Podocyte Biology in Segmental Sclerosis and Progressive Glomerular Injury

Advances in Chronic Kidney Disease

Volumn 19, Issue 2, 2012, Pages 76-83

  Barisoni, Laura ^a,b  

^a NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

^b Department of Medicine ^*  (United States)

Author keywords

Aging; Glomerulosclerosis; Podocytes; Progression; Repair

Indexed keywords

BETA CATENIN; BETA4 INTEGRIN; INTERLEUKIN 2 RECEPTOR ALPHA; NEPHRIN; PIRFENIDONE; PLATELET DERIVED GROWTH FACTOR; PODOCIN; TRANSIENT RECEPTOR POTENTIAL CHANNEL 6; VASCULOTROPIN; WNT PROTEIN;

CELL AGING; CELL DIFFERENTIATION; DISEASE COURSE; GENE MUTATION; GLOMERULOPATHY; GLOMERULOSCLEROSIS; GLOMERULUS BASEMENT MEMBRANE; HUMAN; KIDNEY BIOPSY; NONHUMAN; OBESITY; PODOCYTE; PRACTICE GUIDELINE; PRIORITY JOURNAL; REVIEW; TUMOR SUPPRESSOR GENE;

EID: 84858766288     PISSN: 15485595     EISSN: 15485609     Source Type: Journal    
DOI: 10.1053/j.ackd.2012.02.018     Document Type: Review

References (97)

1. Fries J.W., Sandstrom D.J., Meyer T.W., Rennke H.G. Glomerular hypertrophy and epithelial cell injury modulate progressive glomerulosclerosis in the rat. Lab Invest 1989, 60:205-218.
2. Nagata M., Kriz W. Glomerular damage after uninephrectomy in young rats: part II. Mechanical stress on podocytes as a pathway to sclerosis. Kidney Int 1992, 42:148-160.
3. Nagata M., Scharer K., Kriz W. Glomerular damage after uninephrectomy in young rats: part I. Hypertrophy and distortion of capillary architecture. Kidney Int 1992, 42:136-147.
4. Whiteside C., Prutis K., Cameron R., Thompson J. Glomerular epithelial detachment, not reduced charge density, correlates with proteinuria in adriamycin and puromycin nephrosis. Lab Invest 1989, 61:650-660.
5. Cho C.R., Lumsden C.J., Whiteside C.I. Epithelial cell detachment in the nephrotic glomerulus: a receptor co-operativity model. J Theor Biol 1993, 160:407-426.
6. Kriz W., Gretz N., Lemley K.V. Progression of glomerular diseases: is the podocyte the culprit?. Kidney Int 1998, 54:687-697.
7. Pavenstadt H., Kriz W., Kretzler M. Cell biology of the glomerular podocyte. Physiol Rev 2003, 83:253-307.
8. Rennke H.G. How does glomerular epithelial cell injury contribute to progressive glomerular damage?. Kidney Int Suppl 1994, 45:S58-S63.
9. Drenckhahn D., Franke R.P. Ultrastructural organization of contractile and cytoskeletal proteins in glomerular podocytes of chicken, rat, and man. Lab Invest 1988, 59:673-682.
10. Kriz W., Elger M., Mundel P., Lemley K.V. Structure-stabilizing forces in the glomerular tuft. J Am Soc Nephrol 1995, 5:1731-1739.
11. Kriz W., LeHir M. Pathways to nephron loss starting from glomerular diseases-insights from animal models. Kidney Int 2005, 67:404-419.
12. Brenner B.M., Meyer T.W., Hostetter T.H. Dietary protein intake and the progressive nature of kidney disease: the role of hemodynamically mediated glomerular injury in the pathogenesis of progressive glomerular sclerosis in aging, renal ablation, and intrinsic renal disease. N Engl J Med 1982, 307:652-659.
13. Matsusaka T., Sandgren E., Shintani A., et al. Podocyte injury damages other podocytes. J Am Soc Nephrol 2011, 22:1275-1285.
14. Barisoni L., Schnaper H.W., Kopp J.B. Advances in the biology and genetics of the podocytopathies: implications for diagnosis and therapy. Arch Pathol Lab Med 2009, 133:201-216.
15. Jefferson J.A., Alpers C.E., Shankland S.J. Podocyte biology for the bedside. Am J Kidney Dis 2011, 58:835-845.
16. Barisoni L., Schnaper H.W., Kopp J.B. A proposed taxonomy for the podocytopathies: a reassessment of the primary nephrotic diseases. Clin J Am Soc Nephrol 2007, 2:529-542.
17. Morrison A.A., Viney R.L., Ladomery M.R. The post-transcriptional roles of WT1, a multifunctional zinc-finger protein. Biochim Biophys Acta 2008, 1785:55-62.
18. Yang Y., Gubler M.C., Beaufils H. Dysregulation of podocyte phenotype in idiopathic collapsing glomerulopathy and HIV-associated nephropathy. Nephron 2002, 91:416-423.
19. Yang Y., Jeanpierre C., Dressler G.R., Lacoste M., Niaudet P., Gubler M.C. WT1 and PAX-2 podocyte expression in Denys-Drash syndrome and isolated diffuse mesangial sclerosis. Am J Pathol 1999, 154:181-192.
20. Rohr C., Prestel J., Heidet L., et al. The LIM-homeodomain transcription factor Lmx1b plays a crucial role in podocytes. J Clin Invest 2002, 109:1073-1082.
21. Waters A.M., Wu M.Y., Onay T., et al. Ectopic notch activation in developing podocytes causes glomerulosclerosis. J Am Soc Nephrol 2008, 19:1139-1157.
22. Niranjan T., Bielesz B., Gruenwald A., et al. The Notch pathway in podocytes plays a role in the development of glomerular disease. Nat Med 2008, 14:290-298.
23. Kestila M., Lenkkeri U., Mannikko M., et al. Positionally cloned gene for a novel glomerular protein-nephrin-is mutated in congenital nephrotic syndrome. Mol Cell 1998, 1:575-582.
24. Endlich N., Kress K.R., Reiser J., et al. Podocytes respond to mechanical stress in vitro. J Am Soc Nephrol 2001, 12:413-422.
25. Murphy-Ullrich J.E. The de-adhesive activity of matricellular proteins: is intermediate cell adhesion an adaptive state?. J Clin Invest 2001, 107:785-790.
26. Cybulsky A.V., Kennedy C.R. Podocyte injury associated with mutant alpha-actinin-4. J Signal Transduct 2011, 2011:563128.
27. Liu Z., Blattner S.M., Tu Y., et al. Alpha-actinin-4 and CLP36 protein deficiencies contribute to podocyte defects in multiple human glomerulopathies. J Biol Chem 2011, 286:30795-30805.
28. Kopp J.B., Smith M.W., Nelson G.W., et al. MYH9 is a major-effect risk gene for focal segmental glomerulosclerosis. Nat Genet 2008, 40:1175-1184.
29. Winkler C.A., Nelson G., Oleksyk T.K., Nava M.B., Kopp J.B. Genetics of focal segmental glomerulosclerosis and human immunodeficiency virus-associated collapsing glomerulopathy: the role of MYH9 genetic variation. Semin Nephrol 2010, 30:111-125.
30. Boyer O., Benoit G., Gribouval O., et al. Mutations in INF2 are a major cause of autosomal dominant focal segmental glomerulosclerosis. J Am Soc Nephrol 2011, 22:239-245.
31. Brown E.J., Schlondorff J.S., Becker D.J., et al. Mutations in the formin gene INF2 cause focal segmental glomerulosclerosis. Nat Genet 2010, 42:72-76.
32. Gbadegesin R.A., Lavin P.J., Hall G., et al. Inverted formin 2 mutations with variable expression in patients with sporadic and hereditary focal and segmental glomerulosclerosis. Kidney Int 2012, 81:94-99.
33. Mele C., Iatropoulos P., Donadelli R., et al. MYO1E mutations and childhood familial focal segmental glomerulosclerosis. N Engl J Med 2011, 365:295-306.
34. Winn M.P., Conlon P.J., Lynn K.L., et al. A mutation in the TRPC6 cation channel causes familial focal segmental glomerulosclerosis. Science 2005, 308:1801-1804.
35. Gbadegesin R., Hinkes B.G., Hoskins B.E., et al. Mutations in PLCE1 are a major cause of isolated diffuse mesangial sclerosis (IDMS). Nephrol Dial Transplant 2008, 23:1291-1297.
36. Zenker M., Aigner T., Wendler O., et al. Human laminin beta2 deficiency causes congenital nephrosis with mesangial sclerosis and distinct eye abnormalities. Hum Mol Genet 2004, 13:2625-2632.
37. Kambham N., Tanji N., Seigle R.L., et al. Congenital focal segmental glomerulosclerosis associated with beta4 integrin mutation and epidermolysis bullosa. Am J Kidney Dis 2000, 36:190-196.
38. Akilesh S., Suleiman H., Yu H., et al. Arhgap24 inactivates Rac1 in mouse podocytes, and a mutant form is associated with familial focal segmental glomerulosclerosis. J Clin Invest 2011, 121:4127-4137.
39. Sachs N., Claessen N., Aten J., et al. Blood pressure influences end-stage renal disease of Cd151 knockout mice. J Clin Invest 2012, 122:348-358.
40. Dryer S.E., Reiser J. TRPC6 channels and their binding partners in podocytes: role in glomerular filtration and pathophysiology. Am J Physiol Renal Physiol 2010, 299:F689-F701.
41. Barri Y.M., Munshi N.C., Sukumalchantra S., et al. Podocyte injury associated glomerulopathies induced by pamidronate. Kidney Int 2004, 65:634-641.
42. Markowitz G.S., Appel G.B., Fine P.L., et al. Collapsing focal segmental glomerulosclerosis following treatment with high-dose pamidronate. J Am Soc Nephrol 2001, 12:1164-1172.
43. Rogers M.J., Gordon S., Benford H.L., et al. Cellular and molecular mechanisms of action of bisphosphonates. Cancer 2000, 88(suppl 12):2961-2978.
44. Sauter M., Julg B., Porubsky S., et al. Nephrotic-range proteinuria following pamidronate therapy in a patient with metastatic breast cancer: mitochondrial toxicity as a pathogenetic concept?. Am J Kidney Dis 2006, 47:1075-1080.
45. Barisoni L., Diomedi-Camassei F., Santorelli F.M., et al. Collapsing glomerulopathy associated with inherited mitochondrial injury. Kidney Int 2008, 74:237-243.
46. Cybulsky A.V., Takano T., Papillon J., Kitzler T.M., Bijian K. Endoplasmic reticulum stress in glomerular epithelial cell injury. Am J Physiol Renal Physiol 2011, 301:F496-F508.
47. Kaplan C., Pasternack B., Shah H., Gallo G. Age-related incidence of sclerotic glomeruli in human kidneys. Am J Pathol 1975, 80:227-234.
48. Kappel B., Olsen S. Cortical interstitial tissue and sclerosed glomeruli in the normal human kidney, related to age and sex: a quantitative study. Virchows Arch A Pathol Anat Histol 1980, 387:271-277.
49. Wiggins J.E., Patel S.R., Shedden K.A., et al. NFkappaB promotes inflammation, coagulation, and fibrosis in the aging glomerulus. J Am Soc Nephrol 2010, 21:587-597.
50. Adler A.S., Kawahara T.L., Segal E., Chang H.Y. Reversal of aging by NFkappaB blockade. Cell Cycle 2008, 7:556-559.
51. Adler A.S., Sinha S., Kawahara T.L., Zhang J.Y., Segal E., Chang H.Y. Motif module map reveals enforcement of aging by continual NF-kappaB activity. Genes Dev 2007, 21:3244-3257.
52. Brink T.C., Demetrius L., Lehrach H., Adjaye J. Age-related transcriptional changes in gene expression in different organs of mice support the metabolic stability theory of aging. Biogerontology 2009, 10:549-564.
53. Brink T.C., Regenbrecht C., Demetrius L., Lehrach H., Adjaye J. Activation of the immune response is a key feature of aging in mice. Biogerontology 2009, 10:721-734.
54. Helenius M., Hanninen M., Lehtinen S.K., Salminen A. Changes associated with aging and replicative senescence in the regulation of transcription factor nuclear factor-kappa B. Biochem J 1996, 318(Pt 2):603-608.
55. Hoffmann A., Natoli G., Ghosh G. Transcriptional regulation via the NF-kappaB signaling module. Oncogene 2006, 25:6706-6716.
56. Perkins N.D. Integrating cell-signalling pathways with NF-kappaB and IKK function. Nat Rev Mol Cell Biol 2007, 8:49-62.
57. Keenan K.P., Coleman J.B., McCoy C.L., Hoe C.M., Soper K.A., Laroque P. Chronic nephropathy in ad libitum overfed Sprague-Dawley rats and its early attenuation by increasing degrees of dietary (caloric) restriction to control growth. Toxicol Pathol 2000, 28:788-798.
58. Maeda H., Gleiser C.A., Masoro E.J., Murata I., McMahan C.A., Yu B.P. Nutritional influences on aging of Fischer 344 rats: part II. Pathology. J Gerontol 1985, 40:671-688.
59. Wiggins J.E., Goyal M., Sanden S.K., et al. Podocyte hypertrophy, " adaptation," and " decompensation" associated with glomerular enlargement and glomerulosclerosis in the aging rat: prevention by calorie restriction. J Am Soc Nephrol 2005, 16:2953-2966.
60. Yu B.P., Masoro E.J., McMahan C.A. Nutritional influences on aging of Fischer 344 rats: part I. Physical, metabolic, and longevity characteristics. J Gerontol 1985, 40:657-670.
61. Zhang J., Hansen K.M., Pippin J.W., et al. De novo expression of podocyte proteins in parietal epithelial cells in experimental aging nephropathy. Am J Physiol Renal Physiol 2012, 302:F571-F580.
62. Genovese G., Friedman D.J., Ross M.D., et al. Association of trypanolytic ApoL1 variants with kidney disease in African Americans. Science 2010, 329:841-845.
63. Hostetter T.H., Olson J.L., Rennke H.G., Venkatachalam M.A., Brenner B.M. Hyperfiltration in remnant nephrons: a potentially adverse response to renal ablation. Am J Physiol 1981, 241:F85-F93.
64. Miller P.L., Rennke H.G., Meyer T.W. Hypertension and progressive glomerular injury caused by focal glomerular ischemia. Am J Physiol 1990, 259(2 Pt 2):F239-F245.
65. Miller P.L., Scholey J.W., Rennke H.G., Meyer T.W. Glomerular hypertrophy aggravates epithelial cell injury in nephrotic rats. J Clin Invest 1990, 85:1119-1126.
66. Asano T., Niimura F., Pastan I., Fogo A.B., Ichikawa I., Matsusaka T. Permanent genetic tagging of podocytes: fate of injured podocytes in a mouse model of glomerular sclerosis. J Am Soc Nephrol 2005, 16:2257-2262.
67. Matsusaka T., Xin J., Niwa S., et al. Genetic engineering of glomerular sclerosis in the mouse via control of onset and severity of podocyte-specific injury. J Am Soc Nephrol 2005, 16:1013-1023.
68. 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, 16:2941-2952.
69. Wiggins J. Geriatrics. Am J Kidney Dis 2005, 46:147-158.
70. Kim Y.H., Goyal M., Kurnit D., et al. Podocyte depletion and glomerulosclerosis have a direct relationship in the PAN-treated rat. Kidney Int 2001, 60:957-968.
71. Lemley K.V., Lafayette R.A., Safai M., et al. Podocytopenia and disease severity in IgA nephropathy. Kidney Int 2002, 61:1475-1485.
72. Hara K., Yanagihara N., Minami K., et al. Ketamine interacts with the noradrenaline transporter at a site partly overlapping the desipramine binding site. Naunyn Schmiedebergs Arch Pharmacol 1998, 358:328-333.
73. Vogelmann S.U., Nelson W.J., Myers B.D., Lemley K.V. Urinary excretion of viable podocytes in health and renal disease. Am J Physiol Renal Physiol 2003, 285:F40-F48.
74. Yu D., Petermann A., Kunter U., Rong S., Shankland S.J., Floege J. Urinary podocyte loss is a more specific marker of ongoing glomerular damage than proteinuria. J Am Soc Nephrol 2005, 16:1733-1741.
75. Sato Y., Wharram B.L., Lee S.K., et al. Urine podocyte mRNAs mark progression of renal disease. J Am Soc Nephrol 2009, 20:1041-1052.
76. Gurtner G.C., Werner S., Barrandon Y., Longaker M.T. Wound repair and regeneration. Nature 2008, 453:314-321.
77. Romagnani P. Toward the identification of a " renopoietic system" ?. Stem Cells 2009, 27:2247-2253.
78. Imasawa T., Utsunomiya Y., Kawamura T., et al. The potential of bone marrow-derived cells to differentiate to glomerular mesangial cells. J Am Soc Nephrol 2001, 12:1401-1409.
79. Masuya M., Drake C.J., Fleming P.A., et al. Hematopoietic origin of glomerular mesangial cells. Blood 2003, 101:2215-2218.
80. Rookmaaker M.B., Smits A.M., Tolboom H., et al. Bone-marrow-derived cells contribute to glomerular endothelial repair in experimental glomerulonephritis. Am J Pathol 2003, 163:553-562.
81. Ronconi E., Sagrinati C., Angelotti M.L., et al. Regeneration of glomerular podocytes by human renal progenitors. J Am Soc Nephrol 2009, 20:322-332.
82. Marinides G.N., Groggel G.C., Cohen A.H., Border W.A. Enalapril and low protein reverse chronic puromycin aminonucleoside nephropathy. Kidney Int 1990, 37:749-757.
83. Adamczak M., Gross M.L., Krtil J., et al. Reversal of glomerulosclerosis after high-dose enalapril treatment in subtotally nephrectomized rats. J Am Soc Nephrol 2003, 14:2833-2842.
84. Fujihara C.K., Velho M., Malheiros D.M., Zatz R. An extremely high dose of losartan affords superior renoprotection in the remnant model. Kidney Int 2005, 67:1913-1924.
85. Ma L.J., Nakamura S., Aldigier J.C., et al. Regression of glomerulosclerosis with high-dose angiotensin inhibition is linked to decreased plasminogen activator inhibitor-1. J Am Soc Nephrol 2005, 16:966-976.
86. Ma L.J., Nakamura S., Whitsitt J.S., Marcantoni C., Davidson J.M., Fogo A.B. Regression of sclerosis in aging by an angiotensin inhibition-induced decrease in PAI-1. Kidney Int 2000, 58:2425-2436.
87. Remuzzi A., Fassi A., Bertani T., Perico N., Remuzzi G. ACE inhibition induces regression of proteinuria and halts progression of renal damage in a genetic model of progressive nephropathy. Am J Kidney Dis 1999, 34:626-632.
88. Remuzzi A., Gagliardini E., Donadoni C., et al. Effect of angiotensin II antagonism on the regression of kidney disease in the rat. Kidney Int 2002, 62:885-894.
89. Remuzzi A., Gagliardini E., Sangalli F., et al. ACE inhibition reduces glomerulosclerosis and regenerates glomerular tissue in a model of progressive renal disease. Kidney Int 2006, 69:1124-1130.
90. 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.
91. Gherardi D., D'Agati V., Chu T.H., et al. Reversal of collapsing glomerulopathy in mice with the cyclin-dependent kinase inhibitor CYC202. J Am Soc Nephrol 2004, 15:1212-1222.
92. Nelson P.J., D'Agati V.D., Gries J.M., Suarez J.R., Gelman I.H. Amelioration of nephropathy in mice expressing HIV-1 genes by the cyclin-dependent kinase inhibitor flavopiridol. J Antimicrob Chemother 2003, 51:921-929.
93. Sharma K., Ramachandrarao S., Qiu G., et al. Adiponectin regulates albuminuria and podocyte function in mice. J Clin Invest 2008, 118:1645-1656.
94. Tsioufis C., Dimitriadis K., Chatzis D., et al. Relation of microalbuminuria to adiponectin and augmented C-reactive protein levels in men with essential hypertension. Am J Cardiol 2005, 96:946-951.
95. Yano Y., Hoshide S., Ishikawa J., et al. Differential impacts of adiponectin on low-grade albuminuria between obese and nonobese persons without diabetes. J Clin Hypertens (Greenwich) 2007, 9:775-782.
96. Cho M.E., Kopp J.B. Pirfenidone: an anti-fibrotic therapy for progressive kidney disease. Expert Opin Investig Drugs 2010, 19:275-283.
97. Li Y.C. Podocytes as target of vitamin D. Curr Diakbetes Rev 2011, 7:35-40.