Tzu Chi Medical Journal
Volume 19, Issue 3 , Pages 115-126 , September 2007

Bone Marrow Stem Cell Therapy for Renal Regeneration After Acute Tubular Necrosis: A Dream or a Reality?

  • Te-Chao Fang

      Affiliations

    • Division of Nephrology, Buddhist Tzu Chi General Hospital, Hualien, Taiwan
    • Department of Medicine, Medical College, Tzu Chi University, Hualien, Taiwan
    • Corresponding Author InformationCorresponding author. Division of Nephrology, Buddhist Tzu Chi General Hospital, 707, Section 3, Chung Yang Road, Hualien, Taiwan
    • ,
  • Chih-Hsien Wang

      Affiliations

    • Division of Nephrology, Buddhist Tzu Chi General Hospital, Hualien, Taiwan
    • ,
  • Jen-Pi Tsai

      Affiliations

    • Division of Nephrology, Buddhist Tzu Chi General Hospital, Dalin, Taiwan
    • ,
  • Bang-Gee Hsu

      Affiliations

    • Division of Nephrology, Buddhist Tzu Chi General Hospital, Hualien, Taiwan

Received 17 April 2007 ,Revised 13 June 2007 ,Accepted 15 June 2007.

References 

  1. Thadhani R , Pascual M , Bonventre JV . Acute renal failure . N Engl J Med . 1996;334:1448–1460
  2. Star RA . Treatment of acute renal failure . Kidney Int . 1998;54:1817–1831
  3. Kelly KJ , Molitoris BA . Acute renal failure in the new millen-nium: time to consider combination therapy . Semin Nep hrol . 2000;20:4–19
  4. Singri N , Ahya SN , Levin ML . Acute renal failure . JAMA . 2003;289:747–751
  5. Edelstein CL , Ling H , Wangsiripaisan A , Schrier RW . Emerging therapies for acute renal failure . Am J Kidney Dis . 1997;30:S89–S95
  6. Nash K , Hafeez A , Hou S . Hospital-acquired renal insuf-ficiency . Am J Kidney Dis . 2002;39:930–936
  7. Weissman I . Stem cells: units of development, units of regene ration, and units in evolution . Cell . 2000;100:157–168
  8. Evans MJ , Kaufman MH . Establishment in culture of pluripotential cells from mouse embryos . Nature . 1981;292:154–156
  9. Lemischka IR , Raulet DH , Mulligan RC . Developmental potential and dynamic behavior of hematopoietic stem cells . Cell . 1986;45:917–927
  10. Bussolati B , Bruno S , Grange C , et al.   Isolation of renal progenitor cells from adult human kidney . Am J Pathol . 2005;166:545–555
  11. Al-Awqati Q , Oliver JA . Stem cells in the kidney . Kidney Int . 2002;61:387–395
  12. Poulsom R , Prodromidi EI , Pusey CD , Cook HT . Cell therapy for renal regeneration–time for some joined-up thinking? . Nephrol Dial Transplant . 2006;21:3349–3353
  13. Ratajczak MZ , Kucia M , Majka M , Reca R , Ratajczak J . Heterogeneous populations of bone marrow stem cells–are we spotting on the same cells from the different angles? . Folia Histochem Cytobiol . 2004;42:139–146
  14. Ferrari G , Cusella-De Angelis G , Coletta M , et al.   Muscle regeneration by bone marrow-derived myogenic progenitors . Science . 1998;279:1528–1530
  15. Eglitis MA , Mezey E . Hematopoietic cells differentiate into both microglia and macroglia in the brains of adult mice . Proc Natl Acad Sci U S A . 1997;94:4080–4085
  16. Pereira R , O'Hara M , Laptev A , et al.   Marrow stromal cells a source of progenitor cells for nonhematopoietic tissues in transgenic mice with a phenotype of osteogenesis imper-fecta . Proc Natl Acad Sci U S A . 1998;95:1142–1147
  17. Asahara T , Masuda H , Takahashi T , et al.   Bone marrow origin of endothelial progenitor cells responsible for post-natal vasculogenesis in physiological and pathological conditions . Circ Res . 1999;85:221–228
  18. Bittner R , Schofer C , Weipoltshammer K , et al.   Recruitment of bone-marrow-derived cells by skeletal and cardiac muscle in adult dystrophic mdx mice . Anat Embryol . 1999;199:391–396
  19. Brazelton T , Rossi F , Keshet G , Blau H . From marrow to brain: expression of neuronal phenotypes in adult mice . Science . 2000;290:1775–1779
  20. Mezey E , Chandross K , Harta G , Maki R , McKercher S . Turning blood into brain: cells bearing neuronal antigens generated in vivo from bone marrow . Science . 2000;290:1779–1782
  21. Petersen B , Bowen W , Patrene K , et al.   Bone marrow as a potential source of hepatic oval cells . Science . 1999;284:1168–1170
  22. Krause D , Theise N , Collector M , et al.   Multi-organ, multi-lineage engraftment by a single bone marrow-derived stem cell . Cell . 2001;105:369–377
  23. Kotton DN , Ma BY , Cardoso WV , et al.   Bone marrow-derived cells as progenitors of lung alveolar epithelium . Development . 2001;128:5181–5188
  24. Poulsom R , Forbes SJ , Hodivala-Dilke K , et al.   Bone marrow contributes to renal parenchymal turnover and regeneration . J Pathol . 2001;195:229–235
  25. Brittan M , Hunt T , Jefferey R , et al.   Bone marrow derivation of pericryptal myofibroblasts in the mouse and human small intestine and colon . Gut . 2002;50:752–757
  26. Alison MR , Poulsom R , Jeffery R , et al.   Hepatocytes from non-hepatic adult stem cells . Nature . 2000;406:257
  27. Korbling M , Katz RL , Khanna A , et al.   Hepatocytes and epithelial cells of donor origin in recipients of peripheral-blood stem cells . N Engl J Med . 2002;346:738–746
  28. Gussoni E , Bennett RR , Muskiewicz KR , et al.   Long-term persistence of donor nuclei in a Duchenne muscular dystrophy patient receiving bone marrow transplantation . J Clin Invest . 2002;110:807–814
  29. Quaini F , Urbanek K , Beltrami AP , et al.   Chimerism of the transplanted heart . N Engl J Med . 2002;346:5–15
  30. Spyridonidis A , Schmitt-Graff A , Tomann T , et al.   Epithelial tissue chimerism after human hematopoietic cell trans plantation is a real phenomenon . Am J Pathol . 2004;164:1147–1155
  31. Kleeberger W , Versmold A , Rothamel T , et al.   Increased chimerism of bronchial and alveolar epithelium in human lung allografts undergoing chronic injury . Am J Pathol . 2003;162:1487–1494
  32. Mezey E , Key S , Vogelsang G , Szalayova I , Lange GD , Crain B . Transplanted bone marrow generates new neurons in human brains . Proc Natl Acad Sci U S A . 2003;100:1364–1369
  33. Weimann JM , Charlton CA , Brazelton TR , Hackman RC , Blau HM . Contribution of transplanted bone marrow cells to Purkinje neurons in human adult brains . Proc Natl Acad Sci U S A . 2003;100:2088–2093
  34. Vassilopoulos G , Wang PR , Russell DW . Transplanted bone marrow regenerates liver by cell fusion . Nature . 2003;422:901–904
  35. Wang X , Willenbring H , Akkari Y , et al.   Cell fusion is the principal source of bone-marrow-derived hepatocytes . Nature . 2003;422:897–901
  36. Alvarez-Dolado M , Pardal R , Garcia-Verdugo JM , et al.   Fusion of bone-marrow-derived cells with Purkinje neurons, cardiomyocytes and hepatocytes . Nature . 2003;425:968–973
  37. Weimann JM , Johansson CB , Trejo A , Blau HM . Stable reprogrammed heterokaryons form spontaneously in Purkinje neurons after bone marrow transplant . Nat Cell Biol . 2003;5:959–966
  38. Chambers I , Colby D , Robertson M , et al.   Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells . Cell . 2003;113:643–655
  39. Corbel SY , Lee A , Yi L , et al.   Contribution of hematopoietic stem cells to skeletal muscle . Nat Med . 2003;9:1528–1532
  40. Alison MR , Poulsom R , Otto WR , et al.   Recipes for adult stem cell plasticity: fusion cuisine or readymade? . J Clin Pathol . 2004;57:113–120
  41. Fang TC , Alison MR , Wright NA , Poulsom R . Adult stem cell plasticity: will engineered tissues be rejected? . Int J Exp Pathol . 2004;85:115–124
  42. Touraine JL , Roncarolo MG , Bacchetta R , et al.   Fetal liver transplantation: biology and clinical results . Bone Marrow Transplant . 1993;11(Suppl 1):119–122
  43. Fang TC , Poulsom R . Cell-based therapies for birth defects: a role for adult stem cell plasticity? . Birth Defects Res Part C Embryo Today . 2003;69:238–249
  44. Horwitz E , Prockop D , Fitzpatrick L , et al.   Transplantability and therapeutic effects of bone marrow-derived mesenchymal cells in children with osteogenesis imperfecta . Nature Medicine . 1999;5:309–313
  45. Horwitz E , Prockop D , Fitzpatrick L , Koo W , Marx J , Brenner M . Osteogenesis imperfecta calls for caution . Nature Medicine . 1999;5:466–467
  46. Horwitz EM , Gordon PL , Koo WK , et al.   Isolated allogeneic bone marrow-derived mesenchymal cells engraft and stimulate growth in children with osteogenesis imperfecta: implications for cell therapy of bone . Proc Natl Acad Sci U S A . 2002;99:8932–8937
  47. Tateishi-Yuyama E , Matsubara H , Murohara T , et al.   Therapeutic angiogenesis for patients with limb ischaemia by autologous transplantation of bone-marrow cells: a pilot study and a randomised controlled trial . Lancet . 2002;360:427–435
  48. Perin EC , Dohmann HF , Borojevic R , et al.   Transendocardial, auto logous bone marrow cell transplantation for severe, chronic ischemic heart failure . Circulation . 2003;107:2294–2302
  49. Assmus B , Schachinger V , Teupe C , et al.   Transplantation of Progenitor Cells and Regeneration Enhancement in Acute Myocardial Infarction (TOPCARE-AMI) . Circulation . 2002;106:3009–3017
  50. Stamm C , Westphal B , Kleine HD , et al.   Autologous bonemarrow stem-cell transplantation for myocardial regeneration . Lancet . 2003;361:45–46
  51. Nishida M , Li TS , Hirata K , Yano M , Matsuzaki M , Hamano K . Improvement of cardiac function by bone marrow cell implantation in a rat hypoperfusion heart model . Ann Thorac Surg . 2003;75:768–774
  52. Williams G , Alvarez C . Host repopulation of the endothelium in allografts of kidneys and aorta . Surg Forum . 1969;20:293–294
  53. Williams G , Krajewski C , Dagher F , Ter Haar A , Roth J , Santos G . Host repopulation of endothelium . Transplant Proc . 1971;3:869–872
  54. Sinclair R . Origin of endothelium in human renal allografts . Br Med J . 1972;4:15–16
  55. Andersen CB , Ladefoged SD , Larsen S . Cellular inflammatory infiltrates and renal cell turnover in kidney allografts: a study using in situ hybridization and combined in situ hybridization and immunohistochemistry with a Y-chromosome-specific DNA probe and monoclonal antibodies . Apmis . 1991;99:645–652
  56. Imasawa T , Nagasawa R , Utsunomiya Y , et al.   Bone marrow transplantation attenuates murine IgA nephropathy: role of a stem cell disorder . Kidney Int . 1999;56:1809–1817
  57. 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
  58. Grimm PC , Nickerson P , Jeffery J , et al.   Neointimal and tubulointerstitial infiltration by recipient mesenchymal cells in chronic renal-allograft rejection . N Engl J Med . 2001;345:93–97
  59. 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
  60. Ito T , Suzuki A , Imai E , Okabe M , Hori M . Bone marrow is a reservoir of repopulating mesangial cells during glo merular remodeling . J Am Soc Nephrol . 2001;12:2625–2635
  61. Lagaaij E , Cramer-Knijnenburg G , van Kemenade F , van Es L , Bruijn J , van Krieken J . Endothelial cell chimerism after renal transplantation and vascular rejection . Lancet . 2001;357:33–37
  62. Gupta S , Verfaillie C , Chmielewski D , Kim Y , Rosenberg ME . A role for extrarenal cells in the regeneration following acute renal failure . Kidney Int . 2002;62:1285–1290
  63. Imasawa T , Utsunomiya Y . Stem cells in renal biology: bone marrow transplantation for the treatment of IgA nephropathy . Exp Nephrol . 2002;10:51–58
  64. Iwano M , Plieth D , Danoff TM , Xue C , Okada H , Neilson EG . Evidence that fibroblasts derive from epithelium during tissue fibrosis . J Clin Invest . 2002;110:341–350
  65. Xu W , Baelde HJ , Lagaaij EL , De Heer E , Paul LC , Bruijn JA . Endothelial cell chimerism after renal transplantation in a rat model . Transplantation . 2002;74:1316–1320
  66. Kale S , Karihaloo A , Clark PR , Kashgarian M , Krause DS , Cantley LG . Bone marrow stem cells contribute to repair of the ischemically injured renal tubule . J Clin Invest . 2003;112:42–49
  67. Masuya M , Drake CJ , Fleming PA , et al.   Hematopoietic origin of glomerular mesangial cells . Blood . 2003;101:2215–2218
  68. 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
  69. Mengel M , Jonigk D , Marwedel M , et al.   Tubular chimerism occurs regularly in renal allografts and is not correlated to outcome . J Am Soc Nephrol . 2004;15:978–986
  70. Fang TC , Alison MR , Cook HT , Jeffery R , Wright NA , Poulsom R . Proliferation of bone marrow-derived cells contributes to regeneration after folic acid-induced acute tubular injury . J Am Soc Nephrol . 2005;16:1723–1732
  71. Iwasaki M , Adachi Y , Minamino K , et al.   Mobilization of bone marrow cells by G-CSF rescues mice from cisplatin-induced renal failure, and M-CSF enhances the effects of G-CSF . J Am Soc Nephrol . 2005;16:658–666
  72. Iwatani H , Ito T , Imai E , et al.   Hematopoietic and non-hematopoietic potentials of Hoechst(low)/side population cells isolated from adult rat kidney . Kidney Int . 2004;65:1604–1614
  73. 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
  74. 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
  75. Stokman G , Leemans JC , Claessen N , Weening JJ , Florquin S . Hematopoietic stem cell mobilization therapy accelerates recovery of renal function independent of stem cell contribution . J Am Soc Nephrol . 2005;16:1684–1692
  76. Yokoo T , Ohashi T , Shen JS , et al.   Human mesenchymal stem cells in rodent whole-embryo culture are reprogrammed to contribute to kidney tissues . Proc Natl Acad Sci U S A . 2005;102:3296–3300
  77. Sugimoto H , Mundel TM , Sund M , Xie L , Cosgrove D , Kalluri R . Bone-marrow-derived stem cells repair basement membrane collagen defects and reverse genetic kidney disease . Proc Natl Acad Sci U S A . 2006;103:7321–7326
  78. Guo JK , Schedl A , Krause DS . Bone marrow transplantation can attenuate the progression of mesangial sclerosis . Stem Cells . 2006;24:406–415
  79. Prodromidi EI, Poulsom R, Jeffery R, Roufosse CA, Pollard PJ, Pusey CD, 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
  80. Gupta S , Verfaillie C , Chmielewski D , Kim Y , Rosenberg ME . Erratum: A role for extrarenal cells in the regeneration following acute renal failure . Kidney Int . 2002;62:2311–2314
  81. Lin F , Cordes K , Li L , et al.   Hematopoietic stem cells contribute to the regeneration of renal tubules after renal ischemia-reperfusion injury in mice . J Am Soc Nephrol . 2003;14:1188–1199
  82. Herrera MB , Bussolati B , Bruno S , Fonsato V , Romanazzi GM , Camussi G . Mesenchymal stem cells contribute to the renal repair of acute tubular epithelial injury . Int J Mol Med . 2004;14:1035–1041
  83. 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
  84. Lange C , Togel 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
  85. 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
  86. Togel F , Hu Z , Weiss K , Isaac J , Lange C , Westenfelder C . Administered mesenchymal stem cells protect against ischemic acute renal failure through differentiation-independent mechanisms . Am J Physiol Renal Physiol . 2005;289:F31–F42
  87. Dekel B , Shezen E , Even-Tov-Friedman S , et al.   Transplantation of human hematopoietic stem cells into ischemic and growing kidneys suggests a role in vasculogenesis but not tubulogenesis . Stem Cells . 2006;24:1185–1193
  88. 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
  89. Rasmusson I . Immune modulation by mesenchymal stem cells . Exp Cell Res . 2006;312:2169–2179
  90. Aggarwal S , Pittenger MF . Human mesenchymal stem cells modulate allogeneic immune cell responses . Blood . 2005;105:1815–1822
  91. Jiang XX , Zhang Y , Liu B , et al.   Human mesenchymal stem cells inhibit differentiation and function of monocyte-derived dendritic cells . Blood . 2005;105:4120–4126
  92. Nauta AJ , Westerhuis G , Kruisselbrink AB , Lurvink EG , Willemze R , Fibbe WE . Donor-derived mesenchymal stem cells are immunogenic in an allogeneic host and stimulate donor graft rejection in a nonmyeloablative setting . Blood . 2006;108:2114–2120

PII: S1016-3190(10)60003-1

doi: 10.1016/S1016-3190(10)60003-1

Tzu Chi Medical Journal
Volume 19, Issue 3 , Pages 115-126 , September 2007

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