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Reduced Angiogenesis and Tumor Progression in Gelatinase A-deficient Mice¹

Shionogi Institute for Medical Science, Shionogi & Co., Ltd. [T. I., M. T., H. N.] and Discovery Research Laboratories II, Shionogi & Co., Ltd. [H. Y., T. Y.], Fukushima-ku, Osaka 553, and Institute for Virus Research, Kyoto University, Syogo-in, Sakyo-ku, Kyoto 606-01 [S. I.], Japan

Matrix proteolysis is thought to play a crucial role in several stages of tumor progression, including angiogenesis, and the invasion and metastasis of tumor cells. We investigated the specific role of gelatinase A (matrix metalloproteinase 2) on these events using gelatinase A-deficient mice. In these mice, tumor-induced angiogenesis was suppressed according to dorsal air sac assay. When B16-BL6 melanoma cells or Lewis lung carcinoma cells were implanted intradermally, the tumor volumes at 3 weeks after implantation in the gelatinase A-deficient mice decreased by 39% for B16-BL6 melanoma and by 24% for Lewis lung carcinoma (P < 0.03 for each tumor). The number of lung colonies of i.v. injections fell by 54% for B16-BL6 melanoma and 77% for Lewis lung carcinoma (P < 0.014 and P < 0.0015, respectively). These results indicated that host-derived gelatinase A plays an important role in angiogenesis and tumor progression, suggesting the usefulness of gelatinase A inhibitors for anticancer chemotherapy.

¹ This work was partly supported by a Grant-in-Aid for Scientific Research B from the Ministry of Education, Science, Sports and Culture of Japan (to S. I.).

² To whom requests for reprints should be addressed, at Shionogi Research Laboratory, Shionogi & Co., Ltd., 12-4, Sagisu 5-chome, Fukushima-ku, Osaka 553, Japan. Phone: (81) 6-458-5861; Fax: (81) 6-458-0987; E-mail: takeshi.itoh@shionogi.co.jp.

Received 9/ 9/97. Accepted 12/31/97.

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				M. P. Bendeck Macrophage Matrix Metalloproteinase-9 Regulates Angiogenesis in Ischemic Muscle Circ. Res., February 6, 2004; 94(2): 138 - 139. [Full Text] [PDF]

				D. D. Deo, N. G. Bazan, and J. D. Hunt Activation of Platelet-activating Factor Receptor-coupled G{alpha}q Leads to Stimulation of Src and Focal Adhesion Kinase via Two Separate Pathways in Human Umbilical Vein Endothelial Cells J. Biol. Chem., January 30, 2004; 279(5): 3497 - 3508. [Abstract] [Full Text] [PDF]

				A. M. Tester, M. Waltham, S.-J. Oh, S.-N. Bae, M. M. Bills, E. C. Walker, F. G. Kern, W. G. Stetler-Stevenson, M. E. Lippman, and E. W. Thompson Pro-Matrix Metalloproteinase-2 Transfection Increases Orthotopic Primary Growth and Experimental Metastasis of MDA-MB-231 Human Breast Cancer Cells in Nude Mice Cancer Res., January 15, 2004; 64(2): 652 - 658. [Abstract] [Full Text] [PDF]

				U. B. Hofmann, A. A. O. Eggert, K. Blass, E.-B. Brocker, and J. C. Becker Expression of Matrix Metalloproteinases in the Microenvironment of Spontaneous and Experimental Melanoma Metastases Reflects the Requirements for Tumor Formation Cancer Res., December 1, 2003; 63(23): 8221 - 8225. [Abstract] [Full Text] [PDF]

				K. L. Andarawewa, A. Boulay, R. Masson, C. Mathelin, I. Stoll, C. Tomasetto, M.-P. Chenard, M. Gintz, J.-P. Bellocq, and M.-C. Rio Dual Stromelysin-3 Function during Natural Mouse Mammary Tumor Virus-ras Tumor Progression Cancer Res., September 15, 2003; 63(18): 5844 - 5849. [Abstract] [Full Text] [PDF]

				B. S. Wiseman, M. D. Sternlicht, L. R. Lund, C. M. Alexander, J. Mott, M. J. Bissell, P. Soloway, S. Itohara, and Z. Werb Site-specific inductive and inhibitory activities of MMP-2 and MMP-3 orchestrate mammary gland branching morphogenesis J. Cell Biol., September 15, 2003; 162(6): 1123 - 1133. [Abstract] [Full Text] [PDF]

				H. Solberg, J. Rinkenberger, K. Dano, Z. Werb, and L. R. Lund A functional overlap of plasminogen and MMPs regulates vascularization during placental development Development, September 15, 2003; 130(18): 4439 - 4450. [Abstract] [Full Text] [PDF]

				S. Hayashidani, H. Tsutsui, M. Ikeuchi, T. Shiomi, H. Matsusaka, T. Kubota, K. Imanaka-Yoshida, T. Itoh, and A. Takeshita Targeted deletion of MMP-2 attenuates early LV rupture and late remodeling after experimental myocardial infarction Am J Physiol Heart Circ Physiol, August 7, 2003; 285(3): H1229 - H1235. [Abstract] [Full Text] [PDF]

				X. Miao, C. Yu, W. Tan, P. Xiong, G. Liang, W. Lu, and D. Lin A Functional Polymorphism in the Matrix Metalloproteinase-2 Gene Promoter (-1306C/T) Is Associated with Risk of Development but not Metastasis of Gastric Cardia Adenocarcinoma Cancer Res., July 15, 2003; 63(14): 3987 - 3990. [Abstract] [Full Text] [PDF]

				S. Harendza, D. H. Lovett, U. Panzer, Z. Lukacs, P. Kuhnl, and R. A. K. Stahl Linked Common Polymorphisms in the Gelatinase A Promoter Are Associated with Diminished Transcriptional Response to Estrogen and Genetic Fitness J. Biol. Chem., May 30, 2003; 278(23): 20490 - 20499. [Abstract] [Full Text] [PDF]

				L. Guedez, A. M. Rivera, R. Salloum, M. L. Miller, J. J. Diegmueller, P. M. Bungay, and W. G. Stetler-Stevenson Quantitative Assessment of Angiogenic Responses by the Directed in Vivo Angiogenesis Assay Am. J. Pathol., May 1, 2003; 162(5): 1431 - 1439. [Abstract] [Full Text] [PDF]

				S. Higashi and K. Miyazaki Identification of a Region of beta -Amyloid Precursor Protein Essential for Its Gelatinase A Inhibitory Activity J. Biol. Chem., April 11, 2003; 278(16): 14020 - 14028. [Abstract] [Full Text] [PDF]

				M. Trexler, K. Briknarova, M. Gehrmann, M. Llinas, and L. Patthy Peptide Ligands for the Fibronectin Type II Modules of Matrix Metalloproteinase 2 (MMP-2) J. Biol. Chem., March 28, 2003; 278(14): 12241 - 12246. [Abstract] [Full Text] [PDF]

				A. Collen, R. Hanemaaijer, F. Lupu, P. H. A. Quax, N. van Lent, J. Grimbergen, E. Peters, P. Koolwijk, and V. W. M. van Hinsbergh Membrane-type matrix metalloproteinase-mediated angiogenesis in a fibrin-collagen matrix Blood, March 1, 2003; 101(5): 1810 - 1817. [Abstract] [Full Text] [PDF]

				J.-M. Su, Y.-Q. Wei, L. Tian, X. Zhao, L. Yang, Q.-M. He, Y. Wang, Y. Lu, Y. Wu, F. Liu, et al. Active Immunogene Therapy of Cancer with Vaccine On the Basis of Chicken Homologous Matrix Metalloproteinase-2 Cancer Res., February 1, 2003; 63(3): 600 - 607. [Abstract] [Full Text] [PDF]

				Y.-J. YIN, Z. SALAH, M. MAOZ, S. C. E. RAM, S. OCHAYON, G. NEUFELD, S. KATZAV, and R. BAR-SHAVIT Oncogenic transformation induces tumor angiogenesis: a role for PAR1 activation FASEB J, February 1, 2003; 17(2): 163 - 174. [Abstract] [Full Text] [PDF]

				A. C. Lockhart, R. D. Braun, D. Yu, J. R. Ross, M. W. Dewhirst, J. S. Humphrey, S. Thompson, K. M. Williams, B. Klitzman, F. Yuan, et al. Reduction of Wound Angiogenesis in Patients Treated with BMS-275291, a Broad Spectrum Matrix Metalloproteinase Inhibitor Clin. Cancer Res., February 1, 2003; 9(2): 586 - 593. [Abstract] [Full Text] [PDF]

				L. Berglin, S. Sarman, I. van der Ploeg, B. Steen, Y. Ming, S. Itohara, S. Seregard, and A. Kvanta Reduced Choroidal Neovascular Membrane Formation in Matrix Metalloproteinase-2-Deficient Mice Invest. Ophthalmol. Vis. Sci., January 1, 2003; 44(1): 403 - 408. [Abstract] [Full Text] [PDF]

				C. Yu, K. Pan, D. Xing, G. Liang, W. Tan, L. Zhang, and D. Lin Correlation between a Single Nucleotide Polymorphism in the Matrix Metalloproteinase-2 Promoter and Risk of Lung Cancer Cancer Res., November 15, 2002; 62(22): 6430 - 6433. [Abstract] [Full Text] [PDF]

				V. Lambert, C. Munaut, M. Jost, A. Noel, Z. Werb, J.-M. Foidart, and J.-M. Rakic Matrix Metalloproteinase-9 Contributes to Choroidal Neovascularization Am. J. Pathol., October 1, 2002; 161(4): 1247 - 1253. [Abstract] [Full Text] [PDF]

				M. Hangai, N. Kitaya, J. Xu, C. K. Chan, J. J. Kim, Z. Werb, S. J. Ryan, and P. C. Brooks Matrix Metalloproteinase-9-Dependent Exposure of a Cryptic Migratory Control Site in Collagen is Required before Retinal Angiogenesis Am. J. Pathol., October 1, 2002; 161(4): 1429 - 1437. [Abstract] [Full Text] [PDF]

				I. Rivilis, M. Milkiewicz, P. Boyd, J. Goldstein, M. D. Brown, S. Egginton, F. M. Hansen, O. Hudlicka, and T. L. Haas Differential involvement of MMP-2 and VEGF during muscle stretch- versus shear stress-induced angiogenesis Am J Physiol Heart Circ Physiol, October 1, 2002; 283(4): H1430 - H1438. [Abstract] [Full Text] [PDF]

				T. Itoh, H. Matsuda, M. Tanioka, K. Kuwabara, S. Itohara, and R. Suzuki The Role of Matrix Metalloproteinase-2 and Matrix Metalloproteinase-9 in Antibody-Induced Arthritis J. Immunol., September 1, 2002; 169(5): 2643 - 2647. [Abstract] [Full Text] [PDF]

				S. Huang, M. Van Arsdall, S. Tedjarati, M. McCarty, W. Wu, R. Langley, and I. J. Fidler Contributions of Stromal Metalloproteinase-9 to Angiogenesis and Growth of Human Ovarian Carcinoma in Mice J Natl Cancer Inst, August 7, 2002; 94(15): 1134 - 1142. [Abstract] [Full Text] [PDF]

				P. R. Mertens, K. Steinmann, M. A. Alfonso-Jaume, A. En-Nia, Y. Sun, and D. H. Lovett Combinatorial Interactions of p53, Activating Protein-2, and YB-1 with a Single Enhancer Element Regulate Gelatinase A Expression in Neoplastic Cells J. Biol. Chem., July 5, 2002; 277(28): 24875 - 24882. [Abstract] [Full Text] [PDF]

				T. Sugino, T. Kusakabe, N. Hoshi, T. Yamaguchi, T. Kawaguchi, S. Goodison, M. Sekimata, Y. Homma, and T. Suzuki An Invasion-Independent Pathway of Blood-Borne Metastasis : A New Murine Mammary Tumor Model Am. J. Pathol., June 1, 2002; 160(6): 1973 - 1980. [Abstract] [Full Text] [PDF]

				J. H. Qi, Q. Ebrahem, K. Yeow, D. R. Edwards, P. L. Fox, and B. Anand-Apte Expression of Sorsby's Fundus Dystrophy Mutations in Human Retinal Pigment Epithelial Cells Reduces Matrix Metalloproteinase Inhibition and May Promote Angiogenesis J. Biol. Chem., April 12, 2002; 277(16): 13394 - 13400. [Abstract] [Full Text] [PDF]

				N. E. SOUNNI, L. DEVY, A. HAJITOU, F. FRANKENNE, C. MUNAUT, C. GILLES, C. DEROANNE, E. W. THOMPSON, J. M. FOIDART, and A. NOEL MT1-MMP expression promotes tumor growth and angiogenesis through an up-regulation of vascular endothelial growth factor expression FASEB J, April 1, 2002; 16(6): 555 - 564. [Abstract] [Full Text] [PDF]

				C Cuello, D Wakefield, and N Di Girolamo Neutrophil accumulation correlates with type IV collagenase/gelatinase activity in endotoxin induced uveitis Br J Ophthalmol, March 1, 2002; 86(3): 290 - 295. [Abstract] [Full Text] [PDF]

				E. I. Chen, S. J. Kridel, E. W. Howard, W. Li, A. Godzik, and J. W. Smith A Unique Substrate Recognition Profile for Matrix Metalloproteinase-2 J. Biol. Chem., February 1, 2002; 277(6): 4485 - 4491. [Abstract] [Full Text] [PDF]