Molecular characteristics of bone marrow mesenchymal stem cells, source of regenerative medicine

International Journal of Cardiology

Volumn 163, Issue 2, 2013, Pages 125-131

  Pourrajab, Fatemeh ^a   Forouzannia, Seyed Khalil ^a   Tabatabaee, Seyed Ahmad ^a  

^a SHAHID SADOUGHI UNIVERSITY OF MEDICAL SCIENCES   (Iran)

Author keywords

Bone marrow mesenchymal stem cells; Heart disease; Molecular mechanism

Indexed keywords

CHEMOKINE RECEPTOR CCR2; GAMMA INTERFERON; GELATINASE A; HYPOXIA INDUCIBLE FACTOR 1; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; STAT PROTEIN; TUMOR NECROSIS FACTOR ALPHA; VASCULAR CELL ADHESION MOLECULE 1; VERY LATE ACTIVATION ANTIGEN 4; B7 ANTIGEN; CD86 ANTIGEN; COLLAGEN TYPE 1; COLLAGEN TYPE 4; FIBROBLAST GROWTH FACTOR 2; GRANULOCYTE COLONY STIMULATING FACTOR; INTERLEUKIN 11; INTERLEUKIN 6; INTERLEUKIN 8; JANUS KINASE; MATRIX METALLOPROTEINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MONOCYTE CHEMOTACTIC PROTEIN 1; OSTEOCALCIN; PLATELET DERIVED GROWTH FACTOR BB; SECRETED FRIZZLED RELATED PROTEIN 2; STEM CELL FACTOR; STROMAL CELL DERIVED FACTOR 1ALPHA; TOLL LIKE RECEPTOR 4; TRANSCRIPTION FACTOR RUNX2; VASCULOTROPIN; WNT PROTEIN;

ACUTE HEART INFARCTION; ANTIPROLIFERATIVE ACTIVITY; CELL ADHESION; CELL AGING; CELL CYCLE PROGRESSION; CELL MIGRATION; CELL POLARITY; CELL PROLIFERATION; CELL SURVIVAL; CYTOKINE RESPONSE; ENDOTHELIUM; GENE EXPRESSION; HEART MUSCLE ISCHEMIA; HUMAN; IMMUNOGENICITY; MESENCHYMAL STEM CELL TRANSPLANTATION; MICROVASCULATURE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REGENERATIVE MEDICINE; REVIEW; STEM CELL EXPANSION; T LYMPHOCYTE; VASCULARIZATION; BONE MARROW DERIVED MESENCHYMAL STEM CELL; CALCIUM SIGNALING; CAPILLARY ENDOTHELIAL CELL; CARDITIS; CELL DIFFERENTIATION; CELL FUNCTION; CELL LINEAGE; CELL VIABILITY; CELLULAR SECRETION; CELLULAR STRESS RESPONSE; CELLULAR STRESS SIGNAL; CYTOKINE RELEASE; FIBROBLAST; HEART DISEASE; HEART INFARCTION PREVENTION; HEART MUSCLE CELL; HEART MUSCLE CONTRACTILITY; HYPOXIA; IMMUNOREGULATION; ISCHEMIC HEART DISEASE; NUCLEAR REPROGRAMMING; REPERFUSION INJURY; SEPSIS; SIGNAL TRANSDUCTION; STEM CELL MOBILIZATION; TISSUE REGENERATION;

BIOCHEMICAL PHENOMENA; BONE MARROW CELLS; HUMANS; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; REGENERATIVE MEDICINE;

EID: 84873411314     PISSN: 01675273     EISSN: 18741754     Source Type: Journal    
DOI: 10.1016/j.ijcard.2011.11.017     Document Type: Review

References (128)

1. P.J. Psaltis, A.C. Zannettino, S.G. Worthley, and S. Gronthos Concise review: mesenchymal stromal cells: potential for cardiovascular repair Stem Cells 26 2008 2201 2210
2. M.F. Pittenger, and B.J. Martin Mesenchymal stem cells and their potential as cardiac therapeutics Circ Res 95 2004 9 20
3. K. Le Blanc, F. Frassoni, and L. Ball Mesenchymal stem cells for treatment of steroid-resistant, severe acute graft-versus-host disease: a phase II study Lancet 371 2008 1579 1586
4. G. Vassalli, and T. Moccetti Cardiac repair with allogeneic mesenchymal stem cells after myocardial infarction Swiss Med Wkly 141 2011 w13209
5. A. Giordano, U. Galderisi, and I.R. Marino From the laboratory bench to the patient's bedside: an update on clinical trials with mesenchymal stem cells J Cell Physiol 211 2007 27 35
6. W. Jiang, A. Ma, and T. Wang Intravenous transplantation of mesenchymal stem cells improves cardiac performance after acute myocardial ischemia in female rats Transpl Int 19 7 2006 570 580
7. A. Shabbir, D. Zisa, M. Leiker, C. Johnston, H. Lin, and T. Lee Muscular dystrophy therapy by non-autologous mesenchymal stem cells: muscle regeneration without immunosuppression and inflammation Transplantation 87 2009 1275 1282
8. A. Shabbir, D. Zisa, G. Suzuki, and T. Lee Heart failure therapy mediated by the trophic activities of bone marrow mesenchymal stem cells: a non-invasive therapeutic regimen Am J Physiol Heart Circ Physiol 296 2009 H1888 H1897
9. Y. Miyahara, N. Nagaya, and M. Kataoka Monolayered mesenchymal stem cells repair scarred myocardium after myocardial infarction Nat Med 12 2006 459 465
10. N. Nagaya, K. Kangawa, and T. Itoh Transplantation of mesenchymal stem cells improves cardiac function in a rat model of dilated cardiomyopathy Circulation 112 2005 1128 1135
11. A.M. Abarbanell, A.C. Coffey, and J.W. Fehrenbacher Proinflammatory cytokine effects on mesenchymal stem cell therapy for the ischemic hear Ann Thorac Surg 88 2009 1036 1043
12. J.S. Burchfield, M. Iwasaki, and M. Koyanagi Interleukin-10 from transplanted bone marrow mononuclear cells contributes to cardiac protection after myocardial infarction Circ Res 103 2008 203 211
13. M. Gnecchi, Z. Zhang, A. Ni, and V.J. Dzau Paracrine mechanisms in adult stem cell signaling and therapy Circ Res 103 2008 1204 1219
14. A.I. Caplan Why are MSCs therapeutic? New data: new insight J Pathol 217 2009 318 324
15. D.J. Prockop Stemness does not explain the repair of many tissues by mesenchymal stem/multipotent stromal cells (MSCs) Clin Pharmacol Ther 82 2007 241 243
16. A. Schmidt, D. Ladage, and C. Steingen Mesenchymal stem cells transmigrate over the endothelial barrier Eur J Cell Biol 85 2006 1179 1188
17. J.F. Ji, B.P. He, S.T. Dheen, and S.S. Tay Interactions of chemokines and chemokine receptors mediate the migration of mesenchymal stem cells to the impaired site in the brain after hypoglossal nerve injury Stem Cells 22 2004 415 427
18. J.K. Damas, H.G. Eiken, and E. Oie Myocardial expression of CC- and CXC-chemokines and their receptors in human end-stage heart failure Cardiovasc Res 47 2000 778 787
19. P. De Becker, M. Van Hummelen, I. Bakkus, J. Vande Broek, M. De Wever, and I. De Waele Van Riet Migration of culture-expanded human mesenchymal stem cells through bone marrow endothelium is regulated by matrix metalloproteinase-2 and tissue inhibitor of metalloproteinase-3 Haematologica 92 2007 440 449
20. C. Ries, V. Egea, M. Karow, H. Kolb, M. Jochum, and P. Neth MMP-2, MT1-MMP, and TIMP-2 are essential for the invasive capacity of human mesenchymal stem cells: differential regulation by inflammatory cytokines Blood 109 2007 4055 4063
21. C. Steingen, F. Brenig, L. Baumgartner, J. Schmidt, and W. Bloch Characterization of key mechanisms in transmigration and invasion of mesenchymal stem cells J Mol Cell Card 44 2008 1072 1084
22. J. Mauney, B.R. Olsen, and V. Volloch Matrix remodeling as stem cell recruitment event: a novel in vitro model for homing of human bone marrow stromal cells to the site of injury shows crucial role of extracellular collagen matrix Matrix Biol 29 2010 657 663
23. P.E. Kolattukudy, T. Quach, and S. Bergese Myocarditis induced by targeted expression of the MCP-1 gene in murine cardiac muscle Am J Pathol 152 1998 101 111
24. J. Guo, G.S. Lin, C.Y. Bao, Z.M. Hu, and M.Y. Hu Anti-inflammation role for mesenchymal stem cells transplantation in myocardial infarction Inflammation 30 2007 97 104
25. K. Fuse, M. Kodama, and H. Hanawa Enhanced expression and production of monocyte chemoattractant protein-1 in myocarditis Clin Exp Immunol 124 2001 346 352
26. Z. Li, J. Guo, O. Chang, and A. Zhang Paracrine role for mesenchymal stem cells in acute myocardial infarction Biol Pharm Bull 32 2009 1343 1346
27. N. Nagaya, T. Fujii, and T. Iwase Intravenous administration of mesenchymal stem cells improves cardiac function in rats with acute myocardial infarction through angiogenesis and myogenesis Am J Physiol Heart Circ Physiol 287 2004 H2670 H2676
28. C.H. Liu, and S.M. Hwang Cytokine interactions in mesenchymal stem cells from cord blood Cytokine 32 2005 270 279
29. T. Mracek, B. Cannon, and J. Houstek IL-1 and LPS but not IL-6 inhibits differentiation and down-regulate PPAR gamma in brown adipocytes Cytokine 26 2004 9 15
30. R.H. Lee, A.A. Pulin, and M.J. Seo Intravenous hMSCs improve myocardial infarction in mice because cells embolized in lung are activated to secrete the anti-inflammatory protein TSG-6 Cell Stem Cell 5 2009 54 63
31. D. Zisa, A. Shabbir, G. Suzuki, and T. Lee Vascular endothelial growth factor (VEGF) as a key therapeutic trophic factor in bone marrow mesenchymal stem cell-mediated cardiac repair Biochem Biophys Res Commun 390 2009 834 838
32. S.G. Ball, C.A. Shuttleworth, and C.M. Kielty Vascular endothelial growth factor can signal through platelet-derived growth factor receptors J Cell Biol 177 2007 489 500
33. E. Potier, E. Ferreira, R. Andriamanalijaona, J.P. Pujol, K. Oudina, and D. Logeart-Avramoglou Hypoxia affects mesenchymal stromal cell osteogenic differentiation and angiogenic factor expression Bone 40 2007 1078 1087
34. J.M. Hare, J.H. Traverse, T.D. Henry, N. Dib, R.K. Strumpf, and S.P. Schulman A randomized, double-blind, placebo-controlled, dose-escalation study of intravenous adult human mesenchymal stem cells (prochymal) after acute myocardial infarction J Am Coll Cardiol 54 2009 2277 2286
35. P.R. Crisostomo, Y. Wang, T.A. Markel, M. Wang, T. Lahm, and D.R. Meldrum Human mesenchymal stem cells stimulated by TNF-α, LPS, or hypoxia produce growth factors by an NF-κB but not JNK-dependent mechanism Am J Physiol Cell Physiol 294 2008 C675 C682
36. T.B. Rogers, S. Pati, and S. Gaa Mesenchymal stem cells stimulate protective genetic reprogramming of injured cardiac ventricular myocytes J Mol Cell Cardiol 50 2011 346 356
37. P.C. Smits Myocardial repair with autologous skeletal myoblasts: a review of the clinical studies and problems Minerva Cardioangiol 52 2004 525 535
38. Y.L. Tang, Q. Zhao, and X. Qin Paracrine action enhances the effects of autologous mesenchymal stem cell transplantation on vascular regeneration in rat model of myocardial infarction Ann Thorac Surg 80 2005 229 236
39. G. Hall, I.S. Singh, L. Hester, J.D. Hasday, and T.B. Rogers Inhibitor-{kappa}B kinase-{beta}regulates LPS-induced TNF{alpha}production in cardiac myocytes through NF-{kappa}B p65 subunit phosphorylation Am J Physiol Heart Circ Physiol 289 2005 H2103 H2111
40. M. Bujak, and N.G. Frangogiannis The role of IL-1 in the pathogenesis of heart disease Arch Immunol Ther Exp (Warsz) 57 2009 165 176
41. Z.J. Wang, F. Zhang, L.S. Wang, Y.W. Yao, O. Zhao, and X. Gao Lipopolysaccharides can protect mesenchymal stem cells (MSCs) from oxidative stress-induced apoptosis and enhance proliferation of MSCs via Toll-like receptor(TLR)-4 and PI3K/Akt Cell Biol Int 33 2009 665 674
42. T. Ha, F. Hua, and X. Liu Lipopolysaccharide induced myocardial protection against ischaemia/reperfusion injury is mediated through a PI3K/Akt-dependent mechanism Cardiovasc Res 78 3 2008 546 553
43. J. Tang, J. Wang, and L. Guo Mesenchymal stem cells modified with stromal cell-derived factor 1 alpha improve cardiac remodeling via paracrine activation of hepatocyte growth factor in a rat model of myocardial infarction Mol Cells 29 2010 9 19
44. S.R. Thompson, J. Sanders, J.W. Stephens, G.J. Miller, and S.E. Humphries A common interleukin 18 haplotype is associated with higher body mass index in subjects with diabetes and coronary heart disease Metabolism 56 2007 662 669
45. L. Ao, Y. Song, D.A. Fullerton, C.A. Dinarello, and X. Meng The interaction between myocardial depressant factors in endotoxemic cardiac dysfunction: role of TNF-alpha in TLR4-mediated ICAM-1 expression Cytokine 38 2007 124 129
46. S. Ohnishi, B. Yanagawa, and K. Tanaka Transplantation of mesenchymal stem cells attenuates myocardial injury and dysfunction in a rat model of acute myocarditis J Mol Cell Cardiol 42 2007 88 97
47. R.D. Brown, S.K. Ambler, M.D. Mitchell, and C.S. Long The cardiac fibroblast: therapeutic target in myocardial remodeling and failure Annu Rev Pharmacol Toxicol 45 2005 657 687
48. B.I. Jugdutt Remodeling of the myocardium and potential targets in the collagen degradation and synthesis pathways Curr Drug Targets Cardiovasc Haematol Disord 3 2003 1 30
49. S. Ohnishi, H. Sumiyoshi, S. Kitamura, and N. Nagaya Mesenchymal stem cells attenuate cardiac fibroblast proliferation and collagen synthesis through paracrine actions FEBS Lett 581 2007 3961 3966
50. M. Gnecchi, H. He, and N. Noiseux Evidence supporting paracrine hypothesis for Akt-modified mesenchymal stem cell-mediated cardiac protection and functional improvement FASEB J 20 2006 661 669
51. V. Vasioukhin, C. Bauer, L. Degenstein, B. Wise, and E. Fuchs Hyperproliferation and defects in epithelial polarity upon conditional ablation of alpha-catenin in skin Cell 104 2001 605 617
52. P. Chambon The retinoid signaling pathway: molecular and genetic analyses Semin Cell Biol 5 1994 115 125
53. V.F. Segers, I. Van Riet, and L.J. Andries Mesenchymal stem cell adhesion to cardiac microvascular endothelium: activators and mechanisms Am J Physiol Heart Circ Physiol 290 2006 H1370 H1377
54. B. Ruster, S. Gottig, and R.J. Ludwig Mesenchymal stem cells (MSCs) display coordinated rolling and adhesion behavior on endothelial cells Blood 108 12 2006 3938 3944
55. J.E. Ip, Y. Wu, J. Huang, L. Zhang, R.E. Pratt, and V.J. Dzau Mesenchymal stem cells use integrin beta1 not CXC chemokine receptor 4 for myocardial migration and engraftment Mol Biol Cell 18 2007 2873 2882
56. B.R. Son, L.A. Marquez-Curtis, and M. Kucia 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 24 2006 1254 1264
57. S. Miyamoto, H. Teramoto, and O.A. Coso Integrin function: molecular hierarchies of cytoskeletal and signaling molecules J Cell Biol 131 1995 791 805
58. P. Roca-Cusachs, N.C. Gauthier, R.A. Del, and M.P. Sheetz Clustering of alpha(5) beta(1) integrins determines adhesion strength whereas alpha(v)beta(3) and talin enable mechanotransduction Proc Natl Acad Sci U S A 106 2009 16245 16250
59. + cells across specialized and nonspecialized endothelium requires prior activation by growth factors and is mediated by PECAM-1 (CD31) Blood 91 1998 1196 1205
60. A. Schmidt, D. Ladage, and T. Schinkothe Basic fibroblast growth factor controls migration in human mesenchymal stem cells Stem Cells 24 2006 1750 1758
61. S. Schenk, N. Mal, and A. Finan Monocyte chemotactic protein-3 is a myocardial mesenchymal stem cell homing factor Stem Cells 25 2007 245 251
62. I.F. Charo, and W. Peters Chemokine receptor 2 (CCR2) in atherosclerosis, infectious diseases, and regulation of T-cell polarization Microcirculation 10 2003 259 264
63. S. Struyf, P. Proost, and J. Vandercappellen Synergistic up-regulation of MCP-2/CCL8 activity is counteracted by chemokine cleavage, limiting its inflammatory and anti-tumoral effects Eur J Immunol 39 2009 843 857
64. Y. Terashima, N. Onai, and M. Murai Pivotal function for cytoplasmic protein FROUNT in CCR2-mediated monocyte chemotaxis Nat Immunol 6 2005 827 835
65. M.M. Wong, and E.N. Fish Chemokines: attractive mediators of the immune response Semin Immunol 15 2003 5 14
66. F. Belema-Bedada, S. Uchida, A. Martire, S. Kostin, and T. Braun Efficient homing of multipotent adult mesenchymal stem cells depends on FROUNT-mediated clustering of CCR2 Cell Stem Cell 2 2008 566 575
67. M. Grunewald, I. Avraham, and Y. Dor VEGF-induced adult neovascularization: recruitment, retention, and role of accessory cells Cell 124 2006 175 189
68. M.S. Penn Importance of the SDF-1:CXCR4 axis in myocardial repair Circ Res 104 10 2009 1133 1135
69. E. Eggenhofer, J.F. Steinmann, and P. Renner Mesenchymal stem cells together with mycophenolate mofetil inhibit antigen presenting cell and T cell infiltration into allogeneic heart grafts Transplant Immunol 24 2011 157 163
70. K. Liu, L. Chi, and L. Guo The interactions between brain microvascular endothelial cells and mesenchymal stem cells under hypoxic conditions Microvasc Res 75 2008 59 67
71. S.H. Jeon, B.C. Chae, and H.A. Kim Mechanisms underlying TGF-beta1-induced expression of VEGF and Flk-1 in mouse macrophages and their implications for angiogenesis J Leukoc Biol 81 2007 557 566
72. J. Yamashita, H. Itoh, and M. Hirashima Flk1-positive cells derived from embryonic stem cells serve as vascular progenitors Nature 408 2000 92 96
73. B. Annabi, Y.T. Lee, and S. Turcotte Hypoxia promotes murine bone-marrow-derived stromal cell migration and tube formation Stem Cells 21 2003 337 347
74. C.W. Pugh, and P.J. Ratcliffe Regulation of angiogenesis by hypoxia: role of the HIF system Nat Med 9 2003 677 684
75. G.L. Semenza Hypoxia-inducible factor 1 (HIF-1) pathway Sci STKE 2007 cm8.
76. R.H. Wenger, D.P. Stiehl, and G. Camenisch Integration of oxygen signaling at the consensus HRE Sci STKE 2005 re12
77. D.B.S. Mendonça, G. Mendonça, F.J.L. Aragao, and L.F. Cooper NF-jB suppresses HIF-1a response by competing for P300 binding Biochem Biophys Res Commun 404 2001 997 1003
78. J.L. Lin, M.J. Wang, D. Lee, C.C. Liang, and S. Lin Hypoxia-inducible factor-1a regulates matrix metalloproteinase-1 activity in human bone marrow-derived mesenchymal stem cells FEBS Lett 582 2008 2615 2619
79. O. Levy, T. Dvirb, O. Tsur-Gangb, Y. Granot, and S. Cohenb Signal transducer and activator of transcription 3 - A key molecular switch for human mesenchymal stem cell proliferation Int J Bioche Cell Biol 40 2008 2606 2618
80. D.D. Deo, T.W. Axelrad, E.G. Robert, V. Marcheselli, N.G. Bazan, and J.D. Hunt Phosphorylation of STAT-3 in response to basic fibroblast growth factor occurs through a mechanism involving platelet-activating factor, JAK-2, and Src in human umbilical vein endothelial cells. Evidence for a dual kinase mechanism J Biol Chem 277 2002 21237 21245
81. M. Tsang, and I.B. Dawid Promotion and attenuation of FGF signaling through the Ras-MAPK pathway Sci STKE 2004 pe17
82. R. Treisman Regulation of transcription by MAPkinase cascades Curr Opin Cell Biol 8 1996 205 215
83. T. Kisseleva, S. Bhattacharya, J. Braunstein, and C.W. Schindler Signaling through the JAK/STAT pathway, recent advances and future challenges Gene 285 2002 1 24
84. D.S. Aaronson, and C.M. Horvath A road map for those who don't know JAK-STAT Science 296 2002 1653 1655
85. T. Decker, and P. Kovarik Serine phosphorylation of STATs Oncogene 19 2000 2628 2637
86. Y. HonczarenkoM, Le, M. Swierkowski, I. Ghiran, A.M. Glodek, and L.E. Silberstein Human bone marrow stromal cells express a distinct set of biologically functional chemokine receptors Stem Cells 24 2006 1030 1041
87. L. Longobardi, L. ORear, and S. Aakula Effect of IGF-I in the chondrogenesis of bone marrow mesenchymal stem cells in the presence or absence of TGF-beta signaling J Bone Miner Res 21 2006 626 636
88. W. Zhu, J. Chen, X. Cong, S. Hu, and X. Chen Hypoxia and serum deprivation-induced apoptosis in mesenchymal stem cells Stem Cells 24 2 2006 416 425
89. K.M. Peterson, A. Aly, A. Lerman, L.O. Lerman, and M. Rodriguez-Porcel Improved survival of mesenchymal stromal cell after hypoxia preconditioning: Role of oxidative stress Life Sci 88 2011 65 73
90. C. Fehrer, R. Brunauer, and G. Laschober Reduced oxygen tension attenuates differentiation capacity of human mesenchymal stem cells and prolongs their lifespan Aging Cell 6 2007 745 757
91. J.A. Wang, T.L. Chen, and J. Jiang Hypoxic preconditioning attenuates hypoxia/reoxygenation-induced apoptosis in mesenchymal stem cells Acta Pharmacol Sin 29 1 2008 74 82
92. H. Ren, D. Accili, and C. Duan Hypoxia converts the myogenic action of insulin-like growth factors into mitogenic action by differentially regulating multiple signaling pathways Proc Natl Acad Sci U S A 107 13 2010 5857 5862
93. M. Ushio-Fukai, and N. Urao Novel role of NAD(P)H oxidase in angiogenesis and stem/progenitor cell function Antioxid Redox Signal 11 10 2009 2517 2533
94. R. Xu, J. Chen, X. Cong, S. Hu, and X. Chen Lovastatin protects mesenchymal stem cells against hypoxia and serum deprivation-induced apoptosis by activation of PI3K/Akt and ERK1/2 J Cell Biochem 103 1 2008 256 269
95. Y. Jin, T. Kato, M. Furu, A. Nasu, Y. Kajita, and H. Mitsui Mesenchymal stem cells cultured under hypoxia escape from senescence via down-regulation of p16 and extracellular signal regulated kinase Biochem Biophys Res Commun 391 2010 1471 1476
96. R.K. Jaiswal, N. Jaiswal, S.P. Bruder, G. Mbalaviele, D.R. Marshak, and M.F. Pittenger Adult human mesenchymal stem cell differentiation to the osteogenic or adipogenic lineage is regulated by mitogen-activated protein kinase J Biol Chem 275 2000 9645 9652
97. M. Kanichai, D. Ferguson, P.J. Prendergast, and V.A. Campbell Hypoxia promotes chondrogenesis in rat mesenchymal stem cells: a role for Akt and hypoxia-inducible factor (HIF)-1alpha J Cell Physiol 216 3 2008 708 715
98. F.X. Zhang, M.L. Chen, and Q.J. Shan Hypoxia reoxygenation induces premature senescence in neonatal SD rat cardiomyocytes Acta Pharmacol Sin 28 2007 44 51
99. D.G. Yang, L. Liu, and X.Y. Zheng Cyclin-dependent kinase inhibitor p16INK4a and telomerase may co-modulate endothelial progenitor cells senescence Ageing Re Rev 7 2008 137 146
100. A. Takahashi, N. Ohtani, and K. Yamakoshi Mitogenic signalling and the p16INK4a-Rb pathway cooperate to enforce irreversible cellular senescence Nat Cell Biol 8 2006 1291 1297
101. M. Di Nicola, C. Carlo- Stella, and M. Magni Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli Blood 99 2000 3838 3843
102. K. Le Blanc Immunomodulatory effects of fetal and adult mesenchymal stem cells Cytotherapy 5 2003 485 489
103. W.T. Tse, J.D. Pendleton, W.M. Beyer, M.C. Egalka, and E.C. Guinan Suppression of allogeneic T-cell proliferation by human marrow stromal cells: implications in transplantation Transplantation 75 2003 389 397
104. R. Ramasamy, C.K. Tong, H.F. Seow, S. Vidyadaran, and F. Dazzi The immunosuppressive effects of human bone marrow-derived mesenchymal stem cells target T cell proliferation but not its effector function Cell Immunol 251 2008 131 136
105. M. Krampera, S. Glennie, and J. Dyson Bone marrow mesenchymal stem cells inhibit the response of naive and memory antigen-specific T cells to their cognate peptide Blood 101 2003 3722 3729
106. K. Le Blanc, and O. Ringden Immunomodulation by mesenchymal stem cells and clinical experience J Intern Med 262 2007 509 524
107. F.C. Popp, E. Eggenhofer, and P. Renner Mesenchymal stem cells can induce long-term acceptance of solid organ allografts in synergy with low-dose mycophenolate Transpl Immunol 20 1-2 2008 55 60
108. T.B. Prigozhina, S. Khitrin, and G. Elkin Mesenchymal stromal cells lose their immunosuppressive potential after allotransplantation Exp Hematol 36 10 2008 1370 1376
109. G. Ren, L. Zhang, and X. Zhao Mesenchymal stem cell mediated immunosuppression occurs via concerted action of chemokines and nitric oxide Cell Stem Cell 2 2 2008 141 150
110. J. Stagg, S. Pommey, and N. Eliopoulos Interferon-gamma stimulated marrow stromal cells: a new type of nonhematopoietic antigen-presenting cell Blood 107 6 2006 2570 2577
111. P. Renner, E. Eggenhofer, A. Rosenauer, F.C. Popp, J.F. Steinmann, and P. Slowik Mesenchymal stem cells require a sufficient, ongoing immune response to exert their immunosuppressive function Transplant Proc 41 2009 2607 2611
112. J.L. Chan, K.C. Tang, and A.P. Patel Antigen-presenting property of mesenchymal stem cells occurs during a narrow window at low levels of interferon-gamma Blood 107 2006 4817 4824
113. G. Xu, L. Zhang, and G. Ren Immunosuppressive properties of cloned bone marrow mesenchymal stem cells Cell Res 17 2007 240 247
114. A.J. Nauta, and W.E. Fibbe Immunomodulatory properties of mesenchymal stromal cells Blood 110 2007 3499 3506
115. F. Casiraghi, N. Azzollini, and P. Cassis Pre-transplant infusion of mesenchymal stem cells prolongs the survival of a semi-allogeneic heart transplant through the generation of regulatory T cells J Immunol 181 6 2008 3933 3946
116. T. Reya, and H. Clevers Wnt signalling in stem cells and cancer Nature 434 2005 843 850
117. S.H. Baek, C. Kioussi, and P. Briata Regulated subset of G1 growth-control genes in response to derepression by the Wnt pathway Proc Natl Acad Sci U S A 100 2003 3245 3250
118. G. Chen, N. Shukeir, and A. Potti Up-regulation of Wnt-1 and beta-catenin production in patients with advanced metastatic prostate carcinoma: potential pathogenetic and prognostic implications Cancer 101 2004 1345 1356
119. C.A. Gregory, H. Singh, and A.S. Perry The Wnt signaling inhibitor Dickkopf-1 is required for reentry into the cell cycle of human adult stem cells from bone marrow J Biol Chem 278 2003 28067 28078
120. L. Qiao, Z.L. Xu, T.J. Zhao, L.H. Ye, and X.D. Zhang Dkk-1 secreted by mesenchymal stem cells inhibits growth of breast cancer cells via depression of Wnt signaling Cancer Lett 269 2008 67 77
121. J. De Boer, H.J. Wang, and C. Van Blitterswijk Effects of Wnt signaling on proliferation and differentiation of human mesenchymal stem cells Tissue Eng 10 2004 393 401
122. Y. Yamaguchi, S. Itami, and H. Watabe Mesenchymal-epithelial interactions in the skin: increased expression of dickkopf1 by palmoplantar fibroblasts inhibits melanocyte growth and differentiation J Cell Biol 165 2004 275 285
123. M.V. Semenov, K. Tamai, B.K. Brott, M. Kuhl, S. Sokol, and X. He Head inducer Dickkopf-1 is a ligand for Wnt coreceptor LRP6 Curr Biol 11 2001 951 961
124. B.K. Brott, and S.K. Sokol Regulation of Wnt/LRP signaling by distinct domains of Dickkopf proteins Mol Cell Biol 22 2002 6100 6110
125. L. Ling, V. Nurcombe, and S.M. Cool Wnt signaling controls the fate of mesenchymal stem cells Gene 433 2009 1 7
126. W. Qiu, T.E. Andersen, J. Bollerslev, S. Mandrup, B.M. Abdallah, and M. Kassem Patients with high bone mass phenotype exhibit enhanced osteoblast differentiation and inhibition of adipogenesis of human mesenchymal stem cells J Bone Miner Res 22 2007 1720 1731
127. R.T. Moon, A.D. Kohn, and G.V. De-Ferrari Wnt and betacatenin signalling: diseases and therapies Nat Rev Genet 5 2004 691 701
128. A.Y. Khakoo, S. Pati, and S.A. Anderson Human mesenchymal stem cells exert potent anti-tumourigenic effects in a model of Kaposi's sarcoma J Exp Med 203 2006 1235 1247