Acetylation of the chemotaxis response regulator CheY by acetyl-CoA synthetase purified from Escherichia coli

Journal of Molecular Biology

Volumn 342, Issue 2, 2004, Pages 383-401

  Barak, Rina ^a   Prasad, Krishna ^a   Shainskaya, Alla ^a   Wolfe, Alan J ^b   Eisenbach, Michael ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b LOYOLA UNIVERSITY CHICAGO   (United States)

Author keywords

acetyl CoA synthetase; acetylation; bacterial chemotaxis; CheY; response regulator

Indexed keywords

ACETIC ACID DERIVATIVE; ACETYL COENZYME A SYNTHETASE; ESCHERICHIA COLI PROTEIN; LYSINE; PROTEIN CHEY; UNCLASSIFIED DRUG;

ACETYLATION; ARTICLE; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CHEMOTAXIS; CONTROLLED STUDY; ENZYME ANALYSIS; ENZYME PURIFICATION; EUKARYOTE; IN VITRO STUDY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROKARYOTE; PROTEIN DEGRADATION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY; WESTERN BLOTTING;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; EUKARYOTA; PROKARYOTA;

EID: 4344623303     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2004.07.020     Document Type: Article

References (95)

1. A. Bren, and M. Eisenbach How signals are heard during bacterial chemotaxis: protein-protein interactions in sensory signal propagation J. Bacteriol. 182 2000 6865 6873
2. M. Eisenbach, and S.R. Caplan Bacterial chemotaxis: unsolved mystery of the flagellar switch Curr. Biol. 8 1998 R444 R446
3. R.E. Silversmith, and R.B. Bourret Throwing the switch in bacterial chemotaxis Trends Microbiol. 7 1999 16 22
4. R. Barak, and M. Eisenbach Correlation between phosphorylation of the chemotaxis protein CheY and its activity at the flagellar motor Biochemistry 31 1992 1821 1826
5. R. Barak, M. Welch, A. Yanovsky, K. Oosawa, and M. Eisenbach Acetyladenylate or its derivative acetylates the chemotaxis protein CheY in vitro and increases its activity at the flagellar switch Biochemistry 31 1992 10099 10107
6. R. Barak, W.N. Abouhamad, and M. Eisenbach Both acetate kinase and acetyl coenzyme A synthetase are involved in acetate-stimulated change in the direction of flagellar rotation in Escherichia coli J. Bacteriol. 180 1998 985 988
7. R. Barak, and M. Eisenbach Acetylation of the response regulator, CheY, is involved in bacterial chemotaxis Mol. Microbiol. 40 2001 731 743
8. R. Ramakrishnan, M. Schuster, and R.B. Bourret Acetylation at Lys-92 enhances signaling by the chemotaxis response regulator protein CheY Proc. Natl Acad. Sci. USA 95 1998 4918 4923
9. G.S. Lukat, B.H. Lee, J.M. Mottonen, A. Stock, and J.B. Stock Roles of the highly conserved aspartate and lysine residues in the response regulator of bacterial chemotaxis J. Biol. Chem. 266 1991 8348 8354
10. 19F NMR and protein engineering J. Biol. Chem. 268 1993 13089 13096
11. V.L. Robinson, D.R. Buckler, and A.M. Stock A tale of two components: a novel kinase and a regulatory switch Nature Struct. Biol. 7 2000 626 633
12. F. Campagnari, and L.T. Webster Purification and properties of acetyl coenzyme A synthetase from bovine heart mitochondria J. Biol. Chem. 238 1963 1628 1633
13. J. O'Sullivan, and L. Ettlinger Characterization of the acetyl-CoA synthetase of Acetobacter aceti Biochim. Biophys. Acta 450 1976 410 417
14. E.P. Frenkel, and R.L. Kitchens Acetyl-CoA synthetase from baker's yeast (Saccharomyces cerevisiae) Methods Enzymol. 71 1981 317 324
15. H. Martínez-Blanco, A. Reglero, M. Fernández-Valverde, M.A. Ferrero, M.A. Moreno, M.A. Peñalva, and J.M. Luengo Isolation and characterization of the acetyl-CoA synthetase from Penicillum chrysogenum J. Biol. Chem. 267 1992 5474 5481
16. H. Priefert, and A. Steinbuechel Identification and molecular characterization of acetyl coenzume A synthetase gene (acoE) of Alcaligenes eutrophus J. Bacteriol. 174 1992 6590 6599
17. S. Kumari, R. Tishel, M. Eisenbach, and A.J. Wolfe Cloning, characterization, and functional expression of acs, the gene which encodes acetyl-coenzyme A synthetase in Escherichia coli J. Bacteriol. 177 1995 2878 2886
18. M.S.M. Jetten, A.J.M. Stams, and A.J.B. Zehnder Isolation and characterization of acetyl-coenzyme A synthetase from Methanothrix soehngenii J. Bacteriol. 171 1989 5430 5435
19. D. Karan, J.R. David, and P. Capy Molecular evolution of the AMP-forming acetyl-CoA synthetase Gene 265 2001 95 101
20. M. Musfeldt, M. Selig, and P. Schönheit Acetyl coenzyme A synthetase (ADP forming) from the hyperthermophilic Archaeon Pyrococcus furiosus: identification, cloning, separate expression of the encoding genes, acdAI and acdBI, in Escherichia coli, and in vitro reconstitution of the active heterotetrameric enzyme from its recombinant subunits J. Bacteriol. 181 1999 5885 5888
21. L.B. Sánchez, H.G. Morrison, M.L. Sogin, and M. Müller Cloning and sequencing of an acetyl-CoA synthetase (ADP-forming) gene from the amitochondriate protist, Giardia lamblia Gene 233 1999 225 231
22. P. Berg Acyl adenylates: an enzymatic mechanism of acetate activation J. Biol. Chem. 222 1956 991 1013
23. J.C. Londesborough, and L.T. Webster Fatty acyl-CoA synthetases The Enzymes 10 1974 469 488
24. Metzler, D. E. (1977). Biochemistry: The Chemical Reactions of Living Cells, Academic Press, New York.
25. E.R. Stadtman Adenylyl transfer reactions The Enzymes 8 1973 1 49
26. L.T. Webster Studies of the acetyl coenzyme A synthetase reaction: V. The requirement for monovalent and divalent cations in partial reactions involving enzyme-bound acetyl adenylate J. Biol. Chem. 242 1967 1232 1240
27. V.J. Starai, I. Celic, R.N. Cole, J.D. Boeke, and J.C. Escalante-Semerena Sir2-dependent activation of acetyl-CoA synthetase by deacetylation of active lysine Science 298 2002 2390 2392
28. M.A. Martinez-Balbas, U.M. Bauer, S.J. Nielsen, A. Brehm, and T. Kouzarides Regulation of E2F1 activity by acetylation EMBO J. 19 2000 662 671
29. Y. Sano, and S. Ishii Increased affinity of c-Myb for CREB-binding protein (CBP) after CBP-induced acetylation J. Biol. Chem. 276 2001 3674 3682
30. A. Mal, M. Sturniolo, R.L. Schiltz, M.K. Ghosh, and M.L. Harter A role for histone deacetylase HDAC1 in modulating the transcriptional activity of MyoD: inhibition of the myogenic program EMBO J. 20 2001 1739 1753
31. L.T. Webster Studies of the acetyl coenzyme A synthetase reaction: III. Evidence of a double requirement for divalent cations J. Biol. Chem. 240 1965 4164 4169
32. A. Stock, D.E. Koshland, and J. Stock Homologies between Salmonella typhimurium CheY protein and proteins involved in the regulation of chemotaxis, membrane protein synthesis, and sporulation Proc. Natl Acad. Sci. USA 82 1985 7989 7993
33. E.K. Fridriksson, A. Beavil, D. Holowka, H.J. Gould, B. Baird, and F.W. McLafferty Heterogeneous glycosylation of immunoglobulin E constructs characterized by top-down high-resolution 2-D mass spectrometry Biochemistry 39 2000 3369 3376
34. K.O. Börnsen Influence of salts, buffers, detergents, solvents, and matrices on MALDI-MS protein analysis in complex mixtures J.R. Chapman Protein and Peptide Analysis: New Mass Spectrometric Applications 2000 Humana Press Inc. Totowa, NJ 387 404
35. E. Méndez, I. Valdés, and E. Camafeita Analysis of gluten in foods by MALDI-TOFMS J.R. Chapman Protein and Peptide Analysis: New Mass Spectrometric Applications 2000 Humana Press Inc. Totowa, NJ 355 367
36. S.A. Carr, M.J. Huddleston, and R.S. Annan Selective detection and sequencing of phosphopeptides at the femtomole level by mass spectrometry Anal. Biochem. 239 1996 180 192
37. Y.G. Tsay, Y.H. Wang, C.M. Chiu, B.J. Shen, and S.C. Lee A strategy for identification and quantitation of phosphopeptides by liquid chromatography/tandem mass spectrometry Anal. Biochem. 287 2000 55 64
38. A.V. Vener, A. Harms, M.R. Sussman, and R.D. Vierstra Mass spectrometric resolution of reversible protein phosphorylation in photosynthetic membranes of Arabidopsis thaliana J. Biol. Chem. 276 2001 6959 6966
39. O.N. Jensen, A.V. Podtelejnikov, and M. Mann Identification of the components of simple protein mixtures by high-accuracy peptide mass mapping and database searching Anal. Chem. 69 1997 4741 4750
40. K. Zhang, H. Tang, L. Huang, J.W. Blankenship, P.R. Jones, and F. Xiang Identification of acetylation and methylation sites of histone H3 from chicken erythrocytes by high-accuracy matrix-assisted laser desorption ionization-time-of-flight, matrix-assisted laser desorption ionization- postsource decay, and nanoelectrospray ionization tandem mass spectrometry Anal. Biochem. 306 2002 259 269
41. C. Borchers, C.E. Parker, L.J. Deterding, and K.B. Tomer Preliminary comparison of precursor scans and liquid chromatography-tandem mass spectrometry on a hybrid quadrupole time-of-flight mass spectrometer J. Chromatog. sect. A 854 1999 119 130
42. J.Y. Kim, K.W. Kim, H.J. Kwon, D.W. Lee, and J.S. Yoo Probing lysine acetylation with a modification-specific marker ion using high-performance liquid chromatography/electrospray-mass spectrometry with collision-induced dissociation Anal. Chem. 74 2002 5443 5449
43. G.G. Preston, C. Zeiher, J.D. Wall, and D.W. Emerich Acetate-activating enzymes of Bradyrhizobium japonicum bacteroids Appl. Environ. Microbiol. 55 1989 165 170
44. E. Imesch, and S. Rous Partial purification of rat liver cytoplasmic acetyl-CoA synthetase; characterization of some properties Int. J. Biochem. 16 1984 875 881
45. A.J. Wolfe, M.P. Conley, and H.C. Berg Acetyladenylate plays a role in controlling the direction of flagellar rotation Proc. Natl Acad. Sci. USA 85 1988 6711 6715
46. C.A. Mizzen, J.E. Brownell, R.G. Cook, and C.D. Allis Histone acetyltransferases: preparation of substrates and assay procedures A.P. Wolffe Chromatin vol. 304 1999 Academic Press Inc. San Diego, CA 675 696
47. K. Luby-Phelps Physical properties of cytoplasm Curr. Opin. Cell Biol. 6 1994 3 9
48. K. Luby-Phelps Cytoarchitecture and physical properties of cytoplasm: volume, viscosity, diffusion, intracellular surface area Int. Rev. Cytol. 192 2000 189 221
49. D.A. Nelson Histone acetylation in baker's yeast. Maintenance of the hyperacetylated configuration in log phase protoplasts J. Biol. Chem. 257 1982 1565 1568
50. A. Chestier, and M. Yaniv Rapid turnover of acetyl groups in the four core histones of simian virus 40 minichromosomes Proc. Natl Acad. Sci. USA 76 1979 46 50
51. D.E. Zhang, and D.A. Nelson Histone acetylation in chicken erythrocytes. Rates of acetylation and evidence that histones in both active and potentially active chromatin are rapidly modified Biochem. J. 250 1988 233 240
52. J.H. Waterborg Dynamics of histone acetylation in Saccharomyces cerevisiae Biochemistry 40 2001 2599 2605
53. Y. Katan-Khaykovich, and K. Struhl Dynamics of global histone acetylation and deacetylation in vivo: rapid restoration of normal histone acetylation status upon removal of activators and repressors Genes Dev. 16 2002 743 752
54. V.G. Allfrey, E.A. Di-Paola, and R. Sterner Protein side chains acetylations Methods Enzymol. 107 1984 224 240
55. Barak, R. & Eisenbach, M. (2004). Co-regulation of acetylation and phosphorylation of CheY - the response regulator in chemotaxis of Escherichia coli. J. Mol. Biol. 342, 375 - 381.
56. K. Struhl Histone acetylation and transcriptional regulatory mechanisms Genes Dev. 12 1998 599 606
57. J.R. Davie, and V.A. Spencer Control of histone modifications J. Cell Biochem. Suppl. 32-33 1999 141 148
58. J. Abraham, J. Kelly, P. Thibault, and S. Benchimol Post-translational modification of p53 protein in response to ionizing radiation analyzed by mass spectrometry J. Mol. Biol. 295 2000 853 864
59. R.E. Silversmith, and R.B. Bourret Synthesis and characterization of a stable analog of the phosphorylated form of the chemotaxis protein CheY Protein Eng. 11 1998 205 212
60. S. Napper, P.M. Wolanin, D.J. Webre, J. Kindrachuk, B. Waygood, and J.B. Stock Intramolecular rearrangements as a consequence of the dephosphorylation of phosphoaspartate residues in proteins FEBS Letters 538 2003 77 80
61. A. Kimura, and M. Horikoshi How do histone acetyltransferases select lysine residues in core histones? FEBS Letters 431 1998 131 133
62. J. Boyes, P. Byfield, Y. Nakatani, and V. Ogryzko Regulation of activity of the transcription factor GATA-1 by acetylation Nature 396 1998 594 598
63. W. Gu, and R.G. Roeder Activation of p53 sequence-specific DNA binding by acetylation of the p53 C-terminal domain Cell 90 1997 595 606
64. C. Prives, and J.L. Manley Why is p53 acetylated? Cell 107 2001 815 818
65. G. Marzio, C. Wagener, M.I. Gutierrez, P. Cartwright, K. Helin, and M. Giacca E2F family members are differentially regulated by reversible acetylation J. Biol. Chem. 275 2000 10887 10892
66. B. Furia, L. Deng, K. Wu, S. Baylor, K. Kehn, and H. Li Enhancement of nuclear factor-kappaB acetylation by coactivator p300 and HIV-1 Tat proteins J. Biol. Chem. 277 2002 4973 4980
67. X.Y. Zhu, K. Volz, and P. Matsumura The CheZ-binding surface of CheY overlaps the CheA- and FliM-binding surfaces J. Biol. Chem. 272 1997 23758 23764
68. M. Welch, N. Chinardet, L. Mourey, C. Birck, and J.-P. Samama Structure of the CheY-binding domain of histidine kinase CheA in complex with CheY Nature Struct. Biol. 5 1998 25 29
69. M.M. McEvoy, A.C. Hausrath, G.B. Randolph, S.J. Remington, and F.W. Dahlquist Two binding modes reveal flexibility in kinase/response regulator interactions in the bacterial chemotaxis pathway Proc. Natl Acad. Sci. USA 95 1998 7333 7338
70. D. Shukla, X.Y. Zhu, and P. Matsumura Flagellar motor-switch binding face of CheY and the biochemical basis of suppression by CheY mutants that compensate for motor-switch defects in Escherichia coli J. Biol. Chem. 273 1998 23993 23999
71. M. McEvoy, A. Bren, M. Eisenbach, and F.W. Dahlquist Identification of the binding interfaces on CheY for two of its targets, the phosphatase CheZ and the flagellar switch protein FliM J. Mol. Biol. 289 1999 1423 1433
72. H.-L. Hung, J. Lau, A.Y. Kim, M.J. Weiss, and G.A. Blobel CREB-binding protein acetylates hematopoietic transcription factor GATA-1 at functionally important sites Mol. Cell. Biol. 19 1999 3496 3505
73. M. Fu, C. Wang, A.T. Reutens, J. Wang, R.H. Angeletti, and L. Siconolfi-Baez p300 and p300/cAMP-response element-binding protein-associated factor acetylate the androgen receptor at sites governing hormone-dependent transactivation J. Biol. Chem. 275 2000 20853 20860
74. Y.L. Yao, W.M. Yang, and E. Seto Regulation of transcription factor YY1 by acetylation and deacetylation Mol. Cell. Biol. 21 2001 5979 5991
75. H. Santos-Rosa, E. Valls, T. Kouzarides, and M. Martinez-Balbas Mechanisms of P/CAF auto-acetylation Nucl. Acids Res. 31 2003 4285 4292
76. M. Ott, M. Schnölzer, J. Garnica, W. Fischle, S. Emiliani, H.R. Rackwitz, and E. Verdin Acetylation of the HIV-1 Tat protein by p300 is important for its transcriptional activity Curr. Biol. 9 1999 1489 1492
77. O. Landt, H.P. Grunert, and U. Hahn A general method for rapid site-directed mutagenesis using the polymerase chain reaction Gene 96 1990 125 128
78. Miller, J. H. (1992). A Short Course in Bacterial Genetics, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
79. M.M. Bradford A rapid and sensitive method for the quantitation of microgram quantities of protein, utilizing the principle of protein-dye binding Anal. Biochem. 72 1976 248 254
80. M.E. Jones, and F. Lipmann Aceto-CoA-kinase Methods Enzymol. 1 1955 585 595
81. F.E. Dailey, and H.C. Berg Change in direction of flagellar rotation in Escherichia coli mediated by acetate kinase J. Bacteriol. 175 1993 3236 3239
82. A. Bren, and M. Eisenbach Changing the direction of flagellar rotation in bacteria by modulating the ratio between the rotational states of the switch protein FliM J. Mol. Biol. 312 2001 699 709
83. A. Shevchenko, M. Wilm, O. Vorm, and M. Mann Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels Anal. Chem. 68 1996 850 858
84. Mehlman, T., Benjamin, M., Merhav, D., Osman, F., Ben-Asouli, Y., Goldshleger, R. et al. (2002). Proceedings of the 50th Conference of American Society for Mass Spectrometry, American Society for Mass Spectrometry, Santa Fe, NM.
85. O. Vorm, P. Roepstorff, and M. Mann Matrix surfaces made by fast evaporation yield improved resolution and very high sensitivity in MALDI-TOF Anal. Chem. 66 1994 3281 3287
86. O.N. Jensen, A. Podtelejnikov, and M. Mann Delayed extraction improves specificity in database searches by matrix-assisted laser desorption/ionization peptide maps Rapid Commun. Mass Spect. 10 1996 1371 1378
87. M. Kussmann, U. Lassing, C.A. Sturmer, M. Przybylski, and P. Roepstorff Matrix-assisted laser desorption/ionization mass spectrometric peptide mapping of the neural cell adhesion protein neurolin purified by sodium dodecyl sulfate polyacrylamide gel electrophoresis or acidic precipitation J. Mass Spectrom. 32 1997 483 493
88. M. Wilm, G. Neubauer, and M. Mann Parent ion scans of unseparated peptide mixtures Anal. Chem. 68 1996 527 533
89. M. Kalkum, G.J. Lyon, and B.T. Chait Detection of secreted peptides by using hypothesis-driven multistage mass spectrometry Proc. Natl Acad. Sci. USA 100 2003 2795 2800
90. H. Steen, B. Kuster, and M. Mann Quadrupole time-of-flight versus triple-quadrupole mass spectrometry for the determination of phosphopeptides by precursor ion scanning J. Mass Spectrom. 36 2001 782 790
91. H. Steen, B. Kuster, M. Fernandez, A. Pandey, and M. Mann Detection of tyrosine phosphorylated peptides by precursor ion scanning quadrupole TOF mass spectrometry in positive ion mode Anal. Chem. 73 2001 1440 1448
92. L. Bellsolell, J. Prieto, L. Serrano, and M. Coll Magnesium binding to the bacterial chemotaxis protein CheY results in large conformational changes involving its functional surface J. Mol. Biol. 238 1994 489 495
93. F.W. Studier, A.H. Rosenberg, J.J. Dunn, and J.W. Dubendorff Use of T7 RNA polymerase to direct expression of cloned genes Methods Enzymol. 185 1990 60 89
94. J.S. Parkinson Complementation analysis and deletion mapping of Escherichia coli mutants defective in chemotaxis J. Bacteriol. 135 1978 45 53
95. B.M. Prüss, and A.J. Wolfe Regulation of acetyl phosphate synthesis and degradation, and the control of flagellar expression in Escherichia coli Mol. Microbiol. 12 1994 973 984