Colocalization of fast and slow timescale dynamics in the allosteric signaling protein CheY

Journal of Molecular Biology

Volumn 425, Issue 13, 2013, Pages 2372-2381

  McDonald, Leanna R ^a   Whitley, Matthew J ^a   Boyer, Joshua A ^a   Lee, Andrew L ^a,b  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b University of North Carolina   (United States)

Author keywords

allostery; CPMG relaxation dispersion; NMR; response regulator; side chain dynamics

Indexed keywords

CHEY PROTEIN; METHYL GROUP;

ALLOSTERISM; ARTICLE; CONFORMATIONAL TRANSITION; ESCHERICHIA COLI; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ESCHERICHIA COLI;

EID: 84879088309     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2013.04.029     Document Type: Article

References (54)

1. Q. Cui, and M. Karplus Allostery and cooperativity revisited Protein Sci. 17 2008 1295 1307
2. G. Manley, and J.P. Loria NMR insights into protein allostery Arch. Biochem. Biophys. 519 2012 223 231
3. B.F. Volkman, D. Lipson, D.E. Wemmer, and D. Kern Two-state allosteric behavior in a single-domain signaling protein Science 291 2001 2429 2433
4. P.J. Farber, and A. Mittermaier Concerted dynamics link allosteric sites in the PBX homeodomain J. Mol. Biol. 405 2011 819 830
5. S. Bruschweiler, P. Schanda, K. Kloiber, B. Brutscher, G. Kontaxis, R. Konrat, and M. Tollinger Direct observation of the dynamic process underlying allosteric signal transmission J. Am. Chem. Soc. 131 2009 3063 3068
6. K.K. Frederick, M.S. Marlow, K.G. Valentine, and A.J. Wand Conformational entropy in molecular recognition by proteins Nature 448 2007 325 329
7. C.M. Petit, J. Zhang, P.J. Sapienza, E.J. Fuentes, and A.L. Lee Hidden dynamic allostery in a PDZ domain Proc. Natl Acad. Sci. USA 106 2009 18249 18254
8. S.R. Tzeng, and C.G. Kalodimos Protein activity regulation by conformational entropy Nature 488 2012 236 240
9. K.A. Henzler-Wildman, M. Lei, V. Thai, S.J. Kerns, M. Karplus, and D. Kern A hierarchy of timescales in protein dynamics is linked to enzyme catalysis Nature 450 2007 913 916
10. D.O. Clegg, and D.E. Koshland Jr. The role of a signaling protein in bacterial sensing: behavioral effects of increased gene expression Proc. Natl Acad. Sci. USA 81 1984 5056 5060
11. P. Matsumura, J.J. Rydel, R. Linzmeier, and D. Vacante Overexpression and sequence of the Escherichia coli CheY gene and biochemical activities of the CheY protein J. Bacteriol. 160 1984 36 41
12. D.A. Sanders, B.L. Gillece-Castro, A.M. Stock, A.L. Burlingame, and D.E. Koshland Jr. Identification of the site of phosphorylation of the chemotaxis response regulator protein CheY J. Biol. Chem. 264 1989 21770 21778
13. M.K. Sarkar, K. Paul, and D. Blair Chemotaxis signaling protein CheY binds to the rotor protein FliN to control the direction of flagellar rotation in Escherichia coli Proc. Natl Acad. Sci. USA 107 2010 9370 9375
14. M.D. Baker, P.M. Wolanin, and J.B. Stock Signal transduction in bacterial chemotaxis BioEssays 28 2006 9 22
15. K. Paul, D. Brunstetter, S. Titen, and D.F. Blair A molecular mechanism of direction switching in the flagellar motor of Escherichia coli Proc. Natl Acad. Sci. USA 108 2011 17171 17176
16. S.A. Thomas, J.A. Brewster, and R.B. Bourret Two variable active site residues modulate response regulator phosphoryl group stability Mol. Microbiol. 69 2008 453 465
17. D. Yan, H.S. Cho, C.A. Hastings, M.M. Igo, S.Y. Lee, and J.G. Pelton Beryllofluoride mimics phosphorylation of NtrC and other bacterial response regulators Proc. Natl Acad. Sci. USA 96 1999 14789 14794
18. S.Y. Lee, H.S. Cho, J.G. Pelton, D. Yan, E.A. Berry, and D.E. Wemmer Crystal structure of activated CheY. Comparison with other activated receiver domains J. Biol. Chem. 276 2001 16425 16431
19. S.Y. Lee, H.S. Cho, J.G. Pelton, D. Yan, R.K. Henderson, and D.S. King Crystal structure of an activated response regulator bound to its target Nat. Struct. Biol. 8 2001 52 56
20. H.S. Cho, S.Y. Lee, D. Yan, X. Pan, J.S. Parkinson, and S. Kustu NMR structure of activated CheY J. Mol. Biol. 297 2000 543 551
21. J.L. Appleby, and R.B. Bourret Proposed signal transduction role for conserved CheY residue Thr87, a member of the response regulator active-site quintet J. Bacteriol. 180 1998 3563 3569
22. L.R. McDonald, J.A. Boyer, and A.L. Lee Segmental motions, not a two-state concerted switch, underlie allostery in CheY Structure 20 2012 1363 1373
23. A.K. Gardino, J. Villali, A. Kivenson, M. Lei, C.F. Liu, and P. Steindel Transient non-native hydrogen bonds promote activation of a signaling protein Cell 139 2009 1109 1118
24. V.A. Feher, and J. Cavanagh Millisecond-timescale motions contribute to the function of the bacterial response regulator protein Spo0F Nature 400 1999 289 293
25. S.R. Sheftic, P.P. Garcia, E. White, V.L. Robinson, D.J. Gage, and A.T. Alexandrescu Nuclear magnetic resonance structure and dynamics of the response regulator Sma0114 from Sinorhizobium meliloti Biochemistry 51 2012 6932 6941
26. A.G. Palmer, C.D. Kroenke, and J.P. Loria Nuclear magnetic resonance methods for quantifying microsecond-to-millisecond motions in biological macromolecules Methods Enzymol. 339 2001 204 238
27. J.P. Loria, M. Rance, and A.G. Palmer A relaxation-compensated Carr-Purcell-Meiboom-Gill sequence for characterizing chemical exchange by NMR spectroscopy J. Am. Chem. Soc. 121 1999 2331 2332
28. G. Lipari, and A. Szabo 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
29. G. Lipari, and A. Szabo Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 2. Analysis of experimental results J. Am. Chem. Soc. 104 1982 4559 4570
30. F.J. Moy, D.F. Lowry, P. Matsumura, F.W. Dahlquist, J.E. Krywko, and P.J. Domaille Assignments, secondary structure, global fold, and dynamics of chemotaxis-Y protein using 3-dimensional and 4-dimensional heteronuclear (C-13, N-15) NMR spectroscopy Biochemistry 33 1994 10731 10742
31. T.I. Igumenova, K.K. Frederick, and A.J. Wand Characterization of the fast dynamics of protein amino acid side chains using NMR relaxation in solution Chem. Rev. 106 2006 1672 1699
32. D.R. Muhandiram, T. Yamazaki, B.D. Sykes, and L.E. Kay Measurement of H-2 T-1 and T-1p relaxation-times in uniformly C-13-labeled and fractionally H-2-labeled proteins in solution J. Am. Chem. Soc. 117 1995 11536 11544
33. A.L. Lee, S.A. Kinnear, and A.J. Wand Redistribution and loss of side chain entropy upon formation of a calmodulin-peptide complex Nat. Struct. Biol. 7 2000 72 77
34. A.P. Loh, N. Pawley, L.K. Nicholson, and R.E. Oswald An increase in side chain entropy facilitates effector binding: NMR characterization of the side chain methyl group dynamics is Cdc42Hs Biochemistry 40 2001 4590 4600
35. M.W. Clarkson, S.A. Gilmore, M.H. Edgell, and A.L. Lee Dynamic coupling and allosteric behavior in a nonallosteric protein Biochemistry 45 2006 7693 7699
36. M. Simonovic, and K. Volz A distinct meta-active conformation in the 1.1-Å resolution structure of wild-type ApoCheY J. Biol. Chem. 276 2001 28637 28640
37. C.M. Dyer, and F.W. Dahlquist Switched or not?: the structure of unphosphorylated CheY bound to the N terminus of FliM J. Bacteriol. 188 2006 7354 7363
38. J.G. Smith, J.A. Latiolais, G.P. Guanga, S. Citineni, R.E. Silversmith, and R.B. Bourret Investigation of the role of electrostatic charge in activation of the Escherichia coli response regulator CheY J. Bacteriol. 185 2003 6385 6391
39. J.G. Smith, J.A. Latiolais, G.P. Guanga, J.D. Pennington, R.E. Silversmith, and R.B. Bourret A search for amino acid substitutions that universally activate response regulators Mol. Microbiol. 51 2004 887 901
40. M. Schuster, R. Zhao, R.B. Bourret, and E.J. Collins Correlated switch binding and signaling in bacterial chemotaxis J. Biol. Chem. 275 2000 19752 19758
41. 2 + binding by Calbindin-D(9k) J. Am. Chem. Soc. 115 1993 9832 9833
42. D. Yang, and L.E. Kay Contributions to conformational entropy arising from bond vector fluctuations measured from NMR-derived order parameters: application to protein folding J. Mol. Biol. 263 1996 369 382
43. Z. Li, S. Raychaudhuri, and A.J. Wand Insights into the local residual entropy of proteins provided by NMR relaxation Protein Sci. 5 1996 2647 2650
44. J.R. Schnell, H.J. Dyson, and P.E. Wright Effect of cofactor binding and loop conformation on side chain methyl dynamics in dihydrofolate reductase Biochemistry 43 2004 374 383
45. M. Schuster, R.E. Silversmith, and R.B. Bourret Conformational coupling in the chemotaxis response regulator CheY Proc. Natl Acad. Sci. USA 98 2001 6003 6008
46. D. Uhrin, S. Uhrinova, C. Leadbeater, J. Nairn, N.C. Price, and P.N. Barlow 3D HCCH(3)-TOCSY for resonance assignment of methyl-containing side chains in (13)C-labeled proteins J. Magn. Reson. 142 2000 288 293
47. C. Zwahlen, K.H. Gardner, S.P. Sarma, D.A. Horita, R.A. Byrd, and L.E. Kay An NMR experiment for measuring methyl-methyl NOEs in C-13-labeled proteins with high resolution J. Am. Chem. Soc. 120 1998 7617 7625
48. F. Delaglio, S. Grzesiek, G.W. Vuister, G. Zhu, J. Pfeifer, and A. Bax NMRPipe: a multidimensional spectral processing system based on UNIX pipes J. Biomol. NMR 6 1995 277 293
49. B.A. Johnson Using NMRView to visualize and analyze the NMR spectra of macromolecules Methods Mol. Biol. 278 2004 313 352
50. F.A. Mulder, A. Mittermaier, B. Hon, F.W. Dahlquist, and L.E. Kay Studying excited states of proteins by NMR spectroscopy Nat. Struct. Biol. 8 2001 932 935
51. N.A. Farrow, R. Muhandiram, A.U. Singer, S.M. Pascal, C.M. Kay, and G. Gish Backbone dynamics of a free and a phosphopeptide-complexed Src homology-2 domain studied by N-15 Nmr relaxation Biochemistry 33 1994 5984 6003
52. O. Millet, D.R. Muhandiram, N.R. Skrynnikov, and L.E. Kay Deuterium spin probes of side-chain dynamics in proteins. 1. Measurement of five relaxation rates per deuteron in (13)C-labeled and fractionally (2)H-enriched proteins in solution J. Am. Chem. Soc. 124 2002 6439 6448
53. E.J. d'Auvergne, and P.R. Gooley The use of model selection in the model-free analysis of protein dynamics J. Biomol. NMR 25 2003 25 39
54. E.J. Fuentes, C.J. Der, and A.L. Lee Ligand-dependent dynamics and intramolecular signaling in a PDZ domain J. Mol. Biol. 335 2004 1105 1115