Examination of matrix metalloproteinase-1 in Solution A: Preference for the pre-collagenolysis state

Journal of Biological Chemistry

Volumn 288, Issue 42, 2013, Pages 30659-30671

  Cerofolini, Linda ^a   Fields, Gregg B ^b   Fragai, Marco ^a   Geraldes, Carlos F G C ^c,d   Luchinat, Claudio ^a   Parigi, Giacomo ^a   Ravera, Enrico ^a   Svergun, Dmitri I ^e   Teixeira, João M C ^a,c,d  

^a UNIVERSITY OF FLORENCE   (Italy)

^b TORREY PINES INSTITUTE FOR MOLECULAR STUDIES   (United States)

^c UNIVERSITY OF COIMBRA   (Portugal)

^d UNIVERSITY OF COIMBRA   (Portugal)

^e EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGENOLYSIS; INTER-DOMAIN; MATRIX METALLOPROTEINASE-1; MULTI-DOMAIN ENZYMES;

BIOCHEMISTRY; BIOLOGY;

COLLAGEN;

COLLAGEN; HEMOPEXIN; INTERSTITIAL COLLAGENASE;

ARTICLE; COLLAGEN DEGRADATION; ENZYME ANALYSIS; ENZYME CONFORMATION; ENZYME STRUCTURE; ENZYME SUBSTRATE COMPLEX; ESCHERICHIA COLI; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; TRIPLE HELIX; X RAY CRYSTALLOGRAPHY;

CHEMICAL BIOLOGY; COLLAGEN; COLLAGENOLYSIS; MATRIX METALLOPROTEINASE (MMP); MAXIMUM OCCURRENCE; METALLOPROTEASE; STRUCTURAL BIOLOGY;

HUMANS; MATRIX METALLOPROTEINASE 1; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SCATTERING, SMALL ANGLE;

EID: 84886882050     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.477240     Document Type: Article

References (69)

1. Overall, C. M. (2002) Molecular determinants of metalloproteinase substrate specificity. Mol. Biotechnol. 22, 51-86
2. Bode, W. (2003) in Proteases and the Regulation of Biological Processes: Biochemical Society Symposia Volume 70 (Saklatvala, J., Nagase, H., and Salvesen, G. S., eds) pp. 1-14, Portland Press, Portland, OR
3. Rosenblum, G., Van den Steen, P. E., Cohen, S. R., Grossmann, J. G., Frenkel, J., Sertchook, R., Slack, N., Strange, R. W., Opdenakker, G., and Sagi, I. (2007) Insights into the structure and domain flexibility of fulllength pro-matrix metalloproteinase-9/gelatinase B. Structure 15, 1227- 1236
4. Fields, G. B. (2013) Interstitial collagen catabolism. J. Biol. Chem. 288, 8785-8793
5. Chung, L., Dinakarpandian, D., Yoshida, N., Lauer-Fields, J. L., Fields, G. B., Visse, R., and Nagase, H. (2004) Collagenase unwinds triple-helical collagen prior to peptide bond hydrolysis. EMBO J. 23, 3020-3030
6. 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
7. Bertini, I., Calderone, V., Fragai, M., Luchinat, C., Maletta, M., and Yeo, K. J. (2006) Snapshots of the reaction mechanism of matrix metalloproteinases. Angew. Chem. Int. Ed. Engl. 45, 7952-7955
8. Bertini, I., Fragai, M., Luchinat, C., Melikian, M., Mylonas, E., Sarti, N., and Svergun, D. I. (2009) Interdomain flexibility in full-length matrix metalloproteinase- 1 (MMP-1). J. Biol. Chem. 284, 12821-12828
9. Bertini, I., Fragai, M., Luchinat, C., Melikian, M., Toccafondi, M., Lauer, J. L., and Fields, G. B. (2012) Structural basis for matrix metalloproteinase 1 catalyzed collagenolysis. J. Am. Chem. Soc. 134, 2100-2110
10. Minond, D., Lauer-Fields, J. L., Cudic, M., Overall, C. M., Pei, D., Brew, K., Moss, M. L., and Fields, G. B. (2007) Differentiation of secreted and membrane- type matrix metalloproteinase activities based on substitutions and interruptions of triple-helical sequences. Biochemistry 46, 3724-3733
11. Lu, K. G., and Stultz, C. M. (2013) Insight into the degradation of type-I collagen fibrils by MMP-8. J. Mol. Biol. 425, 1815-1825
12. 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., and Cawston, T. E. (1995) Structure of full-length porcine synovial collagenase reveals a C-terminal do-main containing a calcium-linked, four bladed β-propeller. Structure 3, 541-549
13. 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
14. Iyer, S., Visse, R., Nagase, H., and Acharya, K. R. (2006) Crystal structure of an active form of human MMP-1. J. Mol. Biol. 362, 78-88
15. Arnold, L. H., Butt, L. E., Prior, S. H., Read, C. M., Fields, G. B., and Pickford, A. R. (2011) The interface between catalytic and hemopexin domains in matrix metalloproteinase 1 conceals a collagen binding exosite. J. Biol. Chem. 286, 45073-45082
16. Manka, S. W., Carafoli, F., Visse, R., Bihan, D., Raynal, N., Farndale, R. W., Murphy, G., Enghild, J. J., Hohenester, E., and Nagase, H. (2012) Structural insights into triple-helical collagen cleavage by matrix metalloproteinase 1. Proc. Natl. Acad. Sci. U.S.A. 109, 12461-12466
17. Lauer-Fields, J. L., Chalmers, M. J., Busby, S. A., Minond, D., Griffin, P. R., and Fields, G. B. (2009) Identification of specific hemopexin-like domain residues that facilitate matrix metalloproteinase collagenolytic activity. J. Biol. Chem. 284, 24017-24024
18. Valafar, H., and Prestegard, J. H. (2004) REDCAT. A residual dipolar coupling analysis tool. J. Magn Reson. 167, 228-241
19. Bernadó, P., Blanchard, L., Timmins, P., Marion, D., Ruigrok, R. W., and Blackledge, M. (2005) A structural model for unfolded proteins from residual dipolar couplings and small-angle x-ray scattering. Proc. Natl. Acad. Sci. U.S.A. 102, 17002-17007
20. Bernadó, P., Mylonas, E., Petoukhov, M. V., Blackledge, M., and Svergun, D. I. (2007) Structural characterization of flexible proteins using smallangle x-ray scattering. J. Am. Chem. Soc. 129, 5656-5664
21. Berlin, K., O'Leary, D. P., and Fushman, D. (2009) Improvement and analysis of computational methods for prediction of residual dipolar couplings. J. Magn. Reson. 201, 25-33
22. Anthis, N. J., Doucleff, M., and Clore, G. M. (2011) Transient, sparsely populated compact states of apo and calcium-loaded calmodulin probed by paramagnetic relaxation enhancement. Interplay of conformational selection and induced fit. J. Am. Chem. Soc. 133, 18966-18974
23. Lange, O. F., Lakomek, N.-A., Fares, C., Schröder, G. F., Walter, K. F., Becker, S., Meiler, J., Grubmüller, H., Griesinger, C., and de Groot, B. L. (2008) Recognition dynamics up to microseconds revealed from an RDCderived ubiquitin ensemble in solution. Science 320, 1471-1475
24. Bashir, Q., Volkov, A. N., Ullmann, G. M., and Ubbink, M. (2010) Visualization of the encounter ensemble of the transient electron transfer complex of cytochrome c and cytochrome c peroxidase. J. Am. Chem. Soc. 132, 241-247
25. Bertini, I., Del Bianco, C., Gelis, I., Katsaros, N., Luchinat, C., Parigi, G., Peana, M., Provenzani, A., and Zoroddu, M. A. (2004) Experimentally exploring the conformational space sampled by domain reorientation in calmodulin. Proc. Natl. Acad. Sci. U.S.A. 101, 6841-6846
26. Lindorff-Larsen, K., Best, R. B., Depristo, M. A., Dobson, C. M., and Vendruscolo, M. (2005) Simultaneous determination of protein structure and dynamics. Nature 433, 128-132
27. Iwahara, J., and Clore, G. M. (2006) Detecting transient intermediates in macromolecular binding by paramagnetic NMR. Nature 440, 1227-1230
28. Volkov, A. N., Worrall, J. A., Holtzmann, E., and Ubbink, M. (2006) Solution structure and dynamics of the complex between cytochrome c and cytochrome c peroxidase determined by paramagnetic NMR. Proc. Natl. Acad. Sci. U.S.A. 103, 18945-18950
29. Zhang, Q., Stelzer, A. C., Fisher, C. K., and Al-Hashimi, H. M. (2007) Visualizing spatially correlated dynamics that directs RNA conformational transitions. Nature 450, 1263-1267
30. Bertini, I., Gupta, Y. K., Luchinat, C., Parigi, G., Peana, M., Sgheri, L., and Yuan, J. (2007) Paramagnetism-based NMR restraints provide maximum allowed probabilities for the different conformations of partially independent protein domains. J. Am. Chem. Soc. 129, 12786-12794
31. Bertini, I., Giachetti, A., Luchinat, C., Parigi, G., Petoukhov, M. V., Pierattelli, R., Ravera, E., and Svergun, D. I. (2010) Conformational space of flexible biological macromolecules from average data. J. Am. Chem. Soc. 132, 13553-13558
32. Fragai, M., Luchinat, C., Parigi, G., and Ravera, E. (2013) Conformational freedom of metalloproteins revealed by paramagnetism-assisted NMR. Coord. Chem. Rev. 257, 2652-2667
33. Dasgupta, S., Hu, X., Keizers, P. H., Liu, W.-M., Luchinat, C., Nagulapalli, M., Overhand, M., Parigi, G., Sgheri, L., and Ubbink, M. (2011) Narrowing the conformational space sampled by two-domain proteins with paramagnetic probes in both domains. J. Biomol. NMR 51, 253-263
34. Bertini, I., Luchinat, C., Nagulapalli, M., Parigi, G., and Ravera, E. (2012) Paramagnetic relaxation enhancement for the characterization of the conformational heterogeneity in two-domain proteins. Phys. Chem. Chem. Phys. 14, 9149-9156
35. Nagulapalli, M., Parigi, G., Yuan, J., Gsponer, J., Deraos, G., Bamm, V. V., Harauz, G., Matsoukas, J., de Planque, M. R., Gerothanassis, I. P., Babu, M. M., Luchinat, C., and Tzakos, A. G. (2012) Recognition pliability is coupled to structural heterogeneity. A calmodulin intrinsically disordered binding region complex. Structure 20, 522-533
36. Bertini, I., Gelis, I., Katsaros, N., Luchinat, C., and Provenzani, A. (2003) Tuning the affinity for lanthanides of calcium binding proteins. Biochemistry 42, 8011-8021
37. Bertini, I., Calderone, V., Cerofolini, L., Fragai, M., Geraldes, C. F., Hermann, P., Luchinat, C., Parigi, G., and Teixeira, J. M. (2012) The catalytic domain of MMP-1 studied through tagged lanthanides. FEBS Lett. 586, 557-567
38. Roessle, M. W., Klaering, R., Ristau, U., Robrahn, B., Jahn, D., Gehrmann, T., Konarev, P. V., Round, A., Fiedler, S., Hermes, S., and Svergun, D. I. (2007) Upgrade of the small-angle x-ray scattering beamline X33 at the European Molecular Biology Laboratory, Hamburg. J. Appl. Crystallogr. 40, s190-s194
39. Konarev, P. V., Volkov, V. V., Sokolova, A. V., Koch, M. H. J., and Svergun, D. I. (2003) PRIMUS. A Windows PC-based system for small-angle scattering data analysis. J. Appl. Crystallogr. 36, 1277-1282
40. Svergun, D. I., Barberato, C., and Koch, M. H. J. (1995) CRYSOL. A program to evaluate x-ray solution scattering of biological macromolecules from atomic coordinates. J. Appl. Crystallogr. 28, 768-773
41. Petoukhov, M. V., Franke, D., Shkumatov, A. V., Tria, G., Kikheney, A. G., Gajda, M., Gorba, C., Mertens, H. D. T., Konarev, P. V., and Svergun, D. I. (2012) New developments in the ATSAS program package for small-angle scattering data analysis. J. Appl. Crystallogr. 45, 342-350
42. Bertini, I., Ferella, L., Luchinat, C., Parigi, G., Petoukhov, M. V., Ravera, E., Rosato, A., and Svergun, D. I. (2012) MaxOcc. A web portal for maximum occurrence analysis. J. Biomol. NMR 53, 271-280
43. Bertini, I., Luchinat, C., and Parigi, G. (2002) Magnetic susceptibility in paramagnetic NMR. Progr. NMR Spectrosc. 40, 249-273
44. Longinetti, M., Parigi, G., and Sgheri, L. (2002) Uniqueness and degeneracy in the localization of rigid structural elements in paramagnetic proteins. J. Phys. A Math. Gen. 35, 8153-8169
45. Bertini, I., Fragai, M., Lee, Y. M., Luchinat, C., and Terni, B. (2004) Paramagnetic metal ions in ligand screening. The Co(II) matrix metalloproteinase 12. Angew. Chem. Int. Ed. Engl. 43, 2254-2256
46. Bertini, I., Calderone, V., Fragai, M., Jaiswal, R., Luchinat, C., Melikian, M., Mylonas, E., and Svergun, D. I. (2008) Evidence of reciprocal reorientation of the catalytic and hemopexin-like domains of full-length MMP-12. J. Am. Chem. Soc. 130, 7011-7021
47. Wöhnert, J., Franz, K. J., Nitz, M., Imperiali, B., and Schwalbe, H. (2003) Protein alignment by a coexpressed lanthanide-binding tag for the measurement of residual dipolar couplings. J. Am. Chem. Soc. 125, 13338 -13339
48. Ikegami, T., Verdier, L., Sakhaii, P., Grimme, S., Pescatore, B., Saxena, K., Fiebig, K. M., and Griesinger, C. (2004) Novel techniques for weak alignment of proteins in solution using chemical tags coordinating lanthanide ions. J. Biomol. NMR 29, 339-349
49. Su, X. C., Man, B., Beeren, S., Liang, H., Simonsen, S., Schmitz, C., Huber, T., Messerle, B. A., and Otting, G. (2008) A dipicolinic acid tag for rigid lanthanide tagging of proteins and paramagnetic NMR spectroscopy. J. Am. Chem. Soc. 130, 10486-10487
50. Keizers, P. H., Saragliadis, A., Hiruma, Y., Overhand, M., and Ubbink, M. (2008) Design, synthesis, and evaluation of a lanthanide chelating protein probe. CLaNP-5 yields predictable paramagnetic effects independent of environment. J. Am. Chem. Soc. 130, 14802-14812
51. Tolman, J. R., Al-Hashimi, H. M., Kay, L. E., and Prestegard, J. H. (2001) Structural and dynamic analysis of residual dipolar coupling data for proteins. J. Am. Chem. Soc. 123, 1416-1424
52. Xu, X., Reinle, W., Hannemann, F., Konarev, P. V., Svergun, D. I., Bernhardt, R., and Ubbink, M. (2008) Dynamics in a pure encounter complex of two proteins studied by solution scattering and paramagnetic NMR spectroscopy. J. Am. Chem. Soc. 130, 6395-6403
53. Kuffner, J. J. (2004) Effective sampling and distance metrics for 3D rigid body path planning. Proceedings of the IEEE International Conference on Robotics and Automation 4, 3993-3998
54. Bertini, I., Luchinat, C., and Parigi, G. (2011) Moving the frontiers in solution and solid-state bioNMR. Coord. Chem. Rev. 255, 649-663
55. Longinetti, M., Luchinat, C., Parigi, G., and Sgheri, L. (2006) Efficient determination of the most favoured orientations of protein domains from paramagnetic NMR data. Inv. Probl. 22, 1485-1502
56. Luchinat, C., Nagulapalli, M., Parigi, G., and Sgheri, L. (2012) Maximum occurrence analysis of protein conformations for different distributions of paramagnetic metal ions within flexible two-domain proteins. J. Magn. Reson. 215, 85-93
57. Bertini, I., Fragai, M., Giachetti, A., Luchinat, C., Maletta, M., Parigi, G., and Yeo, K. J. (2005) Combining in silico tools and NMR data to validate protein-ligand structural models. Application to matrix metalloproteinases. J. Med. Chem. 48, 7544-7559
58. Tang, C., Iwahara, J., and Clore, G. M. (2006) Visualization of transient encounter complexes in protein-protein association. Nature 444, 383-386
59. Yuwen, T., Post, C. B., and Skrynnikov, N. R. (2011) Domain cooperativity in multidomain proteins. What can we learn from molecular alignment in anisotropic media? J. Biomol. NMR 51, 131-150
60. Ryabov, Y. E., and Fushman, D. (2007) A model of interdomain mobility in a multidomain protein. J. Am. Chem. Soc. 129, 3315-3327
61. Shealy, P., Simin, M., Park, S. H., Opella, S. J., and Valafar, H. (2010) Simultaneous structure and dynamics of a membrane protein using REDCRAFT. Membrane-bound form of Pf1 coat protein. J. Magn. Reson. 207, 8-16
62. Weiss, D. R., and Levitt, M. (2009) Can morphing methods predict intermediate structures? J. Mol. Biol. 385, 665-674
63. Ye, Y., and Godzik, A. (2003) Flexible structure alignment by chaining aligned fragment pairs allowing twists. Bioinformatics 19, ii246-ii255
64. Tsukada, H., and Pourmotabbed, T. (2002) Unexpected crucial role of residue 272 in substrate specificity of fibroblast collagenase. J. Biol. Chem. 277, 27378-27384
65. Fasciglione, G. F., Gioia, M., Tsukada, H., Liang, J., Iundusi, R., Tarantino, U., Coletta, M., Pourmotabbed, T., and Marini, S. (2012) The collagenolytic action of MMP-1 is regulated by the interaction between the catalytic domain and the hinge region. J. Biol. Inorg. Chem. 17, 663-672
66. Sun, H. B., Smith, G. N., Jr., Hasty, K. A., and Yokota, H. (2000) Atomic force microscopy-based detection of binding and cleavage site of matrix metalloproteinase on individual type II collagen helices. Anal. Biochem. 283, 153-158
67. Saffarian, S., Collier, I. E., Marmer, B. L., Elson, E. L., and Goldberg, G. (2004) Interstitial collagenase is a Brownian rachet driven by proteolysis of collagen. Science 306, 108-111
68. Overall, C. M., and Butler, G. S. (2007) Protease yoga. Extreme flexibility of a matrix metalloproteinase. Structure 15, 1159-1161
69. Sarkar, S. K., Marmer, B., Goldberg, G., and Neuman, K. C. (2012) Singlemolecule tracking of collagenase on native type I collagen fibrils reveals degradation mechanism. Curr. Biol. 22, 1047-1056