Bone marrow-derived mesenchymal stem cells promote angiogenic processes in a time- and dose-Dependent manner in vitro

Tissue Engineering - Part A

Volumn 15, Issue 9, 2009, Pages 2459-2470

  Duffy, Garry P ^a,b   Ahsan, Tabassum ^b   O'Brien, Timothy ^a   Barry, Frank ^a   Nerem, Robert M ^b  

^a NATIONAL UNIVERSITY OF IRELAND   (Ireland)

^b GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD VESSEL PROSTHESES; BONE; CAPILLARITY; CELL MEMBRANES; ELECTRIC CONDUCTIVITY MEASUREMENT; ENDOTHELIAL CELLS; FLOWCHARTING; MONOLAYERS; SELF ASSEMBLY; STABILIZATION;

ANGIOGENESIS; ANGIOGENIC PROCESS; BONE MARROW-DERIVED MESENCHYMAL STEM CELLS; CARDIAC REPAIR; CELLULAR PROCESS; CO-CULTURE SYSTEM; COCULTURE; COMPLEX VESSELS; DIRECT CONTACT; DOSE-DEPENDENT; DOSE-DEPENDENT MANNER; IN-VITRO; MODE OF ACTION; MYOCARDIAL INFARCTION; NEOVASCULARIZATION; NON-CONTACT; PARACRINE; STEM CELL; VESSEL FORMATION;

CELL CULTURE;

5' NUCLEOTIDASE; ENDOGLIN;

ADIPOGENESIS; ANGIOGENESIS; ANTIGEN EXPRESSION; ARTICLE; BONE DEVELOPMENT; CELL INTERACTION; CELL MEMBRANE PERMEABILITY; CELL MIGRATION; CELL PROLIFERATION; COCULTURE; ENDOTHELIUM CELL; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; MESENCHYMAL STEM CELL; MONOLAYER CULTURE; NORMAL HUMAN; PRIORITY JOURNAL;

EID: 69249126590     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2008.0341     Document Type: Article

References (52)

1. American Heart Association. Heart Disease and Stroke Statistics-2007 Update: A Report From the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation 115, e69, 2007.
2. Pfeffer, J.M., Pfeffer, M.A., Fletcher, P.J., and Braunwald, E. Ventricular performance in rats with myocardial infarction and failure. Am J Med 76, 99, 1984.
3. Orlic, D., Kajstura, J., Chimenti, S., Jakoniuk, I., Anderson, S.M., Li, B., Pickel, J., McKay, R., Nadal-Ginard, B., Bodine, D.M., Leri, A., and Anversa, P. Bone marrow cells regenerate infarcted myocardium. Nature 410, 701, 2001.
4. Barry, F.P., and Murphy, J.M. Mesenchymal stem cells: clinical applications and biological characterization. Int J Biochem Cell Biol 36, 568, 2004.
5. Baksh, D., Song, L., and Tuan, R.S. Adult mesenchymal stem cells: characterization, differentiation, and application in cell and gene therapy. J Cell Mol Med 8, 301, 2004.
6. Bittira, B., Kuang, J.Q., Al-Khaldi, A., Shum-Tim, D., and Chiu, R.C. In vitro preprogramming of marrow stromal cells for myocardial regeneration. Ann Thorac Surg 74, 1154, 2002.
7. Toma, C., Pittenger, M.F., Cahill, K.S., Byrne, B.J., and Kessler, P.D. Human mesenchymal stem cells differentiate to a cardiomyocyte phenotype in the adult murine heart. Circulation 105, 93, 2002.
8. Yoon, J., Shim, W.J., Ro, Y.M., and Lim, D.S. Transdifferentiation of mesenchymal stem cells into cardiomyocytes by direct cell-to-cell contact with neonatal cardiomyocyte but not adult cardiomyocytes. Ann Hematol 84, 715, 2005.
9. Orlic, D. Stem cell repair in ischemic heart disease: an experimental model. Int J Hematol 76 Suppl 1, 144, 2002.
10. Nagaya, N., Fujii, T., Iwase, T., Ohgushi, H., Itoh, T., Uematsu, M., Yamagishi, M., Mori, H., Kangawa, K., and Kitamura, S. Intravenous administration of mesenchymal stem cells improves cardiac function in rats with acute myocardial infarction through angiogenesis and myogenesis. Am J Physiol 287, H2670, 2004.
11. Krause, U., Harter, C., Seckinger, A., Wolf, D., Reinhard, A., Bea, F., Dengler, T., Hardt, S., Ho, A., Katus, H.A., Kuecherer, H., and Hansen, A. Intravenous delivery of autologous mesenchymal stem cells limits infarct size and improves left ventricular function in the infarcted porcine heart. Stem Cells Dev 16, 31, 2007.
12. Silva, G.V., Litovsky, S., Assad, J.A., Sousa, A.L., Martin, B.J., Vela, D., Coulter, S.C., Lin, J., Ober, J., Vaughn, W.K., Branco, R.V., Oliveira, E.M., He, R., Geng, Y.J., Willerson, J.T., and Perin, E.C. Mesenchymal stem cells differentiate into an endothelial phenotype, enhance vascular density, and improve heart function in a canine chronic ischemia model. Circulation 111, 150, 2005.
13. Chen, S.L., Fang, W.W., Ye, F., Liu, Y.H., Qian, J., Shan, S.J., Zhang, J.J., Chunhua, R.Z., Liao, L.M., Lin, S., and Sun, J.P. Effect on left ventricular function of intracoronary transplantation of autologous bone marrow mesenchymal stem cell in patients with acute myocardial infarction. Am J Cardiol 94, 92, 2004.
14. Strauer, B.E., Brehm, M., Zeus, T., Kostering, M., Hernandez, A., Sorg, R.V., Kogler, G., and Wernet, P. Repair of infarcted myocardium by autologous intracoronary mononuclear bone marrow cell transplantation in humans. Circulation 106, 1913, 2002.
15. Katritsis, D.G., Sotiropoulou, P.A., Karvouni, E., Karabinos, I., Korovesis, S., Perez, S.A., Voridis, E.M., and Papamichail, M. Transcoronary transplantation of autologous mesenchymal stem cells and endothelial progenitors into infarcted human myocardium. Cathet Cardiovasc Interv 65, 321, 2005.
16. Zhang, S., Jia, Z., Ge, J., Gong, L., Ma, Y., Li, T., Guo, J., Chen, P., Hu, Q., Zhang, P., Liu, Y., Li, Z., Ma, K., Li, L., and Zhou, C. Purified human bone marrow multipotent mesenchymal stem cells regenerate infarcted myocardium in experimental rats. Cell Transplant 14, 787, 2005.
17. Kinnaird, T., Stabile, E., Burnett, M.S., Shou, M., Lee, C.W., Barr, S., Fuchs, S., and Epstein, S.E. Local delivery of marrowderived stromal cells augments collateral perfusion through paracrine mechanisms. Circulation 109, 1543, 2004.
18. Makela, J., Ylitalo, K., Lehtonen, S., Dahlbacka, S., Niemela, E., Kiviluoma, K., Rimpilainen, J., Alaoja, H., Paavonen, T., Lehenkari, P., Juvonen, T., and Anttila, V. Bone marrow-derived mononuclear cell transplantation improves myocardial recovery by enhancing cellular recruitment and differentiation at the infarction site. J Thorac Cardiovasc Surg 134, 565, 2007.
19. Kinnaird, T., Stabile, E., Burnett, M.S., Lee, C.W., Barr, S., Fuchs, S., and Epstein, S.E. Marrow-derived stromal cells express genes encoding a broad spectrum of arteriogenic cytokines and promote in vitro and in vivo arteriogenesis through paracrine mechanisms. Circ Res 94, 678, 2004.
20. Kamihata, H., Matsubara, H., Nishiue, T., Fujiyama, S., Tsutsumi, Y., Ozono, R., Masaki, H., Mori, Y., Iba, O., Tateishi, E., Kosaki, A., Shintani, S., Murohara, T., Imaizumi, T., and Iwasaka, T. 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, 1046, 2001.
21. Tang, J., Xie, Q., Pan, G., Wang, J., and Wang, M. Mesenchymal stem cells participate in angiogenesis and improve heart function in rat model of myocardial ischemia with reperfusion. Eur J Cardiothorac Surg 30, 353, 2006.
22. Criqui, M., Ninomiya, J., Wingard, D., Ji, M., and Fronek, A. Progression of peripheral arterial disease predicts cardiovascular disease morbidity and mortality. J Am Coll Cardiol 52, 1736, 2008.
23. Wu, Y., Chen, L., Scott, P.G., and Tredget, E.E. Mesenchymal stem cells enhance wound healing through differentiation and angiogenesis. Stem Cells 25, 2648, 2007.
24. Au, P., Tarn, J., Fukumura, D., and Jain, R.K. Bone marrowderived mesenchymal stem cells facilitate engineering of long-lasting functional vasculature. Blood 111, 4551, 2008.
25. Murphy, J.M., Fink, D.J., Hunziker, E.B., and Barry, F.P. Stem cell therapy in a caprine model of osteoarthritis. Arthritis Rheum 48, 3464, 2003.
26. Pittenger, M.F., Mackay, A.M., Beck, S.C., Jaiswal, R.K., Douglas, R., Mosca, J.D., Moorman, M.A., Simonetti, D.W., Craig, S., and Marshak, D.R. Multilineage potential of adult human mesenchymal stem cells. Science 284, 143, 1999.
27. Cucina, A., Borrelli, V., Randone, B., Coluccia, P., Spienza, P., and Cavallaro, A. Vascular endothelial growth factor increases the migration and proliferation of smooth muscle cells through the mediation of growth factors released by endothelial cells. J Surg Res 109, 16, 2003.
28. Chen, J., Somanath, P.R., Razorenova, O., Chen, W.S., Hay, N., Bornstein, P., and Byzova, T.V. Akt1 regulates pathological angiogenesis, vascular maturation and permeability in vivo. Nat Med 11, 1188, 2005.
29. Yamaoka-Tojo, M., Tojo, T., Kim, H.W., Hilenski, L., Patrushev, N.A., Zhang, L., Fukai, T., and Ushio-Fukai, M. IQGAP1 mediates VE-cadherin-based cell-cell contacts and VEGF signaling at adherence junctions linked to angiogenesis. Arterioscler Thromb Vase Biol 26, 1991, 2006.
30. Liu, J., Wang, X.B., Park, D.S., and Lisanti, M.P. Caveolin-1 expression enhances endothelial capillary tubule formation. J Biol Chem 277, 10661, 2002.
31. Carmeliet, P. Mechanisms of angiogenesis and arteriogenesis. Nat Med 6, 389, 2000.
32. Carmeliet, P. Angiogenesis in health and disease. Nat Med 9, 653, 2003.
33. Carmeliet, P. Basic concepts of (myocardial) angiogenesis: role of vascular endothelial growth factor and angiopoietin. Curr Interv Cardiol Rep 1, 322, 1999.
34. Tang, Y.L., Zhao, Q., Qin, X., Shen, L., Cheng, L., Ge, J., and Phillips, M.I. Paracrine action enhances the effects of autologous mesenchymal stem cell transplantation on vascular regeneration in rat model of myocardial infarction. Ann Thorac Surg 80, 229, 2005.
35. Dohmann, H.F., Perin, E.C., Takiya, C.M., Silva, G.V., Silva, S.A., Sousa, A.L., Mesquita, C.T., Rossi, M.I., Pascarelli, B.M., Assis, I.M., Dutra, H.S., Assad, J.A., Castello-Branco, R.V., Drummond, C., Dohmann, H.J., Willerson, J.T., and Borojevic, R. Transendocardial autologous bone marrow mononuclear cell injection in ischemic heart failure: postmortem anatomicopathologic and immunohistochemical findings. Circulation 112, 521, 2005.
36. Silva, G.V., Perin, E.C, Dohmann, H.F., Borojevic, R., Silva, S.A., Sousa, A.L., Assad, J. A., Vaughn, W.K., Mesquita, C.T., Belem, L., Carvalho, A.C., Dohmann, H.J., Barroso do Amaral, E., Coutinho, J., Branco, R., Oliveira, E., and Willerson, J.T. Catheter-based transendocardial delivery of autologous bone-marrow-derived mononuclear cells in patients listed for heart transplantation. Tex Heart Inst J 31, 214, 2004.
37. Perin, E.C, Dohmann, H.F., Borojevic, R., Silva, S.A., Sousa, A.L., Silva, G.V., Mesquita, C.T., Belem, L., Vaughn, W.K., Rangel, F.O., Assad, J.A., Carvalho, A.C., Branco, R.V., Rossi, M.I., Dohmann, H.J., and Willerson, J.T. Improved exercise capacity and ischemia 6 and 12 months after transendocardial injection of autologous bone marrow mononuclear cells for ischemic cardiomyopathy. Circulation 110, II213, 2004.
38. Perin, E.C., Dohmann, H.F., Borojevic, R., Silva, S.A., Sousa, A.L., Mesquita, C.T., Rossi, M.I., Carvalho, A.C., Dutra, H.S., Dohmann, H.J., Silva, G.V., Belem, L., Vivacqua, R., Rangel, F.O., Esporcatte, R., Geng, Y.J., Vaughn, W.K., Assad, J.A., Mesquita, E.T., and Willerson, J.T. Transendocardial, autologous bone marrow cell transplantation for severe, chronic ischemic heart failure. Circulation 107, 2294, 2003.
39. Potapova, I.A., Gaudette, G.R., Brink, P.R., Robinson, R.B., Rosen, M.R., Cohen, I.S., and Doronin, S.V. Mesenchymal stem cells support migration, extracellular matrix invasion, proliferation, and survival of endothelial cells in vitro. Stem Cells 25, 1761, 2007.
40. Mirotsou, M., Zhang, Z., Deb, A., Zhang, L., Gnecchi, M., Noiseux, N., Mu, H., Pachori, A., and Dzau, V. Secreted frizzled related protein 2 (Sfrp2) is the key Akt-mesenchymal stem cell-released paracrine factor mediating myocardial survival and repair. Proc Natl Acad Sci USA 104, 1643, 2007.
41. Ladage, D., Brixius, K., Steingen, C., Mehlhorn, U., Schwinger, R.H., Bloch, W., and Schmidt, A. Mesenchymal stem cells induce endothelial activation via paracine mechanisms. Endothelium 14, 53, 2007.
42. Noiseux, N., Gnecchi, M., Lopez-Ilasaca, M., Zhang, L., Solomon, S.D., Deb, A., Dzau, V.J., and Pratt, R.E. Mesenchymal stem cells overexpressing Akt dramatically repair infarcted myocardium and improve cardiac function despite infrequent cellular fusion or differentiation. Mol Ther 14, 840, 2006.
43. Iwase, T., Nagaya, N., Fujii, T., Itoh, T., Murakami, S., Matsumoto, T., Kangawa, K., and Kitamura, S. Comparison of angiogenic potency between mesenchymal stem cells and mononuclear cells in a rat model of hindlimb ischemia. Cardiovasc Res 66, 543, 2005.
44. Griffith, L.G., and Swartz, M.A. Capturing complex 3D tissue physiology in vitro. Nat Rev Mol Cell Biol 7, 211, 2006.
45. Lamalice, L., Le Boeuf, F., and Huot, J. Endothelial cell migration during angiogenesis. Circ Res 100, 782, 2007.
46. Jain, R.K. Molecular regulation of vessel maturation. Nat Med 9, 685, 2003.
47. Zacharek, A., Chen, J., Cui, X., Li, A., Li, Y., Roberts, C., Feng, Y., Gao, Q., and Chopp, M. Angiopoietin1/Tie2 and VEGF/Flk1 induced by MSC treatment amplifies angiogenesis and vascular stabilization after stroke. J Cereb Blood Flow Metab 27, 1684, 2007.
48. Kraling, B.M., Wiederschain, D.G., Boehm, T., Renn, M., Mulliken, J.B., and Moses, M.A. The role of matrix metalloproteinase activity in the maturation of human capillary endothelial cells in vitro. J Cell Sci 112 (Pt 10), 1599, 1999.
49. Wang, Y., Johnsen, H.E., Mortensen, S., Bindslev, L., Ripa, R.S., Haack-Sorensen, M., Jorgensen, E., Fang, W., and Kastrup, J. Changes in circulating mesenchymal stem cells, stem cell homing factor, and vascular growth factors in patients with acute ST elevation myocardial infarction treated with primary percutaneous coronary intervention. Heart 92, 768, 2006.
50. Hu, X., Wang, J., Chen, J., Luo, R., He, A., Xie, X., and Li, J. Optimal temporal delivery of bone marrow mesenchymal stem cells in rats with myocardial infarction. Eur J Cardiothorac Surg 31, 438, 2007.
51. Hung, S.C., Pochampally, R.R., Chen, S.C, Hsu, S.C., and Prockop, D.J. Angiogenic effects of human multipotent stromal cell conditioned medium activate the PI3K-Akt pathway in hypoxic endothelial cells to inhibit apoptosis, increase survival, and stimulate angiogenesis. Stem Cells 25, 2363, 2007.
52. Kasper, G., Dankert, N., Tuischer, J., Hoeft, M., Gaber, T., Glaeser, J.D., Zander, D., Tschirschmann, M., Thompson, M., Matziolis, G., and Duda, G.N. Mesenchymal stem cells regulate angiogenesis according to their mechanical environment. Stem Cells 25, 903, 2007.