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The Morphogenesis of Primordial Vascular Networks

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Vascular Morphogenesis: In Vivo, In Vitro, In Mente

Part of the book series: Cardiovascular Molecular Morphogenesis ((CARDMM))

Abstract

This chapter will address the morphogenesis of the first blood vessels formed in the vertebrate embryo and several mechanisms regulating this process. The focus will be on the development of vessels and vascular networks that arise within the embryo proper. We have chosen to study the formation of the intraembryonic vessels (stage 7–10) because their morphogenesis is both well characterized and is free of associated hematopoiesis. The intraembryonic vessels arise from isolated mesodermal cells, angioblasts, and rapidly organize into a network of endothelial tubes arranged in a reproducible spatial pattern. We refer to these networks as primary vascular networks. The physical characteristics of primary networks, coupled with the fact that they can be studied in vivo, make them an important tool in understanding general principals of vessel formation. We will, in the following pages: (1) describe the early events of vasculogenesis that lead to the formation of the first vessels and vascular networks; (2) review our experimental efforts to understand the formation of this vasculature; and (3) discuss some of the interesting unanswered questions regarding early vessel morphogenesis.

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References

  • Aumailley, M., Gurrath, M., Muller, G., Calvete, J., Timpl, R., and Kessler, H. (1991). Arg-Gly-Asp constrained within cyclic pentapeptides. Strong and selective inhibitors of cell adhesion to vitronectin and a laminin fragment PI. Fed. Eur. Biochem. Soc. 291:50–54.

    Article  CAS  Google Scholar 

  • Britsch, S., Christ, B., and Jacob, H.J. (1989). The influence of cell-matrix interactions on the development of quail chorioallantoic vascular system. Anat. Embryol. 180:479–484.

    Article  PubMed  CAS  Google Scholar 

  • Bronner-Fraser, M. (1985). Alterations in neural crest migration by a monoclonal antibody that affects cell adhesion. J. Cell Biol. 101:610–617.

    Article  PubMed  CAS  Google Scholar 

  • Brooks, PC., Clark, R.A., and Cheresh, D.A. (1994). Requirement of vascular integrin alpha v beta 3 for angiogenesis. Science 264:569–571.

    Article  PubMed  CAS  Google Scholar 

  • Carmeliet, P., Ferreira, V., Brier, G., Pollefeyt, S., Kieckens, L., Gertsenstein, M., Fahrig, M., Van-denhoeck, A., Harpa, H., Eberhardt, C., Declercq, C., Pawling, J., Moons, L., Collen, D., Risau, W., and Nagy, A. (1996). Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 380(April): 435–439.

    Article  PubMed  CAS  Google Scholar 

  • Cheresh, D.A., and Spiro, R.C. (1987). Biosynthetic and functional properties of an Arg-Gly-Asp-directed receptor involved in human melanoma cell attachment of vitronectin, fibrinogen, and von Willebrand factor. J. Biol. Chem. 262:17703–17711.

    PubMed  CAS  Google Scholar 

  • Davis, S., Aldrich, T.H., Jones, P.F., Acheson, A., Compton, D.L., Jain, V., Ryan, T.E., Bruno, J., Radziejewski, C., Maisonpierre, PC., and Yancopoulos, G.D. (1996). Isolation of angiopoietin-1, a ligand for the Tie2 receptor, by secretion-trap expression cloning. Cell 887:1161–1169.

    Article  Google Scholar 

  • Drake, C.J., Cheresh, D.A., and Little, C.D. (1995). An antagonist of integrin avb3 prevents maturation of blood vessels during embryonic neovascularization. J. Cell. Sci. 108:2655–2661.

    PubMed  CAS  Google Scholar 

  • Drake, C.J., Davis, L.A., Hungerford, J.E., and Little, C.D. (1992). Perturbation of beta-1 integrin-mediated adhesions results in altered somite cell shape and behavior. Dev. Biol. 149: 327–338.

    Article  PubMed  CAS  Google Scholar 

  • Drake, C.J., Davis, L.A., and Little, C.D. (1992). Antibodies to beta 1 integrins cause alterations of aortic vasculogenesis, in vivo. Dev. Dyn. 193:83–91.

    Article  PubMed  CAS  Google Scholar 

  • Drake, C.J., Davis, L.A., Walters, L., and Little, C.D. (1990). Avian vasculogenesis and the distribution of collagens I, IV. laminin, and fibronectin in the heart primordia. J. Exp. Zool. 255:418–421.

    Article  Google Scholar 

  • Drake, C.J., and Jacobson, A.G. (1988). A survey by scanning electron microscopy of the extracellular matrix and endothelial components of the primordial chick heart. Anat. Rec. 222: 391–400.

    Article  PubMed  CAS  Google Scholar 

  • Drake, C.J., and Little, C.D. (1995). Exogenous vascular endothelial growth factor induces malformed and hyperfused vessels during embryonic neovascularization. Proc. Natl. Acad. Sci. USA 92:7657–7661.

    Article  PubMed  CAS  Google Scholar 

  • Dumont, D.J., Gradwohl, G., Fong, G.-H., Puri, M.C., Geertsenstein, M., Auerbach, A., and Breitman, M.L. (1994). Dominant-negative and targeted null mutations in the endothelial receptor tyrosine kinase, tek, reveal a critical role in vasculogenesis of the embryo. Genes Dev. 8:18977–1909.

    Article  Google Scholar 

  • Ferrara, N., Carver-Moore, K., Chen, H., Dowd, M., Lu, L., O’Shea, K.S., Powell-Braxton, L., Hillan, K.J., and Moore, M.W. (1996).Heterozygous embryoic lethality induced by targeted inactivation of the VEGF gene. Nature 380:439–442.

    Article  PubMed  CAS  Google Scholar 

  • Ferrara, N., and Henzel, W.J. (1989). Pituitary follicular cells secrete a novel heparin-binding growth factor specific for vascular endothelial cells. Biochem. Biophys. Res. Commun. 161:851.

    Article  PubMed  CAS  Google Scholar 

  • Flamme, I. (1989). Is extraembryonic angiogenesis in the chick embryo controlled by the endoderm? A morphological study. Anat. Embryol. 180:259–272.

    Article  PubMed  CAS  Google Scholar 

  • Flamme, I., Breier, G., and Risau, W. (1995). Vascular endothelial growth factor (VEGF) and VEGF receptor 2 (flk-1) are expressed during vasculogenesis and vascular differentiation in the quail embryo. Dev. Biol. 169:699–712.

    Article  PubMed  CAS  Google Scholar 

  • Folkman, J., and DAmore, PA. (1996). Blood vessel formation: What is its molecular basis? Cell 87:1153–1155.

    Article  PubMed  CAS  Google Scholar 

  • Fong, G.-H., Rossant, J., Gertsenstein, M., and Breitman, M.L. (1995). Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium. Nature 376: 66–70.

    Article  PubMed  CAS  Google Scholar 

  • Friedlander, M., Brooks, PC., Shaffer, R.W., Kincaid, C.M., Varner, J.A., and Cheresh, D.A. (1995). Definition of two angiogenic pathways by distinct av integrins. Science 270: 1500–1502.

    Article  PubMed  CAS  Google Scholar 

  • Gitay-Goren, H., Sokert, S., Vlodavsky, I., and Neufeld, G. (1992). The binding of vascular endothelial growth factor to its receptors is dependent on cell surface-associated heparin-like molecules. J. Biol. Chem. 267:6093–6098.

    PubMed  CAS  Google Scholar 

  • Greve, J.M., and Gottlieb, D.I. (1982). Monoclonal antibodies which alter the morphology of cultured chick myogenic cells. J Cell. Biochem. 18:221–229.

    Article  PubMed  CAS  Google Scholar 

  • Hanahan, D. (1996). Signaling vascular morphogenesis and maintenance. Cell Biol. 277: 48–50.

    Google Scholar 

  • Hogan, B.L.M. (1995). The TGF-B-related signalling system in mouse development. Sem. Dev. Biol. 6:257–265.

    Article  CAS  Google Scholar 

  • Hynes, R.O. (1992). Integrins: versatility, modulation, and signaling in cell adhesion. Cell 69: 11–25.

    Article  PubMed  CAS  Google Scholar 

  • Hynes, R.O., and Bader, B.L. (1997). Targeted mutations in integrins and their ligands: their implications for vascular biology. Thromb. Haemostas. 78:83–87.

    CAS  Google Scholar 

  • Jacob, M., Christ, B., Jacob, H.J., and Poelmann, R.E. (1991). The role of fibronectin and laminin in development and migration of the avian Wolffian duct with reference to somitogenesis. Anat. Embryol.

    Google Scholar 

  • Jaffredo, T., Horwitz, A.F., Buck, C.A., Rong, P.M., and Dieteerlen-Lievre, F. (1988). Myoblast migration specifically inhibited in the chick embryo by grafted CSAT hybridoma cell secreting an anti-integrin antibody. Development 103:431–446.

    PubMed  CAS  Google Scholar 

  • Juliano, R.L., and Haskill, S. (1993). Signal transduction from the extracellular matrix. J. Cell. Biol. 120:577–585.

    Article  PubMed  CAS  Google Scholar 

  • Kallianpur, A.R., Jordan, J.E., and Brandt, S.J. (1994). The SCL/TAL-1 gene is expressed in progenitors of both the hematopoietic and vascular systems during embryogenesis. Blood 83: 1200–1208.

    PubMed  CAS  Google Scholar 

  • Leung, D.W., Cachianes, G., Kuang, W.-J., Goddel, D.V., and Ferrara, N. (1989). Vascular endothelial growth factor is a secreted angiogenic mitogen. Science 246:1306–1309.

    Article  PubMed  CAS  Google Scholar 

  • Maisonpierre, PC., Suri, C., Jones, P.F., Bartunkova, S., Wiegand, S.J., Compton, D., McClain, J., Aldrich, T.H., Papadopoulos, N., Daly, T.J., Davis, S., Sato, T.N., and Yancopoulos, G.D. (1997). Angiopoietin-2, a natural antagonist for Tie2 that disrupts in vivo angiogenesis. Science 277:55–60.

    Article  PubMed  CAS  Google Scholar 

  • Neff, N.T., Lowrey, C., Decker, C., Tovar, A., Damsky, C., Buck, C., and Horwitz, A.F. (1982). A monoclonal antibody detaches embryonic skeletal muscle from extracellular matrices. J. Cell Biol. 95:654–666.

    Article  PubMed  CAS  Google Scholar 

  • New, D., (1955). A new technique for the cultivation of the chick embryo in vitro. J. Exp. Morphol. 3:320–331.

    Google Scholar 

  • Nicosia, R.F., and Bonanno, E. (1991). Inhibition of angiogenesis in vitory by Arg-Gky-Asp-containing synthetic peptide. Am. J. Pathol. 138:829–833.

    PubMed  CAS  Google Scholar 

  • Noden, D. (1989). Embryonic origins and assembly of blood vessels. Am. Rev. Respir. Dis. 140: 1097–1103.

    PubMed  CAS  Google Scholar 

  • Pardanaud, L., Altmann, C., Kitos, P., Dieterien-Lievre, F., and Buck, C.A. (1987). Vasculogene-sis in the early quail blastodisc as studied with a monoclonal antibody recognizing endothelial cells. Development 100:339–349.

    PubMed  CAS  Google Scholar 

  • Park, J.E., Keller, G.-A., and Ferrara, N. (1993). The vascular endothelial growth factor (VEGF) isoforms: differential deposition into the subepithelial extracellular matrix and bioactivity of extracellular matrix-bound VEGF. Mol. Biol. Cell 4:1317–1326.

    PubMed  CAS  Google Scholar 

  • Poole, T.J., and Coffin, J.D. (1989). Vasculogenesis and angiogenesis: two distinct morphogenetic mechanisms establish embryonic vascular pattern. J. Exp. Zool. 251:224–231.

    Article  PubMed  CAS  Google Scholar 

  • Risau, W., and Flamme, I. (1995). Vasculogenesis. Annu. Rev. Cell Dev. Biol. 11:73–91.

    Article  PubMed  CAS  Google Scholar 

  • Ruoslahti, E. (1991). Integrins. J. Clin. Invest. 87:1–5.

    Article  PubMed  CAS  Google Scholar 

  • Sato, T.N., Tozawa, Y., Deutsch, U., Wolburg-Buchholz, K., Fujiwara, Y., Gendron-Maguire, M., Gridley, T., Wolburg, H., Risau, W., and Qin, Y. (1995). Distinct roles of the receptor tyrosine kinases Tie-1 and Tie-2 in blood vessel formation. Nature 376:70–74.

    Article  PubMed  CAS  Google Scholar 

  • Senger, D.R., Ledbetter, S.R., Claffey, K.P., Papadopoulos-Sergiou, A., Perruzzi, C., and Detmar, M. (1996). Stimulation of endothelial cell migration by vascular permeability factor/vascular endothelial growth factor through cooperative mechanisms involving the αvβ3 integrin, osteopontin, and thrombin. Am. J. Pathol. 149:293–305.

    PubMed  CAS  Google Scholar 

  • Shalaby, F., Rossant, J., Yamaguchi, T.P., Gertsenstein, M., Wu, X.-F., Breitman, M.L., and Schuh, A.C. (1995). Failure of blood-island and vasculogenesis in Flk-1-deficient mice. Nature 376:62–66.

    Article  PubMed  CAS  Google Scholar 

  • Sugi, Y., and Markwald, R.R. (1996). Formation and early morphogenesis of endocardial endothelial precursor cells and the role of the endoderm. Dev. Biol. 175:66–83.

    Article  PubMed  CAS  Google Scholar 

  • Suri, C., Jones, P.F., Patan, S., Bartunkova, S., Maisonpierre, PC., Davis, S., Sato, T.N., and Yancopoulos, G.D. (1996). Requisite role of angiopoietin-1, a ligand for the Tie2 receptor, during embryonic angiogenesis. Cell 87:1172–1190.

    Article  Google Scholar 

  • Tessler, S., Rockwell, P, Hicklin, D., Cohen, T., Levi, B.-Z., Witte, L., Lemischka, I.R., and Neufeld, G. (1994). Heparin modulates the interaction of VEGF165 with soluble and cell associated flk-1 receptors. J. Biol. Chem. 269(17): 12456–12461.

    PubMed  CAS  Google Scholar 

  • Vernon, R.B., Lara, S.L., Drake, C.J., Iruela-Arispe, M.L., Angello, J.C., Little, C.D., Wight, T.N., and Sage, E.H. (1994). Organized type I collagen influences endothelial patterns during “spontaneous angiogenesis in vitro”: planar cultures as models of vascular development. In Vitro Cell Dev. Biol. 107:2690–2695.

    Google Scholar 

  • Vikkula, M., Boon, L.M., Carraway, K.L.I., Calvert, J.T., Diamonti, A.J., Goumnerov, B., Pasyk, K.A., Marchuk, D.A., Warman, M.L., Cantley, L.C., Mulliken, J.B., and Olsen, B.R. (1996). Vascular dysmorphogenesis caused by an activating mutation in the receptor tyrosine kinase TIE2. Cell 87:1181–1190.

    Article  PubMed  CAS  Google Scholar 

  • Vlodavsky, I., Fuks, Z., Ishai-Michaeli, R., Bashkin, P., Levi, E., Korner, G., Bar-Shavit, R., and Klagsbrun, M. (1991). Extracellular matrix-resident basic fibroblast growth factor: implication for the control of angiogenesis. J Cell. Biochem. 45:167–176.

    Article  PubMed  CAS  Google Scholar 

  • Wilting, J., and Christ, B. (1996). Embryonic angiogenesis: a review. Naturwissenschaften 153–164.

    Google Scholar 

  • Wilting, J., Christ, B., Bokeloh, M., and Weich, H.A. (1993). In vivo effects of vascular endothelial growth factor on the chicken chorioallantoic membrane. Cell Tissue Res. 274: 163–172.

    Article  PubMed  CAS  Google Scholar 

  • Wilting, J., Christ, B., and Weich, H.A. (1992). The effects of growth factors on the day 13 chorioallantoic membrane (CAM): a study of VEGF165 and PDGF-BB. Anat. Embryol. 186:251–257.

    Article  PubMed  CAS  Google Scholar 

  • Yamada, K.M., and Miyamoto, S. (1995). Integrin transmembrane signaling and cytoskeletal control. Curr. Opin. Cell Biol. 7:681–689.

    Article  PubMed  CAS  Google Scholar 

  • Yamamura, H., Zhang, M., Markwald, R.R., and Mjaatvedt, C.H. (1997). A heart segmental defect in the anterior-posterior axis of a transgenic mutant mouse. Dev. Biol. 186:58–72.

    Article  PubMed  CAS  Google Scholar 

  • Yang, J.T., and Hynes, R.O. (1996). Fibronectin receptor functions in embryonic cells deficient in alpha 5 beta 1 integrin can be replaced by alpha v integrins. Mol. Biol. Cell 7: 1737–1748.

    PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Cell Biology and Anatomy, Medical University of South Carolina, 161 Ashley Avenue, 29425, Charleston, SC, USA

    Christopher J. Drake & Charles D. Little

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  1. Christopher J. Drake
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  2. Charles D. Little
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Editors and Affiliations

  1. Department of Cell Biology and Anatomy, Medical University of South Carolina, 29425-2204, Charleston, SC, USA

    Charles D. Little  & Vladimir Mironov  & 

  2. Department of Biological Structures, University of Washington School of Medicine, 98195-7420, Seattle, WA, USA

    E. Helene Sage

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© 1996 Birkhäuser

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Drake, C.J., Little, C.D. (1996). The Morphogenesis of Primordial Vascular Networks. In: Little, C.D., Mironov, V., Sage, E.H. (eds) Vascular Morphogenesis: In Vivo, In Vitro, In Mente. Cardiovascular Molecular Morphogenesis. Birkhäuser Boston. https://doi.org/10.1007/978-1-4612-4156-0_2

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  • DOI: https://doi.org/10.1007/978-1-4612-4156-0_2

  • Publisher Name: Birkhäuser Boston

  • Print ISBN: 978-1-4612-8678-3

  • Online ISBN: 978-1-4612-4156-0

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