Liver X receptors preserve renal glomerular integrity under normoglycaemia and in diabetes in mice

Diabetologia

Volumn 57, Issue 2, 2014, Pages 435-446

  Patel, Monika ^a   Wang, Xiaoxin X ^b,c   Magomedova, Lilia ^a   John, Rohan ^d   Rasheed, Adil ^a   Santamaria, Hannah ^b,c   Wang, Weidong ^b,c   Tsai, Ricky ^a   Qiu, Liru ^b,c   Orellana, Arturo ^e   Advani, Andrew ^f,g   Levi, Moshe ^b,c   Cummins, Carolyn L ^a,g  

^a UNIVERSITY OF TORONTO   (Canada)

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

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

^d UNIVERSITY HEALTH NETWORK   (Canada)

^e YORK UNIVERSITY   (Canada)

^f ST MICHAEL'S HOSPITAL   (Canada)

^g Banting and Best Diabetes Centre   (Canada)

Author keywords

Cholesterol; Diabetic nephropathy; DMHCA; LDL; Liver x receptor

Indexed keywords

ALBUMIN; CHOLESTEROL; CREATININE; LIVER X RECEPTOR; NEPHRIN; TRIACYLGLYCEROL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DIABETIC NEPHROPATHY; GLUCOSE BLOOD LEVEL; HYPERGLYCEMIA; LIPID STORAGE; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; TRIACYLGLYCEROL BLOOD LEVEL; UPREGULATION;

ANIMALS; BLOTTING, WESTERN; CHOLESTEROL; CHOLIC ACIDS; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC NEPHROPATHIES; GENE EXPRESSION REGULATION; GLOMERULAR MESANGIUM; HYPERGLYCEMIA; LIPID METABOLISM; MALE; MICE; MICE, INBRED DBA; ORPHAN NUCLEAR RECEPTORS;

EID: 84893662034     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-013-3095-6     Document Type: Article

References (50)

1. U.S. Renal Data System (2012) USRDS 2012 annual data report: atlas of chronic kidney disease and end-stage renal disease in the United States. National Institutes of Health, National Institute of Diabetes and Digestive and Kidney Diseases, Bethesda
2. Bonnet F, Cooper ME (2000) Potential influence of lipids in diabetic nephropathy: insights from experimental data and clinical studies. Diabetes Metab 26:254-264
3. Diamond JR (1991) Analogous pathobiologic mechanisms in glomerulosclerosis and atherosclerosis. Kidney Int Suppl 31:S29-S34
4. Keane WF, Kasiske BL, O'Donnell MP (1988) Lipids and progressive glomerulosclerosis. A model analogous to atherosclerosis. Am J Nephrol 8:261-271
5. Moorhead JF, Chan MK, El-Nahas M, Varghese Z (1982) Lipid nephrotoxicity in chronic progressive glomerular and tubulo-interstitial disease. Lancet 2:1309-1311
6. Orchard TJ, Chang YF, Ferrell RE, Petro N, Ellis DE (2002) Nephropathy in type 1 diabetes: a manifestation of insulin resistance and multiple genetic susceptibilities? Further evidence from the Pittsburgh Epidemiology of Diabetes Complication Study. Kidney Int 62:963-970
7. Hovind P, Tarnow L, Rossing P et al (2004) Predictors for the development of microalbuminuria and macroalbuminuria in patients with type 1 diabetes: inception cohort study. BMJ 328:1105
8. de Boer IH, Rue TC, Cleary PA et al (2011) Long-term renal outcomes of patients with type 1 diabetes mellitus and microalbuminuria: an analysis of the Diabetes Control and Complications Trial/Epidemiology of Diabetes Interventions and Complications cohort. Arch Intern Med 171:412-420
9. Jenkins AJ, Lyons TJ, Zheng D et al (2003) Lipoproteins in the DCCT/EDIC cohort: associations with diabetic nephropathy. Kidney Int 64:817-828
10. Morton J, Zoungas S, Li Q et al (2012) Low HDL cholesterol and the risk of diabetic nephropathy and retinopathy: results of the ADVANCE study. Diabetes Care 35:2201-2206
11. Wang XX, Jiang T, Shen Y et al (2011) Diabetic nephropathy is accelerated by farnesoid X receptor deficiency and inhibited by farnesoid X receptor activation in a type 1 diabetes model. Diabetes 59:2916-2927
12. Shevalye H, Lupachyk S, Watcho P et al (2012) Prediabetic nephropathy as an early consequence of the high-calorie/high-fat diet: relation to oxidative stress. Endocrinology 153:1152-1161
13. Yokoyama M, Tanigawa K, Murata T et al (2010) Dietary polyunsaturated fatty acids slow the progression of diabetic nephropathy in streptozotocin- induced diabetic rats. Nutr Res 30:217-225
14. Onozato ML, Tojo A, Goto A, Fujita T (2004) Radical scavenging effect of gliclazide in diabetic rats fed with a high cholesterol diet. Kidney Int 65:951-960
15. Janowski BA, Willy PJ, Devi TR, Falck JR, Mangelsdorf DJ (1996) An oxysterol signalling pathway mediated by the nuclear receptor LXR alpha. Nature 383:728-731
16. Joseph SB, McKilligin E, Pei L et al (2002) Synthetic LXR ligand inhibits the development of atherosclerosis in mice. Proc Natl Acad Sci U S A 99:7604-7609
17. Zelcer N, Tontonoz P (2006) Liver X receptors as integrators of metabolic and inflammatory signaling. J Clin Invest 116:607-614
18. Zelcer N, Hong C, Boyadjian R, Tontonoz P (2009) LXR regulates cholesterol uptake through Idol-dependent ubiquitination of the LDL receptor. Science 325:100-104
19. Repa JJ, Mangelsdorf DJ (2002) The liver X receptor gene team: potential new players in atherosclerosis. Nat Med 8:1243-1248
20. Castrillo A, Joseph SB, Vaidya SA et al (2003) Crosstalk between LXR and toll-like receptor signaling mediates bacterial and viral antagonism of cholesterol metabolism. Mol Cell 12:805-816
21. Joseph SB, Bradley MN, Castrillo A et al (2004) LXR-dependent gene expression is important for macrophage survival and the innate immune response. Cell 119:299-309
22. Ogawa D, Stone JF, Takata Y et al (2005) Liver x receptor agonists inhibit cytokine-induced osteopontin expression in macrophages through interference with activator protein-1 signaling pathways. Circ Res 96:e59-e67
23. Repa JJ, Liang G, Ou J et al (2000) Regulation of mouse sterol regulatory element-binding protein-1c gene (SREBP-1c) by oxysterol receptors, LXRalpha and LXRbeta. Gene Dev 14:2819-2830
24. Quinet EM, Savio DA, Halpern AR, Chen L, Miller CP, Nambi P (2004) Gene-selective modulation by a synthetic oxysterol ligand of the liver X receptor. J Lipid Res 45:1929-1942
25. Kratzer A, Buchebner M, Pfeifer T et al (2009) Synthetic LXR agonist attenuates plaque formation in apoE-/- mice without inducing liver steatosis and hypertriglyceridemia. J Lipid Res 50:312-326
26. Proctor G, Jiang T, Iwahashi M, Wang Z, Li J, Levi M (2006) Regulation of renal fatty acid and cholesterol metabolism, inflammation, and fibrosis in Akita and OVE26 mice with type 1 diabetes. Diabetes 55:2502-2509
27. Martini S, Eichinger F, Nair V, Kretzler M (2008) Defining human diabetic nephropathy on the molecular level: integration of transcriptomic profiles with biological knowledge. Rev Endocr Metab Disord 9:267-274
28. Kiss E, Kranzlin B, Wagenblabeta K et al (2013) Lipid droplet accumulation is associated with an increase in hyperglycemia-induced renal damage: prevention by liver X receptors. Am J Pathol 182:727-741
29. Tachibana H, Ogawa D, Matsushita Y et al (2012) Activation of liver X receptor inhibits osteopontin and ameliorates diabetic nephropathy. J Am Soc Nephrol 23:1835-1846
30. Patel R, Patel M, Tsai R et al (2011) LXRbeta is required for glucocorticoid-induced hyperglycemia and hepatosteatosis in mice. J Clin Invest 121:431-441
31. Breyer MD, Bottinger E, Brosius FC 3rd et al (2005) Mouse models of diabetic nephropathy. J Am Soc Nephrol 16:27-45
32. Brosius FC 3rd, Alpers CE, Bottinger EP et al (2009) Mouse models of diabetic nephropathy. J Am Soc Nephrol 20:2503-2512
33. Ruan XZ, Moorhead JF, Fernando R, Wheeler DC, Powis SH, Varghese Z (2004) Regulation of lipoprotein trafficking in the kidney: role of inflammatory mediators and transcription factors. Biochem Soc Trans 32:88-91
34. Xu ZE, Chen Y, Huang A et al (2011) Inflammatory stress exacerbates lipid-mediated renal injury in ApoE/CD36/SRA triple knockout mice. Am J Physiol Ren Physiol 301:F713-F722
35. Repa JJ, Mangelsdorf DJ (2000) The role of orphan nuclear receptors in the regulation of cholesterol homeostasis. Annu Rev Cell Dev Biol 16:459-481
36. Ruan XZ, Varghese Z, Powis SH, Moorhead JF (2005) Nuclear receptors and their coregulators in kidney. Kidney Int 68:2444-2461
37. Wu J, Zhang Y, Wang N et al (2004) Liver X receptor-alpha mediates cholesterol efflux in glomerular mesangial cells. Am J Physiol Ren Physiol 287:F886-F895
38. Zhang Y, Zhang X, Chen L et al (2006) Liver X receptor agonist TO-901317 upregulates SCD1 expression in renal proximal straight tubule. Am J Physiol Ren Physiol 290:F1065-F1073
39. Kuipers I, van der Harst P, Kuipers F et al (2010) Activation of liver X receptor-alpha reduces activation of the renal and cardiac renin-angiotensin- aldosterone system. Lab Investig J Tech Meth Pathol 90:630-636
40. Leik CE, Carson NL, Hennan JK et al (2007) GW3965, a synthetic liver X receptor (LXR) agonist, reduces angiotensin II-mediated pressor responses in Sprague-Dawley rats. Br J Pharmacol 151:450-456
41. Lee HS, Kim YS (1998) Identification of oxidized low density lipoprotein in human renal biopsies. Kidney Int 54:848-856
42. Lee HS, Lee JS, Koh HI, Ko KW (1991) Intraglomerular lipid deposition in routine biopsies. Clin Nephrol 36:67-75
43. Lee HS, Kruth HS (2003) Accumulation of cholesterol in the lesions of focal segmental glomerulosclerosis. Nephrol (Carlton) 8:224-223
44. Coritsidis G, Rifici V, Gupta S et al (1991) Preferential binding of oxidized LDL to rat glomeruli in vivo and cultured mesangial cells in vitro. Kidney Int 39:858-866
45. Thompson J, Wilson P, Brandewie K et al (2011) Renal accumulation of biglycan and lipid retention accelerates diabetic nephropathy. Am J Pathol 179:1179-1187
46. Morello F, de Boer RA, Steffensen KR et al (2005) Liver X receptors alpha and beta regulate renin expression in vivo. J Clin Invest 115:1913-1922
47. Wang Y, Moser AH, Shigenaga JK, Grunfeld C, Feingold KR (2005) Downregulation of liver X receptor-alpha in mouse kidney and HK-2 proximal tubular cells by LPS and cytokines. J Lipid Res 46:2377-2387
48. Ruan XZ, Varghese Z, Fernando R, Moorhead JF (1998) Cytokine regulation of low-density lipoprotein receptor gene transcription in human mesangial cells. Nephrol Dial Transplant 13:1391-1397
49. Santini E, Lupi R, Baldi S et al (2008) Effects of different LDL particles on inflammatory molecules in human mesangial cells. Diabetologia 51:2117-2125
50. Massy ZA, Kim Y, Guijarro C, Kasiske BL, Keane WF, O'Donnell MP (2000) Low-density lipoprotein-induced expression of interleukin-6, a marker of human mesangial cell inflammation: effects of oxidation and modulation by lovastatin. Biochem Biophys Res Commun 267:536-540