Dedifferentiation of immortalized human podocytes in response to transforming growth factor-β: A model for diabetic podocytopathy

Diabetes

Volumn 60, Issue 6, 2011, Pages 1779-1788

  Herman Edelstein, Michal ^a,b   Thomas, Merlin C ^a   Thallas Bonke, Vicki ^a   Saleem, Moin ^c   Cooper, Mark E ^a   Kantharidis, Phillip ^a  

^a BAKER IDI HEART AND DIABETES INSTITUTE   (Australia)

^b TEL AVIV UNIVERSITY   (Israel)

^c UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

4 [4 (1,3 BENZODIOXOL 5 YL) 5 (2 PYRIDINYL) 1H IMIDAZOL 2 YL]BENZAMIDE; ALBUMIN; ALPHA SMOOTH MUSCLE ACTIN; ANGIOTENSIN II; COLLAGEN; COLLAGEN TYPE 1; COLLAGEN TYPE 4 ALPHA 3; CYCLINE; FIBRONECTIN; KI 67 ANTIGEN; NEPHRIN; NESTIN; P CADHERIN; PROTEIN ZO1; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG; VIMENTIN; WT1 PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ADHESION; CELL ASSAY; CELL COUNT; CELL DEDIFFERENTIATION; CELL IMMORTALIZATION; CELL LINE; CELL MEMBRANE PERMEABILITY; CELL PROLIFERATION; CELL STRUCTURE; CONTROLLED STUDY; CYTOSKELETON; DIABETIC NEPHROPATHY; DIABETIC PODOCYTOPATHY; EXPERIMENTAL STUDY; GENE EXPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE TEST; KNOCKOUT MOUSE; MOUSE; NONHUMAN; PODOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STREPTOZOCIN DIABETES; TIGHT JUNCTION;

ACTINS; ANGIOTENSIN II; APOPTOSIS; BLOTTING, WESTERN; CADHERINS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; COLLAGEN; DIABETIC NEPHROPATHIES; FIBRONECTINS; HUMANS; INTERMEDIATE FILAMENT PROTEINS; MEMBRANE PROTEINS; NERVE TISSUE PROTEINS; PODOCYTES; TRANSFORMING GROWTH FACTOR BETA; VIMENTIN;

EID: 79959439429     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db10-1110     Document Type: Article

References (53)

1. Ziyadeh FN, Wolf G. Pathogenesis of the podocytopathy and proteinuria in diabetic glomerulopathy. Curr Diabetes Rev 2008;4:39-45 (Pubitemid 351210971)
2. Wolf G, Chen S, Ziyadeh FN. From the periphery of the glomerular capillary wall toward the center of disease: podocyte injury comes of age in diabetic nephropathy. Diabetes 2005;54:1626-1634 (Pubitemid 40770751)
3. Li JJ, Kwak SJ, Jung DS, et al. Podocyte biology in diabetic nephropathy. Kidney Int Suppl 2007:S36-S42 (Pubitemid 47172559)
4. Salmon AH, Toma I, Sipos A, et al. Evidence for restriction of fluid and solute movement across the glomerular capillary wall by the subpodocyte space. Am J Physiol Renal Physiol 2007;293:F1777-F1786 (Pubitemid 350179602)
5. Reidy K, Susztak K. Epithelial-mesenchymal transition and podocyte loss in diabetic kidney disease. Am J Kidney Dis 2009;54:590-593
6. Margetts PJ, Bonniaud P, Liu L, et al. Transient overexpression of TGF-beta1 induces epithelial mesenchymal transition in the rodent peritoneum. J Am Soc Nephrol 2005;16:425-436 (Pubitemid 41725138)
7. Yamaguchi Y, Iwano M, Suzuki D, et al. Epithelial-mesenchymal transition as a potential explanation for podocyte depletion in diabetic nephropathy. Am J Kidney Dis 2009;54:653-664
8. Shankland SJ. The podocyte's response to injury: role in proteinuria and glomerulosclerosis. Kidney Int 2006;69:2131-2147 (Pubitemid 43882099)
9. Okada H, Danoff TM, Kalluri R, Neilson EG. Early role of Fsp1 in epithelial-mesenchymal transformation. Am J Physiol 1997;273:F563-F574
10. Fan JM, Huang XR, Ng YY, et al. Interleukin-1 induces tubular epithelialmyofibroblast transdifferentiation through a transforming growth factorbeta1- dependent mechanism in vitro. Am J Kidney Dis 2001;37:820-831
11. Strutz F, Zeisberg M, Ziyadeh FN, et al. Role of basic fibroblast growth factor-2 in epithelial-mesenchymal transformation. Kidney Int 2002;61:1714-1728 (Pubitemid 34437925)
12. Ha H, Lee HB. Reactive oxygen species and matrix remodeling in diabetic kidney. J Am Soc Nephrol 2003;14(Suppl. 3):S246-S249 (Pubitemid 36903934)
13. Lan HY. Tubular epithelial-myofibroblast transdifferentiation mechanisms in proximal tubule cells. Curr Opin Nephrol Hypertens 2003;12:25-29 (Pubitemid 36092311)
14. Yang J, Liu Y. Dissection of key events in tubular epithelial to myofibroblast transition and its implications in renal interstitial fibrosis. Am J Pathol 2001;159:1465-1475 (Pubitemid 32947976)
15. Kalluri R, Neilson EG. Epithelial-mesenchymal transition and its implications for fibrosis. J Clin Invest 2003;112:1776-1784 (Pubitemid 38063698)
16. Lee JM, Dedhar S, Kalluri R, Thompson EW. The epithelial-mesenchymal transition: new insights in signaling, development, and disease. J Cell Biol 2006;172:973-981
17. Zavadil J, Böttinger EP. TGF-beta and epithelial-to-mesenchymal transitions. Oncogene 2005;24:5764-5774
18. Ziyadeh FN. Different roles for TGF-beta and VEGF in the pathogenesis of the cardinal features of diabetic nephropathy. Diabetes Res Clin Pract 2008;82(Suppl. 1):S38-S41
19. Chen S, Lee JS, Iglesias-de la Cruz MC, et al. Angiotensin II stimulates alpha3(IV) collagen production in mouse podocytes via TGF-beta and VEGF signalling: implications for diabetic glomerulopathy. Nephrol Dial Transplant 2005;20:1320-1328
20. Iglesias-de la Cruz MC, Ziyadeh FN, Isono M, et al. Effects of high glucose and TGF-beta1 on the expression of collagen IV and vascular endothelial growth factor in mouse podocytes. Kidney Int 2002;62:901-913
21. Nakamura T, Fukui M, Ebihara I, et al. mRNA expression of growth factors in glomeruli from diabetic rats. Diabetes 1993;42:450-456 (Pubitemid 23066522)
22. Wu DT, Bitzer M, Ju W, Mundel P, Böttinger EP. TGF-beta concentration specifies differential signaling profiles of growth arrest/differentiation and apoptosis in podocytes. J Am Soc Nephrol 2005;16:3211-3221 (Pubitemid 46179327)
23. Susztak K, Raff AC, Schiffer M, Böttinger EP. Glucose-induced reactive oxygen species cause apoptosis of podocytes and podocyte depletion at the onset of diabetic nephropathy. Diabetes 2006;55:225-233 (Pubitemid 43343319)
24. Schiffer M, Bitzer M, Roberts IS, et al. Apoptosis in podocytes induced by TGF-beta and Smad7. J Clin Invest 2001;108:807-816 (Pubitemid 32880291)
25. Saleem MA, O'Hare MJ, Reiser J, et al. A conditionally immortalized human podocyte cell line demonstrating nephrin and podocin expression. J Am Soc Nephrol 2002;13:630-638 (Pubitemid 34183927)
26. Davis BJ, Johnston CI, Burrell LM, et al. Renoprotective effects of vasopeptidase inhibition in an experimental model of diabetic nephropathy. Diabetologia 2003;46:961-971 (Pubitemid 36961320)
27. Maruo N, Morita I, Shirao M, Murota S. IL-6 increases endothelial permeability in vitro. Endocrinology 1992;131:710-714
28. Lassila M, Seah KK, Allen TJ, et al. Accelerated nephropathy in diabetic apolipoprotein e-knockout mouse: role of advanced glycation end products. J Am Soc Nephrol 2004;15:2125-2138 (Pubitemid 39031351)
29. Li Y, Kang YS, Dai C, Kiss LP, Wen X, Liu Y. Epithelial-to-mesenchymal transition is a potential pathway leading to podocyte dysfunction and proteinuria. Am J Pathol 2008;172:299-308 (Pubitemid 351282018)
30. Seiler MW, Rennke HG, Venkatachalam MA, Cotran RS. Pathogenesis of polycation-induced alterations ("fusion") of glomerular epithelium. Lab Invest 1977;36:48-61 (Pubitemid 8021270)
31. Welsh GI, Hale LJ, Eremina V, et al. Insulin signaling to the glomerular podocyte is critical for normal kidney function. Cell Metab 2010;12:329-340
32. Zeisberg M, Neilson EG. Biomarkers for epithelial-mesenchymal transitions. J Clin Invest 2009;119:1429-1437
33. Wang B, Herman-Edelstein M, Koh P, et al. E-cadherin expression is regulated by miR-192/215 by a mechanism that is independent of the profibrotic effects of transforming growth factor-beta. Diabetes 2010;59: 1794-1802
34. Zhao L, Yaoita E, Nameta M, et al. Claudin-6 localized in tight junctions of rat podocytes. Am J Physiol Regul Integr Comp Physiol 2008;294:R1856-R1862
35. Fukasawa H, Bornheimer S, Kudlicka K, Farquhar MG. Slit diaphragms contain tight junction proteins. J Am Soc Nephrol 2009;20:1491-1503
36. Hunt JL, Pollak MR, Denker BM. Cultured podocytes establish a size-selective barrier regulated by specific signaling pathways and demonstrate synchronized barrier assembly in a calcium switch model of junction formation. J Am Soc Nephrol 2005;16:1593-1602 (Pubitemid 41716466)
37. Rincon-Choles H, Vasylyeva TL, Pergola PE, et al. ZO-1 expression and phosphorylation in diabetic nephropathy. Diabetes 2006;55:894-900 (Pubitemid 44100161)
38. Shankland SJ, Pippin JW, Reiser J, Mundel P. Podocytes in culture: past, present, and future. Kidney Int 2007;72:26-36 (Pubitemid 47014453)
39. Krtil J, Pláteník J, Kazderová M, Tesar V, Zima T. Culture methods of glomerular podocytes. Kidney Blood Press Res 2007;30:162-174 (Pubitemid 46976034)
40. Macconi D, Sangalli F, Bonomelli M, et al. Podocyte repopulation contributes to regression of glomerular injury induced by ACE inhibition. Am J Pathol 2009;174:797-807
41. Nakamura T, Ushiyama C, Suzuki S, et al. The urinary podocyte as a marker for the differential diagnosis of idiopathic focal glomerulosclerosis and minimal-change nephrotic syndrome. Am J Nephrol 2000;20:175-179 (Pubitemid 30445310)
42. Kretzler M. Role of podocytes in focal sclerosis: defining the point of no return. J Am Soc Nephrol 2005;16:2830-2832 (Pubitemid 44743478)
43. Lee HS, Song CY. Effects of TGF-beta on podocyte growth and disease progression in proliferative podocytopathies. Kidney Blood Press Res 2010;33:24-29
44. Wiggins JE, Patel SR, Shedden KA, et al. NFkappaB promotes inflammation, coagulation, and fibrosis in the aging glomerulus. J Am Soc Nephrol 2010;21:587-597
45. Bollineni JS, Reddi AS. Transforming growth factor-beta 1 enhances glomerular collagen synthesis in diabetic rats. Diabetes 1993;42:1673-1677 (Pubitemid 23318126)
46. Flores L, Näf S, Hernáez R, Conget I, Gomis R, Esmatjes E. Transforming growth factor beta at clinical onset of type 1 diabetes mellitus. A pilot study. Diabet Med 2004;21:818-822 (Pubitemid 39036993)
47. Pfeiffer A, Middelberg-Bisping K, Drewes C, Schatz H. Elevated plasma levels of transforming growth factor-beta 1 in NIDDM. Diabetes Care 1996; 19:1113-1117 (Pubitemid 26334260)
48. Nishiyama A, Seth DM, Navar LG. Renal interstitial fluid concentrations of angiotensins I and II in anesthetized rats. Hypertension 2002;39:129-134 (Pubitemid 34098101)
49. Asanuma K, Yanagida-Asanuma E, Faul C, Tomino Y, Kim K, Mundel P. Synaptopodin orchestrates actin organization and cell motility via regulation of RhoA signalling. Nat Cell Biol 2006;8:485-491
50. Hsu HH, Hoffmann S, Endlich N, et al. Mechanisms of angiotensin II signaling on cytoskeleton of podocytes. J Mol Med 2008;86:1379-1394
51. Saleem MA, Zavadil J, Bailly M, et al. The molecular and functional phenotype of glomerular podocytes reveals key features of contractile smooth muscle cells. Am J Physiol Renal Physiol 2008;295:F959-F970
52. Takeda T, McQuistan T, Orlando RA, Farquhar MG. Loss of glomerular foot processes is associated with uncoupling of podocalyxin from the actin cytoskeleton. J Clin Invest 2001;108:289-301 (Pubitemid 32656253)
53. Faul C, Asanuma K, Yanagida-Asanuma E, Kim K, Mundel P. Actin up: regulation of podocyte structure and function by components of the actin cytoskeleton. Trends Cell Biol 2007;17:428-437 (Pubitemid 47499042)