Matrix metalloproteinase-1 takes advantage of the induced fit mechanism to cleave the triple-helical type I collagen molecule

Biochemistry

Volumn 45, Issue 51, 2006, Pages 15411-15418

  O'Farrell, Thomas J ^a   Guo, Rong ^a   Hasegawa, Hisashi ^a   Pourmotabbed, Tayebeh ^a  

^a UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CHEMICAL BONDS; COLLAGEN; KINETIC THEORY; SUBSTRATES;

COLLAGEN MOLECULE; COLLAGENOLYTIC ACTIVITY; MATRIX METALLOPROTEINASE-1; PEPTIDE SUBSTRATES;

ENZYMES;

COLLAGEN TYPE 1; COLLAGENASE; GELATIN; GELATINASE B; INTERSTITIAL COLLAGENASE;

AMINO ACID SUBSTITUTION; ARTICLE; CHIMERA; COLLAGEN DEGRADATION; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME SPECIFICITY; PLASMID; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PURIFICATION; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CATALYTIC DOMAIN; CATTLE; COLLAGEN TYPE I; CONSERVED SEQUENCE; FIBROBLASTS; GELATIN; HUMANS; HYDROLYSIS; MATRIX METALLOPROTEINASE 1; MATRIX METALLOPROTEINASE 9; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, SECONDARY; ZINC;

EID: 33845931635     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi060849d     Document Type: Article

References (50)

1. Sellers, A., Reynolds, J. J., and Meikle, M. C. (1978) Neutral metallo-proteinases of rabbit bone. Separation in latent forms of distinct enzymes that when activated degrade collagen, gelatin and proteoglycans, Biochem. J. 171, 493-496.
2. Vu, T. H., Shipley, J. M., Bergers, G., Berger, J. E., Helms, J. A., Hanahan, D., Shapiro, S. D., Senior, R. M., and Werb, Z. (1998) MMP-9/gelatinase B is a key regulator of growth plate angiogenesis and apoptosis of hypertrophic chondrocytes, Cell 93, 411-422.
3. Wolf, C., Chernard, M. P., Durand de Grossouvre, P., Bellocq, J. P., Chambon, P., and Basset, P. (1992) Breast-cancer-associated stromelysin-3 gene is expressed in basal cell carcinoma and during cutaneous wound healing, J. Invest. Dermatol. 99, 870-872.
4. Wysocki, A. B., Staiano-Coico, L., and Grinnell, F. (1993) Wound fluid from chronic leg ulcers contains elevated levels of metalloproteinases MMP-2 and MMP-9, J. Invest. Dermatol. 101, 64-68.
5. Overall, C. M., Sodek, J., McCulloch, A. G., and Birek, P. (1991) Evidence for polymorphonuclear leukocyte collagenase and 92-kilodalton gelatinase in gingival crevicular fluid, Infect. Immun. 59, 4687-4692.
6. Page, R. C. (1991) The role of inflammatory mediators in the pathogenesis of periodontal disease, J. Periodontal Res. 26, 230-242.
7. Liotta, L. A., Tryggvason, K., Garbisa, S., Hart, I., Foltz, C. M., and Shafie, S. (1980) Metastatic potential correlates with enzymatic degradation of basement membrane collagen, Nature 284, 67-68.
8. Liotta, L. A., Abe, S., Robey, P. G., and Martin, G. R. (1979) Preferential digestion of basement membrane collagen by an enzyme derived from a metastatic murine tumor, Proc. Natl. Acad. Sci. U.S.A. 76, 2268-2272.
9. Matrisian, L. M., Bowden, G. T., Krieg, P., Furstenberger, G., Briand, J.-P., Leroy, P., and Breathnach, R. (1986) The mRNA coding for the secreted protease transin is expressed more abundantly in malignant than in benign tumor, Proc. Natl. Acad. Sci. U.S.A. 83, 9413-9417.
10. Bernhard, E. J., Muschel, R. J., and Hughes, E. N. (1990) Mr 92,000 gelatinase release correlates with the metastatic phenotype in transformed rat embryo cells, Cancer Res. 50, 3872-3877.
11. 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.
12. Bafetti, L. M., Young, T. N., Itoh, Y., and Stack, M. S. (1998) Intact vitronectin induces matrix metalloproteinase-2 and tissue inhibitor of metalloproteinases-2 expression and enhanced cellular invasion by melanoma cells, J. Biol. Chem. 273, 143-149.
13. Hayakawa, T., Yamashita, S., Kodama, H., Iwata, H., and Iwata, K. (1991) Tissue inhibitor of metallo-proteinases and collagenase activity in synovial fluid of human rheumatoid arthritis, Biomed. Res. 12, 169-173.
14. Hirose, T., Reife, R. A., Smith, G. M., Jr., Stevens, R. M., Mainardi, C. L., and Hasty, K. A. (1992) Characterization of type V collagenase (gelatinase) in synovial fluid of patients with inflammatory arthritis, J. Rheumatol. 19, 593-599.
15. Yu, L., Smith, G. J., Jr., Brandt, K., and Capello, W. (1990) Type XI collagen-degrading activity in human osteoarthritic cartilage, Arthritis Rheum. 33, 1626-1633.
16. Harris, E. D., Jr. (1990) Rheumatoid arthritis: Pathophysiology and implications for therapy, N. Engl. J. Med. 322, 1277-1289.
17. Woessner, J. F., Jr. (1991) Matrix metalloproteinases and their inhibitors in connective tissue remodeling, FASEB J. 5, 2145-2154.
18. Matrisian, L. M. (1992) The matrix-degrading metalloproteinases, BioEssays 14, 455-463.
19. Birkedal-Hansen, H., Moore, W. G. I., Bodden, M. K., Windsor, L. J., Birkedal-Hansen, B., DeCarlo, A., and Engler, J. A. (1993) Matrix metalloproteinases: A review, Crit. Rev. Oral Biol. Med. 4, 197-250.
20. Massova, I., Kotra, L. P., Fridman, R., and Mobashery, S. (1998) Matrix metalloproteinases: Structures, evolution, and diversification, FASEB J. 12, 1075-1095.
21. Nagase, H., and Woessner, J. F., Jr. (1999) Matrix metalloproteinases, J. Biol. Chem. 274, 21491-21494.
22. Netzel-Arnett, S., Fields, G. B., Birkedal-Hansen, H., Van Wart, H. E., and Fields, G. (1991) Sequence specificities of human fibroblast and neutrophil collagenases, J. Biol. Chem. 266, 6747-6755.
23. Fields, G. B., Van Wart, H. E., and Birkedal-Hansen, H. (1987) Sequence specificity of human skin fibroblast collagenase. Evidence for the role of collagen structure in determining the collagenase cleavage site, J. Biol. Chem. 262, 6221-6226.
24. Hirose, T., Patterson, C. E., Pourmotabbed, T., Mainardi, C. L., and Hasty, K. A. (1993) Structure-function relationship of human neutrophil collagenase: Identification of regions responsible for substrate specificity and general proteinase activity, Proc. Natl. Acad. Sci. U.S.A. 90, 2569-2573.
25. Sanchez-Lopez, R., Alexander, C. M., Behrendsten, O., Breathnach, R., and Werb, Z. (1993) Role of zinc-binding- and hemopexin domain-encoded sequences in the substrate specificity of collagenase and stromelysin-2 as revealed by chimeric proteins, J. Biol. Chem. 268, 7238-7247.
26. Murphy, G., Allan, J. A., Willenbrock, F., Cockett, M. I., O'Connell, J. P., and Docherty, A. J. (1992) The role of the C-terminal domain in collagenase and stromelysin specificity, J. Biol. Chem. 267, 9612-9618.
27. Tsukada, H., and Pourmotabbed, T. (2002) Unexpected crucial role of residue 272 in substrate specificity of fibroblast collagenases, J. Biol. Chem. 277, 27378-27384.
28. Bode, W., Reinemer, P., Huber, R., Kleine, T., Schnierer, S., and Tschesche, H. (1994) The X-ray crystal structure of the catalytic domain of human neutrophil collagenase inhibited by a substrate analogue reveals the essentials for catalysis and specificity, EMBO J. 13, 1263-1269.
29. Chung, L., Dinakarpandian, D., Yoshida, N., Lauer-Fileds, J. L., Fileds, G. B., Visse, R., and Nagase, H. (2004) Collagenase unwinds triple-helical collagen prior to peptide bond hydrolysis, EMBO J. 23, 3020-3030.
30. 191 region as a critical segment of matrix metalloproteinase 1 for the expression of collagenolytic activity, J. Biol. Chem. 275, 29610-29617.
31. Pelman, G. R., Morrison, C. J., and Overall, C. M. (2005) Pivotal molecular determinants of peptidic and collagen triple helicase activities reside in the S3′ subsite of matrix metalloproteinase 8 (MMP-8): The role of hydrogen bonding potential of ASN188 and TYR189 and the connecting cis bond, J. Biol. Chem. 280, 2370-2377.
32. Koshland, D. E., Jr. (1958) Application of a theory of enzyme specificity to protein synthesis, Proc. Natl. Acad. Sci. U.S.A. 44, 98-104.
33. Pourmotabbed, T., Solomon, T. L., Hasty, K. A., and Mainardi, C. L. (1994) Characteristics of 92 kDa type IV collagenase/gelatinase produced by granulocytic leukemia cells: Structure, expression of cDNA in E. coli and enzymic properties, Biochim. Biophys. Acta 1204, 97-107.
34. O'Farrell, T. J., and Pourmotabbed, T. (2000) Identification of structural elements important for matrix metalloproteinase type V collagenolytic activity as revealed by chimeric enzymes. Role of fibronectin-like domain and active site of gelatinase B, J. Biol. Chem. 275, 27964-27972.
35. Pourmotabbed, T., Aelion, J. A., Tyrrell, D., Hasty, K. A., Bu, C. H., and Mainardi, C. L. (1995) Role of the conserved histidine and aspartic acid residues in activity and stabilization of human gelatinase B: An example of matrix metalloproteinases, J. Protein Chem. 14, 527-535.
36. O'Farrell, T. J., and Pourmotabbed, T. (1998) The fibronectin-like domain is required for the type V and XI collagenolytic activity of gelatinase B, Arch. Biochem. Biophys. 354, 24-30.
37. 2+-dependent activity of human neutrophil gelatinase B, J. Biol. Chem. 271, 14308-14315.
38. Welgus, H. G., Jeffrey, J. J., and Eisen, A. Z. (1981) The collagen substrate specificity of human skin fibroblast collagenas, J. Biol. Chem. 256, 9511-9515.
39. Li, J., Brick, P., O'Hare, M. C., Skarzynski, T., Lloyd, L. F., Curry, V. A., Clark, I. M., Bigg, H. F., Hazleman, B. L., Cawston, T. E., and Blow, D. M. (1995) Structure of full-length porcine synovial collagenase reveals a C-terminal domain containing a calcium-linked, four-bladed β-propeller, Structure 3, 541-549.
40. Yan, B. X., and Sun, Y. Q. (1997) Glycine residues provide flexibility for enzyme active sites, J. Biol. Chem. 272, 3190-3194.
41. Veltman, O. R., Eijsink, V. G., Vriend, G., de Kreij, A., Venema, G., and Van den Burg, B. (1998) Probing catalytic hinge bending motions in thermolysin-like proteases by glycine → alanine mutations, Biochemistry 37, 5305-5311.
42. Bone, R., Silen, J. L., and Agard, A. A. (1989) Structural plasticity broadens the specificity of an engineered protease, Nature 339, 191-195.
43. Johnson, K. A. (1993) Conformational coupling in DNA polymerase fidelity, Annu. Rev. Biochem. 62, 685-713.
44. Rowsell, S., Hawtin, P., Minshull, C. A., Jepson, H., Brockbank, S. M., Barratt, D. G., Slater, A. M., McPheat, W. L., Waterson, D., Henney, A. M., and Pauptit, R. A. (2002) Crystal structure of human MMP-9 in complex with a reverse hydroxamate inhibitor, J. Mol. Biol. 319, 173-181.
45. Aimes, R. T., and Quigley, J. P. (1995) Matrix metalloproteinase-2 is an interstitial collagenase. Inhibitor-free enzyme catalyzes the cleavage of collagen fibrils and soluble native type I collagen generating the specific 3/4- and 1/4-length fragments, J. Biol. Chem. 270, 5872-5876.
46. Jozic, D., Bourenkov, G., Lim, N. H., Visse, R., Nagase, H., Bode, W., and Maskos, K. (2005) X-ray structure of human proMMP-1: New insights into procollagenase activation and collagen binding, J. Biol. Chem. 280, 9578-9585.
47. Allan, J. A., Docherty, A. J., Barker, P. J., Huskisson, N. S., Reynolds, J. J., and Murphy, G. (1995) Binding of gelatinases A and B to type-I collagen and other matrix components, Biochem. J. 309, 299-306.
48. Murphy, G., Nguyen, Q., Cockett, M. I., Atkinson, S. J., Allan, J. A., Knight, C. G., Willenbrock, F., and Docherty, A. J. (1994) Assessment of the role of the fibronectin-like domain of gelatinase A by analysis of a deletion mutant, J. Biol. Chem. 269, 6632-6636.
49. 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.
50. Tam, E. M., Moore, T. R., Butler, G. S., and Overall, C. M. (2004) Characterization of the distinct collagen binding, helicase and cleavage mechanisms of matrix metalloproteinase 2 and 14 (gelatinase A and MT1-MMP): The differential roles of the MMP hemopexin C domains and the MMP-2 fibronectin type II modules in collagen triple helicase activities, J. Biol. Chem. 279, 43336-43344.