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Matrix Metalloproteinases: Biologic Activity and Clinical Implications

From the Departments of Hematology/Oncology and Cell Biology, Vanderbilt University Medical Center, and the E. Bronson Ingram Cancer Center at Vanderbilt University, Nashville, TN.

Address reprint requests to Lynn M. Matrisian, PhD, Department of Cell Biology, Vanderbilt University Medical Center, T-2220, MCN, 1161 21st Ave South, Nashville, TN 37232; email lynn.matrisian@ mcmail.vanderbilt.edu.

ABSTRACT

ABSTRACT: Tumor progression is a complex, multistage process by which a normal cell undergoes genetic changes that result in phenotypic alterations and the acquisition of the ability to spread and colonize distant sites in the body. Although many factors regulate malignant tumor growth and spread, interactions between a tumor and its surrounding microenvironment result in the production of important protein products that are crucial to each step of tumor progression. The matrix metalloproteinases (MMPs) are a family of degradative enzymes with clear links to malignancy. These enzymes are associated with tumor cell invasion of the basement membrane and stroma, blood vessel penetration, and metastasis. They have more recently been implicated in primary and metastatic tumor growth and angiogenesis, and they may even have a role in tumor promotion. This review outlines our current understanding of the MMP family, including the association of particular MMPs with malignant phenotypes and the role of MMPs in specific steps of the metastatic cascade. As scientific understanding of the MMPs has advanced, therapeutic strategies that capitalize on blocking the enzymes have rapidly developed. The preclinical and clinical evolution of the synthetic MMP inhibitors (MMPIs) is also examined, with the discussion encompassing important methodologic issues associated with determining clinical efficacy of MMPIs and other novel therapeutic agents.

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				M. Buchholz, A. Biebl, A. Neesse, M. Wagner, T. Iwamura, G. Leder, G. Adler, and T. M. Gress SERPINE2 (Protease Nexin I) Promotes Extracellular Matrix Production and Local Invasion of Pancreatic Tumors in Vivo Cancer Res., August 15, 2003; 63(16): 4945 - 4951. [Abstract] [Full Text] [PDF]

				I. Fajardo and G. Pejler Human Mast Cell {beta}-Tryptase Is a Gelatinase J. Immunol., August 1, 2003; 171(3): 1493 - 1499. [Abstract] [Full Text] [PDF]

				T. Pfefferkorn and G. A. Rosenberg Closure of the Blood-Brain Barrier by Matrix Metalloproteinase Inhibition Reduces rtPA-Mediated Mortality in Cerebral Ischemia With Delayed Reperfusion Stroke, August 1, 2003; 34(8): 2025 - 2030. [Abstract] [Full Text] [PDF]

				J. L. Lauer-Fields, T. Sritharan, M. S. Stack, H. Nagase, and G. B. Fields Selective Hydrolysis of Triple-helical Substrates by Matrix Metalloproteinase-2 and -9 J. Biol. Chem., May 9, 2003; 278(20): 18140 - 18145. [Abstract] [Full Text] [PDF]

				J. D. Cheng and L. M. Weiner Tumors and Their Microenvironments: Tilling the Soil: Commentary re: A. M. Scott et al., A Phase I Dose-Escalation Study of Sibrotuzumab in Patients with Advanced or Metastatic Fibroblast Activation Protein-positive Cancer. Clin. Cancer Res., 9: 1639-1647, 2003. Clin. Cancer Res., May 1, 2003; 9(5): 1590 - 1595. [Full Text] [PDF]

				M. K. King, M. L. Coker, A. Goldberg, J. H. McElmurray III, H. R. Gunasinghe, R. Mukherjee, M. R. Zile, T. P. O'Neill, and F. G. Spinale Selective Matrix Metalloproteinase Inhibition With Developing Heart Failure: Effects on Left Ventricular Function and Structure Circ. Res., February 7, 2003; 92(2): 177 - 185. [Abstract] [Full Text] [PDF]

				Y Hakoda, Y Ito, A Nagate, K Minemura, K Utsumi, M Aoshima, and K Ohyashiki Increased collagenase activity in macrophages from bronchial lavage as a diagnostic marker of non-small cell lung cancer Thorax, February 1, 2003; 58(2): 122 - 126. [Abstract] [Full Text] [PDF]

				J. Lu, H.-H. Chua, S.-Y. Chen, J.-Y. Chen, and C.-H. Tsai Regulation of Matrix Metalloproteinase-1 by Epstein-Barr Virus Proteins Cancer Res., January 1, 2003; 63(1): 256 - 262. [Abstract] [Full Text] [PDF]

				H. Enomoto, I. Inoki, K. Komiya, T. Shiomi, E. Ikeda, K.-i. Obata, H. Matsumoto, Y. Toyama, and Y. Okada Vascular Endothelial Growth Factor Isoforms and Their Receptors Are Expressed in Human Osteoarthritic Cartilage Am. J. Pathol., January 1, 2003; 162(1): 171 - 181. [Abstract] [Full Text] [PDF]

				C. Medina, S. Videla, A. Radomski, M. W. Radomski, M. Antolin, F. Guarner, J. Vilaseca, A. Salas, and J.-R. Malagelada Increased activity and expression of matrix metalloproteinase-9 in a rat model of distal colitis Am J Physiol Gastrointest Liver Physiol, January 1, 2003; 284(1): G116 - G122. [Abstract] [Full Text] [PDF]

				G. A. Rosenberg Matrix Metalloproteinases and Neuroinflammation in Multiple Sclerosis Neuroscientist, December 1, 2002; 8(6): 586 - 595. [Abstract] [PDF]

				C. J. Scotton, J. L. Wilson, K. Scott, G. Stamp, G. D. Wilbanks, S. Fricker, G. Bridger, and F. R. Balkwill Multiple Actions of the Chemokine CXCL12 on Epithelial Tumor Cells in Human Ovarian Cancer Cancer Res., October 15, 2002; 62(20): 5930 - 5938. [Abstract] [Full Text] [PDF]

				M. Shiraga, S. Yano, A. Yamamoto, H. Ogawa, H. Goto, T. Miki, K. Miki, H. Zhang, and S. Sone Organ Heterogeneity of Host-derived Matrix Metalloproteinase Expression and Its Involvement in Multiple-Organ Metastasis by Lung Cancer Cell Lines Cancer Res., October 15, 2002; 62(20): 5967 - 5973. [Abstract] [Full Text] [PDF]

				M. Arlt, C. Kopitz, C. Pennington, K. L. M. Watson, H.-W. Krell, W. Bode, B. Gansbacher, R. Khokha, D. R. Edwards, and A. Kruger Increase in Gelatinase-specificity of Matrix Metalloproteinase Inhibitors Correlates with Antimetastatic Efficacy in a T-Cell Lymphoma Model Cancer Res., October 1, 2002; 62(19): 5543 - 5550. [Abstract] [Full Text] [PDF]

				T. Vargo-Gogola, B. Fingleton, H. C. Crawford, and L. M. Matrisian Matrilysin (Matrix Metalloproteinase-7) Selects for Apoptosis-resistant Mammary Cells in Vivo Cancer Res., October 1, 2002; 62(19): 5559 - 5563. [Abstract] [Full Text] [PDF]

				J. Sanceau, D. D. Boyd, M. Seiki, and B. Bauvois Interferons Inhibit Tumor Necrosis Factor-alpha -mediated Matrix Metalloproteinase-9 Activation via Interferon Regulatory Factor-1 Binding Competition with NF-kappa B J. Biol. Chem., September 13, 2002; 277(38): 35766 - 35775. [Abstract] [Full Text] [PDF]

				D. Baillat, A. Begue, D. Stehelin, and M. Aumercier ETS-1 Transcription Factor Binds Cooperatively to the Palindromic Head to Head ETS-binding Sites of the Stromelysin-1 Promoter by Counteracting Autoinhibition J. Biol. Chem., August 9, 2002; 277(33): 29386 - 29398. [Abstract] [Full Text] [PDF]

				F. Samaniego, D. Young, C. Grimes, V. Prospero, M. Christofidou-Solomidou, H. M. DeLisser, O. Prakash, A. A. Sahin, and S. Wang Vascular Endothelial Growth Factor and Kaposi's Sarcoma Cells in Human Skin Grafts Cell Growth Differ., August 1, 2002; 13(8): 387 - 395. [Abstract] [Full Text] [PDF]

				S. Ito, T. Fukusato, T. Nemoto, H. Sekihara, Y. Seyama, and S. Kubota Coexpression of Glucose Transporter 1 and Matrix Metalloproteinase-2 in Human Cancers J Natl Cancer Inst, July 17, 2002; 94(14): 1080 - 1091. [Abstract] [Full Text] [PDF]

				Y. Mishima, Y. Matsumoto-Mishima, Y. Terui, M. Katsuyama, M. Yamada, M. Mori, Y. Ishizaka, K. Ikeda, J.-i. Watanabe, N. Mizunuma, et al. Leukemic Cell-Surface CD13/Aminopeptidase N and Resistance to Apoptosis Mediated by Endothelial Cells J Natl Cancer Inst, July 3, 2002; 94(13): 1020 - 1028. [Abstract] [Full Text] [PDF]

				E. Llano, G. Adam, A. M. Pendas, V. Quesada, L. M. Sanchez, I. Santamaria, S. Noselli, and C. Lopez-Otin Structural and Enzymatic Characterization of Drosophila Dm2-MMP, a Membrane-bound Matrix Metalloproteinase with Tissue-specific Expression J. Biol. Chem., June 21, 2002; 277(26): 23321 - 23329. [Abstract] [Full Text] [PDF]

				A. D. LAIRD, J. G. CHRISTENSEN, G. LI, J. CARVER, K. SMITH, X. XIN, K. G. MOSS, S. G. LOUIE, D. B. MENDEL, and J. M. CHERRINGTON SU6668 inhibits Flk-1/KDR and PDGFR{beta} in vivo, resulting in rapid apoptosis of tumor vasculature and tumor regression in mice FASEB J, May 1, 2002; 16(7): 681 - 690. [Abstract] [Full Text] [PDF]

				L. M. Coussens, B. Fingleton, and L. M. Matrisian Matrix Metalloproteinase Inhibitors and Cancer--Trials and Tribulations Science, March 29, 2002; 295(5564): 2387 - 2392. [Abstract] [Full Text] [PDF]