Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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The Diversity of Lysine-Acetylated Proteins in Escherichia coli

  • Yu, Byung-Jo (Systems Microbiology Research Center, Korea Research Institute of Bioscience and Biotechnology) ;
  • Kim, Jung-Ae (Systems Microbiology Research Center, Korea Research Institute of Bioscience and Biotechnology) ;
  • Moon, Jeong-Hee (Systemic Proteomics Research Center, Korea Research Institute of Bioscience and Biotechnology) ;
  • Ryu, Seong-Eon (Systemic Proteomics Research Center, Korea Research Institute of Bioscience and Biotechnology) ;
  • Pan, Jae-Gu (Systems Microbiology Research Center, Korea Research Institute of Bioscience and Biotechnology)
  • Published : 2008.09.30
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Abstract

Acetylation of lysine residues in proteins is a reversible and highly regulated posttranslational modification. However, it has not been systematically studied in prokaryotes. By affinity immunoseparation using an anti-acetyllysine antibody together with nano-HPLC/MS/MS, we identified 125 lysine-acetylated sites in 85 proteins among proteins derived from Escherichia coli. The lysine-acetylated proteins identified are involved in diverse cellular functions including protein synthesis, carbohydrate metabolism, the TCA cycle, nucleotide and amino acid metabolism, chaperones, and transcription. Interestingly, we found a higher level of acetylation during the stationary phase than in the exponential phase; proteins acetylated during the stationary phase were immediately deacetylated when the cells were transferred to fresh LB culture medium. These results demonstrate that lysine acetylation is abundant in E. coli and might be involved in modifying or regulating the activities of various enzymes involved in critical metabolic processes and the synthesis of building blocks in response to environmental changes.

Keywords

References

  1. Barak, R., J. Yan, A. Shainskaya, and M. Eisenbach. 2006. The chemotaxis response regulator CheY can catalyze its own acetylation. J. Mol. Biol. 359: 251-265 https://doi.org/10.1016/j.jmb.2006.03.033
  2. Barak, R., K. Prasad, A. Shainskaya, A. J. Wolfe, and M. Eisenbach. 2004. Acetylation of the chemotaxis response regulator CheY by acetyl-CoA synthetase purified from Escherichia coli. J. Mol. Biol. 342: 383-401 https://doi.org/10.1016/j.jmb.2004.07.020
  3. Blander, G. and L. Guarente. 2004. The Sir2 family of protein deacetylases. Annu. Rev. Biochem. 73: 417-435 https://doi.org/10.1146/annurev.biochem.73.011303.073651
  4. Bordone, L. and L. Guarente. 2005. Calorie restriction, SIRT1 and metabolism: Understanding longevity. Nat. Rev. Mol. Cell Biol. 6: 298-305 https://doi.org/10.1038/nrm1616
  5. Brunet, A., L. B. Sweeney, J. F. Sturgill, K. F. Chua, P. L. Greer, Y. Lin, et al. 2004. Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science 303: 2011-2015 https://doi.org/10.1126/science.1094637
  6. Caron, C., C. Boyault, and S. Khochbin. 2005. Regulatory cross-talk between lysine acetylation and ubiquitination: Role in the control of protein stability. Bioessays 27: 408-415 https://doi.org/10.1002/bies.20210
  7. Carrozza, M. J., R. T. Utley, J. L. Workman, and J. Cote. 2003. The diverse functions of histone acetyltransferase complexes. Trends Genet. 19: 321-329 https://doi.org/10.1016/S0168-9525(03)00115-X
  8. Cohen, H. Y., C. Miller, K. J. Bitterman, N. R. Wall, B. Hekking, B. Kessler, et al. 2004. Calorie restriction promotes mammalian cell survival by inducing the SIRT1 deacetylase. Science 305: 390-392 https://doi.org/10.1126/science.1099196
  9. Cohen, T. and T. P. Yao. 2004. AcK-knowledge reversible acetylation. Sci. STKE 245: 42
  10. Gardner, J. G., F. J. Grundy, T. M. Henkin, and J. C. Escalante- Semerena. 2006. Control of acetyl-coenzyme A synthetase (AcsA) activity by acetylation/deacetylation without $NAD^+$ involvement in Bacillus subtilis. J. Bacteriol. 188: 5460-5468 https://doi.org/10.1128/JB.00215-06
  11. Hubbert, C., A. Guardiola, R. Shao, Y. Kawaguchi, A. Ito, A. Nixon, M. Yoshida, X. F. Wang, and T. P. Yao. 2002. HDAC6 is a microtubule-associated deacetylase. Nature 417: 455-458 https://doi.org/10.1038/417455a
  12. Hughes, R. M. and M. L. Waters. 2006. Effects of lysine acetylation in a ${\beta}-hairpin$ peptide: Comparison of an $amide-{\pi}$ and a $cation-{\pi}$ interaction. J. Am. Chem. Soc. 128: 13586-13591 https://doi.org/10.1021/ja0648460
  13. Kaiser, C. and S. R. James. 2004. Acetylation of insulin receptor substrate-1 is permissive for tyrosine phosphorylation. BMC Biol. 2: 23 https://doi.org/10.1186/1741-7007-2-23
  14. Kim, S. C., R. Sprung, Y. Chen, Y. Xu, H. Ball, J. Pei, et al. 2006. Substrate and functional diversity of lysine acetylation revealed by a proteomics survey. Mol. Cell. 23: 607-618 https://doi.org/10.1016/j.molcel.2006.06.026
  15. Kouzarides, T. 2000. Acetylation: A regulatory modification to rival phosphorylation. EMBO J. 19: 1176-1179 https://doi.org/10.1093/emboj/19.6.1176
  16. Lahti, R., K. Pohjanoksa, T. Pitkaranta, P. Heikinheimo, T. Salminen, P. Meyer, and J. Heinonen. 1990. A site-directed mutagenesis study on Escherichia coli inorganic pyrophosphatase. Biochemistry 29: 5761-5766 https://doi.org/10.1021/bi00476a017
  17. McKinsey, T. A. and E. N. Olson. 2004. Cardiac histone acetylation - therapeutic opportunities abound. Trends Genet. 20: 206-213 https://doi.org/10.1016/j.tig.2004.02.002
  18. Starai, V. J. and J. C. Escalante-Semerena. 2004. Identification of the protein acetyltransferase (Pat) enzyme that acetylates acetyl-CoA synthetase in Salmonella enterica. J. Mol. Biol. 340: 1005-1012 https://doi.org/10.1016/j.jmb.2004.05.010
  19. Starai, V. J., I. Celic, R. N. Cole, J. D. Boeke, and J. C. Escalante-Semerena. 2002. Sir2-dependent activation of acetyl- CoA synthetase by deacetylation of active lysine. Science 298: 2390-2392 https://doi.org/10.1126/science.1077650
  20. Vidali, G., E. L. Gershey, and V. G. Allfrey. 1968. Chemical studies of histone acetylation. The distribution of ${\varepsilon}-N-acetyllysine$ in calf thymus histones. J. Biol. Chem. 243: 6361-6366
  21. Vaziri, H., S. K. Dessain, E. Ng Eaton, S. I. Imai, R. A. Frye, T. K. Pandita, L. Guarente, and R. A. Weinberg. 2001. $hSIR2^{SIRT1}$ functions as an NAD-dependent p53 deacetylase. Cell 107: 149-159 https://doi.org/10.1016/S0092-8674(01)00527-X
  22. Yang, X. J. 2004. The diverse superfamily of lysine acetyltransferases and their roles in leukemia and other diseases. Nucleic Acids Res. 32: 959-976 https://doi.org/10.1093/nar/gkh252