Modulation of microvascular growth and morphogenesis by reconstituted basement membrane gel in three-dimensional cultures of rat aorta: A comparative study of angiogenesis in Matrigel, collagen, fibrin, and plasma clot
Purchase on Springer.com
$39.95 / €34.95 / £29.95*
Rent the article at a discountRent now
* Final gross prices may vary according to local VAT.
Rings of rat aorta cultured in Matrigel, a reconstituted gel composed of basement membrane molecules, gave rise to three-dimensional networks composed of solid cellular cords and occasional microvessels with slitlike lumina. Immunohistochemical and ultrastructural studies showed that the solid cords were composed of endothelial sprouts surrounded by nonendothelial mesenchymal cells. The angiogenic response of the aortic rings in Matrigel was compared to that obtained in interstitial collagen, fibrin, or plasma clot. Morphometric analysis demonstrated that the mean luminal area of the microvascular sprouts and channels was significantly smaller in Matrigel than in collagen, fibrin, or plasma clot. The percentage of patent microvessels in Matrigel was also markedly reduced. Autoradiographic studies of3H-thymidine-labeled cultures showed reduced DNA synthesis by developing microvessels in Matrigel. The overall number of solid endothelial cords and microvessels was lower in Matrigel than in fibrin or plasma clot. A mixed cell population isolated from Matrigel cultures formed a monolayer in collagen or fibrin-coated dishes but rapidly reorganized into a polygonal network when plated on Matrigel. The observation that gels composed of basement membrane molecules modulate the canalization, proliferation, and organization into networks of vasoformative endothelial cells in three-dimensional cultures supports the hypothesis that the basement membrane is a potent regulator of microvascular growth and morphogenesis.
- Alessandri, G.; Raju, K.; Gullino, P. M. Mobilization of capillary endothelium in vitro induced by effectors of angiogenesis in vitro. Cancer Res. 43: 1790–1797; 1983.
- Banda, M. J.; Knighton, D. R.; Hunt, T. K., et al. Isolation of non-mitogenic angiogenesis factor from wound fluid. Proc. Natl. Acad. Sci. USA 79: 7773–7777; 1982. CrossRef
- Bissell, D. M.; Arenson, D. M.; Maher, J. J., et al. Support of cultured hepatocytes by a laminin-rich gel. J. Clin. Invest. 79: 801–812; 1986. CrossRef
- Chen, W. T.; Chen, J. M.; Mueller, S. C. Coupled expression and colocalization of 140K adhesion molecules, fibronectin and laminin during morphogenesis and cytodifferentiation of chick lung cells. J. Cell Biol. 103: 1073–1090; 1986. CrossRef
- Cliff, W. J. Observations on healing tissue: a combined light and electron microscopic investigation. Philos. Trans. R. Soc. Lond. Biol. Sci. 246: 305–325; 1962. CrossRef
- Dvorak, H. F.; Harvey, V. S.; Estrella, P., et al. Fibrincontaining gels induce angiogenesis: implications for tumor stroma generation and wound healing. Lab. Invest. 57: 673–686; 1987.
- Elsdale, T.; Bard, J. Collagen substrata for studies on cell behavior. J. Cell Biol. 54: 626–637; 1972. CrossRef
- Esch, F.; Baird, A.; Ling, N., et al. Primary structure of bovine basic fibroblast growth factor (bFGF) and comparison with the amino-terminal sequence of bovine brain acidic FGF. Proc. Natl. Acad. Sci. USA 82: 6507–6511; 1985. CrossRef
- Emonard, H.; Calle, A.; Grimaud, J. A., et al. Interactions between fibroblasts and a reconstituted basement membrane matrix. J. Invest. Dermatol. 89: 156–163; 1987. CrossRef
- Feder, J.; Marasa, J. C.; Olander, J. V. The formation of capillary-like tubes by calf aortic endothelial cells grown in vitro. J. Cell. Physiol. 116: 1–6; 1983. CrossRef
- Folkman, J.; Haudenschild, C. Angiogenesis in vitro. Nature 288: 551–556; 1980. CrossRef
- Folkman, J.; Klagsburn, M. Angiogenic factors. Science 235: 442–447; 1987. CrossRef
- Form, D. M.; Pratt, B. M.; Madri, J. A. Endothelial cell proliferation during angiogenesis: in vitro modulation by basement membrane components. Lab. Invest 55: 521–530; 1986.
- Gospodarowicz, D.; Neufeld, G.; Schweigerer, L. Fibroblast growth factor. Mol. Cell. Endocrinol. 46: 187–204; 1986. CrossRef
- Gospodarowicz, D.; Massoglia, S.; Cheng, J., et al. Effect of fibroblast growth factor and lipoproteins on the proliferation of endothelial cells derived from bovine adrenal cortex, brain cortex, and corpus luteum capillaries. J. Cell. Physiol. 127: 121–136; 1986. CrossRef
- Gross, J. L.; Moscatelli, D.; Rifkin, D. B. Increased capillary endothelial cell protease activity in response to angiogenic stimuli in vitro. Proc. Natl. Acad. Sci. USA 80: 2623–2627; 1983. CrossRef
- Hadley, M. A.; Byers, S. W.; Suarez-Quian, C. A., et al. Extracellular matrix regulates Sertoli cells differentiation, testicular cord formation, and germ cell development in vitro. J. Cell Biol. 101: 1511–1522; 1985. CrossRef
- Herbst, T. J.; McCarthy, J. B.; Tsilibary, E. C., et al. Differential effects of laminin, intact type IV collagen and specific domains of type IV collagen on endothelial cell adhesion and migration. J. Cell Biol. 106: 1365–1373; 1988. CrossRef
- Ingber, D. E.; Madri, J. A.; Folkman, J. A possible mechanism for inhibition of angiogenesis by angiostatic steroids: induction of capillary basement membrane dissolution. Endocrinology 119: 1768–1774; 1986. CrossRef
- Ingber, D. E.; Madri, J. A.; Folkman, J. Endothelial growth factors and extracellular matrix regulate DNA synthesis through modulation of cell and nuclear expansion. In Vitro Cell. Dev. Biol. 23: 387–394; 1987. CrossRef
- Ingber, D.; Folkman, J. Inhibition of angiogenesis through modulation of collagen metabolism. Lab. Invest. 59: 44–51; 1988.
- Kalebic, T.; Garbisa, S.; Glaser, B., et al. Basement membrane collagen: degradation by migrating endothelial cells. Science 221: 281–283; 1983. CrossRef
- Kleinman, H. K.; McGarvey, M. L.; Hassell, J. R., et al. Basement membrane complexes with biological activity. Biochemistry 25: 312–318; 1986. CrossRef
- Kubota, Y.; Kleinman, H. K.; Martin, G. R., et al. Role of laminin and basement membrane in the morphological differentiation of human endothelial cells into capillary-like structures. J. Cell Biol. 107: 1589–1598; 1988. CrossRef
- Leibovich, S. J.; Polverini, P. J.; Shepard, H. M., et al. Macrophage-induced angiogenesis is mediated by tumor necrosis factor-alpha. Science 329: 630–631; 1987.
- Maciag, T.; Kadish, J.; Wilkins, L., et al. Organizational behavior of human umbilical vein endothelial cells. J. Cell Biol. 94: 511–520; 1982. CrossRef
- Macarak, E. J.; Howard, P. S. Adhesion of endothelial cells to extracellular matrix proteins. J. Cell Physiol. 116: 76–86; 1983. CrossRef
- McGuire, P. G.; Orkin, R. W. Isolation of rat aortic endothelial cells by primary explant techniques and their phenotypic modulation by defined substrata. Lab. Invest. 57: 94–104; 1987.
- Madri, J. A.; Williams, S. T. Capillary endothelial cell cultures: phenotypic modulation by matrix components. J. Cell Biol. 97: 153–165; 1983. CrossRef
- Madri, J. A.; Pratt, B. M.; Tucker, A. M. Phenotypic modulation of endothelial cells by TGF-beta depends upon the composition and organization of the extracellular matrix. J. Cell Biol. 106: 1375–1384; 1988. CrossRef
- Mignatti, P.; Tsuboi, R.; Robbins, E., et al. In vitro angiogenesis on the human amniotic basement membrane: requirement for basic fibroblast growth factor-induced proteinases. J. Cell Biol. 108: 671–682; 1989. CrossRef
- Montesano, R.; Orci, L.; Vassalli, P. In Vitro rapid organization of endothelial cells into capillary-like networks is promoted by collagen matrices. J. Cell Biol. 97: 1648–1652; 1983. CrossRef
- Montesano, R.; Orci, L. Tumor-promoting phorbol esters induce angiogenesis in vitro. Cell 42: 469–477; 1985. CrossRef
- Montesano, R.; Vassalli, J. D.; Baird, A., et al. Basic fibroblast growth factor induces angiogenesis in vitro. Proc. Natl. Acad. Sci. USA 83: 7297–7301; 1986. CrossRef
- Nicosia, R. F.; Tchao, R.; Leighton, J. Histotypic angiogenesis in vitro: light microscopic, ultrastructural, and radio-autographic studies. In Vitro 18: 538–549; 1982. CrossRef
- Nicosia, R. F. Angiogenesis and the formation of lymphaticlike channels in cultures of thoracic duct. In Vitro Cell. Dev. Biol. 23: 167–174; 1987. CrossRef
- Nicosia, R. F.; Madri, J. A. The microvascular extracellular matrix: developmental changes during angiogenesis in the aortic ring plasma clot model. Am. J. Pathol. 128: 78–90; 1987.
- Nicosia, R. F.; Madri, J. A. The extracellular matrix produced during angiogenesis in culture. In: Gallo, L. L., ed. Cardiovascular disease. New York: Plenum Press; 1987; 185–192.
- Risau, W.; Lemmon, V. Changes in the vascular extracellular matrix during embryonic vasculogenesis and angiogenesis. Dev. Biol. 125: 441–450; 1988. CrossRef
- Roberts, A. B.; Sporn, M. B.; Assoian, R. K., et al. Transforming growth factor type-beta: rapid induction of fibrosis and angiogenesis in vivo and stimulation of collagen formation in vitro. Proc. Natl. Acad. Sci. USA 83: 4167–4171; 1986. CrossRef
- Sariola, H.; Peault, B.; LeDouarin, N. M., et al. Extracellular matrix and capillary ingrowth in interspecies chimeric kidneys. Cell. Differ. 15: 43–52; 1984. CrossRef
- Schoefl, G. I. Studies on inflammation. III. Growing capillaries: their structure and permeability. Virchows Arch. Pathol. Anat. 337: 97–141; 1963. CrossRef
- Shing, Y.; Folkman, J.; Sullivan, R., et al. Heparin affinity: purification of a tumor-derived capillary endothelial cell growth factor. Science 223: 1296–1299; 1984. CrossRef
- Thomas, K. A.; Gimenez-Gallego, G. Fibroblast growth factors: broad spectrum mitogens with potent angiogenic activity. Trends Biochem. Sci. 11: 81–84; 1986. CrossRef
- Tonnesen, M. G.; Jenkins, D.; Siegal, S. L., et al. Expression of fibronectin, laminin, and factor VIII-related antigen during development of the human cutaneous microvasculature. J. Invest. Dermatol. 85: 564–568; 1985. CrossRef
- Ungari, S.; Katari, R. S.; Alessandri, G., et al. Cooperation between fibronectin and heparin in the mobilization of capillary endothelium. Invasion & Metastasis 5: 193–205; 1985.
- Young, W. C.; Herman, I. M. Extracellular matrix modulation of endothelial cell shape and motility following injury in vitro. J. Cell Sci. 73: 19–32; 1985.
- Modulation of microvascular growth and morphogenesis by reconstituted basement membrane gel in three-dimensional cultures of rat aorta: A comparative study of angiogenesis in Matrigel, collagen, fibrin, and plasma clot
In Vitro Cellular & Developmental Biology
Volume 26, Issue 2 , pp 119-128
- Cover Date
- Print ISSN
- Online ISSN
- Additional Links
- basement membrane
- extracellular matrix
- Industry Sectors