Nonconserved active site residues modulate CheY autophosphorylation kinetics and phosphodonor preference

Biochemistry

Volumn 52, Issue 13, 2013, Pages 2262-2273

  Thomas, Stephanie A ^a   Immormino, Robert M ^a   Bourret, Robert B ^a   Silversmith, Ruth E ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE RESIDUES; AUTOPHOSPHORYLATION; AUTOPHOSPHORYLATION REACTION; NONPOLAR SURFACE AREA; PHOSPHO-TRANSFER; RESPONSE REGULATORS; STRUCTURAL MIMICRY; TWO-COMPONENT SIGNAL TRANSDUCTION;

AMINO ACIDS; CHAINS; ELECTROSTATICS; ENZYMES; ESCHERICHIA COLI; IONIC STRENGTH; MACHINERY; PLANTS (BOTANY); RATE CONSTANTS; SENSORS; SIGNAL TRANSDUCTION;

KINETICS;

ACETYL PHOSPHATE; CHEY PROTEIN; MONOPHOSPHOIMIDAZOLE; PHOSPHATE; PHOSPHORAMIDIC ACID DERIVATIVE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; AUTOPHOSPHORYLATION; CARBOXY TERMINAL SEQUENCE; ENZYME ACTIVE SITE; ENZYME KINETICS; ESCHERICHIA COLI; IONIC STRENGTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; SIGNAL TRANSDUCTION; STATIC ELECTRICITY;

AMIDES; BACTERIAL PROTEINS; CATALYTIC DOMAIN; ESCHERICHIA COLI; IMIDAZOLES; KINETICS; MEMBRANE PROTEINS; MOLECULAR DOCKING SIMULATION; MUTAGENESIS, SITE-DIRECTED; ORGANOPHOSPHATES; OSMOLAR CONCENTRATION; PHOSPHORIC ACIDS; PHOSPHORYLATION;

ESCHERICHIA COLI;

EID: 84875781231     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi301654m     Document Type: Article

References (56)

1. Bourret, R. B. and Silversmith, R. E. (2010) Two-component signal transduction Curr. Opin. Microbiol. 13, 113-115
2. Capra, E. J. and Laub, M. T. (2012) Evolution of two-component signal transduction systems Annu. Rev. Microbiol. 66, 325-347
3. Galperin, M. Y. (2010) Diversity of structure and function of response regulator output domains Curr. Opin. Microbiol. 13, 150-159
4. Lukat, G. S., McCleary, W. R., Stock, A. M., and Stock, J. B. (1992) Phosphorylation of bacterial response regulator proteins by low molecular weight phospho-donors Proc. Natl. Acad. Sci. U.S.A. 89, 718-722
5. Wolfe, A. J. (2005) The acetate switch Microbiol. Mol. Biol. Rev. 69, 12-50
6. Wolfe, A. J. (2010) Physiologically relevant small phosphodonors link metabolism to signal transduction Curr. Opin. Microbiol. 13, 204-209
7. Bourret, R. B., Thomas, S. A., Page, S. C., Creager-Allen, R. L., Moore, A. M., and Silversmith, R. E. (2010) Measurement of response regulator autodephosphorylation rates spanning six orders of magnitude Methods Enzymol. 471, 89-114
8. 32P] phosphoramidate for use as a low molecular weight phosphodonor reagent Anal. Biochem. 283, 222-227
9. Gao, R., Tao, Y., and Stock, A. M. (2008) System-level mapping of Escherichia coli response regulator dimerization with FRET hybrids Mol. Microbiol. 69, 1358-1372
10. Bourret, R. B. (2010) Receiver domain structure and function in response regulator proteins Curr. Opin. Microbiol. 13, 142-149
11. Lee, S. Y., Cho, H. S., Pelton, J. G., Yan, D., Berry, E. A., and Wemmer, D. E. (2001) Crystal structure of activated CheY. Comparison with other activated receiver domains J. Biol. Chem. 276, 16425-16431
12. Wang, W., Cho, H. S., Kim, R., Jancarik, J., Yokota, H., Nguyen, H. H., Grigoriev, I. V., Wemmer, D. E., and Kim, S. H. (2002) Structural characterization of the reaction pathway in phosphoserine phosphatase: Crystallographic "snapshots" of intermediate states J. Mol. Biol. 319, 421-431
13. Chanley, J. D. and Feageson, E. (1963) A study of hydrolysis of phosphoramides. II. Solvolysis of phosphoramidic acid and comparison with phosphate esters J. Am. Chem. Soc. 85, 1181-1190
14. Koshland, D. E. (1952) Efffect of catalysts on the hydrolysis of acetyl phosphate. Nucleophilic displacement mechanisms in enzymic reactions J. Am. Chem. Soc. 74, 2286-2296
15. Da Re, S. S., Deville-Bonne, D., Tolstykh, T., Veron, M., and Stock, J. B. (1999) Kinetics of CheY phosphorylation by small molecule phosphodonors FEBS Lett. 457, 323-326
16. Mayover, T. L., Halkides, C. J., and Stewart, R. C. (1999) Kinetic characterization of CheY phosphorylation reactions: Comparison of P-CheA and small-molecule phosphodonors Biochemistry 38, 2259-2271
17. Schuster, M., Silversmith, R. E., and Bourret, R. B. (2001) Conformational coupling in the chemotaxis response regulator CheY Proc. Natl. Acad. Sci. U.S.A. 98, 6003-6008
18. Silversmith, R. E., Appleby, J. L., and Bourret, R. B. (1997) Catalytic mechanism of phosphorylation and dephosphorylation of CheY: Kinetic characterization of imidazole phosphates as phosphodonors and the role of acid catalysis Biochemistry 36, 14965-14974
19. Stewart, R. C., Jahreis, K., and Parkinson, J. S. (2000) Rapid phosphotransfer to CheY from a CheA protein lacking the CheY-binding domain Biochemistry 39, 13157-13165
20. Barbieri, C. M., Mack, T. R., Robinson, V. L., Miller, M. T., and Stock, A. M. (2010) Regulation of response regulator autophosphorylation through interdomain contacts J. Biol. Chem. 285, 32325-32335
21. Zapf, J. W., Hoch, J. A., and Whiteley, J. M. (1996) A phosphotransferase activity of the Bacillus subtilis sporulation protein Spo0F that employs phosphoramidate substrates Biochemistry 35, 2926-2933
22. Ulrich, L. E. and Zhulin, I. B. (2010) The MiST2 database: A comprehensive genomics resource on microbial signal transduction Nucleic Acids Res. 38, D401-D407
23. Ames, S. K., Frankema, N., and Kenney, L. J. (1999) C-terminal DNA binding stimulates N-terminal phosphorylation of the outer membrane protein regulator OmpR from Escherichia coli Proc. Natl. Acad. Sci. U.S.A. 96, 11792-11797
24. Volz, K. (1993) Structural conservation in the CheY superfamily Biochemistry 32, 11741-11753
25. Pazy, Y., Wollish, A. C., Thomas, S. A., Miller, P. J., Collins, E. J., Bourret, R. B., and Silversmith, R. E. (2009) Matching biochemical reaction kinetics to the timescales of life: Structural determinants that influence the autodephosphorylation rate of response regulator proteins J. Mol. Biol. 392, 1205-1220
26. Thomas, S. A., Brewster, J. A., and Bourret, R. B. (2008) Two variable active site residues modulate response regulator phosphoryl group stability Mol. Microbiol. 69, 453-465
27. Boesch, K. C., Silversmith, R. E., and Bourret, R. B. (2000) Isolation and characterization of nonchemotactic CheZ mutants of Escherichia coli J. Bacteriol. 182, 3544-3552
28. Sheridan, R. C., McCullough, J. F., Wakefield, Z. T., Allcock, H. R., and Walsh, E. J. (1971) Phospharamidic acid and its salts Inorg. Synth. 13, 23-26
29. Rathlev, T. and Rosenberg, T. (1956) Non-enzymic formation and rupture of phosphorus to nitrogen linkages in phosphoramido derivatives Arch. Biochem. Biophys. 65, 319-339
30. Park, C. and Raines, R. T. (2001) Quantitative analysis of the effect of salt concentration on enzymatic catalysis J. Am. Chem. Soc. 123, 11472-11479
31. Hicks, S. N., Smiley, R. D., Hamilton, J. B., and Howell, E. E. (2003) Role of ionic interactions in ligand binding and catalysis of R67 dihydrofolate reductase Biochemistry 42, 10569-10578
32. Plantinga, M. J., Korennykh, A. V., Piccirilli, J. A., and Correll, C. C. (2008) Electrostatic interactions guide the active site face of a structure-specific ribonuclease to its RNA substrate Biochemistry 47, 8912-8908
33. Word, J. M., Lovell, S. C., Richardson, J. S., and Richardson, D. C. (1999) Asparagine and glutamine: Using hydrogen atom contacts in the choice of side-chain amide orientation J. Mol. Biol. 285, 1735-1747
34. Chen, V. B., Arendall, W. B., III, Headd, J. J., Keedy, D. A., Immormino, R. M., Kapral, G. J., Murray, L. W., Richardson, J. S., and Richardson, D. C. (2010) MolProbity: All-atom structure validation for macromolecular crystallography Acta Crystallogr. D66, 12-21
35. Silversmith, R. E., Guanga, G. P., Betts, L., Chu, C., Zhao, R., and Bourret, R. B. (2003) CheZ-mediated dephosphorylation of the Escherichia coli chemotaxis response regulator CheY: Role for CheY glutamate 89 J. Bacteriol. 185, 1495-1502
36. Meyer, E. A., Castellano, R. K., and Diederich, F. (2003) Interactions with aromatic rings in chemical and biological recognition Angew. Chem., Int. Ed. 42, 1210-1250
37. Sines, J. J., Allison, S. A., and McCammon, J. A. (1990) Point charge distributions and electrostatic steering in enzyme/substrate encounter: Brownian dynamics of modified copper/zinc superoxide dismutases Biochemistry 29, 9403-9412
38. Schreiber, G. and Fersht, A. R. (1996) Rapid, electrostatically assisted association of proteins Nat. Struct. Biol. 3, 427-431
39. McDonald, L. R., Boyer, J. A., and Lee, A. L. (2012) Segmental motions, not a two-state concerted switch, underlie allostery in CheY Structure 20, 1363-1373
40. Stock, A. M. and Guhaniyogi, J. (2006) A new perspective on response regulator activation J. Bacteriol. 188, 7328-7330
41. Baker, N. A., Sept, D., Joseph, S., Holst, M. J., and McCammon, J. A. (2001) Electrostatics of nanosystems: Application to microtubules and the ribosome Proc. Natl. Acad. Sci. U.S.A. 98, 10037-10041
42. 2+-bound form of CheY and mechanism of phosphoryl transfer in bacterial chemotaxis Biochemistry 32, 13375-13380
43. Roberts, A., Lee, S. Y., McCullagh, E., Silversmith, R. E., and Wemmer, D. E. (2005) YbiV from Escherichia coli K12 is a HAD phosphatase Proteins 58, 790-801
44. Lassila, J. K., Zalatan, J. G., and Herschlag, D. (2011) Biological phosphoryl-transfer reactions: Understanding mechanism and catalysis Annu. Rev. Biochem. 80, 669-702
45. Janin, J. and Chothia, C. (1976) Stability and specificity of protein-protein interactions: The case of the trypsin-trypsin inhibitor complexes J. Mol. Biol. 100, 197-211
46. Groban, E. S., Clarke, E. J., Salis, H. M., Miller, S. M., and Voigt, C. A. (2009) Kinetic buffering of cross talk between bacterial two-component sensors J. Mol. Biol. 390, 380-393
47. Skerker, J. M., Prasol, M. S., Perchuk, B. S., Biondi, E. G., and Laub, M. T. (2005) Two-component signal transduction pathways regulating growth and cell cycle progression in a bacterium: A system-level analysis PLoS Biol. 3, e334
48. Janiak-Spens, F., Cook, P. F., and West, A. H. (2005) Kinetic analysis of YPD1-dependent phosphotransfer reactions in the yeast osmoregulatory phosphorelay system Biochemistry 44, 377-386
49. Zhao, X., Copeland, D. M., Soares, A. S., and West, A. H. (2008) Crystal structure of a complex between the phosphorelay protein YPD1 and the response regulator domain of SLN1 bound to a phosphoryl analog J. Mol. Biol. 375, 1141-1151
50. Casino, P., Rubio, V., and Marina, A. (2009) Structural insight into partner specificity and phosphoryl transfer in two-component signal transduction Cell 139, 325-336
51. Yamada, S., Akiyama, S., Sugimoto, H., Kumita, H., Ito, K., Fujisawa, T., Nakamura, H., and Shiro, Y. (2006) The signaling pathway in histidine kinase and the response regulator complex revealed by X-ray crystallography and solution scattering J. Mol. Biol. 362, 123-139
52. Skerker, J. M., Perchuk, B. S., Siryaporn, A., Lubin, E. A., Ashenberg, O., Goulian, M., and Laub, M. T. (2008) Rewiring the specificity of two-component signal transduction systems Cell 133, 1043-1054
53. Szurmant, H. and Hoch, J. A. (2010) Interaction fidelity in two-component signaling Curr. Opin. Microbiol. 13, 190-197
54. Pazy, Y., Motaleb, M. A., Guarnieri, M. T., Charon, N. W., Zhao, R., and Silversmith, R. E. (2010) Identical phosphatase mechanisms achieved through distinct modes of binding phosphoprotein substrate Proc. Natl. Acad. Sci. U.S.A. 107, 1924-1929
55. Zhao, R., Collins, E. J., Bourret, R. B., and Silversmith, R. E. (2002) Structure and catalytic mechanism of the E. coli chemotaxis phosphatase CheZ Nat. Struct. Biol. 9, 570-575
56. Silversmith, R. E., Smith, J. G., Guanga, G. P., Les, J. T., and Bourret, R. B. (2001) Alteration of a nonconserved active site residue in the chemotaxis response regulator CheY affects phosphorylation and interaction with CheZ J. Biol. Chem. 276, 18478-18484