Table of Contents Author Guidelines Submit a Manuscript
Stem Cells International
Volume 2015, Article ID 362562, 7 pages
http://dx.doi.org/10.1155/2015/362562
Review Article

Human Urine as a Noninvasive Source of Kidney Cells

1Department of Development and Regeneration, Catholic University Leuven, Herestraat 49, 3000 Leuven, Belgium
2Institute of Translational Medicine, University of Liverpool, Crown Street, Liverpool L69 3BX, UK
3Center for Molecular Biotechnology, Department of Molecular Biotechnology and Health Sciences, University of Turin, Via Nizza 52, 10126 Turin, Italy

Received 7 November 2014; Accepted 3 December 2014

Academic Editor: Akito Maeshima

Copyright © 2015 Fanny Oliveira Arcolino et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. B. Dekel and Y. Reisner, “Engraftment of human early kidney precursors,” Transplant Immunology, vol. 12, no. 3-4, pp. 241–247, 2004. View at Publisher · View at Google Scholar · View at Scopus
  2. L. F. Prescott, “The normal urinary excretion rates of renal tubular cells, leucocytes and red blood cells,” Clinical Science, vol. 31, no. 3, pp. 425–435, 1966. View at Google Scholar · View at Scopus
  3. A. Dörrenhaus, J. I. F. Müller, K. Golka, P. Jedrusik, H. Schulze, and W. Föllmann, “Cultures of exfoliated epithelial cells from different locations of the human urinary tract and the renal tubular system,” Archives of Toxicology, vol. 74, no. 10, pp. 618–626, 2000. View at Publisher · View at Google Scholar · View at Scopus
  4. K. Sabin and N. Kikyo, “Microvesicles as mediators of tissue regeneration,” Translational Research, vol. 163, no. 4, pp. 286–295, 2014. View at Publisher · View at Google Scholar · View at Scopus
  5. A. Greka and P. Mundel, “Cell biology and pathology of podocytes,” Annual Review of Physiology, vol. 74, pp. 299–323, 2012. View at Publisher · View at Google Scholar · View at Scopus
  6. H. Burlington and E. P. Cronkite, “Characteristics of cell cultures derived from renal glomeruli,” Proceedings of the Society for Experimental Biology and Medicine, vol. 142, no. 1, pp. 143–149, 1973. View at Publisher · View at Google Scholar · View at Scopus
  7. R. J. Quigg, A. V. Cybulsky, J. B. Jacobs, and D. J. Salant, “Anti-Fx1A produces complement-dependent cytotoxicity of glomerular epithelial cells,” Kidney International, vol. 34, no. 1, pp. 43–52, 1988. View at Publisher · View at Google Scholar · View at Scopus
  8. P. Mundel, J. Reiser, and W. Kriz, “Induction of differentiation in cultured rat and human podocytes,” Journal of the American Society of Nephrology, vol. 8, no. 5, pp. 697–705, 1997. View at Google Scholar · View at Scopus
  9. T. Nakamura, C. Ushiyama, S. Suzuki et al., “Urinary podocytes for the assessment of disease activity in lupus nephritis,” The American Journal of the Medical Sciences, vol. 320, no. 2, pp. 112–116, 2000. View at Publisher · View at Google Scholar · View at Scopus
  10. M. Hara, T. Yanagihara, T. Takada et al., “Urinary excretion of podocytes reflects disease activity in children with glomerulonephritis,” The American Journal of Nephrology, vol. 18, no. 1, pp. 35–41, 1998. View at Publisher · View at Google Scholar · View at Scopus
  11. M. Hara, T. Yanagihara, and I. Kihara, “Urinary podocytes in primary focal segmental glomerulosclerosis,” Nephron, vol. 89, no. 3, pp. 342–347, 2001. View at Publisher · View at Google Scholar · View at Scopus
  12. Y. Sato, B. L. Wharram, K. L. Sang et al., “Urine podocyte mRNAs mark progression of renal disease,” Journal of the American Society of Nephrology, vol. 20, no. 5, pp. 1041–1052, 2009. View at Publisher · View at Google Scholar · View at Scopus
  13. A. L. Al-Malki, “Assessment of urinary osteopontin in association with podocyte for early predication of nephropathy in diabetic patients,” Disease Markers, vol. 2014, Article ID 493736, 5 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  14. S. U. Vogelmann, W. J. Nelson, B. D. Myers, and K. V. Lemley, “Urinary excretion of viable podocytes in health and renal disease,” American Journal of Physiology: Renal Physiology, vol. 285, no. 1, pp. F40–F48, 2003. View at Google Scholar · View at Scopus
  15. J. J. Bollain-Y-Goytia, M. González-Castañeda, F. Torres-Del-Muro et al., “Increased excretion of urinary podocytes in lupus nephritis,” Indian Journal of Nephrology, vol. 21, no. 3, pp. 166–171, 2011. View at Publisher · View at Google Scholar · View at Scopus
  16. T. Nakamura, C. Ushiyama, N. Shimada et al., “Effect of cyclophosphamide or azathioprine on urinary podocytes in patients with diffuse proliferative lupus nephritis,” Nephron, vol. 87, no. 2, pp. 192–193, 2001. View at Publisher · View at Google Scholar · View at Scopus
  17. T. Nakamura, C. Ushiyama, S. Suzuki et al., “Urinary excretion of podocytes in patients with diabetic nephropathy,” Nephrology Dialysis Transplantation, vol. 15, no. 9, pp. 1379–1383, 2000. View at Publisher · View at Google Scholar · View at Scopus
  18. V. D. Garovic, S. J. Wagner, S. T. Turner et al., “Urinary podocyte excretion as a marker for preeclampsia,” American Journal of Obstetrics & Gynecology, vol. 196, no. 4, pp. 320.e1–320.e7, 2007. View at Publisher · View at Google Scholar · View at Scopus
  19. D. Yu, A. Petermann, U. Kunter, S. Rong, S. J. Shankland, and J. Floege, “Urinary podocyte loss is a more specific marker of ongoing glomerular damage than proteinuria,” Journal of the American Society of Nephrology, vol. 16, no. 6, pp. 1733–1741, 2005. View at Publisher · View at Google Scholar · View at Scopus
  20. L. Ni, M. Saleem, and P. W. Mathieson, “Podocyte culture: tricks of the trade,” Nephrology, vol. 17, no. 6, pp. 525–531, 2012. View at Publisher · View at Google Scholar · View at Scopus
  21. M. A. Saleem, M. J. O'Hare, J. Reiser et al., “A conditionally immortalized human podocyte cell line demonstrating nephrin and podocin expression,” Journal of the American Society of Nephrology, vol. 13, no. 3, pp. 630–638, 2002. View at Google Scholar · View at Scopus
  22. T. Sakairi, Y. Abe, H. Kajiyama et al., “Conditionally immortalized human podocyte cell lines established from urine,” The American Journal of Physiology—Renal Physiology, vol. 298, no. 3, pp. F557–F567, 2010. View at Publisher · View at Google Scholar · View at Scopus
  23. K. Peeters, M. J. Wilmer, J. P. Schoeber et al., “Role of P-glycoprotein expression and function in cystinotic renal proximal tubular cells,” Pharmaceutics, vol. 3, no. 4, pp. 782–792, 2011. View at Publisher · View at Google Scholar · View at Scopus
  24. L. C. Racusen, B. A. Fivush, H. Andersson, and W. A. Gahl, “Culture of renal tubular cells from the urine of patients with nephropathic cystinosis,” Journal of the American Society of Nephrology, vol. 1, no. 8, pp. 1028–1033, 1991. View at Google Scholar · View at Scopus
  25. C. N. Inoue, N. Sunagawa, T. Morimoto et al., “Reconstruction of tubular structures in three-dimensional collagen gel culture using proximal tubular epithelial cells voided in human urine,” In Vitro Cellular & Developmental Biology—Animal, vol. 39, no. 8-9, pp. 364–367, 2003. View at Publisher · View at Google Scholar · View at Scopus
  26. K. L. Price, S.-A. Hulton, W. G. van'T Hoff, J. R. Masters, and G. Rumsby, “Primary cultures of renal proximal tubule cells derived from individuals with primary hyperoxaluria,” Urological Research, vol. 37, no. 3, pp. 127–132, 2009. View at Publisher · View at Google Scholar · View at Scopus
  27. L. C. Racusen, P. D. Wilson, P. A. Hartz, B. A. Fivush, C. R. Burrow, and E. T. Philip, “Renal proximal tubular epithelium from patients with nephropathic cystinosis: immortalized cell lines as in vitro model systems,” Kidney International, vol. 48, no. 2, pp. 536–543, 1995. View at Publisher · View at Google Scholar · View at Scopus
  28. M. J. Wilmer, M. A. Saleem, R. Masereeuw et al., “Novel conditionally immortalized human proximal tubule cell line expressing functional influx and efflux transporters,” Cell and Tissue Research, vol. 339, no. 2, pp. 449–457, 2010. View at Publisher · View at Google Scholar · View at Scopus
  29. C. M. Gorvin, M. J. Wilmer, S. E. Piret et al., “Receptor-mediated endocytosis and endosomal acidification is impaired in proximal tubule epithelial cells of Dent disease patients,” Proceedings of the National Academy of Sciences of the United States of America, vol. 110, no. 17, pp. 7014–7019, 2013. View at Publisher · View at Google Scholar · View at Scopus
  30. J. Jansen, C. M. S. Schophuizen, M. J. Wilmer et al., “A morphological and functional comparison of proximal tubule cell lines established from human urine and kidney tissue,” Experimental Cell Research, vol. 323, no. 1, pp. 87–99, 2014. View at Publisher · View at Google Scholar · View at Scopus
  31. H. D. Humes, W. F. Weitzel, R. H. Bartlett et al., “Initial clinical results of the bioartificial kidney containing human cells in ICU patients with acute renal failure,” Kidney International, vol. 66, no. 4, pp. 1578–1588, 2004. View at Publisher · View at Google Scholar · View at Scopus
  32. J. Tumlin, R. Wali, W. Williams et al., “Efficacy and safety of renal tubule cell therapy for acute renal failure,” Journal of the American Society of Nephrology, vol. 19, no. 5, pp. 1034–1040, 2008. View at Publisher · View at Google Scholar · View at Scopus
  33. S. Boyle, A. Misfeldt, K. J. Chandler et al., “Fate mapping using Cited1-CreERT2 mice demonstrates that the cap mesenchyme contains self-renewing progenitor cells and gives rise exclusively to nephronic epithelia,” Developmental Biology, vol. 313, no. 1, pp. 234–245, 2008. View at Publisher · View at Google Scholar · View at Scopus
  34. M. Self, O. V. Lagutin, B. Bowling et al., “Six2 is required for suppression of nephrogenesis and progenitor renewal in the developing kidney,” The EMBO Journal, vol. 25, no. 21, pp. 5214–5228, 2006. View at Publisher · View at Google Scholar · View at Scopus
  35. S. Metsuyanim, O. Harari-Steinberg, E. Buzhor et al., “Expression of stem cell markers in the human fetal kidney,” PLoS ONE, vol. 4, no. 8, Article ID e6709, 2009. View at Publisher · View at Google Scholar · View at Scopus
  36. M. A. Underwood, W. M. Gilbert, and M. P. Sherman, “Amniotic fluid: not just fetal urine anymore,” Journal of Perinatology, vol. 25, no. 5, pp. 341–348, 2005. View at Publisher · View at Google Scholar · View at Scopus
  37. S. Da Sacco, S. Sedrakyan, F. Boldrin et al., “Human amniotic fluid as a potential new source of organ specific precursor cells for future regenerative medicine applications,” The Journal of Urology, vol. 183, no. 3, pp. 1193–1200, 2010. View at Publisher · View at Google Scholar · View at Scopus
  38. S. da Sacco, K. V. Lemley, S. Sedrakyan et al., “A novel source of cultured podocytes,” PLoS ONE, vol. 8, no. 12, Article ID e81812, 2013. View at Publisher · View at Google Scholar · View at Scopus
  39. B. Bussolati, S. Bruno, C. Grange et al., “Isolation of renal progenitor cells from adult human kidney,” The American Journal of Pathology, vol. 166, no. 2, pp. 545–555, 2005. View at Publisher · View at Google Scholar · View at Scopus
  40. C. Sagrinati, G. S. Netti, B. Mazzinghi et al., “Isolation and characterization of multipotent progenitor cells from the Bowman's capsule of adult human kidneys,” Journal of the American Society of Nephrology, vol. 17, no. 9, pp. 2443–2456, 2006. View at Publisher · View at Google Scholar · View at Scopus
  41. B. Bussolati, A. Moggio, F. Collino et al., “Hypoxia modulates the undifferentiated phenotype of human renal inner medullary CD133+ progenitors through Oct4/miR-145 balance,” The American Journal of Physiology—Renal Physiology, vol. 302, no. 1, pp. 116–128, 2012. View at Publisher · View at Google Scholar · View at Scopus
  42. Y. Zhang, E. McNeill, H. Tian et al., “Urine derived cells are a potential source for urological tissue reconstruction,” The Journal of Urology, vol. 180, no. 5, pp. 2226–2233, 2008. View at Publisher · View at Google Scholar · View at Scopus
  43. S. Bharadwaj, G. Liu, Y. Shi et al., “Characterization of urine-derived stem cells obtained from upper urinary tract for use in cell-based urological tissue engineering,” Tissue Engineering Part A, vol. 17, no. 15-16, pp. 2123–2132, 2011. View at Publisher · View at Google Scholar · View at Scopus
  44. B. D. Humphreys, S. Czerniak, D. P. DiRocco, W. Hasnain, R. Cheema, and J. V. Bonventre, “Repair of injured proximal tubule does not involve specialized progenitors,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 22, pp. 9226–9231, 2011. View at Publisher · View at Google Scholar · View at Scopus
  45. T. Kusaba, M. Lalli, R. Kramann, A. Kobayashi, and B. D. Humphreys, “Differentiated kidney epithelial cells repair injured proximal tubule,” Proceedings of the National Academy of Sciences of the United States of America, vol. 111, no. 4, pp. 1527–1532, 2014. View at Publisher · View at Google Scholar · View at Scopus
  46. J. W. Pippin, M. A. Sparks, S. T. Glenn et al., “Cells of renin lineage are progenitors of podocytes and parietal epithelial cells in experimental glomerular disease,” The American Journal of Pathology, vol. 183, no. 2, pp. 542–557, 2013. View at Publisher · View at Google Scholar · View at Scopus
  47. E. Ronconi, C. Sagrinati, M. L. Angelotti et al., “Regeneration of glomerular podocytes by human renal progenitors,” Journal of the American Society of Nephrology, vol. 20, no. 2, pp. 322–332, 2009. View at Publisher · View at Google Scholar · View at Scopus
  48. O. Harari-Steinberg, S. Metsuyanim, D. Omer et al., “Identification of human nephron progenitors capable of generation of kidney structures and functional repair of chronic renal disease,” EMBO Molecular Medicine, vol. 5, no. 10, pp. 1556–1568, 2013. View at Publisher · View at Google Scholar · View at Scopus
  49. M. L. Angelotti, E. Ronconi, L. Ballerini et al., “Characterization of renal progenitors committed toward tubular lineage and their regenerative potential in renal tubular injury,” Stem Cells, vol. 30, no. 8, pp. 1714–1725, 2012. View at Publisher · View at Google Scholar · View at Scopus
  50. G. Liu, X. Wang, X. Sun, C. Deng, A. Atala, and Y. Zhang, “The effect of urine-derived stem cells expressing VEGF loaded in collagen hydrogels on myogenesis and innervation following after subcutaneous implantation in nude mice,” Biomaterials, vol. 34, no. 34, pp. 8617–8629, 2013. View at Publisher · View at Google Scholar · View at Scopus
  51. S. Wu, Y. Liu, S. Bharadwaj, A. Atala, and Y. Zhang, “Human urine-derived stem cells seeded in a modified 3D porous small intestinal submucosa scaffold for urethral tissue engineering,” Biomaterials, vol. 32, no. 5, pp. 1317–1326, 2011. View at Publisher · View at Google Scholar · View at Scopus
  52. L. Biancone, S. Bruno, M. C. Deregibus, C. Tetta, and G. Camussi, “Therapeutic potential of mesenchymal stem cell-derived microvesicles,” Nephrology Dialysis Transplantation, vol. 27, no. 8, pp. 3037–3042, 2012. View at Publisher · View at Google Scholar · View at Scopus
  53. F. T. Borges, L. A. Reis, and N. Schor, “Extracellular vesicles: structure, function, and potential clinical uses in renal diseases,” Brazilian Journal of Medical and Biological Research, vol. 46, no. 10, pp. 824–830, 2013. View at Publisher · View at Google Scholar · View at Scopus
  54. G. Camussi, M.-C. Deregibus, S. Bruno, C. Grange, V. Fonsato, and C. Tetta, “Exosome/microvesicle-mediated epigenetic reprogramming of cells,” American Journal of Cancer Research, vol. 1, no. 1, pp. 98–110, 2011. View at Google Scholar
  55. J. M. Street, W. Birkhoff, R. I. Menzies, D. J. Webb, M. A. Bailey, and J. W. Dear, “Exosomal transmission of functional aquaporin 2 in kidney cortical collecting duct cells,” The Journal of Physiology, vol. 589, part 24, pp. 6119–6127, 2011. View at Publisher · View at Google Scholar · View at Scopus
  56. J. J. Gildea, J. E. Seaton, K. G. Victor et al., “Exosomal transfer from human renal proximal tubule cells to distal tubule and collecting duct cells,” Clinical Biochemistry, vol. 47, no. 15, pp. 89–94, 2014. View at Publisher · View at Google Scholar
  57. V. Dimuccio, A. Ranghino, L. P. Barbato et al., “Urinary CD133+ extracellular vesicles are decreased in kidney transplanted patients with slow graft function and vascular damage,” PloS ONE, vol. 9, no. 8, Article ID e104490, 2014. View at Google Scholar
  58. S. Bruno, C. Grange, F. Collino et al., “Microvesicles derived from mesenchymal stem cells enhance survival in a lethal model of acute kidney injury,” PLoS ONE, vol. 7, no. 3, Article ID e33115, 2012. View at Publisher · View at Google Scholar · View at Scopus
  59. S. Bruno, C. Grange, M. C. Deregibus et al., “Mesenchymal stem cell-derived microvesicles protect against acute tubular injury,” Journal of the American Society of Nephrology, vol. 20, no. 5, pp. 1053–1067, 2009. View at Publisher · View at Google Scholar · View at Scopus
  60. S. Gatti, S. Bruno, M. C. Deregibus et al., “Microvesicles derived from human adult mesenchymal stem cells protect against ischaemia-reperfusion-induced acute and chronic kidney injury,” Nephrology Dialysis Transplantation, vol. 26, no. 5, pp. 1474–1483, 2011. View at Publisher · View at Google Scholar · View at Scopus
  61. A. T. Petermann, R. Krofft, M. Blonski et al., “Podocytes that detach in experimental membranous nephropathy are viable,” Kidney International, vol. 64, no. 4, pp. 1222–1231, 2003. View at Publisher · View at Google Scholar · View at Scopus
  62. L. de Petris, J. Patrick, E. Christen, and H. Trachtman, “Urinary podocyte mRNA excretion in children with D+HUS: a potential marker of long-term outcome,” Renal Failure, vol. 28, no. 6, pp. 475–482, 2006. View at Publisher · View at Google Scholar · View at Scopus
  63. Y. Ikezumi, T. Suzuki, T. Karasawa et al., “Glomerular epithelial cell phenotype in diffuse mesangial sclerosis: a report of 2 cases with markedly increased urinary podocyte excretion,” Human Pathology, vol. 45, no. 8, pp. 1778–1783, 2014. View at Publisher · View at Google Scholar
  64. J. Eyre, K. Ioannou, B. D. Grubb et al., “Statin-sensitive endocytosis of albumin by glomerular podocytes,” American Journal of Physiology: Renal Physiology, vol. 292, no. 2, pp. F674–F681, 2007. View at Publisher · View at Google Scholar · View at Scopus
  65. E. Dobrinskikh, K. Okamura, J. B. Kopp, R. B. Doctor, and J. Blaine, “Human podocytes perform polarized, caveolae-dependent albumin endocytosis,” American Journal of Physiology—Renal Physiology, vol. 306, no. 9, pp. F941–F951, 2014. View at Publisher · View at Google Scholar · View at Scopus
  66. L. C. Racusen, B. A. Fivush, Y.-L. Li et al., “Dissociation of tubular cell detachment and tubular cell death in clinical and experimental “acute tubular necrosis”,” Laboratory Investigation, vol. 64, no. 4, pp. 546–556, 1991. View at Google Scholar · View at Scopus
  67. C. J. Detrisac, R. K. Mayfield, J. A. Colwell, A. J. Garvin, and D. A. Sens, “In vitro culture of cells exfoliated in the urine by patents with diabetes mellitus,” Journal of Clinical Investigation, vol. 71, no. 1, pp. 170–173, 1983. View at Publisher · View at Google Scholar · View at Scopus
  68. M. Vicinanza, A. Di Campli, E. Polishchuk et al., “OCRL controls trafficking through early endosomes via PtdIns4,5P 2-dependent regulation of endosomal actin,” The EMBO Journal, vol. 30, no. 24, pp. 4970–4985, 2011. View at Publisher · View at Google Scholar · View at Scopus
  69. C. N. Inoue, Y. Kondo, S. Ohnuma, T. Morimoto, T. Nishio, and K. Iinuma, “Use of cultured tubular cells isolated from human urine for investigation of renal transporter,” Clinical Nephrology, vol. 53, no. 2, pp. 90–98, 2000. View at Google Scholar
  70. R. Moghadasali, H. A. M. Mutsaers, M. Azarnia et al., “Mesenchymal stem cell-conditioned medium accelerates regeneration of human renal proximal tubule epithelial cells after gentamicin toxicity,” Experimental and Toxicologic Pathology, vol. 65, no. 5, pp. 595–600, 2013. View at Publisher · View at Google Scholar · View at Scopus
  71. S. Bharadwaj, G. Liu, Y. Shi et al., “Multipotential differentiation of human urine-derived stem cells: potential for therapeutic applications in urology,” Stem Cells, vol. 31, no. 9, pp. 1840–1856, 2013. View at Publisher · View at Google Scholar · View at Scopus
  72. R. Lang, G. Liu, Y. Shi et al., “Self-renewal and differentiation capacity of urine-derived stem cells after urine preservation for 24 hours,” PLoS ONE, vol. 8, no. 1, Article ID e53980, 2013. View at Publisher · View at Google Scholar · View at Scopus
  73. E. Lazzeri, C. Crescioli, E. Ronconi et al., “Regenerative potential of embryonic renal multipotent progenitors in acute renal failure,” Journal of the American Society of Nephrology, vol. 18, no. 12, pp. 3128–3138, 2007. View at Publisher · View at Google Scholar · View at Scopus
  74. S. Wu, Z. Wang, S. Bharadwaj, S. J. Hodges, A. Atala, and Y. Zhang, “Implantation of autologous urine derived stem cells expressing vascular endothelial growth factor for potential use in genitourinary reconstruction,” The Journal of Urology, vol. 186, no. 2, pp. 640–647, 2011. View at Publisher · View at Google Scholar · View at Scopus
  75. A. Bodin, S. Bharadwaj, S. Wu, P. Gatenholm, A. Atala, and Y. Zhang, “Tissue-engineered conduit using urine-derived stem cells seeded bacterial cellulose polymer in urinary reconstruction and diversion,” Biomaterials, vol. 31, no. 34, pp. 8889–8901, 2010. View at Publisher · View at Google Scholar · View at Scopus
  76. B. Ouyang, X. Sun, D. Han et al., “Human urine-derived stem cells alone or genetically-modified with FGF2 improve type 2 diabetic erectile dysfunction in a rat model,” PLoS ONE, vol. 9, no. 3, Article ID e92825, 2014. View at Publisher · View at Google Scholar · View at Scopus
  77. W. Chen, M. Xie, B. Yang et al., “Skeletal myogenic differentiation of human urine-derived cells as a potential source for skeletal muscle regeneration,” Journal of Tissue Engineering and Regenerative Medicine, 2014. View at Publisher · View at Google Scholar
  78. G. Liu, R. A. Pareta, R. Wu et al., “Skeletal myogenic differentiation of urine-derived stem cells and angiogenesis using microbeads loaded with growth factors,” Biomaterials, vol. 34, no. 4, pp. 1311–1326, 2013. View at Publisher · View at Google Scholar · View at Scopus
  79. J. J. Guan, X. Niu, F. X. Gong et al., “Biological characteristics of human-urine-derived stem cells: potential for cell-based therapy in neurology,” Tissue Engineering Part A, vol. 20, no. 13-14, pp. 1794–1806, 2014. View at Publisher · View at Google Scholar
  80. H. Zhou, A. Cheruvanky, X. Hu et al., “Urinary exosomal transcription factors, a new class of biomarkers for renal disease,” Kidney International, vol. 74, no. 5, pp. 613–621, 2008. View at Publisher · View at Google Scholar · View at Scopus
  81. S. Keller, C. Rupp, A. Stoeck et al., “CD24 is a marker of exosomes secreted into urine and amniotic fluid,” Kidney International, vol. 72, no. 9, pp. 1095–1102, 2007. View at Publisher · View at Google Scholar · View at Scopus
  82. M. C. Hogan, K. L. Johnson, R. M. Zenka et al., “Subfractionation, characterization, and in-depth proteomic analysis of glomerular membrane vesicles in human urine,” Kidney International, vol. 85, no. 5, pp. 1225–1237, 2014. View at Publisher · View at Google Scholar · View at Scopus
  83. T. Pisitkun, R.-F. Shen, and M. A. Knepper, “Identification and proteomic profiling of exosomes in human urine,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 36, pp. 13368–13373, 2004. View at Publisher · View at Google Scholar · View at Scopus
  84. P. A. Gonzales, T. Pisitkun, J. D. Hoffert et al., “Large-scale proteomics and phosphoproteomics of urinary exosomes,” Journal of the American Society of Nephrology, vol. 20, no. 2, pp. 363–379, 2009. View at Publisher · View at Google Scholar · View at Scopus