Partial podocyte replenishment in experimental FSGS derives from nonpodocyte sources

American Journal of Physiology - Renal Physiology

Volumn 310, Issue 11, 2016, Pages F1397-F1413

  Kaverina, Natalya V ^a   Eng, Diana G ^a   Schneider, Remington R S ^a   Pippin, Jeffrey W ^a   Shankland, Stuart J ^a  

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

Author keywords

Enalapril; Glomerular parietal epithelial cells; Glomerulus; P57; Podocin; Progenitor; Regeneration; RTTA reporter mouse; Synaptopodin

Indexed keywords

4',6 DIAMIDINO 2 PHENYLINDOLE; BROXURIDINE; CLAUDIN 1; CYCLIN DEPENDENT KINASE INHIBITOR 1C; CYTOTOXIC ANTIBODY; ENALAPRIL; GREEN FLUORESCENT PROTEIN; PODOCIN; PROTEIN; SSECKS PROTEIN; SYNAPTOPODIN; TRANSCRIPTION FACTOR PAX8; UNCLASSIFIED DRUG; ACTIN BINDING PROTEIN; MEMBRANE PROTEIN; SIGNAL PEPTIDE; SYNPO PROTEIN, MOUSE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BOWMAN CAPSULE; CELL LABELING; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; DISEASE COURSE; FOCAL GLOMERULOSCLEROSIS; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; KIDNEY TUBULE CELL; MOUSE; NONHUMAN; PODOCYTE; PRIORITY JOURNAL; ANIMAL; DISEASE MODEL; GLOMERULUS; METABOLISM; PATHOLOGY;

ANIMALS; BOWMAN CAPSULE; DISEASE MODELS, ANIMAL; GLOMERULOSCLEROSIS, FOCAL SEGMENTAL; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; KIDNEY GLOMERULUS; MEMBRANE PROTEINS; MICE; MICROFILAMENT PROTEINS; PODOCYTES;

EID: 84984622658     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00369.2015     Document Type: Article

References (58)

1. Altintas MM, Reiser J. Bridges to cross, burn, and mend: cells of renin lineage as podocyte progenitors. Am J Physiol Renal Physiol 309: F499-F500, 2015.
2. Appel D, Kershaw DB, Smeets B, Yuan G, Fuss A, Frye B, Elger M, Kriz W, Floege J, Moeller MJ. Recruitment of podocytes from glomerular parietal epithelial cells. J Am Soc Nephrol 20: 333-343, 2009.
3. Asanuma K. [The role of podocyte injury in chronic kidney disease]. Nihon Rinsho Meneki Gakkai Kaishi 38: 26-36, 2015.
4. Asanuma K, Yanagida-Asanuma E, Takagi M, Kodama F, Tomino Y. The role of podocytes in proteinuria. Nephrology 12, Suppl 3: S15-S20, 2007.
5. Bariety J, Mandet C, Hill GS, Bruneval P. Parietal podocytes in normal human glomeruli. J Am Soc Nephrol 17: 2770-2780, 2006.
6. D’Agati VD. Pathobiology of focal segmental glomerulosclerosis: new developments. Curr Opin Nephrol Hypertens 21: 243-250, 2012.
7. Eng DG, Sunseri MW, Kaverina NV, Roeder SS, Pippin JW, Shankland SJ. Glomerular parietal epithelial cells contribute to adult podocyte regeneration in experimental focal segmental glomerulosclerosis. Kidney Int 88: 999-1012, 2015.
8. Fogo AB. Causes and pathogenesis of focal segmental glomerulosclerosis. Nat Rev Nephrol 11: 76-87, 2015.
9. Gagliardini E, Benigni A. Drugs to foster kidney regeneration in experimental animals and humans. Nephron Exp Nephrol 126: 91, 2014.
10. Gardiner DS, Downie I, Gibson IW, More IA, Lindop GB. The glomerular peripolar cell: a review. Histol Histopathol 6: 567-573, 1991.
11. Gibson IW, More IA, Lindop GB. A scanning electron-microscopic study of the peripolar cell of the rat renal glomerulus. Cell Tissue Res 257: 201-206, 1989.
12. Griffin SV, Krofft RD, Pippin JW, Shankland SJ. Limitation of podocyte proliferation improves renal function in experimental crescentic glomerulonephritis. Kidney Int 67: 977-986, 2005.
13. Guhr SS, Sachs M, Wegner A, Becker JU, Meyer TN, Kietzmann L, Schlossarek S, Carrier L, Braig M, Jat PS, Stahl RA, Meyer-Schwesinger C. The expression of podocyte-specific proteins in parietal epithelial cells is regulated by protein degradation. Kidney Int 84: 532-544, 2013.
14. Hackl MJ, Burford JL, Villanueva K, Lam L, Susztak K, Schermer B, Benzing T, Peti-Peterdi J. Tracking the fate of glomerular epithelial cells in vivo using serial multiphoton imaging in new mouse models with fluorescent lineage tags. Nat Med 19: 1661-1666, 2013.
15. Kietzmann L, Guhr SS, Meyer TN, Ni L, Sachs M, Panzer U, Stahl RA, Saleem MA, Kerjaschki D, Gebeshuber CA, Meyer-Schwesinger C. MicroRNA-193a regulates the transdifferentiation of human parietal epithelial cells toward a podocyte phenotype. J Am Soc Nephrol 26: 1389-1401, 2015.
16. Kopp JB. Replenishment of the podocyte compartment by parietal epithelial cells. Kidney Int 88: 934-935, 2015.
17. Kuppe C, Grone HJ, Ostendorf T, van Kuppevelt TH, Boor P, Floege J, Smeets B, Moeller MJ. Common histological patterns in glomerular epithelial cells in secondary focal segmental glomerulosclerosis. Kidney Int 88: 990-998, 2015.
18. Lasagni L, Angelotti ML, Ronconi E, Lombardi D, Nardi S, Peired A, Becherucci F, Mazzinghi B, Sisti A, Romoli S, Burger A, Schaefer B, Buccoliero A, Lazzeri E, Romagnani P. Podocyte regeneration driven by renal progenitors determines glomerular disease remission and can be pharmacologically enhanced. Stem Cell Rep 5: 248-263, 2015.
19. Lasagni L, Lazzeri E, Shankland SJ, Anders HJ, Romagnani P. Podocyte mitosis -a catastrophe. Curr Mol Med 13: 13-23, 2013.
20. Lasagni L, Romagnani P. Basic research: podocyte progenitors and ectopic podocytes. Nat Rev Nephrol 9: 715-716, 2013.
21. Lichtnekert J, Kaverina NV, Eng DG, Gross KW, Kutz JN, Pippin JW, Shankland SJ. Renin-angiotensin-aldosterone system inhibition increases podocyte derivation from cells of renin lineage. J Am Soc Nephrol. [Epub ahead of print].
22. Lin X, Tombler E, Nelson PJ, Ross M, Gelman IH. A novel src-and ras-suppressed protein kinase C substrate associated with cytoskeletal architecture. J Biol Chem 271: 28430-28438, 1996.
23. Macconi D, Sangalli F, Bonomelli M, Conti S, Condorelli L, Gagliardini E, Remuzzi G, Remuzzi A. Podocyte repopulation contributes to regression of glomerular injury induced by ACE inhibition. Am J Pathol 174: 797-807, 2009.
24. Maezawa Y, Onay T, Scott RP, Keir LS, Dimke H, Li C, Eremina V, Maezawa Y, Jeansson M, Shan J, Binnie M, Lewin M, Ghosh A, Miner JH, Vainio SJ, Quaggin SE. Loss of the podocyte-expressed transcription factor Tcf21/Pod1 results in podocyte differentiation defects and FSGS. J Am Soc Nephrol 25: 2459-2470, 2014.
25. Marshall CB, Shankland SJ. Cell cycle regulatory proteins in podocyte health and disease. Nephron Exp Nephrol 106: e51-e59, 2007.
26. Matsusaka T, Xin J, Niwa S, Kobayashi K, Akatsuka A, Hashizume H, Wang QC, Pastan I, Fogo AB, Ichikawa I. Genetic engineering of glomerular sclerosis in the mouse via control of onset and severity of podocyte-specific injury. J Am Soc Nephrol 16: 1013-1023, 2005.
27. Miyazaki Y, Shimizu A, Ichikawa I, Hosoya T, Pastan I, Matsusaka T. Mice are unable to endogenously regenerate podocytes during the repair of immunotoxin-induced glomerular injury. Nephrol Dial Transplant 29: 1005-1012, 2014.
28. Moustafa FE, Soliman NA, Bakr AM, El Shwaf IM. Assessment of detached podocytes in the Bowman’s space as a marker of disease activity in lupus nephritis. Lupus 23: 146-150, 2014.
29. Mundel P, Shankland SJ. Podocyte biology and response to injury. JAm Soc Nephrol 13: 3005-3015, 2002.
30. Nemeth Z, Kokeny G, Godo M, Mozes M, Rosivall L, Gross ML, Ritz E, Hamar P. Increased renoprotection with ACE inhibitor plus aldosterone antagonist as compared to monotherapies-the effect on podocytes. Nephrol Dial Transplant 24: 3640-3651, 2009.
31. Peired A, Lazzeri E, Lasagni L, Romagnani P. Glomerular regeneration: when can the kidney regenerate from injury and what turns failure into success? Nephron Exp Nephrol 126: 70, 2014.
32. Pichaiwong W, Hudkins KL, Wietecha T, Nguyen TQ, Tachaudomdach C, Li W, Askari B, Kobayashi T, O’Brien KD, Pippin JW, Shankland SJ, Alpers CE. Reversibility of structural and functional damage in a model of advanced diabetic nephropathy. J Am Soc Nephrol 24: 1088-1102, 2013.
33. Pippin JW, Glenn ST, Krofft RD, Rusiniak ME, Alpers CE, Hudkins K, Duffield JS, Gross KW, Shankland SJ. Cells of renin lineage take on a podocyte phenotype in aging nephropathy. Am J Physiol Renal Physiol 306: F1198-F1209, 2014.
34. Pippin JW, Kaverina NV, Eng DG, Krofft RD, Glenn ST, Duffield JS, Gross KW, Shankland SJ. Cells of renin lineage are adult pluri-potent progenitors in experimental glomerular disease. Am J Physiol Renal Physiol 309: F341-F358, 2015.
35. Pippin JW, Sparks MA, Glenn ST, Buitrago S, Coffman TM, Duffield JS, Gross KW, Shankland SJ. Cells of renin lineage are progenitors of podocytes and parietal epithelial cells in experimental glomerular disease. Am J Pathol 183: 542-557, 2013.
36. Puelles VG, van der Wolde JW, Schulze KE, Short KM, Wong MN, Bensley JG, Cullen-McEwen LA, Caruana G, Hokke SN, Li J, Firth SD, Harper IS, Nikolic-Paterson DJ, Bertram JF. Validation of a three-dimensional method for counting and sizing podocytes in whole glomeruli. J Am Soc Nephrol [Epub ahead of print].
37. Roeder SS, Stefanska A, Eng DG, Kaverina N, Sunseri MW, McNicholas BA, Rabinovitch P, Engel FB, Daniel C, Amann K, Lichtnekert J, Pippin JW, Shankland SJ. Changes in glomerular parietal epithelial cells in mouse kidneys with advanced age. Am J Physiol Renal Physiol 309: F164-F178, 2015.
38. Romagnani P, Rinkevich Y, Dekel B. The use of lineage tracing to study kidney injury and regeneration. Nat Rev Nephrol 11: 420-431, 2015.
39. Ronconi E, Sagrinati C, Angelotti ML, Lazzeri E, Mazzinghi B, Ballerini L, Parente E, Becherucci F, Gacci M, Carini M, Maggi E, Serio M, Vannelli GB, Lasagni L, Romagnani S, Romagnani P. Regeneration of glomerular podocytes by human renal progenitors. JAm Soc Nephrol 20: 322-332, 2009.
40. Sagrinati C, Netti GS, Mazzinghi B, Lazzeri E, Liotta F, Frosali F, Ronconi E, Meini C, Gacci M, Squecco R, Carini M, Gesualdo L, Francini F, Maggi E, Annunziato F, Lasagni L, Serio M, Romagnani S, Romagnani P. Isolation and characterization of multipotent progenitor cells from the Bowman’s capsule of adult human kidneys. JAmSoc Nephrol 17: 2443-2456, 2006.
41. Sakamoto K, Ueno T, Kobayashi N, Hara S, Takashima Y, Pastan I, Matsusaka T, Nagata M. The direction and role of phenotypic transition between podocytes and parietal epithelial cells in focal segmental glomerulosclerosis. Am J Physiol Renal Physiol 306: F98-F104, 2014.
42. Schulte K, Berger K, Boor P, Jirak P, Gelman IH, Arkill KP, Neal CR, Kriz W, Floege J, Smeets B, Moeller MJ. Origin of parietal podocytes in atubular glomeruli mapped by lineage tracing. JAmSoc Nephrol 25: 129-141, 2014.
43. Schwartzman M, Reginensi A, Wong JS, Basgen JM, Meliambro K, Nicholas SB, D’Agati V, McNeill H, Campbell KN. Podocyte-specific deletion of Yes-associated protein causes FSGS and progressive renal failure. J Am Soc Nephrol 27: 216-226, 2016.
44. Shankland SJ. The podocyte’s response to injury: role in proteinuria and glomerulosclerosis. Kidney Int 69: 2131-2147, 2006.
45. Shankland SJ, Smeets B, Pippin JW, Moeller MJ. The emergence of the glomerular parietal epithelial cell. Nat Rev Nephrol 10: 158-173, 2014.
46. Shigehara T, Zaragoza C, Kitiyakara C, Takahashi H, Lu H, Moeller M, Holzman LB, Kopp JB. Inducible podocyte-specific gene expression in transgenic mice. J Am Soc Nephrol 14: 1998-2003, 2003.
47. Taniguchi Y, Pippin JW, Hagmann H, Krofft RD, Chang AM, Zhang J, Terada Y, Brinkkoetter P, Shankland SJ. Both cyclin I and p35 are required for maximal survival benefit of cyclin-dependent kinase 5 in kidney podocytes. Am J Physiol Renal Physiol 302: F1161-F1171, 2012.
48. Tao J, Polumbo C, Reidy K, Sweetwyne M, Susztak K. A multicolor podocyte reporter highlights heterogeneous podocyte changes in focal segmental glomerulosclerosis. Kidney Int 85: 972-980, 2014.
49. Tuncdemir M, Ozturk M. The effects of angiotensin-II receptor blockers on podocyte damage and glomerular apoptosis in a rat model of experimental streptozotocin-induced diabetic nephropathy. Acta Histochem 113: 826-832, 2011.
50. Venkatareddy M, Wang S, Yang Y, Patel S, Wickman L, Nishizono R, Chowdhury M, Hodgin J, Wiggins PA, Wiggins RC. Estimating podocyte number and density using a single histologic section. JAmSoc Nephrol 25: 1118-1129, 2014.
51. Wanner N, Hartleben B, Herbach N, Goedel M, Stickel N, Zeiser R, Walz G, Moeller MJ, Grahammer F, Huber TB. Unraveling the role of podocyte turnover in glomerular aging and injury. J Am Soc Nephrol 25: 707-716, 2014.
52. Wharram BL, Goyal M, Wiggins JE, Sanden SK, Hussain S, Filipiak WE, Saunders TL, Dysko RC, Kohno K, Holzman LB, Wiggins RC. Podocyte depletion causes glomerulosclerosis: diphtheria toxin-induced podocyte depletion in rats expressing human diphtheria toxin receptor transgene. J Am Soc Nephrol 16: 2941-2952, 2005.
53. Wu DT, Bitzer M, Ju W, Mundel P, Bottinger EP. TGF-beta concentration specifies differential signaling profiles of growth arrest/differentiation and apoptosis in podocytes. J Am Soc Nephrol 16: 3211-3221, 2005.
54. Yang S, Liu L, Xu P, Yang Z. MKL1 inhibits cell cycle progression through p21 in podocytes. BMC Mol Biol 16: 1, 2015.
55. Zhang J, Pippin JW, Krofft RD, Naito S, Liu ZH, Shankland SJ. Podocyte repopulation by renal progenitor cells following glucocorticoids treatment in experimental FSGS. Am J Physiol Renal Physiol 304: F1375-F1389, 2013.
56. Zhang J, Pippin JW, Vaughan MR, Krofft RD, Taniguchi Y, Romagnani P, Nelson PJ, Liu ZH, Shankland SJ. Retinoids augment the expression of podocyte proteins by glomerular parietal epithelial cells in experimental glomerular disease. Nephron Exp Nephrol 121: e23-e37, 2012.
57. Zhang J, Yanez D, Floege A, Lichtnekert J, Krofft RD, Liu ZH, Pippin JW, Shankland SJ. ACE-inhibition increases podocyte number in experimental glomerular disease independent of proliferation. J Renin Angiotensin Aldosterone Syst 16: 234-248, 2015.
58. Ziyadeh FN, Wolf G. Pathogenesis of the podocytopathy and proteinuria in diabetic glomerulopathy. Curr Diabetes Rev 4: 39-45, 2008.