Podocytes, signaling pathways, and vascular factors in diabetic kidney disease

Advances in Chronic Kidney Disease

Volumn 21, Issue 3, 2014, Pages 304-310

  Brosius, Frank C ^a,b   Coward, Richard J ^a,b  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Diabetes; Glomerulus; Glucose; Insulin; Mammalian target of rapamycin

Indexed keywords

ACTIVATED PROTEIN C; ADIPOCYTOKINE; ANGIOPOIETIN; BINDING PROTEIN; ESTROGEN; GROWTH FACTOR; INSULIN; MAMMALIAN TARGET OF RAPAMYCIN; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; SOMATOMEDIN; SOMATOMEDIN C RECEPTOR; VASCULOTROPIN A; VITAMIN D; GLUCOSE BLOOD LEVEL; MTOR PROTEIN, HUMAN; TARGET OF RAPAMYCIN KINASE; VEGFA PROTEIN, HUMAN;

ALBUMINURIA; APOPTOSIS; ARTICLE; CELL DAMAGE; CELL DEATH; CELL LOSS; CELL PROTECTION; CELL SURVIVAL; CELL VIABILITY; CYTOPATHOLOGY; DIABETES MELLITUS; DIABETIC NEUROPATHY; ENDOTHELIUM CELL; GLOMERULOSCLEROSIS; GLOMERULUS BASEMENT MEMBRANE; HORMONE RESPONSE; HUMAN; INSULIN SENSITIVITY; KIDNEY HYPERTROPHY; NONHUMAN; PARACRINE SIGNALING; PODOCYTE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; DIABETIC NEPHROPATHY; GLUCOSE BLOOD LEVEL; METABOLISM; PATHOLOGY; PHYSIOLOGY;

BLOOD GLUCOSE; DIABETIC NEPHROPATHIES; HUMANS; INSULIN; PODOCYTES; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84899585241     PISSN: 15485595     EISSN: 15485609     Source Type: Journal    
DOI: 10.1053/j.ackd.2014.03.011     Document Type: Review

References (79)

1. Pagtalunan M.E., Miller P.L., Jumping-Eagle S., et al. Podocyte loss and progressive glomerular injury in type II diabetes. J Clin Invest 1997, 99(2):342-348.
2. Steffes M.W., Schmidt D., McCrery R., Basgen J.M. Glomerular cell number in normal subjects and in type 1 diabetic patients. Kidney Int 2001, 59(6):2104-2113.
3. Toyoda M., Najafian B., Kim Y., Caramori M.L., Mauer M. Podocyte detachment and reduced glomerular capillary endothelial fenestration in human type 1 diabetic nephropathy. Diabetes 2007, 56(8):2155-2160.
4. Meyer T.W., Bennett P.H., Nelson R.G. Podocyte number predicts long-term urinary albumin excretion in Pima Indians with Type II diabetes and microalbuminuria. Diabetologia 1999, 42(11):1341-1344.
5. Wharram B.L., Goyal M., Wiggins J.E., et al. Podocyte depletion causes glomerulosclerosis: diphtheria toxin-induced podocyte depletion in rats expressing human diphtheria toxin receptor transgene. J Am Soc Nephrol 2005, 16(10):2941-2952.
6. Weil E.J., Lemley K.V., Mason C.C., et al. Podocyte detachment and reduced glomerular capillary endothelial fenestration promote kidney disease in type 2 diabetic nephropathy. Kidney Int 2012, 82(9):1010-1017.
7. Petermann A.T., Pippin J., Krofft R., et al. Viable podocytes detach in experimental diabetic nephropathy: potential mechanism underlying glomerulosclerosis. Nephron Exp Nephrol 2004, 98(4):e114-e123.
8. Dessapt C., Baradez M.O., Hayward A., et al. Mechanical forces and TGF{beta}1 reduce podocyte adhesion through {alpha}3{beta}1 integrin downregulation. Nephrol Dial Transplant 2009, 24(9):2645-2655.
9. Susztak K., Raff A.C., Schiffer M., Bottinger E.P. Glucose-induced reactive oxygen species cause apoptosis of podocytes and podocyte depletion at the onset of diabetic nephropathy. Diabetes 2006, 55(1):225-233.
10. 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.
11. Eremina V., Baelde H.J., Quaggin S.E. Role of the VEGF-A signaling pathway in the glomerulus: evidence for crosstalk between components of the glomerular filtration barrier. Nephron Physiol 2007, 106(2):p32-p37.
12. Yuen D.A., Stead B.E., Zhang Y., et al. eNOS deficiency predisposes podocytes to injury in diabetes. J Am Soc Nephrol 2012, 23(11):1810-1823.
13. Coward R.J., Welsh G.I., Yang J., et al. The human glomerular podocyte is a novel target for insulin action. Diabetes 2005, 54(11):3095-3102.
14. Kim E.Y., Dryer S.E. Effects of insulin and high glucose on mobilization of Slo1 BKCa channels in podocytes. J Cell Physiol 2011, 226(9):2307-2315.
15. Kim E.Y., Anderson M., Dryer S.E. Insulin increases surface expression of TRPC6 channels in podocytes: role of NADPH oxidases and reactive oxygen species. Am J Physiol Renal Physiol 2012, 302(3):F298-F2307.
16. Welsh G.I., Hale L.J., Eremina V., et al. Insulin signaling to the glomerular podocyte is critical for normal kidney function. Cell Metab 2010, 12(4):329-340.
17. Tejada T., Catanuto P., Ijaz A., et al. Failure to phosphorylate AKT in podocytes from mice with early diabetic nephropathy promotes cell death. Kidney Int 2008, 73(12):1385-1393.
18. Mima A., Ohshiro Y., Kitada M., et al. Glomerular-specific protein kinase C-beta-induced insulin receptor substrate-1 dysfunction and insulin resistance in rat models of diabetes and obesity. Kidney Int 2011, 79(8):883-896.
19. Tiwari S., Singh R.S., Li L., et al. Deletion of the insulin receptor in theproximal tubule promotes hyperglycemia. J Am Soc Nephrol 2013, 24(8):1209-1214.
20. Mykkanen L., Zaccaro D.J., Wagenknecht L.E., Robbins D.C., Gabriel M., Haffner S.M. Microalbuminuria is associated with insulin resistance in nondiabetic subjects: the insulin resistance atherosclerosis study. Diabetes 1998, 47(5):793-800.
21. Orchard T.J., Chang Y.F., Ferrell R.E., Petro N., Ellis D.E. 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 2002, 62(3):963-970.
22. Yip J., Mattock M.B., Morocutti A., Sethi M., Trevisan R., Viberti G. Insulin resistance in insulin-dependent diabetic patients with microalbuminuria. Lancet 1993, 342(8876):883-887.
23. Ekstrand A.V., Groop P.H., Gronhagen-Riska C. Insulin resistance precedes microalbuminuria in patients with insulin-dependent diabetes mellitus. Nephrol Dial Transplant 1998, 13(12):3079-3083.
24. Parvanova A.I., Trevisan R., Iliev I.P., et al. Insulin resistance and microalbuminuria: a cross-sectional, case-control study of 158 patients with type 2 diabetes and different degrees of urinary albumin excretion. Diabetes 2006, 55(5):1456-1462.
25. Drapeau N., Lizotte F., Denhez B., Guay A., Kennedy C.R., Geraldes P. Expression of SHP-1 induced by hyperglycemia prevents insulin actions in podocytes. Am J Physiol Endocrinol Metab 2013, 304(11):E1188-E1198.
26. Mora C., Navarro J.F. Inflammation and diabetic nephropathy. Curr Diabetes Rep 2006, 6(6):463-468.
27. Du P., Fan B., Han H., et al. NOD2 promotes renal injury by exacerbating inflammation and podocyte insulin resistance in diabetic nephropathy. Kidney Int 2013, 84(2):265-276.
28. Lennon R., Pons D., Sabin M.A., et al. Saturated fatty acids induce insulin resistance in human podocytes: implications for diabetic nephropathy. Nephrol Dial Transplant 2009, 24(11):3288-3296.
29. Hale L.J., Welsh G.I., Perks C.M., et al. Insulin-like growth factor-II is produced by, signals to and is an important survival factor for the mature podocyte in man and mouse. J Pathol 2013, 230(1):95-106.
30. Amin R., Schultz C., Ong K., et al. Low IGF-I and elevated testosterone during puberty in subjects with type 1 diabetes developing microalbuminuria in comparison to normoalbuminuric control subjects: the Oxford Regional Prospective Study. Diabetes Care 2003, 26(5):1456-1461.
31. Teppala S., Shankar A. Association between serum IGF-1 and diabetes among U.S. adults. Diabetes Care 2010, 33(10):2257-2259.
32. Segev Y., Landau D., Marbach M., Shehadeh N., Flyvbjerg A., Phillip M. Renal hypertrophy in hyperglycemic non-obese diabetic mice is associated with persistent renal accumulation of insulin-like growth factor I. J Am Soc Nephrol 1997, 8(3):436-444.
33. Rajpathak S.N., Gunter M.J., Wylie-Rosett J., et al. The role of insulin-like growth factor-I and its binding proteins in glucose homeostasis and type 2 diabetes. Diabetes Metab Res Rev 2009, 25(1):3-12.
34. Vasylyeva T.L., Ferry R.J. Novel roles of the IGF-IGFBP axis in etiopathophysiology of diabetic nephropathy. Diabetes Res Clin Pract 2007, 76(2):177-186.
35. Kadowaki T., Yamauchi T., Kubota N., Hara K., Ueki K., Tobe K. Adiponectin and adiponectin receptors in insulin resistance, diabetes, and the metabolic syndrome. J Clin Invest 2006, 116(7):1784-1792.
36. Meyvis K., Verrijken A., Wouters K., Van Gaal L. Plasma adiponectin level is inversely correlated with albuminuria in overweight and obese nondiabetic individuals. Metabolism 2013, 62(11):1570-1576.
37. Sharma K., Ramachandrarao S., Qiu G., et al. Adiponectin regulates albuminuria and podocyte function in mice. J Clin Invest 2008, 118(5):1645-1656.
38. Sarbassov D.D., Ali S.M., Kim D.H., et al. Rictor, a novel binding partner of mTOR, defines a rapamycin-insensitive and raptor-independent pathway that regulates the cytoskeleton. Curr Biol 2004, 14(14):1296-1302.
39. 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(6):2181-2196.
40. Cina D.P., Onay T., Paltoo A., et al. Inhibition of mTOR disrupts autophagic flux in podocytes. J Am Soc Nephrol 2012, 23(3):412-420.
41. 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(6):2197-2209.
42. Zhang H., Schin M., Saha J., et al. Podocyte-specific overexpression of GLUT1 surprisingly reduces mesangial matrix expansion indiabetic nephropathy in mice. Am J Physiol Renal Physiol 2010, 299(1):F91-F98.
43. Guzman J., Jauregui A.N., Merscher-Gomez S., et al. Podocyte-specificGLUT4 deficient mice have fewer and larger podocytes and are protected from diabetic nephropathy. Diabetes 2014, 63(2):701-714.
44. Wang Y., Heilig K., Saunders T., et al. Transgenic overexpression of GLUT1 in mouse glomeruli produces renal disease resembling diabetic glomerulosclerosis. Am J Physiol Renal Physiol 2010, 299(1):F99-F111.
45. Canaud G., Bienaime F., Viau A., et al. AKT2 is essential to maintain podocyte viability and function during chronic kidney disease. Nat Med 2013, 19(10):1288-1296.
46. Wang Y., Zhou J., Minto A.W., et al. Altered vitamin D metabolism in type II diabetic mouse glomeruli may provide protection from diabetic nephropathy. Kidney Int 2006, 70(5):882-891.
47. Kuhlmann A., Haas C.S., Gross M.L., et al. 1,25-Dihydroxyvitamin D3 decreases podocyte loss and podocyte hypertrophy in the subtotally nephrectomized rat. Am J Physiol Renal Physiol 2004, 286(3):F526-F533.
48. Deb D.K., Sun T., Wong K.E., et al. Combined vitamin D analog and AT1 receptor antagonist synergistically block the development of kidney disease in a model of type 2 diabetes. Kidney Int 2010, 77(11):1000-1009.
49. Zhang Y., Deb D.K., Kong J., et al. Long-term therapeutic effect of vitamin D analog doxercalciferol on diabetic nephropathy: strong synergism with AT1 receptor antagonist. Am J Physiol 2009, 297(3):F791-F801.
50. de Zeeuw D., Agarwal R., Amdahl M., et al. Selective vitamin D receptor activation with paricalcitol for reduction of albuminuria in patients with type 2 diabetes (VITAL study): a randomised controlled trial. Lancet 2010, 376(9752):1543-1551.
51. Wang Y., Deb D.K., Zhang Z., et al. Vitamin D receptor signaling in podocytes protects against diabetic nephropathy. J Am Soc Nephrol 2012, 23(12):1977-1986.
52. Li Y.C. Podocytes as target of vitamin D. Curr Diabetes Rev 2011, 7(1):35-40.
53. Neugarten J., Acharya A., Silbiger S.R. Effect of gender on the progression of nondiabetic renal disease: a meta-analysis. J Am Soc Nephrol 2000, 11(2):319-329.
54. Doublier S., Lupia E., Catanuto P., Elliot S.J. Estrogens and progression of diabetic kidney damage. Curr Diabetes Rev 2011, 7(1):28-34.
55. Kummer S., Jeruschke S., Wegerich L.V., et al. Estrogen receptor alpha expression in podocytes mediates protection against apoptosis in-vitro and in-vivo. PLoS One 2011, 6(11):e27457.
56. Sandholm N., McKnight A.J., Salem R.M., et al. Chromosome 2q31.1 associates with ESRD in women with type 1 diabetes. J Am Soc Nephrol 2013, 24(10):1537-1543.
57. Catanuto P., Doublier S., Lupia E., et al. 17-Beta-estradiol and tamoxifen upregulate estrogen receptor beta expression and control podocyte signaling pathways in a model of type 2 diabetes. Kidney Int 2009, 75(11):1194-1201.
58. Catanuto P., Fornoni A., Pereira-Simon S., et al. Invivo 17beta-estradiol treatment contributes to podocyte actin stabilization in female db/db mice. Endocrinology 2012, 153(12):5888-5895.
59. Lu M., Amano S., Miyamoto K., et al. Insulin-induced vascular endothelial growth factor expression in retina. Invest Ophthalmol Vis Sci 1999, 40(13):3281-3286.
60. Ferrara N., Gerber H.P., LeCouter J. The biology of VEGF and its receptors. Nat Med 2003, 9(6):669-676.
61. Foster R.R., Hole R., Anderson K., et al. Functional evidence that vascular endothelial growth factor may act as an autocrine factor on human podocytes. Am J Physiol Renal Physiol 2003, 284(6):F1263-F1273.
62. Eremina V., Sood M., Haigh J., et al. Glomerular-specific alterations of VEGF-A expression lead to distinct congenital and acquired renal diseases. J Clin Invest 2003, 111(5):707-716.
63. Eremina V., Jefferson J.A., Kowalewska J., et al. VEGF inhibition and renal thrombotic microangiopathy. N Engl J Med 2008, 358(11):1129-1136.
64. Sivaskandarajah G.A., Jeansson M., Maezawa Y., Eremina V., Baelde H.J., Quaggin S.E. VEGFA protects the glomerular microvasculature in diabetes. Diabetes 2012, 61(11):2958-2966.
65. Cooper M.E., 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(11):2229-2239.
66. Hohenstein B., Hausknecht B., Boehmer K., Riess R., Brekken R.A., Hugo C.P. Local VEGF activity but not VEGF expression is tightly regulated during diabetic nephropathy in man. Kidney Int 2006, 69(9):1654-1661.
67. Baelde H.J., Eikmans M., Lappin D.W., et al. Reduction of VEGF-A and CTGF expression in diabetic nephropathy is associated with podocyte loss. Kidney Int 2007, 71(7):637-645.
68. Flyvbjerg A., Dagnaes-Hansen F., De Vriese A.S., Schrijvers B.F., Tilton R.G., Rasch R. Amelioration of long-term renal changes in obese type 2 diabetic mice by a neutralizing vascular endothelial growth factor antibody. Diabetes 2002, 51(10):3090-3094.
69. Hale L.J., Hurcombe J., Lay A., et al. Insulin directly stimulates VEGF-A production in the glomerular podocyte. Am J Physiol Renal Physiol 2013, 305(2):F182-F188.
70. Woolard J., Wang W.Y., Bevan H.S., et al. VEGF165b, an inhibitory vascular endothelial growth factor splice variant: mechanism of action, invivo effect on angiogenesis and endogenous protein expression. Cancer Res 2004, 64(21):7822-7835.
71. Harris S., Craze M., Newton J., et al. Do anti-angiogenic VEGF (VEGFxxxb) isoforms exist? A cautionary tale. PLoS One 2012, 7(5):e35231.
72. Bates D.O., Mavrou A., Qiu Y., et al. Detection of VEGF-A(xxx)b isoforms in human tissues. PLoS One 2013, 8(7):e68399.
73. 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(6):2278-2289.
74. Dessapt-Baradez C., Woolf A.S., White K.E., et al. Targeted glomerular angiopoietin-1 therapy for early diabetic kidney disease. J Am Soc Nephrol 2014, 25(1):33-42.
75. Lee S., Kim W., Moon S.O., et al. Renoprotective effect of COMP-angiopoietin-1 in db/db mice with type 2 diabetes. Nephrol Dial Transplant 2007, 22(2):396-408.
76. Davis B., Dei Cas A., Long D.A., et al. Podocyte-specific expression of angiopoietin-2 causes proteinuria and apoptosis of glomerular endothelia. J Am Soc Nephrol 2007, 18(8):2320-2329.
77. Isermann B., Vinnikov I.A., Madhusudhan T., et al. Activated protein C protects against diabetic nephropathy by inhibiting endothelial and podocyte apoptosis. Nat Med 2007, 13(11):1349-1358.
78. Esmon C.T. Inflammation and the activated protein C anticoagulant pathway. Semin Thromb Hemost 2006, 32(suppl 1):49-60.
79. Bock F., Shahzad K., Wang H., et al. Activated protein C ameliorates diabetic nephropathy by epigenetically inhibiting the redox enzyme p66Shc. Proc Natl Acad Sci U S A 2013, 110(2):648-653.