Acetylation of the response regulator, CheY, is involved in bacterial chemotaxis

Molecular Microbiology

Volumn 40, Issue 3, 2001, Pages 731-743

  Barak, R ^a   Eisenbach, M ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYL COENZYME A SYNTHETASE; ARGININE; LYSINE; MUTANT PROTEIN;

ACETYLATION; AMINO ACID SUBSTITUTION; ARTICLE; BACTERIUM MUTANT; CHEMOTAXIS; ESCHERICHIA COLI; FLAGELLUM; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ESCHERICHIA COLI;

EID: 0034996629     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.2001.02425.x     Document Type: Article

References (60)

1. Adler, J. (1966) Chemotaxis in bacteria. Science 153: 708–716.
2. Adler, J. (1973) A method for measuring chemotaxis and use of the method to determine optimum conditions for chemotaxis by Escherichia coli. J Gen Microbiol 74: 77–91.
3. Barak, R. & Eisenbach, M. (1992) Correlation between phosphorylation of the chemotaxis protein CheY and its activity at the flagellar motor. Biochemistry 31: 1821–1826.
4. Barak, R. & Eisenbach, M. (1999) Possible involvement of acetyl‐CoA‐mediated acetylation of CheY in chemotaxis, p.39 (abstract). In Bacterial Locomotion and Signal Transduction. Cuernavaca, Mexico.
5. Barak, R., Welch, M., Yanovsky, A., Oosawa, K., Eisenbach, M. (1992) Acetyladenylate or its derivative acetylates the chemotaxis protein CheY in vitro and increases its activity at the flagellar switch. Biochemistry 31: 10099–10107.
6. Barak, R., Abouhamad, W.N., Eisenbach, M. (1998) 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: 985–988.
7. Berg, H.C. & Block, S.M. (1984) A miniature flow cell designed for rapid exchange of media under high‐power microscope objectives. J Gen Microbiol 130: 2915–2920.
8. Berg, H.C. & Tedesco, P.M. (1975) Transient response to chemotactic stimuli in Escherichia coli. Proc Natl Acad Sci USA 72: 3235–3239.
9. Bourret, R.B., Hess, J.F., Borkovich, K.A., Pakula, A.A., Simon, M.I. (1989) Protein phosphorylation in chemotaxis and two‐component regulatory systems of bacteria. J Biol Chem 264: 7085–7088.
10. Bourret, R.B., Hess, J.F., Simon, M.I. (1990) Conserved aspartate residues and phosphorylation in signal transduction by the chemotaxis protein CheY. Proc Natl Acad Sci USA 87: 41–45.
11. Bourret, R.B., Drake, S.K., Chervitz, S.A., Simon, M.I., Falke, J.J. (1993) Activation of the phosphosignaling protein CheY II. Analysis of activated mutants by 19 F NMR and protein engineering. J Biol Chem 268: 13089–13096.
12. Boyes, J., Byfield, P., Nakatani, Y., Ogryzko, V. (1998) Regulation of activity of the transcription factor GATA‐1 by acetylation. Nature 396: 594–598. DOI: 10.1038/25166
13. Bren, A. & Eisenbach, M. (1998) The N terminus of the flagellar switch protein, FliM, is the binding domain for the chemotactic response regulator, CheY. J Mol Biol 278: 507–514. DOI: 10.1006/jmbi.1998.1730
14. Bren, A. & Eisenbach, M. (2000) How signals are heard during bacterial chemotaxis: protein–protein interactions in sensory signal propagation. J Bacteriol 182: 6865–6873.
15. Cheung, P., Tanner, K.G., Cheung, W.L., Sassone‐Corsi, P., Denu, J.M., Allis, C.D. (2000) Synergistic coupling of histone H3 phosphorylation and acetylation in response to epidermal growth factor stimulation. Mol Cell 5: 905–915.
16. Chiarugi, V., Cinelli, M., Magnelli, L. (1998) Acetylation and phosphorylation of the carboxy‐terminal domain of p53: regulative significance. Oncol Res 10: 55–57.
17. Clayton, A.L., Rose, S., Barratt, M.J., Mahadevan, L.C. (2000) Phosphoacetylation of histone H3 on c‐fos‐ and c‐jun‐associated nucleosomes upon gene activation. EMBO J 19: 3714–3726. DOI: 10.1093/emboj/19.14.3714
18. Eisenbach, M. (1990) Functions of the flagellar modes of rotation in bacterial motility and chemotaxis. Mol Microbiol 4: 161–167.
19. Eisenbach, M. (1996) Control of bacterial chemotaxis. Mol Microbiol 20: 903–910.
20. Gu, W. & Roeder, R.G. (1997) Activation of p53 sequence‐specific DNA binding by acetylation of the p53 C‐terminal domain. Cell 90: 595–606.
21. Guzman, L.‐M., Belin, D., Carson, M.J., Beckwith, J. (1995) Tight regulation, modulation, and high‐level expression by vectors containing the arabinose P BAD promoter. J Bacteriol 177: 4121–4130.
22. Jasuja, R., Keyoung, J., Reid, G.P., Trentham, D.R., Khan, S. (1999) Chemotactic responses of Escherichia coli to small jumps of photoreleased l‐aspartate. Biophys J 76: 1706–1719.
23. Kaiser, A.D. & Hogness, D.S. (1960) The transformation of Escherichia coli with deoxyribonucleic acid isolated from bacteriophage λdg. J Mol Biol 2: 392–415.
24. Khan, S. (2000) On bacterial tactic response times and latencies. Biophys J 78: 2186–2187.
25. Khan, S., Castellano, F., Spudich, J.L., McCray, J.A., Goody, R.S., Reid, G.P., Trentham, D.R. (1993) Excitatory signaling in bacteria probed by caged chemoeffectors. Biophys J 65: 2368–2382.
26. Khlebnikov, A., Risa, O., Skaug, T., Carrier, T.A., Keasling, J.D. (2000) Regulatable arabinose‐inducible gene expression system with consistent control in all cells of a culture. J Bacteriol 182: 7029–7034.
27. Kumari, S., Tishel, R., Eisenbach, M., Wolfe, A.J. (1995) Cloning, characterization, and functional expression of acs, the gene which encodes acetyl‐coenzyme A synthetase in Escherichia coli. J Bacteriol 177: 2878–2886.
28. Kuo, S.C. & Koshland, D.E., Jr (1989) Multiple kinetic states for the flagellar motor switch. J Bacteriol 171: 6279–6287.
29. Lambert, P.F., Kashanchi, F., Radonovich, M.F., Shiekhattar, R., Brady, J.N. (1998) Phosphorylation of p53 serine increases interaction with CBP. J Biol Chem 273: 33048–33053.
30. Larsen, S.H., Reader, R.W., Kort, E.N., Tso, W.‐W., Adler, J. (1974) Change in direction of flagellar rotation is the basis of the chemotactic response in Escherichia coli. Nature 249: 74–77.
31. Lo, W.S., Trievel, R.C., Rojas, J.R., Duggan, L., Hsu, J.Y., Allis, C.D., et al. (2000) Phosphorylation of serine 10 in histone H3 is functionally linked in vitro and in vivo to Gcn5‐mediated acetylation at lysine 14. Mol Cell 5: 917–926.
32. Lukat, G.S., Lee, B.H., Mottonen, J.M., Stock, A., Stock, J.B. (1991) Roles of the highly conserved aspartate and lysine residues in the response regulator of bacterial chemotaxis. J Biol Chem 266: 8348–8354.
33. Macnab, R.M. (1995) Flagellar switch. In Two‐Component Signal Transduction. Hoch, J.A., and Silhavy, T.J. (eds). Washington, DC: American Society for Microbiology Press, pp. 181–199.
34. Martinez‐Balbas, M.A., Bauer, U.M., Nielsen, S.J., Brehm, A., Kouzarides, T. (2000) Regulation of E2F1 activity by acetylation. EMBO J 19: 662–671. DOI: 10.1093/emboj/19.4.662
35. Marzio, G., Wagener, C., Gutierrez, M.I., Cartwright, P., Helin, K., Giacca, M. (2000) E2F family members are differentially regulated by reversible acetylation. J Biol Chem 275: 10887–10892.
36. Ordal, G.W. & Adler, J. (1974) Isolation and complementation of mutants in galactose taxis and transport. J Bacteriol 117: 509–516.
37. Parkinson, J.S. (1978) Complementation analysis and deletion mapping of Escherichia coli mutants defective in chemotaxis. J Bacteriol 135: 45–53.
38. Parkinson, J.S. (1981) Genetics of bacterial chemotaxis. Soc Gen Microbiol Symp 31: 265–290.
39. Polesskaya, A., Duquet, A., Naguibneva, I., Weise, C., Vervisch, A., Bengal, E., et al. (2000) CREB‐binding Protein/p300 activates MyoD by acetylation. J Biol Chem 275: 34359–34364.
40. Prüss, B.M. & Wolfe, A.J. (1994) Regulation of acetyl phosphate synthesis and degradation, and the control of flagellar expression in Escherichia coli. Mol Microbiol 12: 973–984.
41. Ramakrishnan, R., Schuster, M., Bourret, R.B. (1998) Acetylation at Lys‐92 enhances signaling by the chemotaxis response regulator protein CheY. Proc Natl Acad Sci USA 95: 4918–4923.
42. Ravid, S. & Eisenbach, M. (1983) Correlation between bacteriophage chi adsorption and mode of flagellar rotation of Escherichia coli chemotaxis mutants. J Bacteriol 154: 604–611.
43. Robinson, V.L., Buckler, D.R., Stock, A.M. (2000) A tale of two components: a novel kinase and a regulatory switch. Nature Struct Biol 7: 626–633.
44. Sartorelli, V., Puri, P.L., Hamamori, Y., Ogryzko, V., Chung, G., Nakatani, Y., et al. (1999) Acetylation of MyoD directed by PCAF is necessary for the execution of the muscle program. Mol Cell 4: 725–734.
45. Shin, S., Song, S.G., Lee, D.S., Pan, J.G., Park, C. (1997) Involvement of iclR and rpoS in the induction of acs, the gene for acetyl coenzyme A synthetase of Escherichia coli K‐12. FEMS Microbiol Lett 146: 103–108. DOI: 10.1016/s0378-1097(96)00461-2
46. Siegele, D.A. & Hu, J.C. (1997) Gene expression from plasmids containing the araBAD promoter at subsaturating inducer concentrations represents mixed populations. Proc Natl Acad Sci USA 94: 8168–8172.
47. Silverman, M. & Simon, M. (1974) Flagellar rotation and the mechanism of bacterial motility. Nature 249: 73–74.
48. Silversmith, R.E. & Bourret, R.B. (1999) Throwing the switch in bacterial chemotaxis. Trends Microbiol 7: 16–22. DOI: 10.1016/s0966-842x(98)01409-7
49. Springer, M.S., Goy, M.F., Adler, J. (1979) Protein methylation in behavioral control mechanisms and in signal transduction. Nature 280: 279–284.
50. Spudich, J.L. & Koshland, D.E., Jr (1975) Quantitation of the sensory response in bacterial chemotaxis. Proc Natl Acad Sci USA 72: 710–713.
51. Toker, A.S., Kihara, M., Macnab, R.M. (1996) Deletion analysis of the FliM flagellar switch protein of Salmonella typhimurium. J Bacteriol 178: 7069–7079.
52. Tomita, A., Towatari, M., Tsuzuki, S., Hayakawa, F., Kosugi, H., Tamai, K., et al. (2000) c‐Myb acetylation at the carboxyl‐terminal conserved domain by transcriptional co‐activator p300. Oncogene 19: 444–451.
53. Tso, W.‐W. & Adler, J. (1974) Negative chemotaxis in Escherichia coli. J Bacteriol 118: 560–576.
54. Valentin, H.E., Mitsky, T.A., Mahadeo, D.A., Tran, M., Gruys, K.J. (2000) Application of a propionyl coenzyme A synthetase for poly (3‐hydroxypropionate‐co‐3‐hydroxybutyrate) accumulation in recombinant Escherichia coli. Appl Environ Microbiol 66: 5253–5258.
55. Vogel, H.J. & Bonner, D.M. (1956) Acetylornithinase of Escherichia coli, partial purification and some properties. J Biol Chem 218: 97–106.
56. Volz, K. (1993) Structural conservation in the CheY superfamily. Biochemistry 32: 11741–11753.
57. Welch, M., Oosawa, K., Aizawa, S.‐I., Eisenbach, M. (1993) Phosphorylation‐dependent binding of a signal molecule to the flagellar switch of bacteria. Proc Natl Acad Sci USA 90: 8787–8791.
58. Wolfe, A.J., Conley, M.P., Kramer, T.J., Berg, H.C. (1987) Reconstitution of signaling in bacterial chemotaxis. J Bacteriol 169: 1878–1885.
59. Wolfe, A.J., Conley, M.P., Berg, H.C. (1988) Acetyladenylate plays a role in controlling the direction of flagellar rotation. Proc Natl Acad Sci USA 85: 6711–6715.
60. Yanisch‐Perron, C., Vieira, J., Messing, J. (1985) Improved M13 phage cloning vectors and host strains: nucleotide sequence of the M13mp18 and pUC19 vectors. Gene 33: 103–119.