NMR structure of tissue inhibitor of metalloproteinases-1 implicates localized induced fit in recognition of matrix metalloproteinases

Journal of Molecular Biology

Volumn 295, Issue 2, 2000, Pages 257-268

  Wu, Bin ^a   Arumugam, S ^a   Gao, Guanghua ^a   Lee, Gui In ^a   Semenchenko, Valentyna ^a   Huang, Wen ^b   Brew, Keith ^b   Van Doren, Steven R ^a  

^a University of Missouri   (United States)

^b UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

Angiogenesis inhibitor; Heteronuclear NOE; MMP inhibitor; NMR solution structure; Protein protein interactions

Indexed keywords

ALANINE; CYSTEINE; MATRIX METALLOPROTEINASE; RECOMBINANT PROTEIN; STROMELYSIN; TISSUE INHIBITOR OF METALLOPROTEINASE 1;

AMINO TERMINAL SEQUENCE; ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; EXTRACELLULAR MATRIX; HUMAN; HYDROPHOBICITY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEAR OVERHAUSER EFFECT; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE;

EID: 0034645727     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1999.3362     Document Type: Article

References (71)

1. Albini A., Celchiori A., Santi L., Liotta L. A., Brown P. D., Stetler-Stevenson W. G. Tumor cell invasion inhibited by TIMP-2. J. Natl. Cancer Inst. 83:1991;775-779.
2. Albini A., Fontanini G., Masiello L., Tacchetti C., Bigini D., Luzzi P., Noonan D. M., Stetler-Stevenson W. G. Angiogenic potential in vivo by Kaposi's sarcoma cell-free supernatants and HIV-1 tat product: inhibition of KS-like lesions by tissue inhibitor of metalloproteinase-2. AIDS. 8:1994;1237-1244.
3. Andersson P., Weigelt J., Otting G. Spin-state selection filters for the measurement of heteronuclear one-bond coupling constants. J. Biomol. NMR. 12:1998;435-441.
4. 15N with side-chain Hβ resonances in larger proteins. J. Magn. Reson. 95:1991;636-641.
5. Arumugam S., Hemme C. L., Yoshida N., Suzuki K., Nagase M., Wu B., Van Doren S. R. TIMP-1 contact sites and perturbations of stromelysin 1 mapped by NMR and a paramagnetic surface probe. Biochemistry. 37:1998;9650-9657.
6. 15N relaxation using inverse detected two-dimensional NMR spectroscopy: the central helix is flexible. Biochemistry. 31:1992;5269-5278.
7. Bertaux B., Hornebeck W., Eisen A. Z., Dubertret L. Growth stimulation of human keratinocytes by tissue inhibitor of metalloproteinases. J. Invest. Dermatol. 97:1991;679-685.
8. 15N) doubly labeled proteins. J. Biomol. NMR. 4:1994;201-213.
9. Boujrad N., Ogwuegbu S. O., Garnier M., Lee C.-H., Martin B. M., Papadopoulos V. Identification of a stimulator of steroid hormone synthesis isolated from testis. Science. 268:1995;1609-1612.
10. Brünger A. T., Adams P. D., Clore G. M., Delano W. L., Gros P., Grosse-Kunstleve R. W., Jiang J. S., Kuszewski J., Nilges M., Pannu N. S., Read R. J., Rice L. M., Simonson T., Warren G. L. Crystallography and NMR system (CNS): a new software suite for macromolecular structure determination. Acta Crystallog. sect. D. 54:1998;905-921.
11. Chambers A. F., Matrisian L. M. Changing views of the role of matrix metalloproteinases in metastasis. J. Natl. Cancer Inst. 89:1998;1260-1270.
12. Clore G. M., Gronenborn A. M., Bax A. A robust method for determining the magnitude of the fully asymmetric alignment tensor of oriented macromolecules in the absence of structural information. J. Magn. Reson. 133:1998;216-221.
13. Cornilescu G., Delaglio F., Bax A. Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J. Biomol. NMR. 13:1999;289-302.
14. DeClerck Y. A., Perez N., Shimada H., Boone T. C., Langley K. E., Taylor S. M. Inhibition of invasion and metastasis in cells transfected with an inhibitor of metalloproteinases. Cancer Res. 52:1992;701-708.
15. Docherty A. J. P., Lyons A., Smith B. J., Wright E. M., Stephens P. E., Harris T. J. R., Murphy G., Reynolds J. J. Sequence of human tissue inhibitor of metalloproteinases and its identity to erythroid-potentiating activity. Nature. 318:1985;66-69.
16. Douglas D. A., Shi Y. E., Sang Q. A. Computational sequence analysis of the tissue inhibitor of metalloproteinase family. J. Protein Chem. 16:1997;237-255.
17. Fernandez-Catalan C., Bode W., Huber R., Turk D., Calvette J. J., Lichte A., Tschesche H., Maskos K. Crystal structure of the complex formed by the membrane type 1-matrix metalloproteinase with the tissue inhibitor of metalloproteinases-2, the soluble progelatinase A receptor. EMBO J. 17:1998;5238-5248.
18. Fesik S. W., Zuiderweg E. R. P. Heteronuclear three dimensional NMR spectroscopy; a strategy for the simplification of homonuclear two dimensional NMR spectra. J. Magn. Reson. 78:1988;588-593.
19. Fletcher C. M., Jones D. N. M., Diamond R., Neuhaus D. Treatment of NOE constraints involving equivalent or nonstereoassigned protons in calculations of biomacromolecular structures. J. Biomol. NMR. 8:1996;292-310.
20. Freire E. The propagation of binding interactions to remote sites in proteins: analysis of the binding of the monoclonal antibody D1.3 to lysozyme. Proc. Natl Acad. Sci. USA. 96:1999;10118-10122.
21. Fujiwara T., Anai T., Kurihara N., Nagayama K. Frequency-switched composite pulses for decoupling carbon-13 spins over ultrabroad bandwidths. J. Magn. Reson. sect. A. 104:1993;103-105.
22. Gomis-Rüth F.-X., Maskos K., Betz M., Bergner A., Huber R., Suzuki K., Yoshida N., Nagase H., Brew K., Bourenkov G. P., Bartunik H., Bode W. Mechanism of inhibition of the human matrix metalloproteinase stromelysin-1 by TIMP-1. Nature. 389:1997;77-81.
23. cc couplings between backbone carbonyl and methyl carbons in isotopically enriched proteins. J. Biomol. NMR. 3:1993;487-493.
24. βJ couplings in isotopically enriched proteins. J. Am. Chem. Soc. 117:1995;5312-5315.
25. Hajduk P. J., Sheppard G., Nettesheim D. G., Olejniczak E. T., Shuker S. B., Meadows R. P., Steinman D. H., Carrera G. M. Jr, Marcotte P. A., Severin J., Walter K., Smith H., Gubbins E., Simmer R., Holzman T. F., Morgan D. W., Davidsen S. K., Summers J. B., Fesik S. W. Discovery of potent non-peptide inhibitors of stromelysin using SAR by NMR. J. Am. Chem. Soc. 119:1997;5818-5827.
26. Hansen M. R., Mueller L., Pardi A. Tunable alignment of macromolecules by filamentous phage yields dipolar coupling interactions. Nat. Struct. Biol. 5:1998;1065-1074.
27. Hayakawa T., Yamashita K., Tanzawa K., Uchijima E., Iwata K. Growth-promoting activity of tissue inhibitor of metalloproteinases-1 (TIMP-1) for a wide range of cells. A possible new growth factor in serum. FEBS Letters. 298:1992;29-32.
28. Hayakawa T., Yamashita K., Ohuchi E., Shinagawa A. Cell growth-promoting activity of tissue inhibitor of metalloproteinases-2 (TIMP-2). J. Cell Sci. 107:1994;2373-2379.
29. Hicks N. J., Ward R. V., Reynolds J. J. A fibrosarcoma model derived form mouse embryo cells: growth properties and secretion of collagenaseand metalloproteinase inhibitor (TIMP) by tumour cell lines. Int. J. Cancer. 33:1984;835-844.
30. Holm L., Sander C. Protein structure comparison by alignment of distance matrices. J. Mol. Biol. 233:1993;123-128.
31. NCγ couplings. J. Am. Chem. Soc. 119:1997;1803-1804.
32. Huang W., Suzuki K., Nagase H., Arumugam S., Van Doren S. R., Brew K. Folding and characterization of the amino-terminal domain of human tissue inhibitor of metalloproteinases-1 (TIMP-1) expressed at high yield in E. coli. FEBS Letters. 384:1996;155-161.
33. Huang W., Meng Q., Suzuki K., Nagase H., Brew K. Mutational study of the amino-terminal domain of human tissue inhibitor of metalloproteinases-1 (TIMP-1) locates an inhibitory region for matrix metalloproteinases. J. Biol. Chem. 272:1997;22086-22091.
34. Johnson M. D., Kim H.-R. C., Chesler L., Tsao-Wu G., Bouck N., Polverini P. J. Inhibition of angiogenesis by tissue inhibitor of metalloproteinase. J. Cell. Physiol. 160:1994;194-202.
35. 15N-labeled proteins. J. Magn. Reson. 86:1990;110-126.
36. Khokha R. Suppression of the tumorigenic and metastatic abilities of murine B16-F10 melanoma cells in vivo by the overexpression of tssue inhibitor of metalloproteinases-1. J. Natl Cancer Inst. 86:1994;299-304.
37. Khokha R., Waterhouse P., Yagel S., Lala P. K., Overall C. M., NOrton G., Denhardt D. T. Antisense RNA-induced reduction in murine TIMP levels confers oncogenicity on Swiss 3T3 cells. Science. 243:1989;947-950.
38. Khokha R., Zimmer M. J., Graham C. H., Lala P. K., Waterhouse P. Suppression of invasion by inducible expression of tissue inhibitor of metalloproteinase-1 (TIMP-1) in B16-F10 melanoma cells. J. Natl Cancer Inst. 84:1992;1017-1022.
39. Kikuchi K., Kadono T., Furue M., Tamaki K. Tissue inhibitor of metalloproteinase 1 (TIMP-1) may be an autocrine growth factor in scleroderma fibroblasts. J. Invest. Dermatol. 108:1997;281-284.
40. Koradi R., Billeter M., Wüthrich K. MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graphics. 14:1996;51-55.
41. Lasowski R. A., Rullman J. A., MacArthur M. W., Kaptein R., Thornton J. M. AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR. 8:1997;477-486.
42. Levitt M. H., Freeman R. Compensation for pulse imperfections in NMR spin-echo experiments. J. Magn. Reson. 43:1981;65-80.
43. Li R., Woodward C. The hydrogen exchange core and protein folding. Protein Sci. 8:1999;1571-1590.
44. Marion D., Ikura M., Tschudin R., Bax A. Rapid recording of 2D NMR spectra without phase cycling. Application to the study of hydrogen exchange in proteins. J. Magn. Reson. 85:1989;393-399.
45. Meng Q., Malinovskii V., Huang W., Hu Y., Chung L., Nagase H., Bode W., Maskos K., Brew K. Residue 2 of TIMP-1 is a major determinant of affinity and specificity for matrix metalloproteinases but effects of substitutions do not correlate with those of the corresponding p1' residue of substrate. J. Biol. Chem. 274:1999;10184-10189.
46. Mignatti P., Robbins E., Rifkin D. B. Tumor invasion through the human amniotic membrane: requirement for a proteinase cascade. Cell. 47:1986;487-498.
47. Mori S., Abeygunawardana C., O'Neil Johnson M., Van Zijl P. C. M. 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. sect. B. 108:1995;94-98.
48. Moses M. A., Sudhalter J., Langer R. Identification of an inhibitor of neovascularization from cartilage. Science. 248:1990;1408-1410.
49. Murphy G., Houbrechts A., Cockett M. I., Williamson R. A., O'Shea M., Docherty A. J. P. The N-terminal domain of tissue inhibitor of metalloproteinases retains metalloproteinase inhibitor activity. Biochemistry. 30:1991;8097-8102.
50. Murphy G., Willenbrock F. Tissue inhibitors of matrix metalloendopeptidases. Methods Enzymol. 248:1995;496-510.
51. Murzin A. OB(oligonucleotide/oligosaccharide binding)-fold: common structural and functional solution for non-homologous sequences. EMBO J. 12:1993;861-867.
52. Muskett F. W., Frenkiel T. A., Feeney J., Freedman R. B., Carr M. D., Williamson R. A. High resolution structure of the N-terminal domain of tissue inhibitor of metalloproteinases-2 and characterization of its interaction site with matrix metalloproteinase-3. J. Biol. Chem. 273:1998;21736-21743.
53. Nicholls A., Sharp K. A., Honig B. Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins: Struct. Funct. Genet. 11:1991;281-296.
54. Ojennus D. D., Mitton-Fry R. M., Wuttke D. S. Induced alignment and measurement of dipolar couplings of an SH2 domain through direct binding with filamentous phage. J. Biomol. NMR. 14:1999;175-179.
55. Ottiger M., Delaglio F., Bax A. Measurement of J and dipolar couplings from simplified two-dimensional NMR spectra. J. Magn. Reson. 131:1998;373-378.
56. 13C heteronuclear NMR spectroscopy. J. Am. Chem. Soc. 113:1991;4371-4380.
57. Shaka A. J., Barker P. B., Freeman R. Computer-optimized decoupling scheme for wideband applications and low-level operation. J. Magn. Reson. 64:1985;547-552.
58. Stein E. G., Rice L. M., Brunger A. T. Torsion-angle molecular dynamics as a new efficient tool for NMR structure calculation. J. Magn. Reson. 124:1996;154-164.
59. 15N NMR relaxation measurements. Biochemistry. 32:1993;426-435.
60. Takigawa M., Nishida Y., Suzuki F., Kishi J., Yamashita K., Hayakawa T. Induction of angiogenesis in chick yolk-sac membrane by polyamines and its inhibition by tissue inhibitor of metalloproteinases. Biochem. Biophys. Res. Commun. 171:1990;1264-1271.
61. Tjandra N., Bax A. Direct measurement of distances and angles in biomolecules by NMR in a dilute liquid crystalline medium. Science. 278:1997;1111-1114.
62. Tuuttila A., Morgunova E., Bergmann U., Lindqvist Y., Maskos K., Fernandez-Catalan C., Bode W., Tryggvason K., Schneider G. Three-dimensional structure of human tissue inhibitor of metalloproteinases-2 at 2.1 Å resolution. J. Mol. Biol. 284:1998;1133-1140.
63. Van Doren S. R., Kurochkin A. V., Ye Q. Z., Johnson L. L., Hupe D. L., Zuiderweg E. R. P. Assignments for the main-chain nuclear magnetic resonances and delineation of the secondary structure of the catalytic domain of human stromelysin-1 as obtained from triple-resonance 3D NMR experiments. Biochemistry. 32:1993;13109-13122.
64. Van Doren S. R., Zuiderweg E. R. P. Improvements in HSMQC-type double- and triple-resonance NMR experiments by using full-sweep (semi-) constant-time shift labeling. J. Magn. Reson. sect. B. 104:1994;193-198.
65. CαHα and protein backbone conformation. J. Am. Chem. Soc. 114:1992;9674-9675.
66. 13C. J. Am. Chem. Soc. 115:1993;5334-5335.
67. Williams D. C. Jr, Benjamin D. C., Poljak R. J., Rule G. S. Global changes in amide hydrogen exchange rates for a protein antigen in complex with three different antibodies. J. Mol. Biol. 257:1996;866-876.
68. Williamson R. A., Bartels H., Murphy G., Freedman R. B. Folding and stability of the active N-terminal domain of tissue inhibitor of metalloproteinases-1 and -2. Protein Eng. 7:1994a;1035-1040.
69. Williamson R. A., Martorell G., Carr M. D., Murphy G., Docherty A. J. P., Freedman R. B., Feeney J. Solution structure of the active domain of tissue inhibitor of metalloproteinases-2. A new member of the OB fold protein family. Biochemistry. 33:1994b;11745-11759.
70. HNHα coupling constants from HMQC-J spectra. J. Biomol. NMR. 11:1998;329-336.
71. 15N resonance assignments and secondary structure of the N-terminal domain of human tissue inhibitor of metalloproteinases-1. J. Biomol. NMR. 14:1999;289-290.