In Vivo Acetylation of CheY, a Response Regulator in Chemotaxis of Escherichia coli

Journal of Molecular Biology

Volumn 376, Issue 5, 2008, Pages 1260-1271

  Yan, Jianshe ^a   Barak, Rina ^a   Liarzi, Orna ^a   Shainskaya, Alla ^a   Eisenbach, Michael ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

acetylation; bacterial chemotaxis; chemotaxis; CheY; response regulator

Indexed keywords

ACETIC ACID C 14; ACETYL COENZYME A SYNTHETASE; CARBON 14; CHEY PROTEIN; UNCLASSIFIED DRUG;

ACETYLATION; ARTICLE; CHEMOTAXIS; CONTROLLED STUDY; ESCHERICHIA COLI; IN VITRO STUDY; IN VIVO STUDY; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; PROTEIN SYNTHESIS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 39149083406     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.12.070     Document Type: Article

References (55)

1. Bren A., and Eisenbach M. How signals are heard during bacterial chemotaxis: protein-protein interactions in sensory signal propagation. J. Bacteriol. 182 (2000) 6865-6873
2. Bourret R.B., and Stock A.M. Molecular information processing: lessons from bacterial chemotaxis. J. Biol. Chem. 277 (2002) 9625-9628
3. Parkinson J.S. Bacterial chemotaxis: a new player in response regulator dephosphorylation. J. Bacteriol. 185 (2003) 1492-1494
4. Eisenbach M. Chemotaxis (2004), Imperial College Press, London, UK
5. Sourjik V. Receptor clustering and signal processing in E. coli chemotaxis. Trends Microbiol. 12 (2004) 569-576
6. Barak R., Welch M., Yanovsky A., Oosawa K., and Eisenbach M. Acetyladenylate or its derivative acetylates the chemotaxis protein CheY in vitro and increases its activity at the flagellar switch. Biochemistry 31 (1992) 10099-10107
7. Barak R., Prasad K., Shainskaya A., Wolfe A.J., and Eisenbach M. Acetylation of the chemotaxis response regulator CheY by acetyl-CoA synthetase from Escherichia coli. J. Mol. Biol. 342 (2004) 383-401
8. Barak R., Yan J., Shainskaya A., and Eisenbach M. The chemotaxis response regulator CheY can catalyze its own acetylation. J. Mol. Biol. 359 (2006) 251-265
9. Barak R., and Eisenbach M. Acetylation of the response regulator, CheY, is involved in bacterial chemotaxis. Mol. Microbiol. 40 (2001) 731-743
10. Barak R., and Eisenbach M. Co-regulation of acetylation and phosphorylation of CheY, a response regulator in chemotaxis of Escherichia coli. J. Mol. Biol. 342 (2004) 375-381
11. Whitlock J.P., Galeazzi D., and Schulman H. Acetylation and calcium-dependent phosphorylation of histone H3 in nuclei from butyrate-treated HeLa cells. J. Biol. Chem. 258 (1983) 1299-1304
12. Clayton A.L., Rose S., Barratt M.J., and Mahadevan L.C. Phosphoacetylation of histone H3 on c-fos- and c-jun-associated nucleosomes upon gene activation. EMBO J. 19 (2000) 3714-3726
13. Edmondson D.G., Davie J.K., Zhou J., Mirnikjoo B., Tatchell K., and Dent S.Y. Site-specific loss of acetylation upon phosphorylation of histone H3. J. Biol. Chem. 277 (2002) 29496-29502
14. Cheung P., Tanner K.G., Cheung W.L., Sassone-Corsi P., Denu J.M., and Allis C.D. Synergistic coupling of histone H3 phosphorylation and acetylation in response to epidermal growth factor stimulation. Mol. Cell 5 (2000) 905-915
15. Lambert P.F., Kashanchi F., Radonovich M.F., Shiekhattar R., and Brady J.N. Phosphorylation of p53 serine increases interaction with CBP. J. Biol. Chem. 273 (1998) 33048-33053
16. Kumar B.R., Swaminathan V., Banerjee S., and Kundu T.K. p300-mediated acetylation of human transcriptional coactivator PC4 is inhibited by phosphorylation. J. Biol. Chem. 276 (2001) 16804-16809
17. Ramakrishnan R., Schuster M., and Bourret R.B. Acetylation at Lys-92 enhances signaling by the chemotaxis response regulator protein CheY. Proc. Natl Acad. Sci. USA 95 (1998) 4918-4923
18. Lee S.-Y., Cho H.S., Pelton J.G., Yan D.L., Henderson R.K., King D.S., et al. Crystal structure of an activated response regulator bound to its target. Nat. Struct. Biol. 8 (2001) 52-56
19. D13K Y106W alone and in complex with a FliM peptide. J. Mol. Biol. 342 (2004) 1325-1335
20. Gu W., and Roeder R.G. Activation of p53 sequence-specific DNA binding by acetylation of the p53 C-terminal domain. Cell 90 (1997) 595-606
21. Sano Y., and Ishii S. Increased affinity of c-Myb for CREB-binding protein (CBP) after CBP-induced acetylation. J. Biol. Chem. 276 (2001) 3674-3682
22. Hung H.-L., Lau J., Kim A.Y., Weiss M.J., and Blobel G.A. CREB-binding protein acetylates hematopoietic transcription factor GATA-1 at functionally important sites. Mol. Cell. Biol. 19 (1999) 3496-3505
23. Naryzhny S.N., and Lee H. The post-translational modifications of proliferating cell nuclear antigen: acetylation, not phosphorylation, plays an important role in the regulation of its function. J. Biol. Chem. 279 (2004) 20194-20199
24. Adler J. Chemotaxis in bacteria. Science 153 (1966) 708-716
25. Parkinson J.S., and Houts S.E. Isolation and behavior of Escherichia coli deletion mutants lacking chemotaxis functions. J. Bacteriol. 151 (1982) 106-113
26. Barak R., and Eisenbach M. Chemotactic-like response of Escherichia coli cells lacking the known chemotaxis machinery but containing overexpressed CheY. Mol. Microbiol. 31 (1999) 1125-1137
27. Vallari D.S., and Jackowski S. Biosynthesis and degradation both contribute to the regulation of coenzyme A content in Escherichia coli. J. Bacteriol. 170 (1988) 3961-3966
28. Wolfe A.J., Conley M.P., Kramer T.J., and Berg H.C. Reconstitution of signaling in bacterial chemotaxis. J. Bacteriol. 169 (1987) 1878-1885
29. Wolfe A.J. The acetate switch. Microbiol. Mol. Biol. Rev. 69 (2005) 12-50
30. Springer M.S., Goy M.F., and Adler J. Protein methylation in behavioral control mechanisms and in signal transduction. Nature 280 (1979) 279-284
31. Sterner D.E., and Berger S.L. Acetylation of histones and transcription-related factors. Microbiol. Mol. Biol. Rev. 64 (2000) 435-459
32. Glozak M.A., Sengupta N., Zhang X., and Seto E. Acetylation and deacetylation of non-histone proteins. Gene 363 (2005) 15-23
33. Kimura A., Matsubara K., and Horikoshi M. A decade of histone acetylation: marking eukaryotic chromosomes with specific codes. J. Biochem. (Tokyo) 138 (2005) 647-662
34. Chen L., Fischle W., Verdin E., and Greene W.C. Duration of nuclear NF-kappaB action regulated by reversible acetylation. Science 293 (2001) 1653-1657
35. Ott M., Schnölzer M., Garnica J., Fischle W., Emiliani S., Rackwitz H.R., and Verdin E. Acetylation of the HIV-1 Tat protein by p300 is important for its transcriptional activity. Curr. Biol. 9 (1999) 1489-1492
36. Starai V.J., Celic I., Cole R.N., Boeke J.D., and Escalante-Semerena J.C. Sir2-dependent activation of acetyl-CoA synthetase by deacetylation of active lysine. Science 298 (2002) 2390-2392
37. Kunze G., Zipfel C., Robatzek S., Niehaus K., Boller T., and Felix G. The N terminus of bacterial elongation factor Tu elicits innate immunity in Arabidopsis plants. Plant Cell 16 (2004) 3496-3507
38. Ramagopal S., and Subramanian A.R. Alteration in the acetylation level of ribosomal protein L12 during growth cycle of Escherichia coli. Proc. Natl Acad. Sci. USA 71 (1974) 2136-2140
39. Volz K., and Matsumura P. Crystal structure of Escherichia coli CheY refined at 1.7-Å resolution. J. Biol. Chem. 266 (1991) 15511-15519
40. Dyer C.M., and Dahlquist F.W. Switched or not?: the structure of unphosphorylated CheY bound to the N terminus of FliM. J. Bacteriol. 188 (2006) 7354-7363
41. Luby-Phelps K. Physical properties of cytoplasm. Curr. Opin. Cell Biol. 6 (1994) 3-9
42. Luby-Phelps K. Cytoarchitecture and physical properties of cytoplasm: volume, viscosity, diffusion, intracellular surface area. Int. Rev. Cytol. 192 (2000) 189-221
43. Wolfe A.J., Conley M.P., and Berg H.C. Acetyladenylate plays a role in controlling the direction of flagellar rotation. Proc. Natl Acad. Sci. USA 85 (1988) 6711-6715
44. Barak R., Abouhamad W.N., and Eisenbach M. 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
45. Oppenheimer H.L., Labouesse B., and Hess G.P. Implication of an ionizing group in the control of conformation and activity of chymotrypsin. J. Biol. Chem. 241 (1966) 2720-2730
46. Harlow E., and Lane D. Antibodies: A Laboratory Manual (1988), Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 298-299
47. Wilchek M., and Miron T. Immobilization of enzymes and affinity ligands onto agarose via stable and uncharged carbamate linkages. Biochem. Int. 4 (1982) 629-635
48. Riordan J.F., and Vallee B.L. O-Acetyltyrosine. Methods Enzymol. 11 (1967) 570-576
49. Miller J.H. A Short Course in Bacterial Genetics (1992), Cold Spring Harbor Laboratory, Cold Spring Harbor, NY
50. Bradford M.M. 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
51. Bren A., and Eisenbach M. 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
52. Kaiser A.D., and Hogness D.S. The transformation of Escherichia coli with deoxyribonucleic acid isolated from bacteriophage λdg. J. Mol. Biol. 2 (1960) 392-415
53. Vogel H.J., and Bonner D.M. Acetylornithinase of Escherichia coli, partial purification and some properties. J. Biol. Chem. 218 (1956) 97-106
54. 2+-ATPase reveal novel features of its pumping mechanism. J. Biol. Chem. 279 (2004) 43971-43981
55. Shevchenko A., Wilm M., Vorm O., and Mann M. Anal. Chem. 68 (1966) 850-858