Renal stem cells: Fact or science fiction?

Biochemical Journal

Volumn 444, Issue 2, 2012, Pages 153-168

  Mccampbell, Kristen K ^a   Wingert, Rebecca A ^a  

^a UNIVERSITY OF NOTRE DAME   (United States)

Author keywords

Kidney; Kidney development; Kidney disease; Neonephrogenesis; Regeneration; Repair; Stem cell

Indexed keywords

BONE MORPHOGENETIC PROTEIN; BROXURIDINE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; GREEN FLUORESCENT PROTEIN; HOMEODOMAIN PROTEIN; HOX PROTEIN; HOX11 PROTEIN; OSR1 PROTEIN; SINE OCULIS RELATED HOMEOBOX 2 PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR PAX2; UNCLASSIFIED DRUG;

BIOMETRY; CELL AGING; CELL DIFFERENTIATION; CELL DIVISION; CELL FATE; CELL GROWTH; CELL INTERACTION; CELL PROLIFERATION; CELL REGENERATION; CELL RENEWAL; CELL TYPE; FLOW CYTOMETRY; GLOMERULUS; GLOMERULUS BASEMENT MEMBRANE; HEMATOPOIETIC STEM CELL; HUMAN; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; KIDNEY; KIDNEY CELL; KIDNEY DEVELOPMENT; KIDNEY DISEASE; KIDNEY FUNCTION; KIDNEY STEM CELL; KIDNEY TUBULE CELL; MULTIPOTENT STEM CELL; NEPHRON; NONHUMAN; ONTOGENY; PODOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REGENERATIVE MEDICINE; REVIEW; SIGNAL TRANSDUCTION; STEM CELL;

ANIMALS; HUMANS; KIDNEY; KIDNEY DISEASES; KIDNEY TRANSPLANTATION; REGENERATION; STEM CELLS;

EID: 84860875507     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20120176     Document Type: Review

References (154)

1. Levey, A. S., Atkins, R., Coresh, J., Cohen, E. P., Collins, A. J., Eckardt, K. U., Nahas, M. E., Jaber, B. L., Jadoul, M., Levin, A. et al. (2007) Chronic kidney disease as a global public health problem: approaches and initiatives - a position statement from Kidney Disease Improving Global Outcomes. Kidney Int. 72, 247-259 (Pubitemid 47172384)
2. Meguid El Nahas, A. and Bello, A. K. (2005) Chronic kidney disease: the global challenge. Lancet 365, 331-340
3. Little, M. H. (2006) Regrow or repair: potential regenerative therapies for the kidney. J. Am. Soc. Nephrol. 17, 2390-2401
4. Potter, E. L. and Thierstein, S. T. (1943) Glomerular development in the kidney as an index of fetal maturity. J. Pediatr. 22, 695-706
5. Hartman, H. A., Lai, H. L. and Patterson, L. T. (2007) Cessation of renal morphogenesis in mice. Dev. Biol. 310, 379-387 (Pubitemid 47496040)
6. Messier, B. and Leblond, C. P. (1960) Cell proliferation and migration as revealed by radioautography after injection of thymidine-H3 into male rats and mice. Am. J. Anat. 106, 247-285
7. Romagnani, P. (2011) Family portrait: renal progenitor of Bowman's capsule and its tubular brothers. Am. J. Pathol. 178, 490-493
8. Toback, F. G. (1992) Regeneration after acute tubular necrosis. Kidney Int. 41, 226-246
9. Thadhani, R., Pascual, M. and Bonventre, J. V. (1996) Acute renal failure. N. Engl. J. Med. 334, 1448-1460 (Pubitemid 126590563)
10. Bonventre, J. V. (2003) Dedifferentiation and proliferation of surviving epithelial cells in acute renal failure. J. Am. Soc. Nephrol. 14, S55-S61
11. Romagnani, P. and Kalluri, R. (2009) Possible mechanisms of kidney repair. Fibrog. Tissue Repair 2, 3
12. Chhabra, P. and Brayman, K. L. (2009) The use of stem cells in kidney disease. Curr. Opin. Organ Transplant. 14, 72-78
13. Guo, J. K. and Cantley, L. G. (2010) Cellular maintenance and repair of the kidney. Annu. Rev. Physiol. 72, 357-376
14. Hopkins, C., Li, J., Rae, F. and Little, M. H. (2009) Stem cell options for kidney disease. J. Pathol. 217, 265-281
15. Little, M. H. and Bertram, J. F. (2009) Is there such a thing as a renal stem cell? J. Am. Soc. Nephrol. 20, 2112-2117
16. Pleniceanu, O., Harari-Steinberg, O. and Dekel, B. (2010) Concise review: kidney stem/progenitor cells: differentiate, sort out, or reprogram? Stem Cells 28, 1649-1660
17. Sagrinati, C., Ronconi, E., Lazzeri, E., Lasagni, L. and Romagnani, P. (2008) Stem-cell approaches for kidney repair: choosing the right cells. Trends Mol. Med. 14, 277-285
18. Zubko, R. and Frishman, W. (2009) Stem cell therapy for the kidney? Am. J. Ther. 16, 247-256
19. Benigni, A., Morigi, M. and Remuzzi, G. (2010) Kidney regeneration. Lancet 375, 1310-1317
20. Davidson, A. J. (2011) Uncharted waters: nephrogenesis and renal regeneration in fish and mammals. Pediatr. Nephrol. 26, 1435-1443
21. Reilly, R. F., Bulger, R. E. and Kriz, W. (2007) Structural-functional relationships in the kidney. In Diseases of the Kidney and Urinary Tract (Schrier, R. W., ed.), pp. 2-53, Lippincott Williams & Wilkins, Philadelphia, PA
22. Khairallah, W., Merheb, M., Chaiban, J. and Badr, K. F. (2007) Hormones and the kidney. In Diseases of the Kidney and Urinary Tract (Schrier, R. W., ed.), pp. 234-284, Lippincott Williams & Wilkins, Philadelphia, PA
23. Hallgrimsson, B., Benediktsson, H. and Vize, P. D. (2003) Anatomy and histology of the human urinary system. In The Kidney, From Normal Development to Congenital Disease (Vize, P. D., Woolf, A. S. and Bard, J.B.L., eds), pp. 149-164, Academic Press, London
24. Hoy, W. E., Douglas-Denton, R. N., Hughson, M. D., Cass, A., Johnson, K. and Bertram, J. F. (2003) A stereological study of glomerular number and volume: preliminary findings in a multiracial study of kidneys at autopsy. Kidney Int. Suppl. 83, S31-S37 (Pubitemid 36126840)
25. Hughson, M., Farris, III, A. B., Douglas-Denton, R., Hoy, W. E. and Bertram, J. F. (2003) Glomerular number and size in autopsy kidneys: the relationship to birth weight. Kidney Int. 63, 2113-2122 (Pubitemid 36605822)
26. Nyengaard, J. R. and Bendtsen, T. F. (1992) Glomerular number and size in relation to age, kidney weight, and body surface in normal man. Anat. Rec. 232, 194-201
27. Wingert, R. A. and Davidson, A. J. (2008) The zebrafish pronephros: a model to study nephron segmentation. Kidney Int. 73, 1120-1127 (Pubitemid 351620435)
28. Arendshorst, W. J. and Navar, L. G. (2007) Renal circulation and glomerular hemodynamics. In Diseases of the Kidney and Urinary Tract (Schrier, R. W., ed.), pp. 54-95, Lippincott Williams & Wilkins, Philadelphia, PA
29. Schedl, A. (2007) Renal abnormalities and their developmental origin. Nat. Rev. Genet. 8, 791-802
30. Kerecuk, L., Schreuder, M. F. and Woolf, A. S. (2008) Renal tract malformations: perspectives for nephrologists. Nat. Clin. Pract. Nephrol. 4, 312-325 (Pubitemid 351769332)
31. Song, R. and Yosypiv, I. V. (2011) Genetics of congenital anomalies of the kidney and urinary tract. Pediatr. Nephrol. 26, 353-364
32. Woolf, A. S. (2000) A molecular and genetic view of human renal and urinary tract malformations. Kidney Int. 58, 500-512
33. Renkema, K. Y., Winyard, P. J., Skovorodkin, I. N., Levtchenko, E., Hindryckx, A., Jeanpierre, C., Weber, S., Salomon, R., Antignac, C., Vainio, S. et al. (2011) Novel perspectives for investigating congenital anomalies of the kidney and urinary tract (CAKUT). Nephrol. Dial. Transplant. 26, 3843-3851
34. Cain, J. E., Di Giovanni, V., Smeeton, J. and Rosenblum, N. D. (2010) Genetics of renal hypoplasia: insights into the mechanisms controlling nephron endowment. Pediatr. Res. 68, 91-98
35. Wiggins, R. C. (2007) The spectrum of podocytopathies: a unifying view of glomerular diseases. Kidney Int. 71, 1205-1214
36. Murugan, R. and Kellum, J. A. (2011) Acute kidney injury: what's the prognosis? Nat. Rev. Nephrol. 7, 209-217
37. Ricci, Z., Cruz, D. N. and Ronco, C. (2011) Classification and staging of acute kidney injury: beyond the RIFLE and AKIN criteria. Nat. Rev. Nephrol. 7, 201-208
38. Liu, Y. (2011) Cellular and molecular mechanisms of renal fibrosis. Nat. Rev. Nephrol. 7, 684-696
39. Teo, A. K. and Vallier, L. (2010) Emerging use of stem cells in regenerative medicine. Biochem. J. 428, 11-23
40. Hipp, J. and Atala, A. (2008) Sources of stem cells for regenerative medicine. Stem Cell Rev. 4, 3-11
41. Jaenisch, R. and Young, R. (2008) Stem cells, the molecular circuitry of pluripotency and nuclear reprogramming. Cell 132, 567-582 (Pubitemid 351253686)
42. Hanna, J. H., Saha, K. and Jaenisch, R. (2010) Pluripotency and cellular reprogramming: facts, hypotheses, unresolved issues. Cell 143, 508-525
43. Morrison, S. J. and Spradling, A. C. (2008) Stem cells and niches: mechanisms that promote stem cell maintenance throughout life. Cell 132, 598-611 (Pubitemid 351253690)
44. Simons, B. D. and Clevers, H. (2011) Strategies for homeostatic stem cell self-renewal in adult tissues. Cell 145, 851-862
45. Trumpp, A., Essers, M. and Wilson, A. (2010) Awakening dormant haematopoietic stem cells. Nat. Rev. Immunol. 10, 201-209
46. Eckfeldt, C. E., Mendenhall, E. M. and Verfaillie, C. M. (2005) The molecular repertoire of the 'almighty' stem cell. Nat. Rev. Mol. Cell Biol. 6, 726-737 (Pubitemid 41742796)
47. Mikkers, H. and Frisen, J. (2005) Deconstructing stemness. EMBO J. 24, 2715-2719 (Pubitemid 41170021)
48. Graf, T. and Stadtfeld, M. (2008) Heterogeneity of embryonic and adult stem cells. Cell Stem Cell 3, 480-483
49. Al-Awqati, Q. and Oliver, J. A. (2002) Stem cells in the kidney. Kidney Int. 61, 387-395 (Pubitemid 34102578)
50. He, S., Nakada, D. and Morrison, S. J. (2009) Mechanisms of stem cell self-renewal. Annu. Rev. Cell Dev. Biol. 25, 377-406
51. Bloushtain-Qimron, N., Yao, J., Shipitsin, M., Maruyama, R. and Polyak, K. (2009) Epigenetic patterns of embryonic and adult stem cells. Cell Cycle 8, 809-817
52. Challen, G. A. and Little, M. H. (2006) A side order of stem cells: the SP phenotype. Stem Cells 24, 3-12
53. Orford, K. W. and Scadden, D. S. (2008) Deconstructing stem cell self-renewal: genetic insights into cell-cycle regulation. Nat. Rev. Genet. 9, 115-128
54. Orkin, S. H. and Zon, L. I. (2008) Hematopoiesis: an evolving paradigm for stem cell biology. Cell 132, 631-644 (Pubitemid 351260057)
55. Lee, Z., Dennis, J. E. and Gerson, S. L. (2008) Imaging stem cell implant for cellular-based therapies. Exp. Biol. Med. 233, 930-940
56. Duffield, J. S. and Humphreys, B. D. (2011) Origin of new cells in the adult kidney: results from genetic labeling techniques. Kidney Int. 79, 494-501
57. Dressler, G. R. (2006) The cellular basis of kidney development. Annu. Rev. Cell Dev. Biol. 22, 509-529
58. Dressler, G. R. (2009) Advances in early kidney specification, development, and patterning. Development 136, 3863-3874
59. Costantini, F. and Kopan, R. (2010) Patterning a complex organ: branching morphogenesis and nephron segmentation in kidney development. Dev. Cell 18, 698-712
60. Hendry, C., Rumballe, B., Moritz, K. and Little, M. H. (2010) Defining and redefining the nephron progenitor population. Pediatr. Nephrol. 26, 1395-1406
61. Saxen, L. and Sariola, H. (1987) Early organogenesis of the kidney. Pediatr. Nephrol. 1, 385-392 (Pubitemid 18016633)
62. Auerbach, R. and Grobstein, C. (1958) Inductive interaction of embryonic tissues after dissociation and reaggregation. Exp. Cell Res. 15, 384-397
63. Herzlinger, D., Koseki, C., Mikawa, T. and Al-Awqati, Q. (1992) Metanephric mesenchyme contains multipotent stem cells whose fate is restricted after induction. Development 114, 565-572
64. Qiao, J., Cohen, D. and Herzlinger, D. (1995) The metanephric blastema differentiates into collecting system and nephron epithelia in vitro. Development 121, 3207-3214
65. Mugford, J. W., Sipila, P., McMahon, J. A. and McMahon, A. P. (2008) Osr1 expression demarcates a multi-potent population of intermediate mesoderm that undergoes progressive restriction to an Osr1-dependent nephron progenitor compartment within the mammalian kidney. Dev. Biol. 324, 88-98
66. Mugford, J. W., Yu, J., Kobayashi, A. and McMahon, A. P. (2009) High-resolution gene expression analysis of the developing mouse kidney defines novel cellular compartments within the nephron progenitor population. Dev. Biol. 333, 312-323
67. Oliver, G., Wehr, R., Jenkins, N. A., Copeland, N. G., Cheyette, B. N. R., Hartenstein, V., Zipursky, S. L. and Gruss, P. (1995) Homeobox genes and connective tissue patterning. Development 121, 693-705
68. Self, M., Lagutin, O. V., Bowling, B., Hendrix, J., Cai, Y., Dressler, G. R. and Oliver, G. (2006) Six2 is required for suppression of nephrogenesis and progenitor renewal in the developing kidney. EMBO J. 25, 5214-5228 (Pubitemid 44658538)
69. Georgas, K., Rumballe, B., Valerius, M. T., Chiu, H. S., Thiagarajan, R. D., Lesieur, E., Aronow, B. J., Brunskill, E. W., Combes, A. N., Tang, D. et al. (2009) Analysis of early nephron patterning reveals a role for distal RV proliferation in fusion to the ureteric tip via a cap mesenchyme-derived connecting segment. Dev. Biol. 332, 273-286
70. Rumballe, B. A., Georgas, K. M., Combes, A. N., Ju, A. L., Gilbert, T. and Little, M. H. (2011) Nephron formation adopts a novel spatial topology at cessation of nephrogenesis. Dev. Biol. 360, 110-122
71. Thiagarajan, R. D., Georgas, K. M., Rumballe, B. A., Lesieur, E., Chiu, H. S., Taylor, D., Tang, D.T.P., Grimmond, S. M. and Little, M. H. (2011) Identification of anchor genes during kidney development defines ontological relationships, molecular subcompartments and regulatory pathways. PLoS ONE 6, e17286
72. Hatini, V., Huh, S. O., Herzlinger, D., Soares, V. C. and Lai, E. (1996) Essential role of stromal mesenchyme in kidney morphogenesis revealed by targeted disruption of Winged Helix transcription factor BF-2. Genes Dev. 10, 1467-1478 (Pubitemid 26260704)
73. Levinson, R. S., Batourina, E., Choi, C., Vorontchikhina, M., Kitajewski, J. and Mendelsohn, C. L. (2005) Foxd1-dependent signals control cellularity in the renal capsule, a structure required for normal renal development. Development 132, 529-539 (Pubitemid 40277693)
74. Boyle, S., Misfeldt, A., Chandler, K. J., Deal, K. K., Southard-Smith, E. M., Mortlock, D. P., Baldwin, H. S. and de Caestecker, M. (2008) Fate mapping using Cited1-CreERT2 mice demonstrates that the cap mesenchyme contains self-renewing progenitor cells and gives rise exclusively to nephronic epithelia. Dev. Biol. 313, 234-245 (Pubitemid 350298313)
75. Kobayashi, A., Valerius, M. T., Mugford, J. W., Carroll, T. J., Self, M., Oliver, G. and McMahon, A. P. (2008) Six2 defines and regulates a multipotent self-renewing nephron progenitor population throughout mammalian kidney development. Cell Stem Cell 3, 169-181
76. Di Giovanni, V., Alday, A., Chi, L., Mishina, Y. and Rosenblum, N. D. (2011) Alk3 controls nephron number and androgen production via lineage-specific effects in intermediate mesoderm. Development 138, 2717-2727
77. Mugford, J. W., Sipila, P., Kobayashi, A., Behringer, R. R. and McMahon, A. P. (2008) Hoxd11 specifies a program of metanephric kidney development within the intermediate mesoderm of the mouse embryo. Dev. Biol. 319, 396-405
78. Dressler, G. R., Deutsch, U., Chowdhury, K., Nornes, H. O. and Gruss, P. (1990) Pax2, a new murine paired-box-containing gene and its expression in the developing excretory system. Development 109, 787-795
79. Karner, C. M., Das, A., Ma, Z., Self, M., Chen, C., Lum, L., Oliver, G. and Carroll, T. J. (2011) Canonical Wnt9b signaling balances progenitor cell expansion and differentiation during kidney development. Development 138, 1247-1257
80. Vaughan, M. R. and Quaggin, S. E. (2008) How do mesangial and endothelial cells form the glomerular tuft? J. Am. Soc. Nephrol. 19, 24-33
81. Quaggin, S. E. and Kreidberg, J. A. (2008) Development of the renal glomerulus: good neighbors and good fences. Development 135, 609-620 (Pubitemid 351405014)
82. Shankland, S. J. (2006) The podocyte's response to injury: role in proteinuria and glomerulosclerosis. Kidney Int. 69, 2131-2147
83. He, J. C., Husain, M., Sunamoto, M., D'Agati, V. D., Klotman, M. E., Iyengar, R. and Klotman, P. E. (2004) Nef stimulates proliferation of glomerular podocytes through activation of Src-dependent Stat3 and MAPK1,2 pathways. J. Clin. Invest. 114, 643-651 (Pubitemid 39578754)
84. Moeller, M. J., Soofi, A., Hartmann, I., Le Hir, M., Wiggins, R., Kriz, W. and Holzman, L. B. (2004) Podocytes populate cellular crescents in a murine model of inflammatory glomerulonephritis. J. Am. Soc. Nephrol. 15, 61-67 (Pubitemid 38020698)
85. Vogelmann, S. U., Nelson, W. J., Myers, B. D. and Lemley, K. V. (2003) Urinary excretion of viable podocytes in health and renal disease. Am. J. Physiol. Renal Physiol. 285, F40-F48 (Pubitemid 36818460)
86. Bhathena, D. B. (2003) Glomerular basement membrane length to podocyte ratio in human nephronopenia: implications for focal segmental glomerulosclerosis. Am. J. Kidney Dis. 41, 1179-1188
87. Gross, M. L., Ritz, E., Schoof, A., Adamczak, M., Koch, A., Tulp, O., Parkman, A., El-Shakmak, A., Szabo, A. and Amann, K. (2004) Comparison of renal morphology in the Streptozotocin and the SHR/N-cp models of diabetes. Lab. Invest. 84, 452-464 (Pubitemid 41656473)
88. Gross, M. L., Heiss, N., Weckbach, M., Hansen, A., El-Shakmak, A., Szabo, A., Munter, K., Ritz, E. and Amann, K. (2004) ACE-inhibition is superior to endothelin A receptor blockade in preventing abnormal capillary supply and fibrosis of the heart in experimental diabetes. Diabetologia 47, 316-324 (Pubitemid 38315369)
89. Xu, Z. G., Yoo, T. H., Ryu, D. R., Cheon Park, H., Ha, S. K., Han, D. S., Adler, S. G., Natarajan, R. and Kang, S. W. (2005) Angiotensin II receptor blocker inhibits p27Kip1 expression in glucose-stimulated podocytes and in diabetic glomeruli. Kidney Int. 67, 944-952 (Pubitemid 41623318)
90. Petermann, A. T., Pippin, J., Durvasula, R., Pichler, R., Hiromura, K., Monkawa, T., Couser, W. G. and Shankland, S. J. (2005) Mechanical stretch induces podocyte hypertrophy in vitro. Kidney Int. 67, 157-166 (Pubitemid 40019237)
91. Fioretto, P., Steffes, M. W., Sutherland, D. E., Goetz, F. C. and Mauer, M. (1998) Reversal of lesions of diabetic nephropathy after pancreas transplantation. N. Engl. J. Med. 339, 69-75 (Pubitemid 28304880)
92. Ruggenenti, P., Perna, A, Benini, R., Bertani, T., Zoccali, C., Maggiore, Q., Salvadori, M. and Remuzzi, G. (1999) In chronic nephropathies prolonged ACE inhibition can induce remission: dynamics of time-dependent changes in GFR. J. Am. Soc. Nephrol. 10, 997-1006 (Pubitemid 29203086)
93. Remuzzi, G., Benigni, A. and Remuzzi, A. (2006) Mechanisms of progression and regression of renal lesions of chronic nephropathies and diabetes. J. Clin. Invest. 116, 288-296 (Pubitemid 43228342)
94. Macconi, D., Sangalli, F., Bonomelli, M., Conti, S., Condorelli, L., Gagliardini, E., Remuzzi, G. and Remuzzi, A. (2009) Podocyte repopulation contributes to regression of glomerular injury induced by ACE inhibition. Am. J. Pathol. 174, 797-807
95. Lasagni, L. and Romagnani, P. (2010) Glomerular epithelial stem cells: the good, the bad, and the ugly. J. Am. Soc. Nephrol. 21, 1612-1619
96. Sagrinati, C., Netti, G. S., Mazzinghi, B., Lazzeri, E., Liotta, F., Frosali, F., Ronconi, E., Meini, C., Gacci, M., Squecco, R. et al. (2006) Isolation and characterization of multipotent progenitor cells from the Bowman's capsule of adult human kidneys. J. Am. Soc. Nephrol. 17, 2443-2456 (Pubitemid 44300960)
97. Lazzeri, E., Crescioli, C., Ronconi, E., Mazzinghi, B., Sagrinati, C., Netti, G. S., Angelotti, M. L., Parente, E., Ballerini, L., Cosmi, L. et al. (2007) Regenerative potential of embryonic renal multipotent progenitors in acute renal failure. J. Am. Soc. Nephrol. 18, 3128-3138 (Pubitemid 350223972)
98. Gibson, I. W., Downie, I., Downie, T. T., Han, S. W., More, I.A.R. and Lindop, G.B.M. (1992) The parietal podocyte: a study of the vascular pole of the human glomerulus. Kidney Int. 41, 211-214
99. Bariety, J., Mandet, C., Hill, G. S. and Bruneval, P. (2006) Parietal podocytes in normal human glomeruli. J. Am. Soc. Nephrol. 17, 2770-2780 (Pubitemid 44484667)
100. Ryan, G. B., Coghlan, J. P. and Scoggins, B. A. (1979) The granulated peripolar epithelial cell: a potential secretory component of the renal juxtaglomerular complex. Nature 277, 655-656 (Pubitemid 9114283)
101. Kelly, G., Downie, I., Gardiner, D. S., More, I.A.R. and Lindop, G.B.M. (1990) The peripolar cell: a distinctive cell type in the mammalian glomerulus. Morphological evidence from a study of sheep. J. Anat. 168, 217-227 (Pubitemid 20053162)
102. Poulsom, R. and Little, M. H. (2009) Parietal epithelial cells regenerate podocytes. J. Am. Soc. Nephrol. 20, 231-233
103. Ronconi, E., Sagrinati, C., Angelotti, M. L., Lazzeri, E., Mazzinghi, B., Ballerini, L., Parente, E., Becherucci, F., Gacci, M., Carini, M. et al. (2009) Regeneration of glomerular podocytes by human renal progenitors. J. Am. Soc. Nephrol. 20, 322-332
104. Appel, D., Kershaw, D. B., Smeets, B., Yuan, G., Fuss, A., Frye, B., Elger, M., Kriz, W., Floege, J. and Moeller, M. J. (2009) Recruitment of podocytes from glomerular parietal epithelial cells. J. Am. Soc. Nephrol. 20, 333-343
105. Gibson, I. W., Downie, T. T., More, I.A.R. and Lindop, G.B.M. (1998) Tuft-to-capsule adhesions and their precursors: differences between the vascular and tubular poles of the human glomerulus. J. Pathol. 184, 430-435 (Pubitemid 28179904)
106. Grouls, S., Iglesias, D. M., Wentzensen, N., Moeller, M. J., Bouchard, M., Kemler, R., Goodyer, P., Niggli, F., Grone, H. J., Kriz, W. and Koesters, R. (2012) Lineage specification of parietal epithelial cells requires β-catenin/Wnt signaling. J. Am. Soc. Nephrol. 23, 63-72
107. Smeets, B., Angelotti, M. L., Rizzo, P., Dijkman, H., Lazzeri, E., Mooren, F., Ballerini, L., Parente, E., Sagrinati, C., Mazzinghi, B. et al. (2009) Renal progenitor cells contribute to hyperplastic lesions of podocytopathies and crescentic glomerulonephritis. J. Am. Soc. Nephrol. 20, 2593-2603
108. Smeets, B., Uhlig, S., Fuss, A., Mooren, F., Wetzels, J.F. M., Floege, J. and Moeller, M. J. (2009) Tracing the origin of glomerular extracapillary lesions from parietal epithelial cells. J. Am. Soc. Nephrol. 20, 2604-2615
109. Lasagni, L., Ballerini, L., Angelotti, M. L., Parente, E., Sagrinati, C., Mazzinghi, B., Peired, A., Ronconi, E., Becherucci, F., Bani, D. et al. (2010) Notch activation differentially regulates renal progenitors proliferation and differentiation toward the podocyte lineage in glomerular disorders. Stem Cells 28, 1674-1685
110. Benigni, A., Morigi, M., Rizzo, P., Gagliardini, E., Rota, C., Abbate, M., Ghezzi, S., Remuzzi, A. and Remuzzi, G. (2011) Inhibiting angiotensin-converting enzyme promotes renal repair by limiting progenitor cell proliferation and restoring the glomerular architecture. Am. J. Pathol. 179, 628-638
111. Nadasdy, T., Laszik, Z., Blick, K. E., Johnson, L. D. and Silva, F. G. (1994) Proliferative activity of intrinsic cell populations in the normal human kidney. J. Am. Soc. Nephrol. 4, 2032-2039
112. Vogetseder, A., Karadeniz, A., Kaissling, B. and Le Hir, M. (2005) Tubular cell proliferation in the healthy rat kidney. Histochem. Cell Biol. 124, 97-104 (Pubitemid 41429764)
113. Vogetseder, A., Palan, T., Bacic, D., Kaissling, B. and Le Hir, M. (2007) Proximal tubular epithelial cells are generated by division of differentiated cells in the healthy kidney. Am. J. Physiol. Cell Physiol. 292, C807-C813
114. Vogetseder, A., Picard, N., Gaspert, A., Walch, M., Kaissling, B. and Le Hir, M. (2008) Proliferation capacity of the renal proximal tubule involves the bulk of differentiated epithelial cells. Am. J. Physiol. Cell Physiol. 294, C22-C28
115. Oliver, J., MacDowell, M. and Tracy, A. (1951) The pathogenesis of acute renal failure associated with traumatic and toxic injury; renal ischemia, nephrotoxic damage, and the ischemic episode. J. Clin. Invest. 30, 1307-1439
116. Cuppage, F. E. and Tate, A. (1967) Repair of the nephron following injury with mercuric chloride. Am. J. Pathol. 51, 405-429
117. Houghton, D. C., Hartnett, M., Campbell-Boswell, M., Porter, G. and Bennett, W. (1976) A light and electron microscopic analysis of gentamicin nephrotoxicity in rats. Am. J. Pathol. 82, 589-612
118. Venkatachalam, M. A., Bernard, D. B., Donohoe, J. F. and Levinsky, N. G. (1978) Ischemic damage and repair in the rat proximal tubule: differences among the S1, S2, and S3 segments. Kidney Int. 14, 31-49 (Pubitemid 8396236)
119. Ledda-Columbano, G. M., Columbano, A., Coni, P., Curto, M., Faa, G. and Pani, P. (1987) Cell proliferation in rat kidney induced by 1, 2-dibromoethane. Toxicol. Lett. 37, 85-90
120. Grone, H. J., Weber, K., Grone, E., Helmchen, U. and Osborn, M. (1987) Coexpression of keratin and vimentin in damaged and regenerating tubular epithelia of the kidney. Am. J. Pathol. 129, 1-8 (Pubitemid 17157764)
121. Moll, R., Hage, C. and Thoenes, W. (1991) Expression of intermediate filament proteins in fetal and adult human kidney: modulations of intermediate filament patterns during development and in damaged tissue. Lab. Invest. 65, 74-86
122. Witzgall, R., Brown, D., Schwarz, C. and Bonventre, J. V. (1994) Localization of proliferating cell nuclear antigen, vimentin, c-Fos, and clusterin in the postischemic kidney. J. Clin. Invest. 93, 2175-2188
123. Zuk, A., Bonventre, J. V., Brown, D. and Matlin, K. S. (1998) Polarity, integrin, and extracellular matrix dynamics in the postischemic rat kidney. Am. J. Physiol. 275, C711-C731
124. Imgrund, M., Grone, E., Grone, H. J., Kretzler, M., Holzman, L., Schlondorff, D. and Rothenpieler, U. W. (1999) Re-expression of the developmental gene Pax-2 during experimental acute tubular necrosis in mice. Kidney Int. 56, 1423-1431 (Pubitemid 29451249)
125. Abbate, M., Brown, D. and Bonventre, J. V. (1999) Expression of NCAM recapitulates tubulogenic development in kidneys recovering from acute ischemia. Am. J. Physiol. 277, F454-F463 (Pubitemid 29459658)
126. Villanueva, S., Cespedes, C. and Vio, C. P. (2006) Ischemic acute renal failure induces the expression of a wide range of nephrogenic proteins. Am. J. Physiol. Regul. Integr. Comp. Physiol. 290, R861-R870
127. Lin, F., Moran, A. and Igarashi, P. (2005) Intrarenal cells, not bone marrow-derived cells, are the major source for regeneration in postischemic kidney. J. Clin. Invest. 115, 1756-1764 (Pubitemid 40979714)
128. Humphreys, B. D., Valerius, M. T., Kobayashi, A., Mugford, J. W., Soeung, S., Duffield, J. S., McMahon, A. P. and Bonventre, J. V. (2008) Intrinsic epithelial cells repair the kidney after injury. Cell Stem Cell 2, 284-291 (Pubitemid 351298594)
129. Humphreys, B. D., Czerniak, S., DiRocco, D. P., Hasnain, W., Cheema, R. and Bonventre, J. V. (2011) Repair of injured proximal tubule does not involve specialized progenitors. Proc. Natl. Acad. Sci. U.S.A. 108, 9226-9231
130. Maeshima, A., Yamashita, S. and Nojima, Y. (2003) Identification of renal progenitor-like tubular cells that participate in the regeneration processes of the kidney. J. Am. Soc. Nephrol. 14, 3138-3146 (Pubitemid 37509291)
131. Maeshima, A., Sakurai, H. and Nigam, S. K. (2006) Adult kidney tubular cell population showing phenotypic plasticity, tubulogenic capacity, and integration capability into developing kidney. J. Am. Soc. Nephrol. 17, 188-198
132. Oliver, J. A., Maarouf, O., Cheema, F. H., Martens, T. P. and Al-Awqati, Q. (2004) The renal papilla is a niche for adult kidney stem cells. J. Clin. Invest. 114, 795-804 (Pubitemid 39578738)
133. Kitamura, S., Yamasaki, Y., Kinomura, M., Sugaya, T., Sugiyama, H., Maeshima, Y. and Makino, H. (2005) Establishment and characterization of renal progenitor like cells from S3 segment of nephron in rat adult kidney. FASEB J. 19, 1789-1797 (Pubitemid 41598763)
134. Langworthy, M., Zhou, B., de Caestecker, M., Moeckel, G. and Baldwin, H. S. (2009) NFATc1 identifies a population of proximal tubule cell progenitors. J. Am. Soc. Nephrol. 20, 311-321
135. Sallustio, F., De Benedictis, L., Castellano, G., Zaza, G., Loverre, A., Costantino, V., Grandaliano, G. and Schena, F. P. (2010) TLR2 plays a role in the activation of human resident renal stem/progenitor cells. FASEB J. 24, 514-525
136. Lindgren, D., Bostrom, A. K., Nilsson, K., Hansson, J., Sjolund, J., Moller, C., Jirstrom, K., Nilsson, E., Landberg, G., Axelson, H. et al. (2011) Isolation and characterization of progenitor-like cells from human renal proximal tubules. Am. J. Pathol. 178, 828-837
137. Ma, I. and Allan, A. L. (2011) The role of human aldehyde dehydrogenase in normal and cancer stem cells. Stem Cell Rev. 7, 292-306
138. Bussolati, B., Bruno, S., Grange, C., Buttiglieri, S., Deregibus, M. C., Cantino, D. and Camussi, G. (2005) Isolation of renal progenitor cells from adult human kidney. Am. J. Pathol. 166, 545-555 (Pubitemid 40189050)
139. Oliver, J. A., Klinakis, A., Cheema, F. H., Friedlander, J., Sampogna, R. V., Martens, T. P., Liu, C., Efstratiadis, A. and Al-Awqati, Q. (2009) Proliferation and migration of label-retaining cells of the kidney papilla. J. Am. Soc. Nephrol. 20, 2315-2327
140. Patschan, D., Michurina, T., Shi, H. K., Dolff, S., Brodsky, S. V., Vasilieva, T., Cohen-Gould, L., Winaver, J., Chander, P. N., Enikolopov, G. and Goligorsky, M. S. (2007) Normal distribution and medullary-to-cortical shift of Nestin-expressing cells in acute renal ischemia. Kidney Int. 71, 744-754 (Pubitemid 46624019)
141. Song, J., Czerniak, S., Wang, T., Ying, W., Carlone, D. L., Breault, D. T. and Humphreys, B. D. (2011) Characterization and fate of telomerase- expressing epithelia during kidney repair. J. Am. Soc. Nephrol. 22, 2256-2265
142. Ward, H. H., Romero, E., Welford, A., Pickett, G., Bacallao, R., Gattone, 2nd, V. H., Ness, S. A., Wandinger-Ness, A. and Roitbak, T. (2011) Adult human CD133/1+ kidney cells isolated from papilla integrate into developing kidney tubules. Biochim. Biophys. Acta 1812, 1344-1357
143. Dekel, B., Zangi, L., Shezen, E., Reich-Zeliger, S., Eventov-Friedman, S., Katchman, H., Jacob-Hirsch, J., Amariglio, N., Rechavi, G., Margalit, R. and Reisner, Y. (2006) Isolation and characterization of non-tubular Sca-1+Lin- multipotent stem/progenitor cells from adult mouse kidney. J. Am. Soc. Nephrol. 17, 3300-3314 (Pubitemid 44865273)
144. Hishikawa, K., Marumo, T., Miura, S., Nakanishi, A., Matsuzaki, Y., Shibata, K., Ichiyanagi, T., Kohike, H., Komori, T., Takahashi, I. et al. (2005) Musculin/MyoR is expressed in kidney side population cells and can regulate their function. J. Cell Biol. 169, 921-928 (Pubitemid 41002868)
145. Challen, G. A., Bertoncello, I., Deane, J. A., Ricardo, S. D. and Little, M. H. (2006) Kidney side population reveals multilineage potential and renal functional capacity but also cellular heterogeneity. J. Am. Soc. Nephrol. 17, 1896-1912 (Pubitemid 44036174)
146. Imai, N., Hishikawa, K., Marumo, T., Hirahashi, J., Inowa, T., Matsuzaki, Y., Okano, H., Kitamura, T., Salant, D. and Fujita, T. (2007) Inhibition of histone deacetylase activates side population cells in kidney and partially reverses chronic renal injury. Stem Cells 25, 2469-2475 (Pubitemid 47582739)
147. Inowa, T., Hishikawa, K., Takeuchi, T., Kitamura, T. and Fujita, T. (2008) Isolation and potential existence of side population cells in adult human kidney. Int. J. Urol. 15, 272-274 (Pubitemid 351316944)
148. Gupta, S., Verfaillie, C., Chmielewski, D., Kren, S., Eidman, K., Connaire, J., Heremans, Y., Lund, T., Blackstad, M., Jiang, Y. et al. (2006) Isolation and characterization of kidney-derived stem cells. J. Am. Soc. Nephrol. 17, 3028-3040 (Pubitemid 44707763)
149. Lee, P. T., Lin, H. H., Jiang, S. T., Lu, P. J., Chou, K. J., Fang, H. C., Chiou, Y. Y. and Tang, M. J. (2010) Mouse kidney progenitor cells accelerate renal regeneration and prolong survival after ischemic injury. Stem Cells 28, 573-584
150. Benigni, A., Morigi, M. and Remuzzi, G. (2010) Kidney regeneration. Lancet 375, 1310-1317
151. Reimschuessel, R. (2001) A fish model of renal regeneration and development. ILAR J. 42, 285-291
152. Elger, M., Hentschel, H., Litteral, J., Wellner, M., Kirsch, T., Luft, F. C. and Haller, H. (2003) Nephrogenesis is induced by partial nephrectomy in the elasmobranch Leucoraja erinacea . J. Am. Soc. Nephrol. 14, 1506-1518 (Pubitemid 36687052)
153. Diep, C. Q., Ma, D., Deo, R. C., Holm, T. M., Naylor, R. W., Arora, N., Wingert, R. A., Bollig, F., Djordjevic, G., Lichman, B. et al. (2011) Identification of adult nephron progenitors capable of kidney regeneration in zebrafish. Nature 470, 95-100
154. Woolf, A. S., Palmer, S. J., Snow, M. L. and Fine, L. G. (1990) Creation of a functioning chimeric mammalian kidney. Kidney Int. 38, 991-997 (Pubitemid 20362875)