Concise review: Stem/progenitor cells for renal tissue repair: Current knowledge and perspectives

Stem Cells Translational Medicine

Volumn 2, Issue 12, 2013, Pages 1011-1019

  Aggarwal, Shikhar ^a   Moggio, Aldo ^a   Bussolati, Benedetta ^a  

^a UNIVERSITY OF TURIN   (Italy)

Author keywords

Kidney; Marrow stromal stem cells; Progenitor cells; Renal

Indexed keywords

CD133 ANTIGEN; CISPLATIN; GLYCEROL; MERCURIC CHLORIDE; SCATTER FACTOR; SOMATOMEDIN; VASCULOTROPIN;

ACUTE KIDNEY FAILURE; ADIPOSE TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BIOLUMINESCENCE; BLASTOCYST; CELL THERAPY; CYTOPLASM; EMBRYONIC STEM CELL; HUMAN; KIDNEY ALLOGRAFT REJECTION; KIDNEY FIBROSIS; KIDNEY FUNCTION; KIDNEY PARENCHYMA; KIDNEY REGENERATION; KIDNEY TUBULE CELL; MESENCHYMAL STEM CELL; NEPHRECTOMY; NONHUMAN; PARACRINE SIGNALING; PERICYTE; PLURIPOTENT STEM CELL; REGENERATION; REPERFUSION INJURY; STEM CELL; TISSUE REPAIR;

RODENTIA;

EID: 84888415820     PISSN: 21576564     EISSN: 21576580     Source Type: Journal    
DOI: 10.5966/sctm.2013-0097     Document Type: Article

References (97)

1. Hass R, Kasper C, Böhm S et al. Different populations and sources of human mesenchymal stem cells (MSC): A comparison of adult and neonatal tissue-derived MSC. Cell Commun Signal 2011;9:12.
2. Chamberlain G, Fox J, Ashton B et al. Concise review: Mesenchymal stem cells: Their phenotype, differentiation capacity, immunological features, and potential for homing. STEM CELLS 2007;25:2739-2749.
3. Herrera MB, Bussolati B, Bruno S et al. Mesenchymal stem cells contribute to the renal repair of acute tubular epithelial injury. Int J Mol Med 2004;14:1035-1041.
4. Morigi M, Imberti B, Zoja C et al. Mesenchymal stem cells are renotropic, helping to repair the kidney and improve function in acute renal failure. J Am Soc Nephrol 2004;15:1794-1804.
5. Morigi M, Introna M, Imberti B et al. Human bone marrow mesenchymal stem cells accelerate recovery of acute renal injury and prolong survival in mice. STEM CELLS 2008;26: 2075-2082.
6. Lange C, Tögel F, Ittrich H et al. Administered mesenchymal stem cells enhance recovery from ischemia/reperfusion-induced acute renal failure in rats. Kidney Int 2005;68:1613-1617.
7. Morigi M, Rota C, Montemurro T et al. Life-sparing effect of human cord blood-mesenchymal stem cells in experimental acute kidney injury. STEM CELLS 2010;28:513-522.
8. Panepucci RA, Siufi JL, Silva WA Jr. et al. Comparison of gene expression of umbilical cord vein and bone marrow-derived mesenchymal stem cells. STEM CELLS 2004;22:1263-1278.
9. Hauser PV, De Fazio R, Bruno S et al. Stem cells derived from human amniotic fluid contribute to acute kidney injury recovery. Am J Pathol 2010;177:2011-2021.
10. Brunswig-Spickenheier B, Boche J, Westenfelder C et al. Limited immune-modulating activity of porcine mesenchymal stromal cells abolishes their protective efficacy in acute kidney injury. Stem Cells Dev 2010;19:719-729.
11. Choi S, Park M, Kim J et al. The role of mesenchymal stem cells in the functional improvement of chronic renal failure. Stem Cells Dev 2009;18:521-529.
12. Asanuma H, Vanderbrink BA, Campbell MT et al. Arterially delivered mesenchymal stem cells prevent obstruction-induced renal fibrosis. J Surg Res 2011;168:e51-e59.
13. Eirin A, Zhu XY, Krier JD et al. Adipose tissue-derived mesenchymal stem cells improve evascularization outcomes to restore renal function in swine atherosclerotic renal artery stenosis. STEM CELLS 2012;30:1030-1041.
14. Franquesa M, Herrero E, Torras J et al. Mesenchymal stem cell therapy prevents interstitial fibrosis and tubular atrophy in a rat kidney allograft model. Stem Cells Dev 2012; 21:3125-3135.
15. Quimby JM, Webb TL, Habenicht LM et al. Safety and efficacy of intravenous infusion of allogeneic cryopreserved mesenchymal stem cells for treatment of chronic kidney disease in cats: Results of three sequential pilot studies. Stem Cell Res Ther 2013;4:48.
16. Kramann R, Couson SK, Neuss S et al. Exposure to uremic serum induces a procalcific phenotype in human mesenchymal stem cells. Arterioscler Thromb Vasc Biol 2011;31:e45-e54.
17. Kramann R, Couson SK, Neuss S et al. Uraemia disrupts the vascular niche in a 3D coculture system of human mesenchymal stem cells and endothelial cells. Nephrol Dial Transplant 2012;27:2693-2702.
18. Reinders ME, Roemeling-van Rhijn M, Khairoun M et al. Bone marrow-derived mesenchymal stromal cells from patients with endstage renal disease are suitable for autologous therapy. Cytotherapy 2013;15:663-672.
19. Roemeling-van Rhijn M, Reinders ME, de Klein A et al. Mesenchymal stem cells derived from adipose tissue are not affected by renal disease. Kidney Int 2012;82:748-758.
20. Villanueva S, Carreno JE, Salazar L et al. Human mesenchymal stem cells derived from adipose tissue reduce functional and tissue damage in a rat model of chronic renal failure. Clin Sci 2013;125:199-210.
21. Gao J, Dennis JE, Muzic RF et al. The dynamic in vivo distribution of bone marrow-derived mesenchymal stem cells after infusion. Cells Tissues Organs 2001;169:12-20.
22. Furlani D, Ugurlucan M, Ong L et al. Is the intravascular administration of mesenchymal stem cells safe? Mesenchymal stem cells and intravital microscopy. Microvasc Res 2009;77: 370-376.
23. Caldas HC, Fernandes IM, Gerbi F et al. Effect of whole bone marrow cell infusion in the progression of experimental chronic renal failure. Transplant Proc 2008;40:853-855.
24. Cavaglieri RC, Martini D, Sogayar MC et al. Mesenchymal stem cells delivered at the subcapsule of the kidney ameliorate renal disease in the rat remnant kidney model. Transplant Proc 2009;41:947-951.
25. Zhuo W, Liao L, Fu Y et al. Efficiency of endovenous versus arterial administration of mesenchymal stem cells for ischemia-reperfusion-induced renal dysfunction in rats. Transplant Proc 2013;45:503-510.
26. Wang Y, He J, Pei X et al. Systematic review and meta-analysis of mesenchymal stem/ stromal cells therapy for impaired renal function in small animal models. Nephrology 2013; 18:201-208.
27. Gnecchi M, Zhang Z, Ni A et al. Paracrine mechanisms in adult stem cell signaling and therapy. Circ Res 2008;103:1204-1219.
28. Nauta AJ, Fibbe WE. Immunomodulatory properties of mesenchymal stromal cells. Blood 2007;110:3499-3506.
29. Tögel FE, Westenfelder C. Mesenchymal stem cells: A new therapeutic tool for AKI. Nat Rev Nephrol 2010;6:179-183.
30. Perico N, Casiraghi F, Introna M et al. Autologous mesenchymal stromal cells and kidney transplantation: A pilot study of safety and clinical feasibility. Clin J Am Soc Nephrol 2011;6:412-422.
31. Tan J, WuW, Xu X et al. Induction therapy with autologous mesenchymal stem cells in living-related kidney transplants: A randomized controlled trial. JAMA 2012;307:1169-1177.
32. Casiraghi F, Perico N, Remuzzi G. Mesenchymal stromal cells to promote solid organ transplantation tolerance. Curr Opin Organ Transplant 2013;18:51-58.
33. Reinders ME, de Fijter JW, Roelofs H et al. Autologous bone marrow-derived mesenchymal stromal cells for the treatment of allograft rejection after renal transplantation: Results of a phase I study. STEM CELLS TRANSLATIONAL MEDICINE 2013;2:107-111.
34. Imberti B, Morigi M, Tomasoni S et al. Insulin-like growth factor-1 sustains stem cell mediated renal repair. J Am Soc Nephrol 2007; 18:2921-2928.
35. Bi B, Schmitt R, IsrailovaMet al. Stromal cells protect against acute tubular injury via an endocrine effect. J Am Soc Nephrol 2007;18: 2486-2496.
36. Eliopoulos N, Zhao J, Bouchentouf M et al. Human marrow-derived mesenchymal stromal cells decrease cisplatin renotoxicity in vitro and in vivo and enhance survival of mice postintraperitoneal injection. Am J Physiol Renal Physiol 2010;299:F1288-F1298.
37. Tögel F, Zhang P, Hu Z et al. VEGF is a mediator of the renoprotective effects of multipotent marrow stromal cells in acute kidney injury. J Cell Mol Med 2009;13:2109-2114.
38. György B, Szabó TG, Pásztói M et al. Membrane vesicles, current state-of-the-art: Emerging role of extracellular vesicles. Cell Mol Life Sci 2011;68:2667-2688.
39. Bruno S, Grange C, Deregibus MC et al. Mesenchymal stem cell-derived microvesicles protect against acute tubular injury. J Am Soc Nephrol 2009;20:1053-1067.
40. Bruno S, Grange C, Collino F et al. Microvesicles derived from mesenchymal stem cells enhance survival in a lethal model of acute kidney injury. PLoS One 2012;7:e33115.
41. Reis LA, Borges FT, Simoes MJ et al. Bone marrow-derived mesenchymal stem cells repaired but did not prevent gentamicin-induced acute kidney injury through paracrine effects in rats. PLoS One 2012;7:e44092.
42. Tomasoni S, Longaretti L, Rota C et al. Transfer of growth factor receptor mRNA via exosomes unravels the regenerative effect of mesenchymal stem cells. Stem Cells Dev 2013; 22:772-780.
43. Gatti S, Bruno S, Deregibus MC et al. Microvesicles derived from human adult mesenchymal stem cells protect against ischaemiareperfusion-induced acute and chronic kidney injury. Nephrol Dial Transplant 2011;26:1474-1483.
44. Del Tatto M, Ng T, Aliotta JM et al. Marrow cell genetic phenotype change induced by human lung cancer cells. Exp Hematol 2011;39: 1072-1080.
45. Chang JW, Tsai HL, Chen CW et al. Conditioned mesenchymal stem cells attenuate progression of chronic kidney disease through inhibition of epithelial-to-mesenchymal transition and immune modulation. J Cell Mol Med 2012; 16:2935-2949.
46. Costantini F, Kopan R. Patterning a complex organ: Branching morphogenesis and nephron segmentation in kidney development. Dev Cell 2010;18:698-712.
47. Kobayashi A, Valerius MT, Mugford JW et al. Six2 defines and regulates a multipotent self-renewing nephron progenitor population throughout mammalian kidney development. Cell Stem Cell 2008;3:169-181.
48. Hartman HA, Lai HL, Patterson. Cessation of renal morphogenesis in mice. Dev Biol 2007; 310:379-387.
49. Maeshima A, Yamashita S, Nojima Y. Identification of renal progenitor-like tubular cells that participate in the regeneration processes of the kidney. J Am Soc Nephrol 2003; 14:3138-3146.
50. Dekel B, Zangi L, Shezen E et al. Isolation and characterization of nontubular sca-1_linmultipotent stem/ progenitor cells from adult mouse kidney. J Am Soc Nephrol 2006;17: 3300-3314.
51. Kinomura M, Kitamura S, Tanabe K et al. Amelioration of cisplatin-induced acute renal injury by renal progenitor-like cells derived from the adult rat kidney. Cell Transplant 2008; 17:143-158.
52. Langworthy M, Zhou B, de CaesteckerM et al. NFATc1 identifies a population of proximal tubule cell progenitors. J Am Soc Nephrol 2009;20:311-321.
53. Oliver JA, Maarouf O, Cheema FH et al. The renal papilla is a niche for adult kidney stem cells. J Clin Invest 2004;114:795-804.
54. Maeshima A, Sakurai H, Nigam SK. Adult kidney tubular cell population showing phenotypic plasticity, tubulogenic capacity and integration capability into developing kidney. J Am Soc Nephrol 2006;17:188-198.
55. Humphreys BD, Czerniak S, DiRocco DP et al. Repair of injured proximal tubule does not involve specialized progenitors. Proc Natl Acad Sci USA 2011;108:9226-9231.
56. Bussolati B, Bruno S, Grange C et al. Isolation of renal progenitor cells from adult human kidney. Am J Pathol 2005;166:545-555.
57. Sagrinati C, Netti GS, Mazzinghi B et al. Isolation and characterization of multipotent progenitor cells from the Bowman's capsule of adult human kidneys. J Am Soc Nephrol 2006; 17:2443-2456.
58. Bussolati B, Moggio A, Collino F et al. Hypoxia modulates the undifferentiated phenotype of human renal inner medullary CD133_ progenitors through Oct4/miR-145 balance. Am J Physiol Renal Physiol 2012;302: F116-F128.
59. Loverre A, Capobianco C, Ditonno P et al. Increase of proliferating renal progenitor cells in acute tubular necrosis underlying delayed graft function. Transplantation 2008;85:1112-1119.
60. Smeets B, Boor P, Dijkman H et al. Proximal tubular cells contain a phenotypically distinct, scattered cell population involved in tubular regeneration. J Pathol 2013;229:645-659.
61. Bussolati B, Lauritano C, Moggio A et al. Renal CD133_/CD73_ progenitors produce erythropoietin under hypoxia and prolyl hydroxylase inhibition. J Am Soc Nephrol 2013; 24:1234-1241.
62. Ronconi E, Sagrinati C, Angelotti ML et al. Regeneration of glomerular podocytes by human renal progenitors. JAmSoc Nephrol 2009; 20:322-332.
63. Simone S, Cosola C, Loverre A et al. BMP-2 induces a profibrotic phenotype in adult renal progenitor cells through Nox4 activation. Am J Physiol Renal Physiol 2012;303: F23-F34.
64. Benigni A, Morigi M, Rizzo P et al. G inhibiting angiotensin-converting enzyme promotes renal repair by limiting progenitor cell proliferation and restoring the glomerular architecture. Am J Pathol 2011;179:628-638.
65. Crisan M, Yap S, Casteilla L et al. A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 2008; 3:301-313.
66. da Silva Meirelles L, Chagastelles PC, Nardi NB. Mesenchymal stem cells reside in virtually all post-natal organs and tissues. J Cell Sci 2006;119:2204-2213.
67. Bruno S, Bussolati B, Grange C et al. Isolation and characterization of resident mesenchymal stem cells in human glomeruli. Stem Cells Dev 2009;18:867-880.
68. Wang H, Gomez JA, Klein S et al. Mesenchymal stem cell-like cells contribute to juxtaglomerular cell recruitment. J Am Soc Nephrol 2013;24:1263-1273.
69. Pelekanos RA, Li J, GongoraMet al. Comprehensive transcriptome and immunophenotype analysis of renal and cardiac MSC-like populations supports strong congruence with bone marrow MSC despite maintenance of distinct identities. Stem Cell Res 2012;8:58-73.
70. Lanza RP, Chung HY, Yoo JJ et al. Generation of histocompatible tissues using nuclear transplantation. Nat Biotechnol 2002;20:689-696.
71. Rosines E, Sampogna RV, Johkura K et al. Staged in vitro reconstitution and implantation of engineered rat kidney tissue. Proc Natl Acad Sci USA 2007;104:20938-20943.
72. Rosines E, Johkura K, Zhang X et al. Constructing kidney-like tissues from cells based on programs for organ development: Toward a method of in vitro tissue engineering of the kidney. Tissue Eng Part A 2010;16:2441-2455.
73. Joraku A, Stern KA, Atala A et al. In vitro generation of three-dimensional renal structures. Methods 2009;47:129-133.
74. Xinaris C, Benedetti V, Rizzo P et al. In vivo maturation of functional renal organoids formed from embryonic cell suspensions. J Am Soc Nephrol 2012;23:1857-1868.
75. Unbekandt M, Davies JA. Dissociation of embryonic kidneys followed by reaggregation allows the formation of renal tissues. Kidney Int 2010;77:407-416.
76. Buzhor E, Harari-Steinberg O, Omer D et al. Kidney spheroids recapitulate tubular organoids leading to enhanced tubulogenic potency of human kidney-derived cells. Tissue Eng Part A 2011;17:2305-2319.
77. Ross EA, Williams MJ, Hamazaki T et al. Embryonic stem cells proliferate and differentiate when seeded into kidney scaffolds. J Am Soc Nephrol 2009;20:2338-2347.
78. Nakayama KH, Batchelder CA, Lee CI et al. Decellularized rhesus monkey kidney as a three-dimensional scaffold for renal tissue engineering. Tissue Eng Part A 2010;16:2207-2216.
79. Sullivan DC, Mirmalek-Sani SH, Deegan DB et al. Decellularization methods of porcine kidneys for whole organ engineering using a high-throughput system. Biomaterials 2012; 33:7756-7764.
80. Song JJ, Guyette JP, Gilpin SE et al. Regeneration and experimental orthotopic transplantation of a bioengineered kidney. Nat Med 2013;19:646-651.
81. Thomson JA, Itskovitz-Eldor J, Shapiro SS et al. Embryonic stem cell lines derived from human blastocysts. Science 1998;282:1145-1147.
82. Osafune K. In vitro regeneration of kidney from pluripotent stem cells. Exp Cell Res 2010;316:2571-2577.
83. Bruce SJ, Rea RW, Steptoe AL et al. In vitro differentiation of murine embryonic stem cells toward a renal lineage. Differentiation 2007;75:337-334.
84. Schuldiner M, Yanuka O, Itskovitz-Eldor J. Effects of eight growth factors on the differentiation of cells derived from human embryonic stem cells. Proc Natl Acad Sci USA 2000; 97:11307-11312.
85. Steenhard BM, Isom KS, Cazcarro P et al. Integration of embryonic stem cells in metanephric kidney organ culture. JAmSoc Nephrol 2005;16:1623-1631.
86. Vigneau C, Polgar K, Striker G et al. Mouse embryonic stem cell-derived embryoid bodies generate progenitors that integrate long term into renal proximal tubules in vivo. J Am Soc Nephrol 2007;18:1709-1720.
87. Kim D, Dressler GR. Nephrogenic factors promote differentiation of mouse embryonic stem cells into renal epithelia. J Am Soc Nephrol 2005;16:3527-3534.
88. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006;126:663-676.
89. Kim K, Doi A, Wen B et al. Epigenetic memory in induced pluripotent stem cells. Nature 2010;467:285-290.
90. Song B, Niclis JC, Alikhan MA et al. Generation of induced pluripotent stem cells from human kidney mesangial cells. J Am Soc Nephrol 2011;22:1213-1220.
91. Song B, Smink AM, Jones CV et al. The directed differentiation of human iPS cells into kidney podocytes. PLoS One 2012;7:e46453.
92. Montserrat N, Ramírez-Bajo MJ, Xia Y et al. Generation of induced pluripotent stem cells from human renal proximal tubular cells with only two transcription factors, OCT4 and SOX2. J Biol Chem 2012;287:24131-24138.
93. Wang WW, Wang W, Jiang Y et al. Reprogramming of mouse renal tubular epithelial cells to induced pluripotent stem cells. Cytotherapy 2013;15:578-585.
94. Zhou T, Benda C, Dunzinger S. Generation of human induced pluripotent stem cells from urine samples. Nat Protoc 2012;7:2080-2089.
95. Kobayashi T, Yamaguchi T, Hamanaka S et al. Generation of rat pancreas in mouse by interspecific blastocyst injection of pluripotent stem cells. Cell 2010;142:787-799.
96. Matsunari H, Nagashima H, WatanabeM et al. Blastocyst complementation generates exogenic pancreas in vivo in apancreatic cloned pigs. Proc Natl Acad Sci USA 2013;110: 4557-4562.
97. Usui J, Kobayashi T, Yamaguchi T et al. Generation of kidney from pluripotent stem cells via blastocyst complementation. Am J Pathol 2012;180:2417-2426.