Abstract
This study compares phenotypic changes of human umbilical endothelial vein cells cultured in three-dimensional collagen matrixes in the presence of basic fibroblast growth factor or on Matrigel coats. Under both conditions, endothelial cells rapidly assembled into an irregular network of tubular structures with a high frequency of intercellular or lumen-like spaces. Tubular structures were characterized and compared by phase-contrast, confocal and electron microscopy. The dominant mechanism of lumen-like formation was highly model-dependent. Ultrastructural analyses of capillary-like structures and the mechanism of lumen-like formation indicated that the in vivo angiogenesis was better reproduced in the collagen model.
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Risau W, Flamme I. Vasculogenesis. Annu Rev Cell Dev Biol 1995; 11: 73–91.
Folkman J. Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat Med 1995; 1(1): 27–31.
Carmeliet P, Jain RK. Angiogenesis in cancer and other diseases. Nature 2000; 407(6801): 249–57.
Ilan N, Mahooti S, Madri JA. Distinct signal transduction pathways are utilized during the tube formation and survival phases of in vitro angiogenesis. J Cell Sci 1998; 111(Pt 24): 3621–31.
Bach TL, Barsigian C, Chalupowicz DG et al. VE-Cadherin mediates endothelial cell capillary tube formation in fibrin and collagen gels. Exp Cell Res 1998; 238(2): 324–4.
Chalupowicz DG, Chowdhury ZA, Bach TL et al. Fibrin II induces endothelial cell capillary tube formation. J Cell Biol 1995; 130(1): 207–15.
Kubota Y, Kleinman HK, Martin GR, Lawley TJ. Role of laminin and basement membrane in the morphological differentiation of human endothelial cells into capillary-like structures. J Cell Biol 1988; 107(4): 1589–98.
Esser S, Lampugnani MG, Corada M et al. Vascular endothelial growth factor induces VE-cadherin tyrosine phosphorylation in endothelial cells. J Cell Sci 1998; 111(Pt 13): 1853–65.
Davis GE, Camarillo CW. An alpha 2 beta 1 integrin-dependent pinocytic mechanism involving intracellular vacuole formation and coalescence regulates capillary lumen and tube formation in threedimensional collagen matrix. Exp Cell Res 1996; 224(1): 39–51.
Gamble J, Meyer G, Noack L et al. B1 integrin activation inhibits in vitro tube formation: Effects on cell migration, vacuole coalescence and lumen formation. Endothelium 1999; 7(1): 23–34.
Meyer GT, Matthias LJ, Noack L et al. Lumen-like formation during angiogenesis in vitro involves phagocytic activity, formation and secretion of vacuoles, cell death, and capillary tube remodelling by different populations of endothelial cells. Anat Rec 1997; 249(3): 327–40.
Yang S, Graham J, Kahn JW et al. Functional roles for PECAM-1 (CD31) and VE-cadherin (CD144) in tube assembly and lumen formation in three-dimensional collagen gels. Am J Pathol 1999; 155(3): 887–95.
Montañez E, Pagan R, Reina M, Vilaró S. A computerized analysis system for screening new angiogenic factors. Microscopy and Analysis (in press).
Dorovini-Zis K, Huynh HK. Ultrastructural localization of factor VIII-related antigen in cultured human brain microvessel endothelial cells. J Histochem Cytochem 1992; 40(5): 689–96.
Marszalek A, Daa T, Kashima K, Nakayama I, Yokoyama S. Ultrastructural and morphometric studies related to expression of the cell adhesion molecule PECAM-1/CD31 in developing rat lung. J Histochem Cytochem 2000; 48(9): 1283–89.
Kagawa H, Fujimoto S. Electron-microscopic and immunocytochemical analyses of Weibel-Palade bodies in the human umbilical vein during pregnancy. Cell Tissue Res 1987; 249(3): 557–63.
Jaffe EA, Hoyer LW, Nachman RL. Synthesis of von Willebrand factor by cultured human endothelial cells. Proc Natl Acad Sci USA 1974; 71(5): 1906–9.
Wagner DD, Olmsted JB, Marder VJ. Immunolocalization of von Willebrand protein in Weibel-Palade bodies of human endothelial cells. J Cell Biol 1982; 95(1): 355–60.
Albelda SM, Muller WA, Buck CA, Newman PJ. Molecular and cellular properties of PECAM-1 (endoCAM/CD31): A novel vascular cell-cell adhesion molecule. J Cell Biol 1991; 114(5): 1059–68.
DeLisser HM, Christofidou-Solomidou M, Strieter RM et al. Involvement of endothelial PECAM-1/CD31 in angiogenesis. Am J Pathol 1997; 151(3): 671–7.
Newman PJ. The biology of PECAM-1. J Clin Invest 1997; 100(Suppl 11): S25–9.
Schechner JS, Nath AK, Zheng L et al. In vivo formation of complex microvessels lined by human endothelial cells in an immunodeficient mouse. Proc Natl Acad Sci USA 2000; 97(16): 9191–6.
Brooks PC, Montgomery AM, Rosenfeld M et al. Integrin alpha v beta 3 antagonists promote tumor regression by inducing apoptosis of angiogenic blood vessels. Cell 1994; 79(7): 1157–64.
Ghadially FN. Ultrastructural Pathology of the Cell and Matrix, 4th edition. Boston: Butterworths-Heinemann 1997.
Ingber DE, Folkman J. Mechanochemical switching between growth and differentiation during fibroblast growth factor-stimulated angiogenesis in vitro: Role of extracellular matrix. J Cell Biol 1989; 109: 317–30.
Bloom W, Fawcett DW. Textbook of Histology, 8th edition, New York: Chapman & Hall 1994.
Bikfalvi A, Cramer EM, Tenza D, Tobelem G. Phenotypic modulations of human umbilical vein endothelial cells and human dermal fibroblasts using two angiogenic assays. Biol Cell 1991; 72(3): 275–8.
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Montañez, E., Casaroli-Marano, R.P., Vilaró, S. et al. Comparative study of tube assembly in three-dimensional collagen matrix and on Matrigel coats. Angiogenesis 5, 167–172 (2002). https://doi.org/10.1023/A:1023837821062
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DOI: https://doi.org/10.1023/A:1023837821062