Podocyte number in children and adults: Associations with glomerular size and numbers of other glomerular resident cells

Journal of the American Society of Nephrology

Volumn 26, Issue 9, 2015, Pages 2277-2288

  Puelles, Victor G ^a   Douglas Denton, Rebecca N ^a   Cullen McEwen, Luise A ^a   Li, Jinhua ^a   Hughson, Michael D ^b   Hoy, Wendy E ^c   Kerr, Peter G ^a,d   Bertram, John F ^a  

^a MONASH UNIVERSITY   (Australia)

^b UNIVERSITY OF MISSISSIPPI SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF QUEENSLAND   (Australia)

^d MONASH MEDICAL CENTRE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ADOLESCENT; ADULT; ARTICLE; AUTOPSY; CELL COUNT; CELL DENSITY; CELL POPULATION; CELL STRUCTURE; CELL VOLUME; CELLULAR PARAMETERS; CHILD; CONFOCAL MICROSCOPY; CONTROLLED STUDY; EPITHELIUM CELL; FEMALE; GLOMERULAR RESIDENT CELL; GLOMERULAR SIZE; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; INDIVIDUAL GLOMERULAR VOLUME; INFANT; KIDNEY HYPERTROPHY; LIFE CYCLE; MALE; NEWBORN; PODOCYTE; PRIORITY JOURNAL; STEREOLOGY; YOUNG ADULT; ANATOMY AND HISTOLOGY; CHEMISTRY; CYTOLOGY; GLOMERULUS; MIDDLE AGED; ORGAN SIZE; PRESCHOOL CHILD;

VON WILLEBRAND FACTOR; WT1 PROTEIN; WT1 PROTEIN, HUMAN;

ADULT; CELL COUNT; CHILD, PRESCHOOL; HUMANS; IMMUNOHISTOCHEMISTRY; INFANT; KIDNEY GLOMERULUS; MALE; MICROSCOPY, CONFOCAL; MIDDLE AGED; ORGAN SIZE; PODOCYTES; VON WILLEBRAND FACTOR; WT1 PROTEINS;

EID: 84928493827     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2014070641     Document Type: Article

References (89)

1. Saran R, Shahinian V: CKD: A pandemic calling for concerted public health action. Adv Chronic Kidney Dis 17: 213-214, 2010
2. Wiggins RC: The spectrum of podocytopathies: A unifying view of glomerular diseases. Kidney Int 71: 1205-1214, 2007
3. Reiser J, Sever S: Podocyte biology and pathogenesis of kidney disease. Annu Rev Med 64: 357-366, 2013
4. Jefferson JA, Alpers CE, Shankland SJ: Podocyte biology for the bedside. Am J Kidney Dis 58: 835-845, 2011
5. 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
6. Kriz W, Elger M, Nagata M, Kretzler M, Uiker S, Koeppen-Hageman I, Tenschert S, Lemley KV: The role of podocytes in the development of glomerular sclerosis. Kidney Int Suppl 45: S64-S72, 1994
7. Mundel P, Shankland SJ: Podocyte biology and response to injury. J Am Soc Nephrol 13: 3005-3015, 2002
8. Durvasula RV, Shankland SJ: Podocyte injury and targeting therapy: An update. Curr Opin Nephrol Hypertens 15: 1-7, 2006
9. Shankland SJ: The podocyte's response to injury: Role in proteinuria and glomerulosclerosis. Kidney Int 69: 2131-2147, 2006
10. Jefferson JA, Nelson PJ, Najafian B, Shankland SJ: Podocyte disorders: Core Curriculum 2011. AmJ Kidney Dis 58: 666-677, 2011
11. Lemley KV, Bertram JF, Nicholas SB,White K: Estimation of glomerular podocyte number: A selection of valid methods. J AmSoc Nephrol 24: 1193-1202, 2013
12. Puelles VG, Douglas-Denton RN, Cullen-McEwen L, McNamara BJ, Salih F, Li J, Hughson MD, HoyWE, Nyengaard JR, BertramJF: Designbased stereological methods for estimating numbers of glomerular podocytes. Ann Anat 196: 48-56, 2014
13. Guo M, Ricardo SD, Deane JA, Shi M, Cullen-McEwen L, Bertram JF: A stereological study of the renal glomerular vasculature in the db/db mouse model of diabetic nephropathy. J Anat 207: 813-821, 2005
14. Wei P, Lane PH, Lane JT, Padanilam BJ, Sansom SC: Glomerular structural and functional changes in a high-fat diet mouse model of early-stage Type 2 diabetes. Diabetologia 47: 1541-1549, 2004
15. Cusumano AM, Bodkin NL, Hansen BC, Iotti R, Owens J, Klotman PE, Kopp JB: Glomerular hypertrophy is associated with hyperinsulinemia and precedes overt diabetes in aging rhesus monkeys.AmJKidneyDis 40: 1075-1085, 2002
16. Osterby R, Parving HH, Hommel E, Jrgensen HE, Lkkegaard H: Glomerular structure and function in diabetic nephropathy. Early to advanced stages. Diabetes 39: 1057-1063, 1990
17. Osterby R, Gundersen HJ, Nyberg G, Aurell M: Advanced diabetic glomerulopathy. Quantitative structural characterization of nonoccluded glomeruli. Diabetes 36: 612-619, 1987
18. Ijpelaar DH, Schulz A, Koop K, Schlesener M, Bruijn JA, Kerjaschki D, Kreutz R, deHeer E:Glomerular hypertrophy precedes albuminuria and segmental loss of podoplanin in podocytes in Munich-Wistar-Frömter rats. Am J Physiol Renal Physiol 294: F758-F767, 2008
19. Young RJ, Hoy WE, Kincaid-Smith P, Seymour AE, Bertram JF: Glomerular size and glomerulosclerosis in Australian aborigines. Am J Kidney Dis 36: 481-489, 2000
20. Nol LH: Morphological features of primary focal and segmental glomerulosclerosis. Nephrol Dial Transplant 14[Suppl 3]: 53-57, 1999
21. Cahill MM, Ryan GB, Bertram JF: Biphasic glomerular hypertrophy in rats administered puromycin aminonucleoside. Kidney Int 50: 768-775, 1996
22. Lee HS, Lim SD: The significance of glomerular hypertrophy in focal segmental glomerulosclerosis. Clin Nephrol 44: 349-355, 1995
23. Suzuki J, Yoshikawa N, Nakamura H: A quantitative analysis of the glomeruli in focal segmental glomerulosclerosis. Pediatr Nephrol 8: 416-419, 1994
24. Nyberg E, Bohman SO, Berg U: Glomerular volume and renal function in children with different types of the nephrotic syndrome. Pediatr Nephrol 8: 285-289, 1994
25. Brenner BM: Nephron adaptation to renal injury or ablation. Am J Physiol 249: F324-F337, 1985
26. Puelles VG, Hoy WE, Hughson MD, Diouf B, Douglas-Denton RN, Bertram JF: Glomerular number and size variability and risk for kidney disease. Curr Opin Nephrol Hypertens 20: 7-15, 2011
27. Pagtalunan ME, Miller PL, Jumping-Eagle S, Nelson RG, Myers BD, Rennke HG, Coplon NS, Sun L, Meyer TW: Podocyte loss and progressive glomerular injury in type II diabetes. J Clin Invest 99: 342-348, 1997
28. Meyer TW, Bennett PH, Nelson RG: Podocyte number predicts longterm urinary albumin excretion in Pima Indians with Type II diabetes and microalbuminuria. Diabetologia 42: 1341-1344, 1999
29. Dalla Vestra M,Masiero A, Roiter AM, Saller A, Crepaldi G, Fioretto P: Is podocyte injury relevant in diabetic nephropathy? Studies in patients with type 2 diabetes. Diabetes 52: 1031-1035, 2003
30. Su J, Li SJ, Chen ZH, Zeng CH, Zhou H, Li LS, Liu ZH: Evaluation of podocyte lesion in patients with diabetic nephropathy:Wilms' tumor-1 protein used as a podocyte marker. Diabetes Res Clin Pract 87: 167-175, 2010
31. Lemley KV, Lafayette RA, Safai M, Derby G, Blouch K, Squarer A,Myers BD: Podocytopenia and disease severity in IgAnephropathy. Kidney Int 61: 1475-1485, 2002
32. WangG, Lai FM, Kwan BC, Lai KB, ChowKM, Li PK, Szeto CC: Podocyte loss in human hypertensive nephrosclerosis. Am J Hypertens 22: 300-306, 2009
33. Zimanyi MA, HoyWE, Douglas-Denton RN, Hughson MD, Holden LM, Bertram JF: Nephron number and individual glomerular volumes in male Caucasian and African American subjects. Nephrol Dial Transplant 24: 2428-2433, 2009
34. Boulet SL, Schieve LA, Boyle CA: Birth weight and health and developmental outcomes in US children, 1997-2005.Matern Child Health J 15: 836-844, 2011
35. Stackhouse S, Miller PL, Park SK, Meyer TW: Reversal of glomerular hyperfiltration and renal hypertrophy by blood glucose normalization in diabetic rats. Diabetes 39: 989-995, 1990
36. Fabris B, Candido R, Armini L, Fischetti F, Calci M, Bardelli M, Fazio M, Campanacci L, Carretta R: Control of glomerular hyperfiltration and renal hypertrophy by an angiotensin converting enzyme inhibitor prevents the progression of renal damage in hypertensive diabetic rats. J Hypertens 17: 1925-1931, 1999
37. Herbach N, Schairer I, Blutke A, Kautz S, Siebert A, Göke B, Wolf E, Wanke R: Diabetic kidney lesions of GIPRdn transgenicmice: Podocyte hypertrophy and thickening of the GBM precede glomerular hypertrophy and glomerulosclerosis. Am J Physiol Renal Physiol 296: F819-F829, 2009
38. Lemley KV: A basis for accelerated progression of diabetic nephropathy in Pima Indians. Kidney Int Suppl 83: S38-S42, 2003
39. Cortes P, Zhao X, Dumler F, Tilley BC, Atherton J: Age-related changes in glomerular volume and hydroxyproline content in rat and human. J Am Soc Nephrol 2: 1716-1725, 1992
40. Hughson M, Farris AB 3rd, Douglas-Denton R, Hoy WE, Bertram JF: Glomerular number and size in autopsy kidneys: The relationship to birth weight. Kidney Int 63: 2113-2122, 2003
41. Puelles VG, ZimanyiMA, Samuel T, HughsonMD, Douglas-Denton RN, Bertram JF, Armitage JA: Estimating individual glomerular volume in the human kidney: Clinical perspectives. Nephrol Dial Transplant 27: 1880-1888, 2012
42. Samuel T, Hoy WE, Douglas-Denton R, Hughson MD, Bertram JF: Determinants of glomerular volume in different cortical zones of the human kidney. J Am Soc Nephrol 16: 3102-3109, 2005
43. Hoy WE, Hughson MD, Zimanyi M, Samuel T, Douglas-Denton R, Holden L, Mott S, Bertram JF: Distribution of volumes of individual glomeruli in kidneys at autopsy:Associationwith age, nephron number, birth weight and body mass index. Clin Nephrol 74[Suppl 1]: S105-S112, 2010
44. Hoy WE, Hughson MD, Diouf B, Zimanyi M, Samuel T, McNamara BJ, Douglas-Denton RN, Holden L, Mott SA, Bertram JF: Distribution of volumes of individual glomeruli in kidneys at autopsy: Association with physical and clinical characteristics and with ethnic group. Am J Nephrol 33[Suppl 1]: 15-20, 2011
45. Hughson MD, Puelles VG, Hoy WE, Douglas-Denton RN, Mott SA, Bertram JF: Hypertension, glomerular hypertrophy and nephrosclerosis: The effect of race. Nephrol Dial Transplant 29: 1399-1409, 2014
46. Puelles VG, Douglas-Denton RN, Zimanyi MA, Armitage JA, Hughson MD, Kerr PG, Bertram JF: Glomerular hypertrophy in subjects with low nephron number: Contributions of sex, body size and race. Nephrol Dial Transplant 29: 1686-1695, 2014
47. Olivetti G, Anversa P, Melissari M, Loud AV: Morphometry of the renal corpuscle during postnatal growth and compensatory hypertrophy. Kidney Int 17: 438-454, 1980
48. Marshall CB, Shankland SJ: Cell cycle regulatory proteins in podocyte health and disease. Nephron, Exp Nephrol 106: e51-e59, 2007
49. Marshall CB, Shankland SJ: Cell cycle and glomerular disease: A minireview. Nephron, Exp Nephrol 102: e39-e48, 2006
50. Griffin SV, Hiromura K, Pippin J, Petermann AT, Blonski MJ, Krofft R, Takahashi S, Kulkarni AB, Shankland SJ: Cyclin-dependent kinase 5 is a regulator of podocyte differentiation, proliferation, and morphology. Am J Pathol 165: 1175-1185, 2004
51. Hiromura K, Haseley LA, Zhang P,Monkawa T, Durvasula R, Petermann AT, Alpers CE, Mundel P, Shankland SJ: Podocyte expression of the CDK-inhibitor p57 during development and disease. Kidney Int 60: 2235-2246, 2001
52. Combs HL, Shankland SJ, Setzer SV, Hudkins KL, Alpers CE: Expression of the cyclin kinase inhibitor, p27kip1, in developing and mature human kidney. Kidney Int 53: 892-896, 1998
53. Conaldi PG, Bottelli A, Baj A, Serra C, Fiore L, Federico G, Bussolati B, Camussi G: Human immunodeficiency virus-1 that induces hyperproliferation and dysregulation of renal glomerular epithelial cells. Am J Pathol 161: 53-61, 2002
54. Lasagni L, Lazzeri E, Shankland SJ, Anders HJ, Romagnani P: Podocyte mitosis - a catastrophe. Curr Mol Med 13: 13-23, 2013
55. Mundel P, Reiser J, Kriz W: Induction of differentiation in cultured rat and human podocytes. J Am Soc Nephrol 8: 697-705, 1997
56. 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
57. Smeets B, Moeller MJ: Parietal epithelial cells and podocytes in glomerular diseases. Semin Nephrol 32: 357-367, 2012
58. 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
59. Shankland SJ, Anders HJ, Romagnani P: Glomerular parietal epithelial cells in kidney physiology, pathology, and repair. Curr Opin Nephrol Hypertens 22: 302-309, 2013
60. Zhang J, Hansen KM, Pippin JW, Chang AM, Taniguchi Y, Krofft RD, Pickering SG, Liu ZH, Abrass CK, Shankland SJ: De novo expression of podocyte proteins in parietal epithelial cells in experimental aging nephropathy. Am J Physiol Renal Physiol 302: F571-F580, 2012
61. PichaiwongW, 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
62. Poulsom R, Forbes SJ, Hodivala-Dilke K, Ryan E, Wyles S, Navaratnarasah S, Jeffery R, Hunt T, AlisonM, Cook T, Pusey C,Wright NA: Bone marrow contributes to renal parenchymal turnover and regeneration. J Pathol 195: 229-235, 2001
63. Perry J, Tam S, Zheng K, Sado Y, Dobson H, Jefferson B, Jacobs R, Thorner PS: Type IV collagen induces podocytic features in bone marrow stromal stem cells in vitro. J Am Soc Nephrol 17: 66-76, 2006
64. Prodromidi EI, Poulsom R, Jeffery R, Roufosse CA, Pollard PJ, Pusey CD, Cook HT: Bone marrow-derived cells contribute to podocyte regeneration and amelioration of renal disease in a mouse model of Alport syndrome. Stem Cells 24: 2448-2455, 2006
65. Shankland SJ, Smeets B, Pippin JW, MoellerMJ: The emergence of the glomerular parietal epithelial cell. Nat Rev Nephrol 10: 158-173, 2014
66. WannerN,Hartleben B,HerbachN,GoedelM, StickelN, 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
67. Berger K, Schulte K, Boor P, Kuppe C, van Kuppevelt TH, Floege J, Smeets B, Moeller MJ: The regenerative potential of parietal epithelial cells in adult mice. J Am Soc Nephrol 25: 693-705, 2014
68. Berger K, Moeller MJ: Podocytopenia, parietal epithelial cells and glomerulosclerosis. Nephrol Dial Transplant 29: 948-950, 2014
69. Walker KA, Bertram JF: Kidney development: Core curriculum 2011. Am J Kidney Dis 57: 948-958, 2011
70. Bertram JF, Douglas-Denton RN, Diouf B, Hughson MD, Hoy WE: Human nephron number: Implications for health and disease. Pediatr Nephrol 26: 1529-1533, 2011
71. Hughson MD, Gobe GC, HoyWE, Manning RD Jr., Douglas-Denton R, Bertram JF: Associations of glomerular number and birth weight with clinicopathological features of African Americans and whites. Am J Kidney Dis 52: 18-28, 2008
72. Hoy WE, Bertram JF, Denton RD, Zimanyi M, Samuel T, Hughson MD: Nephron number, glomerular volume, renal disease and hypertension. Curr Opin Nephrol Hypertens 17: 258-265, 2008
73. Hughson MD, Douglas-Denton R, Bertram JF, Hoy WE: Hypertension, glomerular number, and birth weight in African Americans and white subjects in the southeastern United States. Kidney Int 69: 671-678, 2006
74. Hoy WE, Hughson MD, Singh GR, Douglas-Denton R, Bertram JF: Reduced nephron number and glomerulomegaly in Australian Aborigines: A group at high risk for renal disease and hypertension. Kidney Int 70: 104-110, 2006
75. Douglas-Denton RN, McNamara BJ, Hoy WE, Hughson MD, Bertram JF: Does nephron number matter in the development of kidney disease? Ethn Dis 16: S2-40-5, 2006
76. Mauer SM, Lane P, Zhu D, Fioretto P, Steffes MW: Renal structure and function in insulin-dependent diabetes mellitus in man. J Hypertens Suppl 10: S17-S20, 1992
77. Steffes MW, Schmidt D, McCrery R, Basgen JM; International Diabetic Nephropathy Study Group: Glomerular cell number in normal subjects and in type 1 diabetic patients. Kidney Int 59: 2104-2113, 2001
78. White KE, Bilous RW, Marshall SM, El Nahas M, Remuzzi G, Piras G, De Cosmo S, Viberti G: Podocyte number in normotensive type 1 diabetic patients with albuminuria. Diabetes 51: 3083-3089, 2002
79. Nadasdy T, Laszik Z, Blick KE, Johnson LD, Silva FG: Proliferative activity of intrinsic cell populations in the normal human kidney. J AmSoc Nephrol 4: 2032-2039, 1994
80. DaneMJ, van den BergBM, AvramutMC, Faas FG, van der Vlag J, Rops AL, Ravelli RB, Koster BJ, van Zonneveld AJ, Vink H, Rabelink TJ: Glomerular endothelial surface layer acts as a barrier against albumin filtration. Am J Pathol 182: 1532-1540, 2013
81. Abboud HE: Mesangial cell biology. Exp Cell Res 318: 979-985, 2012
82. Fukuda A, Chowdhury MA, Venkatareddy MP, Wang SQ, Nishizono R, Suzuki T, Wickman LT, Wiggins JE, Muchayi T, Fingar D, Shedden KA, Inoki K, Wiggins RC: Growth-dependent podocyte failure causes glomerulosclerosis. J Am Soc Nephrol 23: 1351-1363, 2012
83. Moeller MJ, Kuppe C: Glomerular disease: The role of parietal epithelial cells in hyperplastic lesions. Nat Rev Nephrol 10: 5-6, 2014
84. Romagnani P: Parietal epithelial cells: Their role in health and disease. Contrib Nephrol 169: 23-36, 2011
85. Smeets B, Kuppe C, Sicking EM, Fuss A, Jirak P, van Kuppevelt TH, Endlich K, Wetzels JF, Gröne HJ, Floege J, Moeller MJ: Parietal epithelial cells participate in the formation of sclerotic lesions in focal segmental glomerulosclerosis. J Am Soc Nephrol 22: 1262-1274, 2011
86. Hoy WE, Douglas-Denton RN, Hughson MD, Cass A, Johnson K, Bertram JF: A stereological study of glomerular number and volume: Preliminary findings in a multiracial study of kidneys at autopsy. Kidney Int Suppl 83: S31-S37, 2003
87. Gundersen HJ, Jensen EB: The efficiency of systematic sampling in stereology and its prediction. J Microsc 147: 229-263, 1987
88. Niksic M, Slight J, Sanford JR, Caceres JF, Hastie ND: The Wilms' tumour protein (WT1) shuttles between nucleus and cytoplasm and is present in functional polysomes. Hum Mol Genet 13: 463-471, 2004
89. Collins TJ: ImageJ for microscopy. Biotechniques 43[Suppl]: 25-30, 2007