Identification of a novel 82 kDa proMMP-9 species associated with the surface of leukaemic cells: (Auto-)catalytic activation and resistance to inhibition by TIMP-1

Biochemical Journal

Volumn 405, Issue 3, 2007, Pages 547-558

  Ries, Christian ^a   Pitsch, Thomas ^a   Mentele, Reinhard ^a   Zahler, Stefan ^a   Egea, Virginia ^a   Nagase, Hideaki ^b   Jochum, Marianne ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Acute myeloid leukaemia; Gelatinase B; Glycosylation; Matrix metalloproteinase (MMP); Tissue inhibitor of metalloproteinase (TIMP); Tumour cell invasion

Indexed keywords

AMINO ACIDS; CATALYST ACTIVITY; ESTERS; GLYCOSYLATION;

ACUTE MYELOID LEUKAEMIA; GELATINASE B; MATRIX METALLOPROTEINASE (MMP); TISSUE INHIBITOR OF METALLOPROTEINASE (TIMP); TUMOUR CELL INVASION;

CELLS;

AMINO ACID; COLLAGEN TYPE 4; ENZYME PRECURSOR; FIBRONECTIN; GELATIN; GELATINASE B; ILOMASTAT; TISSUE INHIBITOR OF METALLOPROTEINASE;

ACUTE GRANULOCYTIC LEUKEMIA; AMINO ACID SEQUENCE; ARTICLE; BIOTINYLATION; CELL INVASION; CELL MEMBRANE; CONTROLLED STUDY; ENZYME INHIBITION; ENZYME SPECIFICITY; FLUORESCENCE MICROSCOPY; GEL FILTRATION; GLYCOSYLATION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOPRECIPITATION; LEUKEMIA CELL; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN PURIFICATION; ZYMOGRAPHY;

AMINO ACID SEQUENCE; CATALYSIS; CELL LINE, TUMOR; ENZYME ACTIVATION; ENZYME PRECURSORS; FIBROSARCOMA; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; LEUKEMIA; MATRIX METALLOPROTEINASE 9; MEMBRANE PROTEINS; PROTEIN TRANSPORT; SUBSTRATE SPECIFICITY; TISSUE INHIBITOR OF METALLOPROTEINASE-1;

EID: 34547469532     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20070191     Document Type: Article

References (59)

1. Nagase, H. and Woessner, J. F. (1999) Matrix metalloproteinases. J. Biol. Chem. 274, 21491-21494
2. Stetler-Stevenson, W. G., Aznavoorian, S. and Liotta, L. A. (1993) Tumor cell interactions with the extracellular matrix during invasion and metastasis. Annu. Rev. Cell Biol. 9, 541-573
3. Egeblad, M. and Werb, Z. (2002) New functions for the matrix metalloproteinases in cancer progression. Nat. Rev. Cancer 2, 161-174
4. Woessner, J. F. and Nagase, H. (2000) Matrix metalloproteinases and TIMPs, Oxford University Press, Oxford
5. Ries, C. and Petrides, P. E. (1995) Cytokine regulation of matrix metalloproteinase activity and its regulatory dysfunction in disease. Biol. Chem. 376, 345-355
6. Yu, Q. and Stamenkovic, I. (2000) Cell surface-localized matrix metalloproteinase-9 proteolytically activates TGF-β and promotes tumor invasion and angiogenesis. Genes Dev. 14, 163-176
7. Van den Steen, P. E., Proost, P., Wuyts, A., van Damme, J. and Opdenakker, G. (2000) Neutrophil gelatinase B potentiates interleukin-8 tenfold by N-terminal processing, whereas it degrades CTAP-III, PF-4, and GRO-α and leaves RANTES and MCP-2 intact. Blood 96, 2673-2681
8. Schonbeck, U., Mach, F. and Libby, P. (1998) Generation of biologically active IL-1β by matrix metalloproteinases: a novel caspase-1-independent pathway of IL-1β processing. J. Immunol. 161, 3340-3346
9. Masure, S., Proost, P., van Damme, J. and Opdenakker, G. (1991) Purification and identification of 91-kDa neutrophil gelatinase: release by the activating peptide interleukin-8. Eur. J. Biochem. 198, 391-398
10. Opdenakker, G., Masure, S., Proost, P., Billiau, A. and van Damme, J. (1991) Natural human monocyte gelatinase and its inhibitor. FEBS Lett. 284, 73-78
11. Welgus, H. G., Campbell, E. J., Cury, J. D., Eisen, A. Z., Senior, R. M., Wilhelm, S. M. and Goldberg, G. I. (1990) Neutral metalloproteinases produced by human mononuclear phagocytes: enzyme profile, regulation, and expression during cellular development. J. Clin. Invest. 86, 1496-1502
12. Coussens, L. M., Tinkle, C. L., Hanahan, D. and Werb, Z. (2000) MMP-9 supplied by bone marrow-derived cells contributes to skin carcinogenesis. Cell 103, 481-490
13. Van Ranst, M., Norga, K., Masure, S., Proost, P., Vandekerckhove, F., Auwerx, J., van Damme, J. and Opdenakker, G. (1991) The cytokine-protease connection: identification of a 96-kD THP-1 gelatinase and regulation by interleukin-1 and cytokine inducers. Cytokine 3, 231-239
14. Ries, C., Kolb, H. and Petrides, P. E. (1994) Regulation of 92-kD gelatinase release in HL-60 leukemia cells: tumor necrosis factor-α as an autocrine stimulus for basal- and phorbol ester-induced secretion. Blood 83, 3638-3646
15. Ismair, M. G., Ries, C., Lottspeich, F., Zang, C., Kolb, H. J. and Petrides, P. E. (1998) Autocrine regulation of matrix metalloproteinase-9 gene expression and secretion by tumor necrosis factor-α (TNF-α) in NB4 leukemic cells: specific involvement of TNF receptor type 1. Leukemia 12, 1136-1143
16. Ries, C., Loher, F., Zang, C., Ismair, M. G. and Petrides, P. E. (1999) Matrix metalloproteinase production by bone marrow mononuclear cells from normal individuals and patients with acute and chronic myeloid leukemia or myelodysplastic syndromes. Clin. Cancer Res. 5, 1115-1124
17. Janowska-Wieczorek, A., Marquez, L. A., Matsuzaki, A., Hashmi, H. R., Larratt, L. M., Boshkov, L. M., Turner, A. R., Zhang, M. C., Edwards, D. R. and Kossakowska, A. E. (1999) Expression of matrix metalloproteinases (MMP-2 and -9) and tissue inhibitors of metalloproteinases (TIMP-1 and -2) in acute myelogenous leukaemia blasts: comparison with normal bone marrow cells. Br. J. Haematol. 105, 402-411
18. Klein, G., Vellenga, E., Fraaije, M. W., Kamps, W. A. and de Bont, E. S. (2004) The possible role of matrix metalloproteinase (MMP)-2 and MMP-9 in cancer, e.g. acute leukemia. Crit Rev. Oncol. Hematol. 50, 87-100
19. Bernhard, E. J., Gruber, S. B. and Muschel, R. J. (1994) Direct evidence linking expression of matrix metalloproteinase 9 (92-kDa gelatinase/collagenase) to the metastatic phenotype in transformed rat embryo cells. Proc. Natl. Acad. Sci. U.S.A. 91, 4293-4297
20. Hua, J. and Muschel, R. J. (1996) Inhibition of matrix metalloproteinase 9 expression by a ribozyme blocks metastasis in a rat sarcoma model system. Cancer Res. 56, 5279-5284
21. Wilhelm, S. M., Collier, I. E., Marmer, B. L., Eisen, A. Z., Grant, G. A. and Goldberg, G. I. (1989) SV40-transformed human lung fibroblasts secrete a 92-kDa type IV collagenase, which is identical to that secreted by normal human macrophages. J. Biol. Chem. 264, 17213-17221
22. Moll, U. M., Youngleib, G. L., Rosinski, K. B. and Quigley, J. P. (1990) Tumor promoter-stimulated Mr 92,000 gelatinase secreted by normal and malignant human cells: isolation and characterization of the enzyme from HT1080 tumor cells. Cancer Res. 50, 6162-6170
23. Nagase, H. (1997) Activation mechanisms of matrix metalloproteinases. Biol. Chem. 378, 151-160
24. Mazzieri, R., Masiero, L., Zanetta, L., Monea, S., Onisto, M., Garbisa, S. and Mignatti, P. (1997) Control of type IV collagenase activity by components of the urokinase-plasmin system: a regulatory mechanism with cell-bound reactants. EMBO J. 16, 2319-2332
25. Ramos-DeSimone, N., Hahn-Dantona, E., Sipley, J., Nagase, H., French, D. L. and Quigley, J. P. (1999) Activation of matrix metalloproteinase-9 (MMP-9) via a converging plasmin/stromelysin-1 cascade enhances tumor cell invasion. J. Biol. Chem. 274, 13066-13076
26. Toth, M., Gervasi, D. C. and Fridman, R. (1997) Phorbol ester-induced cell surface association of matrix metalloproteinase-9 in human MCF10A breast epithelial cells. Cancer Res. 57, 3159-3167
27. Partridge, C. A., Phillips, P. G., Niedbala, M. J. and Jeffrey, J. J. (1997) Localization and activation of type IV collagenase/gelatinase at endothelial focal contacts. Am. J. Physiol. 272, L813-L822
28. Stefanidakis, M., Ruohtula, T., Borregaard, N., Gahmberg, C. G. and Koivunen, E. (2004) Intracellular and cell surface localization of a complex between αMβ2 integrin and promatrix metalloproteinase-9 progelatinase in neutrophils. J. Immunol. 172, 7060-7068
29. Owen, C. A., Hu, B., Barrick, B. and Shapiro, S. D. (2003) Inducible expression of tissue inhibitor of metalloproteinases-resistant matrix metalloproteinase-9 on the cell surface of neutrophils. Am. J. Respir. Cell Mol. Biol. 29, 283-294
30. Rahat, M. A., Marom, B., Bitterman, H., Weiss-Cerem, L., Kinarty, A. and Lahat, N. (2006) Hypoxia reduces the output of matrix metalloproteinase-9 (MMP-9) in monocytes by inhibiting its secretion and elevating membranal association. J. Leukoc. Biol. 79, 706-718
31. Bourguignon, L. Y., Gunja-Smith, Z., Iida, N., Zhu, H. B., Young, L. J., Muller, W. J. and Cardiff, R. D. (1998) CD44v(3,8-10) is involved in cytoskeleton-mediated tumor cell migration and matrix metalloproteinase (MMP-9) association in metastatic breast cancer cells. J. Cell Physiol. 176, 206-215
32. Ellerbroek, S. M., Halbleib, J. M., Benavidez, M., Warmka, J. K., Wattenberg, E. V., Stack, M. S. and Hudson, L. G. (2001) Phosphatidylinositol 3-kinase activity in epidermal growth factor-stimulated matrix metalloproteinase-9 production and cell surface association, Cancer Res. 61, 1855-1861
33. Olson, M. W., Toth, M., Gervasi, D. C., Sado, Y., Ninomiya, Y. and Fridman, R. (1998) High affinity binding of latent matrix metalloproteinase-9 to the α2(IV) chain of collagen IV. J. Biol. Chem. 273, 10672-10681
34. Yu, Q. and Stamenkovic, I. (1999) Localization of matrix metalloproteinase 9 to the cell surface provides a mechanism for CD44-mediated tumor invasion. Genes Dev. 13, 35-48
35. Fridman, R., Toth, M., Chvyrkova, I., Meroueh, S. O. and Mobashery, S. (2003) Cell surface association of matrix metalloproteinase-9 (gelatinase B). Cancer Metastasis Rev. 22, 153-166
36. Stefanidakis, M. and Koivunen, E. (2006) Cell-surface association between matrix metalloproteinases and integrins: role of the complexes in leukocyte migration and cancer progression. Blood 108, 1441-1450
37. Bergers, G., Brekken, R., McMahon, G., Vu, T. H., Itoh, T., Tamaki, K., Tanzawa, K., Thorpe, P., Itohara, S., Werb, Z. and Hanahan, D. (2000) Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis. Nat. Cell Biol. 2, 737-744
38. Seiki, M. (2002) The cell surface: the stage for matrix metalloproteinase regulation of migration. Curr. Opin. Cell Biol. 14, 624-632
39. Kleiner, D. E. and Stetler-Stevenson, W. G. (1994) Quantitative zymography: detection of picogram quantities of gelatinases. Anal. Biochem. 218, 325-329
40. Heukeshoven, J. and Dernick, R. (1985) Simplified method for silver staining of proteins in polyacrylamide gels and the mechanism of the staining. Electrophoresis 6, 103
41. Ries, C., Lottspeich, F., Dittmann, K. H. and Petrides, P. E. (1996) HL-60 leukemia cells produce an autocatalytically truncated form of matrix metalloproteinase-9 with impaired sensitivity to inhibition by tissue inhibitors of metalloproteinases. Leukemia 10, 1520-1526
42. Dean, D. D., Martel Pelletier, J., Pelletier, J. P., Howell, D. S. and Woessner, J. F. J. (1989) Evidence for metalloproteinase and metalloproteinase inhibitor imbalance in human osteoarthritic cartilage. J. Clin. Invest. 84, 678-685
43. Eckerskorn, C., Mewes, W., Goretzki, H. and Lottspeich, F. (1988) A new siliconized-glass fiber as support for protein-chemical analysis of electroblotted proteins. Eur. J. Biochem. 176, 509-519
44. Eckerskorn, C. and Lottspeich, F. (2001) Internal amino acid sequence analysis of proteins separated by gel electrophoresis after tryptic digestion in polyacrylamide matrix. Chromatographia 28, 92-94
45. Meister, G., Buhler, D., Laggerbauer, B., Zobawa, M., Lottspeich, F. and Fischer, U. (2000) Characterization of a nuclear 20S complex containing the survival of motor neurons (SMN) protein and a specific subset of spliceosomal Sm proteins. Hum. Mol. Genet. 9, 1977-1986
46. Suzuki, K., Kan, C. C., Hung, W., Gehring, M. R., Brew, K. and Nagase, H. (1998) Expression of human pro-matrix metalloproteinase 3 that lacks the N-terminal 34 residues in Escherichia coli: autoactivation and interaction with tissue inhibitor of metalloproteinase 1 (TIMP-1). Biol. Chem. 379, 185-191
47. Huang, W., Meng, Q., Suzuki, K., Nagase, H. and Brew, K. (1997) Mutational study of the N-terminal domain of human tissue inhibitor of metalloproteinases 1 (TIMP-1) locates an inhibitory region for matrix metalloproteinases. J. Biol. Chem. 272, 22086-22091
48. Olson, M. W., Bernardo, M. M., Pietila, M., Gervasi, D. C., Toth, M., Kotra, L. P., Massova, I., Mobashery, S. and Fridman, R. (2000) 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, 2661-2668
49. Ogata, Y., Enghild, J. J. and Nagase, H. (1992) Matrix metalloproteinase 3 (stromelysin) activates the precursor for the human matrix metalloproteinase 9. J. Biol. Chem. 267, 3581-3584
50. Barrett, A. J. and Starkey, P. M. (1973) The interaction of α2-macroglobulin with proteinases: characteristics and specificity of the reaction, and a hypothesis concerning its molecular mechanism. Biochem. J. 133, 709-724
51. Basbaum, C. B. and Werb, Z. (1996) Focalized proteolysis: spatial and temporal regulation of extracellular matrix degradation at the cell surface. Curr. Opin. Cell Biol. 8, 731-738
52. Nguyen, M., Arkell, J. and Jackson, C. J. (1998) Active and tissue inhibitor of matrix metalloproteinase-free gelatinase B accumulates within human microvascular endothelial vesicles. J. Biol. Chem. 273, 5400-5404
53. Mattu, T. S., Royle, L., Langridge, J., Wormald, M. R., van den Steen, P. E., van Damme, J., Opdenakker, G., Harvey, D. J., Dwek, R. A. and Rudd, P. M. (2000) O-glycan analysis of natural human neutrophil gelatinase B using a combination of normal phase-HPLC and online tandem mass spectrometry: implications for the domain organization of the enzyme. Biochemistry 39, 15695-15704
54. Rudd, P. M., Mattu, T. S., Masure, S., Bratt, T., van den Steen, P. E., Wormald, M. R., Kuster, B., Harvey, D. J., Borregaard, N., van Damme, J. et al. (1999) Glycosylate of natural human neutrophil gelatinase B and neutrophil gelatinase B-associated lipocalin. Biochemistry 38, 13937-13950
55. van den Steen, P. E., van Aelst, I., Hvidberg, V., Piccard, H., Fiten, P., Jacobsen, C., Moestrup, S. K., Fry, S., Royle, L., Wormald, M. R. et al. (2006) The hemopexin and O-glycosylated domains tune gelatinase B/MMP-9 bioavailability via inhibition and binding to cargo receptors. J. Biol. Chem. 281, 18626-18637
56. Wu, Y. I., Munshi, H. G., Sen, R., Snipas, S. J., Salvesen, G. S., Fridman, R. and Stack, M. S. (2004) Glycosylate broadens the substrate profile of membrane type 1 matrix metalloproteinase. J. Biol. Chem. 279, 8278-8289
57. Fry, S. A., Steen, P. E., Royle, L., Wormald, M. R., Leathern, A. J., Opdenakker, G., McDonnell, J. M., Dwek, R. A. and Rudd, P. M. (2006) Cancer-associated glycoforms of gelatinase B exhibit a decreased level of binding to galectin-3. Biochemistry 45, 15249-15258
58. Olson, M. W., Gervasi, D. C., Mobashery, S. and Fridman, R. (1997) 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, 29975-29983
59. Galardy, R. E., Grobelny, D., Foellmer, H. G. and Fernandez, L. A. (1994) Inhibition of angiogenesis by the matrix metalloprotease inhibitor N-[2R-2-(hydroxamidocarbonymethyl)-4-methylpentanoyl]-L- tryptophan methylamide. Cancer Res. 54, 4715-4718