Bone Marrow Mesenchymal Stem Cells in Organ Repair and Strategies to Optimize their Efficacy

Regenerative Nephrology

Volumn , Issue , 2011, Pages 299-312

  Xinaris, Christodoulos ^a   Imberti, Barbara ^a   Remuzzi, Giuseppe ^a,b   Morigi, Marina ^a  

^a MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

^b OSPEDALI RIUNITI   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84877284499     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1016/B978-0-12-380928-5.10020-X     Document Type: Chapter

References (127)

1. J. Garcia-Castro, C. Trigueros, J. Madrenas, J.A. Perez-Simon, R. Rodriguez and P. Menendez (2008) Mesenchymal stem cells and their use as cell replacement therapy and disease modelling tool. J. Cell Mol. Med. 12 2552-2565.
2. M.M. Cook, K. Kollar, G.P. Brooke and K. Atkinson (2009) Cellular therapy for repair of cardiac damage after acute myocardial infarction. Int. J. Cell Biol. 2009 906507
3. V. Sueblinvong and D.J. Weiss (2009) Cell therapy approaches for lung diseases: current status. Curr. Opin. Pharmacol. 9 268-273.
4. T.R. Flohr, H. Bonatti Jr., K.L. Brayman and T.L. Pruett (2009) The use of stem cells in liver disease. Curr. Opin. Organ Transplant. 14 64-71.
5. J.C. George (2010) Stem cell therapy in acute myocardial infarction: a review of clinical trials. Transl. Res. 155 10-19.
6. R. Thadhani, M. Pascual and J.V. Bonventre (1996) Acute renal failure. N. Engl. J. Med. 334 1448-1460.
7. M.B. Herrera, B. Bussolati, S. Bruno, V. Fonsato, G.M. Romanazzi and G. Camussi (2004) Mesenchymal stem cells contribute to the renal repair of acute tubular epithelial injury. Int. J. Mol. Med. 14 1035-1041.
8. M. Morigi, B. Imberti, C. Zoja, et al. (2004) Mesenchymal stem cells are renotropic, helping to repair the kidney and improve function in acute renal failure. J. Am. Soc. Nephrol. 15 1794-1804.
9. M. Morigi, M. Introna, B. Imberti, et al. (2008) Human bone marrow mesenchymal stem cells accelerate recovery of acute renal injury and prolong survival in mice. Stem Cells 26 2075-2082.
10. R. Poulsom, S.J. Forbes, K. Hodivala-Dilke, et al. (2001) Bone marrow contributes to renal parenchymal turnover and regeneration. J. Pathol. 195 229-235.
11. C. Roufosse and H.T. Cook (2008) Stem cells and renal regeneration. Nephron. Exp. Nephrol. 109 e39-e45.
12. F. Lin (2008) Renal repair: role of bone marrow stem cells. Pediatr. Nephrol. 23 851-861.
13. S. Gupta, C. Verfaillie, D. Chmielewski, Y. Kim and M.E. Rosenberg (2002) A role for extrarenal cells in the regeneration following acute renal failure. Kidney Int. 62 1285-1290.
14. M. Mengel, D. Jonigk, M. Marwedel, et al. (2004) Tubular chimerism occurs regularly in renal allografts and is not correlated to outcome. J. Am. Soc. Nephrol. 15 978-986.
15. T.C. Fang, M.R. Alison, H.T. Cook, R. Jeffery, N.A. Wright and R. Poulsom (2005) Proliferation of bone marrow-derived cells contributes to regeneration after folic acid-induced acute tubular injury. J. Am. Soc. Nephrol. 16 1723-1732.
16. P.K. Held, M. Al-Dhalimy, H. Willenbring, et al. (2006) In vivo genetic selection of renal proximal tubules. Mol. Ther. 13 49-58.
17. M. Huls, F.G. Russel and R. Masereeuw (2008) Insights into the role of bone marrow-derived stem cells in renal repair. Kidney Blood Press Res. 31 104-110.
18. F. Tögel, J. Isaac and C. Westenfelder (2004) Hematopoietic stem cell mobilization-associated granulocytosis severely worsens acute renal failure. J. Am. Soc. Nephrol. 15 1261-1267.
19. T.C. Fang, W.R. Otto, J. Rao, et al. (2008) Haematopoietic lineage-committed bone marrow cells, but not cloned cultured mesenchymal stem cells, contribute to regeneration of renal tubular epithelium after HgCl 2-induced acute tubular injury. Cell Prolif. 41 575-591.
20. E.I. Prodromidi, R. Poulsom, R. Jeffery, et al. (2006) Bone marrow-derived cells contribute to podocyte regeneration and amelioration of renal disease in a mouse model of Alport syndrome. Stem Cells 24 2448-2455.
21. T. Ito, A. Suzuki, E. Imai, M. Okabe and M. Hori (2001) Bone marrow is a reservoir of repopulating mesangial cells during glomerular remodeling. J. Am. Soc. Nephrol. 12 2625-2635.
22. B. Li, T. Morioka, M. Uchiyama and T. Oite (2006) Bone marrow cell infusion ameliorates progressive glomerulosclerosis in an experimental rat model. Kidney Int. 69 323-330.
23. B.D. Humphreys, M.T. Valerius, A. Kobayashi, et al. (2008) Intrinsic epithelial cells repair the kidney after injury. Cell Stem Cell 2 284-291.
24. J.S. Duffield, K.M. Park, L.L. Hsiao, et al. (2005) Restoration of tubular epithelial cells during repair of the postischemic kidney occurs independently of bone marrow-derived stem cells. J. Clin. Invest. 115 1743-1755.
25. F. Lin, A. Moran and P. Igarashi (2005) Intrarenal cells, not bone marrow-derived cells, are the major source for regeneration in postischemic kidney. J. Clin. Invest. 115 1756-1764.
26. A. Giordano, U. Galderisi and I.R. Marino (2007) From the laboratory bench to the patient’s bedside: an update on clinical trials with mesenchymal stem cells. J. Cell Physiol. 211 27-35.
27. A. Uccelli, L. Moretta and V. Pistoia (2008) Mesenchymal stem cells in health and disease. Nat. Rev. Immunol. 8 726-736.
28. F.P. Barry, J.M. Murphy, K. English and B.P. Mahon (2005) Immunogenicity of adult mesenchymal stem cells: lessons from the fetal allograft. Stem Cells Dev. 14 252-265.
29. A.I. Caplan and J.E. Dennis (2006) Mesenchymal stem cells as trophic mediators. J. Cell Biochem. 98 1076-1084.
30. F. Dazzi, R. Ramasamy, S. Glennie, S.P. Jones and I. Roberts (2006) The role of mesenchymal stem cells in haemopoiesis. Blood Rev. 20 161-171.
31. A.L. Ponte, E. Marais, N. Gallay, et al. (2007) The in vitro migration capacity of human bone marrow mesenchymal stem cells: comparison of chemokine and growth factor chemotactic activities. Stem Cells 25 1737-1745.
32. S.C. Hung, R.R. Pochampally, S.C. Chen, S.C. Hsu and D.J. Prockop (2007) 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 25 2363-2370.
33. T. Kinnaird, E. Stabile, M.S. Burnett, et al. (2004) 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. 94 678-685.
34. J.Y. Oh, M.K. Kim, M.S. Shin, W.R. Wee and J.H. Lee (2009) Cytokine secretion by human mesenchymal stem cells cocultured with damaged corneal epithelial cells. Cytokine 46 100-103.
35. R.J. Deans and A.B. Moseley (2000) Mesenchymal stem cells: biology and potential clinical uses. Exp. Hematol. 28 875-884.
36. M. Crisan, S. Yap, L. Casteilla, et al. (2008) A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 3 301-313.
37. S. Bruno, B. Bussolati, C. Grange, et al. (2009) Isolation and characterization of resident mesenchymal stem cells in human glomeruli. Stem Cells Dev. 18 867-880.
38. E.M. Horwitz, P.L. Gordon, W.K. Koo, et al. (2002) 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. 99 8932-8937.
39. S.L. Chen, W.W. Fang, F. Ye, et al. (2004) Effect on left ventricular function of intracoronary transplantation of autologous bone marrow mesenchymal stem cell in patients with acute myocardial infarction. Am. J. Cardiol. 94 92-95.
40. K. Le Blanc, F. Frassoni, L. Ball, et al. (2008) Mesenchymal stem cells for treatment of steroid-resistant, severe, acute graft-versus-host disease: a phase II study. Lancet 371 1579-1586.
41. A.I. Caplan (2007) Adult mesenchymal stem cells for tissue engineering versus regenerative medicine. J. Cell Physiol. 213 341-347.
42. K. Le Blanc, C. Tammik, K. Rosendahl, E. Zetterberg and O. Ringden (2003) HLA expression and immunologic properties of differentiated and undifferentiated mesenchymal stem cells. Exp. Hematol. 31 890-896.
43. M. Di Nicola, C. Carlo-Stella, M. Magni, et al. (2002) Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood 99 3838-3843.
44. J.M. Ryan, F.P. Barry, J.M. Murphy and B.P. Mahon (2005) Mesenchymal stem cells avoid allogeneic rejection. J. Inflamm. (Lond.) 2 8.
45. A. Bartholomew, C. Sturgeon, M. Siatskas, et al. (2002) Mesenchymal stem cells suppress lymphocyte proliferation in vitro and prolong skin graft survival in vivo. Exp. Hematol. 30 42-48.
46. S. Inoue, F.C. Popp, G.E. Koehl, et al. (2006) Immunomodulatory effects of mesenchymal stem cells in a rat organ transplant model. Transplantation 81 1589-1595.
47. G. Ren, L. Zhang, X. Zhao, et al. (2008) Mesenchymal stem cell-mediated immunosuppression occurs via concerted action of chemokines and nitric oxide. Cell Stem Cell 2 141-150.
48. F. Gieseke, B. Schutt, S. Viebahn, et al. (2007) Human multipotent mesenchymal stromal cells inhibit proliferation of PBMCs independently of IFNgammaR1 signaling and IDO expression. Blood 110 2197-2200.
49. F. Tögel, A. Cohen, P. Zhang, Y. Yang, Z. Hu and C. Westenfelder (2009) Autologous and allogeneic marrow stromal cells are safe and effective for the treatment of acute kidney injury. Stem Cells Dev. 18 475-485.
50. L.C. Amado, A.P. Saliaris, K.H. Schuleri, et al. (2005) Cardiac repair with intramyocardial injection of allogeneic mesenchymal stem cells after myocardial infarction. Proc. Natl. Acad. Sci. U.S.A. 102 11474-11479.
51. H.C. Quevedo, K.E. Hatzistergos, B.N. Oskouei, et al. (2009) Allogeneic mesenchymal stem cells restore cardiac function in chronic ischemic cardiomyopathy via trilineage differentiating capacity. Proc. Natl. Acad. Sci. U.S.A. 106 14022-14027.
52. H. Li, Z.K. Guo, X.S. Li, C.M. Hou, P.H. Tang and N. Mao (2007) Functional and phenotypic alteration of intrasplenic lymphocytes affected by mesenchymal stem cells in a murine allosplenocyte transfusion model. Cell Transplant. 16 85-95.
53. F. Casiraghi, N. Azzollini, P. Cassis, et al. (2008) Pretransplant infusion of mesenchymal stem cells prolongs the survival of a semiallogeneic heart transplant through the generation of regulatory T cells. J. Immunol. 181 3933-3946.
54. H.P. Zhou, D.H. Yi, S.Q. Yu, et al. (2006) Administration of donor-derived mesenchymal stem cells can prolong the survival of rat cardiac allograft. Transplant. Proc. 38 3046-3051.
55. S.M. Devine, A.M. Bartholomew, N. Mahmud, et al. (2001) Mesenchymal stem cells are capable of homing to the bone marrow of non-human primates following systemic infusion. Exp. Hematol. 29 244-255.
56. L. Wang, Y. Li, J. Chen, et al. (2002) Ischemic cerebral tissue and MCP-1 enhance rat bone marrow stromal cell migration in interface culture. Exp. Hematol. 30 831-836.
57. M.J. Price, M. Frantzen, S. Kar, et al. (2003) Intravenous allogeneic mesenchymal stem cells home to myocardial injury and reduce left ventricular remodeling in a porcine balloon occlusion–reperfusion model of myocardial infarction. J. Am. Coll. Cardiol. 41 269A.
58. M.B. Herrera, B. Bussolati, S. Bruno, et al. (2007) Exogenous mesenchymal stem cells localize to the kidney by means of CD44 following acute tubular injury. Kidney Int. 72 430-441.
59. F. Tögel, K. Weiss, Y. Yang, Z. Hu, P. Zhang and C. Westenfelder (2007) Vasculotropic, paracrine actions of infused mesenchymal stem cells are important to the recovery from acute kidney injury. Am. J. Physiol. Renal. Physiol. 292 F1626-F1635.
60. B. Imberti, M. Morigi, S. Tomasoni, et al. (2007) Insulin-like growth factor-1 sustains stem cell mediated renal repair. J. Am. Soc. Nephrol. 18 2921-2928.
61. M. Morigi, C. Rota, T. Montemurro, et al. (2010) Life-sparing effect of human cord-blood mesenchymal stem cells in experimental acute kidney injury. Stem Cells 28 513-522.
62. C. Lange, F. Tögel, H. Ittrich, et al. (2005) Administered mesenchymal stem cells enhance recovery from ischemia/reperfusion-induced acute renal failure in rats. Kidney Int. 68 1613-1617.
63. F. Tögel, Z. Hu, K. Weiss, J. Isaac, C. Lange and C. Westenfelder (2005) Administered mesenchymal stem cells protect against ischemic acute renal failure through differentiation-independent mechanisms. Am. J. Physiol. Renal. Physiol. 289 F31-F42.
64. B. Bi, R. Schmitt, M. Israilova, H. Nishio and L.G. Cantley (2007) Stromal cells protect against acute tubular injury via an endocrine effect. J. Am. Soc. Nephrol. 18 2486-2496.
65. L. Cai, B.H. Johnstone, T.G. Cook, et al. (2007) Suppression of hepatocyte growth factor production impairs the ability of adipose-derived stem cells to promote ischemic tissue revascularization. Stem Cells 25 3234-3243.
66. A. Danilkovitch-Miagkova and B. Zbar (2002) Dysregulation of Met receptor tyrosine kinase activity in invasive tumors. J. Clin. Invest. 109 863-867.
67. P.C. Baer and H. Geiger (2010) Mesenchymal stem cell interactions with growth factors on kidney repair. Curr. Opin. Nephrol. Hypertens. 19 1-6.
68. K. Urbanek, M. Rota, S. Cascapera, et al. (2005) Cardiac stem cells possess growth factor-receptor systems that after activation regenerate the infarcted myocardium, improving ventricular function and long-term survival. Circ. Res. 97 663-673.
69. U. Kunter, S. Rong, P. Boor, et al. (2007) Mesenchymal stem cells prevent progressive experimental renal failure but maldifferentiate into glomerular adipocytes. J. Am. Soc. Nephrol. 18 1754-1764.
70. T. Yoshimura, K. Matsushima, S. Tanaka, et al. (1987) Purification of a human monocyte-derived neutrophil chemotactic factor that has peptide sequence similarity to other host defense cytokines. Proc. Natl. Acad. Sci. U.S.A. 84 9233-9237.
71. A. Zlotnik, J. Morales and J.A. Hedrick (1999) Recent advances in chemokines and chemokine receptors. Crit. Rev. Immunol. 19 1-47.
72. M. Baggiolini, B. Dewald and B. Moser (1997) Human chemokines: an update. Annu. Rev. Immunol. 15 675-705.
73. A.D. Luster (1998) Chemokines – chemotactic cytokines that mediate inflammation. N. Engl. J. Med. 338 436-445.
74. C. Gerard and B.J. Rollins (2001) Chemokines and disease. Nat. Immunol. 2 108-115.
75. M. Honczarenko, Y. Le, M. Swierkowski, I. Ghiran, A.M. Glodek and L.E. Silberstein (2006) Human bone marrow stromal cells express a distinct set of biologically functional chemokine receptors. Stem Cells 24 1030-1041.
76. I. Von Luttichau, M. Notohamiprodjo, A. Wechselberger, et al. (2005) Human adult CD34− progenitor cells functionally express the chemokine receptors CCR1, CCR4, CCR7, CXCR5, and CCR10 but not CXCR4. Stem Cells Dev. 14 329-336.
77. V. Sordi, M.L. Malosio, F. Marchesi, et al. (2005) Bone marrow mesenchymal stem cells express a restricted set of functionally active chemokine receptors capable of promoting migration to pancreatic islets. Blood 106 419-427.
78. B. Ruster, S. Gottig, R.J. Ludwig, et al. (2006) Mesenchymal stem cells display coordinated rolling and adhesion behavior on endothelial cells. Blood 108 3938-3944.
79. R.F. Wynn, C.A. Hart, C. Corradi-Perini, et al. (2004) A small proportion of mesenchymal stem cells strongly expresses functionally active CXCR4 receptor capable of promoting migration to bone marrow. Blood 104 2643-2645.
80. J. Ringe, S. Strassburg, K. Neumann, et al. (2007) Towards in situ tissue repair: human mesenchymal stem cells express chemokine receptors CXCR1, CXCR2 and CCR2, and migrate upon stimulation with CXCL8 but not CCL2. J. Cell Biochem. 101 135-146.
81. V.F. Segers, I. Van Riet, L.J. Andries, et al. (2006) Mesenchymal stem cell adhesion to cardiac microvascular endothelium: activators and mechanisms. Am. J. Physiol. Heart Circ. Physiol. 290 H1370-H1377.
82. C. Steingen, F. Brenig, L. Baumgartner, J. Schmidt, A. Schmidt and W. Bloch (2008) Characterization of key mechanisms in transmigration and invasion of mesenchymal stem cells. J. Mol. Cell Cardiol. 44 1072-1084.
83. A.D. Luster, R. Alon and U.H. von Andrian (2005) Immune cell migration in inflammation: present and future therapeutic targets. Nat. Immunol. 6 1182-1190.
84. K. Ley, C. Laudanna, M.I. Cybulsky and S. Nourshargh (2007) Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat. Rev. Immunol. 7 678-689.
85. S.P. Bruder, N.S. Ricalton, R.E. Boynton, et al. (1998) Mesenchymal stem cell surface antigen SB-10 corresponds to activated leukocyte cell adhesion molecule and is involved in osteogenic differentiation. J. Bone Miner. Res. 13 655-663.
86. P.A. Conget and J.J. Minguell (1999) Phenotypical and functional properties of human bone marrow mesenchymal progenitor cells. J. Cell Physiol. 181 67-73.
87. E.K. Waller, J. Olweus, F. Lund-Johansen, et al. (1995) The "common stem cell" hypothesis reevaluated: human fetal bone marrow contains separate populations of hematopoietic and stromal progenitors. Blood 85 2422-2435.
88. H. Li, Z. Guo, X. Jiang, H. Zhu, X. Li and N. Mao (2008) Mesenchymal stem cells alter migratory property of T and dendritic cells to delay the development of murine lethal acute graft-versus-host disease. Stem Cells 26 2531-2541.
89. M.K. Majumdar, M. Keane-Moore, D. Buyaner, et al. (2003) Characterization and functionality of cell surface molecules on human mesenchymal stem cells. J. Biomed. Sci. 10 228-241.
90. X. Wang, H. Hisha, S. Taketani, et al. (2005) Neural cell adhesion molecule contributes to hemopoiesis-supporting capacity of stromal cell lines. Stem Cells 23 1389-1399.
91. M.F. Pittenger, A.M. Mackay, S.C. Beck, et al. (1999) Multilineage potential of adult human mesenchymal stem cells. Science 284 143-147.
92. J.D. Abbott, Y. Huang, D. Liu, R. Hickey, D.S. Krause and F.J. Giordano (2004) Stromal cell-derived factor-1alpha plays a critical role in stem cell recruitment to the heart after myocardial infarction but is not sufficient to induce homing in the absence of injury. Circulation 110 3300-3305.
93. Y. Wang, H.E. Johnsen, S. Mortensen, et al. (2006) Changes in circulating mesenchymal stem cells, stem cell homing factor, and vascular growth factors in patients with acute ST elevation myocardial infarction treated with primary percutaneous coronary intervention. Heart 92 768-774.
94. Y. Takabatake, T. Sugiyama, H. Kohara, et al. (2009) The CXCL12 (SDF-1)/CXCR4 axis is essential for the development of renal vasculature. J. Am. Soc. Nephrol. 20 1714-1723.
95. F. Tögel, J. Isaac, Z. Hu, K. Weiss and C. Westenfelder (2005) Renal SDF-1 signals mobilization and homing of CXCR4-positive cells to the kidney after ischemic injury. Kidney Int. 67 1772-1784.
96. B. Mazzinghi, E. Ronconi, E. Lazzeri, et al. (2008) Essential but differential role for CXCR4 and CXCR7 in the therapeutic homing of human renal progenitor cells. J. Exp. Med. 205 479-490.
97. A. Kortesidis, A. Zannettino, S. Isenmann, S. Shi, T. Lapidot and S. Gronthos (2005) Stromal-derived factor-1 promotes the growth, survival, and development of human bone marrow stromal stem cells. Blood 105 3793-3801.
98. R. Sackstein, J.S. Merzaban, D.W. Cain, et al. (2008) Ex vivo glycan engineering of CD44 programs human multipotent mesenchymal stromal cell trafficking to bone. Nat. Med. 14 181-187.
99. L. Wang, Y. Li, X. Chen, et al. (2002) MCP-1, MIP-1, IL-8 and ischemic cerebral tissue enhance human bone marrow stromal cell migration in interface culture. Hematology 7 113-117.
100. Y. Li, X. Yu, S. Lin, X. Li, S. Zhang and Y.H. Song (2007) Insulin-like growth factor 1 enhances the migratory capacity of mesenchymal stem cells. Biochem. Biophys. Res. Commun. 356 780-784.
101. H. Sariola and M. Saarma (2003) Novel functions and signalling pathways for GDNF. J. Cell Sci. 116 3855-3862.
102. H. Shi, D. Patschan, G.P. Dietz, M. Bahr, M. Plotkin and M.S. Goligorsky (2008) 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. 294 F229-F235.
103. G. Schultz, D.S. Rotatori and W. Clark (1991) EGF and TGF-alpha in wound healing and repair. J. Cell. Biochem. 45 346-352.
104. S. Zhuang, Y. Dang and R.G. Schnellmann (2004) Requirement of the epidermal growth factor receptor in renal epithelial cell proliferation and migration. Am. J. Physiol. Renal. Physiol. 287 F365-F372.
105. P.C. Baer, R. Schubert, J. Bereiter-Hahn, M. Plosser and H. Geiger (2009) Expression of a functional epidermal growth factor receptor on human adipose-derived mesenchymal stem cells and its signaling mechanism. Eur. J. Cell Biol. 88 273-283.
106. Y. Liu (2002) Hepatocyte growth factor and the kidney. Curr. Opin. Nephrol. Hypertens. 11 23-30.
107. K. Matsumoto and T. Nakamura (2001) Hepatocyte growth factor: renotropic role and potential therapeutics for renal diseases. Kidney Int. 59 2023-2038.
108. G.K. Michalopoulos and M.C. DeFrances (1997) Liver regeneration. Science 276 60-66.
109. G. Forte, M. Minieri, P. Cossa, et al. (2006) Hepatocyte growth factor effects on mesenchymal stem cells: proliferation, migration, and differentiation. Stem Cells 24 23-33.
110. S. Villanueva, C. Cespedes, A. Gonzalez and C.P. Vio (2006) bFGF induces an earlier expression of nephrogenic proteins after ischemic acute renal failure. Am. J. Physiol. Regul. Integr. Comp. Physiol. 291 R1677-R1687.
111. C. Michiels, F. De Leener, T. Arnould, M. Dieu and J. Remacle (1994) Hypoxia stimulates human endothelial cells to release smooth muscle cell mitogens: role of prostaglandins and bFGF. Exp. Cell Res. 213 43-54.
112. C.M. Gajdusek and S. Carbon (1989) Injury-induced release of basic fibroblast growth factor from bovine aortic endothelium. J. Cell Physiol. 139 570-579.
113. A. Schmidt, D. Ladage, T. Schinkothe, et al. (2006) Basic fibroblast growth factor controls migration in human mesenchymal stem cells. Stem Cells 24 1750-1758.
114. M. Shi, J. Li, L. Liao, et al. (2007) Regulation of CXCR4 expression in human mesenchymal stem cells by cytokine treatment: role in homing efficiency in NOD/SCID mice. Haematologica 92 897-904.
115. Z. Pasha, Y. Wang, R. Sheikh, D. Zhang, T. Zhao and M. Ashraf (2008) Preconditioning enhances cell survival and differentiation of stem cells during transplantation in infarcted myocardium. Cardiovasc. Res. 77 134-142.
116. S.C. Hung, R.R. Pochampally, S.C. Hsu, et al. (2007) Short-term exposure of multipotent stromal cells to low oxygen increases their expression of CX3CR1 and CXCR4 and their engraftment in vivo. PLoS ONE 2 e416.
117. B. Annabi, Y.T. Lee, S. Turcotte, et al. (2003) Hypoxia promotes murine bone-marrow-derived stromal cell migration and tube formation. Stem Cells 21 337-347.
118. H. Haider, S. Jiang, N.M. Idris and M. Ashraf (2008) IGF-1-overexpressing mesenchymal stem cells accelerate bone marrow stem cell mobilization via paracrine activation of SDF-1alpha/CXCR4 signaling to promote myocardial repair. Circ. Res. 103 1300-1308.
119. Z. Cheng, L. Ou, X. Zhou, et al. (2008) Targeted migration of mesenchymal stem cells modified with CXCR4 gene to infarcted myocardium improves cardiac performance. Mol. Ther. 16 571-579.
120. K. Sasaki, C. Heeschen, A. Aicher, et al. (2006) Ex vivo pretreatment of bone marrow mononuclear cells with endothelial NO synthase enhancer AVE9488 enhances their functional activity for cell therapy. Proc. Natl. Acad. Sci. U.S.A. 103 14537-14541.
121. C. Heeschen, R. Lehmann, J. Honold, et al. (2004) Profoundly reduced neovascularization capacity of bone marrow mononuclear cells derived from patients with chronic ischemic heart disease. Circulation 109 1615-1622.
122. A.A. Mangi, N. Noiseux, D. Kong, et al. (2003) Mesenchymal stem cells modified with Akt prevent remodeling and restore performance of infarcted hearts. Nat. Med. 9 1195-1201.
123. Y.L. Tang, Y. Tang, Y.C. Zhang, K. Qian, L. Shen and M.I. Phillips (2005) Improved graft mesenchymal stem cell survival in ischemic heart with a hypoxia-regulated heme oxygenase-1 vector. J. Am. Coll. Cardiol. 46 1339-1350.
124. W. Li, N. Ma, L.L. Ong, et al. (2007) Bcl-2 engineered MSCs inhibited apoptosis and improved heart function. Stem Cells 25 2118-2127.
125. M. Hagiwara, B. Shen, L. Chao and J. Chao (2008) Kallikrein-modified mesenchymal stem cell implantation provides enhanced protection against acute ischemic kidney injury by inhibiting apoptosis and inflammation. Hum. Gene. Ther. 19 807-819.
126. M. Zhang, N. Mal, M. Kiedrowski, et al. (2007) SDF-1 expression by mesenchymal stem cells results in trophic support of cardiac myocytes after myocardial infarction. FASEB J. 21 3197-3207.
127. C. Mias, E. Trouche, M.H. Seguelas, et al. (2008) Ex vivo pretreatment with melatonin improves survival, proangiogenic/mitogenic activity, and efficiency of mesenchymal stem cells injected into ischemic kidney. Stem Cells 26 1749-1757.