Development of Glomerular Circulation and Function

  • Alda Tufro
  • Ashima Gulati
Living reference work entry


From the Malpighian corpuscle description and Bowman’s sketch to defining its ultrastructure and molecular function, the ways we look at the kidney glomerulus have evolved tremendously. The first systematic exploration of the body with a microscope led to the identification of “Malpighian corpuscles” as “glands” within the kidney [1]. Two centuries later, a more sophisticated microscope enabled Sir William Bowman to identify glomerular capillary tufts in animal and human kidneys and demonstrate a relationship between the capillary tuft and the renal tubule [2]. Since then, the understanding of the human glomerulus as a specialized structure uniquely adapted for renal filtration at the proximal part of the nephron has considerably advanced.


Renal Blood Flow Glomerular Basement Membrane Renal Plasma Flow Slit Diaphragm Oncotic Pressure 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. 1.
    Malpighi M. De viscerum structura exercitatio anatomica (la-cobi Montij, Bononiae); 1666.Google Scholar
  2. 2.
    Bowman W. On the structure and use of the Malpighian bodies of the kidney, with observations on the circulation through that gland. Philos Trans R Soc Lond B Biol Sci. 1842;132:57–80.Google Scholar
  3. 3.
    O’Brien LL, McMahon AP. Induction and patterning of the metanephric nephron. Semin Cell Dev Biol. 2014.
  4. 4.
    Herzlinger D, Hurtado R. Patterning the renal vascular bed. Semin Cell Dev Biol. 2014.
  5. 5.
    Noden DW. Embryonic origins and assembly of blood vessels. Am Rev Respir Dis. 1989;140(4):1097–103.PubMedGoogle Scholar
  6. 6.
    Wilting JR, Christ B. Embryonic angiogenesis: a review. Naturwissenschaften. 1996;83:153–64.PubMedGoogle Scholar
  7. 7.
    Espinoza-Valdez A, Femat R, Ordaz-Salazar FC. A model for renal arterial branching based on graph theory. Math Biosci. 2010;2010(225):36–43.Google Scholar
  8. 8.
    Tomake RJ. Assembly of the vasculature and its regulation. Berlin: Birkhäuser; 2001.Google Scholar
  9. 9.
    Sequeria López ML, Gomez RA. Desarrollo de la vasculatura renal. Medicina. 2000;60:694 (In Spanish) // Sequeira Lopez ML, Gomez RA. Development of the renal arterioles. JASN. 2011;22:2156–65.Google Scholar
  10. 10.
    Tufro A, Tufro-McReddie A, Norwood VF, Aylor KW, Botkin SJ, Carey RM, Gomez RA. Oxygen regulates vascular endothelial growth factor-mediated vasculogenesis and tubulogenesis. Dev Biol. 1997;183:139–49.Google Scholar
  11. 11.
    Potter EL. Development of the human glomerulus. Arch Pathol. 1965;80:241–55.PubMedGoogle Scholar
  12. 12.
    Grobstein C. Inductive interaction in the development of the mouse metanephros. J Exp Zool. 1955;130:319–40.Google Scholar
  13. 13.
    Bernstein J, Cheng F, Roska J. Glomerular differentiation in metanephric culture. Lab Invest. 1981;45:183–90.PubMedGoogle Scholar
  14. 14.
    Poole TJ, Coffin JD. Vasculogenesis and angiogenesis: two distinct morphogenetic mechanisms establish embryonic vascular pattern. J Exp Zool. 1989;251(2):224–31.PubMedGoogle Scholar
  15. 15.
    Sariola H, Ekblom P, Lehtonen E, Saxén L. Differentiation and vascularization of the metanephric kidney grafted on the chorioallantoic membrane. Dev Biol. 1983;96:427–35.PubMedGoogle Scholar
  16. 16.
    Sariola H, Saarma M, Sainio K, Arumäe U, Palgi J, Vaahtokari A, Thesleff I, Karavanov A. Dependence of kidney morphogenesis on the expression of nerve growth factor receptor. Science. 1991;254(5031):571–3.PubMedGoogle Scholar
  17. 17.
    Ekblom P, Sariola H, Karkinen-Jaaskelainen M, Saxen L. The origin of the glomerular endothelium. Cell Differ. 1982;11:35–9.PubMedGoogle Scholar
  18. 18.
    Abrahamson DR, Robert B, Hyink DP, St John PL, Daniel TO. Origins and formation of microvasculature in the developing kidney. Kidney Int Suppl. 1998;67:S7–11.PubMedGoogle Scholar
  19. 19.
    Hyink DP, Tucker DC, St John PL, Leardkamolkarn V, Accavitti MA, Abrass CK, Abrahamson DR. Endogenous origin of glomerular endothelial and mesangial cells in grafts of embryonic kidneys. Am J Physiol. 1996;270:F886–99.PubMedGoogle Scholar
  20. 20.
    Robert B, St John PL, Hyink DP, Abrahamson DR. Evidence that embryonic kidney cells expressing flk-1 are intrinsic, vasculogenic angioblasts. Am J Physiol. 1996;271:F744–53.PubMedGoogle Scholar
  21. 21.
    Robert B, St John PL, Abrahamson DR. Direct visualization of renal vascular morphogenesis in Flk1 heterozygous mutant mice. Am J Physiol. 1998;275:F164–72.PubMedGoogle Scholar
  22. 22.
    Shalaby F, Rossant J, Yamaguchi TP. Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature. 1995;376:62–6.PubMedGoogle Scholar
  23. 23.
    Fong G-H, Rossant J, Gertsenstein M, Breitman ML. Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium. Nature. 1995;376:66–70.PubMedGoogle Scholar
  24. 24.
    Yamaguchi TP, Dumont DJ, Conlon RA, Breitman ML. Rossant J: flk-1, an flt-related receptor tyrosine kinase, is an early marker for endothelial precursors. Development. 1993;118:489–98.PubMedGoogle Scholar
  25. 25.
    Tufro A, Norwood VF, Carey RM, Gomez RA. Vascular endothelial growth factor induces nephrogenesis, and vasculogenesis. J Am Soc Nephrol. 1999;10:2125–34.PubMedGoogle Scholar
  26. 26.
    Simon M, Grone HJ, Johren O. Expression of vascular endothelial growth factor and its receptors in human renal ontogenesis and adult kidney. Am J Physiol. 1995;268:F240–50.PubMedGoogle Scholar
  27. 27.
    Flamme I, von Reutern M, Drexler HCA, Syed-Ali S, Risau W. Overexpression of vascular endothelial growth factor in the avian embryo induces hypervascularization and increased vascular permeability without alterations of embryonic pattern formation. Dev Biol. 1995;171:399–414.PubMedGoogle Scholar
  28. 28.
    Sims-Lucas S, Schaefer C, Bushnell D, Ho J, Logar A, et al. Endothelial progenitors exist within the kidney and lung mesenchyme. PLoS One. 2013;8(6):e65993.PubMedCentralPubMedGoogle Scholar
  29. 29.
    Tufro-McReddie A, Norwood VF, Aylor KW, Botkin SJ, Carey RM, Gomez RA. Oxygen regulates vascular endothelial growth factor-mediated vasculogenesis and tubulogenesis. Dev Biol. 1997;183:139–49.PubMedGoogle Scholar
  30. 30.
    Tufro A. VEGF spatially directs angiogenesis during metanephric development in vitro. Dev Biol. 2000;227:558–66.PubMedGoogle Scholar
  31. 31.
    Loughna S, Landels EC, Woolf AS. Growth factor control of developing kidney endothelial cells. Exp Nephrol. 1996;4:112–8.PubMedGoogle Scholar
  32. 32.
    Woolf AS, Loughna S. Origin of glomerular capillaries: is the verdict in? Exp Nephrol. 1998;6:17–21.PubMedGoogle Scholar
  33. 33.
    Hyink DP, Abrahamson DR. Origin of the glomerular vasculature in the developing kidney. Semin Nephrol. 1995;15:300–14.PubMedGoogle Scholar
  34. 34.
    Humphreys BD, Lin SL, Kobayashi A, Hudson TE, Nowlin BT, Bonventre JV, et al. Fate tracing reveals the pericyte and not epithelial origin of myofibroblasts in kidney fibrosis. Am J Pathol. 2010;176:85–97.PubMedCentralPubMedGoogle Scholar
  35. 35.
    Risau W. Differentiation of endothelium. FASEB J. 1995;9:926–33.PubMedGoogle Scholar
  36. 36.
    Risau W, Hallmann R, Albrecht U, Henke-Fahle S. Brain induces the expression of an early cell surface marker for blood–brain barrier-specific endothelium. EMBO J. 1986;5:3179–83.PubMedCentralPubMedGoogle Scholar
  37. 37.
    Schell C, Wanner N, Huber TB. Glomerular development–shaping the multi-cellular filtration unit. Se. Cell Dev Biol. 2014;36:39–49.Google Scholar
  38. 38.
    Leung DW, Cachianes G, Kuang WJ, Goeddel DV, Ferrara N. Vascular endothelial growth factor is a secreted angiogenic mitogen. Science. 1989;246:1306–9. PubMed: 2479986.PubMedGoogle Scholar
  39. 39.
    Keck PJ, Hauser SD, Krivi G, Sanzo K, Warren T, Feder J, et al. Vascular permeability factor, an endothelial cell mitogen related to PDGF. Science. 1989;246:1309–12. PubMed: 2479987.PubMedGoogle Scholar
  40. 40.
    Senger DR. Vascular endothelial growth factor: much more than an angiogenesis factor. Mol Biol Cell. 2010;21:377–9. PubMed: 20124007.PubMedCentralPubMedGoogle Scholar
  41. 41.
    Ferrara N, Houck K, Jakeman L, Leung DW. Molecular and biological properties of the vascular endothelial growth factor family of proteins. Endocr Rev. 1992;13:18–32.PubMedGoogle Scholar
  42. 42.
    Coultas L, Chawengsaksophak K, Rossant J. Endothelial cells and VEGF in vascular development. Nature. 2005;438:937–45. PubMed: 16355211.PubMedGoogle Scholar
  43. 43.
    Tischer E, Mitchell R, Haertman T, et al. The human gene for vascular endothelial growth factor. Multiple protein forms are encoded through alternative exon splicing. J Biol Chem. 1991;266:11947–54.PubMedGoogle Scholar
  44. 44.
    Guan F, Villegas G, Teichman J, Mundel P, Tufro A. Autocrine VEGF-A system in podocytes regulates podocin and its interaction with CD2AP. Am J Physiol Renal Physiol. 2006;291:F422–8. PubMed: 16597608.PubMedGoogle Scholar
  45. 45.
    Eremina V, Sood M, Haigh J, Nagy A, Lajoie G, Ferrara N, et al. Glomerular-specific alterations of VEGF-A expression lead to distinct congenital and acquired renal diseases. J Clin Invest. 2003;111:707–16. PubMed: 12618525.PubMedCentralPubMedGoogle Scholar
  46. 46.
    Roberts WG, Palade GE. Neovasculature induced by vascular endothelial growth factor is fenestrated. Cancer Res. 1997;57:765–72.PubMedGoogle Scholar
  47. 47.
    Kamba T, et al. VEGF-dependent plasticity of fenestrated capillaries in the normal adult microvasculature. Am J Physiol. 2006;290:H560–76.Google Scholar
  48. 48.
    Esser S, Wolburg K, Wolburg H, Breier G, Kurzchalia T, Risau W. Vascular endothelial growth factor induces endothelial fenestration in vitro. J Cell Biol. 1998;140:947–59.PubMedCentralPubMedGoogle Scholar
  49. 49.
    Kretzler M, Schroppel B, Merkle M, et al. Detection of multiple vascular endothelial growth factor splice isoforms in single glomerular podocytes. Kidney Int Suppl. 1998;67:S159–61.PubMedGoogle Scholar
  50. 50.
    Breier G, Albrecht U, Sterrer S, Risau W. Expression of vascular endothelial growth factor during embryonic angiogenesis and endothelial cell differentiation. Development. 1992;114(2):521–32.PubMedGoogle Scholar
  51. 51.
    Brown LF, Berse B, Tognazzi K, Manseau EJ, Van de Water L, Senger DR, Dvorak HF, Rosen S. Vascular permeability factor mRNA and protein expression in human kidney. Kidney Int. 1992;42(6):1457–61.PubMedGoogle Scholar
  52. 52.
    Eremina V, Cui S, Gerber H, Ferrara N, Haigh J, Nagy A, et al. Vascular endothelial growth factor a signaling in the podocyte-endothelial compartment is required for mesangial cell migration and survival. J Am Soc Nephrol. 2006;17:724–35. PubMed: 16436493.PubMedGoogle Scholar
  53. 53.
    Veron D, Reidy K, Villegas G, Kopp J, Thomas D, Tufro A. Induction of podocyte VEGF-A overexpression in adult mice causes glomerular disease. Kidney Int. 2010;77:989–99. PubMed: 20375978.PubMedGoogle Scholar
  54. 54.
    Veron D, Reidy K, Marlier A, Villegas G, Kashgarian M, Tufro A. Induction of podocyte VEGF164 overexpression at different stages of development causes congenital nephrosis or steroid-resistant nephrotic syndrome. Am J Pathol. 2010;177:2225–33. PubMed: 20829436.PubMedCentralPubMedGoogle Scholar
  55. 55.
    Jin J, Sison K, Li C, et al. Soluble FLT1 binds lipid micro-domains in podocytes to control cell morphology and glomerular barrier function. Cell. 2012;151:384–99.PubMedGoogle Scholar
  56. 56.
    Tufro A, Veron D. VEGF and podocytes in diabetic nephropathy. Semin Nephrol. 2012;32:385–93.PubMedCentralPubMedGoogle Scholar
  57. 57.
    Bertuccio C, Veron D, Aggarwal PK, et al. Vascular endothelial growth factor receptor 2 direct interaction with nephrin links VEGF-A signals to actin in kidney podocytes. J Biol Chem. 2011;286:39933–44.PubMedCentralPubMedGoogle Scholar
  58. 58.
    Lee S, Chen TT, Barber CL, Jordan MC, Murdock J, Desai S, Ferrara N, Nagy A, Roos KP, Iruela-Arispe ML. Autocrine VEGF signaling is required for vascular homeostasis. Cell. 2007;130(4):691–703.PubMedCentralPubMedGoogle Scholar
  59. 59.
    Villegas G, Lange-Sperandio GB, Tufro A. Autocrine and paracrine functions of vascular endothelial growth factor (VEGF) in renal tubular epithelial cells. Kidney Int. 2005;67:449–57. PubMed: 15673292.PubMedGoogle Scholar
  60. 60.
    Kanellis J, Fraser S, Katerelos M, Power DA. Vascular endothelial growth factor is a survival factor for renal tubular epithelial cells. Am J Physiol Renal Physiol. 2000;278:F905–15. PubMed: 10836978.PubMedGoogle Scholar
  61. 61.
    Eremina V, Jefferson JA, Kowalewska J, Hochster H, Haas M, Weisstuch J, et al. VEGF inhibition and renal thrombotic microangiopathy. N Engl J Med. 2008;358:1129–36. PubMed: 18337603.PubMedCentralPubMedGoogle Scholar
  62. 62.
    Veron D, Villegas G, Aggarwal P, Moeckel G, Kashgarian M, Tufro A. Acute podocyte VEGF-A knockdown disrupts αVβ3 integrin signaling in the glomerulus. J Am Soc Nephrol. 2011;22:9A. PubMed: 21164024.Google Scholar
  63. 63.
    Müller-Deile J, Worthmann K, Saleem M, Tossidou I, Haller H, Schiffer M. The balance of autocrine VEGF-A and VEGF-C determines podocyte survival. Am J Physiol Renal Physiol. 2009;297:F1656–67. PubMed: 19828679.PubMedGoogle Scholar
  64. 64.
    Ku CH, White KE, Dei Cas A, Hayward A, Webster Z, Bilous R, et al. Inducible overexpression of sFlt-1 in podocytes ameliorates glomerulopathy in diabetic mice. Diabetes. 2008;57:2824–33. PubMed: 18647955.PubMedCentralPubMedGoogle Scholar
  65. 65.
    Weis SM, Cheresh DA. Pathophysiological consequences of VEGF-induced vascular permeability. Nature. 2005;437:497–504. PubMed: 16177780.PubMedGoogle Scholar
  66. 66.
    Carmeliet P, et al. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature. 1996;380:435–9.PubMedGoogle Scholar
  67. 67.
    Ferrara N, Carver-Moore K, Chen H. Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature. 1996;380:439–42.PubMedGoogle Scholar
  68. 68.
    Breier G, Risau W. The role of vascular endothelial growth factor in blood vessel formation. Trends Cell Biol. 1996;6:454.PubMedGoogle Scholar
  69. 69.
    Carmeliet P. Mechanisms of angiogenesis and arteriogenesis. Nat Med. 2000;6:389–95.PubMedGoogle Scholar
  70. 70.
    Eichmann A, Makinen T, Alitalo K. Neural guidance molecules regulate vascular remodeling and vessel navigation. Genes Dev. 2005;19:1013–21.PubMedGoogle Scholar
  71. 71.
    Gelfand MV, Hong S, Gu C. Guidance from above: common cues direct distinct signaling outcomes in vascular and neural patterning. Trends Cell Biol. 2009;19:99–110.PubMedCentralPubMedGoogle Scholar
  72. 72.
    Reidy KJ, Villegas G, Teichman J, Veron D, Shen W, Jimenez J, et al. Semaphorin 3a regulates endothelial cell number and podocyte differentiation during glomerular development. Development. 2009;136:3979–89.PubMedCentralPubMedGoogle Scholar
  73. 73.
    Lindahl P, Hellstrom M, Kalen M, Karlsson L, Pekny M, Pekna M, et al. Paracrine PDGF-B/PDGF-R beta signaling controls mesangial cell development in kidney glomeruli. Development. 1998;125:3313–22.PubMedGoogle Scholar
  74. 74.
    Lindahl P, Johansson BR, Leveen P, Betsholtz C. Pericyte loss and microaneurysm formation in PDGF-B-deficient mice. Science. 1997;277:242–5.PubMedGoogle Scholar
  75. 75.
    Boyle SC, Liu Z, Kopan R. Notch signaling is required for the formation of mesangial cells from a stromal mesenchyme precursor during kidney development. Development. 2014;141:346–54.PubMedCentralPubMedGoogle Scholar
  76. 76.
    Lin EE, Sequeira-Lopez ML, Gomez RA. RBP-J in FOXD1+ renal stromal progenitors is crucial for the proper development and assembly of the kidney vasculature and glomerular mesangial cells. Am J Physiol Renal Physiol. 2014;306:F249–58.PubMedCentralPubMedGoogle Scholar
  77. 77.
    Takabatake Y, Sugiyama T, Kohara H, Matsusaka T, Kurihara H, Koni PA, et al. The CXCL12 (SDF-1)/CXCR4 axis is essential for the development of renal vasculature. J Am Soc Nephrol. 2009;20:1714–23.PubMedCentralPubMedGoogle Scholar
  78. 78.
    Jeansson M, Gawlik A, Anderson G, Li C, Kerjaschki D, Henkelman M, et al. Angiopoietin-1 is essential in mouse vasculature during development and in response to injury. J Clin Invest. 2011;121:2278–89.PubMedCentralPubMedGoogle Scholar
  79. 79.
    Dimke H, Sparks MA, Thomson BR, Frische S, Coffman TM, Quaggin SE. Tubulovascular Cross-Talk by vascular endothelial growth factor a maintains peritubular microvasculature in kidney. J Am Soc Nephrol. 2014;pii:ASN.2014010060. (Epub ahead of print).Google Scholar
  80. 80.
    Tufro A. Tubular vascular endothelial growth factor-A, erythropoietin, and medullary vessels: a trio linked by hypoxia. J Am Soc Nephrol. 2014;pii:ASN.2014101004.Google Scholar
  81. 81.
    Pitera JE, Woolf AS, Gale NW, Yancopoulos GD, Yuan HT. Dysmorphogenesis of kidney cortical peritubular capillaries in angiopoietin-2-deficient mice. Am J Pathol. 2004;165:1895–906.PubMedCentralPubMedGoogle Scholar
  82. 82.
    Madsen K, Marcussen N, Pedersen M, Kjaersgaard G, Facemire C, Coffman TM, et al. Angiotensin II promotes development of the renal microcirculation through AT1 receptors. J Am Soc Nephrol. 2010;21:448–59.PubMedCentralPubMedGoogle Scholar
  83. 83.
    Pappenheimer JR. Über die Permeabilität der Glomerulummembranen in der Niere. Klir Wochenschr. 1955;33:362.Google Scholar
  84. 84.
    Landis EM, Pappenheimer JR. Exchange of substances through the capillary walls. Handb Physiol. 1963;2(2):961.Google Scholar
  85. 85.
    Dressler GR. The cellular basis of kidney development. Annu Rev Cell Dev Biol. 2006;22:509–29.PubMedGoogle Scholar
  86. 86.
    Mundel P, Kriz W. Structure and function of podocytes: an update. Anat Embryol (Berl). 1995;192:385–97.Google Scholar
  87. 87.
    Rodewald R, Karnovsky MJ. Porous substructure of the glomerular slit diaphragm in the rat and mouse. J Cell Biol. 1974;60:423–33.PubMedCentralPubMedGoogle Scholar
  88. 88.
    Hora K, Ohno S, Ogushi H, Furukawa T, Furuta S. Three-dimensional study of glomerular slit diaphragm by the quick-freezing and deep-etching replica method. Eur J Cell Biol. 1990;53:402–6.PubMedGoogle Scholar
  89. 89.
    Wartiovaara J, Ofverstedt LG, Khoshnoodi J, Zhang J, Makela E, Sandin S, Ruotsalainen V, Cheng RH, Jalanko H, Skoglund U, Tryggvason K. Nephrin strands contribute to a porous slit diaphragm scaffold as revealed by electron tomography. J Clin Invest. 2004;114:1475–83.PubMedCentralPubMedGoogle Scholar
  90. 90.
    Gagliardini E, Conti S, Benigni A, Remuzzi G, Remuzzi A. Imaging of the porous ultrastructure of the glomerular epithelial filtration slit. J Am Soc Nephrol. 2012;21:2081–9.Google Scholar
  91. 91.
    Farquhar MG, Wissig SL, Palade GE. Glomerular permeability. I. Ferritin transfer across the normal glomerular capillary wall. J Exp Med. 1961;113:47.PubMedCentralPubMedGoogle Scholar
  92. 92.
    Farquhar MG, Palade GE. Glomerular permeability. II. Ferritin transfer across the glomerular capillary wall in nephrotic rats. J Exp Med. 1961;114:699.PubMedCentralPubMedGoogle Scholar
  93. 93.
    Venkatachalam MA, Karnovsky MJ, Cotran RS. Glomerular permeability. Ultrastructural studies in experimental nephrosis using horseradish peroxidase as a tracer. J Exp Med. 1969;130:381–99.PubMedCentralPubMedGoogle Scholar
  94. 94.
    Kestilä M, Lenkkeri U, Männikkö M, Lamerdin J, McCready P, Putaala H, Ruotsalainen V, Morita T, Nissinen M, Herva R, Kashtan CE, Peltonen L, Holmberg C, Olsen A, Tryggvason K. Positionally cloned gene for a novel glomerular protein–nephrin–is mutated in congenital nephrotic syndrome. Mol Cell. 1998;1:575–82.PubMedGoogle Scholar
  95. 95.
    Wanner N, Noutsou F, Baumeister R, Walz G, Huber TB, Neumann-Haefelin E. Functional and spatial analysis of C. elegans SYG-1 and SYG-2, orthologs of the Neph/nephrin cell adhesion module directing selective synaptogenesis. PLoS One. 2011;6:e23598.PubMedCentralPubMedGoogle Scholar
  96. 96.
    Helmstädter M, Lüthy K, Gödel M, Simons M, Ashish ND, Rensing SA, Fischbach KF, Huber TB. Functional study of mammalian Neph proteins in Drosophila melanogaster. PLoS One. 2012;7:e40300.PubMedCentralPubMedGoogle Scholar
  97. 97.
    Huber TB, Benzing T. The slit diaphragm: a signaling plat- form to regulate podocyte function. Curr Opin Nephrol Hypertens. 2005;14:211–6.PubMedGoogle Scholar
  98. 98.
    Neumann-Haefelin E, Kramer-Zucker A, Slanchev K, Hartleben B, Noutsou F, Martin K, Wanner N, Ritter A, Gödel M, Pagel P, Fu X, Müller A, Baumeister R, Walz G, Huber TB. A model organism approach: defining the role of Neph proteins as regulators of neuron and kidney morphogenesis. Hum Mol Genet. 2010;19:2347–59.PubMedGoogle Scholar
  99. 99.
    Rantanen M, Palmén T, Pätäri A, Ahola H, Lehtonen S, Aström E, Floss T, Vauti F, Wurst W, Ruiz P, Kerjaschki D, Holthöfer H. Nephrin TRAP mice lack slit diaphragms and show fibrotic glomeruli and cystic tubular lesions. J Am Soc Nephrol. 2002;13:1586–94.PubMedGoogle Scholar
  100. 100.
    Ruotsalainen V, Ljungberg P, Wartiovaara J, et al. Nephrin is specifically located at the slit diaphragm of glomerular podocytes. Proc Natl Acad Sci U S A. 1999;96:7962–7. PubMed: 10393930.PubMedCentralPubMedGoogle Scholar
  101. 101.
    Sellin L, Huber TB, Gerke P, Quack I, Pavenstädt H, Walz G. NEPH1 defines a novel family of podocin interacting proteins. FASEB J. 2003;17:115–7.PubMedGoogle Scholar
  102. 102.
    Donoviel DB, Freed DD, Vogel H, et al. Proteinuria and perinatal lethality in mice lacking NEPH1, a novel protein with homology to NEPHRIN. Mol Cell Biol. 2001;21:4829–36.PubMedCentralPubMedGoogle Scholar
  103. 103.
    Doné SC, Takemoto M, He L, et al. Nephrin is involved in podocyte maturation but not survival during glomerular development. Kidney Int. 2008;73:697–704.PubMedGoogle Scholar
  104. 104.
    Simons M, Huber TB. It’s not all about nephrin. Kidney Int. 2008;73:671–3.PubMedGoogle Scholar
  105. 105.
    Boute N, Gribouval O, Roselli S, Benessy F, Lee H, Fuchshuber A, Dahan K, Gubler MC, Niaudet P, Antignac C. NPHS2, encoding the glomerular protein podocin, is mutated in autosomal recessive steroid-resistant nephrotic syndrome. Nat Genet. 2000;24:349–54.PubMedGoogle Scholar
  106. 106.
    Miner JH. Focusing on the glomerular slit diaphragm: podocin enters the picture. Am J Pathol. 2002;160:3–5.PubMedCentralPubMedGoogle Scholar
  107. 107.
    Asanuma K, Campbell KN, Kim K, Faul C, Mundel P. Nuclear relocation of the nephrin and CD2AP-binding protein dendrin promotes apoptosis of podocytes. Proc Natl Acad Sci U S A. 2007;104:10134–9.PubMedCentralPubMedGoogle Scholar
  108. 108.
    Shih NY, Li J, Karpitskii V, Nguyen A, Dustin ML, Kanagawa O, Miner JH, Shaw AS. Congenital nephrotic syndrome in mice lacking CD2-associated protein. Science. 1999;286:312–5.PubMedGoogle Scholar
  109. 109.
    Li C, Ruotsalainen V, Tryggvason K, et al. CD2AP is expressed with nephrin in developing podocytes and is found widely in mature kidney and elsewhere. Am J Physiol Renal Physiol. 2000;279:F785–92. PubMed: 10997929.PubMedGoogle Scholar
  110. 110.
    Hinkes B, Wiggins RC, Gbadegesin R, Vlangos CN, Seelow D, Nürnberg G, Garg P, Verma R, Chaib H, Hoskins BE, Ashraf S, Becker C, Hennies HC, Goyal M, Wharram BL, Schachter AD, Mudumana S, Drummond I, Kerjaschki D, Waldherr R, Dietrich A, Ozaltin F, Bakkaloglu A, Cleper R, Basel-Vanagaite L, Pohl M, Griebel M, Tsygin AN, Soylu A, Müller D, Sorli CS, Bunney TD, Katan M, Liu J, Attanasio M, O’toole JF, Hasselbacher K, Mucha B, Otto EA, Airik R, Kispert A, Kelley GG, Smrcka AV, Gudermann T, Holzman LB, Nürnberg P, Hildebrandt F. Positional cloning uncovers mutations in PLCE1 responsible for a nephrotic syndrome variant that may be reversible. Nat Genet. 2006;38:1397–405.PubMedGoogle Scholar
  111. 111.
    Reiser J, Polu KR, Möller CC, Kenlan P, Altintas MM, Wei C, Faul C, Herbert S, Villegas I, Avila-Casado C, McGee M, Sugimoto H, Brown D, Kalluri R, Mundel P, Smith PL, Clapham DE, Pollak MR. TRPC6 is a glomerular slit diaphragm- associated channel required for normal renal function. Nat Genet. 2005;37:739–44.PubMedCentralPubMedGoogle Scholar
  112. 112.
    Timpl R. Structure and biological activity of basement membrane proteins. Eur J Biochem. 1989;180:487–502.PubMedGoogle Scholar
  113. 113.
    Miner JH. Developmental biology of glomerular basement membrane components. Curr Opin Nephrol Hypertens. 1998;7:13–9.PubMedGoogle Scholar
  114. 114.
    St John PL, Wang R, Yin Y, Miner JH, Robert B, Abrahamson DR. Glomerular laminin isoform transitions: errors in metanephric culture are corrected by grafting. Am J Physiol Renal Physiol. 2001;280(4):F695–705.PubMedGoogle Scholar
  115. 115.
    Miner JH, Patton BL, Lentz SI, Gilbert DJ, Snider WD, Jenkins NA, Copeland NG, Sanes JR. The laminin alpha chains: expression, developmental transitions, and chromosomal locations of alpha1-5, identification of heterotrimeric laminins 8-11, and cloning of a novel alpha3 isoform. J Cell Biol. 1997;137:685–701.PubMedCentralPubMedGoogle Scholar
  116. 116.
    Miner JH, Sanes JR. Collagen IV α3, α4, and α5 chains in rodent basal laminae: sequence, distribution, association with laminins, and developmental switches. J Cell Biol. 1994;127:879–91.PubMedGoogle Scholar
  117. 117.
    Poschl E, Schlotzer-Schrehardt U, Brachvogel B, Saito K, Ninomiya Y, Mayer U. Collagen IV is essential for basement membrane stability but dispensable for initiation of its assembly during early development. Development. 2004;131:1619–28.PubMedGoogle Scholar
  118. 118.
    Bohrer MP, Baylis C, Humes HD, Glassock RJ, Robertson CR, Brenner BM. Permselectivity of the glomerular capillary wall. Facilitated filtration of circulating polycations. J Clin Invest. 1978;61:72–8. PubMed: 618914.PubMedCentralPubMedGoogle Scholar
  119. 119.
    Smithies O. Why the kidney glomerulus does not clog: a gel permeation/diffusion hypothesis of renal function. Proc Natl Acad Sci U S A. 2003;100(7):4108–13.PubMedCentralPubMedGoogle Scholar
  120. 120.
    Moeller MJ, Tenten V. Renal albumin filtration: alternative models to the standard physical barriers. Nat Rev Nephrol. 2013;9(5):266–77.PubMedGoogle Scholar
  121. 121.
    Satchell S. The role of the glomerular endothelium in albumin handling. Nat Rev Nephrol. 2013;9(12):717–25.PubMedGoogle Scholar
  122. 122.
    Haraldsson B, Nyström J, Deen WM. Properties of the glomerular barrier and mechanisms of proteinuria. Physiol Rev. 2008;88:451–87.PubMedGoogle Scholar
  123. 123.
    Harvey SJ, Jarad G, Cunningham J, Rops AL, van der Vlag J, Berden JH, Moeller MJ, Holzman LB, Burgess RW, Miner JH. Disruption of glomerular basement membrane charge through podocyte-specific mutation of agrin does not alter glomerular permselectivity. Am J Pathol. 2007;171:139–52.PubMedCentralPubMedGoogle Scholar
  124. 124.
    Goldberg S, Harvey SJ, Cunningham J, Tryggvason K, Miner JH. Glomerular filtration is normal in the absence of both agrin and perlecan-heparan sulfate from the glomerular basement membrane. Nephrol Dial Transplant. 2009;24:2044–51.PubMedCentralPubMedGoogle Scholar
  125. 125.
    van den Hoven MJ, Wijnhoven TJ, Li JP, Zcharia E, Dijkman HB, Wismans RG, Rops AL, Lensen JF, van den Heuvel LP, van Kuppevelt TH, Vlodavsky I, Berden JH, van der Vlag J. Reduction of anionic sites in the glomerular basement membrane by heparanase does not lead to proteinuria. Kidney Int. 2008;73:278–87.PubMedGoogle Scholar
  126. 126.
    Axelsson J, Sverrisson K, Rippe A, Fissell W, Rippe B. Reduced diffusion of charge modified, conformationally intact anionic Ficoll relative to neutral Ficoll across the rat glomerular filtration barrier in vivo. Am J Physiol Renal Physiol. 2011;301:F708–12.PubMedGoogle Scholar
  127. 127.
    Hausmann R, Kuppe C, Egger H, Schweda F, Knecht V, Elger M, Menzel S, Somers D, Braun G, Fuss A, Uhlig S, Kriz W, Tanner G, Floege J, Moeller MJ. Electrical forces determine glomerular permeability. J Am Soc Nephrol. 2010;21:2053–8.PubMedCentralPubMedGoogle Scholar
  128. 128.
    Ryan GB, Karnovsky MJ. Distribution of endogenous albumin in the rat glomerulus: role of hemodynamic factors in glomerular barrier function. Kidney Int. 1976;9:36–45.PubMedGoogle Scholar
  129. 129.
    Bevan HS, Slater SC, Clarke H, et al. Acute laminar shear stress reversibly & increases human glomerular endothelial cell permeability via activation of endothelial nitric oxide synthase. Am J Physiol Renal Physiol. 2011;301:F733–42.PubMedCentralPubMedGoogle Scholar
  130. 130.
    Friden V, Oveland E, Tenstad O, et al. The glomerular endothelial cell coat is essential for glomerular filtration. Kidney Int. 2011;79:1322–30.PubMedGoogle Scholar
  131. 131.
    Haraldsson B, Nyström J. The glomerular endothelium: new insights on function and structure. Curr Opin Nephrol Hypertens. 2012;21(3):258–63.PubMedGoogle Scholar
  132. 132.
    Oubaha M, Gratton JP. Phosphorylation of endothelial nitric oxide synthase by atypical PKC zeta contributes to angiopoietin-1-dependent inhibition of VEGF-induced endothelial permeability in vitro. Blood. 2009;114(15):3343–51.PubMedGoogle Scholar
  133. 133.
    Eklund L, Saharinen P. Angiopoietin signaling in the vasculature. Exp Cell Res. 2013;319(9):1271–80.PubMedGoogle Scholar
  134. 134.
    Davis B, Dei Cas A, Long DA, White KE, Hayward A, Ku CH, Woolf AS, Bilous R, Viberti G, Gnudi L. Podocyte-specific expression of angiopoietin-2 causes proteinuria and apoptosis of glomerular endothelia. J Am Soc Nephrol. 2007;18(8):2320–9.PubMedGoogle Scholar
  135. 135.
    Khan S, Lakhe-Reddy S, McCarty JH, et al. Mesangial cell integrin alphavbeta8 provides glomerular endothelial cell cytoprotection by sequestering TGF-beta and regulating PECAM-1. Am J Pathol. 2011;178:609–20.PubMedCentralPubMedGoogle Scholar
  136. 136.
    Clement LC, Avila-Casado C, Mace C, et al. Podocyte-secreted angiopoietin-like-4 mediates proteinuria in glucocorticoid-sensitive nephrotic syndrome. Nat Med. 2011;17:117–22.PubMedCentralPubMedGoogle Scholar
  137. 137.
    Huang RL, Teo Z, Chong HC, et al. ANGPTL4 modulates vascular junction & integrity by integrin signaling and disruption of intercellular VE-cadherin and claudin-5 clusters. Blood. 2011;118:3990–4002.PubMedGoogle Scholar
  138. 138.
    El-Banawy HS, Gaber EW, Maharem DA, Matrawy KA. Angiopoietin-2, & endothelial dysfunction and renal involvement in patients with systemic lupus erythematosus. J Nephrol. 2011. doi:10.5301/jn.5000030. The effect of Angiopoeitin-2 and endothelial dysfunction.Google Scholar
  139. 139.
    Pappenheimer JR. Passage of molecules through capillary walls. Physiol Rev. 1953;33:387–423.PubMedGoogle Scholar
  140. 140.
    Blouch K, Deen WM, Fauvel JP, Bialek J, Derby G, Myers BD. Molecular configuration and glomerular size selectivity in healthy and nephrotic humans. Am J Physiol. 1997;273:F430–7.PubMedGoogle Scholar
  141. 141.
    Deen WM, Bridges CR, Brenner BM, Myers BD. Heteroporous model of glomerular size selectivity: application to normal and nephrotic humans. Am J Physiol. 1985;249:F374–89.PubMedGoogle Scholar
  142. 142.
    Öberg CM, Rippe B. A distributed two-pore model: theoretical implications and practical application to the glomerular sieving of Ficoll. Am J Physiol Renal Physiol. 2014;306(8):F844–54.PubMedGoogle Scholar
  143. 143.
    Deen WM, Bohrer MP, Brenner BM. Macromolecule transport across glomerular capillaries: application of pore theory. Kidney Int. 1979;16(3):353–65.PubMedGoogle Scholar
  144. 144.
    Katz MA, Schaeffer Jr RC, Gratrix M, Mucha D, Carbajal J. The glomerular barrier fits a two-pore-and-fiber-matrix model: derivation and physiologic test. Microvasc Res. 1999;57(3):227–43.PubMedGoogle Scholar
  145. 145.
    Drummond MC, Kristal B, Myers BD, Deen WM. Structural basis for reduced glomerular filtration capacity in nephrotic humans. J Clin Invest. 1994;94:1187–95.Google Scholar
  146. 146.
    Drummond MC, Deen WM. Structural determinants of glomerular hydraulic permeability. Am J Physiol Renal Fluid Electrolyte Physiol. 1994;266:F1–12.Google Scholar
  147. 147.
    Kedem O, Katchalsky A. Thermodynamic analysis of the permeability of biological membranes to non-electrolytes. Biochim Biophys Acta. 1958;27:229.PubMedGoogle Scholar
  148. 148.
    Bohman SO, Jaremko G, Bohlin AB, Berg U. Foot process fusion and glomerular filtration rate in minimal change nephrotic syndrome. Kidney Int. 1984;25(4):696–700.PubMedGoogle Scholar
  149. 149.
    Brenner BM, Troy JL, Daugharty TM. The dynamics of glomerular ultrafiltration in the rat. J Clin Invest. 1971;50:1776–80.PubMedCentralPubMedGoogle Scholar
  150. 150.
    Chasis H, Ranges HA, Goldring W, Smith HW. The control of renal blood flow and glomerular filtration in normal man. J Clin Invest. 1938;17:683.PubMedCentralPubMedGoogle Scholar
  151. 151.
    Smith HW, Goldring W, Chasis H. The measurement of the tubular excretory mass, effective blood flow and filtration rate in the normal human kidney. J Clin Invest. 1938;17:263.PubMedCentralPubMedGoogle Scholar
  152. 152.
    Smith HW, Chasis H, Goldring W, Ranges HA. Glomerular dynamics in the normal human kidney. J Clin Invest. 1940;19:751–64.PubMedCentralPubMedGoogle Scholar
  153. 153.
    Lafferty HM, Anderson S, Brenner BM. Anemia: a potent modulator of renal hemodynamics in models of progressive renal disease. Am J Kidney Dis. 1991;17(5 Suppl 1):2–7.PubMedGoogle Scholar
  154. 154.
    Larsson L, Aperia A, Elinder G. Structural and functional development of the nephron. Acta Paediatr Scand Suppl. 1983;305:56–60.PubMedGoogle Scholar
  155. 155.
    Paton JB, Fisher DE, Peterson EN, DeLannoy CW, Behrman RE. Cardiac output and organ blood flows in the baboon fetus. Biol Neonate. 1973;22(1):50–7.PubMedGoogle Scholar
  156. 156.
    Rudolph AM, Heymann MA. Circulatory changes during growth in the fetal lamb. Circ Res. 1970;26(3):289–99.PubMedGoogle Scholar
  157. 157.
    Rudolph AM, Heymann MA, Teramo KAW, et al. Studies on the circulation of the previable human fetus. Pediatr Res. 1971;5:452.Google Scholar
  158. 158.
    Rubin MI, Bruck E, Rapoport M. Maturation of renal function in childhood; clearance studies. J Clin Invest. 1949;28(5 Pt 2):1144–62.PubMedCentralGoogle Scholar
  159. 159.
    Calcagno PL, Rubin MI. Renal extraction of para-aminohippurate in infants and children. J Clin Invest. 1963;42:1632–9.PubMedCentralPubMedGoogle Scholar
  160. 160.
    Gruskin AB, Edelmann Jr CM, Yuan S. Maturational changes in renal blood flow in piglets. Pediatr Res. 1970;4(1):7–13.PubMedGoogle Scholar
  161. 161.
    Barnett HL, Hare K, McNamara H, Hare R. Measurement of glomerular filtration rate in premature infants. J Clin Invest. 1948;27(6):691–9.PubMedCentralGoogle Scholar
  162. 162.
    Spitzer A. Edelman CH Jr. Maturational changes in pressure gradients for glomerular filtration. Am J Physiol. 1971;221:1431–1435.Google Scholar
  163. 163.
    Horster M, Valtin H. Postnatal development of renal function: micropuncture and clearance studies in the dog. J Clin Invest. 1971;50(4):779–95.PubMedCentralPubMedGoogle Scholar
  164. 164.
    Friis C. Postnatal development of renal function in piglets: glomerular filtration rate, clearance of PAH and PAH extraction. Biol Neonate. 1979;35(3–4):180–7.PubMedGoogle Scholar
  165. 165.
    Barnett HL, Hare WK, et al. Influence of postnatal age on kidney function of premature infants. Proc Soc Exp Biol Med. 1948;69(1):55–7.PubMedGoogle Scholar
  166. 166.
    Arant Jr BS. Developmental patterns of renal functional maturation compared in the human neonate. J Pediatr. 1978;92(5):705–12.PubMedGoogle Scholar
  167. 167.
    Abitbol CL, Seeherunvong W, Galarza MG, Katsoufis C, Francoeur D, Defreitas M, Edwards-Richards A, Master Sankar Raj V, Chandar J, Duara S, Yasin S, Zilleruelo G. Neonatal kidney size and function in preterm infants: what is a true estimate of glomerular filtration rate? J Pediatr. 2014;164(5):1026–31.PubMedGoogle Scholar
  168. 168.
    Carl Ludwig original reference: Ludwig CFW. Beitraege zur Lehre vom Mechanismus der Harnsekretion. Marburg: N.G. Elwert; 1843.Google Scholar
  169. 169.
    Heidenhain RP. Absonderungsvorgaenge. Sechster Abschnitt. Die Harnabsonderung (Viertes Capitel. Die Absonderung der festen Harnbestandteile). In: Leipzig HL, editor. Handbuch d Physiol Fuenfter Teil. Germany: Vogel; 1883. p. 341–43.Google Scholar
  170. 170.
    Wearn JT, Richards AN. From: observations on the composition of glomerular urine, with particular reference to the problem of reabsorption in the renal tubules. Am J Physiol. 1924;71:209–27.Google Scholar
  171. 171.
    Starling EH. The glomerular functions of the kidney. J Physiol Lond. 1899;24:317–30.PubMedCentralPubMedGoogle Scholar
  172. 172.
    Wies CH, Peters JP. The osmotic pressure of proteins in whole serum. J Clin Invest. 1937;16:93.PubMedCentralPubMedGoogle Scholar
  173. 173.
    Levinsky NG, Berliner RW. Changes in composition of the ureter and bladder at low urine flow. Am J Physiol. 1959;196:549–53.PubMedGoogle Scholar
  174. 174.
    Levinsky NG, Lieberthal W. Clearance techniques. In: Windhager E. editor. Handbook of physiology. Renal physiology. New York: Oxford University Press; 1992, sect. 8, pp. 227–47.Google Scholar
  175. 175.
    Shannon JA, Smith HW. The excretion of inulin, xylose and urea by normal and phlorinized man. J Clin Invest. 1935;112:405–13.Google Scholar
  176. 176.
    Heiskanen T, Weber T, Grasbeck R. Determination of I131 hippuric acid renal clearances using single-injection techniques. Scand J Clin Lab Invest. 1968;21:211–5.PubMedGoogle Scholar
  177. 177.
    Smith HW. The kidney- structure and function in health and disease. New York: Oxford University Press; 1951.Google Scholar
  178. 178.
    Earle Jr DP, Berliner RW. A simplified clinical procedure for measurement of glomerular filtration rate and renal plasma flow. Proc Soc Exp Biol Med. 1946;62(2):262–4.PubMedGoogle Scholar
  179. 179.
    Orlando R, Floreani M, Padrini R, Palatini P. Determination of inulin clearance by bolus intravenous injection in healthy subjects and ascitic patients: equivalence of systemic and renal clearances as glomerular filtration markers. Br J Clin Pharmacol. 1998;46(6):605–9.PubMedCentralPubMedGoogle Scholar
  180. 180.
    Brismar J, Jacobsson BF, Jorulf H. Miscellaneous adverse effects of low-versus high-osmolality contrast media: a study revised. Radiology. 1991;179(1):19–22.PubMedGoogle Scholar
  181. 181.
    Berglund F. Renal clearance of inulin, polyfructosan-S and a polyethy-lene glycol (PE6 1000) in the rat. Acta Physiol Scand. 1965;64:238–44.PubMedGoogle Scholar
  182. 182.
    Bing J, Effersoe P. Comparative tests of the thiosulphate and creatinine clearances in rabbits and cats. Acta Physiol Scand. 1948;15:231–6.Google Scholar
  183. 183.
    Shemesh O, Golbetz H, Kriss JP, Myers BD. Limitations of creatinine as a filtration marker in glomerulopathic patients. Kidney Int. 1985;28:830–8.PubMedGoogle Scholar
  184. 184.
    Schwartz GJ, Munoz A, Schneider MF, et al. New equations to estimate GFR in children with CKD. J Am Soc Nephrol. 2009;20:629–37.PubMedCentralPubMedGoogle Scholar
  185. 185.
    Dharnidharka VR, Kwon C, Stevens G. Serum cystatin C is superior to serum creatinine as a marker of kidney function: a meta-analysis. Am J Kidney Dis. 2002;40(2):221–6.PubMedGoogle Scholar
  186. 186.
    Roos JF, Doust J, Tett SE, Kirkpatrick CM. Diagnostic accuracy of cystatin C compared to serum creatinine for the estimation of renal dysfunction in adults and children–a meta-analysis. Clin Biochem. 2007;40(5–6):383–91.PubMedGoogle Scholar
  187. 187.
    Filler G, Yasin A, Medeiros M. Methods of assessing renal function. Pediatr Nephrol. 2014;29(2):183–92.PubMedGoogle Scholar
  188. 188.
    Filler G, Kusserow C, Lopes L, Kobrzyński M. Beta-trace protein as a marker of GFR–history, indications, and future research. Clin Biochem. 2014;47(13–14):1188–94.PubMedGoogle Scholar
  189. 189.
    Lorenz JN, Gruenstein E. A simple, nonradioactive method for evaluating single-nephron filtration rate using FITC-inulin. Am J Physiol. 1999;276(1 Pt 2):F172–7.PubMedGoogle Scholar
  190. 190.
    Yu W, Sandoval RM, Molitoris BA. Quantitative intravital microscopy using a generalized polarity concept for kidney studies. Am J Physiol Cell Physiol. 2005;289:C1197–208.PubMedGoogle Scholar
  191. 191.
    Wang E, Meier DJ, Sandoval RM, Von Hendy-Willson VE, Presser BM, Bunch RM, Alloosh M, Sturek MS, Schwartz GJ, Molitoris BA. A portable fiberoptic ratiometric fluorescence analyzer provides rapid point-of-care determination of glomerular filtration rate in large animals. Kidney Int. 2012;81:112–7.PubMedGoogle Scholar
  192. 192.
    Yu W, Sandoval RM, Molitoris BA. Rapid determination of renal filtration fraction using an optical ratiometric imaging approach. Am J Physiol Renal Physiol. 2007;292:F1837–80.Google Scholar
  193. 193.
    Quaggin SE. Transcriptional regulation of podocyte specification and differentiation. Microsc Res Tech. 2002;57(4):208–11.PubMedGoogle Scholar
  194. 194.
    Abrahamson DR. Role of the podocyte (and glomerular endothelium) in building the GBM. Semin Nephrol. 2012;32(4):342–9.PubMedCentralPubMedGoogle Scholar
  195. 195.
    Patrakka J, Tryggvason K. Molecular make-up of the glomerular filtration barrier. Biochem Biophys Res Commun. 2010;396(1):164–9.PubMedGoogle Scholar
  196. 196.
    Aperia A, Herin P. Development of glomerular perfusion rate and nephron filtration rate in rats 17 to 20 days old. Am J Physiol. 1975;228:1319.PubMedGoogle Scholar
  197. 197.
    Aperia A, Broberger O, Thodenius K, et al. Development of renal control of salt and fluid homeostasis during the first year of life. Acta Paediatr Scand. 1975;64:393.PubMedGoogle Scholar
  198. 198.
    Chevalier RL. Developmental renal physiology of the low birth weight preterm newborn. J Urol. 1996;156(2 Pt 2):714–9.PubMedGoogle Scholar
  199. 199.
    Stonestreet BS, Oh W. Plasma creatinine levels in low-birth-weight infants during the first three months of life. Pediatrics. 1978;61:788.PubMedGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.Department of Pediatrics, Nephrology SectionYale School of MedicineNew HavenUSA

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