Inhibition of human MDA-MB-231 breast cancer cell invasion by matrix metalloproteinase 3 involves degradation of plasminogen

European Journal of Biochemistry

Volumn 269, Issue 18, 2002, Pages 4476-4483

  Farina, Antonietta R ^a   Tacconelli, Antonella ^a   Cappabianca, Lucia ^a   Gulino, Alberto ^b   Mackay, Andrew R ^a,c  

^a UNIVERSITY OF L'AQUILA   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

^c UNIVERSITY OF L'AQUILA   (Italy)

Author keywords

Angiostatin like; Invasion; Laminin; Matrix metalloproteinase 3; Plasminogen

Indexed keywords

ANGIOSTATIN; LAMININ; LYSINE; MATRIX METALLOPROTEINASE INHIBITOR; PLASMIN; PLASMINOGEN; PROUROKINASE; STROMELYSIN; TISSUE PLASMINOGEN ACTIVATOR;

ARTICLE; BASEMENT MEMBRANE; BINDING SITE; BREAST CARCINOMA; CANCER CELL CULTURE; CANCER INHIBITION; CANCER INVASION; CELL MEMBRANE; CONTROLLED STUDY; ENZYME ACTIVATION; HUMAN; HUMAN CELL; IN VITRO STUDY; KRINGLE DOMAIN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PURIFICATION;

ANGIOSTATINS; BREAST NEOPLASMS; CELL MEMBRANE; FEMALE; HUMANS; LAMININ; MATRIX METALLOPROTEINASE 3; NEOPLASM INVASIVENESS; PEPTIDE FRAGMENTS; PLASMINOGEN; TUMOR CELLS, CULTURED;

EID: 0036379273     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1432-1033.2002.03142.x     Document Type: Article

References (47)

1. Gusterson, B.A., Warburton, M.J., Mitchell, D., Ellison, M., Munro Neville, A. & Rudland, P.S. (1982) Distribution of myoepithelial cells and basement membrane proteins in the normal breast and in benign and malignant breast diseases. Cancer Res. 42, 4763-4770.
2. Guelstein, V.I., Tchypysheva, T.A., Ermilova, V.D. & Ljubimov, A.V. (1993) Myoepithelial and basement membrane antigens in benign and malignant breast tumors. Int. J. Cancer 53, 269-277.
3. Soini, Y., Hurskainen, T., Hoyta, M., Oikarinen, A. & Autio-Harmainen, H. (1994) 72 kDa and 92 kDa type IV collagenase, type IV collagen and laminin mRNAs in breast cancer: a study by in situ hybridisation. J. Histochem. Cytochem. 42, 945-951.
4. Lebbeau, A., Nerlich, A.G., Sauer, U., Lichtinghagen, R. & Lohrs, U. (1999) Tissue distribution of major matrix metalloproteinases and their transcripts in human breast carcinomas. Anti-cancer Res. 19, 4257-4264.
5. Basset, P., Bellocq, J.P., Wolf, C., Stoll, I., Huntin, P., Limbacker, J.M., Podhajcer, O.L., Chenard, M.P., Rio, M.C. & Chambon, P. (1990) A novel metalloproteinase gene specifically expressed in stromal cells of breast carcinomas. Nature 348, 699-704.
6. Remacle, A.G., Noel, A., Duggen, C., McDermott, E., O'Higgins, N., Foidart, J.M. & Duffy, M.J. (1998) Assay of metalloproteinases types 1, 2, 3 and 9 in breast cancer. Br. J. Cancer 77, 926-931.
7. Heppner, K.J., Matrisian, L.M., Jensen, R.A. & Rogers, W.H. (1996) Expression of most metalloproteinase family members in breast cancer represents a tumor induced host response. Am. J. Pathol. 149, 273-282.
8. Foekens, J.A., Schmitt, M., Van Putten, W.L.J., Peters, H.A., Bontenbal, M., Janicke, F. & Klijn, J.G.M. (1992) Prognostic value of urokinase-type plasminogen activator in 671 primary breast cancer patients. Cancer Res. 52, 6101-6105.
9. Janicke, F., Schmitt, M. & Graeff, H. (1991) Clinical relevance of urokinase-type and tissue type plasminogen activators and their type-1 inhibitor breast cancer. Semin. Thromb. Hemostasis 17, 303-332.
10. Grant, D.S., Kleinman, H.K., Leblond, C.P., Inoue, S., Chung, A.E. & Martin, G.R. (1985) The basement membrane-like matrix of the mouse EHS tumor. Immunohistochemical quantitation of six of its components. Am. J. Anat. 174, 387-398.
11. Kleinman, H.K., McGarvey, M.L., Hassell, J.R., Star, V.L., Cannon, F.B., Laurie, G.W. & Martin, G.R. (1986) Basement membrane complexes with biological activities. Biochemistry 25, 312-318.
12. Albini, A., Iwamoto, Y., Kleinman, H.K., Martin, G.R., Aaronson, S.A., Kozlowski, J.M. & McEwan. T.N. (1987) A rapid in vitro assay for quantitating the invasive potential of tumor cells. Cancer Res. 47, 3239-3245.
13. Repesh, L.A. (1989) A new in vitro assay for quantitating tumor cell invasion. Invasion Metastasis 9, 192-208.
14. Farina, A.R., Coppa, A., Tiberio, A., Tacconelli, A., Turco, A., Colletta, G., Gulino, A. & Mackay, A.R. (1998) Transforming growth factor beta-1 enhances the invasiveness of human MDA-MB-231 breast cancer cells by up-regulating urokinase activity. Int. J. Cancer 75, 721-730.
15. Ramos-DeSimone, N., Hahn-Dantona, E., Sipley, J., Nagase, H., French, D.L. & Quigley, J.P. (1999) Activation of matrix metalloproteinase-9 (MMP-9) via a converging plasmin/strom-elysin-1 cascade enhances tumor cell invasion. J. Biol. Chem. 274, 13066-13076.
16. Deryugina, E.I., Luo, G.X., Reisfeld, R.A., Bourdon, M.A. & Strongin, A. (1997) Tumor cell invasion through Matrigel is regulated by activated matrix metalloproteinase. Anticancer Res. 17, 3201-3210.
17. Mignatti, P. & Rifkin, D.B. (1993) Biology and biochemistry of proteinases in tumor invasion. Physiol. Rev. 73, 161-195.
18. Andreasen, P.A., Egelund, R. & Petersen, H.H. (2000) The plasminogen system in tumor growth, invasion and metastasis. Cell. Mol. Life Sci. 57, 25-40.
19. Woessner, F.J. & Nagase, H., eds (2000) Matrix Metalloproteinases and TIMPs. Oxford University Press, Oxford.
20. Stahl, A. & Mueller, B.M. (1994) Binding of urokinase to its receptor promotes migration and invasion of human melanoma cells in vitro. Cancer Res. 54, 3066-3071.
21. Tiberio, A., Farina, A.R., Tacconelli, A., Cappabianca, L., Gulino, A. & Mackay, A.R. (1997) Retinoic acid enhanced invasion through reconstituted basement membrane by human SK-N-SH neuroblastoma cells involves membrane associated tissue-type plasminogen activator. Int. J. Cancer 73, 740-748.
22. Bejarano, P.A., Noeòken, M.E., Suzuki, K., Hudson, B.G. & Nagase, H. (1988) Degradation of basement membranes by human matrix metalloproteinase-3 (stromelysin). Biochem. J. 256, 413-419.
23. Sternlicht, M.D., Lochter, A., Sympson, C.J., Huey, B., Rougier, J.-P., Gray, J.W., Pinkel, D., Bissell, M.J. & Werb, Z. (1999) The stromal proteinase MMP-3/stromelysin-1 promotes mammary tumorigenesis. Cell 98, 137-146.
24. Lecheter, A., Srebrow, A., Sympson, C.J., Terracio, N., Werb, Z. & Bissel M.J. (1997) Misregulation of stromelysin-1 expression in mouse mammary tumor cells accompanies acquisition of stromelysin-1-dependent invasive properties. J. Biol. Chem. 272, 5007-5015.
25. Chambers, A.F. & Matrisian, L.M. (1997) Changing views of the role of matrix metalloproteinases in metastasis. J. Natl Cancer Inst. 89, 1260-1270.
26. Nakopoulou, L., Giannopoulou, J., Gakiopoulou, H., Liapis, H., Tzonou, A. & Davaris, P.S. (1999) Matrix metalloproteinase-1 and -3 in breast cancer: correlation with progesterone receptors and other clinico-pathologic features. Hum. Pathol. 30, 436-442.
27. Brummer, O., Athar, S., Riethdorf, L., Loning, T. & Herbst, H. (1999) Matrix-metalloproteinase, 1, 2, 3, their tissue inhibitors, 1, 2 in benign and malignant breast lesions: an in situ hybridisation study. Virchows Arch. 435, 566-573.
28. Bisgaard, H.C., Mackay, A.R., Gomez, D.E., Ton, P.T., Thorgeirsson, S.S. & Thorgeirsson, U.P. (1999) Spontaneous metastasis of rat liver epithelial cells transformed with v-raf and v-raf/v-myc: association with different phenotypic properties. Invasion Metastasis 17, 240-250.
29. McCarthy, K., Maguire, T., McGreal, G., McDermott, E., O'Higgins, N. & Duffy, M.J. (1999) High levels of tissue inhibitor of metalloproteinase-1 predict poor outcome in patients with breast cancer. Int. J. Cancer 84, 44-48.
30. Visscher, D.W., Hoyhtya, M., Ottosen, S.K., Liang, C.M., Sarcar, F.H., Crissman, J.D. & Fridman, R. (1994) Enhanced expression of tissue inhibitor of metalloproteinases 2 (TIMP2) in the stroma of breast carcinomas correlates with tumour recurrence. Int. J. Cancer Res. 58, 1-6.
31. Lijnen, H.R. (2002) Matrix metalloproteinases and cellular fibrinolytic activity. Biochemistry (Moscow) 67, 92-98.
32. Lijnen, H.R., Ugwu, F., Bini, A. & Collen, D. (1998) Generation of an angiostatin-like fragment from plasminogen by stromelysin-1 (MMP-3). Biochemistry 37, 4699-4702.
33. Ugwu, F., Van Hoef, B., Bini, A., Collen, D. & Lijnen, H.R. (1998) Proteolytic cleavage of urokinase-type plasminogen activator by stromelysin-1 (MMP-3). Biochemistry 37, 7231-7236.
34. Orgel, D., Schroder, W., Hecker-Kia, A., Weithmann, K.U., Kolkenbrock, H. & Ulbrich, N. (1998) The cleavage of pro-urokinase type plasminogen activator by stromelysin-1. Clin. Chem. Lab. Med. 36, 697-702.
35. Ugwu, F., Lemmens, G., Collen, D. & Lijnen, H.R. (1999) Modulation of cell-associated plasminogen activation by stromelysin-1 (MMP-3). Thromb. Haemost. 82, 1127-1131.
36. Patterson, B.C. & Sang, Q.A. (1997) Angiostatin-converting enzyme activities of human matrilysin (MMP-7) and gelatinase B/type IV collagenase (MMP-9). J. Biol. Chem. 272, 28823-28825.
37. O'Reilly, M.S., Wiederschain, D., Stetler-Stevenson, W.G., Folkman, J. & Moses, M.A. (1999) Regulation of angiostatin production by matrix metalloproteinase-2 in a model of concomitant resistance. J. Biol. Chem. 274, 29568-29571.
38. O'Reilly, M.S., Holmgren, L., Shing, Y., Chen, C., Rosenthal, R.A., Moses, M., Lane, W.S., Cao, Y., Sage, E.H. & Folkman, J. (1994) Angiostatin: a novel angiogenesis inhibitor that mediates the suppression of metastases by a Lewis lung carcinoma. Cell 79, 315-328.
39. Fotouhi, N., Lugo, A., Visnick, M., Lusch, L., Walsky, R., Coffey, J.W. & Hanglow, A.C. (1994) Potent peptide inhibitors of stromelysin based on the pro-domain region of matrix metalloproteinases. J. Biol. Chem. 269, 30227-30231.
40. Odake, S., Morita, Y., Morikawa, T., Yoshida, N., Hori, H. & Nagai, Y. (1994) Inhibition of matrix metalloproteinases by peptidyl hydroxamic acids. Biochem. Biophys. Res. Commun. 199, 1442-1446.
41. Stack, S., Gately, S., Bafetti, L.M., Enghild, J.J. & Soff, G.A. (1999) Angiostatin inhibits endothelial and melanoma cellular invasion by blocking matrix enhanced plasminogen activation. Biochem. J. 340, 77-84.
42. Shi, G.Y., Wu, D.H. & Wu, H.L. (1991) Kringle domains and plasmin denaturation. Biochem. Biophys. Res. Commun. 178, 360-368.
43. Komorowicz, E., Kolev, K. & Machovich, R. (1998) Fibrinolysis with des-kringle derivatives of plasmin and its modulation by plasma protease inhibitors. Biochemistry 37, 9112-9118.
44. Arnoletti, J.P., Albo, D., Granick, M.S., Solomon, M.P., Castiglioni, A., Rothman, B.S. & Tuszynski, G.P. (1995) Thrombospondin and transforming growth factor-beta 1 increase expression of urokinase-type plasminogen activator and plasminogen activator inhibitor-1 in human MDA-MB-231 breast cancer cells. Cancer 76, 998-1005.
45. Ranson, M., Andronicos, N.M., O'Mullane, M.J. & Baker, M.S. (1998) Increased plasminogen binding is associated with metastatic breast cancer cells: differential expression of plasminogen binding proteins. Br. J. Cancer 77, 1586-1597.
46. Shi, G.Y. & Wu, H.L. (1988) Isolation and characterisation of microplasminogen. A low molecular weight form of plasminogen. J. Biol. Chem. 263, 17071-17075.
47. Wiman, B., Lijnen, H.R. & Collen, D. (1979) On the specific interaction between the lysine-binding sites in plasmin and complementary sites in alpha2-antiplasmin and in fibrinogen. Biochim. Biophys. Acta. 579, 142-154.