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J. Cell Biol. 153 (5): 893-904

Copyright © 2001 by the Rockefeller University Press.

Original Article

Membrane-Type 1 Matrix Metalloproteinase Cleaves Cd44 and Promotes Cell Migration

Masahiro Kajitaa, Yoshifumi Itoha, Tadashige Chibaa, Hidetoshi Moria, Akiko Okadaa, Hiroaki Kinoha, , and Motoharu Seikia

a Department of Cancer Cell Research, Institute of Medical Science, The University of Tokyo, Minato-ku, Tokyo 108-8639, Japan
Department of Cancer Cell Research, Institute of Medical Science, University of Tokyo, 4-6-1 Shirokane-dai, Minato-ku, Tokyo 108-8639, Japan.81-3-5449-541481-3-5449-5255

mseiki{at}ims.u-tokyo.ac.jp

Abstract: Migratory cells including invasive tumor cells frequently express CD44, a major receptor for hyaluronan and membrane-type 1 matrix metalloproteinase (MT1-MMP) that degrades extracellular matrix at the pericellular region. In this study, we demonstrate that MT1-MMP acts as a processing enzyme for CD44H, releasing it into the medium as a soluble 70-kD fragment. Furthermore, this processing event stimulates cell motility; however, expression of either CD44H or MT1-MMP alone did not stimulate cell motility. Coexpression of MT1-MMP and mutant CD44H lacking the MT1-MMP–processing site did not result in shedding and did not promote cell migration, suggesting that the processing of CD44H by MT1-MMP is critical in the migratory stimulation. Moreover, expression of the mutant CD44H inhibited the cell migration promoted by CD44H and MT1-MMP in a dominant-negative manner. The pancreatic tumor cell line, MIA PaCa-2, was found to shed the 70-kD CD44H fragment in a MT1-MMP–dependent manner. Expression of the mutant CD44H in the cells as well as MMP inhibitor treatment effectively inhibited the migration, suggesting that MIA PaCa-2 cells indeed use the CD44H and MT1-MMP as migratory devices. These findings revealed a novel interaction of the two molecules that have each been implicated in tumor cell migration and invasion.

Key Words: MT-MMP • metalloproteinase • motility • CD44 • invasion and metastasis

Abbreviations used in this paper: AEBSF, 4-(2-Aminoethyl)-benzenesulfonyl fluoride hydrochloride; E-64, N-[N-(L-3-Trans-carboxirane-2-carbonyl)-L-leucyl]-agmatine; ECM, extracellular matrix; FITC-HA, fluorescein-conjugated HA; GAPDH, glyceraldehyde-3-phosphate dehydrogenase; GFP, green fluorescent protein; HA, hyaluronic acid; MMP, matrix metalloproteinase; MT-MMP, membrane-type MMP; RT-PCR, reverse transcript PCR; sCD44, soluble CD44; TIMP, tissue inhibitor of metalloproteinases.

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Mechanisms of Soluble Cytokine Receptor Generation.
S. J. Levine (2004)
J. Immunol. 173, 5343-5348
   Abstract »    Full Text »    PDF »
CD44 modulates Smad1 activation in the BMP-7 signaling pathway.
R. S. Peterson, R. A. Andhare, K. T. Rousche, W. Knudson, W. Wang, J. B. Grossfield, R. O. Thomas, R. E. Hollingsworth, and C. B. Knudson (2004)
J. Cell Biol. 166, 1081-1091
   Abstract »    Full Text »    PDF »
Induction of membrane-type-1 matrix metalloproteinase by epidermal growthfactor-mediated signaling in gliomas.
T. E. Van Meter, W. C. Broaddus, H. K. Rooprai, G. J. Pilkington, and H. L. Fillmore (2004)
Neuro Oncology 6, 188-199
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Cell-matrix interaction via CD44 is independently regulated by different metalloproteinases activated in response to extracellular Ca2+ influx and PKC activation.
O. Nagano, D. Murakami, D. Hartmann, B. de Strooper, P. Saftig, T. Iwatsubo, M. Nakajima, M. Shinohara, and H. Saya (2004)
J. Cell Biol. 165, 893-902
   Abstract »    Full Text »    PDF »
Membrane associated proteases and their inhibitors in tumour angiogenesis.
A Noel, C Maillard, N Rocks, M Jost, V Chabottaux, N E Sounni, E Maquoi, D Cataldo, and J M Foidart (2004)
J. Clin. Pathol. 57, 577-584
   Abstract »    Full Text »    PDF »
Hyaluronan Cell Surface Binding Is Induced by Type I Collagen and Regulated by Caveolae in Glioma Cells.
B. Annabi, S. Thibeault, R. Moumdjian, and R. Beliveau (2004)
J. Biol. Chem. 279, 21888-21896
   Abstract »    Full Text »    PDF »
Cleavage of Focal Adhesion Kinase in Vascular Smooth Muscle Cells Overexpressing Membrane-Type Matrix Metalloproteinases.
T. Shofuda, K.-i. Shofuda, N. Ferri, R. D. Kenagy, E. W. Raines, and A. W. Clowes (2004)
Arterioscler Thromb Vasc Biol 24, 839-844
   Abstract »    Full Text »
Membrane type 1-matrix metalloproteinase (MT1-MMP) cooperates with sphingosine 1-phosphate to induce endothelial cell migration and morphogenic differentiation.
S. Langlois, D. Gingras, and R. Beliveau (2004)
Blood 103, 3020-3028
   Abstract »    Full Text »    PDF »
Up-regulation of Vascular Endothelial Growth Factor-A by Active Membrane-type 1 Matrix Metalloproteinase through Activation of Src-Tyrosine Kinases.
N. E. Sounni, C. Roghi, V. Chabottaux, M. Janssen, C. Munaut, E. Maquoi, B. G. Galvez, C. Gilles, F. Frankenne, G. Murphy, et al. (2004)
J. Biol. Chem. 279, 13564-13574
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Distinct Roles for the Catalytic and Hemopexin Domains of Membrane Type 1-Matrix Metalloproteinase in Substrate Degradation and Cell Migration.
J. Cao, P. Kozarekar, M. Pavlaki, C. Chiarelli, W. F. Bahou, and S. Zucker (2004)
J. Biol. Chem. 279, 14129-14139
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Stromal Cell-Derived Factor-1{alpha} Promotes Melanoma Cell Invasion across Basement Membranes Involving Stimulation of Membrane-Type 1 Matrix Metalloproteinase and Rho GTPase Activities.
R. A. Bartolome, B. G. Galvez, N. Longo, F. Baleux, G. N. P. van Muijen, P. Sanchez-Mateos, A. G. Arroyo, and J. Teixido (2004)
Cancer Res. 64, 2534-2543
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The Shedding of Betaglycan Is Regulated by Pervanadate and Mediated by Membrane Type Matrix Metalloprotease-1.
G. Velasco-Loyden, J. Arribas, and F. Lopez-Casillas (2004)
J. Biol. Chem. 279, 7721-7733
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Engagement of CD44 Promotes Rac Activation and CD44 Cleavage during Tumor Cell Migration.
T. Murai, Y. Miyazaki, H. Nishinakamura, K. N. Sugahara, T. Miyauchi, Y. Sako, T. Yanagida, and M. Miyasaka (2004)
J. Biol. Chem. 279, 4541-4550
   Abstract »    Full Text »    PDF »
The Low Density Lipoprotein Receptor-related Protein LRP Is Regulated by Membrane Type-1 Matrix Metalloproteinase (MT1-MMP) Proteolysis in Malignant Cells.
D. V. Rozanov, E. Hahn-Dantona, D. K. Strickland, and A. Y. Strongin (2004)
J. Biol. Chem. 279, 4260-4268
   Abstract »    Full Text »    PDF »
Constitutive and Induced CD44 Shedding by ADAM-Like Proteases and Membrane-Type 1 Matrix Metalloproteinase.
H. Nakamura, N. Suenaga, K. Taniwaki, H. Matsuki, K. Yonezawa, M. Fujii, Y. Okada, and M. Seiki (2004)
Cancer Res. 64, 876-882
   Abstract »    Full Text »    PDF »
Mature Human Thymocytes Migrate on Laminin-5 with Activation of Metalloproteinase-14 and Cleavage of CD44.
M. Vivinus-Nebot, P. Rousselle, J.-P. Breittmayer, C. Cenciarini, S. Berrih-Aknin, S. Spong, P. Nokelainen, F. Cottrez, M. P. Marinkovich, and A. Bernard (2004)
J. Immunol. 172, 1397-1406
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Caveolae Are a Novel Pathway for Membrane-Type 1 Matrix Metalloproteinase Traffic in Human Endothelial Cells.
B. G. Galvez, S. Matias-Roman, M. Yanez-Mo, M. Vicente-Manzanares, F. Sanchez-Madrid, and A. G. Arroyo (2004)
Mol. Biol. Cell 15, 678-687
   Abstract »    Full Text »    PDF »
The role of the CD44 transmembrane and cytoplasmic domains in co-ordinating adhesive and signalling events.
R. F. Thorne, J. W. Legg, and C. M. Isacke (2004)
J. Cell Sci. 117, 373-380
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Clinical Significance of Cellular Distribution of Moesin in Patients with Oral Squamous Cell Carcinoma.
H. Kobayashi, J. Sagara, H. Kurita, M. Morifuji, M. Ohishi, K. Kurashina, and S.'i. Taniguchi (2004)
Clin. Cancer Res. 10, 572-580
   Abstract »    Full Text »    PDF »
Activation of Syndecan-1 Ectodomain Shedding by Staphylococcus aureus {alpha}-Toxin and {beta}-Toxin.
P. W. Park, T. J. Foster, E. Nishi, S. J. Duncan, M. Klagsbrun, and Y. Chen (2004)
J. Biol. Chem. 279, 251-258
   Abstract »    Full Text »    PDF »
Monoclonal Antibodies with Defined Recognition Sequences in the Stem Region of CD44: Detection of Differential Glycosylation of CD44 between Tumor and Stromal Cells in Tissue.
H. Matsuki, K. Yonezawa, K.'i. Obata, K. Iwata, H. Nakamura, Y. Okada, and M. Seiki (2003)
Cancer Res. 63, 8278-8283
   Abstract »    Full Text »    PDF »
Cleavage of Syndecan-1 by Membrane Type Matrix Metalloproteinase-1 Stimulates Cell Migration.
K. Endo, T. Takino, H. Miyamori, H. Kinsen, T. Yoshizaki, M. Furukawa, and H. Sato (2003)
J. Biol. Chem. 278, 40764-40770
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Membrane type I-matrix metalloproteinase (MT1-MMP) is internalised by two different pathways and is recycled to the cell surface.
A. Remacle, G. Murphy, and C. Roghi (2003)
J. Cell Sci. 116, 3905-3916
   Abstract »    Full Text »    PDF »

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