Original Article

Role of Cell Surface Metalloprotease MT1-MMP in Epithelial Cell Migration over Laminin-5

Correspondence to: Vito Quaranta, The Scripps Research Institute, SBR-12, 10550 North Torrey Pines Road, La Jolla, CA 92037. Tel:858-784-8793 Fax:858-784-2246 E-mail:quaranta{at}scripps.edu.

Laminin-5 (Ln-5) is an extracellular matrix substrate for cell adhesion and migration, which is found in many epithelial basement membranes. Mechanisms eliciting migration on Ln-5 need to be elucidated because of their relevance to tissue remodeling and cancer metastasis. We showed that exogenous addition of activated matrix metalloprotease (MMP) 2 stimulates migration onto Ln-5 in breast epithelial cells via cleavage of the 2 subunit. To investigate the biological scope of this proteolytic mechanism, we tested a panel of cells, including colon and breast carcinomas, hepatomas, and immortalized hepatocytes, selected because they migrated or scattered constitutively in the presence of Ln-5. We found that constitutive migration was inhibited by BB94 or TIMPs, known inhibitors of MMPs. Limited profiling by gelatin zymography and Western blotting indicated that the ability to constitutively migrate on Ln-5 correlated with expression of plasma membrane bound MT1-MMP metalloprotease, rather than secretion of MMP2, since MMP2 was not produced by three cell lines (one breast and two colon carcinomas) that constitutively migrated on Ln-5. Moreover, migration on Ln-5 was reduced by MT1-MMP antisense oligonucleotides both in MMP2+ and MMP2- cell lines. MT1-MMP directly cleaved Ln-5, with a pattern similar to that of MMP2. The hemopexin-like domain of MMP2, which interferes with MMP2 activation, reduced Ln-5 migration in MT1-MMP+, MMP2+ cells, but not in MT1-MMP+, MMP2- cells. These results suggest a model whereby expression of MT1-MMP is the primary trigger for migration over Ln-5, whereas MMP2, which is activated by MT1-MMP, may play an ancillary role, perhaps by amplifying the MT1-MMP effects. Codistribution of MT1-MMP with Ln-5 in colon and breast cancer tissue specimens suggested a role for this mechanism in invasion. Thus, Ln-5 cleavage by MMPs may be a widespread mechanism that triggers migration in cells contacting epithelial basement membranes.

Key Words: migration, extracellular matrix, epithelial cell, invasion

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• Cao, J., Kozarekar, P., Pavlaki, M., Chiarelli, C., Bahou, W. F., Zucker, S. (2004). Distinct Roles for the Catalytic and Hemopexin Domains of Membrane Type 1-Matrix Metalloproteinase in Substrate Degradation and Cell Migration. J. Biol. Chem. 279: 14129-14139 [Abstract] [Full Text]  
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• Siu, M. K.Y., Cheng, C. Y. (2004). Interactions of Proteases, Protease Inhibitors, and the {beta}1 Integrin/Laminin {gamma}3 Protein Complex in the Regulation of Ectoplasmic Specialization Dynamics in the Rat Testis. Biol. Reprod. 70: 945-964 [Abstract] [Full Text]  
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• Vivinus-Nebot, M., Rousselle, P., Breittmayer, J.-P., Cenciarini, C., Berrih-Aknin, S., Spong, S., Nokelainen, P., Cottrez, F., Marinkovich, M. P., Bernard, A. (2004). Mature Human Thymocytes Migrate on Laminin-5 with Activation of Metalloproteinase-14 and Cleavage of CD44. J. Immunol. 172: 1397-1406 [Abstract] [Full Text]  
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• Solberg, H., Rinkenberger, J., Dano, K., Werb, Z., Lund, L. R. (2003). A functional overlap of plasminogen and MMPs regulates vascularization during placental development. Development 130: 4439-4450 [Abstract] [Full Text]  
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• Natarajan, E., Saeb, M., Crum, C. P., Woo, S. B., McKee, P. H., Rheinwald, J. G. (2003). Co-Expression of p16INK4A and Laminin 5 {gamma}2 by Microinvasive and Superficial Squamous Cell Carcinomas in Vivo and by Migrating Wound and Senescent Keratinocytes in Culture. Am. J. Pathol. 163: 477-491 [Abstract] [Full Text]  
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• Visse, R., Nagase, H. (2003). Matrix Metalloproteinases and Tissue Inhibitors of Metalloproteinases: Structure, Function, and Biochemistry. Circ. Res. 92: 827-839 [Abstract] [Full Text]  
• Udayakumar, T. S., Chen, M. L., Bair, E. L., von Bredow, D. C., Cress, A. E., Nagle, R. B., Bowden, G. T. (2003). Membrane Type-1-Matrix Metalloproteinase Expressed by Prostate Carcinoma Cells Cleaves Human Laminin-5 {beta}3 Chain and Induces Cell Migration. Cancer Res. 63: 2292-2299 [Abstract] [Full Text]  
• Veitch, D. P., Nokelainen, P., McGowan, K. A., Nguyen, T.-T., Nguyen, N. E., Stephenson, R., Pappano, W. N., Keene, D. R., Spong, S. M., Greenspan, D. S., Findell, P. R., Marinkovich, M. P. (2003). Mammalian Tolloid Metalloproteinase, and Not Matrix Metalloprotease 2 or Membrane Type 1 Metalloprotease, Processes Laminin-5 in Keratinocytes and Skin. J. Biol. Chem. 278: 15661-15668 [Abstract] [Full Text]  
• Schenk, S., Hintermann, E., Bilban, M., Koshikawa, N., Hojilla, C., Khokha, R., Quaranta, V. (2003). Binding to EGF receptor of a laminin-5 EGF-like fragment liberated during MMP-dependent mammary gland involution. J. Cell Biol. 161: 197-209 [Abstract] [Full Text]  
• Katayama, M., Sanzen, N., Funakoshi, A., Sekiguchi, K. (2003). Laminin {gamma}2-Chain Fragment in the Circulation: A Prognostic Indicator of Epithelial Tumor Invasion. Cancer Res. 63: 222-229 [Abstract] [Full Text]  
• Hirosaki, T., Tsubota, Y., Kariya, Y., Moriyama, K., Mizushima, H., Miyazaki, K. (2002). Laminin-6 Is Activated by Proteolytic Processing and Regulates Cellular Adhesion and Migration Differently from Laminin-5. J. Biol. Chem. 277: 49287-49295 [Abstract] [Full Text]  
• Deugnier, M.-A., Faraldo, M. M., Janji, B., Rousselle, P., Thiery, J. P., Glukhova, M. A. (2002). EGF controls the in vivo developmental potential of a mammary epithelial cell line possessing progenitor properties. J. Cell Biol. 159: 453-463 [Abstract] [Full Text]  
• Galvez, B. G., Matias-Roman, S., Yanez-Mo, M., Sanchez-Madrid, F., Arroyo, A. G. (2002). ECM regulates MT1-MMP localization with {beta}1 or {alpha}v{beta}3 integrins at distinct cell compartments modulating its internalization and activity on human endothelial cells. J. Cell Biol. 159: 509-521 [Abstract] [Full Text]  
• Munshi, H. G., Wu, Y. I., Ariztia, E. V., Stack, M. S. (2002). Calcium Regulation of Matrix Metalloproteinase-mediated Migration in Oral Squamous Cell Carcinoma Cells. J. Biol. Chem. 277: 41480-41488 [Abstract] [Full Text]  
• Hintermann, E., Haake, S. K., Christen, U., Sharabi, A., Quaranta, V. (2002). Discrete Proteolysis of Focal Contact and Adherens Junction Components in Porphyromonas gingivalis-Infected Oral Keratinocytes: a Strategy for Cell Adhesion and Migration Disabling. Infect. Immun. 70: 5846-5856 [Abstract] [Full Text]  
• Schilperoort-Haun, K. R., Menino, A. R. Jr. (2002). Factors affecting cellular outgrowth from porcine inner cell masses in vitro. J ANIM SCI 80: 2671-2681 [Abstract] [Full Text]  
• Rattenholl, A., Pappano, W. N., Koch, M., Keene, D. R., Kadler, K. E., Sasaki, T., Timpl, R., Burgeson, R. E., Greenspan, D. S., Bruckner-Tuderman, L. (2002). Proteinases of the Bone Morphogenetic Protein-1 Family Convert Procollagen VII to Mature Anchoring Fibril Collagen. J. Biol. Chem. 277: 26372-26378 [Abstract] [Full Text]  
• Giannelli, G., Fransvea, E., Marinosci, F., Bergamini, C., Colucci, S., Schiraldi, O., Antonaci, S. (2002). Transforming Growth Factor-{beta}1 Triggers Hepatocellular Carcinoma Invasiveness via {alpha}3{beta}1 Integrin. Am. J. Pathol. 161: 183-193 [Abstract] [Full Text]  
• Llano, E., Adam, G., Pendas, A. M., Quesada, V., Sanchez, L. M., Santamaria, I., Noselli, S., Lopez-Otin, C. (2002). Structural and Enzymatic Characterization of Drosophila Dm2-MMP, a Membrane-bound Matrix Metalloproteinase with Tissue-specific Expression. J. Biol. Chem. 277: 23321-23329 [Abstract] [Full Text]  
• Wiseman, B. S., Werb, Z. (2002). Stromal Effects on Mammary Gland Development and Breast Cancer. Science 296: 1046-1049 [Abstract] [Full Text]  
• Khan, K. M. F., Laurie, G. W., McCaffrey, T. A., Falcone, D. J. (2002). Exposure of Cryptic Domains in the alpha 1-chain of Laminin-1 by Elastase Stimulates Macrophages Urokinase and Matrix Metalloproteinase-9 Expression. J. Biol. Chem. 277: 13778-13786 [Abstract] [Full Text]  
• SOUNNI, N. E., DEVY, L., HAJITOU, A., FRANKENNE, F., MUNAUT, C., GILLES, C., DEROANNE, C., THOMPSON, E. W., FOIDART, J. M., NOEL, A. (2002). MT1-MMP expression promotes tumor growth and angiogenesis through an up-regulation of vascular endothelial growth factor expression. FASEB J. 16: 555-564 [Abstract] [Full Text]  
• Fan, W.-H., Karnovsky, M. J. (2002). Increased MMP-2 Expression in Connective Tissue Growth Factor Over-expression Vascular Smooth Muscle Cells. J. Biol. Chem. 277: 9800-9805 [Abstract] [Full Text]  
• Gilles, C., Polette, M., Coraux, C., Tournier, J.-M., Meneguzzi, G., Munaut, C., Volders, L., Rousselle, P., Birembaut, P., Foidart, J.-M. (2002). Contribution of MT1-MMP and of human laminin-5 {gamma}2 chain degradation to mammary epithelial cell migration. J. Cell Sci. 114: 2967-2976 [Abstract] [Full Text]  
• Niki, T., Kohno, T., Iba, S., Moriya, Y., Takahashi, Y., Saito, M., Maeshima, A., Yamada, T., Matsuno, Y., Fukayama, M., Yokota, J., Hirohashi, S. (2002). Frequent Co-Localization of Cox-2 and Laminin-5 {gamma}2 Chain at the Invasive Front of Early-Stage Lung Adenocarcinomas. Am. J. Pathol. 160: 1129-1141 [Abstract] [Full Text]  
• Kheradmand, F., Rishi, K., Werb, Z. (2002). Signaling through the EGF receptor controls lung morphogenesis in part by regulating MT1-MMP-mediated activation of gelatinase A/MMP2. J. Cell Sci. 115: 839-848 [Abstract] [Full Text]  
• Hotary, K. B., Yana, I., Sabeh, F., Li, X.-Y., Holmbeck, K., Birkedal-Hansen, H., Allen, E. D., Hiraoka, N., Weiss, S. J. (2002). Matrix Metalloproteinases (MMPs) Regulate Fibrin-invasive Activity via MT1-MMP-dependent and -independent Processes. J. Exp. Med. 195: 295-308 [Abstract] [Full Text]  
• Gudjonsson, T., Ronnov-Jessen, L., Villadsen, R., Rank, F., Bissell, M. J., Petersen, O. W. (2002). Normal and tumor-derived myoepithelial cells differ in their ability to interact with luminal breast epithelial cells for polarity and basement membrane deposition. J. Cell Sci. 115: 39-50 [Abstract] [Full Text]  
• Deryugina, E. I., Soroceanu, L., Strongin, A. Y. (2002). Up-Regulation of Vascular Endothelial Growth Factor by Membrane-type 1 Matrix Metalloproteinase Stimulates Human Glioma Xenograft Growth and Angiogenesis. Cancer Res. 62: 580-588 [Abstract] [Full Text]  
• Hlubek, F., Jung, A., Kotzor, N., Kirchner, T., Brabletz, T. (2001). Expression of the Invasion Factor Laminin {gamma}2 in Colorectal Carcinomas Is Regulated by {beta}-Catenin. Cancer Res. 61: 8089-8093 [Abstract] [Full Text]  
• Seftor, R. E. B., Seftor, E. A., Koshikawa, N., Meltzer, P. S., Gardner, L. M. G., Bilban, M., Stetler-Stevenson, W. G., Quaranta, V., Hendrix, M. J. C. (2001). Cooperative Interactions of Laminin 5 {gamma}2 Chain, Matrix Metalloproteinase-2, and Membrane Type-1-Matrix/Metalloproteinase Are Required for Mimicry of Embryonic Vasculogenesis by Aggressive Melanoma. Cancer Res. 61: 6322-6327 [Abstract] [Full Text]  
• Aznavoorian, S., Moore, B. A., Alexander-Lister, L. D., Hallit, S. L., Windsor, L. J., Engler, J. A. (2001). Membrane Type I-Matrix Metalloproteinase-Mediated Degradation of Type I Collagen by Oral Squamous Cell Carcinoma Cells. Cancer Res. 61: 6264-6275 [Abstract] [Full Text]  
• Määttä, M., Virtanen, I., Burgeson, R., Autio–Harmainen, H. (2001). Comparative Analysis of the Distribution of Laminin Chains in the Basement Membranes in Some Malignant Epithelial Tumors: The {{alpha}}1 Chain of Laminin Shows a Selected Expression Pattern in Human Carcinomas. J. Histochem. Cytochem. 49: 711-726 [Abstract] [Full Text]  
• Kajita, M., Itoh, Y., Chiba, T., Mori, H., Okada, A., Kinoh, H., Seiki, M. (2001). Membrane-type 1 Matrix Metalloproteinase Cleaves CD44 and Promotes Cell Migration. J. Cell Biol. 153: 893-904 [Abstract] [Full Text]  
• Gagnoux-Palacios, L., Allegra, M., Spirito, F., Pommeret, O., Romero, C., Ortonne, J.-p., Meneguzzi, G. (2001). The Short Arm of the Laminin {gamma}2 Chain Plays a Pivotal Role in the Incorporation of Laminin 5 into the Extracellular Matrix and in Cell Adhesion. J. Cell Biol. 153: 835-850 [Abstract] [Full Text]  
• Decline, F, Rousselle, P (2001). Keratinocyte migration requires alpha2beta1 integrin-mediated interaction with the laminin 5 gamma2 chain. J. Cell Sci. 114: 811-823 [Abstract]  
• Vu, T. H., Werb, Z. (2000). Matrix metalloproteinases: effectors of development and normal physiology. Genes Dev. 14: 2123-2133 [Full Text]  
• Määttä, M., Soini, Y., Liakka, A., Autio-Harmainen, H. (2000). Differential Expression of Matrix Metalloproteinase (MMP)-2, MMP-9, and Membrane Type 1-MMP in Hepatocellular and Pancreatic Adenocarcinoma: Implications for Tumor Progression and Clinical Prognosis. Clin. Cancer Res. 6: 2726-2734 [Abstract] [Full Text]  
• Hotary, K., Allen, E., Punturieri, A., Yana, I., Weiss, S. J. (2000). Regulation of Cell Invasion and Morphogenesis in a Three-dimensional Type I Collagen Matrix by Membrane-type Matrix Metalloproteinases 1, 2, and 3. J. Cell Biol. 149: 1309-1323 [Abstract] [Full Text]  
• Hirosaki, T., Mizushima, H., Tsubota, Y., Moriyama, K., Miyazaki, K. (2000). Structural Requirement of Carboxyl-terminal Globular Domains of Laminin alpha 3 Chain for Promotion of Rapid Cell Adhesion and Migration by Laminin-5. J. Biol. Chem. 275: 22495-22502 [Abstract] [Full Text]  
• Llano, E., Pendas, A. M., Aza-Blanc, P., Kornberg, T. B., Lopez-Otin, C. (2000). Dm1-MMP, a Matrix Metalloproteinase from Drosophila with a Potential Role in Extracellular Matrix Remodeling during Neural Development. J. Biol. Chem. 275: 35978-35985 [Abstract] [Full Text]  
• Nguyen, B. P., Gil, S. G., Carter, W. G. (2000). Deposition of Laminin 5 by Keratinocytes Regulates Integrin Adhesion and Signaling. J. Biol. Chem. 275: 31896-31907 [Abstract] [Full Text]  
• Pei, D., Kang, T., Qi, H. (2000). Cysteine Array Matrix Metalloproteinase (CA-MMP)/MMP-23 Is a Type II Transmembrane Matrix Metalloproteinase Regulated by a Single Cleavage for Both Secretion and Activation. J. Biol. Chem. 275: 33988-33997 [Abstract] [Full Text]  
• Rozanov, D. V., Deryugina, E. I., Ratnikov, B. I., Monosov, E. Z., Marchenko, G. N., Quigley, J. P., Strongin, A. Y. (2001). Mutation Analysis of Membrane Type-1 Matrix Metalloproteinase (MT1-MMP). THE ROLE OF THE CYTOPLASMIC TAIL CYS574, THE ACTIVE SITE GLU240, AND FURIN CLEAVAGE MOTIFS IN OLIGOMERIZATION, PROCESSING, AND SELF-PROTEOLYSIS OF MT1-MMP EXPRESSED IN BREAST CARCINOMA CELLS. J. Biol. Chem. 276: 25705-25714 [Abstract] [Full Text]  
• Dans, M., Gagnoux-Palacios, L., Blaikie, P., Klein, S., Mariotti, A., Giancotti, F. G. (2001). Tyrosine Phosphorylation of the beta 4 Integrin Cytoplasmic Domain Mediates Shc Signaling to Extracellular Signal-regulated Kinase and Antagonizes Formation of Hemidesmosomes. J. Biol. Chem. 276: 1494-1502 [Abstract] [Full Text]  
• Belkin, A. M., Akimov, S. S., Zaritskaya, L. S., Ratnikov, B. I., Deryugina, E. I., Strongin, A. Y. (2001). Matrix-dependent Proteolysis of Surface Transglutaminase by Membrane-type Metalloproteinase Regulates Cancer Cell Adhesion and Locomotion. J. Biol. Chem. 276: 18415-18422 [Abstract] [Full Text]  
• Fujiwara, H., Kikkawa, Y., Sanzen, N., Sekiguchi, K. (2001). Purification and Characterization of Human Laminin-8. LAMININ-8 STIMULATES CELL ADHESION AND MIGRATION THROUGH alpha 3beta 1 AND alpha 6beta 1 INTEGRINS. J. Biol. Chem. 276: 17550-17558 [Abstract] [Full Text]  
• Zhuge, Y., Xu, J. (2001). Rac1 Mediates Type I Collagen-dependent MMP-2 Activation. ROLE IN CELL INVASION ACROSS COLLAGEN BARRIER. J. Biol. Chem. 276: 16248-16256 [Abstract] [Full Text]  
• Shang, M., Koshikawa, N., Schenk, S., Quaranta, V. (2001). The LG3 Module of Laminin-5 Harbors a Binding Site for Integrin alpha 3beta 1 That Promotes Cell Adhesion, Spreading, and Migration. J. Biol. Chem. 276: 33045-33053 [Abstract] [Full Text]  
• Utani, A., Nomizu, M., Matsuura, H., Kato, K., Kobayashi, T., Takeda, U., Aota, S., Nielsen, P. K., Shinkai, H. (2001). A Unique Sequence of the Laminin alpha 3 G Domain Binds to Heparin and Promotes Cell Adhesion through Syndecan-2 and -4. J. Biol. Chem. 276: 28779-28788 [Abstract] [Full Text]  
• Khatib, A.-M., Siegfried, G., Prat, A., Luis, J., Chretien, M., Metrakos, P., Seidah, N. G. (2001). Inhibition of Proprotein Convertases Is Associated with Loss of Growth and Tumorigenicity of HT-29 Human Colon Carcinoma Cells. IMPORTANCE OF INSULIN-LIKE GROWTH FACTOR-1 (IGF-1) RECEPTOR PROCESSING IN IGF-1-MEDIATED FUNCTIONS. J. Biol. Chem. 276: 30686-30693 [Abstract] [Full Text]  
• Galvez, B. G., Matias-Roman, S., Albar, J. P., Sanchez-Madrid, F., Arroyo, A. G. (2001). Membrane Type 1-Matrix Metalloproteinase Is Activated during Migration of Human Endothelial Cells and Modulates Endothelial Motility and Matrix Remodeling. J. Biol. Chem. 276: 37491-37500 [Abstract] [Full Text]  
• Pavlaki, M., Cao, J., Hymowitz, M., Chen, W.-T., Bahou, W., Zucker, S. (2002). A Conserved Sequence within the Propeptide Domain of Membrane Type 1 Matrix Metalloproteinase Is Critical for Function as an Intramolecular Chaperone. J. Biol. Chem. 277: 2740-2749 [Abstract] [Full Text]  
• Uekita, T., Itoh, Y., Yana, I., Ohno, H., Seiki, M. (2001). Cytoplasmic tail-dependent internalization of membrane-type 1 matrix metalloproteinase is important for its invasion-promoting activity. J. Cell Biol. 155: 1345-1356 [Abstract] [Full Text]  

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