Lysine succinylation is a frequently occurring modification in prokaryotes and eukaryotes and extensively overlaps with acetylation

Cell Reports

Volumn 4, Issue 4, 2013, Pages 842-851

  Weinert, Brian T ^a   Schölz, Christian ^a   Wagner, Sebastian A ^a   Iesmantavicius, Vytautas ^a   Su, Dan ^a   Daniel, Jeremy A ^a   Choudhary, Chunaram ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

LYSINE; SUCCINYL COENZYME A; TRICARBOXYLIC ACID;

ACETYLATION; ANIMAL CELL; ARTICLE; CITRIC ACID CYCLE; CONTROLLED STUDY; ENZYME METABOLISM; ESCHERICHIA COLI; EUKARYOTE; GENE MUTATION; GROWTH RATE; HELA CELL; HUMAN; HUMAN CELL; ION EXCHANGE CHROMATOGRAPHY; LIQUID CHROMATOGRAPHY; LIVER PARENCHYMA; MASS SPECTROMETRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROKARYOTE; PROTEIN MODIFICATION; QUANTITATIVE ANALYSIS; SACCHAROMYCES CEREVISIAE; SUCCINYLATION; TANDEM MASS SPECTROMETRY;

ACETYLATION; ACYL COENZYME A; AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; CITRIC ACID CYCLE; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HELA CELLS; HUMANS; LYSINE; MICE; MOLECULAR SEQUENCE DATA; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOME; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EUKARYOTA; PROKARYOTA;

EID: 84883307077     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2013.07.024     Document Type: Article

References (53)

1. Arikawa Y., Kuroyanagi T., Shimosaka M., Muratsubaki H., Enomoto K., Kodaira R., Okazaki M. Effect of gene disruptions of the TCA cycle on production of succinic acid in Saccharomyces cerevisiae. J.Biosci. Bioeng. 1999, 87:28-36.
2. Baba T., Ara T., Hasegawa M., Takai Y., Okumura Y., Baba M., Datsenko K.A., Tomita M., Wanner B.L., Mori H. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol. Syst. Biol. 2006, 2:0008.
3. Cai L., Sutter B.M., Li B., Tu B.P. Acetyl-CoA induces cell growth and proliferation by promoting the acetylation of histones at growth genes. Mol. Cell 2011, 42:426-437.
4. Chen Y., Sprung R., Tang Y., Ball H., Sangras B., Kim S.C., Falck J.R., Peng J., Gu W., Zhao Y. Lysine propionylation and butyrylation are novel post-translational modifications in histones. Mol. Cell. Proteomics 2007, 6:812-819.
5. Chen Y., Zhang J., Lin Y., Lei Q., Guan K.L., Zhao S., Xiong Y. Tumour suppressor SIRT3 deacetylates and activates manganese superoxide dismutase to scavenge ROS. EMBO Rep. 2011, 12:534-541.
6. Choudhary C., Kumar C., Gnad F., Nielsen M.L., Rehman M., Walther T.C., Olsen J.V., Mann M. Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 2009, 325:834-840.
7. Colaert N., Helsens K., Martens L., Vandekerckhove J., Gevaert K. Improved visualization of protein consensus sequences by iceLogo. Nat. Methods 2009, 6:786-787.
8. Cox J., Mann M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 2008, 26:1367-1372.
9. Cox J., Neuhauser N., Michalski A., Scheltema R.A., Olsen J.V., Mann M. Andromeda: a peptide search engine integrated into the MaxQuant environment. J.Proteome Res. 2011, 10:1794-1805.
10. Du J., Zhou Y., Su X., Yu J.J., Khan S., Jiang H., Kim J., Woo J., Kim J.H., Choi B.H., et al. Sirt5 is a NAD-dependent protein lysine demalonylase and desuccinylase. Science 2011, 334:806-809.
11. Elias J.E., Gygi S.P. Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry. Nat. Methods 2007, 4:207-214.
12. Ghaemmaghami S., Huh W.K., Bower K., Howson R.W., Belle A., Dephoure N., O'Shea E.K., Weissman J.S. Global analysis of protein expression in yeast. Nature 2003, 425:737-741.
13. Guan K.L., Xiong Y. Regulation of intermediary metabolism by protein acetylation. Trends Biochem. Sci. 2010, 36:108-116.
14. Haigis M.C., Mostoslavsky R., Haigis K.M., Fahie K., Christodoulou D.C., Murphy A.J., Valenzuela D.M., Yancopoulos G.D., Karow M., Blander G., et al. SIRT4 inhibits glutamate dehydrogenase and opposes the effects of calorie restriction in pancreatic beta cells. Cell 2006, 126:941-954.
15. Hallows W.C., Yu W., Smith B.C., Devries M.K., Ellinger J.J., Someya S., Shortreed M.R., Prolla T., Markley J.L., Smith L.M., et al. Sirt3 promotes the urea cycle and fatty acid oxidation during dietary restriction. Mol. Cell 2011, 41:139-149.
16. Hausinger R.P. FeII/alpha-ketoglutarate-dependent hydroxylases and related enzymes. Crit. Rev. Biochem. Mol. Biol. 2004, 39:21-68.
17. Henriksen P., Wagner S.A., Weinert B.T., Sharma S., Bacinskaja G., Rehman M., Juffer A.H., Walther T.C., Lisby M., Choudhary C. Proteome-wide analysis of lysine acetylation suggests its broad regulatory scope in Saccharomyces cerevisiae. Mol. Cell. Proteomics 2012, 11:1510-1522.
18. Hirschey M.D., Shimazu T., Goetzman E., Jing E., Schwer B., Lombard D.B., Grueter C.A., Harris C., Biddinger S., Ilkayeva O.R., et al. SIRT3 regulates mitochondrial fatty-acid oxidation by reversible enzyme deacetylation. Nature 2010, 464:121-125.
19. Hirschey M.D., Shimazu T., Huang J.Y., Schwer B., Verdin E. SIRT3 regulates mitochondrial protein acetylation and intermediary metabolism. Cold Spring Harb. Symp. Quant. Biol. 2011, 76:267-277.
20. Huang da W., Sherman B.T., Lempicki R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 2009, 4:44-57.
21. Huh W.K., Falvo J.V., Gerke L.C., Carroll A.S., Howson R.W., Weissman J.S., O'Shea E.K. Global analysis of protein localization in budding yeast. Nature 2003, 425:686-691.
22. Kawai Y., Fujii H., Okada M., Tsuchie Y., Uchida K., Osawa T. Formation of Nepsilon-(succinyl)lysine invivo: a novel marker for docosahexaenoic acid-derived protein modification. J.Lipid Res. 2006, 47:1386-1398.
23. Kelstrup C.D., Young C., Lavallee R., Nielsen M.L., Olsen J.V. Optimized fast and sensitive acquisition methods for shotgun proteomics on a quadrupole orbitrap mass spectrometer. J.Proteome Res. 2012, Published online May 10, 2012.
24. Kim S.C., Sprung R., Chen Y., Xu Y., Ball H., Pei J., Cheng T., Kho Y., Xiao H., Xiao L., et al. Substrate and functional diversity of lysine acetylation revealed by a proteomics survey. Mol. Cell 2006, 23:607-618.
25. Kim E.Y., Kim W.K., Kang H.J., Kim J.H., Chung S.J., Seo Y.S., Park S.G., Lee S.C., Bae K.H. Acetylation of malate dehydrogenase 1 promotes adipogenic differentiation via activating its enzymatic activity. J.Lipid Res. 2012, 53:1864-1876.
26. Lin H., Su X., He B. Protein lysine acylation and cysteine succination by intermediates of energy metabolism. ACS Chem. Biol. 2012, 7:947-960.
27. Michalski A., Damoc E., Hauschild J.P., Lange O., Wieghaus A., Makarov A., Nagaraj N., Cox J., Mann M., Horning S. Mass spectrometry-based proteomics using Q Exactive, a high-performance benchtop quadrupole Orbitrap mass spectrometer. Mol. Cell. Proteomics 2011, 10. M111.011015.
28. Montellier E., Rousseaux S., Zhao Y., Khochbin S. Histone crotonylation specifically marks the haploid male germ cell gene expression program: post-meiotic male-specific gene expression. Bioessays 2012, 34:187-193.
29. Nakagawa T., Lomb D.J., Haigis M.C., Guarente L. SIRT5 Deacetylates carbamoyl phosphate synthetase 1 and regulates the urea cycle. Cell 2009, 137:560-570.
30. Olsen J.V., Macek B., Lange O., Makarov A., Horning S., Mann M. Higher-energy C-trap dissociation for peptide modification analysis. Nat. Methods 2007, 4:709-712.
31. Ong S.E., Blagoev B., Kratchmarova I., Kristensen D.B., Steen H., Pandey A., Mann M. Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol. Cell. Proteomics 2002, 1:376-386.
32. Pagliarini D.J., Calvo S.E., Chang B., Sheth S.A., Vafai S.B., Ong S.E., Walford G.A., Sugiana C., Boneh A., Chen W.K., et al. A mitochondrial protein compendium elucidates complex I disease biology. Cell 2008, 134:112-123.
33. Paik W.K., Pearson D., Lee H.W., Kim S. Nonenzymatic acetylation of histones with acetyl-CoA. Biochim. Biophys. Acta 1970, 213:513-522.
34. Peng C., Lu Z., Xie Z., Cheng Z., Chen Y., Tan M., Luo H., Zhang Y., He W., Yang K., et al. The first identification of lysine malonylation substrates and its regulatory enzyme. Mol. Cell. Proteomics 2011, 10. M111.012658.
35. Przybyla-Zawislak B., Dennis R.A., Zakharkin S.O., McCammon M.T. Genes of succinyl-CoA ligase from Saccharomyces cerevisiae. Eur. J. Biochem. 1998, 258:736-743.
36. Rappsilber J., Mann M., Ishihama Y. Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips. Nat. Protoc. 2007, 2:1896-1906.
37. Repetto B., Tzagoloff A. Structure and regulation of KGD1, the structural gene for yeast alpha-ketoglutarate dehydrogenase. Mol. Cell. Biol. 1989, 9:2695-2705.
38. Rosen R., Becher D., Büttner K., Biran D., Hecker M., Ron E.Z. Probing the active site of homoserine trans-succinylase. FEBS Lett. 2004, 577:386-392.
39. Schwanhäusser B., Busse D., Li N., Dittmar G., Schuchhardt J., Wolf J., Chen W., Selbach M. Global quantification of mammalian gene expression control. Nature 2011, 473:337-342.
40. Takahashi H., McCaffery J.M., Irizarry R.A., Boeke J.D. Nucleocytosolic acetyl-coenzyme a synthetase is required for histone acetylation and global transcription. Mol. Cell 2006, 23:207-217.
41. Tan M., Luo H., Lee S., Jin F., Yang J.S., Montellier E., Buchou T., Cheng Z., Rousseaux S., Rajagopal N., et al. Identification of 67 histone marks and histone lysine crotonylation as a new type of histone modification. Cell 2011, 146:1016-1028.
42. Tao R., Coleman M.C., Pennington J.D., Ozden O., Park S.H., Jiang H., Kim H.S., Flynn C.R., Hill S., Hayes McDonald W., et al. Sirt3-mediated deacetylation of evolutionarily conserved lysine 122 regulates MnSOD activity in response to stress. Mol. Cell 2010, 40:893-904.
43. Ting L., Rad R., Gygi S.P., Haas W. MS3 eliminates ratio distortion in isobaric multiplexed quantitative proteomics. Nat. Methods 2011, 8:937-940.
44. Weinert B.T., Wagner S.A., Horn H., Henriksen P., Liu W.R., Olsen J.V., Jensen L.J., Choudhary C. Proteome-wide mapping of the Drosophila acetylome demonstrates a high degree of conservation of lysine acetylation. Sci. Signal. 2011, 4:ra48.
45. Weinert B.T., Iesmantavicius V., Wagner S.A., Schölz C., Gummesson B., Beli P., Nyström T., Choudhary C. Acetyl-Phosphate Is a Critical Determinant of Lysine Acetylation in E. coli. Mol. Cell 2013, 51:265-272. 10.1016/j.molcel.2013.06.003.
46. Wellen K.E., Thompson C.B. A two-way street: reciprocal regulation of metabolism and signalling. Nat. Rev. 2012, 13:270-276.
47. Wellen K.E., Hatzivassiliou G., Sachdeva U.M., Bui T.V., Cross J.R., Thompson C.B. ATP-citrate lyase links cellular metabolism to histone acetylation. Science 2009, 324:1076-1080.
48. Wiśniewski J.R., Zougman A., Mann M. Combination of FASP and StageTip-based fractionation allows in-depth analysis of the hippocampal membrane proteome. J.Proteome Res. 2009, 8:5674-5678.
49. Xie Z., Dai J., Dai L., Tan M., Cheng Z., Wu Y., Boeke J.D., Zhao Y. Lysine succinylation and lysine malonylation in histones. Mol. Cell. Proteomics 2012, 11:100-107.
50. Yi C.H., Pan H., Seebacher J., Jang I.H., Hyberts S.G., Heffron G.J., Vander Heiden M.G., Yang R., Li F., Locasale J.W., et al. Metabolic regulation of protein N-alpha-acetylation by Bcl-xL promotes cell survival. Cell 2011, 146:607-620.
51. Yu W., Lin Y., Yao J., Huang W., Lei Q., Xiong Y., Zhao S., Guan K.L. Lysine 88 acetylation negatively regulates ornithine carbamoyltransferase activity in response to nutrient signals. J.Biol. Chem. 2009, 284:13669-13675.
52. Zhang Z., Tan M., Xie Z., Dai L., Chen Y., Zhao Y. Identification of lysine succinylation as a new post-translational modification. Nat. Chem. Biol. 2011, 7:58-63.
53. Zhao S., Xu W., Jiang W., Yu W., Lin Y., Zhang T., Yao J., Zhou L., Zeng Y., Li H., et al. Regulation of cellular metabolism by protein lysine acetylation. Science 2010, 327:1000-1004.