Human urine as a noninvasive source of kidney cells

Stem Cells International

Volumn 2015, Issue , 2015, Pages

  Oliveira Arcolino, Fanny ^a   Tort Piella, Agnès ^b   Papadimitriou, Elli ^c   Bussolati, Benedetta ^c   Antonie, Daniel J ^b   Murray, Patricia ^b   Van Den Heuvel, Lamberthus ^a   Levtchenko, Elena ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b UNIVERSITY OF LIVERPOOL   (United Kingdom)

^c UNIVERSITY OF TURIN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; NEPHRIN; PODOCIN;

CELL DIFFERENTIATION; CELL VIABILITY; DISEASE COURSE; EXOSOME; GLOMERULAR FILTRATION BARRIER; GLOMERULUS BASEMENT MEMBRANE; HUMAN; HUMAN CELL; IN VIVO STUDY; KIDNEY CELL; KIDNEY INJURY; KIDNEY PROXIMAL TUBULE; KIDNEY STEM CELL; PODOCYTE; PRIORITY JOURNAL; REVIEW; STEM CELL; URINE;

EID: 84930684251     PISSN: None     EISSN: 16879678     Source Type: Journal    
DOI: 10.1155/2015/362562     Document Type: Review

References (84)

1. B. Dekel and Y. Reisner, "Engraftment of human early kidney precursors," Transplant Immunology, vol. 12, no. 3-4, pp. 241-247, 2004.
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.
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.
4. K. Sabin and N. Kikyo, "Microvesicles as mediators of tissue regeneration," Translational Research, vol. 163, no. 4, pp. 286-295, 2014.
5. A. Greka and P. Mundel, "Cell biology and pathology of podocytes," Annual Review of Physiology, vol. 74, pp. 299-323, 2012.
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.
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.
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.
9. T. Nakamura, C. Ushiyama, S. Suzuki et al., "Urinary podocytes for the assessment of disease activity in lupus nephritis," The AmericanJournal of theMedical Sciences, vol. 320, no. 2, pp. 112-116, 2000.
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.
11. M. Hara, T. Yanagihara, and I. Kihara, "Urinary podocytes in primary focal segmental glomerulosclerosis," Nephron, vol. 89, no. 3, pp. 342-347, 2001.
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.
13. A. L. Al-Malki, "Assessment of urinary osteopontin in association with podocyte for early predication of nephropathy in diabetic patients," DiseaseMarkers, vol. 2014, Article ID493736, 5 pages, 2014.
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.
15. J. J. Bollain-Y-Goytia, M. González-Castaneda, 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.
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.
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.
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.
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.
20. L. Ni,M. Saleem, and P. W. Mathieson, "Podocyte culture: tricks of the trade," Nephrology, vol. 17, no. 6, pp. 525-531, 2012.
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.
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.
23. K. Peeters, M. J. Wilmer, J. P. Schoeber et al., "Role of Pglycoprotein expression and function in cystinotic renal proximal tubular cells," Pharmaceutics, vol. 3, no. 4,pp. 782-792, 2011.
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.
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.
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.
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.
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.
29. C. M. Gorvin, M. J. Wilmer, S. E. Piret et al., "Receptormediated 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.
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.
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.
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.
33. S. Boyle, A. Misfeldt, K. J. Chandler et al., "Fatemapping 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.
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.
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.
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.
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.
38. S. da Sacco, K. V. Lemley, S. Sedrakyan et al., "A novel source of cultured podocytes," PLoS ONE, vol. 8, no. 12, Article IDe81812, 2013.
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.
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 theAmerican Society of Nephrology, vol. 17, no. 9, pp. 2443-2456, 2006.
41. B. Bussolati, A. Moggio, F. Collino et al., "Hypoxia modulates the undifferentiated phenotype of human renal inner medullary CD133+ progenitors throughOct4/miR-145 balance,"TheAmerican Journal of Physiology-Renal Physiology, vol. 302, no. 1, pp. 116-128, 2012.
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.
43. S. Bharadwaj, G. Liu, Y. Shi et al., "Characterization of urinederived 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.
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.
45. T. Kusaba, M. Lalli, R. Kramann, A. Kobayashi, and B. D. Humphreys, "Differentiated kidney epithelial cells repair injured proximal tubule," Proceedings of theNationalAcademy of Sciences of the United States of America, vol. 111, no. 4, pp. 1527-1532, 2014.
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.
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.
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.
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.
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.
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.
52. L. Biancone, S. Bruno, M. C. Deregibus, C. Tetta, and G. Camussi, "Therapeutic potential of mesenchymal stem cellderived microvesicles," Nephrology Dialysis Transplantation, vol. 27, no. 8, pp. 3037-3042, 2012.
53. F. T. Borges, L. A. Reis, and N. Schor, "Extracellular vesicles: structure, function, and potential clinical uses in renal diseases," Brazilian Journal ofMedical and Biological Research, vol. 46, no. 10, pp. 824-830, 2013.
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.
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.
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.
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.
58. S. Bruno, C. Grange, F. Collino et al., "Microvesicles derived frommesenchymal stem cells enhance survival in a lethalmodel of acute kidney injury," PLoSONE, vol. 7, no. 3,Article IDe33115, 2012.
59. S. Bruno, C. Grange,M. C. Deregibus et al., "Mesenchymal stem cell-derived microvesicles protect against acute tubular injury," Journal of theAmerican Society of Nephrology, vol. 20, no. 5, pp. 1053-1067, 2009.
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.
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.
62. L. de Petris, J. Patrick, E. Christen, and H. Trachtman, "Urinary podocytemRNAexcretion in childrenwithD+HUS: A potential marker of long-term outcome," Renal Failure, vol. 28, no. 6, pp. 475-482, 2006.
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.
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.
65. E. Dobrinskikh, K. Okamura, J. B. Kopp, R. B. Doctor, and J. Blaine, "Human podocytes perform polarized, caveolaedependent albumin endocytosis," American Journal of Physiology-Renal Physiology, vol. 306, no. 9, pp. F941-F951, 2014.
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.
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.
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.
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," ClinicalNephrology, vol. 53, no. 2, pp. 90-98, 2000.
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.
71. S. Bharadwaj, G. Liu, Y. Shi et al., "Multipotential differentiation of human urine-derived stem cells: potential for therapeutic applications in urology," StemCells, vol. 31, no. 9, pp. 1840-1856, 2013.
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.
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.
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.
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.
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 IDe92825, 2014.
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.
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.
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.
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.
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.
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.
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.
84. P. A. Gonzales, T. Pisitkun, J. D. Hoffert et al., "Large-scale proteomics and phosphoproteomics of urinary exosomes," Journal of the American Society ofNephrology, vol. 20,no. 2, pp. 363-379, 2009.