Protein lysine acetylation in bacteria: Current state of the art

Proteomics

Volumn 16, Issue 2, 2016, Pages 301-309

  Ouidir, Tassadit ^a,b,c   Kentache, Takfarinas ^a,b,c   Hardouin, Julie ^a,b,c  

^a CNRS   (France)

^b NORMANDIE UNIVERSITÉ   (France)

^c UNIVERSITY OF ROUEN   (France)

Author keywords

Bacteria; Lysine acetylation; Microbiology

Indexed keywords

LYSINE; BACTERIAL PROTEIN;

BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIAL VIRULENCE; BACTERIUM; CELL METABOLISM; EUKARYOTE; METABOLISM; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ACETYLATION; PROTEIN ANALYSIS; PROTEIN MODIFICATION; PROTEOMICS; REVIEW; ACETYLATION; HUMAN; PROTEIN PROCESSING;

ACETYLATION; BACTERIA; BACTERIAL PROTEINS; HUMANS; LYSINE; METABOLIC NETWORKS AND PATHWAYS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOMICS;

EID: 84956592602     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.201500258     Document Type: Review

References (78)

1. Priyaja, P., Jayesh, P., Correya, N. S., Sreelakshmi, B. et al., Antagonistic effect of Pseudomonas aeruginosa isolates from various ecological niches on Vibrio species pathogenic to crustaceans. J. Coast Life Med. 2014, 2, 76-84.
2. Seo, J., Lee, K. J., Post-translational modifications and their biological functions: proteomic analysis and systematic approaches. J. Biochem. Mol. Biol. 2004, 37, 35-44.
3. Kim, G. W., Yang, X. J., Comprehensive lysine acetylomes emerging from bacteria to humans. Trends Biochem. Sci. 2011, 36, 211-220.
4. Cain, J. A., Solis, N., Cordwell, S. J., Beyond gene expression: the impact of protein post-translational modifications in bacteria. J. Proteomics 2014, 97, 265-286.
5. Bonissone, S., Gupta, N., Romine, M., Bradshaw, R. A., Pevzner, P. A., N-terminal protein processing: a comparative proteogenomic analysis. Mol. Cell. Proteomics 2013, 12, 14-28.
6. Ouidir, T., Jarnier, F., Cosette, P., Jouenne, T., Hardouin, J., Characterization of N-terminal protein modifications in Pseudomonas aeruginosa PA14. J. Proteomics 2015, 114, 214-225.
7. Kentache, T., Jouenne, T., De, E., Hardouin, J., N-alpha and N-epsilon acetylation in Acinetobacter baumannii. In progress 2015.
8. Mukherjee, S., Hao, Y. H., Orth, K., A newly discovered post-translational modification-the acetylation of serine and threonine residues. Trends Biochem. Sci. 2007, 32, 210-216.
9. Paquette, N., Conlon, J., Sweet, C., Rus, F. et al., Serine/threonine acetylation of TGFbeta-activated kinase (TAK1) by Yersinia pestis YopJ inhibits innate immune signaling. Proc. Natl. Acad. Sci. U S A 2012, 109, 12710-12715.
10. Boyer, J. B., Dedieu, A., Armengaud, J., Verdie, P. et al., N- and O-acetylation of threonine residues in the context of proteomics. J. Proteomics 2014, 108, 369-372.
11. Jones, J. D., O'Connor, C. D., Protein acetylation in prokaryotes. Proteomics 2011, 11, 3012-3022.
12. Hu, L. I., Lima, B. P., Wolfe, A. J., Bacterial protein acetylation: the dawning of a new age. Mol. Microbiol. 2010, 77, 15-21.
13. Barak, R., Yan, J., Shainskaya, A., Eisenbach, M., The chemotaxis response regulator CheY can catalyze its own acetylation. J. Mol. Biol. 2006, 359, 251-265.
14. Weinert, B. T., Iesmantavicius, V., Wagner, S. A., Scholz, C. et al., Acetyl-phosphate is a critical determinant of lysine acetylation in E. coli. Mol. Cell. 2013, 51, 265-272.
15. Kuhn, M. L., Zemaitaitis, B., Hu, L. I., Sahu, A. et al., Structural, kinetic and proteomic characterization of acetyl phosphate-dependent bacterial protein acetylation. PloS one 2014, 9, e94816.
16. Vetting, M. W., de Carvalho, L. P., Roderick, S. L., Blanchard, J. S., A novel dimeric structure of the RimL Nalpha-acetyltransferase from Salmonella typhimurium. J. Biol. Chem. 2005, 280, 22108-22114.
17. Xie, L., Li, W., Xie, J., Prokaryotic Nepsilon-lysine acetylomes and implications for new antibiotics. J. Cell. Biochem. 2012, 113, 3601-3609.
18. Bernal, V., Castano-Cerezo, S., Gallego-Jara, J., Ecija-Conesa, A. et al., Regulation of bacterial physiology by lysine acetylation of proteins. Nat. Biotechnol. 2014, 31, 586-595.
19. Xie, L., Zeng, J., Luo, H., Pan, W., Xie, J., The roles of bacterial GCN5-related N-acetyltransferases. Crit. Rev. Eukaryot. Gene Expr. 2014, 24, 77-87.
20. Dyda, F., Klein, D. C., Hickman, A. B., GCN5-related N-acetyltransferases: a structural overview. Annu. Rev. Biophys. Biomol. Struct. 2000, 29, 81-103.
21. Allfrey, V. G., Faulkner, R., Mirsky, A. E., Acetylation and methylation of histones and their possible role in the regulation of Rna synthesis. Proc. Natl. Acad. Sci. U S A 1964, 51, 786-794.
22. Kouzarides, T., Acetylation: a regulatory modification to rival phosphorylation? Embo J. 2000, 19, 1176-1179.
23. Starai, V. J., Celic, I., Cole, R. N., Boeke, J. D., Escalante-Semerena, J. C., Sir2-dependent activation of acetyl-CoA synthetase by deacetylation of active lysine. Science 2002, 298, 2390-2392.
24. Barak, R., Eisenbach, M., Acetylation of the response regulator, CheY, is involved in bacterial chemotaxis. Mol. Microbiol. 2001, 40, 731-743.
25. Kim, S. C., Sprung, R., Chen, Y., Xu, Y. et al., Substrate and functional diversity of lysine acetylation revealed by a proteomics survey. Mol. Cell 2006, 23, 607-618.
26. Choudhary, C., Kumar, C., Gnad, F., Nielsen, M. L. et al., Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 2009, 325, 834-840.
27. Yu, B. J., Kim, J. A., Moon, J. H., Ryu, S. E., Pan, J. G., The diversity of lysine-acetylated proteins in Escherichia coli. J. Microbiol. Biotech. 2008, 18, 1529-1536.
28. Zhang, J., Sprung, R., Pei, J., Tan, X. et al., Lysine acetylation is a highly abundant and evolutionarily conserved modification in Escherichia coli. Mol. Cell. Proteomics 2009, 8, 215-225.
29. Zhang, K., Zheng, S., Yang, J. S., Chen, Y., Cheng, Z., Comprehensive profiling of protein lysine acetylation in Escherichia coli. J. Proteome Res. 2013, 12, 844-851.
30. Wu, X., Vellaichamy, A., Wang, D., Zamdborg, L. et al., Differential lysine acetylation profiles of Erwinia amylovora strains revealed by proteomics. J. Proteomics 2013, 79, 60-71.
31. Wang, Q., Zhang, Y., Yang, C., Xiong, H. et al., Acetylation of metabolic enzymes coordinates carbon source utilization and metabolic flux. Science 2010, 327, 1004-1007.
32. Ouidir, T., Cosette, P., Jouenne, T., Hardouin, J., Proteomic profiling of lysine acetylation in Pseudomonas aeruginosa reveals the diversity of acetylated proteins. Proteomics 2015, 0, 1-6.
33. Pan, J., Ye, Z., Cheng, Z., Peng, X. et al., Systematic analysis of the lysine acetylome in Vibrio parahemolyticus. J. Proteome Res. 2014, 13, 3294-3302.
34. Crosby, H. A., Pelletier, D. A., Hurst, G. B., Escalante-Semerena, J. C., System-wide studies of N-lysine acetylation in Rhodopseudomonas palustris reveal substrate specificity of protein acetyltransferases. J. Biol. Chem. 2012, 287, 15590-15601.
35. Okanishi, H., Kim, K., Masui, R., Kuramitsu, S., Acetylome with structural mapping reveals the significance of lysine acetylation in Thermus thermophilus. J. Proteome Res. 2013, 12, 3952-3968.
36. Mo, R., Yang, M., Chen, Z., Cheng, Z. et al., Acetylome analysis reveals the involvement of lysine acetylation in photosynthesis and carbon metabolism in the model Cyanobacterium synechocystissp. PCC 6803. J. Proteome Res. 2015, 14, 1275-1286.
37. Cao, X. J., Dai, J., Xu, H., Nie, S. et al., High-coverage proteome analysis reveals the first insight of protein modification systems in the pathogenic Spirochete leptospira interrogans. Cell Res. 2010, 20, 197-210.
38. Kim, D., Yu, B. J., Kim, J. A., Lee, Y. J. et al., The acetylproteome of Gram-positive model bacterium Bacillus subtilis. Proteomics 2013, 13, 1726-1736.
39. Lee, D. W., Kim, D., Lee, Y. J., Kim, J. A. et al., Proteomic analysis of acetylation in thermophilic Geobacillus kaustophilus. Proteomics 2013, 13, 2278-2282.
40. Huang, D., Li, Z. H., You, D., Zhou, Y., Ye, B. C., Lysine acetylproteome analysis suggests its roles in primary and secondary metabolism in Saccharopolyspora erythraea. Appl. Microbiol. Biotechno. 2015, 99, 1399-1413.
41. Liao, G., Xie, L., Li, X., Cheng, Z., Xie, J., Unexpected extensive lysine acetylation in the trump-card antibiotic producer Streptomyces roseosporus revealed by proteome-wide profiling. J. Proteomics 2014, 106, 260-269.
42. van Noort, V., Seebacher, J., Bader, S., Mohammed, S. et al., Cross-talk between phosphorylation and lysine acetylation in a genome-reduced bacterium. Mol. Syst. Biol. 2012, 8, 571.
43. Liu, F., Yang, M., Wang, X., Yang, S. et al., Acetylome analysis reveals diverse functions of lysine acetylation in Mycobacterium tuberculosis. Mol. Cell Proteomics 2014, 13, 3352-3366.
44. Xie, L., Wang, X., Zeng, J., Zhou, M. et al., Proteome-wide lysine acetylation profiling of the human pathogen Mycobacterium tuberculosis. Int. J. Biochem. Cell Biol. 2015, 59, 193-202.
45. Zhang, K., Tian, S., Fan, E., Protein lysine acetylation analysis: current MS-based proteomic technologies. Analyst 2013, 138, 1628-1636.
46. Guan, K. L., Yu, W., Lin, Y., Xiong, Y., Zhao, S., Generation of acetyllysine antibodies and affinity enrichment of acetylated peptides. Nat. Protoc. 2010, 5, 1583-1595.
47. Xu, W., Zhao, S., Generation and characterization of pan-specific anti-acetyllysine antibody. Methods Mol. Biol. 2013, 981, 137-150.
48. Qiang, L., Xiao, H., Campos, E. I., Ho, V. C., Li, G., Development of a PAN-specific, affinity-purified anti-acetylated lysine antibody for detection, identification, isolation, and intracellular localization of acetylated protein. J. Immunoassay Immunochem. 2005, 26, 13-23.
49. Garcia, B. A., Shabanowitz, J., Hunt, D. F., Characterization of histones and their post-translational modifications by mass spectrometry. Curr. Opin. Chem. Biol. 2007, 11, 66-73.
50. Trelle, M. B., Jensen, O. N., Utility of immonium ions for assignment of epsilon-N-acetyllysine-containing peptides by tandem mass spectrometry. Anal. Chem. 2008, 80, 3422-3430.
51. Macek, B., Mijakovic, I., Olsen, J. V., Gnad, F. et al., The serine/threonine/tyrosine phosphoproteome of the model bacterium Bacillus subtilis. Mol. Cell Proteomics 2007, 6, 697-707.
52. Macek, B., Gnad, F., Soufi, B., Kumar, C. et al., Phosphoproteome analysis of E. coli reveals evolutionary conservation of bacterial Ser/Thr/Tyr phosphorylation. Mol. Cell Proteomics 2008, 7, 299-307.
53. Soufi, B., Gnad, F., Jensen, P. R., Petranovic, D. et al., The Ser/Thr/Tyr phosphoproteome of Lactococcus lactis IL1403 reveals multiply phosphorylated proteins. Proteomics 2008, 8, 3486-3493.
54. Misra, S. K., Milohanic, E., Ake, F., Mijakovic, I. et al., Analysis of the serine/threonine/tyrosine phosphoproteome of the pathogenic bacterium Listeria monocytogenes reveals phosphorylated proteins related to virulence. Proteomics 2011, 11, 4155-4165.
55. Baeza, J., Dowell, J. A., Smallegan, M. J., Fan, J. et al., Stoichiometry of site-specific lysine acetylation in an entire proteome. J. Biol. Chem. 2014, 289, 21326-21338.
56. Soufi, B., Soares, N. C., Ravikumar, V., Macek, B., Proteomics reveals evidence of cross-talk between protein modifications in bacteria: focus on acetylation and phosphorylation. Curr. Opin Microbiol. 2012, 15, 357-363.
57. Baker, M. D., Wolanin, P. M., Stock, J. B., Signal transduction in bacterial chemotaxis. BioEssays 2006, 28, 9-22.
58. Topp, S., Gallivan, J. P., Guiding bacteria with small molecules and RNA. J. Am. Chem. Soc. 2007, 129, 6807-6811.
59. Yan, J., Barak, R., Liarzi, O., Shainskaya, A., Eisenbach, M., In vivo acetylation of CheY, a response regulator in chemotaxis of Escherichia coli. J. Mol. Biol. 2008, 376, 1260-1271.
60. Barak, R., Prasad, K., Shainskaya, A., Wolfe, A. J., Eisenbach, M., Acetylation of the chemotaxis response regulator CheY by acetyl-CoA synthetase purified from Escherichia coli. J. Mol biol. 2004, 342, 383-401.
61. Zhang, Z., Tan, M., Xie, Z., Dai, L. et al., Identification of lysine succinylation as a new post-translational modification. Nat. Chem. Biol. 2011, 7, 58-63.
62. Peng, C., Lu, Z., Xie, Z., Cheng, Z. et al., The first identification of lysine malonylation substrates and its regulatory enzyme. Mol. Cell Proteomics 2011, 10, M111 012658.
63. Lanouette, S., Mongeon, V., Figeys, D., Couture, J. F., The functional diversity of protein lysine methylation. Mol. Syst. Biol. 2014, 10, 724-749.
64. Masui, R., Takahata, Y., Inoue, M., Iio, Y. et al., Structural insights of post-translational modification sites in the proteome of Thermus thermophilus. J. Struct. Funct. Genomics 2014, 15, 137-151.
65. Starai, V. J., Escalante-Semerena, J. C., Identification of the protein acetyltransferase (Pat) enzyme that acetylates acetyl-CoA synthetase in Salmonella enterica. J. Mol Biol. 2004, 340, 1005-1012.
66. Thao, S., Escalante-Semerena, J. C., Control of protein function by reversible N-epsilon-lysine acetylation in bacteria. Curr. Opin. Microbiol. 2011, 14, 200-204.
67. Xing, S., Poirier, Y., The protein acetylome and the regulation of metabolism. Trends Plant Sci. 2012, 17, 423-430.
68. Eisenbach, M., A hitchhiker's guide through advances and conceptual changes in chemotaxis. J. Cell Physiol. 2007, 213, 574-580.
69. Zhang, Q. F., Gu, J., Gong, P., Wang, X. D. et al., Reversibly acetylated lysine residues play important roles in the enzymatic activity of Escherichia coli N-hydroxyarylamine O-acetyltransferase. FEBS J. 2013, 280, 1966-1979.
70. Liang, W., Deutscher, M. P., Post-translational modification of RNase R is regulated by stress-dependent reduction in the acetylating enzyme Pka (YfiQ). Rna 2012, 18, 37-41.
71. Lima, B. P., Antelmann, H., Gronau, K., Chi, B. K. et al., Involvement of protein acetylation in glucose-induced transcription of a stress-responsive promoter. Mol. Microbiol. 2011, 81, 1190-1204.
72. Ma, Q., Wood, T. K., Protein acetylation in prokaryotes increases stress resistance. Biochem. Biophys. Res. Commun. 2011, 410, 846-851.
73. Ren, J., Sang, Y., Ni, J., Tao, J. et al., Acetylation regulates survival of Salmonella typhimurium in acid stress. Appl. Environ. Microbiol. 2015, 81, 5675-5682.
74. Thao, S., Chen, C. S., Zhu, H., Escalante-Semerena, J. C., Nepsilon-lysine acetylation of a bacterial transcription factor inhibits Its DNA-binding activity. PloS one 2010, 5, e15123.
75. Hu, L. I., Chi, B. K., Kuhn, M. L., Filippova, E. V. et al., Acetylation of the response regulator RcsB controls transcription from a small RNA promoter. J. Bacteriol. 2013, 195, 4174-4186.
76. Majdalani, N., Hernandez, D., Gottesman, S., Regulation and mode of action of the second small RNA activator of RpoS translation, RprA. Mol. Microbiol. 2002, 46, 813-826.
77. Grove, A., Saavedra, T. C., The role of surface-exposed lysines in wrapping DNA about the bacterial histone-like protein HU. Biochemistry 2002, 41, 7597-7603.
78. Zhou, Y., Chen, T., Zhou, L., Fleming, J. et al., Discovery and characterization of Ku acetylation in Mycobacterium smegmatis. FEMS Microbiol. Lett. 2015, doi: 10.1093/femsle/fnu051.