HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS		QUICK SEARCH:   [advanced] Author: Keyword(s): Year:  Vol:  Page:

J. Biol. Chem., Vol. 279, Issue 50, 52132-52140, December 10, 2004

This Article Full Text Full Text (PDF) All Versions of this Article: 279/50/52132    most recent M409617200v1 Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Labrecque, L. Articles by Béliveau, R. Search for Related Content PubMed PubMed Citation Articles by Labrecque, L. Articles by Béliveau, R. Social Bookmarking                      What's this?

Src-mediated Tyrosine Phosphorylation of Caveolin-1 Induces Its Association with Membrane Type 1 Matrix Metalloproteinase^*

Lyne Labrecque, Carine Nyalendo, Stéphanie Langlois, Yves Durocher, Christian Roghi¶, Gillian Murphy¶, Denis Gingras, and Richard Béliveau||

From the Laboratoire de Médecine Moléculaire, Hôpital Ste-Justine-Université du Québec à Montréal, Centre de Cancérologie Charles-Bruneau, 3175 Chemin Côte-Ste-Catherine, Montréal, Québec H3T 1C5, Animal Cell Technology Group, Montréal, Quebec H4P2R2, Canada, and the ^¶Department of Oncology, Cambridge Institute for Medical Research, Hills Road, Cambridge CB2 2XY, United Kingdom

We have recently shown that stimulation of endothelial cells with vascular endothelial growth factor (VEGF) induces dissociation of caveolin-1 from the VEGFR-2 receptor, followed by Src family kinase-dependent tyrosine phosphorylation of the protein (Labrecque, L., Royal, I., Surprenant, D. S., Patterson, C., Gingras, D., and Béliveau, R. (2003) Mol. Biol. Cell 14, 334–347). In this study, we provide evidence that the VEGF-dependent tyrosine phosphorylation of caveolin-1 induces interaction of the protein with the membrane-type 1 matrix metalloproteinase (MT1-MMP). This interaction requires the phosphorylation of caveolin-1 on tyrosine 14 by members of the Src family of protein kinases, such as Src and Fyn, because it is completely abolished by expression of a catalytically inactive Src mutant or by site-directed mutagenesis of tyrosine 14 of caveolin-1. Most interestingly, the association of MT1-MMP with phosphorylated caveolin-1 induced the recruitment of Src and a concomitant inhibition of the kinase activity of the enzyme, suggesting that this complex may be involved in the negative regulation of Src activity. The association of MT1-MMP with phosphorylated caveolin-1 occurs in caveolae membranes and involves the cytoplasmic domain of MT1-MMP because it was markedly reduced by mutation of Cys⁵⁷⁴ and Val⁵⁸² residues of the cytoplasmic tail of the enzyme. Most interestingly, the reduction of the interaction between MT1-MMP and caveolin-1 by using these mutants also decreases MT1-MMP-dependent cell locomotion. Overall these results indicate that MT1-MMP associates with tyrosine-phosphorylated caveolin-1 and that this complex may play an important role in MT1-MMP regulation and function.

Received for publication, August 20, 2004 , and in revised form, September 28, 2004.

^* This supported by a grant from the Canadian Institutes for Health Research (to R. B.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

This paper is dedicated to the memory of Dr. Francine Denizeau, whose gentleness, determination, and extraordinary passion for all aspects of biological sciences will always be remembered.

^|| To whom correspondence should be addressed: Laboratoire de Médecine Moléculaire, Centre de Cancérologie Charles-Bruneau, Hôpital Ste-Justine, 3175 Côte Ste-Catherine, Montréal, Québec H3T 1C5, Canada. Tel.: 514-3454931 (ext. 2366); Fax: 514-345-2359; E-mail: molmed{at}justine.umontreal.ca.

CiteULike    Complore    Connotea    Del.icio.us    Digg    Reddit    Technorati    What's this?

This article has been cited by other articles:

				R. Chang, L. G. Chicoine, H. Cui, N. L. Kanagy, B. R. Walker, Y. Liu, B. K. English, and L. D. Nelin Cytokine-induced arginase activity in pulmonary endothelial cells is dependent on Src family tyrosine kinase activity Am J Physiol Lung Cell Mol Physiol, October 1, 2008; 295(4): L688 - L697. [Abstract] [Full Text] [PDF]

				T. R. Lizarbe, C. Garcia-Rama, C. Tarin, M. Saura, E. Calvo, J. A. Lopez, C. Lopez-Otin, A. R. Folgueras, S. Lamas, and C. Zaragoza Nitric oxide elicits functional MMP-13 protein-tyrosine nitration during wound repair FASEB J, September 1, 2008; 22(9): 3207 - 3215. [Abstract] [Full Text] [PDF]

				C. Nyalendo, E. Beaulieu, H. Sartelet, M. Michaud, N. Fontaine, D. Gingras, and R. Beliveau Impaired tyrosine phosphorylation of membrane type 1-matrix metalloproteinase reduces tumor cell proliferation in three-dimensional matrices and abrogates tumor growth in mice Carcinogenesis, August 1, 2008; 29(8): 1655 - 1664. [Abstract] [Full Text] [PDF]

				X.-Y. Li, I. Ota, I. Yana, F. Sabeh, and S. J. Weiss Molecular Dissection of the Structural Machinery Underlying the Tissue-invasive Activity of Membrane Type-1 Matrix Metalloproteinase Mol. Biol. Cell, August 1, 2008; 19(8): 3221 - 3233. [Abstract] [Full Text] [PDF]

				M. Ouyang, S. Lu, X.-Y. Li, J. Xu, J. Seong, B. N. G. Giepmans, J. Y.-J. Shyy, S. J. Weiss, and Y. Wang Visualization of Polarized Membrane Type 1 Matrix Metalloproteinase Activity in Live Cells by Fluorescence Resonance Energy Transfer Imaging J. Biol. Chem., June 20, 2008; 283(25): 17740 - 17748. [Abstract] [Full Text] [PDF]

				S. D'Alessio, G. Ferrari, K. Cinnante, W. Scheerer, A. C. Galloway, D. F. Roses, D. V. Rozanov, A. G. Remacle, E.-S. Oh, S. A. Shiryaev, et al. Tissue Inhibitor of Metalloproteinases-2 Binding to Membrane-type 1 Matrix Metalloproteinase Induces MAPK Activation and Cell Growth by a Non-proteolytic Mechanism J. Biol. Chem., January 4, 2008; 283(1): 87 - 99. [Abstract] [Full Text] [PDF]

				T. Takino, H. Saeki, H. Miyamori, T. Kudo, and H. Sato Inhibition of Membrane-Type 1 Matrix Metalloproteinase at Cell-Matrix Adhesions Cancer Res., December 15, 2007; 67(24): 11621 - 11629. [Abstract] [Full Text] [PDF]

				S. Langlois, C. Nyalendo, G. Di Tomasso, L. Labrecque, C. Roghi, G. Murphy, D. Gingras, and R. Beliveau Membrane-Type 1 Matrix Metalloproteinase Stimulates Cell Migration through Epidermal Growth Factor Receptor Transactivation Mol. Cancer Res., June 1, 2007; 5(6): 569 - 583. [Abstract] [Full Text] [PDF]

				C. Nyalendo, M. Michaud, E. Beaulieu, C. Roghi, G. Murphy, D. Gingras, and R. Beliveau Src-dependent Phosphorylation of Membrane Type I Matrix Metalloproteinase on Cytoplasmic Tyrosine 573: ROLE IN ENDOTHELIAL AND TUMOR CELL MIGRATION J. Biol. Chem., May 25, 2007; 282(21): 15690 - 15699. [Abstract] [Full Text] [PDF]

				J. Nie, J. Pei, M. Blumenthal, and D. Pei Complete Restoration of Cell Surface Activity of Transmembrane-truncated MT1-MMP by a Glycosylphosphatidylinositol Anchor: IMPLICATIONS FOR MT1-MMP-MEDIATED PROMMP2 ACTIVATION AND COLLAGENOLYSIS IN THREE-DIMENSIONS J. Biol. Chem., March 2, 2007; 282(9): 6438 - 6443. [Abstract] [Full Text] [PDF]

				A. N. Shajahan, A. Wang, M. Decker, R. D. Minshall, M. C. Liu, and R. Clarke Caveolin-1 Tyrosine Phosphorylation Enhances Paclitaxel-mediated Cytotoxicity J. Biol. Chem., February 23, 2007; 282(8): 5934 - 5943. [Abstract] [Full Text] [PDF]

				F. Peng, D. Wu, A. J. Ingram, B. Zhang, B. Gao, and J. C. Krepinsky RhoA Activation in Mesangial Cells by Mechanical Strain Depends on Caveolae and Caveolin-1 Interaction J. Am. Soc. Nephrol., January 1, 2007; 18(1): 189 - 198. [Abstract] [Full Text] [PDF]

				E. Ispanovic and T. L. Haas JNK and PI3K differentially regulate MMP-2 and MT1-MMP mRNA and protein in response to actin cytoskeleton reorganization in endothelial cells Am J Physiol Cell Physiol, October 1, 2006; 291(4): C579 - C588. [Abstract] [Full Text] [PDF]

				L. Orlichenko, B. Huang, E. Krueger, and M. A. McNiven Epithelial Growth Factor-induced Phosphorylation of Caveolin 1 at Tyrosine 14 Stimulates Caveolae Formation in Epithelial Cells J. Biol. Chem., February 24, 2006; 281(8): 4570 - 4579. [Abstract] [Full Text] [PDF]

				D. Mehta and A. B. Malik Signaling Mechanisms Regulating Endothelial Permeability Physiol Rev, January 1, 2006; 86(1): 279 - 367. [Abstract] [Full Text] [PDF]

				R. Veluthakal, I. Chvyrkova, M. Tannous, P. McDonald, R. Amin, T. Hadden, D. C. Thurmond, M. J. Quon, and A. Kowluru Essential Role for Membrane Lipid Rafts in Interleukin-1{beta}-Induced Nitric Oxide Release From Insulin-Secreting Cells: Potential Regulation by Caveolin-1+ Diabetes, September 1, 2005; 54(9): 2576 - 2585. [Abstract] [Full Text] [PDF]

				V. S. Golubkov, S. Boyd, A. Y. Savinov, A. V. Chekanov, A. L. Osterman, A. Remacle, D. V. Rozanov, S. J. Doxsey, and A. Y. Strongin Membrane Type-1 Matrix Metalloproteinase (MT1-MMP) Exhibits an Important Intracellular Cleavage Function and Causes Chromosome Instability J. Biol. Chem., July 1, 2005; 280(26): 25079 - 25086. [Abstract] [Full Text] [PDF]

				K. Lehti, E. Allen, H. Birkedal-Hansen, K. Holmbeck, Y. Miyake, T.-H. Chun, and S. J. Weiss An MT1-MMP-PDGF receptor-{beta} axis regulates mural cell investment of the microvasculature Genes & Dev., April 15, 2005; 19(8): 979 - 991. [Abstract] [Full Text] [PDF]