The second type II module from human matrix metalloproteinase 2: Structure, function and dynamics

Structure

Volumn 7, Issue 10, 1999, Pages 1235-1245

  Briknarová, Klára ^a   Grishaev, Alexander ^a   Bányai, László ^b   Tordai, Hedvig ^b   Patthy, László ^b   Llinás, Miguel ^a  

^a CARNEGIE MELLON UNIVERSITY   (United States)

^b INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

Author keywords

Collagen; Fibronectin type II module; Gelatinase A; Matrix metalloproteinase 2; Type IV collagenase

Indexed keywords

GELATINASE A;

ARTICLE; DYNAMICS; ENZYME ANALYSIS; ENZYME BINDING; ENZYME STRUCTURE; HUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN FOLDING; STRUCTURE ANALYSIS;

EID: 0033569704     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0969-2126(00)80057-X     Document Type: Article

References (83)

1. 1. Collier, I.E., et al., & Goldberg, G.I. (1988). H-ras oncogene-transformed human bronchial epithelial cells (TBE-1) secrete a single metalloprotease capable of degrading basement membrane collagen. J. Biol. Chem. 263, 6579-6587.
2. 2. Sato, H., et al., & Seiki, M. (1994). A matrix metalloproteinase expressed on the surface of invasive tumour cells. Nature 370, 61-65.
3. 3. Birkedal-Hansen, H., et al., & Engler, J.A. (1993). Matrix metalloproteinases: a review. Crit. Rev. Oral Biol. Med. 4, 197-250.
4. 4. Mackay, A.R., Hartzler, J.L., Pelina, M.D. & Thorgeirsson, U.P. (1990). Studies on the ability of 65-kDa and 92-kDa tumor cell gelatinases to degrade type IV collagen. J. Biol. Chem. 265, 21929-21934.
5. 5. Aimes, R.T. & Quigley, J.P. (1995). Matrix metalloproteinase-2 is an interstitial collagenase. J. Biol. Chem. 270, 5872-5876.
6. 6. Welgus, H.G., Fliszar, C.J., Seltzer, J.L., Schmid, T.M. & Jeffrey, J.J. (1990). Differential susceptibility of type X collagen to cleavage by two mammalian interstitial collagenases and 72-kDa type IV collagenase. J. Biol. Chem. 265, 13521-13527.
7. 7. Senior, R.M., Griffin, G.L., Fliszar, C.J., Shapiro, S.D., Goldberg, G.I. & Welgus, H.G. (1991). Human 92-and 72-kilodalton type IV collagenases are elastases. J. Biol. Chem. 266, 7870-7875.
8. 8. Murphy, G., Cockett, M.I., Ward, R.V. & Docherty, A.J.P. (1991). Matrix metalloproteinase degradation of elastin, type IV collagen and proteoglycan. Biochem. J. 277, 277-279.
9. 9. Imai, K., Shikata, H. & Okada, Y. (1995). Degradation of vitronectin by matrix metalloproteinases-1, -2, -3, -7 and -9. FEBS Lett. 369, 249-251.
10. 10. Giannelli, G., Falk-Marzillier, J., Schiraldi, O., Stettler-Stevenson, W.G. & Quaranta, V. (1997). Induction of cell migration by matrix metalloproteinase-2 cleavage of laminin-5. Science 277, 225-228.
11. 11. Ray, J.M. & Stetler-Stevenson, W.G. (1995). Gelatinase A activity directly modulates melanoma cell adhesion and spreading. EMBO J. 14, 908-917.
12. 12. Turck, J., Pollock, A.S., Lee, L.K., Marti, H.P. & Lovett, D.H. (1996). Matrix metalloproteinase 2 (gelatinase A) regulates glomerular mesangial cell proliferation and differentiation. J. Biol. Chem. 271, 15074-15083.
13. 13. Yu, A.E., Murphy, A.N. & Stetler-Stevenson, W.G. (1998). 72-kDa gelatinase (gelatinase A): structure, activation, regulation, and substrate specificity. In Matrix Metalloproteinases. (Parks, W.C. & Mecham, R.P. eds), pp. 85-113, Academic Press, San Diego.
14. 14. Murphy, G., Willenbrock, F., Ward, R.V., Cockett, M.I., Eaton, D. & Docherty, A.J.P. (1992). The C-terminal domain of 72 kDa gelatinase A is not required for catalysis, but is essential for membrane activation and modulates interactions with tissue inhibitors of metalloproteinases. Biochem. J. 283, 637-641.
15. 15. Fridman, R., et al., & Stetler-Stevenson, W.G. (1992). Domain structure of human 72-kDa gelatinase/type IV collagenase. J. Biol. Chem. 267, 15398-15405.
16. 16. Kinoshita, T., et al., & Seiki, M. (1998). TIMP-2 promotes activation of progelatinase A by membrane-type 1 matrix metalloproteinase immobilized on agarose beads. J. Biol. Chem. 273, 16098-16103.
17. 17. Brooks, P.C., et al., & Cheresh, D.A. (1996). Localization of matrix metalloproteinase MMP-2 to the surface of invasive cells by interaction with integrin alpha v beta 3. Cell 85, 683-693.
18. 18. Emmert-Buck, M., Emonard, H. Corcoran, M., Krutzsch, H., Foidart, J. & Stetler-Stevenson, W. (1995). Cell surface binding of TIMP-2 and pro-MMP-2/TIMP-2 complex. FEBS Lett. 364, 28-32.
19. 19. Strongin, A.Y., Collier, I., Bannikov, G., Marmer, B.L., Grant, G.A. & Goldberg, G.I. (1995). Mechanism of cell surface activation of 72-kDa type IV collagenase. Isolation of the activated form of the membrane metalloprotease. J. Biol. Chem. 270, 5331-5338.
20. 20. Libson, A.M., Gittis, A.G., Collier, I.E., Marmer, B.L., Goldberg, G.I. & Lattman, E.E. (1995). Crystal structure of the haemopexin-like C-terminal domain of gelatinase A. Nat. Struct. Biol. 2, 938-942.
21. 21. Gohlke, U., Gomis-Rüth, F.-X., Crabbe, T., Murphy, G., Docherty, A.J.P. & Bode, W. (1996). The C-terminal (haemopexin-like) domain structure of human gelatinase Ȧ (MMP2): structural implications for its function. FEBS Lett. 378, 126-130.
22. 22. Li, J., et al., & 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.
23. 23. Becker, J.W., et al., & Springer, J.P. (1995). Stromelysin-1: three dimensional structure of the inhibited catalytic domain and the C-truncated proenzyme. Protein Sci. 4, 1966-1976.
24. 24. Moy, F.J., et al., & Powers, R. (1997). Assignments, secondary structure and dynamics of the inhibitor-free catalytic fragment of human fibroblast collagenase. J. Biomol. NMR 10, 9-19.
25. 25. Borkakoti, N., et al., & Murray, E.J. (1994). Structure of the catalytic domain of human fibroblast collagenase complexed with an inhibitor. Nat. Struct. Biol. 1, 106-110.
26. 26. Lovejoy, B., et al., & Jordan, S.R. (1994). Structure of the catalytic domain of fibroblast collagenase complexed with an inhibitor. Science 263, 375-377.
27. 27. Spurlino, J.C., et al., & Smith, D.L. (1994). 1.56 Å structure of mature truncated human fibroblast collagenase. Proteins 19, 98-109.
28. 28. Reinemer, P., et al., & Bode, W. (1994). Structural implications for the role of the N terminus in the 'superactivation' of collagenases. A crystallographic study. FEBS Lett. 338, 227-233.
29. 29. Stams, T., et al., & Rubin, B. (1994). Structure of human neutrophil collagenase reveals large S1' specificity pocket. Nat. Struct. Biol. 1, 119-123.
30. 30. Gooley, P.R., et al., & Johnson, B.A. (1994). The NMR structure of the inhibited catalytic domain of human stromelysin-1. Nat. Struct. Biol. 1,111-118.
31. 31. Gomis-Rüth, F.-X., et al., & Bode, W. (1997). Mechanism of inhibition of the human metalloproteinase stromelysin-1 by TIMP-1. Nature 389, 77-81.
32. 32. Bányai, L., Tordai, H. & Patthy, L. (1996). Structure and domain-domain interactions of the gelatin-binding site of human 72-kilodalton type IV collagenase (gelatinase A, matrix metalloproteinase 2). J. Biol. Chem. 271, 12003-12008.
33. 33. Jiang, W., et al., & Nussenzweig, M.C. (1995). The receptor DEC-205 expressed by dendritic cells and thymic epithelial cells is involved in antigen processing. Nature 375, 151-155.
34. 34. Bányai, L. & Patthy, L. (1991). Evidence for the involvement of the type II domains in collagen binding by 72 kDa type IV procollagenase. FEBS Lett. 282, 23-25.
35. 35. Bányai, L., Tordai, H. & Patthy, L. (1994). The gelatin-binding site of human 72-kDa type IV collagenase (gelatinase A). Biochem. J. 298, 403-407.
36. 36. Shipley, J.M., et al., & Senior, R.M. (1996). The structural basis for the elastolytic activity of the 92-kDa and 72-kDa gelatinases. J. Biol. Chem. 271, 4335-4341.
37. 37. Murphy, G., et al., & Docherty, A.J.P. (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.
38. 38. Allan, J.A., Docherty, A.J.P., Barker, P.J., Huskisson, N.S., Reynolds, J.J. & Murphy, G. (1995). Binding of gelatinases A and B to type-I collagen and other matrix components. Biochem. J. 309, 299-306.
39. 39. Steffensen, B., Wallon, U.M. & Overall, C.M. (1995). Extracellular matrix binding properties of recombinant fibronectin type II-like modules of human 72-kDa gelatinase/type IV collagenase. J. Biol. Chem. 270, 11555-11566.
40. 40. Tordai, H. & Patthy, L. (1999). The gelatin-binding site of the second type-II domain of gelatinase A/MMP-2. Eur. J. Biochem. 259, 513-518.
41. 41. Collier, I.E., Krasnov, P.A., Strongin, A.Y., Birkedal-Hansen, H. & 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.
42. 42. Constantine, K.L., Madrid, M., Bányai, L., Trexler, M., Patthy, L. & Llinás, M. (1992). Refined solution structure and ligand-binding properties of PDC-109 domain b. J. Mol. Biol. 223, 281-298.
43. 43. Pickford, A.R., Potts, J.R., Bright, J.R., Phan, I. & Campbell, I.D. (1997). Solution structure of a type 2 module from fibronectin: implications for the structure and function of the gelatin-binding domain. Structure 5, 359-370.
44. 44. Sticht, H., Pickford, A.R., Potts, J.R. & Campbell, I.D. (1998). Solution structure of the glycosylated second type 2 module of fibronectin. J. Mol. Biol. 276, 177-187.
45. 45. Wüthrich, K. (1986). NMR of Proteins and Nucleic Acids. John Wiley & Sons, Inc., New York.
46. 46. Eyre, D.R. (1980). Collagen: molecular diversity in the body's protein scaffold. Science 207, 1315-1322.
47. n with defined molecular weight - temperature dependence of molecular weight in aqueous solution. Biopolymers 9, 415-425.
48. 48. Kramer, R.Z., et al., & Berman, H.M. (1998). X-ray crystallographic determination of a collagen-like peptide with the repeating sequence (Pro-Pro-Gly). J. Mol. Biol. 280, 623-638.
49. 49. Lipari, G. & Szabo, A. (1982). Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 1. Theory and range of validity. J. Am. Chem. Soc. 104, 4546-4559.
50. 50. Clore, G.M., Szabo, A., Bax, A., Kay, L.E., Driscoll, P.C. & Gronenborn, A.M. (1990). Deviations from the simple two-parameter model-free approach to the interpretation of nitrogen-15 nuclear magnetic relaxation of proteins. J. Am. Chem. Soc. 112, 4989-4991.
51. 51. Aue, W.P., Bartholdi, E. & Ernst, R.R. (1976). Two-dimensional spectroscopy. Application to nuclear magnetic resonance. J. Chem. Phys. 64, 2229-2246.
52. 52. Braunschweiler, L. & Ernst, R.R. (1983). Coherence transfer by isotropic mixing: application to proton correlation spectroscopy. J. Magn. Reson. 53, 521-528.
53. 53. Bax, A. & Davis, D.G. (1985). MLEV-17-based two-dimensional homonuclear magnetization transfer spectroscopy. J. Magn. Reson. 65, 355-360.
54. 54. Jeener, J., Meier, B.H., Bachmann, P. & Ernst, R.R. (1979). Investigation of exchange processes by two-dimensional NMR spectroscopy. J. Chem. Phys. 71, 4546-4553.
55. 55. Piotto, M., Saudek, V. & Sklenár, V. (1992). Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions. J. Biomol. NMR 2, 661 -665.
56. 15N HSQC experiments optimized to retain full sensitivity. J. Magn. Reson. A 102, 241 -245.
57. 57. Griesinger, C., Sørensen, O.W. & Ernst, R.R. (1985). Two-dimensional correlation of connected NMR transitions. J. Am. Chem. Soc. 107, 6394-6396.
58. 58. Müller, L. (1979). Sensitivity enhanced detection of weak nuclei using heteronuclear multiple quantum coherence. J. Am. Chem. Soc. 101, 4481-4484.
59. 59. Bodenhausen, G. & Ruben, D.J. (1980). Natural abundance nitrogen-15 NMR by enhanced heteronuclear spectroscopy. Chem. Phys. Lett. 69, 185-189.
60. 60. Mori, S., Abeygunawardana, C., Johnson, M.O. & van Zijl, P.C.M. (1995). Improved sensitivity of HSQC spectra of exchanging protons at short interscan delays using a new fast HSQC (FHSQC) detection scheme that avoids water saturation. J. Magn. Reson. B 108, 94-98.
61. 15N Hartmann-Hahn-multiple quantum coherence and nuclear Overhauser-multiple quantum coherence spectroscopy: application to interleukin 1β. Biochemistry 28, 6150-6156.
62. 15N-labeled proteins. J. Am. Chem. Soc. 111, 1515-1517.
63. 63. Zuiderweg, E.R.P. & Fesik, S.W. (1989). Heteronuclear three-dimensional NMR spectroscopy of the inflammatory protein C5a. Biochemistry 28, 2387-2391.
64. 64. Talluri, S. & Wagner, G. (1996). An optimized 3D NOESY-HSQC. J. Magn. Reson. B 112, 200-205.
65. 15N enriched proteins. J. Am. Chem. Soc. 115, 7772-7777.
66. 15N-labeled proteins: application to the photoactive yellow protein. J. Biomol. NMR 10, 301-306.
67. 15N with side chain Hβ resonances in larger proteins. J. Magn. Reson. 95, 636-641.
68. 68. Friedrichs, M.S. (1995). A model-free algorithm for the removal of baseline artifacts. J. Biomol. NMR 5, 147-153.
69. 69. DeMarco, A. (1977). pH dependence of internal references. J. Magn. Reson. 26, 527-528.
70. 15N NMR study of gramicidin S in water and organic solvents. J. Am. Chem. Soc. 106, 1939-1941.
71. 71. Nilges, M., Clore, G.M. & Gronenborn, A.M. (1988). Determination of three-dimensional structures of proteins from interproton distance data by hybrid distance geometry - dynamical simulated annealing calculations. FEBS Lett. 229, 317-324.
72. 72. Kuszewski, J., Nilges, M. & Brünger, A.T. (1992). Sampling and efficiency of metric matrix distance geometry: a novel 'partial' metrization algorithm. J. Biomol. NMR 2, 33-56.
73. 73. Brünger, A.T. (1993). X-PLOR Version 3.1 Manual. Yale University, New Haven, CT.
74. 74. Laskowski, R.A., MacArthur, M.W., Moss, D.S. & Thornton, J.M. (1993). PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26, 283-291.
75. 75. Koradi, R., Billeter, M. & Wüthrich, K. (1996). MOLMOL: a program for display and analysis of macromolecular structures. J. Mot. Graph. 14, 51-55.
76. 76. Shaka, A.J., Lee, C.J. & Pines, A. (1988). Iterative schemes for bilinear operators; application to spin decoupling. J. Magn. Reson. 77, 274-293.
77. 77. Rucker, S.P. & Shaka, A.J. (1989). Broadband homonuclear cross polarization in 2D NMR using DIPSI-2. Mol. Phys. 68, 509-517.
78. 1H-NMR. Biochemistry 36, 11591-11604.
79. 79. An, S.S.A., Marti, D.N., Carreño, C., Albericio, F., Schaller, J. & Llinás. M. (1998). Structural/functional properties of the Glu1-HSer57 N-terminal fragment of human plasminogen: conformational characterization and interaction with kringle domains. Protein Sci. 7, 1947-1959.
80. 1H groups with pulsed-field gradients and preservation of coherence pathways. J. Magn. Reson. A 111, 121-126.
81. 81. Mandel, A.M., Akke, M. & Palmer, A.G., III (1995). Backbone dynamics of Escherichia coli ribonuclease HI: correlations with structure and function in an active enzyme. J. Mol. Biol. 246, 144-163.
82. 15N inverse detected heteronuclear NMR spectroscopy: application to staphylococcal nuclease. Biochemistry 28, 8972-8979.
83. 83. Roseman, M.A. (1988). Hydrophobicity of polar amino acid side-chains is markedly reduced by flanking peptide bonds. J. Mol. Biol. 200, 513-522.