Loop dynamics and ligand binding kinetics in the reaction catalyzed by the Yersinia protein tyrosine phosphatase

Biochemistry

Volumn 46, Issue 14, 2007, Pages 4370-4378

  Khajehpour, Mazdak ^a   Wu, Li ^b   Liu, Sijiu ^b   Zhadin, Nick ^a   Zhang, Zhong Yin ^b   Callender, Robert ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b INDIANA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING KINETICS; P-NITROCATECHOL SULFATE (PNC); YERSINIA PROTEIN TYROSINE PHOSPHATASE (YOPH);

AMINO ACIDS; BINDING SITES; CATALYST ACTIVITY; ENZYME INHIBITION; ENZYME KINETICS; MOLECULAR DYNAMICS;

LIGANDS;

4 NITROCATECHOL; 4 NITROCATECHOL SULFATE; PROTEIN TYROSINE PHOSPHATASE; UNCLASSIFIED DRUG;

ARTICLE; BINDING KINETICS; DYNAMICS; ENZYME ACTIVE SITE; ENZYME ANALYSIS; ENZYME SUBSTRATE; LIGAND BINDING; NONHUMAN; PRIORITY JOURNAL; YERSINIA;

AMINO ACID SEQUENCE; ASPARTIC ACID; BINDING SITES; BINDING, COMPETITIVE; CATALYSIS; CATALYTIC DOMAIN; CATECHOLS; CRYSTALLIZATION; CYSTEINE; HEAT; KINETICS; LASERS; LIGANDS; MODELS, MOLECULAR; MOLECULAR STRUCTURE; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTEIN-TYROSINE-PHOSPHATASE; SPECTROMETRY, FLUORESCENCE; SUBSTRATE SPECIFICITY; THERMODYNAMICS; TRYPTOPHAN; YERSINIA;

YERSINIA;

EID: 34147158317     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi602335x     Document Type: Article

References (61)

1. Neel, B. G., and Tonks, N. K. (1997) Protein tyrosine phosphatases in signal transduction, Curr. Opin. Cell Biol. 9, 193-204.
2. Zhang, Z. Y. (1998) Protein-tyrosine phosphatases: biological function, structural characteristics, and mechanism of catalysis, Crit. Rev. Biochem. Mol. Biol. 33, 1-52.
3. Kappert, K., Peters, K. G., Bohmer, F. D., and Ostman, A. (2005) Tyrosine phosphatases in vessel wall signaling, Cardiovasc. Res. 65, 587-98.
4. Jia, Z. (1997) Protein phosphatases: structures and implications, Biochem. Cell Biol. 75, 17-26.
5. Barford, D., Das, A. K., and Egloff, M. P. (1998) The structure and mechanism of protein phosphatases: insights into catalysis and regulation, Annu. Rev. Biophys. Biomol. Struct. 27, 133-64.
6. Stoker, A. W. (2005) Protein tyrosine phosphatases and signalling, J. Endocrinol. 185, 19-33.
7. Zhang, Z. Y. (2001) Protein tyrosine phosphatases: prospects for therapeutics, Curr. Opin. Chem. Biol. 5, 416-23.
8. van Huijsduijnen, R. H., Bombrun, A., and Swinnen, D. (2002) Selecting protein tyrosine phosphatases as drug targets, Drug Discovery Today 7, 1013-9.
9. Zhang, Z. Y. (2003) Chemical and mechanistic approaches to the study of protein tyrosine phosphatases, Acc. Chem. Res. 36, 385-92.
10. Yang, J., Niu, T., Zhang, A., Mishra, A. K., Zhao, Z. J., and Zhou, G. W. (2001) Relation between the flexibility of the WPD loop and the activity of the catalytic domain of protein tyrosine phosphatase SHP-1, J. Cell. Biochem. 84, 47-55.
11. Juszczak, L. J., Zhang, Z. Y., Wu, L., Gottfried, D. S., and Eads, D. D. (1997) Rapid loop dynamics of Yersinia protein tyrosine phosphatases, Biochemistry 36, 2227-36.
12. Zhang, Z. Y. (2002) Protein tyrosine phosphatases: structure and function, substrate specificity, and inhibitor development, Annu. Rev. Pharmacol. Toxicol. 42, 209-34.
13. Keng, Y. F., Wu, L., and Zhang, Z. Y. (1999) Probing the function of the conserved tryptophan in the flexible loop of the Yersinia protein-tyrosine phosphatase, Eur. J. Biochem. 259, 809-14.
14. Hoff, R. H., Hengge, A. C., Wu, L., Keng, Y. F., and Zhang, Z. Y. (2000) Effects on general acid catalysis from mutations of the invariant tryptophan and arginine residues in the protein tyrosine phosphatase from Yersinia, Biochemistry 39, 46-54.
15. Stuckey, J. A., Schubert, H. L., Fauman, E. B., Zhang, Z. Y., Dixon, J. E., and Saper, M. A. (1994) Crystal structure of Yersinia protein tyrosine phosphatase at 2.5 Å and the complex with tungstate, Nature 370, 571-5.
16. Sun, J. P., Wu, L., Fedorov, A. A., Almo, S. C., and Zhang, Z. Y. (2003) Crystal structure of the Yersinia protein-tyrosine phosphatase YopH complexed with a specific small molecule inhibitor, J. Biol. Chem. 278, 33392-9.
17. Hengge, A. C., Sowa, G. A., Wu, L., and Zhang, Z. Y. (1995) Nature of the transition state of the protein-tyrosine phosphatase-catalyzed reaction, Biochemistry 34, 13982-7.
18. Zhang, Z. Y., Palfey, B. A., Wu, L., and Zhao, Y. (1995) Catalytic function of the conserved hydroxyl group in the protein tyrosine phosphatase signature motif, Biochemistry 34, 16389-96.
19. Zhang, Z. Y. (1995) Kinetic and mechanistic characterization of a mammalian protein-tyrosine phosphatase, PTP1, J. Biol. Chem. 270, 11199-204.
20. Zhang, Z. Y., Clemens, J. C., Schubert, H. L., Stuckey, J. A., Fischer, M. W., Hume, D. M., Saper, M. A., and Dixon, J. E. (1992) Expression, purification, and physicochemical characterization of a recombinant Yersinia protein tyrosine phosphatase, J. Biol. Chem. 267, 23759-66.
21. Hengge, A. C., Zhao, Y., Wu, L., and Zhang, Z. Y. (1997) Examination of the transition state of the low-molecular mass small tyrosine phosphatase 1. Comparisons with other protein phosphatases, Biochemistry 36, 7928-36.
22. Khandelwal, P., Keliikuli, K., Smith, C. L., Saper, M. A., and Zuiderweg, E. R. (2002) Solution structure and phosphopeptide binding to the N-terminal domain of Yersinia YopH: comparison with a crystal structure, Biochemistry 41, 11425-37.
23. Evdokimov, A. G., Tropea, J. E., Routzahn, K. M., Copeland, T. D., and Waugh, D. S. (2001) Structure of the N-terminal domain of Yersinia pestis YopH at 2.0 Å resolution, Acta Crystallogr., Sect. D: Biol. Crystallogr. 57, 793-9.
24. Gandour, R. D., and Schowen, R. L. (1987) Transition States of Biochemical Processes, Plenum Press, New York.
25. Fersht, A. (1985) Enzyme Structure and Mechanism, Freeman & Co., New York.
26. Falzone, C. J., Wright, P. E., and Benkovic, S. J. (1994) Dynamics of a flexible loop in dihydrofolate reductase from Escherichia coli and its implication for catalysis, Biochemistry 33, 439-42.
27. Wang, G. P., Cahill, S. M., Liu, X., Girvin, M. E., and Grubmeyer, C. (1999) Motional dynamics of the catalytic loop in OMP synthase, Biochemistry 38, 284-95.
28. Waldman, A. D., Hart, K. W., Clarke, A. R., Wigley, D. B., Barstow, D. A., Atkinson, T., Chia, W. N., and Holbrook, J. J. (1988) The use of genetically engineered tryptophan to identify the movement of a domain of B. stearothermophilus lactate dehydrogenase with the process which limits the steady-state turnover of the enzyme, Biochem. Biophys. Res. Commun. 150, 752-9.
29. Ito, Y., Yamasaki, K., Iwahara, J., Terada, T., Kamiya, A., Shirouzu, M., Muto, Y., Kawai, G., Yokoyama, S., Laue, E. D., Walchli, M., Shibata, T., Nishimura, S., and Miyazawa, T. (1997) Regional polysterism in the GTP-bound form of the human c-Ha-Ras protein, Biochemistry 36, 9109-19.
30. Rozovsky, S., Jogl, G., Tong, L., and McDermott, A. E. (2001) Solution-state NMR investigations of triosephosphate isomerase active site loop motion: ligand release in relation to active site loop dynamics, J. Mol. Biol. 310, 271-80.
31. Rozovsky, S., Kaizuka, Y., and Groves, J. T. (2005) Formation and spatio-temporal evolution of periodic structures in lipid bilayers, J. Am. Chem. Soc. 127, 36-7.
32. Rozovsky, S., and McDermott, A. E. (2001) The time scale of the catalytic loop motion in triosephosphate isomerase, J. Mol. Biol. 310, 259-70.
33. Desamero, R., Rozovsky, S., Zhadin, N., McDermott, A., and Callender, R. (2003) Active site loop motion in triosephosphate isomerase: T-jump relaxation spectroscopy of thermal activation, Biochemistry 42, 2941-51.
34. Callender, R., and Dyer, R. B. (2002) Probing protein dynamics using temperature jump relaxation spectroscopy, Curr. Opin. Struct. Biol. 12, 628-33.
35. McClendon, S., Zhadin, N., and Callender, R. (2005) The approach to the Michaelis complex in lactate dehydrogenase: the substrate binding pathway, Biophys. J. 89, 2024-32.
36. McClendon, S., Vu, D. M., Clinch, K., Callender, R., and Dyer, R. B. (2005) Structural transformations in the dynamics of Michaelis complex formation in lactate dehydrogenase, Biophys. J. 89, L07-9.
37. Gulotta, M., Deng, H., Dyer, R. B., and Callender, R. H. (2002) Toward an understanding of the role of dynamics on enzymatic catalysis in lactate dehydrogenase, Biochemistry 41, 3353-63.
38. Deng, H., Zhadin, N., and Callender, R. (2001) Dynamics of protein ligand binding on multiple time scales: NADH binding to lactate dehydrogenase, Biochemistry 40, 3767-73.
39. Schubert, H. L., Fauman, E. B., Stuckey, J. A., Dixon, J. E., and Saper, M. A. (1995) A ligand-induced conformational change in the Yersinia protein tyrosine phosphatase, Protein Sci. 4, 1904-13.
40. Eigen, M. (1968) New looks and outlooks on physical enzymology, Q. Rev. Biophys. 1, 3-33.
41. Yapel, A. F., Jr. (1971) A practical guide to the temperature-jump method for measuring the rate of fast reactions, Methods Biochem. Anal. 20, 169-350.
42. Eigen, M., and Hammes, G. G. (1963) Elementary Steps in Enzyme Reactions (as Studied by Relaxation Spectrometry), Adv. Enzymol. Relat. Areas Mol. Biol. 25, 1-38.
43. Eigen, M., and De Maeyer, L. D. (1963) Relaxation Methods, in Techniques of Organic Chemistry (Friess, S. L., Lewis, E. S., and Weissberger, A., Eds.) pp 895-1054, Interscience, New York.
44. Hammes, G. G. (1968) Relaxation spectrometry of biological systems, Adv. Protein Chem. 23, 1-57.
45. Fasella, P., and Hammes, G. G. (1967) A. temperature jump study of aspartate aminotransferase. A reinvestigation, Biochemistry 6, 1798-804.
46. Malcolm, A. D. (1972) Temperature-jump studies on glutamate dehydrogenase, Biochem. J. 128, 98P.
47. Wilson, M. T., Greenwood, C., Brunori, M., and Antonini, E. (1975) Electron transfer between azurin and cytochrone c-551 from Pseudomonas aeruginosa, Biochem. J. 145, 449-57.
48. Baldo, J. H., Halford, S. E., Patt, S. L., and Sykes, B. D. (1975) The stepwise binding of small molecules to proteins. Nuclear magnetic resonance and temperature jump studies of the binding of 4-(N-acetylaminoglucosyl)-N- acetylglucosamine to lysozyme, Biochemistry 14, 1893-9.
49. Koren, R., and Hammes, G. G. (1976) A kinetic study of protein-protein interactions, Biochemistry 15, 1165-71.
50. Rosenberry, T. L., and Neumann, E. (1977) Interaction of ligands with acetylcholinesterase. Use of temperature-jump relaxation kinetics in the binding of specific fluorescent ligands, Biochemistry 16, 3870-8.
51. Vandenbunder, B., Dreyfus, M., and Buc, H. (1978) Conformational changes and local events at the AMP site of glycogen phosphorylase b: a fluorescence temperature-jump relaxation study, Biochemistry 17, 4153-60.
52. Williams, S., Causgrove, T. P., Gilmanshin, R., Fang, K. S., Callender, R. H., Woodruff, W. H., and Dyer, R. B. (1996) Fast events in protein folding: helix melting and formation in a small peptide, Biochemistry 35, 691-7.
53. Gulotta, M., Gilmanshin, R., Buscher, T. C., Callender, R. H., and Dyer, R. B. (2001) Core formation in apomyoglobin: probing the upper reaches of the folding energy landscape, Biochemistry 40, 5137-43.
54. van Holde, K. E., Johnson, W. C., and Ho, S. H. (1998) Principles of Physical Biochemistry, Prentice Hall, Upper Saddle River, NJ.
55. Lakowicz, J. R. (1999) Principles of Fluorescence Spectroscopy, Kluwer Academic/Plenum Publishers, New York.
56. Halford, S. E. (1972) Escherichia coli alkaline phosphatase. Relaxation spectra of ligand binding, Biochem. J. 126, 727-38.
57. Zhang, Z. Y., Malachowski, W. P., Van Etten, R. L., and Dixon, J. E. (1994) Nature of the rate-determining steps of the reaction catalyzed by the Yersinia protein-tyrosine phosphatase, J. Biol. Chem. 269, 8140-5.
58. Hengge, A. C., Denu, J. M., and Dixon, J. E. (1996) Transition-state structures for the native dual-specific phosphatase VHR and D92N and S131A mutants. Contributions to the driving force for catalysis, Biochemistry 35, 7084-92.
59. Hu, X., and Stebbins, C. E. (2006) Dynamics of the WPD loop of the Yersinia protein tyrosine phosphatase, Biophys. J. 91, 948-56.
60. Privalov, P. L., and Makhatadze, G. I. (1993) Contribution of hydration to protein folding thermodynamics. II. The entropy and Gibbs energy of hydration, J. Mol. Biol. 232, 660-79.
61. Robinson, D., Smith, J. N., Spencer, B., and Williams, R. T. (1952) Studies in detoxication. XXXXIII. A study of the arylsulphatase activity of takadiastase towards some phenolic ethereal sulphates, Biochem. J. 51, 202-8.