Mesenchymal stem/stromal cells as a pharmacological and therapeutic approach to accelerate angiogenesis

Pharmacology and Therapeutics

Volumn 143, Issue 2, 2014, Pages 181-196

  Bronckaers, Annelies ^a   Hilkens, Petra ^a   Martens, Wendy ^a   Gervois, Pascal ^a   Ratajczak, Jessica ^a   Struys, Tom ^a   Lambrichts, Ivo ^a  

^a HASSELT UNIVERSITY   (Belgium)

Author keywords

Angiogenesis; Endothelial differentiation; Gene therapy; Mesenchymal stem stromal cells; Secretome

Indexed keywords

ALPHA INTERFERON; ANGIOGENESIS INHIBITOR; ANGIOGENIC FACTOR; ANGIOPOIETIN 1; BETA INTERFERON; CYTOSINE DEAMINASE; FIBROBLAST GROWTH FACTOR 2; GANCICLOVIR; INTERLEUKIN 12; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; PLACENTAL GROWTH FACTOR; THYMIDINE KINASE; VASCULOTROPIN; CYTOKINE; SIGNAL PEPTIDE;

ANGIOGENESIS; ANGIOGENESIS ASSAY; ARTICLE; BASEMENT MEMBRANE; BLOOD VESSEL; BRAIN ISCHEMIA; CANCER GENE THERAPY; CARCINOGENESIS; CELL FUNCTION; CELL TRANSDIFFERENTIATION; CEREBROVASCULAR ACCIDENT; CHICKEN CHORIOALLANTOIC MEMBRANE ASSAY; ENDOTHELIUM CELL; GENE DELIVERY SYSTEM; GENE TARGETING; HEART INFARCTION; HUMAN; IN VITRO STUDY; IN VIVO STUDY; ISCHEMIA; MESENCHYMAL STEM CELL; MESENCHYMAL STROMA CELL; MOUSE MATRIGEL PLUG ASSAY; NONHUMAN; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; WOUND HEALING; ANIMAL; CARDIOVASCULAR DISEASE; CELL DIFFERENTIATION; GENE TRANSFER; MESENCHYMAL STEM CELL TRANSPLANTATION; METABOLISM; NEOPLASM; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; CARDIOVASCULAR DISEASES; CELL DIFFERENTIATION; CELL TRANSDIFFERENTIATION; CYTOKINES; ENDOTHELIAL CELLS; GENE TRANSFER TECHNIQUES; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; NEOPLASMS; NEOVASCULARIZATION, PHYSIOLOGIC;

EID: 84902537549     PISSN: 01637258     EISSN: 1879016X     Source Type: Journal    
DOI: 10.1016/j.pharmthera.2014.02.013     Document Type: Review

References (176)

1. A. Al-Khaldi, H. Al-Sabti, J. Galipeau, and K. Lachapelle Therapeutic angiogenesis using autologous bone marrow stromal cells: improved blood flow in a chronic limb ischemia model Ann Thorac Surg 75 2003 204 209
2. A. Al-Khaldi, N. Eliopoulos, D. Martineau, L. Lejeune, K. Lachapelle, and J. Galipeau Postnatal bone marrow stromal cells elicit a potent VEGF-dependent neoangiogenic response in vivo Gene Ther 10 2003 621 629
3. F. Alviano, V. Fossati, C. Marchionni, M. Arpinati, L. Bonsi, M. Franchina, G. Lanzoni, S. Cantoni, C. Cavallini, F. Bianchi, P.L. Tazzari, G. Pasquinelli, L. Foroni, C. Ventura, A. Grossi, and G.P. Bagnara Term Amniotic membrane is a high throughput source for multipotent Mesenchymal Stem Cells with the ability to differentiate into endothelial cells in vitro BMC Dev Biol 7 2007 11
4. Anonymous Tissue plasminogen activator for acute ischemic stroke. The National Institute of Neurological Disorders and Stroke rt-PA Stroke Study Group N Engl J Med 333 1995 1581 1587
5. A.M. Aranha, Z. Zhang, K.G. Neiva, C.A. Costa, J. Hebling, and J.E. Nor Hypoxia enhances the angiogenic potential of human dental pulp cells J Endod 36 2010 1633 1637
6. A.G. Arroyo, and M.L. Iruela-Arispe Extracellular matrix, inflammation, and the angiogenic response Cardiovasc Res 86 2010 226 235
7. P. Au, J. Tam, D. Fukumura, and R.K. Jain Bone marrow-derived mesenchymal stem cells facilitate engineering of long-lasting functional vasculature Blood 111 2008 4551 4558
8. K. Bai, Y. Huang, X. Jia, Y. Fan, and W. Wang Endothelium oriented differentiation of bone marrow mesenchymal stem cells under chemical and mechanical stimulations J Biomech 43 2010 1176 1181
9. S.G. Ball, C. Bayley, C.A. Shuttleworth, and C.M. Kielty Neuropilin-1 regulates platelet-derived growth factor receptor signalling in mesenchymal stem cells Biochem J 427 2010 29 40
10. S. Banerjee, D.A. Williamson, N. Habib, and J. Chataway The potential benefit of stem cell therapy after stroke: an update Vasc Health Risk Manag 8 2012 569 580
11. O.Y. Bang, J.S. Lee, P.H. Lee, and G. Lee Autologous mesenchymal stem cell transplantation in stroke patients Ann Neurol 57 2005 874 882
12. E. Ben-Ami, S. Berrih-Aknin, and A. Miller Mesenchymal stem cells as an immunomodulatory therapeutic strategy for autoimmune diseases Autoimmun Rev 10 2011 410 415
13. L.W. Bento, Z. Zhang, A. Imai, F. Nor, Z. Dong, and S. Shi et al. Endothelial differentiation of SHED requires MEK1/ERK signaling J Dent Res 92 2013 51 57
14. G. Bergers, and L.E. Benjamin Tumorigenesis and the angiogenic switch Nat Rev Cancer 3 2003 401 410
15. S.V. Bhadada, B.R. Goyal, and M.M. Patel Angiogenic targets for potential disorders Fundam Clin Pharmacol 25 2011 29 47
16. P. Bianco, P.G. Robey, and P.J. Simmons Mesenchymal stem cells: revisiting history, concepts, and assays Cell Stem Cell 2 2008 313 319
17. K. Bieback, P. Wuchter, D. Besser, W. Franke, M. Becker, and M. Ott et al. Mesenchymal stromal cells (MSCs): science and f(r)iction J Mol Med (Berl) 90 2012 773 782
18. G.J. Block, S. Ohkouchi, F. Fung, J. Frenkel, C. Gregory, and R. Pochampally et al. Multipotent stromal cells are activated to reduce apoptosis in part by upregulation and secretion of stanniocalcin-1 Stem Cells 27 2009 670 681
19. R.A. Boomsma, and D.L. Geenen Mesenchymal stem cells secrete multiple cytokines that promote angiogenesis and have contrasting effects on chemotaxis and apoptosis PLoS One 7 2012 e35685
20. A. Bronckaers, P. Hilkens, Y. Fanton, T. Struys, P. Gervois, and C. Politis et al. Angiogenic properties of human dental pulp stem cells PLoS One 8 2013 e71104
21. R. Brown Adam and Victor's Principles of Neurology 8th ed. 2005 McGraw Hill
22. A. Burlacu, G. Grigorescu, A.M. Rosca, M.B. Preda, and M. Simionescu Factors secreted by mesenchymal stem cells and endothelial progenitor cells have complementary effects on angiogenesis in vitro Stem Cells Dev 22 2013 643 653
23. A.I. Caplan, and D. Correa The MSC: an injury drugstore Cell Stem Cell 9 2011 11 15
24. P. Carmeliet Angiogenesis in life, disease and medicine Nature 438 2005 932 936
25. P. Carmeliet, and R.K. Jain Molecular mechanisms and clinical applications of angiogenesis Nature 473 2011 298 307
26. P. Carmeliet, and R.K. Jain Principles and mechanisms of vessel normalization for cancer and other angiogenic diseases Nat Rev Drug Discov 10 2011 417 427
27. S.L. Chen, W.W. Fang, F. Ye, Y.H. Liu, J. Qian, and S.J. Shan et al. 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 2004 92 95
28. X. Chen, X. Lin, J. Zhao, W. Shi, H. Zhang, and Y. Wang et al. A tumor-selective biotherapy with prolonged impact on established metastases based on cytokine gene-engineered MSCs Mol Ther 16 2008 749 756
29. L. Chen, E.E. Tredget, P.Y. Wu, and Y. Wu Paracrine factors of mesenchymal stem cells recruit macrophages and endothelial lineage cells and enhance wound healing PLoS One 3 2008 e1886
30. J. Chen, Z.G. Zhang, Y. Li, L. Wang, Y.X. Xu, and S.C. Gautam et al. Intravenous administration of human bone marrow stromal cells induces angiogenesis in the ischemic boundary zone after stroke in rats Circ Res 92 2003 692 699
31. M.Y. Chen, P.C. Lie, Z.L. Li, and X. Wei Endothelial differentiation of Wharton's jelly-derived mesenchymal stem cells in comparison with bone marrow-derived mesenchymal stem cells Exp Hematol 37 2009 629 640
32. M. Choi, H.S. Lee, P. Naidansaren, H.K. Kim, E. O, and J.H. Cha et al. Proangiogenic features of Wharton's jelly-derived mesenchymal stromal/stem cells and their ability to form functional vessels Int J Biochem Cell Biol 45 2013 560 570
33. N. Chung, B.K. Jee, S.W. Chae, Y.W. Jeon, K.H. Lee, and H.K. Rha HOX gene analysis of endothelial cell differentiation in human bone marrow-derived mesenchymal stem cells Mol Biol Rep 36 2009 227 235
34. B.R. Clark, and A. Keating Biology of bone marrow stroma Ann N Y Acad Sci 770 1995 70 78
35. M. Crisan, S. Yap, L. Casteilla, C.W. Chen, M. Corselli, and T.S. Park et al. A perivascular origin for mesenchymal stem cells in multiple human organs Cell Stem Cell 3 2008 301 313
36. 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
37. J. Croitoru-Lamoury, F.M. Lamoury, J.J. Zaunders, L.A. Veas, and B.J. Brew Human mesenchymal stem cells constitutively express chemokines and chemokine receptors that can be upregulated by cytokines, IFN-beta, and Copaxone J Interferon Cytokine Res 27 2007 53 64
38. B.G. Cuiffo, and A.E. Karnoub Mesenchymal stem cells in tumor development: emerging roles and concepts Cell Adh Migr 6 2012 220 230
39. W. Dai, S.L. Hale, B.J. Martin, J.Q. Kuang, J.S. Dow, and L.E. Wold et al. Allogeneic mesenchymal stem cell transplantation in postinfarcted rat myocardium: short- and long-term effects Circulation 112 2005 214 223
40. A. De Luca, M. Gallo, D. Aldinucci, D. Ribatti, L. Lamura, and A. D'Alessio et al. Role of the EGFR ligand/receptor system in the secretion of angiogenic factors in mesenchymal stem cells J Cell Physiol 226 2011 2131 2138
41. M. De Ryck, J. Van Reempts, M. Borgers, A. Wauquier, and P.A. Janssen Photochemical stroke model: flunarizine prevents sensorimotor deficits after neocortical infarcts in rats Stroke 20 1989 1383 1390
42. T. Deuse, C. Peter, P.W. Fedak, T. Doyle, H. Reichenspurner, and W.H. Zimmermann et al. Hepatocyte growth factor or vascular endothelial growth factor gene transfer maximizes mesenchymal stem cell-based myocardial salvage after acute myocardial infarction Circulation 120 2009 S247 S254
43. F. Djouad, P. Plence, C. Bony, P. Tropel, F. Apparailly, and J. Sany et al. Immunosuppressive effect of mesenchymal stem cells favors tumor growth in allogeneic animals Blood 102 2003 3837 3844
44. G.P. Duffy, T. Ahsan, T. O'Brien, F. Barry, and R.M. Nerem Bone marrow-derived mesenchymal stem cells promote angiogenic processes in a time- and dose-dependent manner in vitro Tissue Eng Part A 15 2009 2459 2470
45. R.M. Dwyer, S. Khan, F.P. Barry, T. O'Brien, and M.J. Kerin Advances in mesenchymal stem cell-mediated gene therapy for cancer Stem Cell Res Ther 1 2010 25
46. J.A. Eble, and S. Niland The extracellular matrix of blood vessels Curr Pharm Des 15 2009 1385 1400
47. A. Erices, P. Conget, and J.J. Minguell Mesenchymal progenitor cells in human umbilical cord blood Br J Haematol 109 2000 235 242
48. R. Estrada, N. Li, H. Sarojini, J. An, M.J. Lee, and E. Wang Secretome from mesenchymal stem cells induces angiogenesis via Cyr61 J Cell Physiol 219 2009 563 571
49. V. Falanga, S. Iwamoto, M. Chartier, T. Yufit, J. Butmarc, and N. Kouttab et al. Autologous bone marrow-derived cultured mesenchymal stem cells delivered in a fibrin spray accelerate healing in murine and human cutaneous wounds Tissue Eng 13 2007 1299 1312
50. W. Fan, R. Crawford, and Y. Xiao The ratio of VEGF/PEDF expression in bone marrow mesenchymal stem cells regulates neovascularization Differentiation 81 2011 181 191
51. N. Ferrara, and R.S. Kerbel Angiogenesis as a therapeutic target Nature 438 2005 967 974
52. L.J. Fischer, S. McIlhenny, T. Tulenko, N. Golesorkhi, P. Zhang, and R. Larson et al. Endothelial differentiation of adipose-derived stem cells: effects of endothelial cell growth supplement and shear force J Surg Res 152 2009 157 166
53. J. Folkman Tumor angiogenesis: therapeutic implications N Engl J Med 285 1971 1182 1186
54. A.J. Friedenstein, R.K. Chailakhjan, and K.S. Lalykina The development of fibroblast colonies in monolayer cultures of guinea-pig bone marrow and spleen cells Cell Tissue Kinet 3 1970 393 403
55. A.J. Friedenstein, S. Piatetzky II, and K.V. Petrakova Osteogenesis in transplants of bone marrow cells J Embryol Exp Morphol 16 1966 381 390
56. R.J. Galas Jr., and J.C. Liu Vascular endothelial growth factor does not accelerate endothelial differentiation of human mesenchymal stem cells J Cell Physiol 229 1 2014 90 96 10.1002/jcp.24421
57. M. Galie, G. Konstantinidou, D. Peroni, I. Scambi, C. Marchini, and V. Lisi et al. Mesenchymal stem cells share molecular signature with mesenchymal tumor cells and favor early tumor growth in syngeneic mice Oncogene 27 2008 2542 2551
58. C. Gandia, A. Arminan, J.M. Garcia-Verdugo, E. Lledo, A. Ruiz, and M.D. Minana et al. Human dental pulp stem cells improve left ventricular function, induce angiogenesis, and reduce infarct size in rats with acute myocardial infarction Stem Cells 26 2008 638 645
59. E.J. Gang, J.A. Jeong, S. Han, Q. Yan, C.J. Jeon, and H. Kim In vitro endothelial potential of human UC blood-derived mesenchymal stem cells Cytotherapy 8 2006 215 227
60. J. Goshima, V.M. Goldberg, and A.I. Caplan The osteogenic potential of culture-expanded rat marrow mesenchymal cells assayed in vivo in calcium phosphate ceramic blocks Clin Orthop Relat Res 1991 298 311
61. S. Gronthos, M. Mankani, J. Brahim, P.G. Robey, and S. Shi Postnatal human dental pulp stem cells (DPSCs) in vitro and in vivo Proc Natl Acad Sci U S A 97 2000 13625 13630
62. R. Gruber, B. Kandler, P. Holzmann, M. Vogele-Kadletz, U. Losert, and M.B. Fischer et al. Bone marrow stromal cells can provide a local environment that favors migration and formation of tubular structures of endothelial cells Tissue Eng 11 2005 896 903
63. M. Gutierrez-Fernandez, B. Rodriguez-Frutos, J. Ramos-Cejudo, M. Teresa Vallejo-Cremades, B. Fuentes, and S. Cerdan et al. Effects of intravenous administration of allogenic bone marrow- and adipose tissue-derived mesenchymal stem cells on functional recovery and brain repair markers in experimental ischemic stroke Stem Cell Res Ther 4 2013 11
64. S. Hacein-Bey-Abina, C. von Kalle, M. Schmidt, F. Le Deist, N. Wulffraat, and E. McIntyre et al. A serious adverse event after successful gene therapy for X-linked severe combined immunodeficiency N Engl J Med 348 2003 255 256
65. W. Hacke, G. Donnan, C. Fieschi, M. Kaste, R. von Kummer, and J.P. Broderick et al. Association of outcome with early stroke treatment: pooled analysis of ATLANTIS, ECASS, and NINDS rt-PA stroke trials Lancet 363 2004 768 774
66. B.K. Hall The neural crest and neural crest cells: discovery and significance for theories of embryonic organization J Biosci 33 2008 781 793
67. J.M. Hare, J.H. Traverse, T.D. Henry, N. Dib, R.K. Strumpf, and S.P. Schulman et al. 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
68. S. Harris, M. Craze, J. Newton, M. Fisher, D.T. Shima, and G.M. Tozer et al. Do anti-angiogenic VEGF (VEGFxxxb) isoforms exist? A cautionary tale PLoS One 7 2012 e35231
69. S.P. Herbert, and D.Y. Stainier Molecular control of endothelial cell behaviour during blood vessel morphogenesis Nat Rev Mol Cell Biol 12 2011 551 564
70. A.M. Hocking, and N.S. Gibran Mesenchymal stem cells: paracrine signaling and differentiation during cutaneous wound repair Exp Cell Res 316 2010 2213 2219
71. O. Honmou, K. Houkin, T. Matsunaga, Y. Niitsu, S. Ishiai, and R. Onodera et al. Intravenous administration of auto serum-expanded autologous mesenchymal stem cells in stroke Brain 134 2011 1790 1807
72. E.M. Horwitz, P.L. Gordon, W.K. Koo, J.C. Marx, M.D. Neel, and R.Y. McNall 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 99 2002 8932 8937
73. E.M. Horwitz, K. Le Blanc, M. Dominici, I. Mueller, I. Slaper-Cortenbach, and F.C. Marini et al. Clarification of the nomenclature for MSC: the International Society for Cellular Therapy position statement Cytotherapy 7 2005 393 395
74. Y.L. Hu, Y.H. Fu, Y. Tabata, and J.Q. Gao Mesenchymal stem cells: a promising targeted-delivery vehicle in cancer gene therapy J Control Release 147 2010 154 162
75. 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
76. N. Ikeda, N. Nonoguchi, M.Z. Zhao, T. Watanabe, Y. Kajimoto, and D. Furutama et al. Bone marrow stromal cells that enhanced fibroblast growth factor-2 secretion by herpes simplex virus vector improve neurological outcome after transient focal cerebral ischemia in rats Stroke 36 2005 2725 2730
77. K. Iohara, L. Zheng, H. Wake, M. Ito, J. Nabekura, and H. Wakita et al. A novel stem cell source for vasculogenesis in ischemia: subfraction of side population cells from dental pulp Stem Cells 26 2008 2408 2418
78. T. Iwase, N. Nagaya, T. Fujii, T. Itoh, S. Murakami, and T. Matsumoto et al. Comparison of angiogenic potency between mesenchymal stem cells and mononuclear cells in a rat model of hindlimb ischemia Cardiovasc Res 66 2005 543 551
79. K. Janebodin, Y. Zeng, W. Buranaphatthana, N. Ieronimakis, and M. Reyes VEGFR2-dependent angiogenic capacity of pericyte-like dental pulp stem cells J Dent Res 92 2013 524 531
80. M. Jazayeri, A. Allameh, M. Soleimani, S.H. Jazayeri, A. Piryaei, and S. Kazemnejad Molecular and ultrastructural characterization of endothelial cells differentiated from human bone marrow mesenchymal stem cells Cell Biol Int 32 2008 1183 1192
81. D. Jeon, K. Chu, S.T. Lee, K.H. Jung, J.J. Ban, and D.K. Park et al. Neuroprotective effect of a cell-free extract derived from human adipose stem cells in experimental stroke models Neurobiol Dis 54 2013 414 420
82. E.S. Jeon, I.H. Lee, S.C. Heo, S.H. Shin, Y.J. Choi, and J.H. Park et al. Mesenchymal stem cells stimulate angiogenesis in a murine xenograft model of A549 human adenocarcinoma through an LPA1 receptor-dependent mechanism Biochim Biophys Acta 1801 2010 1205 1213
83. E.A. Jones, S.E. Kinsey, A. English, R.A. Jones, L. Straszynski, and D.M. Meredith et al. Isolation and characterization of bone marrow multipotential mesenchymal progenitor cells Arthritis Rheum 46 2002 3349 3360
84. S. Kachgal, and A.J. Putnam Mesenchymal stem cells from adipose and bone marrow promote angiogenesis via distinct cytokine and protease expression mechanisms Angiogenesis 14 2011 47 59
85. E.R. Kandel, and C. Pittenger The past, the future and the biology of memory storage Philos Trans R Soc Lond B Biol Sci 354 1999 2027 2052
86. M. Kanehira, H. Xin, K. Hoshino, M. Maemondo, H. Mizuguchi, and T. Hayakawa et al. Targeted delivery of NK4 to multiple lung tumors by bone marrow-derived mesenchymal stem cells Cancer Gene Ther 14 2007 894 903
87. J. Karbanova, T. Soukup, J. Suchanek, R. Pytlik, D. Corbeil, and J. Mokry Characterization of dental pulp stem cells from impacted third molars cultured in low serum-containing medium Cells Tissues Organs 193 2011 344 365
88. H. Kawada, J. Fujita, K. Kinjo, Y. Matsuzaki, M. Tsuma, and H. Miyatake et al. Nonhematopoietic mesenchymal stem cells can be mobilized and differentiate into cardiomyocytes after myocardial infarction Blood 104 2004 3581 3587
89. A. Keating Mesenchymal stromal cells: new directions Cell Stem Cell 10 2012 709 716
90. A.Y. Khakoo, S. Pati, S.A. Anderson, W. Reid, M.F. Elshal, and I.I. Rovira et al. Human mesenchymal stem cells exert potent antitumorigenic effects in a model of Kaposi's sarcoma J Exp Med 203 2006 1235 1247
91. G.E. Kilroy, S.J. Foster, X. Wu, J. Ruiz, S. Sherwood, and A. Heifetz et al. Cytokine profile of human adipose-derived stem cells: expression of angiogenic, hematopoietic, and pro-inflammatory factors J Cell Physiol 212 2007 702 709
92. S.W. Kim, H.Z. Zhang, C.E. Kim, J.M. Kim, and M.H. Kim Amniotic mesenchymal stem cells with robust chemotactic properties are effective in the treatment of a myocardial infarction model Int J Cardiol 168 2 2013 1062 1069 10.1016/j.ijcard.2012.11.003 (Epub 2012 Dec 4)
93. T. Kinnaird, E. Stabile, M.S. Burnett, C.W. Lee, S. Barr, and S. Fuchs et al. Marrow-derived stromal cells express genes encoding a broad spectrum of arteriogenic cytokines and promote in vitro and in vivo arteriogenesis through paracrine mechanisms Circ Res 94 2004 678 685
94. T. Kinnaird, E. Stabile, M.S. Burnett, M. Shou, C.W. Lee, and S. Barr et al. Local delivery of marrow-derived stromal cells augments collateral perfusion through paracrine mechanisms Circulation 109 2004 1543 1549
95. A.H. Klopp, A. Gupta, E. Spaeth, M. Andreeff, and F. Marini III Concise review: dissecting a discrepancy in the literature: do mesenchymal stem cells support or suppress tumor growth? Stem Cells 29 2011 11 19
96. M. Konno, T.S. Hamazaki, S. Fukuda, M. Tokuhara, H. Uchiyama, H. Okazawa, H. Okochi, and M. Asashima Efficiently differentiating vascular endothelial cells from adipose tissue-derived mesenchymal stem cells in serum-free culture Biochem Biophys Res Commun 400 2010
97. G.C. Kopen, D.J. Prockop, and D.G. Phinney Marrow stromal cells migrate throughout forebrain and cerebellum, and they differentiate into astrocytes after injection into neonatal mouse brains Proc Natl Acad Sci U S A 96 1999 10711 10716
98. L. Kucerova, M. Matuskova, A. Pastorakova, S. Tyciakova, J. Jakubikova, and R. Bohovic et al. Cytosine deaminase expressing human mesenchymal stem cells mediated tumour regression in melanoma bearing mice J Gene Med 10 2008 1071 1082
99. M. Kudo, A. Aoyama, S. Ichimori, and N. Fukunaga An animal model of cerebral infarction. Homologous blood clot emboli in rats Stroke 13 1982 505 508
100. K. Kurozumi, K. Nakamura, T. Tamiya, Y. Kawano, K. Ishii, and M. Kobune et al. Mesenchymal stem cells that produce neurotrophic factors reduce ischemic damage in the rat middle cerebral artery occlusion model Mol Ther 11 2005 96 104
101. M.M. Lalu, L. McIntyre, C. Pugliese, D. Fergusson, B.W. Winston, and J.C. Marshall et al. Safety of cell therapy with mesenchymal stromal cells (SafeCell): a systematic review and meta-analysis of clinical trials PLoS One 7 2012 e47559
102. M.W. Laschke, Y. Harder, M. Amon, I. Martin, J. Farhadi, and A. Ring et al. Angiogenesis in tissue engineering: breathing life into constructed tissue substitutes Tissue Eng 12 2006 2093 2104
103. K. Le Blanc, C. Tammik, K. Rosendahl, E. Zetterberg, and O. Ringden HLA expression and immunologic properties of differentiated and undifferentiated mesenchymal stem cells Exp Hematol 31 2003 890 896
104. J.S. Lee, J.M. Hong, G.J. Moon, P.H. Lee, Y.H. Ahn, and O.Y. Bang et al. A long-term follow-up study of intravenous autologous mesenchymal stem cell transplantation in patients with ischemic stroke Stem Cells 28 2010 1099 1106
105. M.Y. Lee, J.P. Huang, Y.Y. Chen, J.D. Aplin, Y.H. Wu, and C.Y. Chen et al. Angiogenesis in differentiated placental multipotent mesenchymal stromal cells is dependent on integrin alpha5beta1 PLoS One 4 2009 e6913
106. K.D. Lee, T.K. Kuo, J. Whang-Peng, Y.F. Chung, C.T. Lin, and S.H. Chou et al. In vitro hepatic differentiation of human mesenchymal stem cells Hepatology 40 2004 1275 1284
107. E.Y. Lee, Y. Xia, W.S. Kim, M.H. Kim, T.H. Kim, and K.J. Kim et al. Hypoxia-enhanced wound-healing function of adipose-derived stem cells: increase in stem cell proliferation and up-regulation of VEGF and bFGF Wound Repair Regen 17 2009 540 547
108. J.W. Liu, S. Dunoyer-Geindre, V. Serre-Beinier, G. Mai, J.F. Lambert, and R.J. Fish et al. Characterization of endothelial-like cells derived from human mesenchymal stem cells J Thromb Haemost 5 2007 826 834
109. Y. Liu, Z.P. Han, S.S. Zhang, Y.Y. Jing, X.X. Bu, and C.Y. Wang et al. Effects of inflammatory factors on mesenchymal stem cells and their role in the promotion of tumor angiogenesis in colon cancer J Biol Chem 286 2011 25007 25015
110. S.H. Liu, J.P. Huang, R.K. Lee, M.C. Huang, Y.H. Wu, and C.Y. Chen et al. Paracrine factors from human placental multipotent mesenchymal stromal cells protect endothelium from oxidative injury via STAT3 and manganese superoxide dismutase activation Biol Reprod 82 2010 905 913
111. T.P. Lozito, C.K. Kuo, J.M. Taboas, and R.S. Tuan Human mesenchymal stem cells express vascular cell phenotypes upon interaction with endothelial cell matrix J Cell Biochem 107 2009 714 722
112. X.L. Ma, K.D. Liu, F.C. Li, X.M. Jiang, L. Jiang, and H.L. Li Human mesenchymal stem cells increases expression of alpha-tubulin and angiopoietin 1 and 2 in focal cerebral ischemia and reperfusion Curr Neurovasc Res 10 2013 103 111
113. M.K. Majumdar, M.A. Thiede, J.D. Mosca, M. Moorman, and S.L. Gerson Phenotypic and functional comparison of cultures of marrow-derived mesenchymal stem cells (MSCs) and stromal cells J Cell Physiol 176 1998 57 66
114. C. Marchionni, L. Bonsi, F. Alviano, G. Lanzoni, A. Di Tullio, R. Costa, M. Montanari, P.L. Tazzari, F. Ricci, G. Pasquinelli, C. Orrico, A. Grossi, C. Prati, and G.P. Bagnara Angiogenic potential of human dental pulp stromal (stem) cells Int J Immunopathol Pharmacol 22 2009 699 706
115. E. Marshall Gene therapy death prompts review of adenovirus vector Science 286 1999 2244 2245
116. T.M. Maul, D.W. Chew, A. Nieponice, and D.A. Vorp Mechanical stimuli differentially control stem cell behavior: morphology, proliferation, and differentiation Biomech Model Mechanobiol 10 2011 939 953
117. S. Meirelles Lda, A.M. Fontes, D.T. Covas, and A.I. Caplan Mechanisms involved in the therapeutic properties of mesenchymal stem cells Cytokine Growth Factor Rev 20 2009 419 427
118. L.G. Menon, V.J. Shi, and R.S. Carroll Mesenchymal Stromal Cells as a Drug Delivery System StemBook 2008 Doug Melton (Harvard Stem Cell Institute, Harvard University) (Cambridge (MA))
119. H. Miletic, Y. Fischer, S. Litwak, T. Giroglou, Y. Waerzeggers, and A. Winkeler et al. Bystander killing of malignant glioma by bone marrow-derived tumor-infiltrating progenitor cells expressing a suicide gene Mol Ther 15 2007 1373 1381
120. Y. Miyahara, N. Nagaya, M. Kataoka, B. Yanagawa, K. Tanaka, and H. Hao et al. Monolayered mesenchymal stem cells repair scarred myocardium after myocardial infarction Nat Med 12 2006 459 465
121. M.H. Moon, S.Y. Kim, Y.J. Kim, S.J. Kim, J.B. Lee, and Y.C. Bae et al. Human adipose tissue-derived mesenchymal stem cells improve postnatal neovascularization in a mouse model of hindlimb ischemia Cell Physiol Biochem 17 2006 279 290
122. S. Nadri, and M. Soleimani Comparative analysis of mesenchymal stromal cells from murine bone marrow and amniotic fluid Cytotherapy 9 2007 729 737
123. A. Nakamizo, F. Marini, T. Amano, A. Khan, M. Studeny, and J. Gumin et al. Human bone marrow-derived mesenchymal stem cells in the treatment of gliomas Cancer Res 65 2005 3307 3318
124. J. Oswald, S. Boxberger, B. Jorgensen, S. Feldmann, G. Ehninger, and M. Bornhauser et al. Mesenchymal stem cells can be differentiated into endothelial cells in vitro Stem Cells 22 2004 377 384
125. K. Otsu, S. Das, S.D. Houser, S.K. Quadri, S. Bhattacharya, and J. Bhattacharya Concentration-dependent inhibition of angiogenesis by mesenchymal stem cells Blood 113 2009 4197 4205
126. D. Pankajakshan, V. Kansal, and D.K. Agrawal In vitro differentiation of bone marrow derived porcine mesenchymal stem cells to endothelial cells J Tissue Eng Regen Med 7 2013 911 920
127. S. Patki, S. Kadam, V. Chandra, and R. Bhonde Human breast milk is a rich source of multipotent mesenchymal stem cells Hum Cell 23 2010 35 40
128. A. Peister, J.A. Mellad, B.L. Larson, B.M. Hall, L.F. Gibson, and D.J. Prockop Adult stem cells from bone marrow (MSCs) isolated from different strains of inbred mice vary in surface epitopes, rates of proliferation, and differentiation potential Blood 103 2004 1662 1668
129. L.K. Phng, and H. Gerhardt Angiogenesis: a team effort coordinated by notch Dev Cell 16 2009 196 208
130. M.F. Pittenger, A.M. Mackay, S.C. Beck, R.K. Jaiswal, R. Douglas, and J.D. Mosca et al. Multilineage potential of adult human mesenchymal stem cells Science 284 1999 143 147
131. C.D. Porada, and G. Almeida-Porada Mesenchymal stem cells as therapeutics and vehicles for gene and drug delivery Adv Drug Deliv Rev 62 2010 1156 1166
132. K.J. Portalska, N. Groen, G. Krenning, N. Georgi, A. Mentink, M.C. Harmsen, C. van Blitterswijk, and J. de Boer The effect of donor variation and senescence on endothelial differentiation of human mesenchymal stromal cells Tissue Eng Part A 19 2013 2318 2329
133. I.A. Potapova, G.R. Gaudette, P.R. Brink, R.B. Robinson, M.R. Rosen, and I.S. Cohen et al. Mesenchymal stem cells support migration, extracellular matrix invasion, proliferation, and survival of endothelial cells in vitro Stem Cells 25 2007 1761 1768
134. M. Potente, H. Gerhardt, and P. Carmeliet Basic and therapeutic aspects of angiogenesis Cell 146 2011 873 887
135. D.J. Prockop, and J.Y. Oh Medical therapies with adult stem/progenitor cells (MSCs): a backward journey from dramatic results in vivo to the cellular and molecular explanations J Cell Biochem 113 2012 1460 1469
136. S.H. Ranganath, O. Levy, M.S. Inamdar, and J.M. Karp Harnessing the mesenchymal stem cell secretome for the treatment of cardiovascular disease Cell Stem Cell 10 2012 244 258
137. J. Rehman, D. Traktuev, J. Li, S. Merfeld-Clauss, C.J. Temm-Grove, and J.E. Bovenkerk et al. Secretion of angiogenic and antiapoptotic factors by human adipose stromal cells Circulation 109 2004 1292 1298
138. D. Ribatti, and E. Crivellato "Sprouting angiogenesis", a reappraisal Dev Biol 372 2012 157 165
139. V.D. Roobrouck, C. Clavel, S.A. Jacobs, F. Ulloa-Montoya, S. Crippa, and A. Sohni et al. Differentiation potential of human postnatal mesenchymal stem cells, mesoangioblasts, and multipotent adult progenitor cells reflected in their transcriptome and partially influenced by the culture conditions Stem Cells 29 2011 871 882
140. C. Ruiz de Almodovar, D. Lambrechts, M. Mazzone, and P. Carmeliet Role and therapeutic potential of VEGF in the nervous system Physiol Rev 89 2009 607 648
141. B. Sacchetti, A. Funari, S. Michienzi, S. Di Cesare, S. Piersanti, and I. Saggio et al. Self-renewing osteoprogenitors in bone marrow sinusoids can organize a hematopoietic microenvironment Cell 131 2007 324 336
142. J.L. Santos, D. Pandita, J. Rodrigues, A.P. Pego, P.L. Granja, and H. Tomas Non-viral gene delivery to mesenchymal stem cells: methods, strategies and application in bone tissue engineering and regeneration Curr Gene Ther 11 2011 46 57
143. M. Sasaki, R. Abe, Y. Fujita, S. Ando, D. Inokuma, and H. Shimizu Mesenchymal stem cells are recruited into wounded skin and contribute to wound repair by transdifferentiation into multiple skin cell type J Immunol 180 2008 2581 2587
144. A. Schiavetta, C. Maione, C. Botti, G. Marino, S. Lillo, and A. Garrone et al. A phase II trial of autologous transplantation of bone marrow stem cells for critical limb ischemia: results of the Naples and Pietra Ligure Evaluation of Stem Cells study Stem Cells Transl Med 1 2012 572 578
145. A. Shabbir, D. Zisa, H. Lin, M. Mastri, G. Roloff, and G. Suzuki et al. Activation of host tissue trophic factors through JAK-STAT3 signaling: a mechanism of mesenchymal stem cell-mediated cardiac repair Am J Physiol Heart Circ Physiol 299 2010 H1428 H1438
146. K. Shah Mesenchymal stem cells engineered for cancer therapy Adv Drug Deliv Rev 64 2012 739 748
147. P.J. Simmons, and B. Torok-Storb Identification of stromal cell precursors in human bone marrow by a novel monoclonal antibody, STRO-1 Blood 78 1991 55 62
148. J.M. Sorrell, M.A. Baber, and A.I. Caplan Influence of adult mesenchymal stem cells on in vitro vascular formation Tissue Eng Part A 15 2009 1751 1761
149. J.L. Spees, S.D. Olson, M.J. Whitney, and D.J. Prockop Mitochondrial transfer between cells can rescue aerobic respiration Proc Natl Acad Sci U S A 103 2006 1283 1288
150. K. Suzuki, R. Sun, M. Origuchi, M. Kanehira, T. Takahata, and J. Itoh et al. Mesenchymal stromal cells promote tumor growth through the enhancement of neovascularization Mol Med 17 2011 579 587
151. M. Takahashi, E. Suzuki, S. Oba, H. Nishimatsu, K. Kimura, and T. Nagano et al. Adipose tissue-derived stem cells inhibit neointimal formation in a paracrine fashion in rat femoral artery Am J Physiol Heart Circ Physiol 298 2010 H415 H423
152. F. Tögel, K. Weiss, Y. Yang, Z. Hu, P. Zhang, and C. Westenfelder Vasculotropic, paracrine actions of infused mesenchymal stem cells are important to the recovery from acute kidney injury Am J Physiol Renal Physiol 292 2007 F1626 1635
153. 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
154. J. Tongers, D.W. Losordo, and U. Landmesser Stem and progenitor cell-based therapy in ischaemic heart disease: promise, uncertainties, and challenges Eur Heart J 32 2011 1197 1206
155. D.O. Traktuev, S. Merfeld-Clauss, J. Li, M. Kolonin, W. Arap, and R. Pasqualini et al. A population of multipotent CD34-positive adipose stromal cells share pericyte and mesenchymal surface markers, reside in a periendothelial location, and stabilize endothelial networks Circ Res 102 2008 77 85
156. L. Tran-Hung, P. Laurent, J. Camps, and I. About Quantification of angiogenic growth factors released by human dental cells after injury Arch Oral Biol 53 2008 9 13
157. R. Ukai, O. Honmou, K. Harada, K. Houkin, H. Hamada, and J.D. Kocsis Mesenchymal stem cells derived from peripheral blood protects against ischemia J Neurotrauma 24 2007 508 520
158. M.T. Valarmathi, J.M. Davis, M.J. Yost, R.L. Goodwin, and J.D. Potts A three-dimensional model of vasculogenesis Biomaterials 30 2009 1098 1112
159. T.I. van der Spoel, S.J. Jansen of Lorkeers, P. Agostoni, E. van Belle, M. Gyongyosi, and J.P. Sluijter et al. Human relevance of pre-clinical studies in stem cell therapy: systematic review and meta-analysis of large animal models of ischaemic heart disease Cardiovasc Res 91 2011 649 658
160. M. van Eekelen, L.S. Sasportas, R. Kasmieh, S. Yip, J.L. Figueiredo, and D.N. Louis et al. Human stem cells expressing novel TSP-1 variant have anti-angiogenic effect on brain tumors Oncogene 29 2010 3185 3195
161. J.C. Voyta, D.P. Via, C.E. Butterfield, and B.R. Zetter Identification and isolation of endothelial cells based on their increased uptake of acetylated-low density lipoprotein J Cell Biol 99 1984 2034 2040
162. J.L. Whyte, S.G. Ball, C.A. Shuttleworth, K. Brennan, and C.M. Kielty
163. V. Windle, A. Szymanska, S. Granter-Button, C. White, R. Buist, and J. Peeling et al. An analysis of four different methods of producing focal cerebral ischemia with endothelin-1 in the rat Exp Neurol 201 2006 324 334
164. K. Wingate, W. Bonani, Y. Tan, S.J. Bryant, and W. Tan Compressive elasticity of three-dimensional nanofiber matrix directs mesenchymal stem cell differentiation to vascular cells with endothelial or smooth muscle cell markers Acta Biomater 8 2012 1440 1449
165. S. Wislet-Gendebien, G. Hans, P. Leprince, J.M. Rigo, G. Moonen, and B. Rogister Plasticity of cultured mesenchymal stem cells: switch from nestin-positive to excitable neuron-like phenotype Stem Cells 23 2005 392 402
166. J. Woolard, H.S. Bevan, S.J. Harper, and D.O. Bates Molecular diversity of VEGF-A as a regulator of its biological activity Microcirculation 16 2009 572 592
167. X. Wu, L. Huang, Q. Zhou, Y. Song, A. Li, J. Jin, and B. Cui Mesenchymal stem cells participating in ex vivo endothelium repair and its effect on vascular smooth muscle cells growth International journal of cardiology 105 2005 274 282
168. C.C. Wu, Y.C. Chao, C.N. Chen, S. Chien, Y.C. Chen, and C.C. Chien et al. Synergism of biochemical and mechanical stimuli in the differentiation of human placenta-derived multipotent cells into endothelial cells J Biomech 41 2008 813 821
169. Y. Wu, L. Chen, P.G. Scott, and E.E. Tredget Mesenchymal stem cells enhance wound healing through differentiation and angiogenesis Stem Cells 25 2007 2648 2659
170. J. Xu, X. Liu, J. Chen, A. Zacharek, X. Cui, and S. Savant-Bhonsale et al. Simvastatin enhances bone marrow stromal cell differentiation into endothelial cells via notch signaling pathway Am J Physiol Cell Physiol 296 2009 C535 C543
171. J. Xu, J. Qu, L. Cao, Y. Sai, C. Chen, and L. He et al. Mesenchymal stem cell-based angiopoietin-1 gene therapy for acute lung injury induced by lipopolysaccharide in mice J Pathol 214 2008 472 481
172. W.M. Yue, W. Liu, Y.W. Bi, X.P. He, W.Y. Sun, and X.Y. Pang et al. Mesenchymal stem cells differentiate into an endothelial phenotype, reduce neointimal formation, and enhance endothelial function in a rat vein grafting model Stem Cells Dev 17 2008 785 793
173. G. Zhang, C.T. Drinnan, L.R. Geuss, and L.J. Suggs Vascular differentiation of bone marrow stem cells is directed by a tunable three-dimensional matrix Acta Biomater 6 2010 3395 3403
174. J. Zhang, Y. Li, Z.G. Zhang, M. Lu, J. Borneman, and B. Buller et al. Bone marrow stromal cells increase oligodendrogenesis after stroke J Cereb Blood Flow Metab 29 2009 1166 1174
175. G. Zhang, J. Zhou, Q. Fan, Z. Zheng, F. Zhang, and X. Liu et al. Arterial-venous endothelial cell fate is related to vascular endothelial growth factor and Notch status during human bone mesenchymal stem cell differentiation FEBS Lett 582 2008 2957 2964
176. P.A. Zuk, M. Zhu, P. Ashjian, D.A. De Ugarte, J.I. Huang, and H. Mizuno et al. Human adipose tissue is a source of multipotent stem cells Mol Biol Cell 13 2002 4279 4295