Autoregulation of Angiogenesis by Cells of the Vessel Wall

https://doi.org/10.1016/S0074-7696(08)60148-5Get rights and content

The cells of the vessel wall can regulate angiogenesis by producing growth factorsd, proteolytic enzymes, extracellular matrix components, cell adhesion molecules, and vasoactive factors. This property enables preexisting blood vessels to generate new vessels in the absence of exogenous angiogenic stimuli. Vascular autoregulation of angiogenesis can be studied by culturing rat aortic or venous explants in collagen gels under serum-free conditions. In this system, the combined effect of injury and exposure of explants to collagen triggers a self-limited angiogenic response. Interactions among endothelial cells, smooth muscle cells, and fibroblasts play a critical role in the regulation of this process. This chapter reviews the literature on angiogenesis, focusing on the vessel wall as a highly specialized and plastic tissue capable of regenerating itself through autocrine, paracrine, and juxtacrine mechanisms.

References (237)

  • A. Fine et al.

    The effect of transforming growth factor-β on cell proliferation and collagen formation by lung fibroblasts.

    J. Biol. Chem.

    (1987)
  • N. Fournier et al.

    In vitro angiogenesis in fibrin matrices containing fibronectin or hyaluronic acid.

    Cell Biol. Int. Rep.

    (1992)
  • R.J. Gorlin

    Fibroblast growth factors, their receptors and receptor disorders.

    J. Cranio-Maxillo-Facial Surg.

    (1997)
  • D. Gospodarowicz et al.

    Molecular and biological characterization of fibroblast growth factor, an angiogenic factor which also controls the proliferation and differentiation of mesoderm and neuroectoderm derived cells.

    Cell Differ.

    (1986)
  • H.A. Hansson et al.

    Transient expression of insulin-like growth factor I immunoreactivity by vascular cells during angiogenesis.

    Exp. Mol. Pathol.

    (1989)
  • S. Higashiyama et al.

    Structure of heparin-binding EGF-like growth factor. Multiple forms, primary structure and glycosylation of the mature protein.

    J. Biol. Chem.

    (1992)
  • D. Ingber et al.

    How does extracellular matrix control capillary morphogenesis?

    Cell

    (1989)
  • W. Jakob et al.

    Demonstration of angiogenesis activity in the corpus luteum of cattle.

    Exp. Pathol.

    (1977)
  • V. Kainulainen et al.

    Suppression of syndecan-1 expression in endothelial cells by tumor necrosis factor-alpha

    J. Biol. Chem.

    (1996)
  • A. Kazlauskas et al.

    Cultured endothelial cells do not respond to a platelet-derived growth factor-like protein in an autocrine manner

    Biochim. Biophys. Acta

    (1985)
  • M. Akita et al.

    Formation of new capillary-like tubes in a three-dimensional in vitro model (aorta/collagen gel)

    Anatomischer Anzeiger.

    (1997)
  • H.N. Antoniades et al.

    Isolation of a cationic polypeptide from human serum which stimulates the proliferation of 3T3 cells.

    Proc. Natl. Acad. Sci. USA

    (1975)
  • H.N. Antoniades et al.

    Injury induces in vivo expression of PDGF and PDGF receptor mRNA in skin epithelial cells and PDGF mRNA in connective tissue fibroblasts.

    Proc. Natl. Acad. Sci. USA

    (1991)
  • D. Ausprunk et al.

    The sequence of events in the regression of corneal capillaries.

    Lab. Invest.

    (1978)
  • E. Bacharach et al.

    In vivo patterns of expression of urokinase and its inhibitor PAI-1 suggest a concerted role in regulating physiological angiogenesis.

    Proc. Natl. Acad. Sci. USA

    (1992)
  • R.S. Bar

    Vascular endothelium and diabetes mellitus.

  • R.S. Bar et al.

    The effects of platelet-derived growth factor in cultured microvessel endothelial cells.

    J. Endocrinol.

    (1989)
  • A.C. Barger et al.

    Hypothesis: Vasa vasorum and neovascularization of human coronary arteries.

    N. Engl. J. Med.

    (1984)
  • B.C. Berk et al.

    Vasoconstriction: A new activity for platelet-derived growth factor.

    Science

    (1986)
  • A. Bobik et al.

    Growth factor activity of endothelin on vascular smooth muscle.

    Am. J. Physiol.

    (1990)
  • P. Borgstrom et al.

    Complete inhibition of angiogenesis and growth of microtumors by anti-vascular endothelial growth factor neutralizing antibody: Novel concepts of angiostatic therapy from intravital videomicroscopy.

    Cancer Res.

    (1996)
  • B.A. Bouchard et al.

    Human brain pericytes differentially regulate expression of procoagulant enzyme complexes comprising the extrinsic pathway of blood coagulation.

    Arterioscl. Thromb. Vasc. Biol.

    (1997)
  • E. Brogi et al.

    Indirect angiogenic cytokines upregulate VEGF and bFGF gene expression in vascular smooth muscle cells, whereas hypoxia upregulates VEGF expression only.

    Circulation

    (1994)
  • P.C. Brooks et al.

    Requirement of vascular integrin αvβ3 for angiogenesis.

    Science

    (1994)
  • J. Brown et al.

    A novel in vitro assay of human angiogenesis.

    Lab. Invest.

    (1996)
  • L.F. Brown et al.

    Expression of vascular permeability factor (vascular endothelial growth factor) by epidermal keratinocytes during wound healing.

    J. Exp. Med.

    (1992)
  • F. Bussolino et al.

    Hepatocyte growth factor is a potent angiogenic factor which stimulates endothelial cell motility and growth.

    J. Cell Biol.

    (1992)
  • P. Carmeliet et al.

    Role of tissue factor in embryonic tissue development.

    Nature

    (1996)
  • P. Carmeliet et al.

    Insights in vessel development and vascular disorders using targeted inactivation and transfer of vascular endothelial growth factor, the tissue factor receptor and the plasminogen system.

  • P. Carmeliet et al.

    Impaired arterial neointima formation in mice with disruption of the plasminogen gene.

    J. Clin. Invest.

    (1997)
  • B. Christ et al.

    Vascular endothelial cells migrate centripetally within embryonic arteries.

    Anat. Embryol.

    (1990)
  • E.R. Clark et al.

    Microscopic observation on the growth of blood capillaries in the living mammal.

    Am. J. Anat.

    (1939)
  • A. Coffer et al.

    Purification and characterization of biologically active scatter factor from ras-transformed NIH 3T3 conditioned medium.

    Biochem. J.

    (1991)
  • J. Contrino et al.

    In situ detection of tissue factor in vascular endothelial cells: Correlation with the malignant phenotype of human breast disease.

    Nature Med.

    (1996)
  • C. Cordon-Cardo et al.

    Expression of basic fibroblast growth factor in normal human tissues.

    Lab. Invest.

    (1990)
  • T. Couffinhal et al.

    Vascular endothelial growth factor/vascular permeability factor (VEGF/VPF) in normal and atherosclerotic human arteries.

    Am. J. Pathol.

    (1997)
  • P. D'Amore et al.

    Growth factor effects on cells of the vascular wall: A survey.

    Growth Factors

    (1993)
  • E. Dejana

    Endothelial adherens junctions: Implications in the control of vascular permeability and angiogenesis.

    J. Clin. Invest.

    (1996)
  • E. Dejana et al.

    Intercellular junctions in the endothelium and control of vascular permeability.

  • P. Delafontaine et al.

    Regulation of insulin-like growth factor I messenger RNA levels in vascular smooth muscle cells.

    Hypertension

    (1991)
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