Cancer Cell Biology

You have full text access to this OnlineOpen article

The YSNSG cyclopeptide derived from tumstatin inhibits tumor angiogenesis by down-regulating endothelial cell migration

  1. Jessica Thevenard1,
  2. Laurent Ramont1,
  3. Jérome Devy1,
  4. Bertrand Brassart1,
  5. Aurélie Dupont-Deshorgue1,
  6. Nicolas Floquet1,†,
  7. Laurence Schneider1,
  8. Farid Ouchani1,
  9. Christine Terryn2,
  10. François-Xavier Maquart1,
  11. Jean-Claude Monboisse1,
  12. Sylvie Brassart-Pasco1,‡,*

Article first published online: 23 JUN 2009

DOI: 10.1002/ijc.24688

Issue

International Journal of Cancer

International Journal of Cancer

Volume 126, Issue 5, pages 1055–1066, 1 March 2010

Additional Information

How to Cite

Thevenard, J., Ramont, L., Devy, J., Brassart, B., Dupont-Deshorgue, A., Floquet, N., Schneider, L., Ouchani, F., Terryn, C., Maquart, F.-X., Monboisse, J.-C. and Brassart-Pasco, S. (2010), The YSNSG cyclopeptide derived from tumstatin inhibits tumor angiogenesis by down-regulating endothelial cell migration. Int. J. Cancer, 126: 1055–1066. doi: 10.1002/ijc.24688

Author Information

  1. 1

    CNRS UMR 6237, Université de Reims Champagne-Ardenne, CHU de Reims, Reims, France

  2. 2

    IFR 53, Plateforme Imagerie Cellulaire et Tissulaire, Université de Reims Champagne-Ardenne, Reims, France

  1. †

    Institut des BioMolécules Max Mousseron, CNRS UMR 5247, Université de Montpellier, Montpellier, France

  1. ‡

    Fax: 33-32-691-8055

*Laboratoire de Biochimie Médicale et de Biologie Moléculaire CNRS UMR 6237, U.F.R. Médecine, 51 Rue Cognacq Jay, REIMS Cedex 51095, France

Publication History

  1. Issue published online: 27 DEC 2009
  2. Article first published online: 23 JUN 2009
  3. Accepted manuscript online: 23 JUN 2009 12:00AM EST
  4. Manuscript Accepted: 12 JUN 2009
  5. Manuscript Received: 11 AUG 2008

Funded by

  • Centre National de la Recherche Scientifique. Grant Number: (UMR 6237)
  • University of Reims Champagne-Ardenne
  • Association pour la Recherche sur le Cancer
  • Ligue Nationale Contre le Cancer (Comités de l'Aisne et de la Haute-Marne)
  • Canceropole Grand Est (ACI 2004, InCa)

SEARCH

SEARCH BY CITATION

ARTICLE TOOLS

View Full Article (HTML) Get PDF (894K)

References

  • 1
    Folkman J. Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat Med 1995; 1: 27–31.
  • 2
    Carmeliet P. Angiogenesis in health and disease. Nat Med 2003; 9: 653–60.
  • 3
    Gálvez BG, Matías-Román S, Albar JP, Sánchez-Madrid F, Arroyo AG. Membrane type 1-matrix metalloproteinase is activated during migration of human endothelial cells and modulates endothelial motility and matrix remodeling. J Biol Chem 2001; 276: 37491–500.
  • 4
    Bacharach E, Itin A, Keshet E. 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; 89: 10686–90.
  • 5
    Pepper MS, Sappino AP, Stöcklin R, Montesano R, Orci L, Vassali JD. Upregulation of urokinase receptor expression on migrating endothelial cells. J Cell Biol 1993; 122: 673–684.
  • 6
    Ragno P. The urokinase receptor: a ligand or a receptor? Story of a sociable molecule. Cell Mol Life Sci 2006; 63: 1028–37.
  • 7
    Chapman HA, Wei Y, Simon DI, Waltz DA. Role of urokinase receptor and caveolin in regulation of integrin signalling. Thromb Haemost 1999; 82: 291–7.
  • 8
    Ortega N, Werb Z. New functional roles for non-collagenous domains of basement membrane collagens. J Cell Sci 2002; 115: 4201–14.
  • 9
    Maeshima Y, Manfredi M, Reimer C, Holthaus KA, Hopfer H, Chandamuri BR, Kharbanda S, Kalluri R. Identification of the antiangiogenic site within vascular basement membrane-derived tumstatin. J Biol Chem 2001; 276: 15240–8.
  • 10
    Shahan TA, Ziaie Z, Pasco S, Fawzi A, Bellon G, Monboisse JC, Kefalides NA. Identification of CD47/integrin-associated protein and alpha(v)beta3 as two receptors for the alpha3(IV) chain of type IV collagen on tumor cells. Cancer Res 1999; 59: 4584–90.
  • 11
    Pasco S, Ramont L, Maquart FX, Monboisse JC. Control of melanoma progression by various matrikines from basement membrane macromolecules. Crit Rev Oncol Hematol 2004; 49: 221–33.
  • 12
    Miyoshi T, Hirohata S, Ogawa H, Doi M, Obika M, Yonezawa T, Sado Y, Kusachi S, Kyo S, Kondo S, Shiratori Y, Hudson BG, et al. Tumor-specific expression of the RGD-alpha3(IV)NC1 domain suppresses endothelial tube formation and tumor growth in mice. FASEB J 2006; 20: 1904–6.
  • 13
    Pasco S, Han J, Gillery P, Bellon G, Maquart FX, Borel JP, Kefalides NA, Monboisse JC. A specific sequence of the noncollagenous domain of the alpha3(IV) chain of type IV collagen inhibits expression and activation of matrix metalloproteinases by tumor cells. Cancer Res 2000; 60: 467–73.
  • 14
    Pasco S, Ramont L, Venteo L, Pluot M, Maquart FX, Monboisse JC. In vivo overexpression of tumstatin domains by tumor cells inhibits their invasive properties in a mouse melanoma model. Exp Cell Res 2004; 301: 251–65.
  • 15
    Floquet N, Pasco S, Ramont L, Derreumaux P, Laronze JY, Nuzillard JM, Maquart FX, Alix AJ, Monboisse JC. The antitumor properties of the alpha3(IV)-(185–203) peptide from the NC1 domain of type IV collagen (tumstatin) are conformation-dependent. J Biol Chem 2004; 279: 2091–100.
  • 16
    Thevenard J, Floquet N, Ramont L, Prost E, Nuzillard JM, Dauchez M, Yezid H, Alix AJ, Maquart FX, Monboisse JC, Brassart-Pasco S. Structural and antitumor properties of the YSNSG cyclopeptide derived from tumstatin. Chem Biol 2006; 13: 1307–15.
  • 17
    Wald M, Olejar T, Sebkova V, Zadinova M, Boubelik M, Pouckova P. Mixture of trypsin, chymotrypsin, and papain reduces formation of metastases and extends survival time of C57Bl6 mice with syngenic melanoma B16. Cancer Chemother Pharmacol 2001; 47: 16–22.
  • 18
    Abramoff MD, Magelhaes PJ. Image processing with ImageJ. Biophotonics Int 2004; 11: 36–42.
  • 19
    Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976; 72: 248–54.
  • 20
    Heussen C, Dowdle EB. Electrophoretic analysis of plasminogen activators in polyacrylamide gels containing sodium dodecyl sulfate and copolymerized substrates. Anal Biochem 1980; 102: 196–202.
  • 21
    Friberger P, Knös M, Gustavsson S, Aurell L, Claeson G. Methods for determination of plasmin, antiplasmin and plasminogen by means of substrate S-2251. Haemostasis 1978; 7: 138–45.
  • 22
    Auge F, Hornebeck W, Decarme M, Laronze JY. Improved gelatinase a selectivity by novel zinc binding groups containing galardin derivatives. Bioorg Med Chem Lett 2003; 13: 1783–6.
  • 23
    Lottenberg R, Sjak-Shie N, Fazleabas AT, Roberts RM. Aprotinin inhibits urokinase but not tissue-type plasminogen activator. Thromb Res 1988; 49: 549–56.
  • 24
    Robinet A, Fahem A, Cauchard JH, Huet E, Vincent L, Lorimier S, Antonicelli F, Soria C, Crepin M, Hornebeck W, Bellon G. Elastin-derived peptides enhance angiogenesis by promoting endothelial cell migration and tubulogenesis through upregulation of MT1-MMP. J Cell Sci 2005; 118: 343–56.
  • 25
    Mazzone M, Baldassarre M, Beznoussenko G, Giacchetti G, Cao J, Zucker S, Luini A, Buccione R. Intracellular processing and activation of membrane type 1 matrix metalloprotease depends on its partitioning into lipid domains. J Cell Sci 2004; 117: 6275–87.
  • 26
    D'ortho MP, Stanton H, Butler M, Atkinson SJ, Murphy G, Hembry RM. MT1-MMP on the cell surface causes focal degradation of gelatin films. FEBS Lett 1998; 421: 159–64.
  • 27
    Ohuchi E, Imai K, Fujii Y, Sato H, Seiki M, Okada Y. Membrane type 1 matrix metalloproteinase digests interstitial collagens and other extracellular matrix macromolecules. J Biol Chem 1997; 272: 2446–51.
  • 28
    Hiraoka N, Allen E, Apel IJ, Gyetko MR, Weiss SJ. Matrix metalloproteinases regulate neovascularization by acting as pericellular fibrinolysins. Cell 1998; 95: 365–77.
  • 29
    Koshikawa N, Giannelli G, Cirulli V, Miyazaki K, Quaranta V. Role of cell surface metalloprotease MT1-MMP in epithelial cell migration over laminin-5. J Cell Biol 2000; 148: 615–24.
  • 30
    Li Y, Aoki T, Mori Y, Ahmad M, Miyamori H, Takino T, Sato H. Cleavage of lumican by membrane-type matrix metalloproteinase-1 abrogates this proteoglycan-mediated suppression of tumor cell colony formation in soft agar. Cancer Res 2004; 64: 7058–64.
  • 31
    Slack JK, Adams RB, Rovin JD, Bissonette EA, Stoker CE, Parsons JT. Alterations in the focal adhesion kinase/Src signal transduction pathway correlate with increased migratory capacity of prostate carcinoma cells. Oncogene 2001; 20: 1152–63.
  • 32
    Nyberg P, Xie L, Kalluri R. Endogenous inhibitors of angiogenesis. Cancer RES 2005; 65: 3967–3979.
  • 33
    Hamano Y, Kalluri R. Tumstatin, the NC1 domain of alpha3 chain of type IV collagen, is an endogenous inhibitor of pathological angiogenesis and suppresses tumor growth. Biochem Biophys Res Commun 2005; 333: 292–8.
  • 34
    Tabruyn SP, Griffioen AW. Molecular pathways of angiogenesis inhibition. Biochem Biophys Res Commun 2007; 355: 1–5.
  • 35
    Collen A, Hanemaaijer R, Lupu F, Quax PH, Van Lent N, Grimbergen J, Peters E, Koolwijk P, Van Hinsbergh VW. Membrane-type matrix metalloproteinase-mediated angiogenesis in a fibrin-collagen matrix. Blood 2003; 101: 1810–7.
  • 36
    Genis L, Galvez BG, Gonzalo P, Arroyo AG. MT1-MMP: universal or particular player in angiogenesis? Cancer Metastasis Rev 2006; 25: 77–86.
  • 37
    Langlois S, Nyalendo C, Di Tomasso G, Labrecque L, Roghi C, Murphy G, Gingras D, Béliveau R. Membrane-type 1 matrix metalloproteinase stimulates cell migration through epidermal growth factor receptor transactivation. Mol Cancer Res 2007; 5: 569–83.
  • 38
    Remacle A, Murphy G, Roghi C. Membrane type I-matrix metalloproteinase (MT1-MMP) is internalised by two different pathways and is recycled to the cell surface. J Cell Sci 2003; 116: 3905–16.
  • 39
    Pepper MS, Montesano R, Mandriota SJ, Orci L, Vassalli JD. Angiogenesis: a paradigm for balanced extracellular proteolysis during cell migration and morphogenesis. Enzyme Protein 1996; 49: 138–62.
  • 40
    Van Hinsbergh VW, Koolwijk P, Hanemaaijer R. Role of fibrin and plasminogen activators in repair-associated angiogenesis: in vitro studies with human endothelial cells. EXS 1997; 79: 391–411.
  • 41
    Heymans S, Luttun A, Nuyens D, Theilmeier G, Creemers E, Moons L, Dyspersin GD, Cleutjens JP, Shipley M, Angellilo A, Levi M, Nübe O, et al. Inhibition of plasminogen activators or matrix metalloproteinases prevents cardiac rupture but impairs therapeutic angiogenesis and causes cardiac failure. Nat Med 1999; 5: 1135–42.
  • 42
    Gutierrez LS, Schulman A, Brito-Robinson T, Noria F, Ploplis VA, Castellino FJ. Tumor development is retarded in mice lacking the gene for urokinase-type plasminogen activator or its inhibitor, plasminogen activator inhibitor-1. Cancer Res 2000; 60: 5839–47.
  • 43
    Mazar AP, Henkin J, Goldfarb RH. The urokinase plasminogen activator system in cancer: implications for tumor angiogenesis and metastasis. Angiogenesis 1999; 3: 15–32.
  • 44
    Blasi F, Carmeliet P. uPAR: a versatile signalling orchestrator. Nat Rev Mol Cell Biol 2002; 3: 932–43.
  • 45
    Tang H, Kerins DM, Hao Q, Inagami T, Vaughan DE. The urokinase-type plasminogen activator receptor mediates tyrosine phosphorylation of focal adhesion proteins and activation of mitogen-activated protein kinase in cultured endothelial cells. J Biol Chem 1998; 273: 18268–72.
  • 46
    Ossowski L, Aguirre-Ghiso JA. Urokinase receptor and integrin partnership: coordination of signalling for cell adhesion, migration and growth. Curr Opin Cell Biol 2000; 12: 613–20.
  • 47
    Wei Y, Eble JA, Wang Z, Kreidberg JA, Chapman HA. Urokinase receptors promote beta1 integrin function through interactions with integrin alpha3beta1. Mol Biol Cell 2001; 12: 2975–86.
  • 48
    Min HY, Doyle LV, Vitt CR, Zandonella CL, Stratton-Thomas JR, Shuman MA, Rosenberg S. Urokinase receptor antagonists inhibit angiogenesis and primary tumor growth in syngeneic mice. Cancer Res 1996; 56: 2428–33.
  • 49
    Li H, Lu H, Griscelli F, Opolon P, Sun LQ, Ragot T, Legrand Y, Belin D, Soria J, Soria C, Perricaudet M, Yeh P. Adenovirus-mediated delivery of a uPA/uPAR antagonist suppresses angiogenesis-dependent tumor growth and dissemination in mice. Gene Ther 1998; 5: 1105–13.
View Full Article (HTML) Get PDF (894K)