Skip to main content
SpringerLink
Log in

Reciprocal Relationship Between VE-Cadherin and Matrix Metalloproteinases Expression in Endothelial Cells and Its Implications to Angiogenesis

  • Conference paper
  • First Online:
Book cover Perspectives in Cancer Prevention-Translational Cancer Research

  • 1518 Accesses

Abstract

Angiogenesis, the process of new blood vessel formation from preexisting ones, is critical in the development and progression of tumor. Since metastasis is favored by increased neovascularization, understanding the molecular mechanism governing angiogenesis gains utmost importance. Endothelial cells respond to numerous angiogenic factors like VEGF and switch over to angiogenic phenotype. Apart from VEGF, another key molecule involved is matrix metalloproteinases which are the enzymes involved in pericellular proteolysis, a process critically important in initiating angiogenesis. But during the later stages, when cell–cell contact formation occurs, MMP expression is downregulated. Regulation of MMPs by cell–cell contact formation was found. This article focuses on a reciprocal relationship between the expression of cell adhesion molecules that modulates cell–cell contact formation and MMP expression.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Anand-Apte B, Pepper M, Voest E, Iwata K, Montesano R, Olsen BR (1997) Inhibition of angiogenesis by tissue inhibitors of matrix metalloproteinases-3. Invest Ophthalmol Vis Sci 38:817–823

    PubMed  CAS  Google Scholar 

  • Anastasiadis PZ, Reynolds AB (2000) The p120 catenin family: complex roles in adhesion, signaling and cancer. J Cell Sci 113:1319–1334

    PubMed  CAS  Google Scholar 

  • Bazzoni G, Dejana E (2004) Endothelial cell to cell junctions: molecular organization and role in vascular homeostasis. Physiol Rev 84:869–901

    Article  PubMed  CAS  Google Scholar 

  • Ben-Ze’ev A, Geiger B (1998) Differential molecular interactions of beta-catenin and plakoglobin in adhesion, signaling and cancer. Curr Opin Cell Biol 10:629–639

    Article  PubMed  Google Scholar 

  • Brooks PC, Stromblad S, Sanders LC, von Schalscha TL, Aimes RT, Stetler-Stevenson WG, Quigley JP, Cheresh DA (1996) Localization of matrix metalloproteinase MMP-2 to the surface of invasive cells by interaction with integrin αvβ3. Cell 85:683–693

    Article  PubMed  CAS  Google Scholar 

  • Carmeliet P, Lampugnani MG, Moons L, Breviario F, Lupu F, Herbert JM, Collen D (1999) Dejana E Targeted deficiency or cytosolic truncation of the VE-cadherin gene in mice impairs VEGF-mediated endothelial survival and angiogenesis. Cell 98:147–157

    Article  PubMed  CAS  Google Scholar 

  • Chade AR, Bentley HD, Zhu X, Rodriguez-Porcel M, Niemeyer S, Amores-Arriaga B, Napolic C, Ritman EL, Lerman A, Lerman LO (2004) Antioxidant intervention prevents renal neovascularization in hypercholesterolemic pigs. J Am Soc Nephrol 15:1816–1825

    Article  PubMed  CAS  Google Scholar 

  • Charlesworth PJ, Harres AL (2006) Mechanisms of disease: angiogenesis in urologic malignancies. Nat Clin Pract Urol 3:157–169

    Article  PubMed  CAS  Google Scholar 

  • Corada M, Mariotti M, Thurston G, Smith K, Kunkel R, Brockhaus M, Lampugnani MG, Martin-Padura I, Stoppacciaro A, Ruco L, McDonald DM, Ward PA, Dejana E (1999) Vascular endothelial-cadherin is an important determinant of microvascular integrity in vivo. Proc Natl Acad Sci USA 96:9815–9820

    Article  PubMed  CAS  Google Scholar 

  • Dejana E, Bazzoni G, Lampugnani MG (1999) Vascular endothelial (VE)-cadherin: only an intercellular glue? Exp Cell Res 252:13–19

    Article  PubMed  CAS  Google Scholar 

  • Eliceiri BP, Cheresh DA (1999) The role of alphaV integrins during angiogenesis: insights into potential mechanisms of action and clinical development. J Clin Invest 103:1227–1230

    Article  PubMed  CAS  Google Scholar 

  • Fisher C, Gilbertsonbeadling S, Powers EA, Petzold G, Poorman R, Mitchell MA (1994) Interstitial collagenase is required for angiogenesis in vitro. Dev Biol 162:499–510

    Article  PubMed  CAS  Google Scholar 

  • Folkman J (1997) Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat Med 1:27–31

    Article  Google Scholar 

  • Gingras D, Bousquet-Gagnon N, Langois S, Lachambre MP, Annabi B, Beliveau R (2001) Activation of the extracellular signal regulated protein kinase (ERK) cascade by membrane type-1matrix metalloproteinase (MT1-MMP). FEBS Lett 507:231–236

    Article  PubMed  CAS  Google Scholar 

  • Hanahan D, Folkman J (1996) Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 86:353–364

    Article  PubMed  CAS  Google Scholar 

  • Hass TL, Davis SJ, Madri JA (1998) Three-dimensional type I collagen lattices induce co ordinate expression of matrix metalloproteinases MT1 MMP and MMP-2 in microvascular endothelial cells. J Biol Chem 273:3604–3610

    Article  Google Scholar 

  • Henriet P, Blavier L, Declerck YA (1999) Tissue inhibitors of matrix metalloproteinases in invasion and proliferation. APMIS 107:111–119

    Article  PubMed  CAS  Google Scholar 

  • Hermann J, Lerman LO, Mukhopadhyay D, Napoli C, Lerman A (2006) Angiogenesis in atherogenesis. Thromb Vasc Biol 26:1948–1957

    Article  Google Scholar 

  • Itoh T, Tanioka M, Yoshida H, Yoshioka T, Nishimoto H, Itohara S (1998) Reduced angiogenesis and tumor progression in gelatinase A deficient mice. Cancer Res 58:1048–1051

    PubMed  CAS  Google Scholar 

  • Kiran MS, Sameer Kumar VB, Viji RI, Sudhakaran PR (2006) Temporal relationship between MMP production and angiogenic process in HUVECs. Cell Biol Inter 30:704–713

    Article  CAS  Google Scholar 

  • Kiran MS, Viji RI, Kumar VB, Sudhakaran PR (2008a) Modulation of angiogenic factors by ursolic acid. Biochem Biophys Res Commun 371:556–560

    Article  PubMed  CAS  Google Scholar 

  • Kiran MS, Kumar VB, Viji RI, Sherin GT, Rajasekharan KN, Sudhakaran PR (2008b) Opposing effects of curcuminoids on serum stimulated and unstimulated angiogenic response. J Cell Physiol 215:251–264

    Article  PubMed  CAS  Google Scholar 

  • Kiran MS, Viji RI, Kumar VB, Athira AP, Sudhakaran PR (2011) Changes in expression of VE-cadherin and MMPs in endothelial cells: Implications for angiogenesis. Vascular Cell 3:6

    Article  PubMed  CAS  Google Scholar 

  • Koch AE, Halloran MM, Haskell CJ (1995) Angiogenesis mediated by soluble form of E selectin and vascular cell adhesion molecule 1. Nature 376:517–519

    Article  PubMed  CAS  Google Scholar 

  • Lampugnani MG, Dejana E (1997) Interendothelial junctions: structure, signaling and functional roles. Curr Opin Cell Biol 9:674–682

    Article  PubMed  CAS  Google Scholar 

  • Lampugnani MG, Resnati M, Raiteri M, Pigott R, Pisacane A, Houen G, Ruco LP, Dejana E (1992) A novel endothelial-specific membrane protein is a marker of cell-cell contacts. J Cell Biol 118:1511–1522

    Article  PubMed  CAS  Google Scholar 

  • Liao F, Li Y, O'Connor W, Zanetta L, Bassi R, Santiago A, Overholser J, Hooper A, Mignatti P, Dejana E, Hicklin DJ, Bohlen P (2000) Monoclonal antibody to vascular endothelial (VE)-cadherin is a potent inhibitor of angiogenesis, tumor growth, and metastasis. Cancer Res 60:6805–6810

    PubMed  CAS  Google Scholar 

  • Lip GY, Blann AD (2004) Thrombogenesis, atherosclerosis, angiogenesis in vascular disease: a new “Vascular triad”. Ann Med 36:119–125

    Article  PubMed  CAS  Google Scholar 

  • Maekawa R, Maki H, Yoshida H, Hojo K, Tanaka H, Wada T (1999) Correlation of anti angiogenic and anti tumor efficacy of N-biphenylsulfonyl phenylalanine hydroxamic acid (BPHA), an orally active, selective matrix metalloproteinase inhibitor. Cancer Res 59:1231–1235

    PubMed  CAS  Google Scholar 

  • Montesano R, Orci L (1985) Tumor promoting phorbol esters induced angiogenesis in vitro. Cell 42:469–477

    Article  PubMed  CAS  Google Scholar 

  • Moses MA (1997) The regulation of neovascularization by matrix metalloproteinases and their inhibitors. Stem Cells 15:180–189

    Article  PubMed  CAS  Google Scholar 

  • Moses MA, Sudhalter J, Langer R (1990) Identification of inhibitor of neovascularization from cartilage. Science 248:1408–1410

    Article  PubMed  CAS  Google Scholar 

  • Muller WA, Gimbrone MA (1986) Plasmalemmal proteins of cultured vascular endothelial cells exhibit apical-basal polarity: analysis by surface-selective iodination. J Cell Biol 103:2389–2402

    Article  PubMed  CAS  Google Scholar 

  • Munshi HG, Stack MS (2006) Reciprocal interactions between adhesion receptor signaling and MMP regulation. Cancer Metastasis Rev 25:45–56

    Article  PubMed  CAS  Google Scholar 

  • Naglich JG, Jure-Kunkel M, Gupta E, Fargnoli J, Henderson AJ, Lewin AC, Talbott R, Baxter A, Bird J, Savopoulos R, Wills R, Kramer RA, Trail PA (2001) Inhibition of angiogenesis and metastasis in two murine models by the matrix metalloproteinase inhibitor. Cancer Res 61:8480–8485

    PubMed  CAS  Google Scholar 

  • Nguyen M, Strubel NA, Bischoff J (1993) A role of sialyl Lewis X/A glycoconjugates in capillary morphogenesis. Nature 365:267–269

    Article  PubMed  CAS  Google Scholar 

  • Overall CM, Lopez-Otin C (2002) Strategies for MMP inhibition in cancer: innovations for the post-trial era. Nat Rev Cancer 2:657–672

    Article  PubMed  CAS  Google Scholar 

  • Pece S, Chiariello M, Murga C, Gutkind J (1999) Activation of the protein kinase Akt/PKB by the formation of E-cadherin-mediated cell-cell junctions. Evidence for the association of phosphatidylinositol 3-kinase with the E-cadherin adhesion complex. J Biol Chem 274:19347–19351

    Article  PubMed  CAS  Google Scholar 

  • Pece S, Gutkind JS (2000) Signaling from E-cadherin to MAPK pathway by the recruitment and activation of epidermal growth factor receptors upon cell-cell contact formation. J Biol Chem 275:41227–41233

    Article  PubMed  CAS  Google Scholar 

  • Qian X, Wang TN, Rothman VL, Nicosia RF, Tuszynski GP (1997) Thrombospondin-1 modulates angiogenesis in vitro by up regulation of matrix metalloproteinase-9 in endothelial cells. Exp Cell Res 235:403–412

    Article  PubMed  CAS  Google Scholar 

  • Risau W (1997) Mechanisms of angiogenesis. Nature 386:671–674

    Article  PubMed  CAS  Google Scholar 

  • Schnaper HW, Grant DS, Stetler Stevenson WG, Fridman R, D’Orazi G, Murphy AN (1993) Type IV collagenase(s) and TIMPs modulate endothelial cell morphogenesis in vitro. J Cell Physiol 156:235–246

    Article  PubMed  CAS  Google Scholar 

  • Schwartz SM, Haudenschild CC, Eddy EM (1978) Endothelial regeneration. Quantitative analysis of initial stages of endothelial regeneration in rat aortic intima. Lab Invest 38:568–580

    PubMed  CAS  Google Scholar 

  • Seiki M, Naohiko Koshikawa, Ikuo Yana (2003) Role of pericellular proteolysis by membrane-type 1 matrix metalloproteinase in cancer invasion and angiogenesis. Cancer Metastasis Rev 22:129–143

    Article  PubMed  CAS  Google Scholar 

  • Sholley MM, Gimbrone MA, Cotran RS (1977) Cellular migration and replication in endothelial regeneration: a study using irradiated endothelial cultures. Lab Invest 36:18–25

    PubMed  CAS  Google Scholar 

  • Shweiki D, Itin A, Soffer D, Keshet E (1992) Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature 359:843–845

    Article  PubMed  CAS  Google Scholar 

  • Simionescu M, Simionescu N (1991) Endothelial transport of macromolecules: transcytosis and endocytosis. A look from cell biology. Cell Biol Rev 25:1–78

    PubMed  CAS  Google Scholar 

  • Victor WM, van Hinsbergh MA, Engelse PHA (2006) Pericellular proteases in angiogenesis and vasculogenesis. Arter Thromb Vasc Biol 26:716–720

    Article  Google Scholar 

  • Visse R, Nagase H (2003) Matrix metalloproteinases and tissue inhibitors of metalloproteinases: structure, function, and biochemistry. Circ Res 92(8):827–839

    Article  PubMed  CAS  Google Scholar 

  • Vu TH, Shipley JM, Bergers G, Berger JE, Helms JA, Hanahan D et al (1998) MMP-9/gelatinase B is a key regulator of growth plate angiogenesis and apoptosis of hypertrophic chondrocytes. Cell 93:411–422

    Article  PubMed  CAS  Google Scholar 

  • Woessner JF (1991) Matrix metalloproteinases and their inhibitors in connective tissue remodeling. FASEB J 5:2145–2154

    PubMed  CAS  Google Scholar 

  • Xu Y, Guo DF, Davidson M, Inagami T, Carpenter G (1997) Interaction of the adaptor protein Shc and the adhesion molecule cadherin. J Biol Chem 272:13463–13466

    Article  PubMed  CAS  Google Scholar 

  • Yan L, Moses MA, Huang S, Ingber DE (2000) Adhesion dependent control of matrix metalloproteinases-2 activation in human capillary endothelial cells. J Cell Sci 113:3979–3987

    PubMed  CAS  Google Scholar 

  • Yang S, Graham J, Kahn JW, Schwartz EA, Gerritsen ME (1999) Functional roles for PECAM-1 (CD31) and VE-cadherin (CD144) in tube assembly and lumen formation in three-dimensional collagen gels. Am J Pathol 155:887–895

    Article  PubMed  CAS  Google Scholar 

  • Yu Q, Stamenkovic I (1999) Localization of matrix metalloproteinase 9 to the cell surface provides a mechanism for CD44-mediated tumor invasion. Genes Dev 13:35–48

    Article  PubMed  CAS  Google Scholar 

  • Zondag GC, Reynolds AB, Moolenaar WH (2000) Receptor protein-tyrosine phosphatase RPTPmu binds to, and dephosphorylates the catenin p120(ctn). J Biol Chem 275:11264–11269

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Financial assistance received from CSIR, New Delhi (MSK), and (KSCSTE), Trivandrum (AAP) is gratefully acknowledged.

Author information

Authors and Affiliations

  1. Department of Biochemistry, University of Kerala, Kariavattom, Thiruvananthapuram, 695 581, Kerala, India

    A. P. Athira & M. S. Kiran

  2. Biomaterials Division, Central Leather Research Institute, Adyar, Chennai, 600 020, Tamil Nadu, India

    M. S. Kiran

  3. Computational Biology & Bioinformatics, University of Kerala, Kariavattom, Thiruvananthapuram, 695 581, Kerala, India

    P. R. Sudhakaran

Authors
  1. A. P. Athira
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. S. Kiran
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. P. R. Sudhakaran
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to P. R. Sudhakaran .

Editor information

Editors and Affiliations

  1. Computational Biology & Bioinformatics, University of Kerala, Kariavattom, Trivandrum, Kerala, India

    Perumana R. Sudhakaran

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer India

About this paper

Cite this paper

Athira, A.P., Kiran, M.S., Sudhakaran, P.R. (2014). Reciprocal Relationship Between VE-Cadherin and Matrix Metalloproteinases Expression in Endothelial Cells and Its Implications to Angiogenesis. In: R. Sudhakaran, P. (eds) Perspectives in Cancer Prevention-Translational Cancer Research. Springer, New Delhi. https://doi.org/10.1007/978-81-322-1533-2_9

Download citation

Publish with us

Policies and ethics

Search

Navigation