Glomerular parietal epithelial cells contribute to adult podocyte regeneration in experimental focal segmental glomerulosclerosis

Kidney International

Volumn 88, Issue 5, 2015, Pages 999-1012

  Eng, Diana G ^a   Sunseri, Maria W ^a   Kaverina, Natalya V ^a   Roeder, Sebastian S ^a   Pippin, Jeffrey W ^a   Shankland, Stuart J ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

CD44; ERK; Glomerulosclerosis; Glomerulus; Podocin; Progenitor

Indexed keywords

CELL ANTIBODY; CELL MARKER; CELL PROTEIN; HERMES ANTIGEN; MITOGEN ACTIVATED PROTEIN KINASE; ACTIN BINDING PROTEIN; BETA GALACTOSIDASE; CDKN1C PROTEIN, MOUSE; CYCLIN DEPENDENT KINASE INHIBITOR 1C; MEMBRANE PROTEIN; PODOCIN; SIGNAL PEPTIDE; SYNPO PROTEIN, MOUSE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; BOWMAN CAPSULE; CELL ACTIVATION; CELL COUNT; CELL FUNCTION; CELL LABELING; CELL MIGRATION; CELL PROLIFERATION; CELL REGENERATION; CONTROLLED STUDY; DISEASE COURSE; DISEASE SEVERITY; DNA MODIFICATION; ENZYME LOCALIZATION; ENZYME PHOSPHORYLATION; EPITHELIUM CELL; FOCAL GLOMERULOSCLEROSIS; GLOMERULAR PARIETAL EPITHELIAL CELL; KIDNEY CELL; MOUSE; NONHUMAN; PHENOTYPE; PODOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; STAINING; STEM CELL; ALBUMINURIA; ANIMAL; CELL MOTION; CHEMISTRY; COMPLICATION; DISEASE MODEL; METABOLISM; PATHOLOGY; PHYSIOLOGY; REGENERATION; SIGNAL TRANSDUCTION;

ALBUMINURIA; ANIMALS; ANTIGENS, CD44; BETA-GALACTOSIDASE; BOWMAN CAPSULE; CELL MOVEMENT; CELL PROLIFERATION; CYCLIN-DEPENDENT KINASE INHIBITOR P57; DISEASE MODELS, ANIMAL; EPITHELIAL CELLS; GLOMERULOSCLEROSIS, FOCAL SEGMENTAL; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MAP KINASE SIGNALING SYSTEM; MEMBRANE PROTEINS; MICE; MICROFILAMENT PROTEINS; PODOCYTES; REGENERATION; STEM CELLS;

EID: 84947618982     PISSN: 00852538     EISSN: 15231755     Source Type: Journal    
DOI: 10.1038/ki.2015.152     Document Type: Article

References (48)

1. Jefferson JA, Shankland SJ. The pathogenesis of focal segmental glomerulosclerosis. Adv Chronic Kidney Dis 2014; 21: 408-416.
2. Wharram BL, Goyal M, Wiggins JE 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.
3. Matsusaka T, Xin J, Niwa S et al. Genetic engineering of glomerular sclerosis in the mouse via control of onset and severity of podocytespecific injury. J Am Soc Nephrol 2005; 16: 1013-1023.
4. Marshall CB, Shankland SJ. Cell cycle regulatory proteins in podocyte health and disease. Nephron Exp Nephrol 2007; 106: e51-e59.
5. Appel D, Kershaw DB, Smeets B et al. Recruitment of podocytes from glomerular parietal epithelial cells. J Am Soc Nephrol 2009; 20: 333-343.
6. Grahammer F, Wanner N, Huber TB. Podocyte regeneration: who can become a podocyte? Am J Pathol 2013; 183: 333-335.
7. Shankland SJ, Smeets B, Pippin JW et al. The emergence of the glomerular parietal epithelial cell. Nat Rev Nephrol 2014; 10: 158-173.
8. Swetha G, Chandra V, Phadnis S et al. Glomerular parietal epithelial cells of adult murine kidney undergo EMT to generate cells with traits of renal progenitors. J Cell Mol Med 2011; 15: 396-413.
9. Sagrinati C, Netti GS, Mazzinghi B et al. Isolation and characterization of multipotent progenitor cells from the Bowman's capsule of adult human kidneys. J Am Soc Nephrol 2006; 17: 2443-2456.
10. Bariety J, Mandet C, Hill GS et al. Parietal podocytes in normal human glomeruli. J Am Soc Nephrol 2006; 17: 2770-2780.
11. Wanner N, Hartleben B, Herbach N et al. Unraveling the role of podocyte turnover in glomerular aging and injury. J Am Soc Nephrol 2014; 25: 707-716.
12. Berger K, Schulte K, Boor P et al. The regenerative potential of parietal epithelial cells in adult mice. J Am Soc Nephrol 2014; 25: 693-705.
13. Rizzo P, Perico N, Gagliardini E et al. Nature and mediators of parietal epithelial cell activation in glomerulonephritides of human and rat. Am J Pathol 2013; 183: 1769-1778.
14. Ohse T, Vaughan MR, Kopp JB et al. De novo expression of podocyte proteins in parietal epithelial cells during experimental glomerular disease. Am J Physiol Renal Physiol 2010; 298: F702-F711.
15. Zhang J, Yanez D, Floege A et al. ACE-inhibition increases podocyte number in experimental glomerular disease independent of proliferation. J Renin Angiotensin Aldosterone Syst 2014 (e-pub ahead of print).
16. Zhang J, Pippin JW, Krofft RD et al. Podocyte repopulation by renal progenitor cells following glucocorticoids treatment in experimental FSGS. Am J Physiol Renal Physiol 2013; 304: F1375-F1389.
17. Zhang J, Pippin JW, Vaughan MR et al. Retinoids augment the expression of podocyte proteins by glomerular parietal epithelial cells in experimental glomerular disease. Nephron Exp Nephrol 2012; 121: e23-e37.
18. Pichaiwong W, Hudkins KL, Wietecha T et al. Reversibility of structural and functional damage in a model of advanced diabetic nephropathy. J Am Soc Nephrol 2013; 24: 1088-1102.
19. Sagrinati C, Netti GS, Mazzinghi B et al. Isolation and characterization of multipotent progenitor cells from the Bowman's capsule of adult human kidneys. J Am Soc Nephrol 2006; 17: 2443-2456.
20. Ronconi E, Sagrinati C, Angelotti ML et al. Regeneration of glomerular podocytes by human renal progenitors. J Am Soc Nephrol 2009; 20: 322-332.
21. Kietzmann L, Guhr SS, Meyer TN et al. MicroRNA-193a regulates the transdifferentiation of human parietal epithelial cells toward a podocyte phenotype. J Am Soc Nephrol 2014 (e-pub ahead of print).
22. Sakamoto K, Ueno T, Kobayashi N et al. The direction and role of phenotypic transition between podocytes and parietal epithelial cells in focal segmental glomerulosclerosis. Am J Physiol Renal Physiol 2014; 306: F98-F104.
23. Hackl MJ, Burford JL, Villanueva K et al. Tracking the fate of glomerular epithelial cells in vivo using serial multiphoton imaging in new mouse models with fluorescent lineage tags. Nat Med 2013; 19: 1661-1666.
24. Miyazaki Y, Shimizu A, Ichikawa I et al. Mice are unable to endogenously regenerate podocytes during the repair of immunotoxin-induced glomerular injury. Nephrol Dial Transplant 2014; 29: 1005-1012.
25. Guhr SS, Sachs M, Wegner A et al. The expression of podocyte-specific proteins in parietal epithelial cells is regulated by protein degradation. Kidney Int 2013; 84: 532-544.
26. Pippin JW, Sparks MA, Glenn ST et al. Cells of renin lineage are progenitors of podocytes and parietal epithelial cells in experimental glomerular disease. Am J Pathol 2013; 183: 542-557.
27. Pippin JW, Glenn ST, Krofft RD et al. Cells of renin lineage take on a podocyte phenotype in aging nephropathy. Am J Physiol Renal Physiol 2014; 306: F1198-F1209.
28. Smeets B, Uhlig S, Fuss A et al. Tracing the origin of glomerular extracapillary lesions from parietal epithelial cells. J Am Soc Nephrol 2009; 20: 2604-2615.
29. Chang AM, Ohse T, Krofft RD et al. Albumin-induced apoptosis of glomerular parietal epithelial cells is modulated by extracellular signalregulated kinase 1/2. Nephrol Dia Transplant 2012; 27: 1330-1343.
30. Fatima H, Moeller MJ, Smeets B et al. Parietal epithelial cell activation marker in early recurrence of FSGS in the transplant. Clin J Am Soc Nephrol 2012; 7: 1852-1858.
31. Smeets B, Moeller MJ. Parietal epithelial cells and podocytes in glomerular diseases. Semin Nephrol 2012; 32: 357-367.
32. Smeets B, Kuppe C, Sicking EM et al. Parietal epithelial cells participate in the formation of sclerotic lesions in focal segmental glomerulosclerosis. J Am Soc Nephrol 2011; 22: 1262-1274.
33. Fanni D, Fanos V, Gerosa C et al. CD44 immunoreactivity in the developing human kidney: a marker of renal progenitor stem cells? Ren Fail 2013; 35: 967-970.
34. Schmits R, Filmus J, Gerwin N et al. CD44 regulates hematopoietic progenitor distribution, granuloma formation, and tumorigenicity. Blood 1997; 90: 2217-2233.
35. Sicking EM, Fuss A, Uhlig S et al. Subtotal ablation of parietal epithelial cells induces crescent formation. J Am Soc Nephrol 2012; 23: 629-640.
36. Okamoto T, Sasaki S, Yamazaki T et al. Prevalence of CD44-positive glomerular parietal epithelial cells reflects podocyte injury in adriamycin nephropathy. Nephron Exp Nephrol 2013; 124: 11-18.
37. Marshall CB, Krofft RD, Blonski MJ et al. Role of smooth muscle protein SM22alpha in glomerular epithelial cell injury. Am J Physiol Renal Physiol 2011; 300: F1026-F1042.
38. Ruggenenti P, Perna A, Benini R et al. In chronic nephropathies prolonged ACE inhibition can induce remission: dynamics of time-dependent changes in GFR. Investigators of the GISEN Group. Gruppo Italiano Studi Epidemiologici in Nefrologia. J Am Soc Nephrol 1999; 10: 997-1006.
39. 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.
40. Benigni A, Morigi M, Rizzo P et al. Inhibiting angiotensin-converting enzyme promotes renal repair by limiting progenitor cell proliferation and restoring the glomerular architecture. Am J Pathol 2011; 179: 628-638.
41. Romagnani P, Lasagni L, Remuzzi G. Renal progenitors: an evolutionary conserved strategy for kidney regeneration. Nat Rev Nephrol 2013; 9: 137-146.
42. Smeets B, Stucker F, Wetzels J et al. Detection of activated parietal epithelial cells on the glomerular tuft distinguishes early focal segmental glomerulosclerosis from minimal change disease. Am J Pathol 2014; 184: 3239-3248.
43. Hakroush S, Cebulla A, Schaldecker T et al. Extensive podocyte loss triggers a rapid parietal epithelial cell response. J Am Soc Nephrol 2014; 25: 927-938.
44. Schulte K, Berger K, Boor P et al. Origin of parietal podocytes in atubular glomeruli mapped by lineage tracing. J Am Soc Nephrol 2014; 25: 129-141.
45. Traykova-Brauch M, Schonig K, Greiner O et al. An efficient and versatile system for acute and chronic modulation of renal tubular function in transgenic mice. Nat Med 2008; 14: 979-984.
46. Ohse T, Vaughan MR, Kopp JB et al. De novo expression of podocyte proteins in parietal epithelial cells during experimental glomerular disease. Am J Physiol Renal Physiol 2010; 298: F702-F711.
47. Ohse T, Chang AM, Pippin JW et al. A new function for parietal epithelial cells: a second glomerular barrier. Am J Physiol Renal Physiol 2009; 297: F1566-F1574.
48. Marshall CB, Krofft RD, Pippin JW et al. The CDK-inhibitor p21 is pro-survival in adriamycin(R)-induced podocyte injury, in vitro and in vivo. Am J Physiol Renal Physiol 2010; 298: F1140-F1151.