Cellular and molecular mechanisms of diabetic glomerulopathy

Nephrology Dialysis Transplantation

Volumn 27, Issue 7, 2012, Pages 2642-2649

  Gnudi, Luigi ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

blood pressure; diabetes; kidney disease; metabolism; proteinuria

Indexed keywords

ANGIOPOIETIN 1; ANGIOPOIETIN 2; ANGIOTENSIN II; BARDOXOLONE; CD2 ASSOCIATED PROTEIN; ENDOTHELIN 1; ENDOTHELIN A RECEPTOR; FIBRIC ACID DERIVATIVE; GLITAZONE DERIVATIVE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 2; PODOCIN; PROTEIN KINASE C; PROTEIN KINASE C ALPHA; PROTEIN KINASE C BETA; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; SCLEROPROTEIN; TRANSFORMING GROWTH FACTOR BETA1; VASCULOTROPIN A;

ALBUMINURIA; CAUSAL ATTRIBUTION; CELL FUNCTION; CELL INTERACTION; CELL LOSS; CYTOKINE RELEASE; DIABETIC NEPHROPATHY; GLOMERULUS FILTRATION RATE; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; HEMODYNAMICS; HUMAN; INSULIN RESISTANCE; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PODOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS; PROTEIN URINE LEVEL; REVIEW; VASOCONSTRICTION;

DIABETIC NEPHROPATHIES; DISEASE PROGRESSION; HUMANS; KIDNEY GLOMERULUS;

EID: 84864397281     PISSN: 09310509     EISSN: 14602385     Source Type: Journal    
DOI: 10.1093/ndt/gfs121     Document Type: Review

References (100)

1. Shaw JE, Sicree RA, Zimmet PZ. Global estimates of the prevalence of diabetes for 2010 and 2030. Diabetes Res Clin Pract 2010; 87: 4-14.
2. Brownlee M. The pathobiology of diabetic complications: a unifying mechanism. Diabetes 2005; 54: 1615-1625.
3. Gnudi L, Thomas SM, Viberti G. Mechanical forces in diabetic kidney disease: a trigger for impaired glucose metabolism. J Am Soc Nephrol 2007; 18: 2226-2232.
4. Schlondorff D. The glomerular mesangial cell: an expanding role for a specialized pericyte. FASEB J 1987; 1: 272-281.
5. Karalliedde J, Viberti G. Proteinuria in diabetes: bystander or pathway to cardiorenal disease? J Am Soc Nephrol 2010; 21: 2020-2027.
6. Wolf G, Ziyadeh FN. Cellular and molecular mechanisms of proteinuria in diabetic nephropathy. Nephron Physiol 2007; 106: 26-31.
7. Satchell SC, Tooke JE. What is the mechanism of microalbuminuria in diabetes: a role for the glomerular endothelium? Diabetologia 2008; 51: 714-725.
8. Singh A, Friden V, Dasgupta I et al. High glucose causes dysfunction of the human glomerular endothelial glycocalyx. Am J Physiol Renal Physiol 2011; 300: F40-F48.
9. Farquhar MG. Editorial: The primary glomerular filtration barrier-basement membrane or epithelial slits? Kidney Int 1975; 8: 197-211.
10. Osterby R, Gundersen HJ, Horlyck A et al. Diabetic glomerulopathy. Structural characteristics of the early and advanced stages. Diabetes 1983; 32 Suppl 2: 79-82.
11. Gassler N, Elger M, Kranzlin B et al. Podocyte injury underlies the progression of focal segmental glomerulosclerosis in the fa/fa Zucker rat. Kidney Int 2001; 60: 106-116.
12. Hoshi S, Shu Y, Yoshida F et al. Podocyte injury promotes progressive nephropathy in zucker diabetic fatty rats. Lab Invest 2002; 82: 25-35.
13. 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; 57: 167-182.
14. Kriz W, Elger M, Nagata M et al. The role of podocytes in the development of glomerular sclerosis. Kidney Int Suppl 1994; 45: S64-S72.
15. Caramori ML, Kim Y, Moore JH et al. Gene expression differences in skin fibroblasts in identical twins discordant for type 1 diabetes. Diabetes 2012; 61: 739-744.
16. Hostetter TH, Rennke HG, Brenner BM. The case for intrarenal hypertension in the initiation and progression of diabetic and other glomerulopathies. Am J Med 1982; 72: 375-380.
17. Anderson S, Vora JP. Current concepts of renal hemodynamics in diabetes. J Diabetes Complications 1995; 9: 304-307.
18. Sharma K, Cook A, Smith M et al. TGF-beta impairs renal autoregulation via generation of ROS. Am J Physiol Renal Physiol 2005; 288: F1069-F1077.
19. Maddox DA, Brenner BMBrenner BM, Rector FC, Jr. Glomerular ultrafiltration. The Kidney 2000Philadelphia, PAWB Saunders Company319-374.
20. Arima S, Ito S. The mechanisms underlying altered vascular resistance of glomerular afferent and efferent arterioles in diabetic nephropathy. Nephrol Dial Transplant 2003; 18: 1966-1969.
21. Forbes JM, Coughlan MT, Cooper ME. Oxidative stress as a major culprit in kidney disease in diabetes. Diabetes 2008; 57: 1446-1454.
22. Block K, Gorin Y, Abboud HE. Subcellular localization of Nox4 and regulation in diabetes. Proc Natl Acad Sci USA 2009; 106: 14385-14390.
23. Ceriello A, Morocutti A, Mercuri F et al. Defective intracellular antioxidant enzyme production in type 1 diabetic patients with nephropathy. Diabetes 2000; 49: 2170-2177.
24. Pergola PE, Raskin P, Toto RD et al. Bardoxolone methyl and kidney function in CKD with type 2 diabetes. N Engl J Med 2011; 365: 327-336.
25. Giunti S, Tesch GH, Pinach S et al. Monocyte chemoattractant protein-1 has prosclerotic effects both in a mouse model of experimental diabetes and in vitro in human mesangial cells. Diabetologia 2008; 51: 198-207.
26. Okada S, Shikata K, Matsuda M et al. Intercellular adhesion molecule-1-deficient mice are resistant against renal injury after induction of diabetes. Diabetes 2003; 52: 2586-2593.
27. Yang J, Zhang D, Li J et al. Role of PPARgamma in renoprotection in type 2 diabetes: molecular mechanisms and therapeutic potential. Clin Sci (Lond) 2009; 116: 17-26.
28. Staels B, Maes M, Zambon A. Fibrates and future PPARalpha agonists in the treatment of cardiovascular disease. Nat Clin Pract Cardiovasc Med 2008; 5: 542-553.
29. Burt DJ, Gruden G, Thomas SM et al. P38 mitogen-activated protein kinase mediates hexosamine-induced TGFbeta1 mRNA expression in human mesangial cells. Diabetologia 2003; 46: 531-537
30. James LR, Tang D, Ingram A et al. Flux through the hexosamine pathway is a determinant of nuclear factor kappaB-dependent promoter activation. Diabetes 2002; 51: 1146-1156.
31. Busch M, Franke S, Ruster C et al. Advanced glycation end-products and the kidney. Eur J Clin Invest 2010; 40: 742-755.
32. Yip J, Mattock MB, Morocutti A et al. Insulin resistance in insulindependent diabetic patients with microalbuminuria. Lancet 1993; 342: 883-887.
33. Welsh GI, Hale LJ, Eremina Vet al. Insulin signaling to the glomerular podocyte is critical for normal kidney function. Cell Metab 2010; 12: 329-340.
34. Coward RJ, Welsh GI, Yang J et al. The human glomerular podocyte is a novel target for insulin action. Diabetes 2005; 54: 3095-3102.
35. Coward RJ, Welsh GI, Koziell A et al. Nephrin is critical for the action of insulin on human glomerular podocytes. Diabetes 2007; 56: 1127-1135.
36. Welsh GI, Saleem MA. The podocyte cytoskeleton-key to a functioning glomerulus in health and disease. Nat Rev Nephrol 2012; 8: 14-21.
37. Meier M, Menne J, Haller H. Targeting the protein kinase C family in the diabetic kidney: lessons from analysis of mutant mice. Diabetologia 2009; 52: 765-775.
38. Groop PH, Forsblom C, Thomas MC. Mechanisms of disease: Pathway-selective insulin resistance and microvascular complications of diabetes. Nat Clin Pract Endocrinol Metab 2005; 1: 100-110.
39. de Kreutzenberg SV, Ceolotto G, Papparella I et al. Downregulation of the longevity-associated protein SIRT1 in insulin resistance and metabolic syndrome. Potential biochemical mechanisms. Diabetes 2010; 59: 1006-1015.
40. Kume S, Thomas MC, Koya D. Nutrient sensing, autophagy, and diabetic nephropathy. Diabetes 2012; 61: 23-29.
41. Haigis MC, Sinclair DA. Mammalian sirtuins: biological insights and disease relevance. Annu Rev Pathol 2010; 5: 253-295.
42. Orimo M, Minamino T, Miyauchi H et al. Protective role of SIRT1 in diabetic vascular dysfunction. Arterioscler Thromb Vasc Biol 2009; 29: 889-894.
43. Tikoo K, Singh K, Kabra D et al. Change in histone H3 phosphorylation, MAP kinase p.38, SIR 2 and p.53 expression by resveratrol in preventing streptozotocin induced type I diabetic nephropathy. Free Radic Res 2008; 42: 397-404.
44. Tikoo K, Tripathi DN, Kabra DG et al. Intermittent fasting prevents the progression of type I diabetic nephropathy in rats and changes the expression of Sir2 and p.53. FEBS Lett 2007; 581: 1071-1078.
45. Kitada M, Takeda A, Nagai T et al. Dietary restriction ameliorates diabetic nephropathy through anti-inflammatory effects and regulation of the autophagy via restoration of Sirt1 in diabetic Wistar fatty (fa/fa) rats: a model of type 2 diabetes. Exp Diabetes Res 2011; 2011: 908185
46. Inoki K, Mori H, Wang J et al. mTORC1 activation in podocytes is a critical step in the development of diabetic nephropathy in mice. J Clin Invest 2011; 121: 2181-2196.
47. Godel M, Hartleben B, Herbach N et al. Role of mTOR in podocyte function and diabetic nephropathy in humans and mice. J Clin Invest 2011; 121: 2197-2209.
48. Schlondorff D, Banas B. The mesangial cell revisited: no cell is an island. J Am Soc Nephrol 2009; 20: 1179-1187.
49. Simon M, Grone HJ, Johren O et al. Expression of vascular endothelial growth factor and its receptors in human renal ontogenesis and in adult kidney. Am J Physiol 1995; 268: F240-F250.
50. Ku CH, White KE, Dei CA et al. Inducible overexpression of sFlt-1 in podocytes ameliorates glomerulopathy in diabetic mice. Diabetes 2008; 57: 2824-2833.
51. Sison K, Eremina V, Baelde H et al. Glomerular structure and function require paracrine, not autocrine, VEGF-VEGFR-2 signaling. J Am Soc Nephrol 2010; 21: 1691-1701.
52. Cooper ME, Vranes D, Youssef S et al. Increased renal expression of vascular endothelial growth factor (VEGF) and its receptor VEGFR-2 in experimental diabetes. Diabetes 1999; 48: 2229-2239.
53. Veron D, Reidy KJ, Bertuccio C et al. Overexpression of VEGF-A in podocytes of adult mice causes glomerular disease. Kidney Int 2010; 77: 989-999.
54. Eremina V, Baelde HJ, Quaggin SE. Role of the VEGF-a signaling pathway in the glomerulus: evidence for crosstalk between components of the glomerular filtration barrier. Nephron Physiol 2007; 106: 32-37.
55. Lindenmeyer MT, Kretzler M, Boucherot A et al. Interstitial vascular rarefaction and reduced VEGF-A expression in human diabetic nephropathy. J Am Soc Nephrol 2007; 18: 1765-1776.
56. Hanahan D. Signaling vascular morphogenesis and maintenance. Science 1997; 277: 48-50.
57. Woolf AS, Gnudi L, Long DA. Roles of angiopoietins in kidney development and disease. J Am Soc Nephrol 2009; 20: 239-244.
58. Davis B, Dei CA, Long DA et al. Podocyte-specific expression of angiopoietin-2 causes proteinuria and apoptosis of glomerular endothelia. J Am Soc Nephrol 2007; 18: 2320-2329.
59. Jeansson M, Gawlik A, Anderson G et al. Angiopoietin-1 is essential in mouse vasculature during development and in response to injury. J Clin Invest 2011; 121: 2278-2289.
60. Neuhofer W, Pittrow D. Endothelin receptor selectivity in chronic kidney disease: rationale and review of recent evidence. Eur J Clin Invest 2009; 39 Suppl 2: 50-67.
61. Mishra R, Emancipator SN, Kern TS et al. Association between endothelin-1 and collagen deposition in db/db diabetic mouse kidneys. Biochem Biophys Res Commun 2006; 339: 65-70.
62. Watson AM, Li J, Schumacher C et al. The endothelin receptor antagonist avosentan ameliorates nephropathy and atherosclerosis in diabetic apolipoprotein E knockout mice. Diabetologia 2010; 53: 192-203.
63. Mann JF, Green D, Jamerson K et al. Avosentan for overt diabetic nephropathy. J Am Soc Nephrol 2010; 21: 527-535.
64. Yokoi H, Mukoyama M, Mori K et al. Overexpression of connective tissue growth factor in podocytes worsens diabetic nephropathy in mice. Kidney Int 2008; 73: 446-455.
65. Yokoi H, Mukoyama M, Nagae T et al. Reduction in connective tissue growth factor by antisense treatment ameliorates renal tubulointerstitial fibrosis. J Am Soc Nephrol 2004; 15: 1430-1440.
66. Chen S, Kasama Y, Lee JS et al. Podocyte-derived vascular endothelial growth factor mediates the stimulation of alpha3(IV) collagen production by transforming growth factor-beta1 in mouse podocytes. Diabetes 2004; 53: 2939-2949.
67. 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; 97: 8015-8020.
68. RamachandraRao SP, Zhu Y, Ravasi T et al. Pirfenidone is renoprotective in diabetic kidney disease. J Am Soc Nephrol 2009; 20: 1765-1775.
69. Sharma K, Ix JH, Mathew AV et al. Pirfenidone for diabetic nephropathy. J Am Soc Nephrol 2011; 22: 1144-1151.
70. Kato M, Arce L, Natarajan R. MicroRNAs and their role in progressive kidney diseases. Clin J Am Soc Nephrol 2009; 4: 1255-1266.
71. Kato M, Arce L, Wang M et al. A microRNA circuit mediates transforming growth factor-beta1 autoregulation in renal glomerular mesangial cells. Kidney Int 2011; 80: 358-368.
72. Kato M, Zhang J, Wang M et al. MicroRNA-192 in diabetic kidney glomeruli and its function in TGF-beta-induced collagen expression via inhibition of E-box repressors. Proc Natl Acad Sci USA 2007; 104: 3432-3437.
73. Wang B, Koh P, Winbanks C et al. miR-200a prevents renal fibrogenesis through repression of TGF-beta2 expression. Diabetes 2011; 60: 280-287.
74. Nakagawa T. Uncoupling of the VEGF-endothelial nitric oxide axis in diabetic nephropathy: an explanation for the paradoxical effects of VEGF in renal disease. Am J Physiol Renal Physiol 2007; 292: F1665-F1672.
75. Prabhakar S, Starnes J, Shi S et al. Diabetic nephropathy is associated with oxidative stress and decreased renal nitric oxide production. J Am Soc Nephrol 2007; 18: 2945-2952.
76. Nakagawa T, Sato W, Glushakova O et al. Diabetic endothelial nitric oxide synthase knockout mice develop advanced diabetic nephropathy. J Am Soc Nephrol 2007; 18: 539-550.
77. Nakagawa T, Kosugi T, Haneda M et al. Abnormal angiogenesis in diabetic nephropathy. Diabetes 2009; 58: 1471-1478.
78. Rosivall L. Intrarenal renin-angiotensin system. Mol Cell Endocrinol 2009; 302: 185-192.
79. Santos RA, Brosnihan KB, Jacobsen DWet al. Production of angiotensin-(1-7) by human vascular endothelium. Hypertension 1992; 19: II56-II61.
80. Hamming I, Cooper ME, Haagmans BL et al. The emerging role of ACE2 in physiology and disease. J Pathol 2007; 212: 1-11.
81. Liu CX, Hu Q, Wang Y et al. Angiotensin-converting enzyme (ACE) 2 overexpression ameliorates glomerular injury in a rat model of diabetic nephropathy: a comparison with ACE inhibition. Mol Med 2011; 17: 59-69.
82. The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. The Diabetes Control and Complications Trial Research Group. N Engl J Med 1993; 329: 977-986.
83. Writing Team for the Diabetes Control and Complications Trial/Epidemiology of Diabetes Interventions and Complications Research Group. Sustained effect of intensive treatment of type 1 diabetes mellitus on development and progression of diabetic nephropathy: the Epidemiology of Diabetes Interventions and Complications (EDIC) study. JAMA 2003; 290: 2159-2167.
84. de Boer IH, Rue TC, Cleary PA et al. 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 2011; 171: 412-420.
85. Abe M, Maruyama N, Okada K et al. Effects of lipid-lowering therapy with rosuvastatin on kidney function and oxidative stress in patients with diabetic nephropathy. J Atheroscler Thromb 2011; 18: 1018-1028.
86. Intensive blood-glucose control with sulphonylureas or insulin compared with conventional treatment and risk of complications in patients with type 2 diabetes (UKPDS 33). UK Prospective Diabetes Study (UKPDS) Group. Lancet 1998; 352: 837-853.
87. Holman RR, Paul SK, Bethel MA et al. 10-year follow-up of intensive glucose control in type 2 diabetes. N Engl J Med 2008; 359: 1577-1589.
88. Gerstein HC, Miller ME, Byington RP et al. Effects of intensive glucose lowering in type 2 diabetes. N Engl J Med 2008; 358: 2545-2559.
89. Patel A, MacMahon S, Chalmers J et al. Intensive blood glucose control and vascular outcomes in patients with type 2 diabetes. N Engl J Med 2008; 358: 2560-2572.
90. Duckworth W, Abraira C, Moritz T et al. Glucose control and vascular complications in veterans with type 2 diabetes. N Engl J Med 2009; 360: 129-139.
91. Agrawal L, Azad N, Emanuele NV et al. Observation on renal outcomes in the Veterans Affairs Diabetes Trial. Diabetes Care 2011; 34: 2090-2094.
92. Dluhy RG, McMahon GT. Intensive glycemic control in the ACCORD and ADVANCE trials. N Engl J Med 2008; 358: 2630-2633.
93. Poulter NR. Blood pressure and glucose control in subjects with diabetes: new analyses from ADVANCE. J Hypertens Suppl 2009; 27 Suppl 1: S3-S8.
94. Lewis JB, Berl T, Bain RP et al. Effect of intensive blood pressure control on the course of type 1 diabetic nephropathy. Collaborative Study Group. Am J Kidney Dis 1999; 34: 809-817.
95. Pohl MA, Blumenthal S, Cordonnier DJ et al. Independent and additive impact of blood pressure control and angiotensin II receptor blockade on renal outcomes in the irbesartan diabetic nephropathy trial: clinical implications and limitations. J Am Soc Nephrol 2005; 16: 3027-3037.
96. Holman RR, Paul SK, Bethel MA et al. Long-term follow-up after tight control of blood pressure in type 2 diabetes. N Engl J Med 2008; 359: 1565-1576.
97. Gnudi L, Goldsmith D. Renin angiotensin aldosterone system (RAAS) inhibitors in the prevention of early renal disease in diabetes. F1000 Med Rep 2010; 2: 18
98. Mauer M, Zinman B, Gardiner R et al. Renal and retinal effects of enalapril and losartan in type 1 diabetes. N Engl J Med 2009; 361: 40-51.
99. Bilous R, Chaturvedi N, Sjolie AK et al. Effect of candesartan on microalbuminuria and albumin excretion rate in diabetes: three randomized trials. Ann Intern Med 2009; 151: 11-14.
100. Ruggenenti P, Fassi A, Ilieva AP et al. Preventing microalbuminuria in type 2 diabetes. N Engl J Med 2004; 351: 1941-1951.