Induction of membrane-type-1 matrix metalloproteinase by epidermal growth factor-mediated signaling in gliomas

Neuro-Oncology

Volumn 6, Issue 3, 2004, Pages 188-199

  Van Meter, Timothy E ^a   Broaddus, William C ^a   Rooprai, Harcharan K ^b,c   Pilkington, Geoffrey J ^b,c   Fillmore, Helen L ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^b UNIVERSITY OF PORTSMOUTH   (United Kingdom)

^c Cell/Molec Neuro Oncol Res Group

Author keywords

[No Author keywords available]

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; 4 (3 CHLOROANILINO) 6,7 DIMETHOXYQUINAZOLINE; CYCLIN D1; EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; GELATINASE A; INTERSTITIAL COLLAGENASE; MATRIX METALLOPROTEINASE 14; MATRIX METALLOPROTEINASE 5; MESSENGER RNA; STROMELYSIN; UNCLASSIFIED DRUG;

ARTICLE; CANCER CELL CULTURE; CANCER INVASION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INDUCTION; ENZYME INHIBITION; GLIOMA; HUMAN; HUMAN CELL; POLYMERASE CHAIN REACTION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

CELL LINE, TUMOR; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INDUCTION; EPIDERMAL GROWTH FACTOR; GLIOMA; HUMANS; MATRIX METALLOPROTEINASE 15; MATRIX METALLOPROTEINASE 16; MATRIX METALLOPROTEINASES, MEMBRANE-ASSOCIATED; METALLOENDOPEPTIDASES; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION;

EID: 4344594952     PISSN: 15228517     EISSN: None     Source Type: Journal    
DOI: 10.1215/S1152851703000486     Document Type: Article

References (51)

1. Burke, R, Schooler, K., and Wiley, H.S. (2001) Regulation of epidermal growth factor receptor signaling by endocytosis and intracellular trafficking. Mol. Biol. Cell 12, 1897-1910.
2. CBTRUS. Central Brain Tumor Registry of the United States (2002-2003) Primary Brain Tumors in the United States: Statistical Report, 1995-1999 (available at http://www.cbtrus.org).
3. Davidson, B., Goldberg, I., Gotlieb, W.H., Kopolovic, J., Ben-Baruch, G., Nesland, J.M., Berner, A., Bryne, M., and Reich, R. (1999) High levels of MMP-2, MMP-9, MT1-MMP and TIMP-2 mRNA correlate with poor survival in ovarian carcinoma. Clin. Exp. Metastasis 17, 799-808.
4. Deryugina, E.I., Soroceanu, L., and 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.
5. d'Ortho, M.P., Will, H., Atkinson, S., Butler, G., Messent, A., Gavrilovic, J., Smith, B., Timpl, R., Zardi, L., and Murphy, G. (1997) Membrane-type matrix metalloproteinases 1 and 2 exhibit broad-spectrum proteolytic capacities comparable to many matrix metalloproteinases. Eur. J. Biochem. 250, 751-757.
6. Ekstrand, A.J., James, C.D., Cavenee, W.K., Seliger, B., Pettersson, R.F., and Collins, V.P. (1991) Genes for epidermal growth factor receptor, transforming growth factor alpha, and epidermal growth factor and their expression in human gliomas in vivo. Cancer Res. 51, 2164-2172.
7. Ekstrand, A.J., Sugawa, N., James, C.D., and Collins, V.P. (1992) Amplified and rearranged epidermal growth factor receptor genes in human glioblastomas reveal deletions of sequences encoding portions of the N- and/or C-terminal tails. Proc. Natl. Acad. Sci. USA 89, 4309-4313.
8. Ekstrand, A.J., Longo, N., Hamid, M.L.; Olson, J.J., Liu, L., Collins, V.P., and James, C.D. (1994) Functional characterization of an EGF receptor with a truncated extracellular domain expressed in glioblastomas with EGFR gene amplification. Oncogene 9, 2313-2320.
9. El-Obeid, A., Bongcam-Rudloff, E., Sorby, M., Ostman, A., Nister, M., and Westermark, B. (1997) Cell scattering and migration induced by autocrine transforming growth factor alpha in human glioma cells in vitro. Cancer Res. 57, 5598-5604.
10. Fillmore, H.L, Van Meter, T.E., and Broaddus, W.C. (2001) Membrane-type matrix metalloproteinases (MT-MMPs): Expression and function during glioma invasion. J. Neurooncol. 53, 187-202.
11. Galvez, B.G., Matias-Roman, S., Albar, J.P, Sanchez-Madrid, F, and 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.
12. Giese, A., and Westphal, M. (1996) Glioma invasion in the central nervous system. Neurosurgery 39, 235-252.
13. Gilles, C., Polette, M., Seiki, M., Birembaut, P., and Thompson, E.W. (1997) Implication of collagen type-I induced membrane-type 1-matrix metalloproteinase expression and matrix metalloproteinase-2 activation in the metastatic progression of breast carcinoma. Lab. Invest. 76, 651-660.
14. Harayama, T., Ohuchi, E., Aoki, T, Sato, H., Seiki, M., and Okada, Y. (1999) Shedding of membrane type 1 matrix metalloproteinase in a human breast carcinoma cell line. Jpn. J. Cancer Res. 90, 942-950.
15. Hernandez-Barrantes, S., Toth, M., Bernardo, M.M., Yurkova, M., Gervasi, D.C., Raz, Y., Sang, Q.A., and Fridman, R. (2000) Binding of active (57 kDa) membrane type 1-matrix metalloproteinase (MT1-MMP) to tissue inhibitor of metalloproteinase (TIMP)-2 regulates MT1-MMP processing and pro-MMP-2 activation. J. Biol. Chem. 275, 12080-12089.
16. Huang, H.S., Nagane, M., Klingbeil, C.K., Lin, H., Nishikawa, R., Ji, X.D., Huang, C.M., Gill, G.N., and Cavenee, W.K. (1997) The enhanced tumorigenic activity of a mutant epidermal growth factor receptor common in human cancers is mediated by threshold levels of constitutive tyrosine phosphorylation and unattenuated signaling. J. Biol. Chem. 272, 2927-2935.
17. Kajita, M., Itoh, Y., Chiba, T., Mori, H., Okada, A., Kinoh, H., and Seiki, M. (2001) Membrane-type 1 matrix metalloproteinase cleaves CD44 and promotes cell migration. J. Cell Biol. 153, 893-904.
18. Kheradmand, F., Rishi, K., and 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.
19. Knäuper, V., Will, H., Lopez-Otin, C., Smith, B., Atkinson, S.J., Stanton, H., Hembry, R.M., and Murphy, G. (1996) Cellular mechanisms for human procollagenase-3 (MMP-13) activation: Evidence that MT1-MMP (MMP-14) and gelatinase A (MMP-2) are able to generate active enzyme. J. Biol. Chem. 248, 17124-17131.
20. Knott, J.C., and Pilkington, G.J. (1990) A2B5 surface ganglioside binding distinguishes between two GFAP-positive clones from a human glioma-derived line. Neurosci. Lett 118, 52-56.
21. Knott, J.C., Edwards, A.J., Gullan, R.W., Clarke, T.M., and Pilkington, G.J. (1990) A human glioma cell line retaining expression of GAP and gangliosides, recognized by A2B5 and LB1 antibodies, after prolonged passage. Neuropathol. Appl. Neurobiol. 16, 489-500.
22. Knott, J.C., Clarke, TM., Sarkar C., and Pilkington, G.J. (1991) Characterisation of a glioma-derived cell line and clones which express GFAP at late passage. Brain Tumor Pathol. 8, 187-189.
23. Koochekpour, S., Merzak, A., and Pilkington, G.J. (1995) Growth factors and gangliosides stimulate laminin production by glioma cells in vitro. Neurosci. Lett. 186, 53-56.
24. Lampert, K., Machein, U., Machein, M.R., Conca, W., Peter, H.H., and Volk, B. (1998) Expression of matrix metalloproteinases and their tissue inhibitors in human brain tumors. Am. J. Pathol. 153, 429-437.
25. Leenstra, S., Bijlsma, E.K, Troost, D., Oosting, J., Westerveld, A., Bosch, D.A., and Hulsebos, T.J. (1994) Allele loss on chromosomes 10 and 17p and epidermal growth factor receptor gene amplification in human malignant astrocytoma related to prognosis. Br. J. Cancer 70, 684-689.
26. Llano, E., Pendas, A.M., Freije, J.P., Nakano, A., Knäuper, V., Murphy, G., and Lopez-Otin, C. (1999) Identification and characterization of human MT5-MMP, a new membrane-bound activator of progelatinase A overexpressed in brain tumors. Cancer Res. 59, 2570-2576.
27. Lohi, J., Lehti, K., Westermarck, J., Kahari, VM., and Keski-Oja, J. (1996) Regulation of membrane-type matrix metalloproteinase-1 expression by growth factors and phorbol 12-myristate 13-acetate. Eur. J. Biochem. 239, 239-247.
28. Maity, A., Pore, N., Lee, J., Solomon, D., and O'Rourke, D.M. (2000) Epidermal growth factor receptor transcriptionally up-regulates vascular endothelial growth factor expression in human glioblastoma cells via a pathway involving phosphatidylinositol 3′-kinase and distinct from that induced by hypoxia. Cancer Res. 60, 5879-5886.
29. Matsumoto, S., Katoh, M., Saito, S., Watanabe, T, and Masuho, Y. (1997) Identification of soluble type of membrane-type matrix metalloproteinase-3 formed by alternatively spliced mRNA. Biochim. Biophys. Acta 1354, 159-170.
30. Merzak, A., Koochekpour, S., Dkhissi, F., Raynal, S., Lawrence, D., and Pilkington, G.J. (1995) Synergism between growth factors in the control of glioma cell proliferation, migration and invasion in vitro. Int. J. Oncol. 6, 1079-1085.
31. Miyagi, N., Kato, S., Terasaki, M., Shigemori, M., and Morimatsu, M. (1998) Fibroblast growth factor-2 and -9 regulate proliferation and production of matrix metalloproteinases in human gliomas. Int. J. Oncol. 12, 1085-1090.
32. Monaghan, M., Mulligan, K.A., Gillespie, H., Trimble, A., Winter, P., Johnston, P.G., and McCormick, D. (2000) Epidermal growth factor upregulates CD44-dependent astrocytoma invasion in vitro. J. Pathol. 192, 519-525.
33. Nakada, M., Kita, D., Futami, K., Yamashita, J., Fujimoto, N., Sato, H., and Okada, Y. (2001) Roles of membrane type 1 matrix metalloproteinase and tissue inhibitor of metalloproteinases 2 in invasion and dissemination of human malignant glioma. J. Neurosurg. 94, 464-473.
34. Nakano, A., Tani, E., Miyazakai, K., Yamamoto, Y., and Furuyama, J.-I. (1995) Matrix metallo-proteinases and tissue inhibitors of metallo-proteinases in human gliomas. J. Neurosurg. 83, 298-307.
35. Nishikawa, R., Ji, X.D., Harmon, R.C., Lazar, C.S., Gill, G.N., Cavenee, W.K., and Huang, H.J. (1994) A mutant epidermal growth factor receptor common in human glioma confers enhanced tumorigenicity. Proc. Natl. Acad. Sci. USA 91, 7727-7731.
36. Okada, Y., Hurwitz, E.E., Esposito, J.M., Brower, M.A., Nutt, C.L., and Louis, D.N. (2003) Selection pressures of TP53 mutation and microenvironmental location influence epidermal growth factor receptor gene amplification in human glioblastomas. Cancer Res. 63, 413-416.
37. Overall, C.M., Tam, E., McQuibban, G.A., Morrison, C., Wallon, U.M., Bigg, H.F., King, A.E., and Roberts, C.R. (2000) Domain interactions in the gelatinase A.TIMP-2.MT1-MMP activation complex. The ectodomain of the 44-kDa form of membrane type-1 matrix metalloproteinase does not modulate gelatinase A activation. J. Biol. Chem. 275, 39497-39506.
38. Prigent, S.A., Nagane, M., Lin, H., Huvar, I., Boss, G.R., Feramisco, J.R., Cavenee, W.K., and Huang, H.-J.S. (1996) Enhanced tumorigenic behavior of glioblastoma cells expressing a truncated epidermal growth factor receptor is mediated through the Ras-Shc-Grb-2 pathway. J. Biol. Chem. 271, 25639-25645.
39. Puente, X.S., Pendas, A.M., Llano, E., Velasco, G., and Lopez-Otin, C. (1996) Molecular cloning of a novel membrane-type matrix metalloproteinase from a human breast carcinoma. Cancer Res. 56, 944-949.
40. Rooprai, H.K., Rucklidge, G.J., Panou, C., and Pilkington, G.J. (2000) The effects of exogenous growth factors on matrix metalloproteinase secretion by human brain tumour cells. Br. J. Cancer 82, 52-55.
41. Sato, H., Takino, T., Okada, Y, Cao, J., Shinagawa, A., Yamamoto, E., and Seiki, M. (1994) A matrix metalloproteinase expressed on the surface of invasive tumour cells. Nature 370, 61-65.
42. Sawaya, R.E., Yamamoto, M., Gokaslan, Z.L., Wang, S.W., Mohanam, S., Fuller, G.N., McCutcheon, I.E., Stetler-Stevenson, W.G., Nicolson, G.L., and Rao, J.S. (1996) Expression and localization of 72 kDa type IV collagenase (MMP-2) in human malignant gliomas in vivo. Clin. Exp. Metastasis 14, 35-42.
43. Shofuda, K.-I., Moriyama, K., Nishihashi, A., Higashi, S., Mizushima, H., Yasumitsu, H., Miki, K., Sato, H., Seiki, M., and Miyazaki, K. (1998) Role of tissue inhibitor of metalloproteinases-2 (TIMP-2) in regulation of progelatinase A activation catalyzed by membrane-type matrix metalloproteinase-1 (MT1 -MMP) in human cancer cells. J. Biochem. 124, 462-470,
44. Takino, T, Sato, H., Shinagawa, A., and 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. J. Biol. Chem. 270, 23013-23120.
45. Van Meter, T.E., Rooprai, H.K., Kibble, M.M., Fillmore, H.L., Broaddus, W.C., and Pilkington, G.J. (2001) The role of matrix metalloproteinase genes in glioma invasion: Co-dependent and interactive proteolysis. J. Neurooncol. 53, 213-235.
46. Velasco, G., Cal, S., Merlos-Suarez, A., Ferrando, A.A., Alvarez, S., Nakano, A., Arribas, J., and Lopez-Otin, C. (2000) Human MT6-matrix metalloproteinase: Identification, progelatinase A activation, and expression in brain tumors. Cancer Res. 60, 877-882.
47. von Deimling, A., Louis, D.N., von Ammon, K., Petersen, I., Hoell, T., Chung, R.Y, Martuza, R.L., Schoenfeld, D.A., Yasargil, M.G., Wiestler, O.D., and Seizinger, B.R. (1992) Association of epidermal growth factor receptor gene amplification with loss of chromosome 10 in human glioblastoma multiforme. J. Neurosurg. 77, 295-301.
48. Watabe, T., Yoshida, K., Shindoh, M., Kaya, M., Fujikawa, K., Sato, H., Seiki, M., Ishii, S., and Fujinaga, K. (1998) The Ets-1 and Ets-2 transcription factors activate the promoters for invasion-associated urokinase and collagenase genes in response to epidermal growth factor. Int. J. Cancer 77, 128-137.
49. Will, H., and Hinzmann, B. (1995) cDNA sequence and mRNA tissue distribution of a novel human matrix metalloproteinase with a potential transmembrane segment. Eur. J. Biochem. 231, 602-608.
50. Yamamoto, M., Mohanam, S., Sawaya, R., Fuller, G.N., Seiki, M., Sato, H., Gokaslan, Z.L., Liotta, L.A., Nicolson, G.L., and Rao, J.S. (1996) Differential expression of membrane-type matrix metalloproteinase and its correlation with gelatinase A activation in human malignant brain tumors in vivo and in vitro. Cancer Res. 56, 384-392.
51. Yu, M., Bowden, E.T., Sitlani, J., Sato, H., Seiki, M., Mueller, S.C., and Thompson, E.W. (1997) Tyrosine phosphorylation mediates ConA-induced membrane type 1-matrix metalloproteinase expression and matrix metalloproteinase-2 activation in MDA-MB-231 human breast carcinoma cells. Cancer Res. 57, 5028-5032.