Stromal cell identity influences the in vivo functionality of engineered capillary networks formed by co-delivery of endothelial cells and stromal cells

Tissue Engineering - Part A

Volumn 19, Issue 9-10, 2013, Pages 1209-1222

  Grainger, Stephanie J ^a   Carrion, Bita ^a   Ceccarelli, Jacob ^a   Putnam, Andrew J ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD VESSELS; CAPILLARITY; CELL CULTURE; ENDOTHELIAL CELLS; MAMMALS; STEM CELLS; TISSUE ENGINEERING;

ADIPOSE DERIVED STEM CELLS; EFFECTIVE APPROACHES; FLUORESCENT TRACERS; FUNCTIONAL PROPERTIES; HUMAN LUNG FIBROBLASTS; HUMAN UMBILICAL VEINS; NEO-VASCULARIZATION; THERAPEUTIC ANGIOGENESIS;

MICROCIRCULATION;

MUS;

ADIPOSE TISSUE; ANIMAL; ARTICLE; BIOLOGICAL MODEL; BONE MARROW CELL; CAPILLARY; CYTOLOGY; ENDOTHELIUM CELL; FIBROBLAST; HUMAN; IMMUNOHISTOCHEMISTRY; MESENCHYMAL STROMA CELL; METHODOLOGY; MOUSE; STROMA CELL; TISSUE ENGINEERING; UMBILICAL VEIN ENDOTHELIAL CELL;

ADIPOSE TISSUE; ANIMALS; BONE MARROW CELLS; CAPILLARIES; ENDOTHELIAL CELLS; FIBROBLASTS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; IMMUNOHISTOCHEMISTRY; MESENCHYMAL STROMAL CELLS; MICE; MODELS, BIOLOGICAL; STROMAL CELLS; TISSUE ENGINEERING;

EID: 84875576994     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2012.0281     Document Type: Article

References (49)

1. Ferrara, N., & Alitalo, K. Clinical applications of angiogenic growth factors and their inhibitors. Nat Med 5, 1359, 1999.
2. Davis, B.H., Schroeder, T., Yarmolenko, P.S., Guilak, F., Dewhirst, M.W., & Taylor, D.A. An in vitro system to evaluate the effects of ischemia on survival of cells used for cell therapy. Ann Biomed Eng 35, 1414, 2007.
3. Chen, R.R., Silva, E.A., Yuen, W.W., Brock, A.A., Fischbach, C., Lin, A.S., Guldberg, R.E., & Mooney, D.J. Integrated approach to designing growth factor delivery systems. FASEB J 21, 3896, 2007.
4. Sun, Q., Silva, E.A., Wang, A., Fritton, J.C., Mooney, D.J., Schaffler, M.B., Grossman, P.M., & Rajagopalan, S. Sustained release of multiple growth factors from injectable polymeric system as a novel therapeutic approach towards angiogenesis. Pharm Res 27, 264, 2010.
5. Lee, K.Y., Peters, M.C., Anderson, K.W., & Mooney, D.J. Controlled growth factor release from synthetic extracellular matrices. Nature 408, 998, 2000.
6. Murphy, W.L., & Mooney, D.J. Controlled delivery of inductive proteins, plasmid DNA and cells from tissue engineering matrices. J Periodontal Res 34, 413, 1999.
7. Sun, Q., Chen, R.R., Shen, Y., Mooney, D.J., Rajagopalan, S., and Grossman, P.M. Sustained vascular endothelial growth factor delivery enhances angiogenesis and perfusion in ischemic hind limb. Pharm Res 22, 1110, 2005.
8. Zisch, A.H., Lutolf, M.P., Ehrbar, M., Raeber, G.P., Rizzi, S.C., Davies, N., Schmokel, H., Bezuidenhout, D., Djonov, V., Zilla, P., & Hubbell, J.A. Cell-demanded release of VEGF from synthetic, biointeractive cell ingrowth matrices for vascularized tissue growth. FASEB J 17, 2260, 2003.
9. Richardson, T.P., Peters, M.C., Ennett, A.B., & Mooney, D.J. Polymeric system for dual growth factor delivery. Nat Biotechnol 19, 1029, 2001.
10. Iba, O., Matsubara, H., Nozawa, Y., Fujiyama, S., Amano, K., Mori, Y., Kojima, H., & Iwasaka, T. Angiogenesis by implantation of peripheral blood mononuclear cells and platelets into ischemic limbs. Circulation 106, 2019, 2002.
11. Kinnaird, T., Stabile, E., Burnett, M.S., Shou, M., Lee, C.W., Barr, S., Fuchs, S., & Epstein, S.E. Local delivery of marrow-derived stromal cells augments collateral perfusion through paracrine mechanisms. Circulation 109, 1543, 2004.
12. Pesce, M., Orlandi, A., Iachininoto, M.G., Straino, S., Torella, A.R., Rizzuti, V., Pompilio, G., Bonanno, G., Scambia, G., and Capogrossi, M.C. Myoendothelial differentiation of human umbilical cord blood-derived stem cells in ischemic limb tissues. Circ Res 93, e51, 2003.
13. Rehman, J., Traktuev, D., Li, J., Merfeld-Clauss, S., Temm-Grove, C.J., Bovenkerk, J.E., Pell, C.L., Johnstone, B.H., Considine, R.V., & March, K.L. Secretion of angiogenic and antiapoptotic factors by human adipose stromal cells. Circulation 109, 1292, 2004.
14. Nor, J.E., Christensen, J., Mooney, D.J., & Polverini, P.J. Vascular endothelial growth factor (VEGF)-mediated angiogenesis is associated with enhanced endothelial cell survival and induction of Bcl-2 expression. Am J Pathol 154, 375, 1999.
15. Nor, J.E., Peters, M.C., Christensen, J.B., Sutorik, M.M., Linn, S., Khan, M.K., Addison, C.L., Mooney, D.J., & Polverini, P.J. Engineering and characterization of functional human microvessels in immunodeficient mice. Lab Invest 81, 453, 2001.
16. Baluk, P., Hashizume, H., & McDonald, D.M. Cellular abnormalities of blood vessels as targets in cancer. Curr Opin Genet Dev 15, 102, 2005.
17. Carmeliet, P., & Jain, R.K. Angiogenesis in cancer and other diseases. Nature 407, 249, 2000.
18. Jain, R.K. Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science 307, 58, 2005.
19. Melero-Martin, J.M., De Obaldia, M.E., Kang, S.Y., Khan, Z.A., Yuan, L., Oettgen, P., & Bischoff, J. Engineering robust and functional vascular networks in vivo with human adult and cord blood-derived progenitor cells. Circ Res 103, 128, 2008.
20. Hashizume, H., Baluk, P., Morikawa, S., McLean, J.W., Thurston, G., Roberge, S., Jain, R.K., & McDonald, D.M. Openings between defective endothelial cells explain tumor vessel leakiness. Am J Pathol 156, 1363, 2000.
21. Ghajar, C.M., Blevins, K.S., Hughes, C.C., George, S.C., and Putnam, A.J.Mesenchymal stemcells enhance angiogenesis in mechanically viable prevascularized tissues via early matrix metalloproteinase upregulation. Tissue Eng 12, 2875, 2006.
22. Kniazeva, E., Kachgal, S., & Putnam, A.J. Effects of extracellular matrix density and mesenchymal stem cells on neovascularization in vivo. Tissue Eng Part A 17, 905, 2011.
23. Bergers, G., & Song, S. The role of pericytes in blood-vessel formation and maintenance. Neuro-Oncol 7, 452, 2005.
24. Ghajar, C.M., Kachgal, S., Kniazeva, E., Mori, H., Costes, S.V., George, S.C., & Putnam, A.J. Mesenchymal cells stimulate capillary morphogenesis via distinct proteolytic mechanisms. Exp Cell Res 316, 813, 2010.
25. Au, P., Tam, J., Fukumura, D., & Jain, R.K. Bone marrowderived mesenchymal stem cells facilitate engineering of long-lasting functional vasculature. Blood 111, 4551, 2008.
26. Kachgal, S., & Putnam, A.J. Mesenchymal stem cells from adipose and bone marrow promote angiogenesis via distinct cytokine and protease expression mechanisms. Angiogenesis 14, 47, 2011.
27. Merfeld-Clauss, S., Gollahalli, N., March, K.L., & Traktuev, D.O. Adipose tissue progenitor cells directly interact with endothelial cells to induce vascular network formation. Tissue Eng Part A 16, 2953, 2010.
28. Ghajar, C.M., Chen, X., Harris, J.W., Suresh, V., Hughes, C.C., Jeon, N.L., Putnam, A.J., & George, S.C. The effect of matrix density on the regulation of 3-D capillary morphogenesis. Biophys J 94, 1930, 2008.
29. Chen, X., Aledia, A.S., Popson, S.A., Him, L., Hughes, C.C., and George, S.C. Rapid anastomosis of endothelial progenitor cell-derived vessels with host vasculature is promoted by a high density of cotransplanted fibroblasts. Tissue Eng Part A 16, 585, 2010.
30. Motegi, S., Leitner, W.W., Lu, M., Tada, Y., Sardy, M., Wu, C., Chavakis, T., & Udey, M.C. Pericyte-derived MFG-E8 regulates pathologic angiogenesis. Arterioscler Thromb Vasc Biol 31, 2024, 2011.
31. Shepherd, B.R., Jay, S.M., Saltzman, W.M., Tellides, G., and Pober, J.S. Human aortic smooth muscle cells promote arteriole formation by coengrafted endothelial cells. Tissue Eng Part A 15, 165, 2009.
32. Grainger, S.J., & Putnam, A.J. Assessing the permeability of engineered capillary networks in a 3D culture. PLoS One 6, e22086, 2011.
33. Chen, X., Aledia, A.S., Ghajar, C.M., Griffith, C.K., Putnam, A.J., Hughes, C.C., & George, S.C. Prevascularization of a fibrin-based tissue construct accelerates the formation of functional anastomosis with host vasculature. Tissue Eng Part A 15, 1363, 2009.
34. Traktuev, D.O., Prater, D.N., Merfeld-Clauss, S., Sanjeevaiah, A.R., Saadatzadeh, M.R., Murphy, M., Johnstone, B.H., Ingram, D.A., & March, K.L. Robust functional vascular network formation in vivo by cooperation of adipose progenitor and endothelial cells. Circ Res 104, 1410, 2009.
35. Allen, P., Melero-Martin, J., & Bischoff, J. Type I collagen, fibrin and PuraMatrix matrices provide permissive environments for human endothelial and mesenchymal progenitor cells to form neovascular networks. J Tissue Eng Regen Med 5, e74, 2011.
36. Melero-Martin, J.M., Khan, Z.A., Picard, A., Wu, X., Paruchuri, S., & Bischoff, J. In vivo vasculogenic potential of human blood-derived endothelial progenitor cells. Blood 109, 4761, 2007.
37. Curry, F.E., Huxley, V.H., & Adamson, R.H. Permeability of single capillaries to intermediate-sized colored solutes. Am J Physiol 245, H495, 1983.
38. Hughes, S., & Chan-Ling, T. Characterization of smooth muscle cell and pericyte differentiation in the rat retina in vivo. Invest Ophthalmol Vis Sci 45, 2795, 2004.
39. Ehrbar, M., Djonov, V.G., Schnell, C., Tschanz, S.A., Martiny-Baron, G., Schenk, U.,Wood, J., Burri, P.H., Hubbell, J.A., and Zisch, A.H. Cell-demanded liberation of VEGF121 from fibrin implants induces local and controlled blood vessel growth. Circ Res 94, 1124, 2004.
40. Hiraoka, N., Allen, E., Apel, I.J., Gyetko, M.R., & Weiss, S.J. Matrix metalloproteinases regulate neovascularization by acting as pericellular fibrinolysins. Cell 95, 365, 1998.
41. Stevens, K.R., Kreutziger, K.L., Dupras, S.K., Korte, F.S., Regnier, M., Muskheli, V., Nourse, M.B., Bendixen, K., Reinecke, H., & Murry, C.E. Physiological function and transplantation of scaffold-free and vascularized human cardiac muscle tissue. Proc Natl Acad Sci U S A 106, 16568, 2009.
42. Phelps, E.A., Landazuri, N., Thule, P.M., Taylor, W.R., and Garcia, A.J. Bioartificial matrices for therapeutic vascularization. Proc Natl Acad Sci U S A 107, 3323, 2010.
43. Silva, E.A., Kim, E.S., Kong, H.J., & Mooney, D.J. Materialbased deployment enhances efficacy of endothelial progenitor cells. Proc Natl Acad Sci U S A 105, 14347, 2008.
44. Bexell, D., Gunnarsson, S., Tormin, A., Darabi, A., Gisselsson, D., Roybon, L., Scheding, S., & Bengzon, J. Bone marrow multipotent mesenchymal stroma cells act as pericytelike migratory vehicles in experimental gliomas. Mol Ther 17, 183, 2009.
45. Shi, S., & Gronthos, S. Perivascular niche of postnatal mesenchymal stem cells in human bone marrow and dental pulp. J Bone Miner Res 18, 696, 2003.
46. Hinz, B. Formation and function of the myofibroblast during tissue repair. J Invest Dermatol 127, 526, 2007.
47. Newman, A.C., Nakatsu, M.N., Chou, W., Gershon, P.D., and Hughes, C.C. The requirement for fibroblasts in angiogenesis: fibroblast-derived matrix proteins are essential for endothelial cell lumen formation. Mol Biol Cell 22, 3791, 2011.
48. Kachgal, S., Carrion, B., Janson, I.A., & Putnam, A.J. Bone marrow stromal cells stimulate an angiogenic program that requires endothelial MT1-MMP. J Cell Physiol 227, 3546, 2012.
49. Schechner, J.S., Nath, A.K., Zheng, L., Kluger, M.S., Hughes, C.C., Sierra-Honigmann, M.R., Lorber, M.I., Tellides, G., Kashgarian, M., Bothwell, A.L., & Pober, J.S. In vivo formation of complex microvessels lined by human endothelial cells in an immunodeficient mouse. Proc Natl Acad Sci U S A 97, 9191, 2000.