Succinylome analysis reveals the involvement of lysine succinylation in metabolism in pathogenic Mycobacterium tuberculosis

Molecular and Cellular Proteomics

Volumn 14, Issue 4, 2015, Pages 796-811

  Yang, Mingkun ^a   Wang, Yan ^a   Chen, Ying ^a   Cheng, Zhongyi ^b   Gu, Jing ^c   Deng, Jiaoyu ^c   Bi, Lijun ^d   Chen, Chuangbin ^e   Mo, Ran ^a   Wang, Xude ^c   Ge, Feng ^a  

^a INSTITUTE OF HYDROBIOLOGY   (China)

^b TONGJI UNIVERSITY   (China)

^c WUHAN INSTITUTE OF VIROLOGY   (China)

^d INSTITUTE OF BIOPHYSICS   (China)

^e Jingjie PTM Biolabs (Hangzhou) Co Ltd   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYL COENZYME A SYNTHETASE; LYSINE; ACETATE COENZYME A LIGASE; BACTERIAL PROTEIN; CARBON; NICOTINAMIDE ADENINE DINUCLEOTIDE; SUCCINIC ACID DERIVATIVE;

AMINO ACID COMPOSITION; AMINO ACID METABOLISM; AMINO ACID SEQUENCE; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CARBON SOURCE; CELL LYSATE; CELL MEMBRANE; CELL METABOLISM; CELLULAR DISTRIBUTION; CHEMICAL MODIFICATION; CITRIC ACID CYCLE; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; ENERGY METABOLISM; ENZYME ACTIVITY; ENZYME CONFORMATION; ENZYME STABILITY; FATTY ACID METABOLISM; GLUCONEOGENESIS; GLYCOLYSIS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; IN VITRO STUDY; MOLECULAR DYNAMICS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; SITE DIRECTED MUTAGENESIS; SUCCINYLATION; TANDEM MASS SPECTROMETRY; CHEMISTRY; CONSERVED SEQUENCE; DRUG EFFECTS; IMMUNOBLOTTING; IMMUNOPRECIPITATION; METABOLISM; METABOLOME; METABOLOMICS; MOLECULAR GENETICS; PROTEIN MOTIF; PROTEIN TRANSPORT; REPRODUCIBILITY; WESTERN BLOTTING;

MYCOBACTERIUM TUBERCULOSIS;

ACETATE-COA LIGASE; AMINO ACID MOTIFS; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BLOTTING, WESTERN; CARBON; CONSERVED SEQUENCE; HUMANS; IMMUNOBLOTTING; IMMUNOPRECIPITATION; LYSINE; METABOLOME; METABOLOMICS; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE ANNOTATION; MOLECULAR SEQUENCE DATA; MYCOBACTERIUM TUBERCULOSIS; NAD; PROTEIN INTERACTION MAPS; PROTEIN TRANSPORT; REPRODUCIBILITY OF RESULTS; SUCCINATES;

EID: 84926431871     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M114.045922     Document Type: Article

References (85)

1. Olsen, J. V., and Mann, M. (2013) Status of large-scale analysis of post-translational modifications by mass spectrometry. Mol. Cell. Proteomics 12, 3444-3452
2. Zhao, Y., and Jensen, O. N. (2009) Modification-specific proteomics: strategies for characterization of post-translational modifications using enrichment techniques. Proteomics 9, 4632-4641
3. Miao, J., Lawrence, M., Jeffers, V., Zhao, F., Parker, D., Ge, Y., Sullivan, W. J., Jr., and Cui, L. (2013) Extensive lysine acetylation occurs in evolutionarily conserved metabolic pathways and parasite-specific functions during Plasmodium falciparum intraerythrocytic development. Mol. Microbiol. 89, 660-675
4. Zhao, S., Xu, W., Jiang, W., Yu, W., Lin, Y., Zhang, T., Yao, J., Zhou, L., Zeng, Y., Li, H., Li, Y., Shi, J., An, W., Hancock, S. M., He, F., Qin, L., Chin, J., Yang, P., Chen, X., Lei, Q., Xiong, Y., and Guan, K. L. (2010) Regulation of cellular metabolism by protein lysine acetylation. Science 327, 1000-1004
5. 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
6. Chen, Y., Zhao, W. H., Yang, J. S., Cheng, Z. Y., Luo, H., Lu, Z. K., Tan, M. J., Gu, W., and Zhao, Y. M. (2012) Quantitative acetylome analysis reveals the roles of SIRT1 in regulating diverse substrates and cellular pathways. Mol. Cell. Proteomics 11, 1048-1062
7. Xie, Z., Dai, J., Dai, L., Tan, M., Cheng, Z., Wu, Y., Boeke, J. D., and Zhao, Y. (2012) Lysine succinylation and lysine malonylation in histones. Mol. Cell. Proteomics 11, 100-107
8. 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
9. Montellier, E., Rousseaux, S., Zhao, Y., and Khochbin, S. (2012) Histone crotonylation specifically marks the haploid male germ cell gene expression program: post-meiotic male-specific gene expression. Bioessays 34, 187-193
10. Tan, M., Luo, H., Lee, S., Jin, F., Yang, J. S., Montellier, E., Buchou, T., Cheng, Z., Rousseaux, S., Rajagopal, N., Lu, Z., Ye, Z., Zhu, Q., Wysocka, J., Ye, Y., Khochbin, S., Ren, B., and Zhao, Y. (2011) Identification of 67 histone marks and histone lysine crotonylation as a new type of histone modification. Cell 146, 1016-1028
11. Zhang, K., Chen, Y., Zhang, Z., and Zhao, Y. (2009) Identification and verification of lysine propionylation and butyrylation in yeast core histones using PTMap software. J. Proteome Res. 8, 900-906
12. Cheng, Z., Tang, Y., Chen, Y., Kim, S., Liu, H., Li, S. S., Gu, W., and Zhao, Y. (2009) Molecular characterization of propionyllysines in nonhistone proteins. Mol. Cell. Proteomics 8, 45-52
13. 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
14. Colak, G., Xie, Z., Zhu, A. Y., Dai, L., Lu, Z., Zhang, Y., Wan, X., Chen, Y., Cha, Y. H., Lin, H., Zhao, Y., and Tan, M. (2013) Identification of lysine succinylation substrates and the succinylation regulatory enzyme CobB in Escherichia coli. Mol. Cell. Proteomics 12, 3509-3520
15. 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
16. Weinert, B. T., Schölz, C., Wagner, S. A., Iesmantavicius, V., Su, D., Daniel, J. A., and Choudhary, C. (2013) Lysine succinylation is a frequently occurring modification in prokaryotes and eukaryotes and extensively overlaps with acetylation. Cell Rep. 4, 842-851
17. Lin, H., Su, X., and He, B. (2012) Protein lysine acylation and cysteine succination by intermediates of energy metabolism. ACS Chem. Biol. 7, 947-960
18. Olsen, C. A. (2012) Expansion of the lysine acylation landscape. Angew. Chem. Int. Ed. Engl. 51, 3755-3756
19. Park, J., Chen, Y., Tishkoff, D. X., Peng, C., Tan, M., Dai, L., Xie, Z., Zhang, Y., Zwaans, B. M., Skinner, M. E., Lombard, D. B., and Zhao, Y. (2013) SIRT5-mediated lysine desuccinylation impacts diverse metabolic pathways. Mol. Cell 50, 919-930
20. Rardin, M. J., He, W., Nishida, Y., Newman, J. C., Carrico, C., Danielson, S. R., Guo, A., Gut, P., Sahu, A. K., Li, B., Uppala, R., Fitch, M., Riiff, T., Zhu, L., Zhou, J., Mulhern, D., Stevens, R. D., Ilkayeva, O. R., Newgard, C. B., Jacobson, M. P., Hellerstein, M., Goetzman, E. S., Gibson, B. W., and Verdin, E. (2013) SIRT5 regulates the mitochondrial lysine succinylome and metabolic networks. Cell Metab. 18, 920-933
21. Newman, J. C., He, W., and Verdin, E. (2012) Mitochondrial protein acylation and intermediary metabolism: regulation by sirtuins and implications for metabolic disease. J. Biol. Chem. 287, 42436-42443
22. He, W., Newman, J. C., Wang, M. Z., Ho, L., and Verdin, E. (2012) Mitochondrial sirtuins: regulators of protein acylation and metabolism. Trends Endocrinol. Metab. 23, 467-476
23. Ehrt, S., and Rhee, K. (2013) Mycobacterium tuberculosis metabolism and host interaction: mysteries and paradoxes. Curr. Top. Microbiol. Immunol. 374, 163-188
24. Team, E. E. (2013) WHO publishes Global tuberculosis report 2013. Euro. Surveill. 18, 20615
25. Corbett, E. L., Watt, C. J., Walker, N., Maher, D., Williams, B. G., Raviglione, M. C., and Dye, C. (2003) The growing burden of tuberculosis: global trends and interactions with the HIV epidemic. Arch. Intern. Med. 163, 1009-1021
26. Sun, G., Luo, T., Yang, C., Dong, X., Li, J., Zhu, Y., Zheng, H., Tian, W., Wang, S., Barry, C. E., 3rd, Mei, J., and Gao, Q. (2012) Dynamic population changes in Mycobacterium tuberculosis during acquisition and fixation of drug resistance in patients. J. Infect. Dis. 206, 1724-1733
27. Zhang, H., Li, D., Zhao, L., Fleming, J., Lin, N., Wang, T., Liu, Z., Li, C., Galwey, N., Deng, J., Zhou, Y., Zhu, Y., Gao, Y., Wang, T., Wang, S., Huang, Y., Wang, M., Zhong, Q., Zhou, L., Chen, T., Zhou, J., Yang, R., Zhu, G., Hang, H., Zhang, J., Li, F., Wan, K., Wang, J., Zhang, X. E., and Bi, L. (2013) Genome sequencing of 161 Mycobacterium tuberculosis isolates from China identifies genes and intergenic regions associated with drug resistance. Nat. Genet. 45, 1255-1260
28. Srinivasan, L., Ahlbrand, S., and Briken, V. (2014) Interaction of Mycobacterium tuberculosis with host cell death pathways. Cold Spring Harb. Perspect. Med. 4, a022459
29. Gengenbacher, M., and Kaufmann, S. H. (2012) Mycobacterium tuberculosis: success through dormancy. FEMS Microbiol. Rev. 36, 514-532
30. Boon, C., and Dick, T. (2012) How Mycobacterium tuberculosis goes to sleep: the dormancy survival regulator DosR a decade later. Future Microbiol. 7, 513-518
31. Wirth, T., Hildebrand, F., Allix-Beguec, C., Wolbeling, F., Kubica, T., Kremer, K., van Soolingen, D., Rusch-Gerdes, S., Locht, C., Brisse, S., Meyer, A., Supply, P., and Niemann, S. (2008) Origin, spread, and demography of the Mycobacterium tuberculosis complex. PLoS Pathog. 4, e1000160
32. de Carvalho, L. P., Fischer, S. M., Marrero, J., Nathan, C., Ehrt, S., and Rhee, K. Y. (2010) Metabolomics of Mycobacterium tuberculosis reveals compartmentalized co-catabolism of carbon substrates. Chem. Biol. 17, 1122-1131
33. Marrero, J., Rhee, K. Y., Schnappinger, D., Pethe, K., and Ehrt, S. (2010) Gluconeogenic carbon flow of tricarboxylic acid cycle intermediates is critical for Mycobacterium tuberculosis to establish and maintain infection. Proc. Natl. Acad. Sci. U.S.A. 107, 9819-9824
34. Shi, S., and Ehrt, S. (2006) Dihydrolipoamide acyltransferase is critical for Mycobacterium tuberculosis pathogenesis. Infect. Immun. 74, 56-63
35. Boshoff, H. I., and Barry, C. E., 3rd (2005) Tuberculosis - metabolism and respiration in the absence of growth. Nat. Rev. Microbiol. 3, 70-80
36. Mehrotra, P., Jamwal, S. V., Saquib, N., Sinha, N., Siddiqui, Z., Manivel, V., Chatterjee, S., and Rao, K. V. (2014) Pathogenicity of Mycobacterium tuberculosis is expressed by regulating metabolic thresholds of the host macrophage. PLoS Pathog. 10, e1004265
37. Chopra, T., Hamelin, R., Armand, F., Chiappe, D., Moniatte, M., and McKinney, J. D. (2014) Quantitative Mass Spectrometry reveals plasticity of metabolic networks in Mycobacterium smegmatis. Mol. Cell. Proteomics 13, 3014-3028
38. Eisenreich, W., Dandekar, T., Heesemann, J., and Goebel, W. (2010) Carbon metabolism of intracellular bacterial pathogens and possible links to virulence. Nat. Rev. Microbiol. 8, 401-412
39. Arora, N., and Banerjee, A. K. (2012) Targeting tuberculosis: a glimpse of promising drug targets. Mini Rev. Med. Chem. 12, 187-201
40. Camus, J. C., Pryor, M. J., Medigue, C., and Cole, S. T. (2002) Reannotation of the genome sequence of Mycobacterium tuberculosis H37Rv. Microbiology 148, 2967-2973
41. Meena, L. S., and Rajni (2010) Survival mechanisms of pathogenic Mycobacterium tuberculosis H37Rv. FEBS J. 277, 2416-2427
42. Yang, M. K., Qiao, Z. X., Zhang, W. Y., Xiong, Q., Zhang, J., Li, T., Ge, F., and Zhao, J. D. (2013) Global phosphoproteomic analysis reveals diverse functions of serine/threonine/tyrosine phosphorylation in the model cyanobacterium Synechococcus sp. Strain PCC 7002. J. Proteome Res. 12, 1909-1923
43. Cox, J., and Mann, M. (2008) MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26, 1367-1372
44. Chen, Y., Kwon, S. W., Kim, S. C., and Zhao, Y. M. (2005) Integrated approach for manual evaluation of peptides identified by searching protein sequence databases with tandem mass spectra. J. Proteome Res. 4, 998-1005
45. Macek, B., Gnad, F., Soufi, B., Kumar, C., Olsen, J. V., Mijakovic, I., and Mann, M. (2008) Phosphoproteome analysis of E. coli reveals evolutionary conservation of bacterial Ser/Thr/Tyr phosphorylation. Mol. Cell. Proteomics 7, 299-307
46. Conesa, A., and Gotz, S. (2008) Blast2GO: A comprehensive suite for functional analysis in plant genomics. Int. J. Plant Genomics 2008: 619832
47. Yu, N. Y., Wagner, J. R., Laird, M. R., Melli, G., Rey, S., Lo, R., Dao, P., Sahinalp, S. C., Ester, M., Foster, L. J., and Brinkman, F. S. (2010) PSORTb 3.0: improved protein subcellular localization prediction with refined localization subcategories and predictive capabilities for all prokaryotes. Bioinformatics 26, 1608-1615
48. Shannon, P., Markiel, A., Ozier, O., Baliga, N. S., Wang, J. T., Ramage, D., Amin, N., Schwikowski, B., and Ideker, T. (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13, 2498-2504
49. Maere, S., Heymans, K., and Kuiper, M. (2005) BiNGO: a Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics 21, 3448-3449
50. 18 prefractionation and titanium dioxide enrichment. J. Proteome Res. 9, 777-788
51. Huang, D. W., Sherman, B. T., and Lempicki, R. A. (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44-57
52. Huang, D. W., Sherman, B. T., and Lempicki, R. A. (2009) Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 37, 1-13
53. Wang, Y., Cui, T., Zhang, C., Yang, M., Huang, Y. X., Li, W. H., Zhang, L., Gao, C. H., He, Y., Li, Y. Q., Huang, F., Zeng, J. M., Huang, C., Yang, Q. O., Tian, Y. X., Zhao, C. C., Chen, H. C., Zhang, H., and He, Z. G. (2010) Global protein-protein interaction network in the human pathogen Mycobacterium tuberculosis H37Rv. J. Proteome Res. 9, 6665-6677
54. Schwartz, D., and Gygi, S. P. (2005) An iterative statistical approach to the identification of protein phosphorylation motifs from large-scale data sets. Nat. Biotechnol. 23, 1391-1398
55. Petersen, B., Petersen, T. N., Andersen, P., Nielsen, M., and Lundegaard, C. (2009) A generic method for assignment of reliability scores applied to solvent accessibility predictions. BMC Struct. Biol. 9, 51
56. Rose, I. A., Grunberg-Manago, M., Korey, S. R., and Ochoa, S. (1954) Enzymatic phosphorylation of acetate. J. Biol. Chem. 211, 737-756
57. Li, R., Gu, J., Chen, P., Zhang, Z. P., Deng, J. Y., and Zhang, X. E. (2011) Purification and characterization of the acetyl-CoA synthetase from Mycobacterium tuberculosis. Acta Biochim. Biophys. Sin. 43, 891-899
58. Hess, B., Kutzner, C., van der Spoel, D., and Lindahl, E. (2008) GROMACS 4: Algorithms for highly efficient, load-balanced, and scalable molecular simulation. J. Chem. Theory Comput. 4, 435-447
59. Kaminski, G. A., Friesner, R. A., Tirado-Rives, J., and Jorgensen, W. L. (2001) Evaluation and reparametrization of the OPLS-AA force field for proteins via comparison with accurate quantum chemical calculations on peptides. J. Phys. Chem. B 105, 6474-6487
60. Berendsen, H. J. C., Postma, J. P. M., van Gunsteren, W. F., and Hermans, J. (1981) Interaction models for water in relation to protein hydration. Intermolecular Forces, pp. 331-342, Springer Netherlands
61. Bussi, G., Donadio, D., and Parrinello, M. (2007) Canonical sampling through velocity rescaling. J. Chem. Phys. 126:014101
62. Hess, B., Bekker, H., Berendsen, H. J. C., and Fraaije, J. G. E. M. (1997) LINCS: A linear constraint solver for molecular simulations. J. Comput. Chem. 18, 1463-1472
63. Darden, T., York, D., and Pedersen, L. (1993) Particle mesh Ewald: an N·log(N) method for Ewald sums in large systems. J. Chem. Phys. 98, 10089-10092
64. Essmann, U., Perera, L., Berkowitz, M. L., Darden, T., Lee, H., and Pedersen, L. G. (1995) A smooth particle mesh Ewald method. J. Chem. Phys. 103, 8577-8593
65. Kabsch, W., and Sander, C. (1983) Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22, 2577-2637
66. Weinert, B. T., Iesmantavicius, V., Wagner, S. A., Scholz, C., Gummesson, B., Beli, P., Nystrom, T., and Choudhary, C. (2013) Acetyl-phosphate is a critical determinant of lysine acetylation in E. coli. Mol. Cell 51, 265-272
67. 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
68. 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
69. 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
70. Imai, S., Armstrong, C. M., Kaeberlein, M., and Guarente, L. (2000) Transcriptional silencing and longevity protein Sir2 is an NAD-dependent histone deacetylase. Nature 403, 795-800
71. Du, J. T., Zhou, Y. Y., Su, X. Y., 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. N. (2011) Sirt5 is a NAD-dependent protein lysine demalonylase and desuccinylase. Science 334, 806-809
72. Gu, J., Deng, J. Y., Li, R., Wei, H., Zhang, Z., Zhou, Y., Zhang, Y., and Zhang, X. E. (2009) Cloning and characterization of NAD-dependent protein deacetylase (Rv1151c) from Mycobacterium tuberculosis. Biochemistry 74, 743-748
73. 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
74. Zuber, B., Chami, M., Houssin, C., Dubochet, J., Griffiths, G., and Daffe, M. (2008) Direct visualization of the outer membrane of mycobacteria and corynebacteria in their native state. J. Bacteriol. 190, 5672-5680
75. Grzegorzewicz, A. E., Kordulakova, J., Jones, V., Born, S. E., Belardinelli, J. M., Vaquie, A., Gundi, V. A., Madacki, J., Slama, N., Laval, F., Vaubourgeix, J., Crew, R. M., Gicquel, B., Daffe, M., Morbidoni, H. R., Brennan, P. J., Quemard, A., McNeil, M. R., and Jackson, M. (2012) A common mechanism of inhibition of the Mycobacterium tuberculosis mycolic acid biosynthetic pathway by isoxyl and thiacetazone. J. Biol. Chem. 287, 38434-38441
76. Russell, D. G., Cardona, P. J., Kim, M. J., Allain, S., and Altare, F. (2009) Foamy macrophages and the progression of the human tuberculosis granuloma. Nat. Immunol. 10, 943-948
77. Shi, L., Sohaskey, C. D., Pfeiffer, C., Datta, P., Parks, M., McFadden, J., North, R. J., and Gennaro, M. L. (2010) Carbon flux rerouting during Mycobacterium tuberculosis growth arrest. Mol. Microbiol. 78, 1199-1215
78. Munoz-Elias, E. J., and McKinney, J. D. (2006) Carbon metabolism of intracellular bacteria. Cell. Microbiol. 8, 10-22
79. Liu, B., Lin, Y. H., Darwanto, A., Song, X. H., Xu, G. L., and Zhang, K. L. (2009) Identification and characterization of propionylation at histone H3 lysine 23 in mammalian cells. J. Biol. Chem. 284, 32288-32295
80. 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
81. Crosby, H. A., Heiniger, E. K., Harwood, C. S., and Escalante-Semerena, J. C. (2010) Reversible N epsilon-lysine acetylation regulates the activity of acyl-CoA synthetases involved in anaerobic benzoate catabolism in Rhodopseudomonas palustris. Mol. Microbiol. 76, 874-888
82. 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
83. Wellen, K. E., and Thompson, C. B. (2012) A two-way street: reciprocal regulation of metabolism and signaling. Nat. Rev. Mol. Cell Bio. 13, 270-276
84. Schluter, H., Apweiler, R., Holzhutter, H. G., and Jungblut, P. R. (2009) Finding one's way in proteomics: a protein species nomenclature. Chem. Cent. J. 3, 11
85. Jungblut, P. R., Holzhutter, H. G., Apweiler, R., and Schluter, H. (2008) The speciation of the proteome. Chem. Cent. J. 2, 16