabolic syndrome. Biochim Biophys Acta 2010;1801:327-337
34. Ruan XZ, Varghese Z, Moorhead JF. An update on the lipid nephrotoxicity hypothesis. Nat Rev Nephrol 2009;5:713-721
35. Harnish D, Hahn A, Hartman H, Huard C, Martinez R, Mahaney P, Evans M, Zhang S. The farnesoid X receptor (FXR) antagonizes oxidized LDL receptor, LOX-1, activation (Abstract). Circulation 2007;116:II-161
36. Kelly KJ, Wu P, Patterson CE, Temm C, Dominguez JH. LOX-1 and inflammation: a new mechanism for renal injury in obesity and diabetes. Am J Physiol Renal Physiol 2008;294:F1136-F1145
37. Paul A, Chang BH, Li L, Yechoor VK, Chan L. Deficiency of adipose differentiation-related protein impairs foam cell formation and protects against atherosclerosis. Circ Res 2008;102:1492-1501
38. Galkina E, Ley K. Leukocyte recruitment and vascular injury in diabetic nephropathy. J Am Soc Nephrol 2006;17:368-377
39. Chow F, Ozols E, Nikolic-Paterson DJ, Atkins RC, Tesch GH. Macrophages in mouse type 2 diabetic nephropathy: correlation with diabetic state and progressive renal injury. Kidney Int 2004;65:116-128
40. Sassy-Prigent C, Heudes D, Mandet C, Belair MF, Michel O, Perdereau B, Bariety J, Bruneval P. Early glomerular macrophage recruitment in streptozotocin-induced diabetic rats. Diabetes 2000;49:466-475
41. Chow FY, Nikolic-Paterson DJ, Atkins RC, Tesch GH. Macrophages in streptozotocin-induced diabetic nephropathy: potential role in renal fibrosis. Nephrol Dial Transplant 2004;19:2987-2996
42. Li YT, Swales KE, Thomas GJ, Warner TD, Bishop-Bailey D. Farnesoid x receptor ligands inhibit vascular smooth muscle cell inflammation and migration. Arterioscler Thromb Vasc Biol 2007;27:2606-2611
43. Wang YD, Chen WD, Wang M, Yu D, Forman BM, Huang W. Farnesoid X receptor antagonizes nuclear factor κB in hepatic inflammatory response. Hepatology 2008;48:1632-1643
44. Schlondorff D, Banas B. The mesangial cell revisited: no cell is an island. J Am Soc Nephrol 2009;20:1179-1187
45. Li J, Wilson A, Kuruba R, Zhang Q, Gao X, He F, Zhang LM, Pitt BR, Xie W, Li S. FXR-mediated regulation of eNOS expression in vascular endothelial cells. Cardiovasc Res 2008;77:169-177 (Pubitemid 351195146)
46. Zhao HJ, Wang S, Cheng H, Zhang MZ, Takahashi T, Fogo AB, Breyer MD, Harris RC. Endothelial nitric oxide synthase deficiency produces accelerated nephropathy in diabetic mice. J Am Soc Nephrol 2006;17:2664-2669 (Pubitemid 44484656)
47. Nakagawa T, Sato W, Glushakova O, Heinig M, Clarke T, Campbell-Thompson M, Yuzawa Y, Atkinson MA, Johnson RJ, Croker B. Diabetic endothelial nitric oxide synthase knockout mice develop advanced diabetic nephropathy. J Am Soc Nephrol 2007;18:539-550
48. Brosius FC 3rd, Alpers CE, Bottinger EP, Breyer MD, Coffman TM, Gurley SB, Harris RC, Kakoki M, Kretzler M, Leiter EH, Levi M, McIndoe RA, Sharma K, Smithies O, Susztak K, Takahashi N, Takahashi T. Mouse models of diabetic nephropathy. J Am Soc Nephrol 2009;20: 2503-2512
49. Maruyama T, Miyamoto Y, Nakamura T, Tamai Y, Okada H, Sugiyama E, Nakamura T, Itadani H, Tanaka K. Identification of membrane-type receptor for bile acids (M-BAR). Biochem Biophys Res Commun 2002;298:714-719
50. Kawamata Y, Fujii R, Hosoya M, Harada M, Yoshida H, Miwa M, Fukusumi S, Habata Y, Itoh T, Shintani Y, Hinuma S, Fujisawa Y, Fujino M. A G protein-coupled receptor responsive to bile acids. J Biol Chem 2003;278: 9435-9440
51. Thomas C, Pellicciari R, Pruzanski M, Auwerx J, Schoonjans K. Targeting bile-acid signalling for metabolic diseases. Nat Rev Drug Discov 2008;7: 678-693