Intrinsic Domain and Loop Dynamics Commensurate with Catalytic Turnover in an Induced-Fit Enzyme

Structure

Volumn 17, Issue 10, 2009, Pages 1356-1367

  Davulcu, Omar ^a   Flynn, Peter F ^b   Chapman, Michael S ^a   Skalicky, Jack J ^c  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b UNIVERSITY OF UTAH   (United States)

^c UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

PROTEINS

Indexed keywords

ARGININE KINASE;

AMINO TERMINAL SEQUENCE; ARTICLE; CATALYSIS; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME BINDING; ENZYME STRUCTURE; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN DOMAIN; RIGIDITY;

ARGININE KINASE; BINDING SITES; CATALYSIS; KINETICS; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN CONFORMATION; STRUCTURE-ACTIVITY RELATIONSHIP; SUBSTRATE SPECIFICITY;

EID: 70349907099     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.str.2009.08.014     Document Type: Article

References (60)

1. Azzi A., Clark S.A., Ellington W.R., and Chapman M.S. The role of phosphagen specificity loops in arginine kinase. Protein Sci. 13 (2004) 575-585
2. Beach H., Cole R., Gill M.L., and Loria J.P. Conservation of mus-ms enzyme motions in the apo- and substrate-mimicked state. J. Am. Chem. Soc. 127 (2005) 9167-9176
3. Blethen S.L. Kinetic properties of the arginine kinase isoenzymes of Limulus polyphemus. Arch. Biochem. Biophys. 149 (1972) 244-251
4. Boehr D.D., and Wright P.E. Biochemistry. How do proteins interact?. Science 320 (2008) 1429-1430
5. Boehr D.D., Dyson H.J., and Wright P.E. An NMR perspective on enzyme dynamics. Chem. Rev. 106 (2006) 3055-3079
6. Boehr D.D., Dyson H.J., and Wright P.E. Conformational relaxation following hydride transfer plays a limiting role in dihydrofolate reductase catalysis. Biochemistry 47 (2008) 9227-9233
7. Bosshard H.R. Molecular recognition by induced fit: how fit is the concept?. News Physiol. Sci. 16 (2001) 171-173
8. Boyer J.A., and Lee A.L. Monitoring aromatic picosecond to nanosecond dynamics in proteins via 13C relaxation: expanding perturbation mapping of the rigidifying core mutation, V54A, in eglin c. Biochemistry 47 (2008) 4876-4886
9. Cavanagh J., Fairbrother W.J., Palmer III A.G., and Skelton A.J. Protein NMR Spectroscopy (1996), Academic Press, San Diego
10. Clarkson M.W., Gilmore S.A., Edgell M.H., and Lee A.L. Dynamic coupling and allosteric behavior in a nonallosteric protein. Biochemistry 45 (2006) 7693-7699
11. Clore G.M., Szabo A., Bax A., Kay L.E., Driscoll P.C., and Gronenborn A.M. 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 (1990) 4989-4991
12. d'Auvergne E.J., and Gooley P.R. The use of model selection in the model-free analysis of protein dynamics. J. Biomol. NMR 25 (2003) 25-39
13. Davulcu O., Clark S.A., Chapman M.S., and Skalicky J.J. Main chain (1)H, (13)C, and (15)N resonance assignments of the 42-kDa enzyme arginine kinase. J. Biomol. NMR 32 (2005) 178
14. Dumas C., and Janin J. Conformational changes in arginine kinase upon ligand binding seen by small-angle X-ray scattering. FEBS Lett. 153 (1983) 128-130
15. Ellington W.R. Evolution and physiological roles of phosphagen systems. Annu. Rev. Physiol. 63 (2001) 289-325
16. Farrow N.A., Muhandiram R., Singer A.U., Pascal S.M., Kay C.M., Gish G., Shoelson S.E., Pawson T., Forman-Kay J.D., and Kay L.E. Backbone dynamics of a free and phosphopeptide-complexed Src homology 2 domain studied by 15N NMR relaxation. Biochemistry 33 (1994) 5984-6003
17. Fritz-Wolf K., Schnyder T., Wallimann T., and Kabsch W. Structure of mitochondrial creatine kinase. Nature 381 (1996) 341-345
18. Furter R., Furter-Graves E.M., and Wallimann T. Creatine kinase: the reactive cysteine is required for synergism but is nonessential for catalysis. Biochemistry 32 (1993) 7022-7029
19. Garcia de la Torre J., Huertas M.L., and Carrasco B. HYDRONMR: prediction of NMR relaxation of globular proteins from atomic-level structures and hydrodynamic calculations. J. Magn. Reson. 147 (2000) 138-146
20. Gattis J.L., Ruben E., Fenley M.O., Ellington W.R., and Chapman M.S. The active site cysteine of arginine kinase: structural and functional analysis of partially active mutants. Biochemistry 43 (2004) 8680-8689
21. Gerstein M., Lesk A.M., and Chothia C. Structural mechanisms for domain movements in proteins. Biochemistry 33 (1994) 6739-6749
22. Goddard, T.D., and Kneller, D.G. (2008). SPARKY 3 (http://www.cgl.ucsf.edu/home/sparky/).
23. Hayward S. Structural principles governing domain motions in proteins. Proteins 36 (1999) 425-435
24. Hayward S., and Berendsen H.J. Systematic analysis of domain motions in proteins from conformational change: new results on citrate synthase and T4 lysozyme. Proteins 30 (1998) 144-154
25. Jencks W.P. Catalysis in Chemistry and Enzymology (1969), McGraw-Hill, New York
26. Jencks W.P. Binding energy, specificity, and enzymic catalysis: the circe effect. Adv. Enzymol. Relat. Areas Mol. Biol. 43 (1975) 219-410
27. Jencks W.P., and Mage M.I. "Orbital steering", entropy, and rate accelerations. Biochem. Biophys. Res. Commun. 57 (1974) 887-892
28. Korzhnev D.M., Skrynnikov N.R., Millet O., Torchia D.A., and Kay L.E. An NMR experiment for the accurate measurement of heteronuclear spin-lock relaxation rates. J. Am. Chem. Soc. 124 (2002) 10743-10753
29. Koshland Jr. D.E. Application of a theory of enzyme specificity to protein synthesis. Proc. Natl. Acad. Sci. USA 44 (1958) 98-104
30. Koshland Jr. D.E. The key-lock theory and the induced-fit theory. Angew. Chem. Int. Ed. Engl. 33 (1994) 2375-2378
31. Kovrigin E.L., and Loria J.P. Enzyme dynamics along the reaction coordinate: critical role of a conserved residue. Biochemistry 45 (2006) 2636-2647
32. --creatine transition-state analogue complex. Biochemistry 41 (2002) 13861-13867
33. Lange O.F., Lakomek N.A., Fares C., Schroder G.F., Walter K.F., Becker S., Meiler J., Grubmuller H., Griesinger C., and de Groot B.L. Recognition dynamics up to microseconds revealed from an RDC-derived ubiquitin ensemble in solution. Science 320 (2008) 1471-1475
34. Lee R.A., Razaz M., and Hayward S. The DynDom database of protein domain motions. Bioinformatics 19 (2003) 1290-1291
35. Lipari G., and Szabo A. Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 1. Theory and range of validity. J. Am. Chem. Soc. 104 (1982) 4546-4559
36. Lipari G., and Szabo A. Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 2. Analysis of experimental results. J. Am. Chem. Soc. 104 (1982) 1559-4570
37. Loria J.P., Rance M., and Palmer III A.G. A TROSY CPMG sequence for characterizing chemical exchange in large proteins. J. Biomol. NMR 15 (1999) 151-155
38. Ma B., Kumar S., Tsai C.J., and Nussinov R. Folding funnels and binding mechanisms. Protein Eng. 12 (1999) 713-720
39. Mandel A.M., Akke M., and Palmer III A.G. Backbone dynamics of Escherichia coli ribonuclease HI: correlations with structure and function in an active enzyme. J. Mol. Biol. 246 (1995) 144-163
40. Markley J.L., Bax A., Arata Y., Hilbers C.W., Kaptein R., Sykes B.D., Wright P.E., and Wuthrich K. Recommendations for the presentation of NMR structures of proteins and nucleic acids. IUPAC-IUBMB-IUPAB Inter-Union Task Group on the Standardization of Data Bases of Protein and Nucleic Acid Structures Determined by NMR Spectroscopy. J. Biomol. NMR 12 (1998) 1-23
41. Mazon H., Marcillat O., Forest E., Smith D.L., and Vial C. Conformational dynamics of the GdmHCl-induced molten globule state of creatine kinase monitored by hydrogen exchange and mass spectrometry. Biochemistry 43 (2004) 5045-5054
42. Mazon H., Marcillat O., Forest E., and Vial C. Local dynamics measured by hydrogen/deuterium exchange and mass spectrometry of creatine kinase digested by two proteases. Biochimie 87 (2005) 1101-1110
43. Ohren J.F., Kundracik M.L., Borders Jr. C.L., Edmiston P., and Viola R.E. Structural asymmetry and intersubunit communication in muscle creatine kinase. Acta Crystallogr. D Biol. Crystallogr. 63 (2007) 381-389
44. Osborne M.J., Schnell J., Benkovic S.J., Dyson H.J., and Wright P.E. Backbone dynamics in dihydrofolate reductase complexes: role of loop flexibility in the catalytic mechanism. Biochemistry 40 (2001) 9846-9859
45. Palmer III A.G., Kroenke C.D., and Loria J.P. Nuclear magnetic resonance methods for quantifying microsecond-to-millisecond motions in biological macromolecules. Methods Enzymol. 339 (2001) 204-238
46. Pruett P.S., Azzi A., Clark S.A., Yousef M., Gattis J.L., Somasundaram T., Ellington W.R., and Chapman M.S. The putative catalytic bases have, at most, an accessory role in the mechanism of arginine kinase. J. Biol. Chem. 278 (2003) 26952-26957
47. Raiford D.S., Fisk C.L., and Becker E.D. Calibration of methanol and ethylene glycol nuclear magnetic resonance thermometers. Anal. Chem. 51 (1979) 2050-2051
48. Rozovsky S., Jogl G., Tong L., and McDermott A.E. Solution-state nmr investigations of triosephosphate isomerase active site loop motion: ligand release in relation to active site loop dynamics. J. Mol. Biol. 310 (2001) 271-280
49. Sullivan S.M., and Holyoak T. Enzymes with lid-gated active sites must operate by an induced fit mechanism instead of conformational selection. Proc. Natl. Acad. Sci. USA 105 (2008) 13829-13834
50. Suzuki T., Kawasaki Y., Furukohri T., and Ellington W.R. Evolution of phosphagen kinase. VI. Isolation, characterization and cDNA-derived amino acid sequence of lombricine kinase from the earthworm Eisenia foetida, and identification of a possible candidate for the guanidine substrate recognition site. Biochim. Biophys. Acta 1343 (1997) 152-159
51. Tjandra N., Feller S.E., Pastor R.W., and Bax A. Rotational diffusion anisotropy of human ubiquitin from 15N NMR relaxation. J. Am. Chem. Soc. 117 (1995) 12562-12566
52. Tjandra N., Kuboniwa H., Ren H., and Bax A. Rotational dynamics of calcium-free calmodulin studied by 15N-NMR relaxation measurements. Eur. J. Biochem. 230 (1995) 1014-1024
53. Vugmeyster L., Raleigh D.P., Palmer III A.G., and Vugmeister B.E. Beyond the decoupling approximation in the model free approach for the interpretation of NMR relaxation of macromolecules in solution. J. Am. Chem. Soc. 125 (2003) 8400-8404
54. Wang C., Rance M., and Palmer III A.G. Mapping chemical exchange in proteins with MW > 50 kD. J. Am. Chem. Soc. 125 (2003) 8968-8969
55. Wang C., Karpowich N., Hunt J.F., Rance M., and Palmer A.G. Dynamics of ATP-binding cassette contribute to allosteric control, nucleotide binding and energy transduction in ABC transporters. J. Mol. Biol. 342 (2004) 525-537
56. Watt E.D., Shimada H., Kovrigin E.L., and Loria J.P. The mechanism of rate-limiting motions in enzyme function. Proc. Natl. Acad. Sci. USA 104 (2007) 11981-11986
57. Wolf-Watz M., Thai V., Henzler-Wildman K., Hadjipavlou G., Eisenmesser E.Z., and Kern D. Linkage between dynamics and catalysis in a thermophilic-mesophilic enzyme pair. Nat. Struct. Mol. Biol. 11 (2004) 945-949
58. Yousef M.S., Fabiola F., Gattis J., Somasundaram T., and Chapman M.S. Refinement of arginine kinase transition-state analogue complex at 1.2 Å resolution: mechanistic insights. Acta Crystallogr. D Biol. Crystallogr. 58 (2002) 2009-2017
59. Yousef M.S., Clark S.A., Pruett P.K., Somasundaram T., Ellington W.R., and Chapman M.S. Induced fit in guanidino kinases-comparison of substrate-free and transition state analog structures of arginine kinase. Protein Sci. 12 (2003) 103-111
60. Zhou G., Somasundaram T., Blanc E., Parthasarathy G., Ellington W.R., and Chapman M.S. Transition state structure of arginine kinase: implications for catalysis of bimolecular reactions. Proc. Natl. Acad. Sci. USA 95 (1998) 8449-8454