System-wide studies of N-lysine acetylation in Rhodopseudomonas palustris reveal substrate specificity of protein acetyltransferases

Journal of Biological Chemistry

Volumn 287, Issue 19, 2012, Pages 15590-15601

  Crosby, Heidi A ^a   Pelletier, Dale A ^b   Hurst, Gregory B ^b   Escalante Semerena, Jorge C ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b OAK RIDGE NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYL-COA; ACETYLATED PROTEINS; ACETYLTRANSFERASES; ACTIVE SITE; ACYL-COA; ACYL-COA SYNTHETASE; GLYCERALDEHYDE-3-PHOSPHATE DEHYDROGENASE; IN-VITRO; LC/MS/MS; LYSINE RESIDUES; METABOLIC ENZYMES; POST-TRANSLATIONAL MODIFICATIONS; PROTEOBACTERIUM; RHODOPSEUDOMONAS PALUSTRIS; SALMONELLA ENTERICA; SUBSTRATE RANGE; SUBSTRATE SPECIFICITY; SYNTHETASES; TAUTOMERASE;

AMINO ACIDS; ENZYMES; METABOLISM; PROTEINS; SALMONELLA;

ACETYLATION;

ACYLTRANSFERASE; ACYLTRANSFERASE KATA; ACYLTRANSFERASE PAT; DEACETYLASE; DEACETYLASE LDAA; DEACETYLASE SRTN; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; LONG CHAIN FATTY ACID COENZYME A LIGASE; LYSINE; PROTEIN RPA1177; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ACETYLATION; ARTICLE; CONTROLLED STUDY; DEACETYLATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME REGULATION; ENZYME SPECIFICITY; ENZYME SUBSTRATE; IN VITRO STUDY; LIQUID CHROMATOGRAPHY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; RHODOPSEUDOMONAS PALUSTRIS; TANDEM MASS SPECTROMETRY;

ACETATE-COA LIGASE; ACETYLATION; ACETYLTRANSFERASES; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CHROMATOGRAPHY, LIQUID; ELECTROPHORESIS, POLYACRYLAMIDE GEL; GLYCERALDEHYDE-3-PHOSPHATE DEHYDROGENASES; ISOMERASES; LYSINE; MASS SPECTROMETRY; MOLECULAR SEQUENCE DATA; RHODOPSEUDOMONAS; SEQUENCE HOMOLOGY, AMINO ACID; SUBSTRATE SPECIFICITY;

BACTERIA (MICROORGANISMS); EUKARYOTA; PROKARYOTA; PROTEOBACTERIA; RHODOPSEUDOMONAS PALUSTRIS; SALMONELLA ENTERICA;

EID: 84860868848     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.352104     Document Type: Article

References (59)

1. Albaugh, B. N., Arnold, K. M., and Denu, J. M. (2011) KAT(ching) metabolism by the tail: insight into the links between lysine acetyltransferases and metabolism. Chembiochem 12, 290-298
2. Kim, G. W., and Yang, X. J. (2011) Comprehensive lysine acetylomes emerging from bacteria to humans. Trends. Biochem. Sci. 36, 211-220
3. Garrity, J., Gardner, J. G., Hawse, W., Wolberger, C., and Escalante-Semerena, J. C. (2007) N-Lysine propionylation controls the activity of propionyl-CoA synthetase. J. Biol. Chem. 282, 30239-30245 (Pubitemid 350035260)
4. Chen, Y., Sprung, R., Tang, Y., Ball, H., Sangras, B., Kim, S. C., Falck, J. R., Peng, J., Gu, W., and Zhao, Y. (2007) Lysine propionylation and butyrylation are novel post-translational modifications in histones. Mol. Cell. Proteomics 6, 812-819 (Pubitemid 46831933)
5. Zhang, Z., Tan, M., Xie, Z., Dai, L., Chen, Y., and Zhao, Y. (2011) Identification of lysine succinylation as a new post-translational modification. Nat. Chem. Biol. 7, 58-63
6. Peng, C., Lu, Z., Xie, Z., Cheng, Z., Chen, Y., Tan, M., Luo, H., Zhang, Y., He, W., Yang, K., Zwaans, B. M., Tishkoff, D., Ho, L., Lombard, D., He, T. C., Dai, J., Verdin, E., Ye, Y., and Zhao, Y. (2011) The first identification of lysine malonylation substrates and its regulatory enzyme. Mol. Cell. Proteomics 10, M111.012658
7. Du, J., Zhou, Y., Su, X., Yu, J. J., Khan, S., Jiang, H., Kim, J., Woo, J., Kim, J. H., Choi, B. H., He, B., Chen, W., Zhang, S., Cerione, R. A., Auwerx, J., Hao, Q., and Lin, H. (2011) Sirt5 is a NAD-dependent protein lysine demalonylase and desuccinylase. Science 334, 806-809
8. Lin, Y. Y., Lu, J. Y., Zhang, J., Walter, W., Dang, W., Wan, J., Tao, S. C., Qian, J., Zhao, Y., Boeke, J. D., Berger, S. L., and Zhu, H. (2009) Protein acetylation microarray reveals that NuA4 controls key metabolic target regulating gluconeogenesis. Cell 136, 1073-1084
9. Starai, V. J., Celic, I., Cole, R. N., Boeke, J. D., and Escalante-Semerena, J. C. (2002) Sir2-dependent activation of acetyl-CoA synthetase by deacetylation of active lysine. Science 298, 2390-2392 (Pubitemid 36014212)
10. Thao, S., and Escalante-Semerena, J. C. (2011) Control of protein function by reversible Nε-lysine acetylation in bacteria. Curr. Opin. Microbiol. 14, 200-204
11. Starai, V. J., and Escalante-Semerena, J. C. (2004) Acetyl-coenzyme A synthetase (AMP forming). Cell. Mol. Life Sci. 61, 2020-2030 (Pubitemid 39149892)
12. Koetsier, M. J., Jekel, P. A., van den Berg, M. A., Bovenberg, R. A., and Janssen, D. B. (2009) Characterization of a phenylacetate-CoA ligase from Penicillium chrysogenum. Biochem. J. 417, 467-476
13. Schaefer, A. L., Greenberg, E. P., Oliver, C. M., Oda, Y., Huang, J. J., Bittan-Banin, G., Peres, C. M., Schmidt, S., Juhaszova, K., Sufrin, J. R., and Harwood, C. S. (2008) A new class of homoserine lactone quorum-sensing signals. Nature 454, 595-599
14. Gardner, J. G., Grundy, F. J., Henkin, T. M., and Escalante-Semerena, J. C. (2006) Control of acetyl-coenzyme A synthetase (AcsA) activity by acetylation/deacetylation without NAD+ involvement in Bacillus subtilis. J. Bacteriol. 188, 5460-5468 (Pubitemid 44157302)
15. Crosby, H. A., Heiniger, E. K., Harwood, C. S., and Escalante-Semerena, J. C. (2010) Reversible Nε-lysine acetylation regulates the activity of acyl-CoA synthetases involved in anaerobic benzoate catabolism in Rhodopseudomonas palustris. Mol. Microbiol. 76, 874-888
16. Xu, H., Hegde, S. S., and Blanchard, J. S. (2011) Reversible acetylation and inactivation of Mycobacterium tuberculosis acetyl-CoA synthetase is dependent on cAMP. Biochemistry 50, 5883-5892
17. Starai, V. J., Takahashi, H., Boeke, J. D., and Escalante-Semerena, J. C. (2003) Short-chain fatty acid activation by acyl-coenzyme A synthetases requires SIR2 protein function in Salmonella enterica and Saccharomyces cerevisiae. Genetics 163, 545-555 (Pubitemid 36314538)
18. Hallows, W. C., Lee, S., and Denu, J. M. (2006) Sirtuins deacetylate and activate mammalian acetyl-CoA synthetases. Proc. Natl. Acad. Sci. U.S.A. 103, 10230-10235 (Pubitemid 44051149)
19. Schwer, B., Bunkenborg, J., Verdin, R. O., Andersen, J. S., and Verdin, E. (2006) Reversible lysine acetylation controls the activity of the mitochondrial enzyme acetyl-CoA synthetase 2. Proc. Natl. Acad. Sci. U.S.A. 103, 10224-10229 (Pubitemid 44051148)
20. Starai, V. J., and Escalante-Semerena, J. C. (2004) Identification of the protein acetyltransferase (Pat) enzyme that acetylates acetyl-CoA synthetase in Salmonella enterica. J. Mol. Biol. 340, 1005-1012 (Pubitemid 38968698)
21. Tanner, K. G., Landry, J., Sternglanz, R., and Denu, J. M. (2000) Silent information regulator 2 family of NAD- dependent histone/protein deacetylases generates a unique product, 1-O-acetyl-ADP-ribose. Proc. Natl. Acad. Sci. U.S.A. 97, 14178-14182 (Pubitemid 32016550)
22. Tanny, J. C., and Moazed, D. (2001) Coupling of histone deacetylation to NAD breakdown by the yeast silencing protein Sir2: evidence for acetyl transfer from substrate to an NAD breakdown product. Proc. Natl. Acad. Sci. U.S.A. 98, 415-420 (Pubitemid 32105055)
23. Denu, J. M. (2005) The Sir 2 family of protein deacetylases. Curr. Opin. Chem. Biol. 9, 431-440
24. Yang, X. J., and Seto, E. (2007) HATs and HDACs: from structure, function and regulation to novel strategies for therapy and prevention. Oncogene 26, 5310-5318
25. Egland, P. G., Gibson, J., and Harwood, C. S. (1995) Benzoate-coenzyme A ligase, encoded by badA, is one of three ligases able to catalyze benzoyl-coenzyme A formation during anaerobic growth of Rhodopseudomonas palustris on benzoate. J. Bacteriol. 177, 6545-6551
26. Yu, B. J., Kim, J. A., Moon, J. H., Ryu, S. E., and Pan, J. G. (2008) The diversity of lysine-acetylated proteins in Escherichia coli. J. Microbiol. Biotechnol. 18, 1529-1536
27. Zhang, J., Sprung, R., Pei, J., Tan, X., Kim, S., Zhu, H., Liu, C. F., Grishin, N. V., and Zhao, Y. (2009) Lysine acetylation is a highly abundant and evolutionarily conserved modification in Escherichia coli. Mol. Cell. Proteomics 8, 215-225
28. Wang, Q., Zhang, Y., Yang, C., Xiong, H., Lin, Y., Yao, J., Li, H., Xie, L., Zhao, W., Yao, Y., Ning, Z. B., Zeng, R., Xiong, Y., Guan, K. L., Zhao, S., and Zhao, G. P. (2010) Acetylation of metabolic enzymes coordinates carbon source utilization and metabolic flux. Science 327, 1004-1007
29. Thao, S., Chen, C. S., Zhu, H., and Escalante-Semerena, J. C. (2010) Nε-Lysine acetylation of a bacterial transcription factor inhibits Its DNA-binding activity. PLoS One 5, e15123
30. Bertani, G. (1951) Studies on lysogenesis. I. The mode of phage liberation by lysogenic Escherichia coli. J. Bacteriol. 62, 293-300
31. Bertani, G. (2004) Lysogeny at mid-twentieth century: P1, P2, and other experimental systems. J. Bacteriol. 186, 595-600
32. Larimer, F. W., Chain, P., Hauser, L., Lamerdin, J., Malfatti, S., Do, L., Land, M. L., Pelletier, D. A., Beatty, J. T., Lang, A. S., Tabita, F. R., Gibson, J. L., Hanson, T. E., Bobst, C., Torres, J. L., Peres, C., Harrison, F. H., Gibson, J., and Harwood, C. S. (2004) Complete genome sequence of the metabolically versatile photosynthetic bacterium Rhodopseudomonas palustris. Nat. Biotechnol. 22, 55-61 (Pubitemid 38057957)
33. Kim, M. K., and Harwood, C. S. (1991) Regulation of benzoate-CoA ligase in Rhodopseudomonas palustris. FEMS Microbiol. Lett. 83, 199-203
34. Bloch, K. D., and Grossman, B. (1995) in Current Protocols in Molecular Biology (Ausubel, F. M., Brent, R., Kingston, R. E., Moore, D. D., Seidman, J. G., Smith, J. A., and Struhl, K., eds) pp. Unit 3.1.1-3.1.21, Greene Publishing Associates and Wiley Interscience, New York
35. Schäfer, A., Tauch, A., Jäger, W., Kalinowski, J., Thierbach, G., and Pühler, A. (1994) Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum. Gene 145, 69-73
36. McDonald, W. H., Ohi, R., Miyamoto, D. T., Mitchison, T. J., and Yates, J. R. (2002) Comparison of three directly coupled HPLC MS/MS strategies for identification of proteins from complex mixtures: single dimension LC-MS/MS, 2-phase MudPIT, and 3-phase MudPIT. Int. J. Mass Spectrom. 219, 245-251
37. Hervey, W. J., 4th, Khalsa-Moyers, G., Lankford, P. K., Owens, E. T., McKeown, C. K., Lu, T. Y., Foote, L. J., Asano, K. G., Morrell-Falvey, J. L., McDonald, W. H., Pelletier, D. A., and Hurst, G. B. (2009) Evaluation of affinity-tagged protein expression strategies using local and global isotope ratio measurements. J. Proteome Res. 8, 3675-3688
38. Moore, R. E., Young, M. K., and Lee, T. D. (2002) Qscore: an algorithm for evaluating SEQUEST database search results. J. Am. Soc. Mass Spectrom. 13, 378-386 (Pubitemid 34280088)
39. Elias, J. E., Gibbons, F. D., King, O. D., Roth, F. P., and Gygi, S. P. (2004) Intensity-based protein identification by machine learning from a library of tandem mass spectra. Nat. Biotechnol. 22, 214-219 (Pubitemid 38160538)
40. Eng, J. K., Mccormack, A. L., and Yates, J. R. (1994) An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. J. Am. Soc. Mass Spectrom. 5, 976-989
41. Tabb, D. L., McDonald, W. H., and Yates, J. R., 3rd. (2002) DTASelect and Contrast: tools for assembling and comparing protein identifications from shotgun proteomics. J. Proteome Res. 1, 21-26
42. Tanner, S., Shu, H., Frank, A., Wang, L. C., Zandi, E., Mumby, M., Pevzner, P. A., and Bafna, V. (2005) InsPecT: identification of posttranslationally modified peptides from tandem mass spectra. Anal. Chem. 77, 4626-4639 (Pubitemid 41542287)
43. Rocco, C. J., Dennison, K. L., Klenchin, V. A., Rayment, I., and Escalante-Semerena, J. C. (2008) Construction and use of new cloning vectors for the rapid isolation of recombinant proteins from Escherichia coli. Plasmid 59, 231-237
44. Blommel, P. G., and Fox, B. G. (2007) A combined approach to improving large-scale production of tobacco etch virus protease. Protein Expr. Purif.55, 53-68 (Pubitemid 47259692)
45. Miroux, B., and Walker, J. E. (1996) Over-production of proteins in Escherichia coli: mutant hosts that allow synthesis of some membrane proteins and globular proteins at high levels. J. Mol. Biol. 260, 289-298 (Pubitemid 26254109)
46. Markowitz, V. M., Korzeniewski, F., Palaniappan, K., Szeto, E., Werner, G., Padki, A., Zhao, X., Dubchak, I., Hugenholtz, P., Anderson, I., Lykidis, A., Mavromatis, K., Ivanova, N., and Kyrpides, N. C. (2006) The integrated microbial genomes (IMG) system. Nucleic Acids Res. 34, D344-D348
47. Zheng, J., Lee, D. C., and Jia, Z. (2009) Purification, crystallization and preliminary x-ray analysis of isocitrate dehydrogenase kinase/phosphatase from Escherichia coli. Acta Chrystallogr. Sect. F Struct. Biol. Cryst. Commun. 65, 536-539
48. Reger, A. S., Carney, J. M., and Gulick, A. M. (2007) Biochemical and crystallographic analysis of substrate binding and conformational changes in acetyl-CoA synthetase. Biochemistry 46, 6536-6546 (Pubitemid 46870119)
49. Finn, R. D., Mistry, J., Schuster-Böckler, B., Griffiths-Jones, S., Hollich, V., Lassmann, T., Moxon, S., Marshall, M., Khanna, A., Durbin, R., Eddy, S. R., Sonnhammer, E. L., and Bateman, A. (2006) Pfam: clans, web tools and services. Nucleic Acids Res. 34, D247-D251
50. Searle, B. C., Turner, M., and Nesvizhskii, A. I. (2008) Improving sensitivity by probabilistically combining results from multiple MS/MS search methodologies. J. Proteome Res. 7, 245-253 (Pubitemid 351171137)
51. Meades, G., Jr., Benson, B. K., Grove, A., and Waldrop, G. L. (2010) A tale of two functions: enzymatic activity and translational repression by carboxyltransferase. Nucleic Acids Res. 38, 1217-1227
52. Liang, W., and Deutscher, M. P. (2012) Post-translational modification of RNase R is regulated by stress-dependent reduction in the acetylating enzyme Pka (YfiQ). RNA 18, 37-41
53. Lima, B. P., Antelmann, H., Gronau, K., Chi, B. K., Becher, D., Brinsmade, S. R., and Wolfe, A. J. (2011) Involvement of protein acetylation in glucose-induced transcription of a stress-responsive promoter. Mol. Microbiol. 81, 1190-1204
54. Liang, W., Malhotra, A., and Deutscher, M. P. (2011) Acetylation regulates the stability of a bacterial protein: growth stage-dependent modification of RNase R. Mol. Cell 44, 160-166
55. Chan, C. H., Garrity, J., Crosby, H. A., and Escalante-Semerena, J. C. (2011) In Salmonella enterica, the sirtuin-dependent protein acylation/deacylation system (SDPADS) maintains energy homeostasis during growth on low concentrations of acetate. Mol. Microbiol. 80, 168-183
56. Strader, M. B., Verberkmoes, N. C., Tabb, D. L., Connelly, H. M., Barton, J. W., Bruce, B. D., Pelletier, D. A., Davison, B. H., Hettich, R. L., Larimer, F. W., and Hurst, G. B. (2004) Characterization of the 70S ribosome from Rhodopseudomonas palustris using an integrated "top-down" and "bottom-up" mass spectrometric approach. J. Proteome Res. 3, 965-978 (Pubitemid 39425652)
57. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R., Thompson, J. D., Gibson, T. J., and Higgins, D. G. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947-2948 (Pubitemid 350162903)
58. Gouet, P., Courcelle, E., Stuart, D. I., and Métoz, F. (1999) ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics 15, 305-308 (Pubitemid 29213756)
59. Bailey, T. L., and Elkan, C. (1994) Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc. Int. Conf. Intell. Syst. Mol. Biol. 2, 28-36