Pro-MMP-9 activation by the MT1-MMP/MMP-2 axis and MMP-3: Role of TIMP-2 and plasma membranes

Biochemical and Biophysical Research Communications

Volumn 308, Issue 2, 2003, Pages 386-395

  Toth, Marta ^a   Chvyrkova, Irina ^a   Bernardo, M Margarida ^a   Hernandez Barrantes, Sonia ^a   Fridman, Rafael ^a  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Matrix metalloproteinases; Plasma membrane; Protease; Protease inhibitor; Zymogen

Indexed keywords

CELL SURFACE PROTEIN; ENZYME PRECURSOR; GELATINASE A; GELATINASE B; MATRIX METALLOPROTEINASE 14; PROTEINASE; PROTEINASE INHIBITOR; RECOMBINANT PROTEIN; TISSUE INHIBITOR OF METALLOPROTEINASE 2;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELL SURFACE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME LOCALIZATION; ENZYME MECHANISM; ENZYME REGULATION; HUMAN; HUMAN CELL; MEMBRANE BIOLOGY; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEINASE INHIBITION;

EID: 0041592501     PISSN: 0006291X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-291X(03)01405-0     Document Type: Article

References (54)

1. Werb Z. ECM and cell surface proteolysis: regulating cellular ecology. Cell. 91:1997;439-442.
2. Rafii S., Lyden D., Benezra R., Hattori K., Heissig B. Vascular and haematopoietic stem cells: novel targets for anti-angiogenesis therapy? Nat. Rev. Cancer. 2:2002;826-835.
3. Yu Q., Stamenkovic I. Localization of matrix metalloproteinase 9 to the cell surface provides a mechanism for CD44-mediated tumor invasion. Genes Dev. 13:1999;35-48.
4. Bergers G., Brekken R., McMahon G., Vu T.H., Itoh T., Tamaki K., Tanzawa K., Thorpe P., Itohara S., Werb Z., Hanahan D. Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis. Nat. Cell Biol. 2:2000;737-744.
5. Yana I., Seiki M. MT-MMPs play pivotal roles in cancer dissemination. Clin. Exp. Metastasis. 19:2002;209-215.
6. Zucker S., Pei D., Cao J., Lopez-Otin C. Membrane type-matrix metalloproteinases (MT-MMP). Curr. Top. Dev. Biol. 54:2003;1-74.
7. Hernandez-Barrantes S., Bernardo M., Toth M., Fridman R. Regulation of membrane type-matrix metalloproteinases. Semin. Cancer Biol. 12:2002;131-138.
8. Butler G.S., Butler M.J., Atkinson S.J., Will H., Tamura T., van Westrum S.S., Crabbe T., Clements J., d'Ortho M.P., Murphy G. The TIMP2 membrane type 1 metalloproteinase "receptor" regulates the concentration and efficient activation of progelatinase A. A kinetic study. J. Biol. Chem. 273:1998;871-880.
9. Strongin A.Y., Collier I., Bannikov G., Marmer B.L., Grant G.A., Goldberg G.I. Mechanism of cell surface activation of 72-kDa type IV collagenase. Isolation of the activated form of the membrane metalloprotease. J. Biol. Chem. 270:1995;5331-5338.
10. Hernandez-Barrantes S., Toth M., Bernardo M.M., Yurkova M., Gervasi D.C., Raz Y., Sang Q.A., Fridman R. 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. 275:2000;12080-12089.
11. Will H., Atkinson S.J., Butler G.S., Smith B., Murphy G. 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. J. Biol. Chem. 271:1996;17119-17123.
12. Jo Y., Yeon J., Kim H.J., Lee S.T. Analysis of tissue inhibitor of metalloproteinases-2 effect on pro-matrix metalloproteinase-2 activation by membrane-type 1 matrix metalloproteinase using baculovirus/insect-cell expression system. Biochem. J. 345(Pt 3):2000;511-519.
13. Bernardo M.M., Fridman R. TIMP-2 regulates MMP-2 activity in the extracellular environment after Pro-MMP-2 activation by MT1-MMP. Biochem. J. (Pt):2003.
14. Olson M.W., Gervasi D.C., Mobashery S., Fridman R. Kinetic analysis of the binding of human matrix metalloproteinase-2 and -9 to tissue inhibitor of metalloproteinase (TIMP)-1 and TIMP-2. J. Biol. Chem. 272:1997;29975-29983.
15. Bigg H.F., Morrison C.J., Butler G.S., Bogoyevitch M.A., Wang Z., Soloway P.D., Overall C.M. Tissue inhibitor of metalloproteinases-4 inhibits but does not support the activation of gelatinase A via efficient inhibition of membrane type 1-matrix metalloproteinase. Cancer Res. 61:2001;3610-3618.
16. Hernandez-Barrantes S., Shimura Y., Soloway P.D., Sang Q.A., Fridman R. Differential roles of TIMP-4 and TIMP-2 in pro-MMP-2 activation by MT1-MMP. Biochem. Biophys. Res. Commun. 281:2001;126-130.
17. Coussens L.M., Tinkle C.L., Hanahan D., Werb Z. MMP-9 supplied by bone marrow-derived cells contributes to skin carcinogenesis. Cell. 103:2000;481-490.
18. Vu T.H., Shipley J.M., Bergers G., Berger J.E., Helms J.A., Hanahan D., Shapiro S.D., Senior R.M., Werb Z. MMP-9/gelatinase B is a key regulator of growth plate angiogenesis and apoptosis of hypertrophic chondrocytes. Cell. 93:1998;411-422.
19. Hahn-Dantona E., Ruiz J.F., Bornstein P., Strickland D.K. The low density lipoprotein receptor-related protein modulates levels of matrix metalloproteinase 9 (MMP-9) by mediating its cellular catabolism. J. Biol. Chem. 276:2001;15498-15503.
20. Oh J., Takahashi R., Kondo S., Mizoguchi A., Adachi E., Sasahara R.M., Nishimura S., Imamura Y., Kitayama H., Alexander D.B., Ide C., Horan T.P., Arakawa T., Yoshida H., Nishikawa S., Itoh Y., Seiki M., Itohara S., Takahashi C., Noda M. The membrane-anchored MMP inhibitor RECK is a key regulator of extracellular matrix integrity and angiogenesis. Cell. 107:2001;789-800.
21. Olson M.W., Toth M., Gervasi D.C., Sado Y., Ninomiya Y., Fridman R. High affinity binding of latent matrix metalloproteinase-9 to the alpha2(IV) chain of collagen IV. J. Biol. Chem. 273:1998;10672-10681.
22. Toth M., Sado Y., Ninomiya Y., Fridman R. Biosynthesis of alpha2(IV) and alpha1(IV) chains of collagen IV and interactions with matrix metalloproteinase-9. J. Cell Physiol. 180:1999;131-139.
23. Okada Y., Gonoji Y., Naka K., Tomita K., Nakanishi I., Iwata K., Yamashita K., Hayakawa T. Matrix metalloproteinase 9 (92-kDa gelatinase/type IV collagenase) from HT 1080 human fibrosarcoma cells. Purification and activation of the precursor and enzymic properties. J. Biol. Chem. 267:1992;21712-21719.
24. Sorsa T., Salo T., Koivunen E., Tyynela J., Konttinen Y.T., Bergmann U., Tuuttila A., Niemi E., Teronen O., Heikkila P., Tschesche H., Leinonen J., Osman S., Stenman U.H. Activation of type IV procollagenases by human tumor-associated trypsin-2. J. Biol. Chem. 272:1997;21067-21074.
25. Menashi S., Fridman R., Desrivieres S., Lu H., Legrand Y., Soria C. Regulation of 92-kDa gelatinase B activity in the extracellular matrix by tissue kallikrein. Ann. NY Acad. Sci. 732:1994;466-468.
26. Coussens L.M., Raymond W.W., Bergers G., Laig-Webster M., Behrendtsen O., Werb Z., Caughey G.H., Hanahan D. Inflammatory mast cells up-regulate angiogenesis during squamous epithelial carcinogenesis. Genes Dev. 13:1999;1382-1397.
27. Han Y.P., Nien Y.D., Garner W.L. Tumor necrosis factor-alpha-induced proteolytic activation of pro-matrix metalloproteinase-9 by human skin is controlled by down-regulating tissue inhibitor of metalloproteinase-1 and mediated by tissue-associated chymotrypsin-like proteinase. J. Biol. Chem. 277:2002;27319-27327.
28. Ogata Y., Enghild J.J., Nagase H. Matrix metalloproteinase 3 (stromelysin) activates the precursor for the human matrix metalloproteinase 9. J. Biol. Chem. 267:1992;3581-3584.
29. Ramos-DeSimone N., Hahn-Dantona E., Sipley J., Nagase H., French D.L., Quigley J.P. Activation of matrix metalloproteinase-9 (MMP-9) via a converging plasmin/stromelysin-1 cascade enhances tumor cell invasion. J. Biol. Chem. 274:1999;13066-13076.
30. Fridman R., Toth M., Pena D., Mobashery S. Activation of progelatinase B (MMP-9) by gelatinase A (MMP-2). Cancer Res. 55:1995;2548-2555.
31. Knauper V., Smith B., Lopez-Otin C., Murphy G. Activation of progelatinase B (proMMP-9) by active collagenase-3 (MMP-13). Eur. J. Biochem. 248:1997;369-373.
32. Sang Q.X., Birkedal-Hansen H., Van Wart H.E. Proteolytic and non-proteolytic activation of human neutrophil progelatinase B. Biochim. Biophys. Acta. 1251:1995;99-108.
33. Uria J.A., Lopez-Otin C. Matrilysin-2, a new matrix metalloproteinase expressed in human tumors and showing the minimal domain organization required for secretion, latency, and activity. Cancer Res. 60:2000;4745-4751.
34. Ogata Y., Itoh Y., Nagase H. Steps involved in activation of the pro-matrix metalloproteinase 9 (progelatinase B)-tissue inhibitor of metalloproteinases-1 complex by 4-aminophenylmercuric acetate and proteinases. J. Biol. Chem. 270:1995;18506-18511.
35. Fuerst T.R., Earl P.L., Moss B. Use of a hybrid vaccinia virus-T7 RNA polymerase system for expression of target genes. Mol. Cell. Biol. 7:1987;2538-2544.
36. Fridman R., Fuerst T.R., Bird R.E., Hoyhtya M., Oelkuct M., Kraus S., Komarek D., Liotta L.A., Berman M.L., Stetler-Stevenson W.G. Domain structure of human 72-kDa gelatinase/type IV collagenase. Characterization of proteolytic activity and identification of the tissue inhibitor of metalloproteinase-2 (TIMP-2) binding regions. J. Biol. Chem. 267:1992;15398-15405.
37. Fridman R., Bird R.E., Hoyhtya M., Oelkuct M., Komarek D., Liang C.M., Berman M.L., Liotta L.A., Stetler-Stevenson W.G., Fuerst T.R. Expression of human recombinant 72 kDa gelatinase and tissue inhibitor of metalloproteinase-2 (TIMP-2): characterization of complex and free enzyme. Biochem. J. 289(Pt 2):1993;411-416.
38. Toth M., Gervasi D.C., Fridman R. Phorbol ester-induced cell surface association of matrix metalloproteinase-9 in human MCF10A breast epithelial cells. Cancer Res. 57:1997;3159-3167.
39. Olson M.W., Bernardo M.M., Pietila M., Gervasi D.C., Toth M., Kotra L.P., Massova I., Mobashery S., Fridman R. Characterization of the monomeric and dimeric forms of latent and active matrix metalloproteinase-9. Differential rates for activation by stromelysin 1. J. Biol. Chem. 275:2000;2661-2668.
40. Knight C.G. Fluorimetric assays of proteolytic enzymes. Methods Enzymol. 248:1995;18-34.
41. Toth M., Bernardo M.M., Gervasi D.C., Soloway P.D., Wang Z., Bigg H.F., Overall C.M., DeClerck Y.A., Tschesche H., Cher M.L., Brown S., Mobashery S., Fridman R. Tissue inhibitor of metalloproteinase (TIMP)-2 acts synergistically with synthetic matrix metalloproteinase (MMP) inhibitors but not with TIMP-4 to enhance the (membrane type 1)-MMP-dependent activation of pro-MMP-2. J. Biol. Chem. 275:2000;41415-41423.
42. Overall C.M. Molecular determinants of metalloproteinase substrate specificity: matrix metalloproteinase substrate binding domains, modules, and exosites. Mol. Biotechnol. 22:2002;51-86.
43. Knight C.G., Willenbrock F., Murphy G. A novel coumarin-labelled peptide for sensitive continuous assays of the matrix metalloproteinases. FEBS Lett. 296:1992;263-266.
44. Stanton H., Gavrilovic J., Atkinson S.J., d'Ortho M.P., Yamada K.M., Zardi L., Murphy G. The activation of ProMMP-2 (gelatinase A) by HT1080 fibrosarcoma cells is promoted by culture on a fibronectin substrate and is concomitant with an increase in processing of MT1-MMP (MMP-14) to a 45 kDa form. J. Cell Sci. 111:1998;2789-2798.
45. Toth M., Fridman R. Assesment of gelatinases by gelatin zymography. Brooks S.A., Schumacher U. Metastasis Research Protocols. 2001;163-174 Humana Press, Totowa, NJ.
46. English W.R., Velasco G., Stracke J.O., Knauper V., Murphy G. Catalytic activities of membrane-type6 matrix metalloproteinase (MMP25). FEBS Lett. 491:2001;137-142.
47. Kang T., Yi J., Guo A., Wang X., Overall C.M., Jiang W., Elde R., Borregaard N., Pei D. Subcellular distribution and cytokine- and chemokine-regulated secretion of leukolysin/MT6-MMP/MMP-25 in neutrophils. J. Biol. Chem. 276:2001;21960-21968.
48. Brown P.D., Levy A.T., Margulies I.M., Liotta L.A., Stetler-Stevenson W.G. Independent expression and cellular processing of Mr 72,000 type IV collagenase and interstitial collagenase in human tumorigenic cell lines. Cancer Res. 50:1990;6184-6191.
49. Gervasi D.C., Raz A., Dehem M., Yang M., Kurkinen M., Fridman R. Carbohydrate-mediated regulation of matrix metalloproteinase-2 activation in normal human fibroblasts and fibrosarcoma cells. Biochem. Biophys. Res. Commun. 228:1996;530-538.
50. Maquoi E., Frankenne F., Noel A., Krell H.W., Grams F., Foidart J.M. Type IV collagen induces matrix metalloproteinase 2 activation in HT1080 fibrosarcoma cells. Exp. Cell Res. 261:2000;348-359.
51. Baramova E.N., Bajou K., Remacle A., L'Hoir C., Krell H.W., Weidle U.H., Noel A., Foidart J.M. Involvement of PA/plasmin system in the processing of pro-MMP-9 and in the second step of pro-MMP-2 activation. FEBS Lett. 405:1997;157-162.
52. von Bredow D.C., Cress A.E., Howard E.W., Bowden G.T., Nagle R.B. Activation of gelatinase-tissue-inhibitors-of-metalloproteinase complexes by matrilysin. Biochem. J. 331(Pt 3):1998;965-972.
53. Zhao Y.G., Xiao A.Z., Newcomer R.G., Park H.I., Kang T., Chung L.W., Swanson M.G., Zhau H.E., Kurhanewicz J., Sang Q.X. Activation of pro-gelatinase B by endometase/matrilysin-2 promotes invasion of human prostate cancer cells. J. Biol. Chem. 278:2003;15056-15064.
54. Fridman R., Toth M., Chvyrkova I., Meroueh S.O., Mobashery S. Cell surface association of matrix metalloproteinase-9 (gelatinase B). Cancer Metastasis Rev. 22:2003;153-166.