Interactions of mesenchymal stem cells with endothelial cells

Stem Cells and Development

Volumn 23, Issue 4, 2014, Pages 319-332

  Nassiri, Seyed Mahdi ^a   Rahbarghazi, Reza ^a  

^a UNIVERSITY OF TEHRAN   (Iran)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENESIS; ANTIANGIOGENIC ACTIVITY; CELL ADHESION; CELL DIFFERENTIATION; CELL INTERACTION; CELL MIGRATION; ENDOTHELIUM CELL; HUMAN; MESENCHYMAL STEM CELL; NEOPLASM; NONHUMAN; PARACRINE SIGNALING; PRIORITY JOURNAL; REVIEW;

ANIMALS; CELL COMMUNICATION; CELL DIFFERENTIATION; ENDOTHELIAL CELLS; HUMANS; MESENCHYMAL STROMAL CELLS; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC;

EID: 84893661701     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2013.0419     Document Type: Review

References (146)

1. Rahbarghazi R, SM Nassiri, P Khazraiinia, AM Kajbafzadeh, SH Ahmadi, E Mohammadi, M Molazem and M Zamani-Ahmadmahmudi. (2013). Juxtacrine and paracrine interactions of rat marrow-derived mesenchymal stem cells, muscle-derived satellite cells, and neonatal cardiomyocytes with endothelial cells in angiogenesis dynamics. Stem Cells Dev 22:855-865.
2. Chavakis E and S Dimmeler. (2002). Regulation of endothelial cell survival and apoptosis during angiogenesis. Arterioscler Thromb Vasc Biol 22:887-893.
3. Ho IAW, HC Toh, WH Ng, YL Teo, CM Guo, KM Hui and PYP Lam. (2013). Human bone marrow-derived mesenchymal stem cells suppress human glioma growth through inhibition of angiogenesis. Stem Cells 31:146-155.
4. Pittenger MF, AM Mackay, SC Beck, RK Jaiswal, R Douglas, JD Mosca, MA Moorman, DW Simonetti, S Craig and DR Marshak. (1999). Multilineage potential of adult human mesenchymal stem cells. Science 284:143-147.
5. Rüster B, S Göttig, RJ Ludwig, R Bistrian, S Müller, E Seifried, J Gille and R Henschler. (2006). Mesenchymal stem cells display coordinated rolling and adhesion behavior on endothelial cells. Blood 108:3938-3944.
6. Veevers-Lowe J, SG Ball, A Shuttleworth and CM Kielty. (2011). Mesenchymal stem cell migration is regulated by fibronectin through a5b1-integrin-mediated activation of PDGFR-b and potentiation of growth factor signals. J Cell Sci 124:1288-1300.
7. Oswald J, S Boxberger, B Jrgensen, S Feldmann, G Ehninger, M Bornhaüser and C Werner. (2004). Mesenchymal stem cells can be differentiated into endothelial cells in vitro. Stem Cells 22:377-384.
8. Silva GV, S Litovsky, JAR Assad, ALS Sousa, BJ Martin, D Vela, SC Coulter, J Lin, J Ober, et al. (2005). Mesenchymal stem cells differentiate into an endothelial phenotype, enhance vascular density, and improve heart function in a canine chronic ischemia model. Circulation 111:150-156.
9. Dhar K, G Dhar, M Majumder, I Haque, S Mehta, PJ Van Veldhuizen, SK Banerjee and S Banerjee. (2010). Tumor cellderived PDGF-B potentiates mouse mesenchymal stem cells-pericytes transition and recruitment through an interaction with NRP-1. Mol Cancer 9:209-221.
10. Chen L, EE Tredget, PYG Wu and Y Wu. (2008). Paracrine factors of mesenchymal stem cells recruit macrophages and endothelial lineage cells and enhance wound healing. PLoS One 3:e1886.
11. Rafii S and D Lyden. (2003). Therapeutic stem and progenitor cell transplantation for organ vascularization and regeneration. Nat Med 9:702-712.
12. Fathke C, L Wilson, J Hutter, V Kapoor, A Smith, A Hocking and F Isik. (2004). Contribution of bone marrow- derived cells to skin: collagen deposition and wound repair. Stem Cells 22:812-822.
13. Otsu K, S Das, SD Houser, SK Quadri, S Bhattacharya and J Bhattacharya. (2009). Concentration-dependent inhibition of angiogenesis by mesenchymal stem cells. Blood 113: 4197-4205.
14. Oh JY, MK Kim, MS Shin, HJ Lee, JH Ko, WR Wee and JH Lee. (2008). The anti-inflammatory and anti-angiogenic role of mesenchymal stem cells in corneal wound healing following chemical injury. Stem Cells 26:1047-1055.
15. Teo GSL, JA Ankrum, R Martinelli, SE Boetto, K Simms, TE Sciuto, AM Dvorak, JM Karp and CV Carman. (2012). Mesenchymal stem cells transmigrate between and directly through tumor necrosis factor-a-activated endothelial cells via both leukocyte-like and novel mechanisms. Stem Cells 30:2472-2486.
16. Ley K, C Laudanna, MI Cybulsky and S Nourshargh. (2007). Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat Rev Immunol 7:678-689.
17. Kasper G, N Dankert, J Tuischer, M Hoeft, T Gaber, JD Glaeser, D Zander, M Tschirschmann, M Thompson, G Matziolis and GN Duda. (2007). Mesenchymal stem cells regulate angiogenesis according to their mechanical environment. Stem Cells 25:903-910.
18. Xue Y, Z Xing, S Hellem, K Arvidson and K Mustafa. (2009). Endothelial cells influence the osteogenic potential of bone marrow stromal cells. Biomed Eng Online 8:34.
19. Semon J, L Nagy, C Llamas, HA Tucker, R Lee and D Prockop. (2010). Integrin expression and integrin-mediated adhesion in vitro of human multipotent stromal cells (MSCs) to endothelial cells from various blood vessels. Cell Tissue Res 341:147-158.
20. Schneider D and DM Engelman. (2004). Involvement of transmembrane domain interactions in signal transduction by a/b Integrins. J Biol Chem 279:9840-9846.
21. Tabe Y, L Jin, Y Tsutsumi-Ishii, Y Xu, T McQueen, W Priebe, GB Mills, A Ohsaka, I Nagaoka, M Andreeff and M Konopleva. (2007). Activation of integrin-linked kinase is a critical prosurvival pathway induced in leukemic cells by bone marrow-derived stromal cells. Cancer Res 67:684-694.
22. Tan C, S Cruet-Hennequart, A Troussard, L Fazli, P Costello, K Sutton, J Wheeler, M Gleave, J Sanghera and S Dedhar. (2004). Regulation of tumor angiogenesis by integrin- linked kinase (ILK). Cancer Cell 5:79-90.
23. Xie W, M Zhao, W Zhou, L Guo, L Huang, W Yu and X Li. (2013). Targeting of integrin-linked kinase with small interfering RNA inhibits VEGF-induced angiogenesis in retinal endothelial cells. Ophthalmic Res 49:139-149.
24. Docheva D, F Haasters and M Schieker. (2008). Mesenchymal stem cells and their cell surface receptors. Curr Rheumatol Rev 4:155-160.
25. Li Y, Y Hiroi and JK Liao. (2010). Notch signaling as an important mediator of cardiac repair and regeneration after myocardial infarction. Trends Cardiovasc Med 20:228-231.
26. Segers VFM, I Van Riet, LJ Andries, K Lemmens, MJ Demolder, AJML De Becker, MM Kockx and GW De Keulenaer. (2006). Mesenchymal stem cell adhesion to cardiac microvascular endothelium: activators and mechanisms. Am J Physiol Heart Circ Physiol 290:H1370-H1377.
27. Isobe M, H Yagita, K Okumura and A Ihara. (1992). Specific acceptance of cardiac allograft after treatment with antibodies to ICAM-1 and LFA-1. Science 255:1125-1127.
28. Chamberlain G, H Smith, GE Rainger and JMiddleton. (2011). Mesenchymal stem cells exhibit firm adhesion, crawling, spreading and transmigration across aortic endothelial cells: effects of chemokines and shear. PLoS One 6:e25663.
29. Zhu H, N Mitsuhashi, A Klein, LW Barsky, K Weinberg, ML Barr, A Demetriou and GD Wu. (2006). The role of the hyaluronan receptor CD44 in mesenchymal stem cell migration in the extracellular matrix. Stem Cells 24:928-935.
30. Zhao W, W Loh, IA Droujinine, W Teo, N Kumar, S Schafer, CH Cui, L Zhang, D Sarkar, R Karnik and JM Karp. (2011). Mimicking the inflammatory cell adhesion cascade by nucleic acid aptamer programmed cell-cell interactions. FASEB J 25:3045-3056.
31. Sackstein R, JS Merzaban, DW Cain, NM Dagia, JA Spencer, CP Lin and R Wohlgemuth. (2008). Ex vivo glycan engineering of CD44 programs human multipotent mesenchymal stromal cell trafficking to bone. Nat Med 14:181-187.
32. Potapova I, I Cohen and S Doronin. (2010). Von willebrand factor increases endothelial cell adhesiveness for human mesenchymal stem cells by activating p38 mitogen-activated protein kinase. Stem Cell Res Ther 1:35.
33. Steingen C, F Brenig, L Baumgartner, J Schmidt, A Schmidt and W Bloch. (2008). Characterization of key mechanisms in transmigration and invasion of mesenchymal stem cells. J Mol Cell Cardiol 44:1072-1084.
34. Haider HK, S Jiang, NM Idris and M Ashraf. (2008). IGF-1- overexpressing mesenchymal stem cells accelerate bone marrow stem cell mobilization via paracrine activation of SDF-1a/CXCR4 signaling to promote myocardial repair. Circ Res 103:1300-1308.
35. Zhang F, C Wang, H Wang, M Lu, Y Li, H Feng, J Lin, Z Yuan and X Wang. (2013). Ox-LDL promotes migration and adhesion of bone marrow-derived mesenchymal stem cells via regulation of MCP-1 expression. Mediators Inflamm 2013:Article ID 691023.
36. Salem HK and C Thiemermann. (2010). Mesenchymal stromal cells: current understanding and clinical status. Stem Cells 28:585-596.
37. Linder S. (2009). Invadosomes at a glance. J Cell Sci 122: 3009-3013.
38. Ringe J, S Strassburg, K Neumann, M Endres, M Notter, GR Burmester, C Kaps and M Sittinger. (2007). Towards in situ tissue repair: Human mesenchymal stem cells express chemokine receptors CXCR1, CXCR2 and CCR2, and migrate upon stimulation with CXCL8 but not CCL2. J Cell Biochem 101:135-146.
39. Smith H, C Whittall, B Weksler and J Middleton. (2011). Chemokines stimulate bidirectional migration of human mesenchymal stem cells across bone marrow endothelial cells. Stem Cells Dev 21:476-486.
40. Johansson U, I Rasmusson, SP Niclou, N Forslund, L Gustavsson, B Nilsson, O Korsgren and PU Magnusson. (2008). Formation of composite endothelial cell-mesenchymal stem cell islets: a novel approach to promote islet revascularization. Diabetes 57:2393-2401.
41. Li N, X Lu, X Zhao, F-L Xiang, A Xenocostas, M Karmazyn and Q Feng. (2009). Endothelial nitric oxide synthase promotes bone marrow stromal cell migration to the ischemic myocardium via upregulation of stromal cell-derived factor- 1a. Stem Cells 27:961-970.
42. Aguirre A, JA Planell and E Engel. (2010). Dynamics of bone marrow-derived endothelial progenitor cell/mesenchymal stem cell interaction in co-culture and its implications in angiogenesis. Biochem Biophys Res Commun 400:284-291.
43. Wang N, R Zhang, S-J Wang, C-L Zhang, L-B Mao, C-Y Zhuang, Y-Y Tang, X-G Luo, H Zhou and T-C Zhang. (2013). Vascular endothelial growth factor stimulates endothelial differentiation from mesenchymal stem cells via Rho/myocardin-related transcription factor-A signaling pathway. Int J Biochem Cell Biol 45:1447-1456.
44. Blocki A, Y Wang, M Koch, P Peh, S Beyer, P Law, J Hui and M Raghunath. (2013). Not all MSCs can act as pericytes: functional in vitro assays to distinguish pericytes from other mesenchymal stem cells in angiogenesis. Stem Cells Dev 22:2347-2355.
45. Chong JJ, H Reinecke, M Iwata, B Torok-Storb, A Stempien- Otero and CE Murry. (2013). Progenitor cells identified by PDGFR-alpha expression in the developing and diseased human heart. Stem Cells Dev 22:1932-1943.
46. Schlosser S, C Dennler, R Schweizer, D Eberli, JV Stein, V Enzmann, P Giovanoli, D Erni and JA Plock. (2012). Paracrine effects of mesenchymal stem cells enhance vascular regeneration in ischemic murine skin. Microvasc Res 83:267-275.
47. Lin RZ, R Moreno-Luna, B Zhou, WT Pu and JM Melero- Martin. (2012). Equal modulation of endothelial cell function by four distinct tissue-specific mesenchymal stem cells. Angiogenesis 15:443-455.
48. Kalinina N, VY Sysoeva, K Rubina, YV Parfenova and V Tkachuk. (2011). Mesenchymal stem cells in tissue growth and repair. Acta Nat 3:30-37.
49. Caplan AI. (2008). All MSCs are pericytes? Cell Stem Cell 3:229-230.
50. Saleh FA, M Whyte, P Ashton and PG Genever. (2010). Regulation of mesenchymal stem cell activity by endothelial cells. Stem Cells Dev 20:391-403.
51. Ball SG, AC Shuttleworth and CM Kielty. (2004). Direct cell contact influences bone marrow mesenchymal stem cell fate. Int J Biochem Cell Biol 36:714-727.
52. Saleh FA, M Whyte and PG Genever. (2011). Effects of endothelial cells on human mesenchymal stem cell activity in a three-dimensional in vitro model. Eur Cell Mater 22:242-257.
53. Pati S, MH Gerber, TD Menge, KA Wataha, Y Zhao, JA Baumgartner, J Zhao, PA Letourneau, MP Huby, et al. (2011). Bone marrow derived mesenchymal stem cells inhibit inflammation and preserve vascular endothelial integrity in the lungs after hemorrhagic shock. PLoS One 6:e25171.
54. Pati S, AY Khakoo, J Zhao, F Jimenez, MH Gerber, M Harting, JB Redell, R Grill, Y Matsuo, et al. (2011). Human mesenchymal stem cells inhibit vascular permeability by modulating vascular endothelial cadherin/beta-catenin signaling. Stem Cells Dev 20:89-101.
55. Menge T, M Gerber, K Wataha, W Reid, S Guha, CS Cox, Jr., P Dash, MS Reitz, Jr., AY Khakoo and S Pati. (2013). Human mesenchymal stem cells inhibit endothelial proliferation and angiogenesis via cell-cell contact through modulation of the VE-Cadherin/beta-catenin signaling pathway. Stem Cells Dev 22:148-157.
56. Stenman JM, J Rajagopal, TJ Carroll, M Ishibashi, J McMahon and AP McMahon. (2008). Canonical Wnt signaling regulates organ-specific assembly and differentiation of CNS vasculature. Science 322:1247-1250.
57. Dufourcq P, B Descamps, NF Tojais, L Leroux, P Oses, D Daret, C Moreau, J-MD Lamazière, T Couffinhal and C Duplaà. (2008). Secreted frizzled-related protein-1 enhances mesenchymal stem cell function in angiogenesis and contributes to neovessel maturation. Stem Cells 26:2991-3001.
58. Alfaro MP, M Pagni, A Vincent, J Atkinson, MF Hill, J Cates, JM Davidson, J Rottman, E Lee and PP Young. (2008). The Wnt modulator sFRP2 enhances mesenchymal stem cell engraftment, granulation tissue formation and myocardial repair. Proc Natl Acad Sci U S A 105:18366-18371.
59. Duffy GP, S DArcy, T Ahsan, RM Nerem, T OBrien and F Barry. (2010). Mesenchymal stem cells overexpressing ephrin-b2 rapidly adopt an early endothelial phenotype with simultaneous reduction of osteogenic potential. Tissue Eng Part A 16:2755-2768.
60. Bidarra SJ, CC Barrias, MA Barbosa, R Soares, J Amédée and PL Granja. (2011). Phenotypic and proliferative modulation of human mesenchymal stem cells via crosstalk with endothelial cells. Stem Cell Res 7:186-197.
61. Sorrell JM, MA Baber and AI Caplan. (2009). Influence of adult mesenchymal stem cells on in vitro vascular formation. Tissue Eng Part A 15:1751-1761.
62. Jimenez E, A Vicente, R Sacedon, JJ Munoz, G Weinmaster, AG Zapata and A Varas. (2001). Distinct mechanisms contribute to generate and change the CD4:CD8 cell ratio during thymus development: a role for the Notch ligand, Jagged1. J Immunol 166:5898-5908.
63. Zacharek A, J Chen, X Cui, A Li, Y Li, C Roberts, Y Feng, Q Gao and M Chopp. (2007). Angiopoietin1/Tie2 and VEGF/ Flk1 induced by MSC treatment amplifies angiogenesis and vascular stabilization after stroke. J Cereb Blood Flow Metab 27:1684-1691.
64. Liu XB, J Jiang, C Gui, XY Hu, MX Xiang and JA Wang. (2008). Angiopoietin-1 protects mesenchymal stem cells against serum deprivation and hypoxia-induced apoptosis through the PI3K/Akt pathway. Acta Pharmacol Sin 29:815-822.
65. Baraniak PR and TC McDevitt. (2010). Stem cell paracrine actions and tissue regeneration. Regen Med 5:121-143.
66. Zhang H-C, X-B Liu, S Huang, X-Y Bi, H-X Wang, L-X Xie, Y-Q Wang, X-F Cao, J Lv and F-J Xiao. (2012). Microvesicles derived from human umbilical cord mesenchymal stem cells stimulated by hypoxia promote angiogenesis both in vitro and in vivo. Stem Cells Dev 21:3289-3297.
67. Baglio SR, DM Pegtel and N Baldini. (2012). Mesenchymal stem cell secreted vesicles provide novel opportunities in (stem) cell-free therapy. Front Physiol 3:359.
68. Kim H-S, D-Y Choi, SJ Yun, S-M Choi, JW Kang, JW Jung, D Hwang, KP Kim and D-W Kim. (2011). Proteomic analysis of microvesicles derived from human mesenchymal stem cells. J Proteome Res 11:839-849.
69. Choi Y-A, J Lim, KM Kim, B Acharya, J-Y Cho, Y-C Bae, HI Shin, S-Y Kim and EK Park. (2010). Secretome analysis of human BMSCs and identification of SMOC1 as an important ECM protein in osteoblast differentiation. J Proteome Res 9:2946-2956.
70. Xin H, Y Li, Y Cui, JJ Yang, ZG Zhang and M Chopp. (2013). Systemic administration of exosomes released from mesenchymal stromal cells promote functional recovery and neurovascular plasticity after stroke in rats. J Cereb Blood Flow Metab 33:1711-1715.
71. Xin H, Y Li, Z Liu, X Wang, X Shang, Y Cui, Z Gang Zhang and M Chopp. (2013). Mir-133b promotes neural plasticity and functional recovery after treatment of stroke with multipotent mesenchymal stromal cells in rats via transfer of exosome-enriched extracellular particles. Stem Cells [Epub ahead of print]; DOI: 10.1002/stem.1409.
72. Lai RC, F Arslan, MM Lee, NS Sze, A Choo, TS Chen, M SaltoTellez, L Timmers, CN Lee, et al. (2010). Exosome secreted by MSC reduces myocardial ischemia/reperfusion injury. Stem Cell Res 4:214-222.
73. Zhu Y-G, X-M Feng, J Abbott, X-H Fang, Q Hao, A Monsel, J-M Qu, MA Matthay and JW Lee. (2013). Human mesenchymal stem cell microvesicles for treatment of E. coli endotoxin-induced acute lung injury in mice. Stem Cells [Epub ahead of print]; DOI: 10.1002/stem.1504.
74. Li T, Y Yan, B Wang, H Qian, X Zhang, L Shen, M Wang, Y Zhou, W Zhu, W Li and W Xu. (2013). Exosomes derived from human umbilical cord mesenchymal stem cells alleviate liver fibrosis. Stem Cells Dev 22:845-854.
75. Maumus M, C Jorgensen and D Noel. (2013). Mesenchymal stem cells in regenerative medicine applied to rheumatic diseases: Role of secretome and exosomes. Biochimie 95:2229-2234.
76. Katakowski M, B Buller, X Zheng, Y Lu, T Rogers, O Osobamiro, W Shu, F Jiang and M Chopp. (2013). Exosomes from marrow stromal cells expressing miR-146b inhibit glioma growth. Cancer Lett 335:201-204.
77. Roccaro AM, A Sacco, P Maiso, AK Azab, YT Tai, M Reagan, F Azab, LM Flores, F Campigotto, et al. (2013). BM mesenchymal stromal cell-derived exosomes facilitate multiple myeloma progression. J Clin Invest 123:1542-1555.
78. Kaigler D, PH Krebsbach, PJ Polverini and DJ Mooney. (2003). Role of vascular endothelial growth factor in bone marrow stromal cell modulation of endothelial cells. Tissue Eng 9:95-103.
79. Burlacu A, G Grigorescu, A-M Rosca, MB Preda and M Simionescu. (2012). Factors secreted by mesenchymal stem cells and endothelial progenitor cells have complementary effects on angiogenesis in vitro. Stem Cells Dev 22:643-653.
80. Findley CM, MJ Cudmore, A Ahmed and CD Kontos. (2007). VEGF induces Tie2 shedding via a phosphoinositide 3-Kinase/Akt-dependent pathway to modulate Tie2 signaling. Arterioscler Thromb Vasc Biol 27:2619-2626.
81. Leroux L, B Descamps, NF Tojais, B Séguy, P Oses, C Moreau, D Daret, Z Ivanovic, J-M Boiron and J-MD Lamaziè re. (2010). Hypoxia preconditioned mesenchymal stem cells improve vascular and skeletal muscle fiber regeneration after ischemia through a Wnt4-dependent pathway. Mol Ther 18:1545-1552.
82. Chang J, W Sonoyama, Z Wang, Q Jin, C Zhang, PH Krebsbach, W Giannobile, S Shi and C-Y Wang. (2007). Noncanonical Wnt-4 signaling enhances bone regeneration of mesenchymal stem cells in craniofacial defects through activation of p38 MAPK. J Biol Chem 282:30938-30948.
83. Kasper G, JD Glaeser, S Geissler, A Ode, J Tuischer, G Matziolis, C Perka and GN Duda. (2007). Matrix metalloprotease activity is an essential link between mechanical stimulus and mesenchymal stem cell behavior. Stem Cells 25:1985-1994.
84. Ghajar CM, KS Blevins, CC Hughes, SC George and AJ Putnam. (2006). Mesenchymal stem cells enhance angiogenesis in mechanically viable prevascularized tissues via early matrix metalloproteinase upregulation. Tissue Eng 12:2875-2888.
85. Portalska KJ, A Leferink, N Groen, H Fernandes, L Moroni, C van Blitterswijk and J de Boer. (2012). Endothelial differentiation of mesenchymal stromal cells. PLoS One 7:e46842.
86. Nassiri SM, Z Khaki, M Soleimani, SH Ahmadi, I Jahanzad, S Rabbani, M Sahebjam, FA Ardalan and MS Fathollahi. (2007). The similar effect of transplantation of marrowderived mesenchymal stem cells with or without prior differentiation induction in experimental myocardial infarction. J Biomed Sci 14:745-755.
87. Vittorio O, E Jacchetti, S Pacini and M Cecchini. (2013). Endothelial differentiation of mesenchymal stromal cells: when traditional biology meets mechanotransduction. Integr Biol 5:291-299.
88. Lionetti V, M Cecchini and C Ventura. (2010). Nanomechanics to drive stem cells in injured tissues: insights from current research and future perspectives. Stem Cells Dev 20:561-568.
89. Portalska KJ, A Leferink, N Groen, H Fernandes, L Moroni, C van Blitterswijk and J de Boer. (2012). Endothelial differentiation of mesenchymal stromal cells. PLoS One 7:e46842.
90. König J, B Huppertz, G Desoye, O Parolini, JD Fröhlich, G Weiss, G Dohr, P Sedlmayr and I Lang. (2011). Amnionderived mesenchymal stromal cells show angiogenic properties but resist differentiation into mature endothelial cells. Stem Cells Dev 21:1309-1320.
91. Davani S, A Marandin, N Mersin, B Royer, B Kantelip, P Hervé, J-P Etievent and J-P Kantelip. (2003). Mesenchymal progenitor cells differentiate into an endothelial phenotype, enhance vascular density, and improve heart function in a rat cellular cardiomyoplasty model. Circulation 108:II-253- II-258.
92. Lee M-Y, J-P Huang, Y-Y Chen, JD Aplin, Y-H Wu, C-Y Chen, P-C Chen and C-P Chen. (2009). Angiogenesis in differentiated placental multipotent mesenchymal stromal cells is dependent on integrin a5b1. PLoS One 4:e6913.
93. Mayer H, H Bertram, W Lindenmaier, T Korff, H Weber and H Weich. (2005). Vascular endothelial growth factor (VEGF-A) expression in human mesenchymal stem cells: Autocrine and paracrine role on osteoblastic and endothelial differentiation. J Cell Biochem 95:827-839.
94. Qiu X, C Sun, W Yu, H Lin, Z Sun, Y Chen, R Wang and Y Dai. (2012). Combined strategy of mesenchymal stem cell injection with vascular endothelial growth factor gene therapy for the treatment of diabetes-associated erectile dysfunction. J Androl 33:37-44.
95. Shabbir A, D Zisa, G Suzuki and T Lee. (2009). Heart failure therapy mediated by the trophic activities of bone marrow mesenchymal stem cells: a noninvasive therapeutic regimen. Am J Physiol Heart Circ Physiol 296:H1888-H1897.
96. Barker TH. (2011). The role of ECM proteins and protein fragments in guiding cell behavior in regenerative medicine. Biomaterials 32:4211-4214.
97. Wu C-C, Y-C Chao, C-N Chen, S Chien, Y-C Chen, C-C Chien, J-J Chiu, B Linju Yen. (2008). Synergism of biochemical and mechanical stimuli in the differentiation of human placenta-derived multipotent cells into endothelial cells. J Biomech 41:813-821.
98. Au P, J Tam, D Fukumura and RK Jain. (2008). Bone marrow-derived mesenchymal stem cells facilitate engineering of long-lasting functional vasculature. Blood 111:4551-4558.
99. Carrion B, CP Huang, CM Ghajar, S Kachgal, E Kniazeva, NL Jeon and AJ Putnam. (2010). Recreating the perivascular niche ex vivo using a microfluidic approach. Biotechnol Bioeng 107:1020-1028.
100. Zhou J, M Cheng, Y-H Liao, Y Hu, M Wu, Q Wang, B Qin, H Wang, Y Zhu, et al. (2013). Rosuvastatin enhances angiogenesis via eNOS-dependent mobilization of endothelial progenitor cells. PLoS One 8:e63126.
101. Ohtani K, GJ Vlachojannis, M Koyanagi, J-N Boeckel, C Urbich, R Farcas, H Bonig, VE Marquez, AM Zeiher and S Dimmeler. (2011). Epigenetic regulation of endothelial lineage committed genes in pro-Angiogenic hematopoietic and endothelial progenitor cells. Circ Res 109:1219-1229.
102. Gomes SA, EB Rangel, C Premer, RA Dulce, Y Cao, V Florea, W Balkan, CO Rodrigues, AV Schally and JM Hare. (2013). S-nitrosoglutathione reductase (GSNOR) enhances vasculogenesis by mesenchymal stem cells. Proc Natl Acad Sci U S A 110:2834-2839.
103. Ahmed RPH, KH Haider, J Shujia, MR Afzal and M Ashraf. (2010). Sonic hedgehog gene delivery to the rodent heart promotes angiogenesis via iNOS/Netrin-1/PKC pathway. PLoS One 5:e8576.
104. Ocarino NM, JN Boeloni, AM Goes, JF Silva, U Marubayashi and R Serakides. (2008). Osteogenic differentiation of mesenchymal stem cells from osteopenic rats subjected to physical activity with and without nitric oxide synthase inhibition. Nitric Oxide 19:320-325.
105. Birmingham E, G Niebur, P McHugh, G Shaw, F Barry and L McNamara. (2012). Osteogenic differentiation of mesenchymal stem cells is regulated by osteocyte and osteoblast cells in a simplified bone niche. Eur Cell Mater 23:13-27.
106. Tasso R, V Ulivi, D Reverberi, C Lo Sicco, F Descalzi and R Cancedda. (2013). In vivo implanted bone marrow-derived mesenchymal stem cells trigger a cascade of cellular events leading to the formation of an ectopic bone regenerative niche. Stem Cells Dev [Epub ahead of print]; DOI:10.1089/ scd.2013.0313.
107. Kurpinski K, H Lam, J Chu, A Wang, A Kim, E Tsay, S Agrawal, DV Schaffer and S Li. (2010). Transforming growth factor-b and notch signaling mediate stem cell differentiation into smooth muscle cells. Stem Cells 28:734-742.
108. Boopathy AV, KD Pendergrass, PL Che, Y-S Yoon and ME Davis. (2013). Oxidative stress-induced Notch1 signaling promotes cardiogenic gene expression in mesenchymal stem cells. Stem Cell Res Ther 4:43.
109. Lee RH, N Yoon, JC Reneau and DJ Prockop. (2012). Preactivation of human MSCs with TNF-a enhances tumorsuppressive activity. Cell Stem Cell 11:825-835.
110. Secchiero P, S Zorzet, C Tripodo, F Corallini, E Melloni, L Caruso, R Bosco, S Ingrao, B Zavan and G Zauli. (2010). Human bone marrow mesenchymal stem cells display anticancer activity in SCID mice bearing disseminated non- Hodgkins lymphoma xenografts. PLoS One 5:e11140.
111. Gomes CM. (2013). The dual role of mesenchymal stem cells in tumor progression. Stem Cell Res Ther 4:42.
112. Dvorak HF. (2003). How tumors make bad blood vessels and stroma. Am J Pathol 162:1747-1757.
113. Zhang Z, KG Neiva, MW Lingen, LM Ellis and JE Nör. (2009). VEGF-dependent tumor angiogenesis requires inverse and reciprocal regulation of VEGFR1 and VEGFR2. Cell Death Differ 17:499-512.
114. Kerbel RS. (2008). Tumor angiogenesis. N Engl J Med 358:2039-2049.
115. Wels J, RN Kaplan, S Rafii and D Lyden. (2008). Migratory neighbors and distant invaders: tumor-associated niche cells. Genes Dev 22:559-574.
116. Ding W, TR Knox, RC Tschumper, W Wu, SM Schwager, JC Boysen, DF Jelinek and NE Kay. (2010). Platelet-derived growth factor (PDGF)-PDGF receptor interaction activates bone marrow-derived mesenchymal stromal cells derived from chronic lymphocytic leukemia: implications for an angiogenic switch. Blood 116:2984-2993.
117. Menon LG, S Picinich, R Koneru, H Gao, SY Lin, M Koneru, P Mayer-Kuckuk, J Glod and D Banerjee. (2007). Differential gene expression associated with migration of mesenchymal stem cells to conditioned medium from tumor cells orbone marrow cells. Stem Cells 25:520-528.
118. Huang W, M Chang, K Tsai, M Hung, H Chen and S Hung. (2012). Mesenchymal stem cells promote growth and angiogenesis of tumors in mice. Oncogene 32:4343-4345.
119. Burns JS, M Kristiansen, LP Kristensen, KH Larsen, MO Nielsen, H Christiansen, J Nehlin, JS Andersen and M Kassem. (2011). Decellularized matrix from tumorigenic human mesenchymal stem cells promotes neovascularization with galectin-1 dependent endothelial interaction. PLoS One 6:e21888.
120. Zhang T, YW Lee, YF Rui, TY Cheng, XH Jiang and G Li. (2013). Bone marrow-derived mesenchymal stem cells promote growth and angiogenesis of breast and prostate tumors. Stem Cell Res Ther 4:70.
121. Proulx-Bonneau S, A Guezguez and B Annabi. (2011). A concerted HIF-1a/MT1-MMP signalling axis regulates the expression of the 3BP2 adaptor protein in hypoxic mesenchymal stromal cells. PLoS One 6:e21511.
122. Wang X, Z Zhang and C Yao. (2010). Angiogenic activity of mesenchymal stem cells in multiple myeloma. Cancer Invest 29:37-41.
123. Fouraschen SM, Q Pan, PE de Ruiter, WR Farid, G Kazemier, J Kwekkeboom, JN Ijzermans, HJ Metselaar, HW Tilanus and J de Jonge. (2012). Secreted factors of human liver-derived mesenchymal stem cells promote liver regeneration early after partial hepatectomy. Stem Cells Dev 21:2410-2419.
124. Gruber R, B Kandler, P Holzmann, M Vögele-Kadletz, U Losert, MB Fischer and G Watzek. (2005). Bone marrow stromal cells can provide a local environment that favors migration and formation of tubular structures of endothelial cells. Tissue Eng 11:896-903.
125. Annabi B, E Naud, Y-T Lee, N Eliopoulos and J Galipeau. (2004). Vascular progenitors derived from murine bone marrow stromal cells are regulated by fibroblast growth factor and are avidly recruited by vascularizing tumors. J Cell Biochem 91:1146-1158.
126. Sun B, S Zhang, C Ni, D Zhang, Y Liu,WZhang, X Zhao, C Zhao and M Shi. (2005). Correlation between melanoma angiogenesis and the mesenchymal stem cells and endothelial progenitor cells derived from bone marrow. Stem Cells Dev 14:292-298.
127. Suzuki K, R Sun,MOriguchi,MKanehira, T Takahata, J Itoh, A Umezawa, H Kijima, S Fukuda and Y Saijo. (2011). Mesenchymal stromal cells promote tumor growth through the enhancement of neovascularization. Mol Med 17:579-587.
128. Liu Y, ZP Han, SS Zhang, YY Jing, XX Bu, CY Wang, K Sun, GC Jiang, X Zhao, et al. (2011). Effects of inflammatory factors on mesenchymal stem cells and their role in the promotion of tumor angiogenesis in colon cancer. J Biol Chem 286:25007-25015.
129. Zhu W, L Huang, Y Li, X Zhang, J Gu, Y Yan, X Xu, M Wang, H Qian and W Xu. (2012). Exosomes derived from human bone marrow mesenchymal stem cells promote tumor growth in vivo. Cancer Lett 315:28-37.
130. Zhu W, L Huang, Y Li, H Qian, X Shan, Y Yan, F Mao, X Wu and W-R Xu. (2011). Mesenchymal stem cell-secreted soluble signaling molecules potentiate tumor growth. Cell Cycle 10:3198-3207.
131. Quante M, S Tu, H Tomita, T Gonda, S Wang, S Takashi, G Baik, W Shibata, B Diprete, et al. (2011). Bone marrowderived myofibroblasts contribute to the mesenchymal stem cell niche and promote tumor growth. Cancer Cell 19:257-272.
132. Mi Z, SD Bhattacharya, VM Kim, H Guo, LJ Talbot and PC Kuo. (2011). Osteopontin promotes CCL5-mesenchymal stromal cell-mediated breast cancer metastasis. Carcinogenesis 32:477-487 133.
133. Stagg J. (2008). Mesenchymal Stem Cells in Cancer. Stem Cell Rev 4:119-124.
134. Paunescu V, FM Bojin, CA Tatu, OI Gavriliuc, A Rosca, AT Gruia, G Tanasie, C Bunu, D Crisnic, et al. (2011). Tumourassociated fibroblasts and mesenchymal stem cells: more similarities than differences. J Cell Mol Med 15:635-646.
135. Calabrese C, H Poppleton, M Kocak, TL Hogg, C Fuller, B Hamner, EY Oh, MW Gaber, D Finklestein and M Allen. (2007). A perivascular niche for brain tumor stem cells. Cancer Cell 11:69-82.
136. Charles N, T Ozawa, M Squatrito, A-M Bleau, CW Brennan, D Hambardzumyan and EC Holland. (2010). Perivascular nitric oxide activates notch signaling and promotes stem-like character in PDGF-induced glioma cells. Cell Stem Cell 6:141-152.
137. Borovski T, E De Sousa, F Melo, L Vermeulen and JP Medema. (2011). Cancer stem cell niche: the place to be. Cancer Res 71:634-639.
138. Orimo A, PB Gupta, DC Sgroi, F Arenzana-Seisdedos, T Delaunay, R Naeem, VJ Carey, AL Richardson and RA Weinberg. (2005). Stromal fibroblasts present in invasive human breast carcinomas promote tumor growth and angiogenesis through elevated SDF-1/CXCL12 secretion. Cell 121:335-348.
139. Bagley RG, W Weber, C Rouleau, M Yao, N Honma, S Kataoka, I Ishida, BL Roberts and BA Teicher. (2009). Human mesenchymal stem cells from bone marrow express tumor endothelial and stromal markers. Int J Oncol 34:619-627.
140. Kucerova L and S Skolekova. (2013). Tumor microenvironment and the role of mesenchymal stromal cells. Neoplasma 60:1-10.
141. Shinagawa K, Y Kitadai, M Tanaka, T Sumida, M Onoyama, M Ohnishi, E Ohara, Y Higashi, S Tanaka,WYasui and K Chayama. (2013). Stroma-directed imatinib therapy impairs the tumor-promoting effect of bone marrow-derived mesenchymal stem cells in an orthotopic transplantation model of colon cancer. Int J Cancer 132:813-823.
142. Potenta S, E Zeisberg and R Kalluri. (2008). The role of endothelial-to-mesenchymal transition in cancer progression. Br J Cancer 99:1375-1379.
143. Ghaedi M, M Soleimani, NM Taghvaie, M Sheikhfatollahi, K Azadmanesh, AS Lotfi and J Wu. (2011). Mesenchymal stem cells as vehicles for targeted delivery of anti-angiogenic protein to solid tumors. J Gene Med 13:171-180.
144. Klopp AH, A Gupta, E Spaeth, M Andreeff and F Marini. (2011). Concise review: Dissecting a discrepancy in the literature: do mesenchymal stem cells support or suppress tumor growth? Stem Cells 29:11-19.
145. Ramasamy R, EW Lam, I Soeiro, V Tisato, D Bonnet and F Dazzi. (2007). Mesenchymal stem cells inhibit proliferation and apoptosis of tumor cells: impact on in vivo tumor growth. Leukemia 21:304-310.
146. Villars F, B Guillotin, T Amedee, S Dutoya, L Bordenave, R Bareille and J Amedee. (2002). Effect of HUVEC on human osteoprogenitor cell differentiation needs heterotypic gap junction communication. Am J Physiol Cell Physiol 282:C775-C785.