Recruitment of matrix metalloproteinase-9 (MMP-9) to the fibroblast cell surface by lysyl hydroxylase 3 (LH3) triggers transforming growth factor-β (TGF-β) activation and fibroblast differentiation

Journal of Biological Chemistry

Volumn 290, Issue 22, 2015, Pages 13763-13778

  Dayer, Cynthia ^a   Stamenkovic, Ivan ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD VESSELS; CELL CULTURE; CELL MEMBRANES; CELLS; CHEMICAL ACTIVATION; CYTOLOGY; ENZYME ACTIVITY; ENZYME INHIBITION; MUSCLE; PROTEINS; TUMORS;

FIBROBLAST CELLS; FUNCTIONAL ASSAYS; MATRIX METALLOPROTEINASE 9 (MMP 9); MATRIX METALLOPROTEINASES; MYOFIBROBLASTS; SMOOTH MUSCLE ACTINS; TRANSFORMING GROWTH FACTORS; TUMOR PROGRESSIONS;

FIBROBLASTS;

ALPHA SMOOTH MUSCLE ACTIN; FIBRONECTIN; GELATINASE B; LYSYL HYDROXYLASE 3; PROCOLLAGEN LYSINE 2 OXOGLUTARATE 5 DIOXYGENASE; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; LYSYL HYDROXYLASE 3, HUMAN; MMP9 PROTEIN, HUMAN; RECOMBINANT PROTEIN;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL SURFACE; CONTROLLED STUDY; EMBRYO; FEMALE; FIBROBLAST; GENE ACTIVATION; HUMAN; HUMAN CELL; MYOFIBROBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; TUMOR GROWTH; ANIMAL; CELL MEMBRANE; CELL SEPARATION; CHO CELL LINE; CRICETULUS; CYTOLOGY; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; HAMSTER; HEK293 CELL LINE; LIVER; METABOLISM; TUMOR CELL LINE; TUMOR MICROENVIRONMENT;

ANIMALS; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL MEMBRANE; CELL SEPARATION; CHO CELLS; CRICETINAE; CRICETULUS; FIBROBLASTS; FLOW CYTOMETRY; HEK293 CELLS; HUMANS; LIVER; MATRIX METALLOPROTEINASE 9; MICROSCOPY, FLUORESCENCE; MYOFIBROBLASTS; PROCOLLAGEN-LYSINE, 2-OXOGLUTARATE 5-DIOXYGENASE; RECOMBINANT PROTEINS; TRANSFORMING GROWTH FACTOR BETA; TUMOR MICROENVIRONMENT;

EID: 84930677103     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.622274     Document Type: Article

References (37)

1. Pietras, K., and Ostman, A. (2010) Hallmarks of cancer: interactions with the tumor stroma. Exp. Cell Res. 316, 1324-1331
2. Mueller, M. M., and Fusenig, N. E. (2004) Friends or foes - bipolar effects of the tumour stroma in cancer. Nat. Rev. Cancer 4, 839-849
3. Bhowmick, N. A., Neilson, E. G., and Moses, H. L. (2004) Stromal fibroblasts in cancer initiation and progression. Nature 432, 332-337
4. Stamenkovic, I. (2000) Matrix metalloproteinases in tumor invasion and metastasis. Sem. Cancer Biol. 10, 415-433
5. Stamenkovic, I. (2003) Extracellular matrix remodelling: the role of matrix metalloproteinases. J. Pathol. 200, 448-464
6. 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
7. 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
8. Xu, X., Chen, Z., Wang, Y., Yamada, Y., and Steffensen, B. (2005) Functional basis for the overlap in ligand interactions and substrate specificities of matrix metalloproteinases-9 and -2. Biochem. J. 392, 127-134
9. Collier, I. E., Krasnov, P. A., Strongin, A. Y., Birkedal-Hansen, H., and Goldberg, G. I. (1992) Alanine scanning mutagenesis and functional analysis of the fibronectin-like collagen-binding domain from human 92-kDa type IV collagenase. J. Biol. Chem. 267, 6776-6781
10. Steffensen, B., Wallon, U. M., and Overall, C. M. (1995) Extracellular matrix binding properties of recombinant fibronectin type II-like modules of human 72-kDa gelatinase/type IV collagenase. High affinity binding to native type I collagen but not native type IV collagen. J. Biol. Chem. 270, 11555-11566
11. Overall, C. M. (2002) Molecular determinants of metalloproteinase substrate specificity: matrix metalloproteinase substrate binding domains, modules, and exosites. Mol. Biotechnol. 22, 51-86
12. Roomi, M. W., Monterrey, J. C., Kalinovsky, T., Rath, M., and Niedzwiecki, A. (2009) Patterns of MMP-2 and MMP-9 expression in human cancer cell lines. Oncol. Rep. 21, 1323-1333
13. Malla, N., Sjøli, S., Winberg, J. O., Hadler-Olsen, E., and Uhlin-Hansen, L. (2008) Biological and pathobiological functions of gelatinase dimers and complexes. Connect. Tissue Res. 49, 180-184
14. Deryugina, E. I., and Quigley, J. P. (2006) Matrix metalloproteinases and tumor metastasis. Cancer Metastasis Rev. 25, 9-34
15. 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
16. Toth, M., Chvyrkova, I., Bernardo, M. M., Hernandez-Barrantes, S., and Fridman, R. (2003) Pro-MMP-9 activation by the MT1-MMP/MMP-2 axis and MMP-3: role of TIMP-2 and plasma membranes. Biochem. Biophys. Res. Commun. 308, 386-395
17. 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
18. 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
19. Mira, E., Lacalle, R. A., Buesa, J. M., de Buitrago, G. G., Jiménez-Baranda, S., Gómez-Moutón, C., Martínez-A, C., and Mañes, S. (2004) Secreted MMP9 promotes angiogenesis more efficiently than constitutive active MMP9 bound to the tumor cell surface. J. Cell Sci. 117, 1847-1857
20. Heikkinen, J., Risteli, M., Wang, C., Latvala, J., Rossi, M., Valtavaara, M., and Myllylä, R. (2000) Lysyl hydroxylase 3 is a multifunctional protein possessing collagen glucosyltransferase activity. J. Biol. Chem. 275, 36158-36163
21. Salo, A. M., Wang, C., Sipilä, L., Sormunen, R., Vapola, M., Kervinen, P., Ruotsalainen, H., Heikkinen, J., and Myllylä, R. (2006) Lysyl hydroxylase 3 (LH3) modifies proteins in the extracellular space, a novel mechanism for matrix remodeling. J. Cell. Physiol. 207, 644-653
22. Abe, M., Harpel, J. G., Metz, C. N., Nunes, I., Loskutoff, D. J., and Rifkin, D. B. (1994) An assay for transforming growth factor-β using cells transfected with a plasminogen activator inhibitor-1 promoter-luciferase construct. Anal. Biochem. 216, 276-284
23. Hahn-Dantona, E., Ruiz, J. F., Bornstein, P., and Strickland, D. K. (2001) The low density lipoprotein receptor-related protein modulates levels of matrix metalloproteinase 9 (MMP-9) by mediating its cellular catabolism. J. Biol. Chem. 276, 15498-15503
24. 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., Wallis, R., Rudd, P. M., Dwek, R. A., and Opdenakker, G. (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
25. Takahashi, C., Sheng, Z., Horan, T. P., Kitayama, H., Maki, M., Hitomi, K., Kitaura, Y., Takai, S., Sasahara, R. M., Horimoto, A., Ikawa, Y., Ratzkin, B. J., Arakawa, T., and Noda, M. (1998) Regulation of matrix metalloproteinase-9 and inhibition of tumor invasion by the membrane-anchored glycoprotein RECK. Proc. Natl. Acad. Sci. U.S.A. 95, 13221-13226
26. Redondo-Muñoz, J., Ugarte-Berzal, E., García-Marco, J. A., del Cerro, M. H., Van den Steen, P. E., Opdenakker, G., Terol, M. J., and García-Pardo, A. (2008) α4β1 integrin and 190-kDa CD44v constitute a cell surface docking complex for gelatinase B/MMP-9 in chronic leukemic but not in normal B cells. Blood 112, 169-178
27. Behrendt, N. (2004) The urokinase receptor (uPAR) and the uPAR-associated protein (uPARAP/Endo180): membrane proteins engaged in matrix turnover during tissue remodeling. Biol. Chem. 385, 103-136
28. Brinckerhoff, C. E., and Matrisian, L. M. (2002) Matrix metalloproteinases: a tail of a frog that became a prince. Nat. Rev. Mol. Cell Biol. 3, 207-214
29. Coussens, L. M., Fingleton, B., and Matrisian, L. M. (2002) Matrix metalloproteinase inhibitors and cancer: trials and tribulations. Science 295, 2387-2392
30. Dufour, A., Sampson, N. S., Li, J., Kuscu, C., Rizzo, R. C., Deleon, J. L., Zhi, J., Jaber, N., Liu, E., Zucker, S., and Cao, J. (2011) Small-molecule anticancer compounds selectively target the hemopexin domain of matrix metalloproteinase-9. Cancer Res. 71, 4977-4988
31. Dufour, A., Zucker, S., Sampson, N. S., Kuscu, C., and Cao, J. (2010) Role of matrix metalloproteinase-9 dimers in cell migration: design of inhibitory peptides. J. Biol. Chem. 285, 35944-35956
32. Lauer-Fields, J. L., Whitehead, J. K., Li, S., Hammer, R. P., Brew, K., and Fields, G. B. (2008) Selective modulation of matrix metalloproteinase 9 (MMP-9) functions via exosite inhibition. J. Biol. Chem. 283, 20087-20095
33. Myllylä, R., Wang, C., Heikkinen, J., Juffer, A., Lampela, O., Risteli, M., Ruotsalainen, H., Salo, A., and Sipilä, L. (2007) Expanding the lysyl hydroxylase toolbox: new insights into the localization and activities of lysyl hydroxylase 3 (LH3). J. Cell. Physiol. 212, 323-329
34. Wang, C., Kovanen, V., Raudasoja, P., Eskelinen, S., Pospiech, H., and Myllylä, R. (2009) The glycosyltransferase activities of lysyl hydroxylase 3 (LH3) in the extracellular space are important for cell growth and viability. J. Cell. Mol. Med. 13, 508-521
35. Kalluri, R., and Zeisberg, M. (2006) Fibroblasts in cancer. Nat. Rev. Cancer 6, 392-401
36. Cirri, P., and Chiarugi, P. (2012) Cancer-associated-fibroblasts and tumour cells: a diabolic liaison driving cancer progression. Cancer Metastasis Rev. 31, 195-208
37. Loeffler, M., Krüger, J. A., Niethammer, A. G., and Reisfeld, R. A. (2006) Targeting tumor-associated fibroblasts improves cancer chemotherapy by increasing intratumoral drug uptake. J. Clin. Investig. 116, 1955-1962