Mesenchymal stem cells as a therapeutic approach to glomerular diseases: Benefits and risks

Kidney International Supplements

Volumn 1, Issue 3, 2011, Pages 68-73

  Kunter, Uta ^a   Rong, Song ^a   Moeller, Marcus J ^a   Floege, Jürgen ^a  

^a RWTH AACHEN UNIVERSITY   (Germany)

Author keywords

cell based therapy; chronic kidney disease; glomerulonephritis; mesenchymal stem cell(s); progenitors; renal regeneration

Indexed keywords

EID: 84857638704     PISSN: 21571724     EISSN: 21571716     Source Type: Journal    
DOI: 10.1038/kisup.2011.16     Document Type: Review

References (87)

1. Kitamura S, Yamasaki Y, Kinomura M et al. Establishment and characterization of renal progenitor like cells from S3 segment of nephron in rat adult kidney. FASEB J 2005; 19: 1789-1797
2. Bussolati B, Bruno S, Grange C et al. Isolation of renal progenitor cells from adult human kidney. Am J Pathol 2005; 166: 545-555
3. 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
4. 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
5. Challen GA, Bertoncello I, Deane JA et al. Kidney side population reveals multilineage potential and renal functional capacity but also cellular heterogeneity. J Am Soc Nephrol 2006; 17: 1896-1912
6. Iwatani H, Ito T, Imai E et al. Hematopoietic and nonhematopoietic potentials of Hoechst(low)/side population cells isolated from adult rat kidney. Kidney Int 2004; 65: 1604-1614
7. 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
8. Dekel B, Zangi L, Shezen E et al. Isolation and characterization of nontubular sca-1+lin- multipotent stem/progenitor cells from adult mouse kidney. J Am Soc Nephrol 2006; 17: 3300-3314
9. Gupta S, Verfaillie C, Chmielewski D et al. Isolation and characterization of kidney-derived stem cells. J Am Soc Nephrol 2006; 17: 3028-3040
10. Oliver JA, Klinakis A, Cheema FH et al. Proliferation and migration of label-retaining cells of the kidney papilla. J Am Soc Nephrol 2009; 20: 2315-2327
11. Smeets B, Angelotti ML, Rizzo P et al. Renal progenitor cells contribute to hyperplastic lesions of podocytopathies and crescentic glomerulonephritis. J Am Soc Nephrol 2009; 20: 2593-2603
12. Son BR, Marquez-Curtis LA, Kucia M et al. Migration of bone marrow and cord blood mesenchymal stem cells in vitro is regulated by stromal-derived factor-1-CXCR4 and hepatocyte growth factor-c-met axes and involves matrix metalloproteinases. Stem Cells 2006; 24: 1254-1264
13. Rookmaaker MB, Verhaar MC, de Boer HC et al. Met-RANTES reduces endothelial progenitor cell homing to activated (glomerular) endothelium in vitro and in vivo. Am J Physiol Renal Physiol 2007; 293: F624-F630
14. Shi H, Patschan D, Dietz GP et al. Glial cell line-derived neurotrophic growth factor increases motility and survival of cultured mesenchymal stem cells and ameliorates acute kidney injury. Am J Physiol Renal Physiol 2008; 294: F229-F235
15. Herrera MB, Bussolati B, Bruno S et al. Exogenous mesenchymal stem cells localize to the kidney by means of CD44 following acute tubular injury. Kidney Int 2007; 72: 430-441
16. Stokman G, Leemans JC, Stroo I et al. Enhanced mobilization of bone marrow cells does not ameliorate renal fibrosis. Nephrol Dial Transplant 2008; 23: 483-491
17. Togel F, Isaac J, Westenfelder C. Hematopoietic stem cell mobilizationassociated granulocytosis severely worsens acute renal failure. J Am Soc Nephrol 2004; 15: 1261-1267
18. Krause D, Cantley LG. Bone marrow plasticity revisited: Protection or differentiation in the kidney tubule? J Clin Invest 2005; 115: 1705-1708
19. Kinnaird T, Stabile E, Burnett MS et al. Marrow-derived stromal cells express genes encoding a broad spectrum of arteriogenic cytokines and promote in vitro and in vivo arteriogenesis through paracrine mechanisms. Circ Res 2004; 94: 678-685
20. Caplan AI, Dennis JE. Mesenchymal stem cells as trophic mediators. J Cell Biochem 2006; 98: 1076-1084
21. Togel F, Hu Z, Weiss K et al. Administered mesenchymal stem cells protect against ischemic acute renal failure through differentiationindependent mechanisms. Am J Physiol Renal Physiol 2005; 289: F31-F42
22. Prockop DJ. 'Stemness' does not explain the repair of many tissues by mesenchymal stem/multipotent stromal cells (MSCs). Clin Pharmacol Ther 2007; 82: 241-243
23. Kinnaird T, Stabile E, Burnett MS et al. Local delivery of marrow-derived stromal cells augments collateral perfusion through paracrine mechanisms. Circulation 2004; 109: 1543-1549
24. Duffield JS, Bonventre JV. Kidney tubular epithelium is restored without replacement with bone marrow-derived cells during repair after ischemic injury. Kidney Int 2005; 68: 1956-1961
25. Duffield JS, Park KM, Hsiao LL et al. Restoration of tubular epithelial cells during repair of the postischemic kidney occurs independently of bone marrow-derived stem cells. J Clin Invest 2005; 115: 1743-1755
26. Bi B, Schmitt R, Israilova M et al. Stromal cells protect against acute tubular injury via an endocrine effect. J Am Soc Nephrol 2007; 18: 2486-2496
27. Hung SC, Pochampally RR, Chen SC et al. Angiogenic effects of human multipotent stromal cell conditioned medium activate the PI3K-Akt pathway in hypoxic endothelial cells to inhibit apoptosis, increase survival, and stimulate angiogenesis. Stem Cells 2007; 25: 2363-2370
28. Chen TS, Lai RC, Lee MM et al. Mesenchymal stem cell secretes microparticles enriched in pre-microRNAs. Nucleic Acids Res 2010; 38: 215-224
29. Cornacchia F, Fornoni A, Plati AR et al. Glomerulosclerosis is transmitted by bone marrow-derived mesangial cell progenitors. J Clin Invest 2001; 108: 1649-1656
30. Poulsom R, Forbes SJ, Hodivala-Dilke K et al. Bone marrow contributes to renal parenchymal turnover and regeneration. J Pathol 2001; 195: 229-235
31. Imasawa T, Utsunomiya Y, Kawamura T et al. The potential of bone marrow-derived cells to differentiate to glomerular mesangial cells. J Am Soc Nephrol 2001; 12: 1401-1409
32. Ito T, Suzuki A, Imai E et al. Bone marrow is a reservoir of repopulating mesangial cells during glomerular remodeling. J Am Soc Nephrol 2001; 12: 2625-2635
33. Rookmaaker MB, Smits AM, Tolboom H et al. Bone-marrow-derived cells contribute to glomerular endothelial repair in experimental glomerulonephritis. Am J Pathol 2003; 163: 553-562
34. Abe-Yoshio Y, Abe K, Miyazaki M et al. Involvement of bone marrowderived endothelial progenitor cells in glomerular capillary repair in habu snake venom-induced glomerulonephritis. Virchows Arch 2008; 453: 97-106
35. Suzuki A, Iwatani H, Ito T et al. Platelet-derived growth factor plays a critical role to convert bone marrow cells into glomerular mesangial-like cells. Kidney Int 2004; 65: 15-24
36. Alexandre CS, Volpini RA, Shimizu MH et al. Lineage-negative bone marrow cells protect against chronic renal failure. Stem Cells 2009; 27: 682-692
37. Nur R, Fukuda N, Matsumoto T et al. Implantation of dedifferentiated fat cells ameliorates habu snake venom-induced chronic renal dysfunction in tenascin-C-deficient mice. Nephron Exp Nephrol 2008; 110: E91-e98
38. 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
39. Wong CY, Cheong SK, Mok PL et al. Differentiation of human mesenchymal stem cells into mesangial cells in post-glomerular injury murine model. Pathology 2008; 40: 52-57
40. Magnasco A, Corselli M, Bertelli R et al. Mesenchymal stem cells protective effect in adriamycin model of nephropathy. Cell Transplant 2008; 17: 1157-1167
41. Horwitz EM, Le Blanc K, Dominici M et al. Clarification of the nomenclature for MSC: The International Society for Cellular Therapy position statement. Cytotherapy 2005; 7: 393-395
42. Dominici M, Le Blanc K, Mueller I et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006; 8: 315-317
43. Wagner W, Ho AD. Mesenchymal stem cell preparations - comparing apples and oranges. Stem Cell Rev 2007; 3: 239-248
44. Wagner W, Feldmann Jr RE, Seckinger A et al. The heterogeneity of human mesenchymal stem cell preparations - evidence from simultaneous analysis of proteomes and transcriptomes. Exp Hematol 2006; 34: 536-548
45. Wiese C, Rolletschek A, Kania G et al. Nestin expression - a property of multi-lineage progenitor cells? Cell Mol Life Sci 2004; 61: 2510-2522
46. Martinez C, Hofmann TJ, Marino R et al. Human bone marrow mesenchymal stromal cells express the neural ganglioside GD2: A novel surface marker for the identification of MSCs. Blood 2007; 109: 4245-4248
47. Buhring HJ, Battula VL, Treml S et al. Novel markers for the prospective isolation of human MSC. Ann NY Acad Sci 2007; 1106: 262-271
48. Le Blanc K, Pittenger M. Mesenchymal stem cells: Progress toward promise. Cytotherapy 2005; 7: 36-45
49. Tolar J, Nauta AJ, Osborn MJ et al. Sarcoma derived from cultured mesenchymal stem cells. Stem Cells 2007; 25: 371-379
50. Zhang ZX, Guan LX, Zhang K et al. Cytogenetic analysis of human bone marrow-derived mesenchymal stem cells passaged in vitro. Cell Biol Int 2007; 31: 645-648
51. 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
52. Lin F, Moran A, Igarashi P. Intrarenal cells, not bone marrow-derived cells, are the major source for regeneration in postischemic kidney. J Clin Invest 2005; 115: 1756-1764
53. Qian H, Yang H, Xu W et al. Bone marrow mesenchymal stem cells ameliorate rat acute renal failure by differentiation into renal tubular epithelial-like cells. Int J Mol Med 2008; 22: 325-332
54. Togel F, Cohen A, Zhang P et al. Autologous and allogeneic marrow stromal cells are safe and effective for the treatment of acute kidney injury. Stem Cells Dev 2009; 18: 475-485
55. Humphreys BD, Bonventre JV. Mesenchymal stem cells in acute kidney injury. Annu Rev Med 2008; 59: 311-325
56. McTaggart SJ, Atkinson K. Mesenchymal stem cells: Immunobiology and therapeutic potential in kidney disease. Nephrology (Carlton) 2007; 12: 44-52
57. Giordano A, Galderisi U, Marino IR. From the laboratory bench to the patient's bedside: An update on clinical trials with mesenchymal stem cells. J Cell Physiol 2007; 211: 27-35
58. Terada N, Hamazaki T, Oka M et al. Bone marrow cells adopt the phenotype of other cells by spontaneous cell fusion. Nature 2002; 416: 542-545
59. Burns TC, Ortiz-Gonzalez XR, Gutierrez-Perez M et al. Thymidine analogs are transferred from prelabeled donor to host cells in the central nervous system after transplantation: A word of caution. Stem Cells 2006; 24: 1121-1127
60. Guo JK, Cheng EC, Wang L et al. The commonly used beta-actin-GFP transgenic mouse strain develops a distinct type of glomerulosclerosis. Transgenic Res 2007; 16: 829-834
61. Li L, Truong P, Igarashi P et al. Renal and bone marrow cells fuse after renal ischemic injury. J Am Soc Nephrol 2007; 18: 3067-3077
62. Majumdar MK, Thiede MA, Haynesworth SE et al. Human marrow-derived mesenchymal stem cells (MSCs) express hematopoietic cytokines and support long-term hematopoiesis when differentiated toward stromal and osteogenic lineages. J Hematother Stem Cell Res 2000; 9: 841-848
63. Kunter U, Rong S, Djuric Z et al. Transplanted mesenchymal stem cells accelerate glomerular healing in experimental glomerulonephritis. J Am Soc Nephrol 2006; 17: 2202-2212
64. Ninichuk V, Gross O, Segerer S et al. Multipotent mesenchymal stem cells reduce interstitial fibrosis but do not delay progression of chronic kidney disease in collagen4A3-deficient mice. Kidney Int 2006; 70: 121-129
65. Rombouts WJ, Ploemacher RE. Primary murine MSC show highly efficient homing to the bone marrow but lose homing ability following culture. Leukemia 2003; 17: 160-170
66. Ostendorf T, Rong S, Boor P et al. Antagonism of PDGF-D by human antibody CR002 prevents renal scarring in experimental glomerulonephritis. J Am Soc Nephrol 2006; 17: 1054-1062
67. Ikarashi K, Li B, Suwa M et al. Bone marrow cells contribute to regeneration of damaged glomerular endothelial cells. Kidney Int 2005; 67: 1925-1933
68. Li B, Morioka T, Uchiyama M et al. Bone marrow cell infusion ameliorates progressive glomerulosclerosis in an experimental rat model. Kidney Int 2006; 69: 323-330
69. Kunter U, Rong S, Boor P et al. Mesenchymal stem cells prevent progressive experimental renal failure but maldifferentiate into glomerular adipocytes. J Am Soc Nephrol 2007; 18: 1754-1764
70. Anjos-Afonso F, Siapati EK, Bonnet D. In vivo contribution of murine mesenchymal stem cells into multiple cell-types under minimal damage conditions. J Cell Sci 2004; 117: 5655-5664
71. Breitbach M, Bostani T, Roell W et al. Potential risks of bone marrow cell transplantation into infarcted hearts. Blood 2007; 110: 1362-1369
72. Urist MR, Mc LF. Osteogenetic potency and new-bone formation by induction in transplants to the anterior chamber of the eye. J Bone Joint Surg Am 1952; 34-A: 443-476
73. Thirabanjasak D, Tantiwongse K, Thorner PS. Angiomyeloproliferative lesions following autologous stem cell therapy. J Am Soc Nephrol 2010; 21: 1218-1222
74. Sugimoto H, Mundel TM, Sund M et al. Bone-marrow-derived stem cells repair basement membrane collagen defects and reverse genetic kidney disease. Proc Natl Acad Sci USA 2006; 103: 7321-7326
75. Prodromidi EI, Poulsom R, Jeffery R et al. Bone marrow-derived cells contribute to podocyte regeneration and amelioration of renal disease in a mouse model of Alport syndrome. Stem Cells 2006; 24: 2448-2455
76. Katayama K, Kawano M, Naito I et al. Irradiation prolongs survival of Alport mice. J Am Soc Nephrol 2008; 19: 1692-1700
77. LeBleu VS, Kalluri R. Stem cell-based therapy for glomerular diseases: An evolving concept. J Am Soc Nephrol 2008; 19: 1621-1623
78. Guillot PV, Cook HT, Pusey CD et al. Transplantation of human fetal mesenchymal stem cells improves glomerulopathy in a collagen type I alpha 2-deficient mouse. J Pathol 2008; 214: 627-636
79. Broekema M, Harmsen MC, van Luyn MJ et al. Bone marrow-derived myofibroblasts contribute to the renal interstitial myofibroblast population and produce procollagen I after ischemia/reperfusion in rats. J Am Soc Nephrol 2007; 18: 165-175
80. di Bonzo LV, Ferrero I, Cravanzola C et al. Human mesenchymal stem cells as a two-edged sword in hepatic regenerative medicine: Engraftment and hepatocyte differentiation versus profibrogenic potential. Gut 2008; 57: 223-231
81. Wu GD, Nolta JA, Jin YS et al. Migration of mesenchymal stem cells to heart allografts during chronic rejection. Transplantation 2003; 75: 679-685
82. Jeon ES, Moon HJ, Lee MJ et al. Cancer-derived lysophosphatidic acid stimulates differentiation of human mesenchymal stem cells to myofibroblast-like cells. Stem Cells 2008; 26: 789-797
83. Appel D, Kershaw DB, Smeets B et al. Recruitment of podocytes from glomerular parietal epithelial cells. J Am Soc Nephrol 2009; 20: 333-343
84. Ronconi E, Sagrinati C, Angelotti ML et al. Regeneration of glomerular podocytes by human renal progenitors. J Am Soc Nephrol 2009; 20: 322-332
85. Hugo C, Shankland SJ, Bowen-Pope DF et al. Extraglomerular origin of the mesangial cell after injury. A new role of the juxtaglomerular apparatus. J Clin Invest 1997; 100: 786-794
86. Fox JM, Chamberlain G, Ashton BA et al. Recent advances into the understanding of mesenchymal stem cell trafficking. Br J Haematol 2007; 137: 491-502
87. Potier E, Ferreira E, Andriamanalijaona R et al. Hypoxia affects mesenchymal stromal cell osteogenic differentiation and angiogenic factor expression. Bone 2007; 40: 1078-1087