Cells of renin lineage are progenitors of podocytes and parietal epithelial cells in experimental glomerular disease

American Journal of Pathology

Volumn 183, Issue 2, 2013, Pages 542-557

  Pippin, Jeffrey W ^a   Sparks, Matthew A ^b   Glenn, Sean T ^c   Buitrago, Sandra ^c   Coffman, Thomas M ^b   Duffield, Jeremy S ^a   Gross, Kenneth W ^c   Shankland, Stuart J ^a  

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

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

^c ROSWELL PARK CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CLAUDIN 1; NEPHRIN; PODOCIN; RENIN; SYNAPTOPODIN; TRANSCRIPTION FACTOR PAX2; TUMOR PROTEIN; UNCLASSIFIED DRUG; WILMS TUMOR PROTEIN 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BOWMAN CAPSULE; CELL LINEAGE; CONTROLLED STUDY; GLOMERULOPATHY; GLOMERULUS CAPILLARY; MOUSE; NONHUMAN; PODOCYTE; PRIORITY JOURNAL; STOMACH PARIETAL CELL;

ANIMALS; CELL LINEAGE; DISEASE MODELS, ANIMAL; EPITHELIAL CELLS; FEMALE; GLOMERULOSCLEROSIS, FOCAL SEGMENTAL; MALE; MICE; MICE, TRANSGENIC; PODOCYTES; RENIN; STEM CELLS;

EID: 84880580891     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2013.04.024     Document Type: Article

References (77)

1. R.N. Foley, and A.J. Collins End-stage renal disease in the United States: an update from the United States Renal Data System J Am Soc Nephrol 18 2007 2644 2648
2. M.E. Pagtalunan, P.L. Miller, S. Jumping-Eagle, R.G. Nelson, B.D. Myers, H.G. Rennke, N.S. Coplon, L. Sun, and T.W. Meyer Podocyte loss and progressive glomerular injury in type II diabetes J Clin Invest 99 1997 342 348
3. T. Nakamura, C. Ushiyama, S. Suzuki, M. Hara, N. Shimada, I. Ebihara, and H. Koide Urinary excretion of podocytes in patients with diabetic nephropathy Nephrol Dial Transplant 15 2000 1379 1383
4. A.T. Petermann, J. Pippin, R. Krofft, M. Blonski, S. Griffin, R. Durvasula, and S.J. Shankland Viable podocytes detach in experimental diabetic nephropathy: potential mechanism underlying glomerulosclerosis Nephron Exp Nephrol 98 2004 e114 e123
5. M.M. Lerco, C.S. Macedo, R.J. Silva, O. Pinheiro Dde, and C.T. Spadella The number of podocyte and slit diaphragm is decreased in experimental diabetic nephropathy Acta Cir Bras 21 2006 87 91
6. A.T. Petermann, R. Krofft, M. Blonski, K. Hiromura, M. Vaughn, R. Pichler, S. Griffin, T. Wada, J. Pippin, R. Durvasula, and S.J. Shankland Podocytes that detach in experimental membranous nephropathy are viable Kidney Int 64 2003 1222 1231
7. R.C. Wiggins The spectrum of podocytopathies: a unifying view of glomerular diseases Kidney Int 71 2007 1205 1214
8. M. Hara, T. Yanagihara, and I. Kihara Urinary podocytes in primary focal segmental glomerulosclerosis Nephron 89 2001 342 347
9. Y.H. Kim, M. Goyal, D. Kurnit, B. Wharram, J. Wiggins, L. Holzman, D. Kershaw, and R. Wiggins Podocyte depletion and glomerulosclerosis have a direct relationship in the PAN-treated rat Kidney Int 60 2001 957 968
10. B.L. Wharram, M. Goyal, J.E. Wiggins, S.K. Sanden, S. Hussain, W.E. Filipiak, T.L. Saunders, R.C. Dysko, K. Kohno, L.B. Holzman, and R.C. Wiggins Podocyte depletion causes glomerulosclerosis: diphtheria toxin-induced podocyte depletion in rats expressing human diphtheria toxin receptor transgene J Am Soc Nephrol 16 2005 2941 2952
11. S.J. Shankland The podocyte's response to injury: role in proteinuria and glomerulosclerosis Kidney Int 69 2006 2131 2147
12. C.J. Kuan, M. al-Douahji, and S.J. Shankland The cyclin kinase inhibitor p21WAF1, CIP1 is increased in experimental diabetic nephropathy: potential role in glomerular hypertrophy J Am Soc Nephrol 9 1998 986 993
13. Y.G. Kim, C.E. Alpers, J. Brugarolas, R.J. Johnson, W.G. Couser, and S.J. Shankland The cyclin kinase inhibitor p21CIP1/WAF1 limits glomerular epithelial cell proliferation in experimental glomerulonephritis Kidney Int 55 1999 2349 2361
14. A.T. Petermann, J. Pippin, K. Hiromura, T. Monkawa, R. Durvasula, W.G. Couser, J. Kopp, and S.J. Shankland Mitotic cell cycle proteins increase in podocytes despite lack of proliferation Kidney Int 63 2003 113 122
15. A. Petermann, K. Hiromura, J. Pippin, M. Blonski, W.G. Couser, J. Kopp, P. Mundel, and S.J. Shankland Differential expression of d-type cyclins in podocytes in vitro and in vivo Am J Pathol 164 2004 1417 1424
16. M. Nagata, K. Nakayama, Y. Terada, S. Hoshi, and T. Watanabe Cell cycle regulation and differentiation in the human podocyte lineage Am J Pathol 153 1998 1511 1520
17. M. Nagata, Y. Yamaguchi, and K. Ito Loss of mitotic activity and the expression of vimentin in glomerular epithelial cells of developing human kidneys Anat Embryol (Berl) 187 1993 275 279
18. K.V. Lemley, R.A. Lafayette, M. Safai, G. Derby, K. Blouch, A. Squarer, and B.D. Myers Podocytopenia and disease severity in IgA nephropathy Kidney Int 61 2002 1475 1485
19. D. Macconi, M. Bonomelli, A. Benigni, T. Plati, F. Sangalli, L. Longaretti, S. Conti, H. Kawachi, P. Hill, G. Remuzzi, and A. Remuzzi Pathophysiologic implications of reduced podocyte number in a rat model of progressive glomerular injury Am J Pathol 168 2006 42 54
20. T. Suzuki, T. Matsusaka, M. Nakayama, T. Asano, T. Watanabe, I. Ichikawa, and M. Nagata Genetic podocyte lineage reveals progressive podocytopenia with parietal cell hyperplasia in a murine model of cellular/collapsing focal segmental glomerulosclerosis [Erratum appeared in Am J Pathol 2009, 175:1349] Am J Pathol 174 2009 1675 1682
21. M. Adamczak, M.L. Gross, J. Krtil, A. Koch, K. Tyralla, K. Amann, and E. Ritz Reversal of glomerulosclerosis after high-dose enalapril treatment in subtotally nephrectomized rats J Am Soc Nephrol 14 2003 2833 2842
22. D. Macconi, F. Sangalli, M. Bonomelli, S. Conti, L. Condorelli, E. Gagliardini, G. Remuzzi, and A. Remuzzi Podocyte repopulation contributes to regression of glomerular injury induced by ACE inhibition Am J Pathol 174 2009 797 807
23. Z. Nemeth, G. Kokeny, M. Godo, M. Mózes, L. Rosivall, M.L. Gross, E. Ritz, and P. Hamar Increased renoprotection with ACE inhibitor plus aldosterone antagonist as compared to monotherapies-the effect on podocytes Nephrol Dial Transplant 24 2009 3640 3651
24. D. Appel, D.B. Kershaw, B. Smeets, G. Yuan, A. Fuss, B. Frye, M. Elger, W. Kriz, J. Floege, and M.J. Moeller Recruitment of podocytes from glomerular parietal epithelial cells J Am Soc Nephrol 20 2009 333 343
25. G. Swetha, V. Chandra, S. Phadnis, and R. Bhonde Glomerular parietal epithelial cells of adult murine kidney undergo EMT to generate cells with traits of renal progenitors J Cell Mol Med 15 2011 396 413
26. R. Poulsom, and M.H. Little Parietal epithelial cells regenerate podocytes J Am Soc Nephrol 20 2009 231 233
27. C. Sagrinati, G.S. Netti, B. Mazzinghi, E. Lazzeri, F. Liotta, F. Frosali, E. Ronconi, C. Meini, M. Gacci, R. Squecco, M. Carini, L. Gesualdo, F. Francini, E. Maggi, F. Annunziato, L. Lasagni, M. Serio, S. Romagnani, and P. Romagnani Isolation and characterization of multipotent progenitor cells from the Bowman's capsule of adult human kidneys J Am Soc Nephrol 17 2006 2443 2456
28. J. Bariety, C. Mandet, G.S. Hill, and P. Bruneval Parietal podocytes in normal human glomeruli J Am Soc Nephrol 17 2006 2770 2780
29. J. Zhang, K.M. Hansen, J.W. Pippin, A.M. Chang, Y. Taniguchi, R.D. Krofft, S.G. Pickering, Z. Liu, C.K. Abrass, and S.J. Shankland De novo expression of podocyte proteins in parietal epithelial cells in experimental aging nephropathy Am J Physiol Renal Physiol 302 2012 F571 F580
30. T. Ohse, M.R. Vaughan, J.B. Kopp, R.D. Krofft, C.B. Marshall, A.M. Chang, K.L. Hudkins, C.E. Alpers, J.W. Pippin, and S.J. Shankland De novo expression of podocyte proteins in parietal epithelial cells during experimental glomerular disease Am J Physiol Renal Physiol 298 2010 F702 F711
31. P. Romagnani Parietal epithelial cells: their role in health and disease Contrib Nephrol 169 2011 23 36
32. L. Lasagni, and P. Romagnani Glomerular epithelial stem cells: the good, the bad, and the ugly J Am Soc Nephrol 21 2010 1612 1619
33. P. Romagnani, and G. Remuzzi Renal progenitors in non-diabetic and diabetic nephropathies Trends Endocrinol Metab 24 2013 13 20
34. M.L.S. Sequeira López, E.S. Pentz, T. Nomasa, O. Smithies, and R.A. Gomez Renin cells are precursors for multiple cell types that switch to the renin phenotype when homeostasis is threatened Dev Cell 6 2004 719 728
35. C. Hugo, S.J. Shankland, D.F. Bowen-Pope, W.G. Couser, and R.J. Johnson Extraglomerular origin of the mesangial cell after injury. A new role of the juxtaglomerular apparatus J Clin Invest 100 1997 786 794
36. L. Barajas Anatomy of the juxtaglomerular apparatus Am J Physiol 237 1979 F333 F343
37. M.R. Celio, and T. Inagami Renin in the human kidney. Immunohistochemical localization Histochemistry 72 1981 1 10
38. T. Faraggiana, E. Gresik, T. Tanaka, T. Inagami, and A. Lupo Immunohistochemical localization of renin in the human kidney J Histochem Cytochem 30 1982 459 465
39. M. Herrera, and T.M. Coffman The kidney and hypertension: novel insights from transgenic models Curr Opin Nephrol Hypertens 21 2012 171 178
40. R. Feil, J. Brocard, B. Mascrez, M. LeMeur, D. Metzger, and P. Chambon Ligand-activated site-specific recombination in mice Proc Natl Acad Sci USA 93 1996 10887 10890
41. T. Sparwasser, S. Gong, J.Y. Li, and G. Eberl General method for the modification of different BAC types and the rapid generation of BAC transgenic mice Genesis 38 2004 39 50
42. S.T. Glenn, C.A. Jones, L. Pan, and K.W. Gross In vivo analysis of key elements within the renin regulatory region Physiol Genomics 35 2008 243 253
43. L. Madisen, T.A. Zwingman, S.M. Sunkin, S.W. Oh, H.A. Zariwala, H. Gu, L.L. Ng, R.D. Palmiter, M.J. Hawrylycz, A.R. Jones, E.S. Lein, and H. Zeng A robust and high-throughput Cre reporting and characterization system for the whole mouse brain Nat Neurosci 13 2010 133 140
44. A. Novak, C. Guo, W. Yang, A. Nagy, and C.G. Lobe Z/EG, a double reporter mouse line that expresses enhanced green fluorescent protein upon Cre-mediated excision Genesis 28 2000 147 155
45. J. Zhang, J.W. Pippin, M.R. Vaughan, R.D. Krofft, Y. Taniguchi, P. Romagnani, P.J. Nelson, Z.H. Liu, and S.J. Shankland Retinoids augment the expression of podocyte proteins by glomerular parietal epithelial cells in experimental glomerular disease Nephron Exp Nephrol 121 2012 e23 e37
46. Y. Taniguchi, J.W. Pippin, H. Hagmann, R.D. Krofft, A.M. Chang, J. Zhang, Y. Terada, P. Brinkkoetter, and S.J. Shankland 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 2012 F1161 F1171
47. V. Ophascharoensuk, J.W. Pippin, K.L. Gordon, S.J. Shankland, W.G. Couser, and R.J. Johnson Role of intrinsic renal cells versus infiltrating cells in glomerular crescent formation Kidney Int 54 1998 416 425
48. M.R. Vaughan, J.W. Pippin, S.V. Griffin, R. Krofft, M. Fleet, L. Haseley, and S.J. Shankland ATRA induces podocyte differentiation and alters nephrin and podocin expression in vitro and in vivo Kidney Int 68 2005 133 144
49. S.V. Griffin, K. Hiromura, J. Pippin, A.T. Petermann, M.J. Blonski, R. Krofft, S. Takahashi, A.B. Kulkarni, and S.J. Shankland Cyclin-dependent kinase 5 is a regulator of podocyte differentiation, proliferation, and morphology Am J Pathol 165 2004 1175 1185
50. S.V. Griffin, R.D. Krofft, J.W. Pippin, and S.J. Shankland Limitation of podocyte proliferation improves renal function in experimental crescentic glomerulonephritis Kidney Int 67 2005 977 986
51. J.A. Jefferson, J.W. Pippin, and S.J. Shankland Experimental models of membranous nephropathy Drug Discov Today Dis Models 7 2010 27 33
52. C.A. Jones, M.I. Hurley, T.A. Black, C.M. Kane, L. Pan, S.C. Pruitt, and K.W. Gross Expression of a renin/GFP transgene in mouse embryonic, extra-embryonic, and adult tissues Physiol Genomics 4 2000 75 81
53. T. Ohse, A.M. Chang, J.W. Pippin, G. Jarad, K.L. Hudkins, C.E. Alpers, J.H. Miner, and S.J. Shankland A new function for parietal epithelial cells: a second glomerular barrier Am J Physiol Renal Physiol 297 2009 F1566 F1574
54. B. Burnworth, J. Pippin, P. Karna, S. Akakura, R. Krofft, G. Zhang, K. Hudkins, C.E. Alpers, K. Smith, S.J. Shankland, I.H. Gelman, and P.J. Nelson SSeCKS sequesters cyclin D1 in glomerular parietal epithelial cells and influences proliferative injury in the glomerulus Lab Invest 92 2012 499 510
55. A.M. Chang, T. Ohse, R.D. Krofft, J.S. Wu, A.A. Eddy, J.W. Pippin, and S.J. Shankland Albumin-induced apoptosis of glomerular parietal epithelial cells is modulated by extracellular signal-regulated kinase 1/2 Nephrol Dial Transplant 27 2012 1330 1343
56. S.V. Griffin, J.P. Olivier, J.W. Pippin, J.M. Roberts, and S.J. Shankland Cyclin I protects podocytes from apoptosis J Biol Chem 281 2006 28048 28057
57. C. Mercure, M.J. Lacombe, K. Khazaie, and T.L. Reudelhuber Cathepsin B is not the processing enzyme for mouse prorenin Am J Physiol Regul Integr Comp Physiol 298 2010 R1212 R1216
58. G. Ryan, V. Steele-Perkins, J.F. Morris, F.J. Rauscher 3rd, and G.R. Dressler Repression of Pax-2 by WT1 during normal kidney development Development 121 1995 867 875
59. Y. Kiuchi-Saishin, S. Gotoh, M. Furuse, A. Takasuga, Y. Tano, and S. Tsukita Differential expression patterns of claudins, tight junction membrane proteins, in mouse nephron segments J Am Soc Nephrol 13 2002 875 886
60. M.A. Ghanem, T.H. Van der Kwast, J.C. Den Hollander, M.K. Sudaryo, M.H. Oomen, M.A. Noordzij, M.M. Van den Heuvel, S.M. Nassef, R.M. Nijman, and G.J. Van Steenbrugge Expression and prognostic value of Wilms' tumor 1 and early growth response 1 proteins in nephroblastoma Clin Cancer Res 6 2000 4265 4271
61. L. Barisoni, W. Kriz, P. Mundel, and V. D'Agati The dysregulated podocyte phenotype: a novel concept in the pathogenesis of collapsing idiopathic focal segmental glomerulosclerosis and HIV-associated nephropathy J Am Soc Nephrol 10 1999 51 61
62. D.H. Tanaka, S. Mikami, T. Nagasawa, J. Miyazaki, K. Nakajima, and F. Murakami CXCR4 is required for proper regional and laminar distribution of cortical somatostatin-, calretinin-, and neuropeptide Y-expressing GABAergic interneurons Cereb Cortex 20 2010 2810 2817
63. S.A. Haley, T. Zhao, L. Zou, J.E. Klysik, J.F. Padbury, and L.K. Kochilas Forced expression of the cell cycle inhibitor p57Kip2 in cardiomyocytes attenuates ischemia-reperfusion injury in the mouse heart BMC Physiol 8 2008 4
64. G. Jarad, J.W. Pippin, S.J. Shankland, J.A. Kreidberg, and J.H. Miner Dystroglycan does not contribute significantly to kidney development or function, in health or after injury Am J Physiol Renal Physiol 300 2011 F811 F820
65. P.T. Brinkkoetter, J.S. Wu, T. Ohse, R.D. Krofft, B. Schermer, T. Benzing, J.W. Pippin, and S.J. Shankland p35, the non-cyclin activator of Cdk5, protects podocytes against apoptosis in vitro and in vivo Kidney Int 77 2010 690 699
66. M.V. Matz, A.F. Fradkov, Y.A. Labas, A.P. Savitsky, A.G. Zaraisky, M.L. Markelov, and S.A. Lukyanov Fluorescent proteins from nonbioluminescent Anthozoa species [Erratum appeared in Nat Biotechnol 1999, 17:1227] Nat Biotechnol 17 1999 969 973
67. P. Romagnani Toward the identification of a "renopoietic system"? Stem Cells 27 2009 2247 2253
68. E. Ronconi, C. Sagrinati, M.L. Angelotti, E. Lazzeri, B. Mazzinghi, L. Ballerini, E. Parente, F. Becherucci, M. Gacci, M. Carini, E. Maggi, M. Serio, G.B. Vannelli, L. Lasagni, S. Romagnani, and P. Romagnani Regeneration of glomerular podocytes by human renal progenitors J Am Soc Nephrol 20 2009 322 332
69. J.R. Fabian, L.J. Field, R.A. McGowan, J.J. Mullins, C.D. Sigmund, and K.W. Gross Allele-specific expression of the murine Ren-1 genes J Biol Chem 264 1989 17589 17594
70. H.S. Kim, N. Maeda, G.T. Oh, L.G. Fernandez, R.A. Gomez, and O. Smithies Homeostasis in mice with genetically decreased angiotensinogen is primarily by an increased number of renin-producing cells J Biol Chem 274 1999 14210 14217
71. D.R. Sherwood Cell invasion through basement membranes: an anchor of understanding Trends Cell Biol 16 2006 250 256
72. J.E. Collar, S. Ladva, T.D. Cairns, and V. Cattell Red cell traverse through thin glomerular basement membranes Kidney Int 59 2001 2069 2072
73. H. Liapis, K. Foster, and J.H. Miner Red cell traverse through thin glomerular basement membrane [Comment] Kidney Int 61 2002 762 763
74. J. Peti-Peterdi, and A. Sipos A high-powered view of the filtration barrier J Am Soc Nephrol 21 2010 1835 1841
75. M. Elger, T. Sakai, and W. Kriz The vascular pole of the renal glomerulus of rat Adv Anat Embryol Cell Biol 139 1998 1 98
76. J.W. Pippin, P.T. Brinkkoetter, F.C. Cormack-Aboud, R.V. Durvasula, P.V. Hauser, J. Kowalewska, R.D. Krofft, C.M. Logar, C.B. Marshall, T. Ohse, and S.J. Shankland Inducible rodent models of acquired podocyte diseases Am J Physiol Renal Physiol 296 2009 F213 F229
77. A. Steege, M. Fähling, A. Paliege, A. Bondke, K.M. Kirschner, P. Martinka, C. Kaps, A. Patzak, P.B. Persson, B.J. Thiele, H. Scholz, and R. Mrowka Wilms' tumor protein (-KTS) modulates renin gene transcription Kidney Int 74 2008 458 466