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MT4-(MMP17) and MT6-MMP (MMP25), A unique set of membrane-anchored matrix metalloproteinases: properties and expression in cancer

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Abstract

The process of cancer progression involves the action of multiple proteolytic systems, among which the family of matrix metalloproteinases (MMPs) play a pivotal role. The MMPs evolved to accomplish their proteolytic tasks in multiple cellular and tissue microenvironments including lipid rafts by incorporation and deletions of specific structural domains. The membrane type-MMPs (MT-MMPs) incorporated membrane anchoring domains that display these proteases at the cell surface, and thus they are optimal pericellular proteolytic machines. Two members of the MT-MMP subfamily, MMP-17 (MT4-MMP) and MMP-25 (MT6-MMP), are anchored to the plasma membrane via a glycosyl-phosphatidyl inositol (GPI) anchor, which confers these enzymes a unique set of regulatory and functional mechanisms that separates them from the rest of the MMP family. Discovered almost a decade ago, the body of work on GPI-MT-MMPs today is still surprisingly limited when compared to other MT-MMPs. However, new evidence shows that the GPI-MT-MMPs are highly expressed in human cancer, where they are associated with progression. Accumulating biochemical and functional evidence also highlights their distinct properties. In this review, we summarize the structural, biochemical, and biological properties of GPI-MT-MMPs and present an overview of their expression and role in cancer. We further discuss the potential implications of GPI-anchoring for enzyme function. Finally, we comment on the new scientific challenges that lie ahead to better understand the function and role in cancer of these intriguing but yet unique MMPs.

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References

  1. McCawley, L. J., & Matrisian, L. M. (2000). Matrix metalloproteinases: Multifunctional contributors to tumor progression. Molecular Medicine Today, 6, 149–156.

    Article  PubMed  CAS  Google Scholar 

  2. Stamenkovic, I. (2000). Matrix metalloproteinases in tumor invasion and metastasis. Seminars in Cancer Biology, 10, 415–433.

    Article  PubMed  CAS  Google Scholar 

  3. Itoh, Y., & Nagase, H. (2002). Matrix metalloproteinases in cancer. Essays in Biochemistry, 38, 21–36.

    PubMed  CAS  Google Scholar 

  4. Lafleur, M. A., Handsley, M. M., & Edwards, D. R. (2003). Metalloproteinases and their inhibitors in angiogenesis. Expert Reviews in Molecular Medicine, 5, 1–39.

    Article  PubMed  Google Scholar 

  5. Deryugina, E. I., & Quigley, J. P. (2006). Matrix metalloproteinases and tumor metastasis. Cancer and Metastasis Reviews, 25, 9–34.

    Article  PubMed  CAS  Google Scholar 

  6. Fingleton, B. (2006). Matrix metalloproteinases: Roles in cancer and metastasis. Frontiers in Bioscience, 11, 479–491.

    Article  CAS  Google Scholar 

  7. Martin, M. D., & Matrisian, L. M. (2007). The other side of MMPs: Protective roles in tumor progression. Cancer and Metastasis Reviews, 26, 717–724.

    Article  PubMed  CAS  Google Scholar 

  8. Noel, A., Jost, M., & Maquoi, E. (2008). Matrix metalloproteinases at cancer tumor-host interface. Seminars in Cell & Developmental Biology, 19, 52–60.

    Article  CAS  Google Scholar 

  9. Jodele, S., Blavier, L., Yoonm, J. M., & DeClerck, Y. A. (2006). Modifying the soil to affect the seed: Role of stromal-derived matrix metalloproteinases in cancer progression. Cancer and Metastasis Reviews, 25, 35–43.

    Article  PubMed  CAS  Google Scholar 

  10. Zucker, S., Pei, D., Cao, J., & Lopez-Otin, C. (2003). Membrane type-matrix metalloproteinases (MT-MMP). Current Topics in Developmental Biology, 54, 1–74.

    Article  PubMed  CAS  Google Scholar 

  11. Holmbeck, K., Bianco, P., Yamada, S., & Birkedal-Hansen, H. (2004). MT1-MMP: A tethered collagenase. Journal of Cellular Physiology, 200, 11–19.

    Article  PubMed  CAS  Google Scholar 

  12. Hotary, K., Li, X. Y., Allen, E., Stevens, S. L., & Weiss, S. J. (2006). A cancer cell metalloprotease triad regulates the basement membrane transmigration program. Genes & Development, 20, 2673–2686.

    Article  CAS  Google Scholar 

  13. Barbolina, M. V., & Stack, M. S. (2008). Membrane type 1-matrix metalloproteinase: Substrate diversity in pericellular proteolysis. Seminars in Cell & Developmental Biology, 19, 24–33.

    Article  CAS  Google Scholar 

  14. Itoh, Y., & Seiki, M. (2006). MT1-MMP: A potent modifier of pericellular microenvironment. Journal of Cellular Physiology, 206, 1–8.

    Article  PubMed  CAS  Google Scholar 

  15. Osenkowski, P., Toth, M., & Fridman, R. (2004). Processing, shedding, and endocytosis of membrane type 1-matrix metalloproteinase (MT1-MMP). Journal of Cellular Physiology, 200, 2–10.

    Article  PubMed  CAS  Google Scholar 

  16. Sato, H., Takino, T., Okada, Y., Cao, J., Shinagawa, A., Yamamoto, E., et al. (1994). A matrix metalloproteinase expressed on the surface of invasive tumour cells. Nature, 370, 61–65.

    Article  PubMed  CAS  Google Scholar 

  17. Strongin, A. Y., Collier, I., Bannikov, G., Marmer, B. L., Grant, G. A., & Goldberg, G. I. (1995). Mechanism of cell surface activation of 72-kDa type IV collagenase. Isolation of the activated form of the membrane metalloprotease. Journal of Biological Chemistry, 270, 5331–5338.

    Article  PubMed  CAS  Google Scholar 

  18. Arroyo, A. G., Genis, L., Gonzalo, P., Matias-Roman, S., Pollan, A., & Galvez, B. G. (2007). Matrix metalloproteinases: New routes to the use of MT1-MMP as a therapeutic target in angiogenesis-related disease. Current Pharmaceutical Design, 13, 1787–1802.

    Article  PubMed  CAS  Google Scholar 

  19. Tanaka, M., Sato, H., Takino, T., Iwata, K., Inoue, M., & Seiki, M. (1997). Isolation of a mouse MT2-MMP gene from a lung cDNA library and identification of its product. FEBS Letters, 402, 219–222.

    Article  PubMed  CAS  Google Scholar 

  20. Takino, T., Sato, H., Shinagawa, A., & Seiki, M. (1995). Identification of the second membrane-type matrix metalloproteinase (MT- MMP-2) gene from a human placenta cDNA library. MT-MMPs form a unique membrane-type subclass in the MMP family. Journal of Biological Chemistry, 270, 23013–23020.

    Article  PubMed  CAS  Google Scholar 

  21. Pei, D. (1999). Identification and characterization of the fifth membrane-type matrix metalloproteinase MT5-MMP. Journal of Biological Chemistry, 274, 8925–8932.

    Article  PubMed  CAS  Google Scholar 

  22. Llano, E., Pendas, A. M., Freije, J. P., Nakano, A., Knauper, V., Murphy, G., et al. (1999). Identification and characterization of human MT5-MMP, a new membrane-bound activator of progelatinase a overexpressed in brain tumors. Cancer Research, 59, 2570–2576.

    PubMed  CAS  Google Scholar 

  23. Kajita, M., Kinoh, H., Ito, N., Takamura, A., Itoh, Y., Okada, A., et al. (1999). Human membrane type-4 matrix metalloproteinase (MT4-MMP) is encoded by a novel major transcript: Isolation of complementary DNA clones for human and mouse mt4-mmp transcripts. FEBS Letters, 457, 353–356.

    Article  PubMed  CAS  Google Scholar 

  24. Puente, X. S., Pendas, A. M., Llano, E., Velasco, G., & Lopez-Otin, C. (1996). Molecular cloning of a novel membrane-type matrix metalloproteinase from a human breast carcinoma. Cancer Research, 56, 944–949.

    PubMed  CAS  Google Scholar 

  25. Pei, D. (1999). Leukolysin/MMP25/MT6-MMP: A novel matrix metalloproteinase specifically expressed in the leukocyte lineage. Cell Research, 9, 291–303.

    Article  PubMed  CAS  Google Scholar 

  26. Velasco, G., Cal, S., Merlos-Suarez, A., Ferrando, A. A., Alvarez, S., Nakano, A., et al. (2000). Human MT6-matrix metalloproteinase: Identification, progelatinase A activation, and expression in brain tumors. Cancer Research, 60, 877–882.

    PubMed  CAS  Google Scholar 

  27. Overall, C. M. (2001). Matrix metalloproteinase substrate binding domains, modules and exosites. Overview and experimental strategies. Methods in Molecular Biology, 151, 79–120.

    PubMed  CAS  Google Scholar 

  28. Udenfriend, S., & Kodukula, K. (1995). How glycosylphosphatidylinositol-anchored membrane proteins are made. Annual Review in Biochemistry, 64, 563–591.

    CAS  Google Scholar 

  29. Itoh, Y., Kajita, M., Kinoh, H., Mori, H., Okada, A., & Seiki, M. (1999). Membrane type 4 matrix metalloproteinase (MT4-MMP, MMP-17) is a glycosylphosphatidylinositol-anchored proteinase. Journal of Biological Chemistry, 274, 34260–34266.

    Article  PubMed  CAS  Google Scholar 

  30. Kang, T., Yi, J., Guo, A., Wang, X., Overall, C. M., Jiang, W., et al. (2001). Subcellular distribution and cytokine- and chemokine-regulated secretion of leukolysin/MT6-MMP/MMP-25 in neutrophils. Journal of Biological Chemistry, 276, 21960–21968.

    Article  PubMed  CAS  Google Scholar 

  31. Kojima, S., Itoh, Y., Matsumoto, S., Masuho, Y., & Seiki, M. (2000). Membrane-type 6 matrix metalloproteinase (MT6-MMP, MMP-25) is the second glycosyl-phosphatidyl inositol (GPI)-anchored MMP. FEBS Letters, 480, 142–146.

    Article  PubMed  CAS  Google Scholar 

  32. Sun, Q., Weber, C. R., Sohail, A., Bernardo, M. M., Toth, M., Zhao, H., et al. (2007). MMP25 (MT6-MMP) is highly expressed in human colon cancer, promotes tumor growth, and exhibits unique biochemical properties. Journal of Biological Chemistry, 282, 21998–22010.

    Article  PubMed  CAS  Google Scholar 

  33. Itoh, Y., Takamura, A., Ito, N., Maru, Y., Sato, H., Suenaga, N., et al. (2001). Homophilic complex formation of MT1-MMP facilitates proMMP-2 activation on the cell surface and promotes tumor cell invasion. EMBO Journal, 20, 4782–4793.

    Article  PubMed  CAS  Google Scholar 

  34. Lehti, K., Lohi, J., Juntunen, M. M., Pei, D., & Keski-Oja, J. (2002). Oligomerization through hemopexin and cytoplasmic domains regulates the activity and turnover of membrane-type 1 matrix metalloproteinase. Journal of Biological Chemistry, 277, 8440–8448.

    Article  PubMed  CAS  Google Scholar 

  35. Galvez, B. G., Genis, L., Matias-Roman, S., Oblander, S. A., Tryggvason, K., Apte, S. S., & Arroyo, A. G. (2005). Membrane type 1-matrix metalloproteinase is regulated by chemokines monocyte-chemoattractant protein-1/ccl2 and interleukin-8/CXCL8 in endothelial cells during angiogenesis. Journal of Biological Chemistry, 280, 1292–1298.

    Article  PubMed  CAS  Google Scholar 

  36. Rozanov, D. V., Deryugina, E. I., Ratnikov, B. I., Monosov, E. Z., Marchenko, G. N., & Quigley, J. P. (2001). Strongin AY: Mutation analysis of membrane type-1 matrix metalloproteinase (MT1-MMP). The role of the cytoplasmic tail Cys(574), the active site Glu(240), and furin cleavage motifs in oligomerization, processing, and self-proteolysis of MT1-MMP expressed in breast carcinoma cells. Journal of Biological Chemistry, 276, 25705–25714.

    Article  PubMed  CAS  Google Scholar 

  37. Paladino, S., Sarnataro, D., Pillich, R., Tivodar, S., Nitsch, L., & Zurzolo, C. (2004). Protein oligomerization modulates raft partitioning and apical sorting of GPI-anchored proteins. Journal of Cell Biology, 167, 699–709.

    Article  PubMed  CAS  Google Scholar 

  38. Paladino, S., Sarnataro, D., Tivodar, S., & Zurzolo, C. (2007). Oligomerization is a specific requirement for apical sorting of glycosyl-phosphatidylinositol-anchored proteins but not for non-raft-associated apical proteins. Traffic, 8, 251–258.

    Article  PubMed  CAS  Google Scholar 

  39. Sharom, F. J., & Lehto, M. T. (2002). Glycosylphosphatidylinositol-anchored proteins: Structure, function, and cleavage by phosphatidylinositol-specific phospholipase C. Biochemistry and Cell Biology, 80, 535–549.

    Article  PubMed  CAS  Google Scholar 

  40. Eisenhaber, B., Bork, P., & Eisenhaber, F. (1998). Sequence properties of GPI-anchored proteins near the omega-site: Constraints for the polypeptide binding site of the putative transamidase. Protein Engineering, 11, 1155–1161.

    Article  PubMed  CAS  Google Scholar 

  41. Eisenhaber, B., Bork, P., & Eisenhaber, F. (1999). Prediction of potential GPI-modification sites in proprotein sequences. Journal of Molecular Biology, 292, 741–758.

    Article  PubMed  CAS  Google Scholar 

  42. Eisenhaber, B., Bork, P., Yuan, Y., Loffler, G., & Eisenhaber, F. (2000). Automated annotation of GPI anchor sites: Case study C. elegans. Trends in Biochemical Sciences, 25, 340–341.

    Article  PubMed  CAS  Google Scholar 

  43. Ferguson, M. A., & Williams, A. F. (1988). Cell-surface anchoring of proteins via glycosyl-phosphatidylinositol structures. Annual Review of Biochemistry, 57, 285–320.

    Article  PubMed  CAS  Google Scholar 

  44. Chen, R., Walter, E. I., Parker, G., Lapurga, J. P., Millan, J. L., Ikehara, Y., et al. (1998). Mammalian glycophosphatidylinositol anchor transfer to proteins and posttransfer deacylation. Proceedings of the National Academy of Sciences of the United States of America, 95, 9512–9517.

    Article  PubMed  CAS  Google Scholar 

  45. Maeda, Y., Tashima, Y., Houjou, T., Fujita, M., Yoko-o, T., Jigami, Y., et al. (2007). Fatty acid remodeling of GPI-anchored proteins is required for their raft association. Molecular Biology of the Cell, 18, 1497–1506.

    Article  PubMed  CAS  Google Scholar 

  46. Nebl, T., Pestonjamasp, K. N., Leszyk, J. D., Crowley, J. L., Oh, S. W., & Luna, E. J. (2002). Proteomic analysis of a detergent-resistant membrane skeleton from neutrophil plasma membranes. Journal of Biological Chemistry, 277, 43399–43409.

    Article  PubMed  CAS  Google Scholar 

  47. Stijlemans, B., Baral, T. N., Guilliams, M., Brys, L., Korf, J., Drennan, M., et al. (2007). A glycosylphosphatidylinositol-based treatment alleviates trypanosomiasis-associated immunopathology. Journal of Immunology, 179, 4003–4014.

    CAS  Google Scholar 

  48. Rollason, R., Korolchuk, V., Hamilton, C., Schu, P., & Banting, G. (2007). Clathrin-mediated endocytosis of a lipid-raft-associated protein is mediated through a dual tyrosine motif. Journal of Cell Science, 120, 3850–3858.

    Article  PubMed  CAS  Google Scholar 

  49. Paladino, S., Pocard, T., Catino, M. A., & Zurzolo, C. (2006). GPI-anchored proteins are directly targeted to the apical surface in fully polarized MDCK cells. Journal of Cell Biology, 172, 1023–1034.

    Article  PubMed  CAS  Google Scholar 

  50. Butler, G. S., & Overall, C. M. (2007). Proteomic validation of protease drug targets: Pharmacoproteomics of matrix metalloproteinase inhibitor drugs using isotope-coded affinity tag labelling and tandem mass spectrometry. Current Pharmaceutical Design, 13, 263–270.

    Article  PubMed  CAS  Google Scholar 

  51. Kumari, S., & Mayor, S. (2008). ARF1 is directly involved in dynamin-independent endocytosis. Nature Cell Biology, 10, 30–41.

    Article  PubMed  CAS  Google Scholar 

  52. Jiang, A., Lehti, K., Wang, X., Weiss, S. J., Keski-Oja, J., & Pei, D. (2001). Regulation of membrane-type matrix metalloproteinase 1 activity by dynamin-mediated endocytosis. Proceedings of the National Academy of Sciences of the United States of America, 98, 13693–13698.

    Article  PubMed  CAS  Google Scholar 

  53. Baker, A. H., Edwards, D. R., & Murphy, G. (2002). Metalloproteinase inhibitors: Biological actions and therapeutic opportunities. Journal of Cell Science, 115, 3719–3727.

    Article  PubMed  CAS  Google Scholar 

  54. Brew, K., Dinakarpandian, D., & Nagase, H. (2000). Tissue inhibitors of metalloproteinases: Evolution, structure and function. Biochimica et Biophysica Acta, 1477, 267–283.

    PubMed  CAS  Google Scholar 

  55. Chirco, R., Liu, X. W., Jung, K. K., & Kim, H. R. (2006). Novel functions of TIMPs in cell signaling. Cancer and Metastasis Reviews, 25, 99–113.

    Article  PubMed  CAS  Google Scholar 

  56. Maskos, K., & Bode, W. (2003). Structural basis of matrix metalloproteinases and tissue inhibitors of metalloproteinases. Molecular Biotechnology, 25, 241–266.

    Article  PubMed  CAS  Google Scholar 

  57. Lambert, E., Dasse, E., Haye, B., & Petitfrere, E. (2004). TIMPs as multifacial proteins. Critical Reviews in Oncology/Hematology, 49, 187–198.

    Article  PubMed  Google Scholar 

  58. Lee, M. H., Rapti, M., Knauper, V., & Murphy, G. (2004). Threonine 98, the pivotal residue of tissue inhibitor of metalloproteinases (TIMP)-1 in metalloproteinase recognition. Journal of Biological Chemistry, 279, 17562–17569.

    Article  PubMed  CAS  Google Scholar 

  59. English, W. R., Puente, X. S., Freije, J. M., Knauper, V., Amour, A., Merryweather, A., et al. (2000). Membrane type 4 matrix metalloproteinase (MMP17) has tumor necrosis factor-alpha convertase activity but does not activate pro-MMP2. Journal of Biological Chemistry, 275, 14046–14055.

    Article  PubMed  CAS  Google Scholar 

  60. Kolkenbrock, H., Essers, L., Ulbrich, N., & Will, H. (1999). Biochemical characterization of the catalytic domain of membrane-type 4 matrix metalloproteinase. Biological Chemistry, 380, 1103–1108.

    Article  PubMed  CAS  Google Scholar 

  61. Wang, Y., Johnson, A. R., Ye, Q. Z., & Dyer, R. D. (1999). Catalytic activities and substrate specificity of the human membrane type 4 matrix metalloproteinase catalytic domain. Journal of Biological Chemistry, 274, 33043–33049.

    Article  PubMed  CAS  Google Scholar 

  62. English, W. R., Velasco, G., Stracke, J. O., Knauper, V., & Murphy, G. (2001). Catalytic activities of membrane-type 6 matrix metalloproteinase (MMP25). FEBS Letters, 491, 137–142.

    Article  PubMed  CAS  Google Scholar 

  63. Matsuda, A., Itoh, Y., Koshikawa, N., Akizawa, T., Yana, I., & Seiki, M. (2003). Clusterin, an abundant serum factor, is a possible negative regulator of MT6-MMP/MMP-25 produced by neutrophils. Journal of Biological Chemistry, 278, 36350–36357.

    Article  PubMed  CAS  Google Scholar 

  64. Shannan, B., Seifert, M., Leskov, K., Willis, J., Boothman, D., Tilgen, W., et al. (2006). Challenge and promise: Roles for clusterin in pathogenesis, progression and therapy of cancer. Cell Death Differentiation, 13, 12–19.

    Article  CAS  Google Scholar 

  65. Rooney, I. A., Heuser, J. E., & Atkinson, J. P. (1996). GPI-anchored complement regulatory proteins in seminal plasma. An analysis of their physical condition and the mechanisms of their binding to exogenous cells. Journal of Clinical Investigation, 97, 1675–1686.

    Article  PubMed  CAS  Google Scholar 

  66. Robertson, C., Booth, S. A., Beniac, D. R., Coulthart, M. B., Booth, T. F., & McNicol, A. (2006). Cellular prion protein is released on exosomes from activated platelets. Blood, 107, 3907–3911.

    Article  PubMed  CAS  Google Scholar 

  67. Suzuki, K., & Okumura, Y. (2000). GPI-linked proteins do not transfer spontaneously from erythrocytes to liposomes. New aspects of reorganization of the cell membrane. Biochemistry, 39, 9477–9485.

    Article  PubMed  CAS  Google Scholar 

  68. Chabottaux, V., Sounni, N. E., Pennington, C. J., English, W. R., van den Brule, F., Blacher, S., et al. (2006). Membrane-type 4 matrix metalloproteinase promotes breast cancer growth and metastases. Cancer Research, 66, 5165–5172.

    Article  PubMed  CAS  Google Scholar 

  69. Lauc, G., & Heffer-Lauc, M. (2006). Shedding and uptake of gangliosides and glycosylphosphatidylinositol-anchored proteins. Biochimica et Biophysica Acta, 1760, 584–602.

    PubMed  CAS  Google Scholar 

  70. Nie, J., & Pei, D. (2004). Rapid inactivation of alpha-1-proteinase inhibitor by neutrophil specific leukolysin/membrane-type matrix metalloproteinase 6. Experimental Cell Research, 296, 145–150.

    Article  PubMed  CAS  Google Scholar 

  71. Nie, J., & Pei, D. (2003). Direct activation of pro-matrix metalloproteinase-2 by leukolysin/membrane-type 6 matrix metalloproteinase/matrix metalloproteinase 25 at the asn(109)-Tyr bond. Cancer Research, 63, 6758–6762.

    PubMed  CAS  Google Scholar 

  72. Hotary, K. B., Yana, I., Sabeh, F., Li, X. Y., Holmbeck, K., Birkedal-Hansen, H., et al. (2002). Matrix metalloproteinases (MMPs) regulate fibrin-invasive activity via MT1-MMP-dependent and -independent processes. Journal of Experimental Medicine, 195, 295–308.

    Article  PubMed  CAS  Google Scholar 

  73. Grant, G. M., Giambernardi, T. A., Grant, A. M., & Klebe, R. J. (1999). Overview of expression of matrix metalloproteinases (MMP-17, MMP-18, and MMP-20) in cultured human cells. Matrix Biology, 18, 145–148.

    Article  PubMed  CAS  Google Scholar 

  74. Rikimaru, A., Komori, K., Sakamoto, T., Ichise, H., Yoshida, N., Yana, I., et al. (2007). Establishment of an MT4-MMP-deficient mouse strain representing an efficient tracking system for MT4-MMP/MMP-17 expression in vivo using beta-galactosidase. Genes Cells, 12, 1091–1100.

    Article  PubMed  CAS  Google Scholar 

  75. Rozanov, D. V., Hahn-Dantona, E., Strickland, D. K., & Strongin, A. Y. (2004). The low density lipoprotein receptor-related protein LRP is regulated by membrane type-1 matrix metalloproteinase (MT1-MMP) proteolysis in malignant cells. Journal of Biological Chemistry, 279, 4260–4268.

    Article  PubMed  CAS  Google Scholar 

  76. Andolfo, A., English, W. R., Resnati, M., Murphy, G., Blasi, F., & Sidenius, N. (2002). Metalloproteases cleave the urokinase-type plasminogen activator receptor in the D1-D2 linker region and expose epitopes not present in the intact soluble receptor. Thrombosis and Haemostasis, 88, 298–306.

    PubMed  CAS  Google Scholar 

  77. Dumic, J., Dabelic, S., & Flogel, M. (2006). Galectin-3: An open-ended story. Biochimica et Biophysica Acta, 1760, 616–635.

    PubMed  CAS  Google Scholar 

  78. McClung, H. M., Thomas, S. L., Osenkowski, P., Toth, M., Menon, P., Raz, A., et al. (2007). SPARC upregulates MT1-MMP expression, MMP-2 activation, and the secretion and cleavage of galectin-3 in U87MG glioma cells. Neuroscience Letters, 419, 172–177.

    Article  PubMed  CAS  Google Scholar 

  79. Ochieng, J., Fridman, R., Nangia-Makker, P., Kleiner, D. E., Liotta, L. A., Stetler-Stevenson, W. G., et al. (1994). Galectin-3 is a novel substrate for human matrix metalloproteinases-2 and -9. Biochemistry, 33, 14109–14114.

    Article  PubMed  CAS  Google Scholar 

  80. Toth, M., Osenkowski, P., Hesek, D., Brown, S., Meroueh, S., Sakr, W., et al. (2005). Cleavage at the stem region releases an active ectodomain of the membrane type 1 matrix metalloproteinase. Biochemistry Journal, 387, 497–506.

    Article  CAS  Google Scholar 

  81. Nagase, H. (1997). Activation mechanisms of matrix metalloproteinases. Biological Chemistry, 378, 151–160.

    PubMed  CAS  Google Scholar 

  82. Giannelli, G., & Antonaci, S. (2002). Gelatinases and their inhibitors in tumor metastasis: From biological research to medical applications. Histology and Histopathology, 17, 339–345.

    PubMed  CAS  Google Scholar 

  83. Bjorklund, M., & Koivunen, E. (2005). Gelatinase-mediated migration and invasion of cancer cells. Biochimica et Biophysica Acta, 1755, 37–69.

    PubMed  Google Scholar 

  84. Hotary, K. B., Allen, E. D., Brooks, P. C., Datta, N. S., Long, M. W., & Weiss, S. J. (2003). Membrane type I matrix metalloproteinase usurps tumor growth control imposed by the three-dimensional extracellular matrix. Cell, 114, 33–45.

    Article  PubMed  CAS  Google Scholar 

  85. Stetler-Stevenson, W. G., & Yu, A. E. (2001). Proteases in invasion: Matrix metalloproteinases. Seminars in Cancer Biology, 11, 143–152.

    Article  PubMed  CAS  Google Scholar 

  86. Wolf, K., Wu, Y. I., Liu, Y., Geiger, J., Tam, E., Overall, C., et al. (2007). Multi-step pericellular proteolysis controls the transition from individual to collective cancer cell invasion. Nature Cell Biology, 9, 893–904.

    Article  PubMed  CAS  Google Scholar 

  87. Hernandez-Barrantes, S., Bernardo, M., Toth, M., & Fridman, R. (2002). Regulation of membrane type-matrix metalloproteinases. Seminars in Cancer Biology, 12, 131–138.

    Article  PubMed  CAS  Google Scholar 

  88. Zhao, H., Bernardo, M. M., Osenkowski, P., Sohail, A., Pei, D., Nagase, H., et al. (2004). Differential inhibition of membrane type 3 (MT3)-matrix metalloproteinase (MMP) and MT1-MMP by tissue inhibitor of metalloproteinase (TIMP)-2 and TIMP-3 rgulates pro-MMP-2 activation. Journal of Biological Chemistry, 279, 8592–8601.

    Article  PubMed  CAS  Google Scholar 

  89. Morrison, C. J., Butler, G. S., Bigg, H. F., Roberts, C. R., Soloway, P. D., & Overall, C. M. (2001). Cellular activation of MMP-2 (gelatinase A) by MT2-MMP occurs via a TIMP-2-independent pathway. Journal of Biological Chemistry, 276, 47402–47410.

    Article  PubMed  CAS  Google Scholar 

  90. Will, H., Atkinson, S. J., Butler, G. S., Smith, B., & Murphy, G. (1996). The soluble catalytic domain of membrane type 1 matrix metalloproteinase cleaves the propeptide of progelatinase A and initiates autoproteolytic activation. Regulation by TIMP-2 and TIMP-3. Journal of Biological Chemistry, 271, 17119–17123.

    Article  PubMed  CAS  Google Scholar 

  91. Miyamori, H., Takino, T., Kobayashi, Y., Tokai, H., Itoh, Y., Seiki, M., et al. (2001). Claudin promotes activation of pro-matrix metalloproteinase-2 mediated by membrane-type matrix metalloproteinases. Journal of Biological Chemistry, 276, 28204–28211.

    Article  PubMed  CAS  Google Scholar 

  92. Tortorella, M. D., Burn, T. C., Pratta, M. A., Abbaszade, I., Hollis, J. M., Liu, R., et al. (1999). Purification and cloning of aggrecanase-1: A member of the ADAMTS family of proteins. Science, 284, 1664–1666.

    Article  PubMed  CAS  Google Scholar 

  93. Gao, G., Plaas, A., Thompson, V. P., Jin, S., Zuo, F., & Sandy, J. D. (2004). ADAMTS4 (aggrecanase-1) activation on the cell surface involves C-terminal cleavage by glycosylphosphatidyl inositol-anchored membrane type 4-matrix metalloproteinase and binding of the activated proteinase to chondroitin sulfate and heparan sulfate on syndecan-1. Journal of Biological Chemistry, 279, 10042–10051.

    Article  PubMed  CAS  Google Scholar 

  94. Patwari, P., Gao, G., Lee, J. H., Grodzinsky, A. J., & Sandy, J. D. (2005). Analysis of ADAMTS4 and MT4-MMP indicates that both are involved in aggrecanolysis in interleukin-1-treated bovine cartilage. Osteoarthritis Cartilage, 13, 269–277.

    Article  PubMed  CAS  Google Scholar 

  95. Gauthier, M. C., Racine, C., Ferland, C., Flamand, N., Chakir, J., & Tremblay, G. M. (2003). Expression of membrane type-4 matrix metalloproteinase (metalloproteinase-17) by human eosinophils. International Journal of Biochemistry and Cell Biology, 35, 1667–1673.

    Article  PubMed  CAS  Google Scholar 

  96. Szabova, L., Yamada, S. S., Birkedal-Hansen, H., & Holmbeck, K. (2005). Expression pattern of four membrane-type matrix metalloproteinases in the normal and diseased mouse mammary gland. Journal of Cellular Physiology, 205, 123–132.

    Article  PubMed  CAS  Google Scholar 

  97. Nuttall, R. K., Pennington, C. J., Taplin, J., Wheal, A., Yong, V. W., Forsyth, P. A., et al. (2003). Elevated membrane-type matrix metalloproteinases in gliomas revealed by profiling proteases and inhibitors in human cancer cells. Molecular Cancer Research, 1, 333–345.

    PubMed  CAS  Google Scholar 

  98. Wallard, M. J., Pennington, C. J., Veerakumarasivamm, A., Burtt, G., Mills, I. G., Warren, A., et al. (2006). Comprehensive profiling and localisation of the matrix metalloproteinases in urothelial carcinoma. British Journal of Cancer, 94, 569–577.

    Article  PubMed  CAS  Google Scholar 

  99. Riddick, A. C., Shukla, C. J., Pennington, C. J., Bass, R., Nuttall, R. K., Hogan, A., et al. (2005). Identification of degradome components associated with prostate cancer progression by expression analysis of human prostatic tissues. British Journal of Cancer, 92, 2171–2180.

    Article  PubMed  CAS  Google Scholar 

  100. Noda, M., Oh, J., Takahashi, R., Kondo, S., Kitayama, H., & Takahashi, C. (2003). RECK: A novel suppressor of malignancy linking oncogenic signaling to extracellular matrix remodeling. Cancer and Metastasis Reviews, 22, 167–175.

    Article  PubMed  CAS  Google Scholar 

  101. Tortorella, M. D., Arner, E. C., Hills, R., Easton, A., Korte-Sarfaty, J., Fok, K., et al. (2004). Alpha2-macroglobulin is a novel substrate for ADAMTS-4 and ADAMTS-5 and represents an endogenous inhibitor of these enzymes. Journal of Biological Chemistry, 279, 17554–17561.

    Article  PubMed  CAS  Google Scholar 

  102. Plaisier, M., Kapiteijn, K., Koolwijk, P., Fijten, C., Hanemaaijer, R., Grimbergen, J. M., et al. (2004). Involvement of membrane-type matrix metalloproteinases (MT-MMPs) in capillary tube formation by human endometrial microvascular endothelial cells: Role of MT3-MMP. Journal of Clinical Endocrinology and Metabolism, 89, 5828–5836.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work is supported by NIH/National Cancer Institute Grant CA-61986 (to R.F.). The authors thank Ms. Sumayya Anjum for preparation of illustration in Fig. 2.

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  1. Department of Pathology, School of Medicine, and Proteases and Cancer Program, Barbara Ann Karmanos Cancer Institute, Wayne State University, 540 E. Canfield Ave., Detroit, MI, 48201, USA

    Anjum Sohail, Qing Sun, Huiren Zhao, M. Margarida Bernardo, Jin-Ah Cho & Rafael Fridman

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  1. Anjum Sohail
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  2. Qing Sun
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  3. Huiren Zhao
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Correspondence to Rafael Fridman.

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Sohail, A., Sun, Q., Zhao, H. et al. MT4-(MMP17) and MT6-MMP (MMP25), A unique set of membrane-anchored matrix metalloproteinases: properties and expression in cancer. Cancer Metastasis Rev 27, 289–302 (2008). https://doi.org/10.1007/s10555-008-9129-8

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