Ischemic preconditioning for cell-based therapy and tissue engineering

Pharmacology and Therapeutics

Volumn 142, Issue 2, 2014, Pages 141-153

  Hsiao, Sarah T ^a   Dilley, Rodney J ^b   Dusting, Gregory J ^c,d   Lim, Shiang Y ^d  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^c ROYAL VICTORIAN EYE AND EAR HOSPITAL   (Australia)

^d UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Cell therapy; Hypoxic preconditioning; Ischemic preconditioning; Paracrine; Stem cell; Tissue engineering

Indexed keywords

CARDITIS; CELL ACTIVITY; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CELL PROTECTION; CELL SURVIVAL; CELL THERAPY; ENGRAFTMENT; HEART INJURY; HEART VENTRICLE REMODELING; HUMAN; IN VITRO STUDY; IN VIVO STUDY; ISCHEMIC PRECONDITIONING; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; OUTCOME ASSESSMENT; PARACRINE SIGNALING; PRIORITY JOURNAL; REVIEW; STEM CELL; STEM CELL TRANSPLANTATION; TISSUE ENGINEERING; TISSUE REGENERATION; TISSUE REPAIR;

CELL THERAPY; HYPOXIC PRECONDITIONING; ISCHEMIC PRECONDITIONING; PARACRINE; STEM CELL; TISSUE ENGINEERING;

ANIMALS; COMBINED MODALITY THERAPY; HUMANS; ISCHEMIC PRECONDITIONING, MYOCARDIAL; MYOCARDIAL REPERFUSION INJURY; REGENERATION; REGENERATIVE MEDICINE; STEM CELL TRANSPLANTATION; TISSUE ENGINEERING; TREATMENT OUTCOME;

EID: 84896402073     PISSN: 01637258     EISSN: 1879016X     Source Type: Journal    
DOI: 10.1016/j.pharmthera.2013.12.002     Document Type: Review

References (141)

1. A. Aicher, C. Heeschen, K. Sasaki, C. Urbich, A.M. Zeiher, and S. Dimmeler Low-energy shock wave for enhancing recruitment of endothelial progenitor cells: a new modality to increase efficacy of cell therapy in chronic hind limb ischemia Circulation 114 2006 2823 2830
2. T. Akita, T. Murohara, H. Ikeda, K. Sasaki, T. Shimada, K. Egami, and T. Imaizumi Hypoxic preconditioning augments efficacy of human endothelial progenitor cells for therapeutic neovascularization Lab Invest 83 2003 65 73
3. L.C. Amado, A.P. Saliaris, K.H. Schuleri, M. St John, J.S. Xie, S. Cattaneo, D.J. Durand, T. Fitton, J.Q. Kuang, G. Stewart, S. Lehrke, W.W. Baumgartner, B.J. Martin, A.W. Heldman, and J.M. Hare Cardiac repair with intramyocardial injection of allogeneic mesenchymal stem cells after myocardial infarction Proc Natl Acad Sci U S A 102 2005 11474 11479
4. B. Annabi, Y.T. Lee, S. Turcotte, E. Naud, R.R. Desrosiers, M. Champagne, N. Eliopoulos, J. Galipeau, and R. Beliveau Hypoxia promotes murine bone-marrow-derived stromal cell migration and tube formation Stem Cells 21 2003 337 347
5. J. Ara, and S. De Montpellier Hypoxic-preconditioning enhances the regenerative capacity of neural stem/progenitors in subventricular zone of newborn piglet brain Stem Cell Res 11 2013 669 686
6. R. Atoui, and R.C. Chiu Concise review: immunomodulatory properties of mesenchymal stem cells in cellular transplantation: update, controversies, and unknowns Stem Cells Transl Med 1 2012 200 205
7. O. Bergmann, R.D. Bhardwaj, S. Bernard, S. Zdunek, F. Barnabe-Heider, S. Walsh, J. Zupicich, K. Alkass, B.A. Buchholz, H. Druid, S. Jovinge, and J. Frisen Evidence for cardiomyocyte renewal in humans Science 324 2009 98 102
8. A.C. Boquest, A. Shahdadfar, K. Fronsdal, O. Sigurjonsson, S.H. Tunheim, P. Collas, and J.E. Brinchmann Isolation and transcription profiling of purified uncultured human stromal stem cells: alteration of gene expression after in vitro cell culture Mol Biol Cell 16 2005 1131 1141
9. A.I. Caplan, and J.E. Dennis Mesenchymal stem cells as trophic mediators J Cell Biochem 98 2006 1076 1084
10. S.M. Chacko, S. Ahmed, K. Selvendiran, M.L. Kuppusamy, M. Khan, and P. Kuppusamy Hypoxic preconditioning induces the expression of prosurvival and proangiogenic markers in mesenchymal stem cells Am J Physiol Cell Physiol 299 2010 C1562 C1570
11. S. Chen, L. Chen, X. Wu, J. Lin, J. Fang, X. Chen, S. Wei, J. Xu, Q. Gao, and M. Kang Ischemia postconditioning and mesenchymal stem cells engraftment synergistically attenuate ischemia reperfusion-induced lung injury in rats J Surg Res 178 2012 81 91
12. J. Chen, Z.D. Shi, X. Ji, J. Morales, J. Zhang, N. Kaur, and S. Wang Enhanced osteogenesis of human mesenchymal stem cells by periodic heat shock in self-assembling peptide hydrogel Tissue Eng Part A 19 2013 716 728
13. P.R. Crisostomo, Y. Wang, T.A. Markel, M. Wang, T. Lahm, and D.R. Meldrum Human mesenchymal stem cells stimulated by TNF-alpha, LPS, or hypoxia produce growth factors by an NF kappa B- but not JNK-dependent mechanism Am J Physiol Cell Physiol 294 2008 C675 C682
14. J.H. Cui, S.R. Park, K. Park, B.H. Choi, and B.H. Min Preconditioning of mesenchymal stem cells with low-intensity ultrasound for cartilage formation in vivo Tissue Eng 13 2007 351 360
15. W. Dai, S.L. Hale, and R.A. Kloner Role of a paracrine action of mesenchymal stem cells in the improvement of left ventricular function after coronary artery occlusion in rats Regen Med 2 2007 63 68
16. M. Das, and D.K. Das Molecular mechanism of preconditioning IUBMB Life 60 2008 199 203
17. S. De Barros, S. Dehez, E. Arnaud, C. Barreau, A. Cazavet, G. Perez, A. Galinier, L. Casteilla, and V. Planat-Benard Aging-related decrease of human ASC angiogenic potential is reversed by hypoxia preconditioning through ROS production Mol Ther 21 2013 399 408
18. J. Desantiago, D.J. Bare, and K. Banach Ischemia-reperfusion injury protection by mesenchymal stem cell derived antioxidant capacity Stem Cells Dev 22 2013 2497 2507
19. S. Dimmeler, A.M. Zeiher, and M.D. Schneider Unchain my heart: the scientific foundations of cardiac repair J Clin Invest 115 2005 572 583
20. G. D'Ippolito, S. Diabira, G.A. Howard, B.A. Roos, and P.C. Schiller Low oxygen tension inhibits osteogenic differentiation and enhances stemness of human MIAMI cells Bone 39 2006 513 522
21. D.C. Dooley, B.K. Oppenlander, and M. Xiao Analysis of primitive CD34- and CD34+ hematopoietic cells from adults: gain and loss of CD34 antigen by undifferentiated cells are closely linked to proliferative status in culture Stem Cells 22 2004 556 569
22. A. Efimenko, E. Starostina, N. Kalinina, and A. Stolzing Angiogenic properties of aged adipose derived mesenchymal stem cells after hypoxic conditioning J Transl Med 9 2011 10
23. Y. Egashira, S. Sugitani, Y. Suzuki, K. Mishiro, K. Tsuruma, M. Shimazawa, S. Yoshimura, T. Iwama, and H. Hara The conditioned medium of murine and human adipose-derived stem cells exerts neuroprotective effects against experimental stroke model Brain Res 1461 2012 87 95
24. 2 tensions and the prevention of differentiation of hES cells Proc Natl Acad Sci U S A 102 2005 4783 4788
25. J. Fang, L. Chen, L. Fan, L. Wu, X. Chen, W. Li, Y. Lin, and W. Wang Enhanced therapeutic effects of mesenchymal stem cells on myocardial infarction by ischemic postconditioning through paracrine mechanisms in rats J Mol Cell Cardiol 51 2011 839 847
26. T. Fink, L. Abildtrup, K. Fogd, B.M. Abdallah, M. Kassem, P. Ebbesen, and V. Zachar Induction of adipocyte-like phenotype in human mesenchymal stem cells by hypoxia Stem Cells 22 2004 1346 1355
27. F. Fleissner, and T. Thum Critical role of the nitric oxide/reactive oxygen species balance in endothelial progenitor dysfunction Antioxid Redox Signal 15 2011 933 948
28. K.R. Francis, and L. Wei Human embryonic stem cell neural differentiation and enhanced cell survival promoted by hypoxic preconditioning Cell Death Dis 1 2010 e22
29. K. Fuse, M. Kodama, H. Hanawa, Y. Okura, M. Ito, T. Shiono, S. Maruyama, S. Hirono, K. Kato, K. Watanabe, and Y. Aizawa Enhanced expression and production of monocyte chemoattractant protein-1 in myocarditis Clin Exp Immunol 124 2001 346 352
30. L. Gepstein, C. Ding, D. Rahmutula, E.E. Wilson, L. Yankelson, O. Caspi, A. Gepstein, I. Huber, and J.E. Olgin In vivo assessment of the electrophysiological integration and arrhythmogenic risk of myocardial cell transplantation strategies Stem Cells 28 2010 2151 2161
31. M. Gnecchi, H. He, O.D. Liang, L.G. Melo, F. Morello, H. Mu, N. Noiseux, L. Zhang, R.E. Pratt, J.S. Ingwall, and V.J. Dzau Paracrine action accounts for marked protection of ischemic heart by Akt-modified mesenchymal stem cells Nat Med 11 2005 367 368
32. M. Gnecchi, H. He, N. Noiseux, O.D. Liang, L. Zhang, F. Morello, H. Mu, L.G. Melo, R.E. Pratt, J.S. Ingwall, and V.J. Dzau Evidence supporting paracrine hypothesis for Akt-modified mesenchymal stem cell-mediated cardiac protection and functional improvement FASEB J 20 2006 661 669
33. W.L. Grayson, F. Zhao, B. Bunnell, and T. Ma Hypoxia enhances proliferation and tissue formation of human mesenchymal stem cells Biochem Biophys Res Commun 358 2007 948 953
34. M. Gyongyosi, A. Posa, N. Pavo, R. Hemetsberger, H. Kvakan, S. Steiner-Boker, Z. Petrasi, F. Manczur, I.J. Pavo, I.F. Edes, J. Wojta, D. Glogar, and K. Huber Differential effect of ischaemic preconditioning on mobilisation and recruitment of haematopoietic and mesenchymal stem cells in porcine myocardial ischaemia-reperfusion Thromb Haemost 104 2010 376 384
35. K.H. Haider, H.W. Kim, and M. Ashraf Hypoxia-inducible factor-1alpha in stem cell preconditioning: mechanistic role of hypoxia-related micro-RNAs J Thorac Cardiovasc Surg 138 2009 257
36. P.A. Hall, and F.M. Watt Stem cells: the generation and maintenance of cellular diversity Development 106 1989 619 633
37. D.J. Hausenloy, and D.M. Yellon The therapeutic potential of ischemic conditioning: an update Nat Rev Cardiol 8 2011 619 629
38. A. He, Y. Jiang, C. Gui, Y. Sun, J. Li, and J.A. Wang The antiapoptotic effect of mesenchymal stem cell transplantation on ischemic myocardium is enhanced by anoxic preconditioning Can J Cardiol 25 2009 353 358
39. S.T. Hollenbeck, A. Senghaas, I. Komatsu, Y. Zhang, D. Erdmann, and B. Klitzman Tissue engraftment of hypoxic-preconditioned adipose-derived stem cells improves flap viability Wound Repair Regen 20 2012 872 878
40. R.E. Horton, and D.T. Auguste Synergistic effects of hypoxia and extracellular matrix cues in cardiomyogenesis Biomaterials 33 2012 6313 6319
41. J.F. Hou, H. Zhang, X. Yuan, J. Li, Y.J. Wei, and S.S. Hu In vitro effects of low-level laser irradiation for bone marrow mesenchymal stem cells: proliferation, growth factors secretion and myogenic differentiation Lasers Surg Med 40 2008 726 733
42. S.T. Hsiao, Z. Lokmic, H. Peshavariya, K.M. Abberton, G.J. Dusting, S.Y. Lim, and R.J. Dilley Hypoxic conditioning enhances the angiogenic paracrine activity of human adipose-derived stem cells Stem Cells Dev 22 2013 1614 1623
43. X. Hu, L. Wei, T.M. Taylor, J. Wei, X. Zhou, J.A. Wang, and S.P. Yu Hypoxic preconditioning enhances bone marrow mesenchymal stem cell migration via Kv2.1 channel and FAK activation Am J Physiol Cell Physiol 301 2011 C362 C372
44. X. Hu, S.P. Yu, J.L. Fraser, Z. Lu, M.E. Ogle, J.A. Wang, and L. Wei Transplantation of hypoxia-preconditioned mesenchymal stem cells improves infarcted heart function via enhanced survival of implanted cells and angiogenesis J Thorac Cardiovasc Surg 135 2008 799 808
45. S.C. Hung, R.R. Pochampally, S.C. Chen, S.C. Hsu, and D.J. Prockop 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 2007 2363 2370
46. S.C. Hung, R.R. Pochampally, S.C. Hsu, C. Sanchez, S.C. Chen, J. Spees, and D.J. Prockop 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 2007 e416
47. H.J. Hwang, W. Chang, B.W. Song, H. Song, M.J. Cha, I.K. Kim, S. Lim, E.J. Choi, O. Ham, S.Y. Lee, J. Shim, B. Joung, H.N. Pak, S.S. Kim, B.R. Choi, Y. Jang, M.H. Lee, and K.C. Hwang Antiarrhythmic potential of mesenchymal stem cell is modulated by hypoxic environment J Am Coll Cardiol 60 2012 1698 1706
48. M. Ii, H. Nishimura, A. Iwakura, A. Wecker, E. Eaton, T. Asahara, and D.W. Losordo Endothelial progenitor cells are rapidly recruited to myocardium and mediate protective effect of ischemic preconditioning via 'imported' nitric oxide synthase activity Circulation 111 2005 1114 1120
49. J. Jaderstad, H. Brismar, and E. Herlenius Hypoxic preconditioning increases gap-junctional graft and host communication Neuroreport 21 2010 1126 1132
50. S. Janssens Stem cells in the treatment of heart disease Annu Rev Med 61 2010 287 300
51. C.H. Jeong, H.J. Lee, J.H. Cha, J.H. Kim, K.R. Kim, D.K. Yoon, and K.W. Kim Hypoxia-inducible factor-1 alpha inhibits self-renewal of mouse embryonic stem cells in vitro via negative regulation of the leukemia inhibitory factor-STAT3 pathway J Biol Chem 282 2007 13672 13679
52. M.F. Jimenez-Navarro, J. Caballero-Borrego, N. Rodriguez-Losada, F. Cabrera-Bueno, J.A. Marchal, J. Estebaranz, A. Munoz-Garcia, M. Peran, R. Perez, G. Ramirez, J.M. Hernandez-Garcia, A. Aranega, and E. de Teresa Galvan Influence of preinfarction angina on the release kinetics of endothelial progenitor cells and cytokines during the week after infarction Eur J Clin Invest 41 2011 1220 1226
53. H. Jung, H.H. Kim, D.H. Lee, Y.S. Hwang, H.C. Yang, and J.C. Park Transforming growth factor-beta 1 in adipose derived stem cells conditioned medium is a dominant paracrine mediator determines hyaluronic acid and collagen expression profile Cytotechnology 63 2011 57 66
54. H. Kamihata, H. Matsubara, T. Nishiue, S. Fujiyama, Y. Tsutsumi, R. Ozono, H. Masaki, Y. Mori, O. Iba, E. Tateishi, A. Kosaki, S. Shintani, T. Murohara, T. Imaizumi, and T. Iwasaka Implantation of bone marrow mononuclear cells into ischemic myocardium enhances collateral perfusion and regional function via side supply of angioblasts, angiogenic ligands, and cytokines Circulation 104 2001 1046 1052
55. T. Kamota, T.S. Li, N. Morikage, M. Murakami, M. Ohshima, M. Kubo, T. Kobayashi, A. Mikamo, Y. Ikeda, M. Matsuzaki, and K. Hamano Ischemic pre-conditioning enhances the mobilization and recruitment of bone marrow stem cells to protect against ischemia/reperfusion injury in the late phase J Am Coll Cardiol 53 2009 1814 1822
56. R.M. Kanashiro-Takeuchi, I.H. Schulman, and J.M. Hare Pharmacologic and genetic strategies to enhance cell therapy for cardiac regeneration J Mol Cell Cardiol 51 2011 619 625
57. K. Kikuchi, and K.D. Poss Cardiac regenerative capacity and mechanisms Annu Rev Cell Dev Biol 28 2012 719 741
58. H. Kim, K. Choi, O.K. Kweon, and W.H. Kim Enhanced wound healing effect of canine adipose-derived mesenchymal stem cells with low-level laser therapy in athymic mice J Dermatol Sci 68 2012 149 156
59. H.W. Kim, H.K. Haider, S. Jiang, and M. Ashraf Ischemic preconditioning augments survival of stem cells via miR-210 expression by targeting caspase-8-associated protein 2 J Biol Chem 284 2009 33161 33168
60. J.H. Kim, S.Y. Song, S.G. Park, S.U. Song, Y. Xia, and J.H. Sung Primary involvement of NADPH oxidase 4 in hypoxia-induced generation of reactive oxygen species in adipose-derived stem cells Stem Cells Dev 21 2012 2212 2221
61. T. Kinnaird, E. Stabile, M.S. Burnett, C.W. Lee, S. Barr, S. Fuchs, and S.E. Epstein 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 2004 678 685
62. M. Kubo, T.S. Li, R. Suzuki, B. Shirasawa, N. Morikage, M. Ohshima, S.L. Qin, and K. Hamano Hypoxic preconditioning increases survival and angiogenic potency of peripheral blood mononuclear cells via oxidative stress resistance Am J Physiol Heart Circ Physiol 294 2008 H590 H595
63. M.V. Kurian, L. Hamilton, J. Keeven, P. Mehl, and J.M. Mullins Enhanced cell survival and diminished apoptotic response to simulated ischemia-reperfusion in H9c2 cells by magnetic field preconditioning Apoptosis 17 2012 1182 1196
64. M.A. Laflamme, J. Gold, C. Xu, M. Hassanipour, E. Rosler, S. Police, V. Muskheli, and C.E. Murry Formation of human myocardium in the rat heart from human embryonic stem cells Am J Pathol 167 2005 663 671
65. M.M. Lalu, L. McIntyre, C. Pugliese, D. Fergusson, B.W. Winston, J.C. Marshall, J. Granton, and D.J. Stewart Safety of cell therapy with mesenchymal stromal cells (SafeCell): a systematic review and meta-analysis of clinical trials PLoS One 7 2012 e47559
66. 2+/PKC, MAPKs and HIF-1alpha Cell Physiol Biochem 19 2007 269 282
67. H. Lee, J.E. Kang, J.K. Lee, J.S. Bae, and H.K. Jin Bone marrow-derived mesenchymal stem cells promote proliferation and neuronal differentiation of Niemann-Pick type C mouse neural stem cells by upregulation and secretion of CCL2 Hum Gene Ther 24 2013 655 669
68. D.P. Lennon, J.M. Edmison, and A.I. Caplan Cultivation of rat marrow-derived mesenchymal stem cells in reduced oxygen tension: effects on in vitro and in vivo osteochondrogenesis J Cell Physiol 187 2001 345 355
69. L. Leroux, B. Descamps, N.F. Tojais, B. Seguy, P. Oses, C. Moreau, D. Daret, Z. Ivanovic, J.M. Boiron, J.M. Lamaziere, P. Dufourcq, T. Couffinhal, and C. Duplaa Hypoxia preconditioned mesenchymal stem cells improve vascular and skeletal muscle fiber regeneration after ischemia through a Wnt4-dependent pathway Mol Ther 18 2010 1545 1552
70. T.S. Li, K. Hamano, K. Suzuki, H. Ito, N. Zempo, and M. Matsuzaki Improved angiogenic potency by implantation of ex vivo hypoxia prestimulated bone marrow cells in rats Am J Physiol Heart Circ Physiol 283 2002 H468 H473
71. J.H. Li, N. Zhang, and J.A. Wang Improved anti-apoptotic and anti-remodeling potency of bone marrow mesenchymal stem cells by anoxic pre-conditioning in diabetic cardiomyopathy J Endocrinol Invest 31 2008 103 110
72. S.Y. Lim, and D.J. Hausenloy Remote ischemic conditioning: from bench to bedside Front Physiol 3 2012 27
73. S.Y. Lim, S.T. Hsiao, Z. Lokmic, P. Sivakumaran, G.J. Dusting, and R.J. Dilley Ischemic preconditioning promotes intrinsic vascularization and enhances survival of implanted cells in an in vivo tissue engineering model Tissue Eng Part A 18 2012 2210 2219
74. S.Y. Lim, D.G. Lee, P. Sivakumaran, D. Crombie, J. Slavin, M. Dottori, B. Conley, M. Denham, J. Leung, R. Tee, G.J. Dusting, A. Pebay, and R.J. Dilley In vivo tissue engineering chamber supports human induced pluripotent stem cell survival and rapid differentiation Biochem Biophys Res Commun 422 2012 75 79
75. J.S. Lin, Y.S. Chen, H.S. Chiang, and M.C. Ma Hypoxic preconditioning protects rat hearts against ischaemia-reperfusion injury: role of erythropoietin on progenitor cell mobilization J Physiol 586 2008 5757 5769
76. C.H. Lin, H.T. Lee, S.D. Lee, W. Lee, C.W. Cho, S.Z. Lin, H.J. Wang, H. Okano, C.Y. Su, Y.L. Yu, C.Y. Hsu, and W.C. Shyu Role of HIF-1alpha-activated Epac1 on HSC-mediated neuroplasticity in stroke model Neurobiol Dis 58 2013 76 91
77. A. Linke, P. Muller, D. Nurzynska, C. Casarsa, D. Torella, A. Nascimbene, C. Castaldo, S. Cascapera, M. Bohm, F. Quaini, K. Urbanek, A. Leri, T.H. Hintze, J. Kajstura, and P. Anversa Stem cells in the dog heart are self-renewing, clonogenic, and multipotent and regenerate infarcted myocardium, improving cardiac function Proc Natl Acad Sci U S A 102 2005 8966 8971
78. H. Liu, S. Liu, Y. Li, X. Wang, W. Xue, G. Ge, and X. Luo The role of SDF-1-CXCR4/CXCR7 axis in the therapeutic effects of hypoxia-preconditioned mesenchymal stem cells for renal ischemia/reperfusion injury PLoS One 7 2012 e34608
79. L. Liu, and T.A. Rando Manifestations and mechanisms of stem cell aging J Cell Biol 193 2011 257 266
80. H. Liu, W. Xue, G. Ge, X. Luo, Y. Li, H. Xiang, X. Ding, P. Tian, and X. Tian Hypoxic preconditioning advances CXCR4 and CXCR7 expression by activating HIF-1alpha in MSCs Biochem Biophys Res Commun 401 2010 509 515
81. P. Malladi, Y. Xu, M. Chiou, A.J. Giaccia, and M.T. Longaker Effect of reduced oxygen tension on chondrogenesis and osteogenesis in adipose-derived mesenchymal cells Am J Physiol Cell Physiol 290 2006 C1139 C1146
82. N. Maulik Ischemic preconditioning mediated angiogenic response in the heart Antioxid Redox Signal 6 2004 413 421
83. A. Maurel, K. Azarnoush, L. Sabbah, N. Vignier, M. Le Lorc'h, C. Mandet, A. Bissery, I. Garcin, C. Carrion, M. Fiszman, P. Bruneval, A. Hagege, A. Carpentier, J.T. Vilquin, and P. Menasche Can cold or heat shock improve skeletal myoblast engraftment in infarcted myocardium? Transplantation 80 2005 660 665
84. P. Menasche, O. Alfieri, S. Janssens, W. McKenna, H. Reichenspurner, L. Trinquart, J.T. Vilquin, J.P. Marolleau, B. Seymour, J. Larghero, S. Lake, G. Chatellier, S. Solomon, M. Desnos, and A.A. Hagege The Myoblast Autologous Grafting in Ischemic Cardiomyopathy (MAGIC) trial: first randomized placebo-controlled study of myoblast transplantation Circulation 117 2008 1189 1200
85. D.N. Miniati, and R.C. Robbins Heart transplantation: a thirty-year perspective Annu Rev Med 53 2002 189 205
86. S. Mohsin, S. Siddiqi, B. Collins, and M.A. Sussman Empowering adult stem cells for myocardial regeneration Circ Res 109 2011 1415 1428
87. C. Muir, L.W. Chung, D.D. Carson, and M.C. Farach-Carson Hypoxia increases VEGF-A production by prostate cancer and bone marrow stromal cells and initiates paracrine activation of bone marrow endothelial cells Clin Exp Metastasis 23 2006 75 86
88. C.E. Murry, R.B. Jennings, and K.A. Reimer Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium Circulation 74 1986 1124 1136
89. N. Nagaya, K. Kangawa, T. Itoh, T. Iwase, S. Murakami, Y. Miyahara, T. Fujii, M. Uematsu, H. Ohgushi, M. Yamagishi, T. Tokudome, H. Mori, K. Miyatake, and S. Kitamura Transplantation of mesenchymal stem cells improves cardiac function in a rat model of dilated cardiomyopathy Circulation 112 2005 1128 1135
90. V. Ninichuk, O. Gross, S. Segerer, R. Hoffmann, E. Radomska, A. Buchstaller, R. Huss, N. Akis, D. Schlondorff, and H.J. Anders Multipotent mesenchymal stem cells reduce interstitial fibrosis but do not delay progression of chronic kidney disease in collagen4A3-deficient mice Kidney Int 70 2006 121 129
91. R. Norgaard, M. Kassem, and S.I. Rattan Heat shock-induced enhancement of osteoblastic differentiation of hTERT-immortalized mesenchymal stem cells Ann N Y Acad Sci 1067 2006 443 447
92. J.S. Oh, Y. Ha, S.S. An, M. Khan, W.A. Pennant, H.J. Kim, H. Yoon do, M. Lee, and K.N. Kim Hypoxia-preconditioned adipose tissue-derived mesenchymal stem cell increase the survival and gene expression of engineered neural stem cells in a spinal cord injury model Neurosci Lett 472 2010 215 219
93. S. Ohnishi, H. Ohgushi, S. Kitamura, and N. Nagaya Mesenchymal stem cells for the treatment of heart failure Int J Hematol 86 2007 17 21
94. 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
95. S. Ohnishi, T. Yasuda, S. Kitamura, and N. Nagaya Effect of hypoxia on gene expression of bone marrow-derived mesenchymal stem cells and mononuclear cells Stem Cells 25 2007 1166 1177
96. L.L. Ong, W. Li, J.K. Oldigs, A. Kaminski, B. Gerstmayer, C. Piechaczek, W. Wagner, R.K. Li, N. Ma, and G. Steinhoff Hypoxic/normoxic preconditioning increases endothelial differentiation potential of human bone marrow CD133+ cells Tissue Eng Part C Methods 16 2010 1069 1081
97. L.A. Ortiz, F. Gambelli, C. McBride, D. Gaupp, M. Baddoo, N. Kaminski, and D.G. Phinney Mesenchymal stem cell engraftment in lung is enhanced in response to bleomycin exposure and ameliorates its fibrotic effects Proc Natl Acad Sci U S A 100 2003 8407 8411
98. S. Oyagi, M. Hirose, M. Kojima, M. Okuyama, M. Kawase, T. Nakamura, H. Ohgushi, and K. Yagi Therapeutic effect of transplanting HGF-treated bone marrow mesenchymal cells into CCl4-injured rats J Hepatol 44 2006 742 748
99. D. Patschan, K. Krupincza, S. Patschan, Z. Zhang, C. Hamby, and M.S. Goligorsky Dynamics of mobilization and homing of endothelial progenitor cells after acute renal ischemia: modulation by ischemic preconditioning Am J Physiol Renal Physiol 291 2006 F176 F185
100. 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
101. L. Pilgaard, P. Lund, M. Duroux, H. Lockstone, J. Taylor, J. Emmersen, T. Fink, J. Ragoussis, and V. Zachar Transcriptional signature of human adipose tissue-derived stem cells (hASCs) preconditioned for chondrogenesis in hypoxic conditions Exp Cell Res 315 2009 1937 1952
102. S. Portron, C. Merceron, O. Gauthier, J. Lesoeur, S. Sourice, M. Masson, B.H. Fellah, O. Geffroy, E. Lallemand, P. Weiss, J. Guicheux, and C. Vinatier Effects of in vitro low oxygen tension preconditioning of adipose stromal cells on their in vivo chondrogenic potential: application in cartilage tissue repair PLoS One 8 2013 e62368
103. E. Potier, E. Ferreira, R. Andriamanalijaona, J.P. Pujol, K. Oudina, D. Logeart-Avramoglou, and H. Petite Hypoxia affects mesenchymal stromal cell osteogenic differentiation and angiogenic factor expression Bone 40 2007 1078 1087
104. S.M. Prasad, M. Czepiel, C. Cetinkaya, K. Smigielska, S.C. Weli, H. Lysdahl, A. Gabrielsen, K. Petersen, N. Ehlers, T. Fink, S.L. Minger, and V. Zachar Continuous hypoxic culturing maintains activation of Notch and allows long-term propagation of human embryonic stem cells without spontaneous differentiation Cell Prolif 42 2009 63 74
105. E. Przybyt, G. Krenning, M.G. Brinker, and M.C. Harmsen Adipose stromal cells primed with hypoxia and inflammation enhance cardiomyocyte proliferation rate in vitro through STAT3 and Erk1/2 J Transl Med 11 2013 39
106. M. Ramalho-Santos, S. Yoon, Y. Matsuzaki, R.C. Mulligan, and D.A. Melton "Stemness": transcriptional profiling of embryonic and adult stem cells Science 298 2002 597 600
107. H. Ren, Y. Cao, Q. Zhao, J. Li, C. Zhou, L. Liao, M. Jia, H. Cai, Z.C. Han, R. Yang, G. Chen, and R.C. Zhao Proliferation and differentiation of bone marrow stromal cells under hypoxic conditions Biochem Biophys Res Commun 347 2006 12 21
108. G.Y. Rochefort, B. Delorme, A. Lopez, O. Herault, P. Bonnet, P. Charbord, V. Eder, and J. Domenech Multipotential mesenchymal stem cells are mobilized into peripheral blood by hypoxia Stem Cells 24 2006 2202 2208
109. I. Rosova, M. Dao, B. Capoccia, D. Link, and J.A. Nolta Hypoxic preconditioning results in increased motility and improved therapeutic potential of human mesenchymal stem cells Stem Cells 26 2008 2173 2182
110. W. Rottbauer, S. Just, G. Wessels, N. Trano, P. Most, H.A. Katus, and M.C. Fishman VEGF-PLCgamma1 pathway controls cardiac contractility in the embryonic heart Genes Dev 19 2005 1624 1634
111. A. Salim, R.P. Nacamuli, E.F. Morgan, A.J. Giaccia, and M.T. Longaker Transient changes in oxygen tension inhibit osteogenic differentiation and Runx2 expression in osteoblasts J Biol Chem 279 2004 40007 40016
112. M. Sandri, V. Adams, S. Gielen, A. Linke, K. Lenk, N. Krankel, D. Lenz, S. Erbs, D. Scheinert, F.W. Mohr, G. Schuler, and R. Hambrecht Effects of exercise and ischemia on mobilization and functional activation of blood-derived progenitor cells in patients with ischemic syndromes: results of 3 randomized studies Circulation 111 2005 3391 3399
113. W. Shi, and J. Vinten-Johansen Endogenous cardioprotection by ischaemic postconditioning and remote conditioning Cardiovasc Res 94 2012 206 216
114. S.L. Stubbs, S.T. Hsiao, H.M. Peshavariya, S.Y. Lim, G.J. Dusting, and R.J. Dilley Hypoxic preconditioning enhances survival of human adipose-derived stem cells and conditions endothelial cells in vitro Stem Cells Dev 21 2012 1887 1896
115. H. Suga, J.P. Glotzbach, M. Sorkin, M.T. Longaker, and G.C. Gurtner Paracrine mechanism of angiogenesis in adipose-derived stem cell transplantation Ann Plast Surg 2013 (in press)
116. K. Suzuki, R.T. Smolenski, J. Jayakumar, B. Murtuza, N.J. Brand, and M.H. Yacoub Heat shock treatment enhances graft cell survival in skeletal myoblast transplantation to the heart Circulation 102 2000 III216 III221
117. M. Takahashi, T.S. Li, R. Suzuki, T. Kobayashi, H. Ito, Y. Ikeda, M. Matsuzaki, and K. Hamano Cytokines produced by bone marrow cells can contribute to functional improvement of the infarcted heart by protecting cardiomyocytes from ischemic injury Am J Physiol Heart Circ Physiol 291 2006 H886 H893
118. S.I. Takashima, D. Tempel, and H.J. Duckers Current outlook of cardiac stem cell therapy towards a clinical application Heart 99 2013 1772 1784
119. Y.L. Tang, W. Zhu, M. Cheng, L. Chen, J. Zhang, T. Sun, R. Kishore, M.I. Phillips, D.W. Losordo, and G. Qin Hypoxic preconditioning enhances the benefit of cardiac progenitor cell therapy for treatment of myocardial infarction by inducing CXCR4 expression Circ Res 104 2009 1209 1216
120. R. Tatara, K. Ozaki, Y. Kikuchi, K. Hatanaka, I. Oh, A. Meguro, H. Matsu, K. Sato, and K. Ozawa Mesenchymal stromal cells inhibit Th17 but not regulatory T-cell differentiation Cytotherapy 13 2011 686 694
121. M.H. Theus, L. Wei, L. Cui, K. Francis, X. Hu, C. Keogh, and S.P. Yu In vitro hypoxic preconditioning of embryonic stem cells as a strategy of promoting cell survival and functional benefits after transplantation into the ischemic rat brain Exp Neurol 210 2008 656 670
122. C. Toma, M.F. Pittenger, K.S. Cahill, B.J. Byrne, and P.D. Kessler Human mesenchymal stem cells differentiate to a cardiomyocyte phenotype in the adult murine heart Circulation 105 2002 93 98
123. R. Uemura, M. Xu, N. Ahmad, and M. Ashraf Bone marrow stem cells prevent left ventricular remodeling of ischemic heart through paracrine signaling Circ Res 98 2006 1414 1421
124. J.P. Vacanti, and R. Langer Tissue engineering: the design and fabrication of living replacement devices for surgical reconstruction and transplantation Lancet 354 Suppl. 1 1999 SI32 SI34
125. M.G. Valorani, E. Montelatici, A. Germani, A. Biddle, D. D'Alessandro, R. Strollo, M.P. Patrizi, L. Lazzari, E. Nye, W.R. Otto, P. Pozzilli, and M.R. Alison Pre-culturing human adipose tissue mesenchymal stem cells under hypoxia increases their adipogenic and osteogenic differentiation potentials Cell Prolif 45 2012 225 238
126. E. Volkmer, B.C. Kallukalam, J. Maertz, S. Otto, I. Drosse, H. Polzer, W. Bocker, M. Stengele, D. Docheva, W. Mutschler, and M. Schieker Hypoxic preconditioning of human mesenchymal stem cells overcomes hypoxia-induced inhibition of osteogenic differentiation Tissue Eng Part A 16 2010 153 164
127. J.A. Wang, T.L. Chen, J. Jiang, H. Shi, C. Gui, R.H. Luo, X.J. Xie, M.X. Xiang, and X. Zhang Hypoxic preconditioning attenuates hypoxia/reoxygenation- induced apoptosis in mesenchymal stem cells Acta Pharmacol Sin 29 2008 74 82
128. D.W. Wang, B. Fermor, J.M. Gimble, H.A. Awad, and F. Guilak Influence of oxygen on the proliferation and metabolism of adipose derived adult stem cells J Cell Physiol 204 2005 184 191
129. L. Wei, J.L. Fraser, Z.Y. Lu, X. Hu, and S.P. Yu Transplantation of hypoxia preconditioned bone marrow mesenchymal stem cells enhances angiogenesis and neurogenesis after cerebral ischemia in rats Neurobiol Dis 46 2012 635 645
130. A.R. Williams, and J.M. Hare Mesenchymal stem cells: biology, pathophysiology, translational findings, and therapeutic implications for cardiac disease Circ Res 109 2011 923 940
131. X.J. Xie, J.A. Wang, J. Cao, and X. Zhang Differentiation of bone marrow mesenchymal stem cells induced by myocardial medium under hypoxic conditions Acta Pharmacol Sin 27 2006 1153 1158
132. R.X. Xu, X. Chen, J.H. Chen, Y. Han, and B.M. Han Mesenchymal stem cells promote cardiomyocyte hypertrophy in vitro through hypoxia-induced paracrine mechanisms Clin Exp Pharmacol Physiol 36 2009 176 180
133. Q. Xu, S. Wang, X. Jiang, Y. Zhao, M. Gao, Y. Zhang, X. Wang, K. Tano, M. Kanehara, W. Zhang, and T. Ishida Hypoxia-induced astrocytes promote the migration of neural progenitor cells via vascular endothelial factor, stem cell factor, stromal-derived factor-1alpha and monocyte chemoattractant protein-1 upregulation in vitro Clin Exp Pharmacol Physiol 34 2007 624 631
134. F. Yan, Y. Yao, L. Chen, Y. Li, Z. Sheng, and G. Ma Hypoxic preconditioning improves survival of cardiac progenitor cells: role of stromal cell derived factor-1alpha-CXCR4 axis PLoS One 7 2012 e37948
135. S. Yang, H.M. Sun, J.H. Yan, H. Xue, B. Wu, F. Dong, W.S. Li, F.Q. Ji, and D.S. Zhou Conditioned medium from human amniotic epithelial cells may induce the differentiation of human umbilical cord blood mesenchymal stem cells into dopaminergic neuron-like cells J Neurosci Res 91 2013 978 986
136. J. Yang, H. Zhang, L. Zhao, Y. Chen, H. Liu, and T. Zhang Human adipose tissue-derived stem cells protect impaired cardiomyocytes from hypoxia/reoxygenation injury through hypoxia-induced paracrine mechanism Cell Biochem Funct 30 2012 505 514
137. Y.S. Yoon, N. Lee, and H. Scadova Myocardial regeneration with bone-marrow-derived stem cells Biol Cell 97 2005 253 263
138. V. Zachar, S.M. Prasad, S.C. Weli, A. Gabrielsen, K. Petersen, M.B. Petersen, and T. Fink The effect of human embryonic stem cells (hESCs) long-term normoxic and hypoxic cultures on the maintenance of pluripotency In Vitro Cell Dev Biol Anim 46 2010 276 283
139. M. Zhang, D. Methot, V. Poppa, Y. Fujio, K. Walsh, and C.E. Murry Cardiomyocyte grafting for cardiac repair: graft cell death and anti-death strategies J Mol Cell Cardiol 33 2001 907 921
140. J. Zhang, and J.H. Wang Human tendon stem cells better maintain their stemness in hypoxic culture conditions PLoS One 8 2013 e61424
141. H. Zimmet, P. Porapakkham, Y. Sata, S.J. Haas, S. Itescu, A. Forbes, and H. Krum Short- and long-term outcomes of intracoronary and endogenously mobilized bone marrow stem cells in the treatment of ST-segment elevation myocardial infarction: a meta-analysis of randomized control trials Eur J Heart Fail 14 2012 91 105