Simvastatin reverses podocyte injury but not mesangial expansion in early stage type 2 diabetes mellitus

Renal Failure

Volumn 31, Issue 6, 2009, Pages 503-513

  Wei, P ^a   Grimm, P R ^a   Settles, D C ^a   Balwanz, C R ^a   Padanilam, B J ^a   Sansom, S C ^a  

^a NEBRASKA MEDICAL CENTER   (United States)

Author keywords

Albuminuria; Diabetic nephropathy; Mice; Simvastatin; Statins

Indexed keywords

ALBUMIN; GLUCOSE; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; INSULIN; LOW DENSITY LIPOPROTEIN CHOLESTEROL; NEPHRIN; SIMVASTATIN; TRIACYLGLYCEROL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; DIABETIC NEPHROPATHY; GLOMERULUS; GLUCOSE BLOOD LEVEL; IMMUNOHISTOCHEMISTRY; INSULIN BLOOD LEVEL; KIDNEY INJURY; MALE; MESANGIUM; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OSMOTIC MINIPUMP; PODOCYTE; PRIORITY JOURNAL; RENAL PROTECTION; TRIACYLGLYCEROL BLOOD LEVEL; URINARY EXCRETION; WEIGHT GAIN;

ANALYSIS OF VARIANCE; ANIMALS; BLOOD GLUCOSE; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 2; DISEASE MODELS, ANIMAL; GLOMERULAR MESANGIUM; IMMUNOHISTOCHEMISTRY; KIDNEY FUNCTION TESTS; MALE; MICE; MICE, INBRED C57BL; MICROSCOPY, ELECTRON; ORGAN SIZE; PODOCYTES; PROBABILITY; RANDOM ALLOCATION; RISK FACTORS; SEVERITY OF ILLNESS INDEX; SIMVASTATIN;

EID: 72649085468     PISSN: 0886022X     EISSN: 15256049     Source Type: Journal    
DOI: 10.1080/08860220902963848     Document Type: Article

References (61)

1. Wei P, Lane PH, Lane JT, Padanilam BJ, Sansom SC. Glomerular structural and functional changes in a high-fat diet mouse model of early-stage Type 2 diabetes. Diabetologia. 2004 Aug 27;47:1541-1549.
2. Erdely A, Freshour G, Maddox DA, Olson JL, Samsell L, Baylis C. Renal disease in rats with Type 2 diabetes is associated with decreased renal nitric oxide production. Diabetologia. 2004 October;47(10):1672-1676.
3. Coimbra TM, Janssen U, Grone HJ, et al. Early events leading to renal injury in obese Zucker (fatty) rats with type II diabetes. Kidney Int. 2000 January;57(1):167-182.
4. Whaley-Connell A, Demarco VG, Lastra G, et al. Insulin resistance, oxidative stress, and podocyte injury: Role of rosuvastatin modulation of filtration barrier injury. Am J Nephrol. 2007 October 3;28(1):67-75.
5. Fujii M, Inoguchi T, Maeda Y, et al. Pitavastatin ameliorates albuminuria and renal mesangial expansion by downregulating NOX4 in db/db mice. Kidney Int. 2007 August;72(4): 473-480.
6. Shibata S, Nagase M, Fujita T.Fluvastatin ameliorates podocyte injury in proteinuric rats viamodulation of excessive Rho signaling. J Am Soc Nephrol. 2006 March;17(3): 754-764.
7. Epstein M, Campese VM. Pleiotropic effects of 3-hydroxy- 3-methylglutaryl coenzyme a reductase inhibitors on renal function. Am J Kidney Dis. 2005 January;45(1):2-14.
8. Senokuchi T, Matsumura T, Sakai M, et al. Statins suppress oxidized low density lipoprotein-induced macrophage proliferation by inactivation of the small G protein-p38 MAPK pathway. J Biol Chem. 2005 February 25;280(8):6627-6633.
9. Young BA, Johnson RJ, Alpers CE, et al. Cellular events in the evolution of experimental diabetic nephropathy. Kidney Int. 1995 March;47(3):935-944.
10. Wolf G, Sharma K, Chen Y, Ericksen M, Ziyadeh FN. Highglucose- induced proliferation in mesangial cells is reversed by autocrine TGF-beta. Kidney Int. 1992 September;42(3): 647-656.
11. Shankland SJ. The podocyte's response to injury: Role in proteinuria and glomerulosclerosis. Kidney Int. 2006 June;69(12): 2131-2147.
12. Lane JT. Microalbuminuria as a marker of cardiovascular and renal risk in type 2 diabetes mellitus: A temporal perspective. Am J Physiol Renal Physiol. 2004 March;286(3): F442-F450.
13. Tojo A, Onozato ML, Kurihara H, Sakai T, Goto A, Fujita T. Angiotensin II blockade restores albumin reabsorption in the proximal tubules of diabetic rats. Hypertens Res. 2003 May;26(5):413-419.
14. Menini S, Iacobini C, Oddi G, et al. Increased glomerular cell (podocyte) apoptosis in rats with streptozotocin-induced diabetes mellitus: Role in the development of diabetic glomerular disease. Diabetologia. 2007;50(12):2591-2599.
15. Pluznick JL, Wei P, Grimm PR, Sansom SC. BK-{beta}1 subunit: Immunolocalization in the mammalian connecting tubule and its role in the kaliuretic response to volume expansion. Am J Physiol Renal Physiol. 2005 April;288(4): F846-F854.
16. Lorenz JN, Gruenstein E. A simple, nonradioactive method for evaluating single-nephron filtration rate using FITCinulin. Am J Physiol. 1999 January;276(1 Pt 2):F172-F177.
17. Basgen JM, Rich SS, Mauer SM, Steffes MW. Measuring the volume density of the glomerular mesangium. Nephron. 1988;50(3):182-186.
18. Nyengaard JR. Stereologic methods and their application in kidney research. J Am Soc Nephrol. 1999 May;10(5): 1100-1123.
19. Brito PL, Fioretto P, Drummond K, et al. Proximal tubular basement membrane width in insulin-dependent diabetes mellitus. Kidney Int. 1998 March;53(3):754-761.
20. Maugeais C, Tietge UJ, Broedl UC, et al. Dose-dependent acceleration of high-density lipoprotein catabolism by endothelial lipase. Circulation. 2003 October 28;108(17): 2121-2126.
21. Park SY, Cho YR, Kim HJ, et al. Unraveling the temporal pattern of diet-induced insulin resistance in individual organs and cardiac dysfunction in C57BL/6 mice. Diabetes 2005 December;54(12):3530-3540.
22. Kobayashi M, Ohno T, Tsuchiya T, Horio F. Characterization of diabetes-related traits in MSM and JF1 mice on highfat diet. J Nutr Biochem. 2004 October;15(10):614-621.
23. Rossmeisl M, Rim JS, Koza RA, Kozak LP. Variation in type 2 diabetes-related traits in mouse strains susceptible to dietinduced obesity. Diabetes. 2003 August;52(8):1958-1966.
24. Tonolo G, Ciccarese M, Brizzi P, et al. Reduction of albumin excretion rate in normotensive microalbuminuric type 2 diabetic patients during long-term simvastatin treatment. Diabetes Care. 1997 December;20(12):1891-1895.
25. Wilson SH, Chade AR, Feldstein A, et al. Lipid-loweringindependent effects of simvastatin on the kidney in experimental hypercholesterolaemia. Nephrol Dial Transplant. 2003 April;18(4):703-709.
26. Attia DM, Ni ZN, Boer P, et al. Proteinuria is preceded by decreased nitric oxide synthesis and prevented by a NO donor in cholesterol-fed rats. Kidney Int. 2002 June;61(5):1776-1787.
27. Bianchi S, Bigazzi R, Caiazza A, Campese VM. A controlled, prospective study of the effects of atorvastatin on proteinuria and progression of kidney disease. Am J Kidney Dis. 2003 March;41(3):565-570.
28. Banes-Berceli AK, Shaw S, Ma G, et al. Effect of simvastatin on high glucose- and angiotensin II-induced activation of the JAK/STAT pathway in mesangial cells. Am J Physiol Renal Physiol. 2006 July;291(1):F116-F121.
29. Usui H, Shikata K, Matsuda M, et al. HMG-CoA reductase inhibitor ameliorates diabetic nephropathy by its pleiotropic effects in rats. Nephrol Dial Transplant. 2003 February; 18(2):265-272.
30. Park YS, Guijarro C, Kim Y, et al. Lovastatin reduces glomerular macrophage influx and expression of monocyte chemoattractant protein-1 mRNA in nephrotic rats. Am J Kidney Dis. 1998 January;31(1):190-194.
31. Yasuda G, Kuji T, Hasegawa K, et al. Safety and efficacy of fluvastatin in hyperlipidemic patients with chronic renal disease. Ren Fail. 2004 July;26(4):411-418.
32. Wanner C, Krane V, Marz W, et al. Atorvastatin in patients with type 2 diabetes mellitus undergoing hemodialysis. N Engl J Med. 2005 July 21;353(3):238-248. (Pubitemid 41058323)
33. Ziyadeh FN. The extracellular matrix in diabetic nephropathy. Am J Kidney Dis. 1993 November;22(5):736-744.
34. Abrass CK. Diabetic nephropathy. Mechanisms of mesangial matrix expansion. West J Med. 1995 April;162(4):318-321.
35. Whiteside CI, Dlugosz JA. Mesangial cell protein kinase C isozyme activation in the diabetic milieu. Am J Physiol Renal Physiol. 2002 June;282(6):F975-F980.
36. Ayo SH, Radnik R, Garoni JA, Troyer DA, Kreisberg JI. High glucose increases diacylglycerol mass and activates protein kinase C in mesangial cell cultures. Am J Physiol. 1991;261:F571-F577.
37. Conti FG, Striker LJ, Lesniak MA, Mackay K, Roth J, Striker GE. Studies on binding and mitogenic effect of insulin and insulin-like growth factor I in glomerular mesangial cells. Endocrinology. 1988 June;122(6):2788-2795.
38. Oemar BS, Foellmer HG, Hodgdon-Anandant L, Rosenzweig SA. Regulation of insulin-like growth factor I receptors in diabetic mesangial cells. J Biol Chem. 1991 February 5;266(4):2369-2373.
39. Nagasawa K, Muraki Y, Matsuda T, Ohnishi N, Yokoyama T. Inhibitory effect of statins on fetal bovine serum-induced proliferation of rat cultured mesangial cells and correlation between their inhibitory effect and transport characteristics. J Pharm Sci. 2000 December;89(12):1594-1604.
40. Terada Y, Inoshita S, Nakashima O, et al. Lovastatin inhibits mesangial cell proliferation via p27Kip1. J Am Soc Nephrol. 1998 December;9(12):2235-2243.
41. Ghosh PM, Mott GE, Ghosh-Choudhury N, et al. Lovastatininduces apoptosis by inhibiting mitotic and post-mitotic events in cultured mesangial cells. Biochim Biophys Acta. 1997 October 30;1359(1):13-24.
42. Chen LM, Li XW, Huang LW, Li Y, Duan L, Zhang XJ. [The early pathological changes of KKAy mice with type 2 diabetes]. Zhongguo Yi Xue Ke Xue Yuan Xue Bao. 2002 February;24(1):71-75.
43. Yoshimura A, Nemoto T, Sugenoya Y, et al. Effect of simvastatin on proliferative nephritis and cell-cycle protein expression. Kidney Int Suppl. 1999 July;71:S84-S87.
44. Ronco P. Proteinuria: Is it all in the foot? J Clin Invest. 2007 August;117(8):2079-2082.
45. Chandie Shaw PK, Berger SP, Mallat M, Frolich M, Dekker FW, Rabelink TJ. Central obesity is an independent risk factor for albuminuria in nondiabetic South Asian subjects. Diabetes Care. 2007 July;30(7):1840-1844.
46. Khoshnoodi J, Sigmundsson K, Ofverstedt LG, et al. Nephrin promotes cell-cell adhesion through homophilic interactions. Am J Pathol. 2003 December;163(6):2337-2346.
47. Koop K, Eikmans M, Baelde HJ, et al. Expression of podocyte-associated molecules in acquired human kidney diseases. J Am Soc Nephrol. 2003 August;14(8):2063-2071.
48. Kawachi H, Koike H, Kurihara H, Sakai T, Shimizu F. Cloning of rat homologue of podocin: Expression in proteinuric states and in developing glomeruli. J Am Soc Nephrol. 2003 January;14(1):46-56.
49. Simons M, Schwarz K, Kriz W, et al. Involvement of lipid rafts in nephrin phosphorylation and organization of the glomerular slit diaphragm. Am J Pathol. 2001 September; 159(3):1069-1077.
50. Cantley LC. The phosphoinositide 3-kinase pathway. Science. 2002 May 31;296(5573):1655-1657.
51. Doublier S, Ruotsalainen V, Salvidio G, et al. Nephrin redistribution on podocytes is a potential mechanism for proteinuria in patients with primary acquired nephrotic syndrome. Am J Pathol. 2001 May;158(5):1723-1731.
52. Sung SH, Wang A, Pyagay PE, Kanwar YS, Ziyadeh FN, Chen S. Blockade of vascular endothelial growth factor signaling ameliorates diabetic albuminuria in mice. J Am Soc Nephrol. 2006;17(11):3093-3104.
53. Zeng L, Xu H, Chew TL, et al. HMG CoA reductase inhibition modulates VEGF-induced endothelial cell hyperpermeability by preventing RhoA activation and myosin regulatory light chain phosphorylation. FASEB J. 2005 November; 19(13):1845-1847.
54. Gnudi L, Thomas SM, Viberti G. Mechanical forces in diabetic kidney disease: A trigger for impaired glucose metabolism. J Am Soc Nephrol. 2007 August;18(8):2226-2232.
55. Park IS, Kiyomoto H, Abboud SL, Abboud HE. Expression of transforming growth factor-βand type IV collagen in early streptozotocin-induced diabetes. Diabetes. 1997;46(3): 473-480.
56. Ziyadeh FN, Hoffman BB, Han DC, et al. Long-term prevention of renal insufficiency, excess matrix gene expression, and glomerular mesangial matrix expansion by treatment with monoclonal antitransforming growth factor-beta antibody in db/db diabetic mice. Proc Natl Acad Sci USA. 2000 July 5;97(14):8015-8020.
57. Flyvbjerg A, Dagnaes-Hansen F, De Vriese AS, Schrijvers BF, Tilton RG, Rasch R. Amelioration of long-term renal changes in obese type 2 diabetic mice by a neutralizing vascular endothelial growth factor antibody. Diabetes. 2002 October; 51(10):3090-3094.
58. Xia L, Wang H, Munk S, et al. Reactive oxygen species, PKC-{beta}1, and PKC-{zeta} mediate high glucoseinduced vascular endothelial growth factor expression in mesangial cells. Am J Physiol Endocrinol Metab. 2007;293(5):1280-1288.
59. Cha DR, Kang YS, Han SY, et al. Vascular endothelial growth factor is increased during early stage of diabetic nephropathy in type II diabetic rats. J Endocrinol. 2004 October;183(1):183-194.
60. Lee EY, Chung CH, Kim JH, Joung HJ, Hong SY. Antioxidants ameliorate the expression of vascular endothelial growth factor mediated by protein kinase C in diabetic podocytes. Nephrol Dial Transplant. 2006 June;21(6): 1496-1503.
61. Gorin Y, Block K, Hernandez J, et al. Nox4 NAD(P)H oxidase mediates hypertrophy and fibronectin expression in the diabetic kidney. J Biol Chem. 2005 November 25;280(47): 39616-39626.