Quantitating the Specificity and Selectivity of Gcn5-Mediated Acetylation of Histone H3

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Kuo, Yin Ming ^a   Andrews, Andrew J ^a  

^a FOX CHASE CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE ACETYLTRANSFERASE GCN5; HISTONE H3;

ARTICLE; CONTROLLED STUDY; ENZYME ASSAY; ENZYME MECHANISM; ENZYME SUBSTRATE; GENETIC CONSERVATION; HISTONE ACETYLATION; NUCLEOSOME; PROCESS OPTIMIZATION; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; STEADY STATE; TANDEM MASS SPECTROMETRY; ULTRA PERFORMANCE LIQUID CHROMATOGRAPHY; VALIDATION PROCESS;

ACETYL COENZYME A; ACETYLATION; AMINO ACID SEQUENCE; HISTONES; HUMANS; KINETICS; LYSINE; MASS SPECTROMETRY; MOLECULAR SEQUENCE DATA; NUCLEOSOMES; P300-CBP TRANSCRIPTION FACTORS; PEPTIDES; REPRODUCIBILITY OF RESULTS; STAINING AND LABELING; SUBSTRATE SPECIFICITY;

EID: 84874344108     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0054896     Document Type: Article

References (54)

1. Berger SL, (2002) Histone modifications in transcriptional regulation. Curr Opin Genet Dev 12: 142-148.
2. Seligson DB, Horvath S, McBrian MA, Mah V, Yu H, et al. (2009) Global levels of histone modifications predict prognosis in different cancers. Am J Pathol 174: 1619-1628.
3. Hou LF, Wang H, Sartori S, Gawron A, Lissowska J, et al. (2010) Blood leukocyte DNA hypomethylation and gastric cancer risk in a high-risk Polish population. Int J Cancer 127: 1866-1874.
4. Fabris S, Bollati V, Agnelli L, Morabito F, Motta V, et al. (2011) Biological and clinical relevance of quantitative global methylation of repetitive DNA sequences in chronic lymphocytic leukemia. Epigenetics 6: 188-194.
5. Sterner DE, Berger SL, (2000) Acetylation of histones and transcription-related factors. Microbiol. Mol Biol Rev 64: 435-459.
6. Lee KK, Workman JL, (2007) Histone acetyltransferase complexes: one size doesn't fit all. Nat Rev Mol Cell Biol 8: 284-295.
7. Fraga MF, Ballestar E, Villar-Garea A, Boix-Chornet M, Espada J, et al. (2005) Loss of acetylation at Lys16 and trimethylation at Lys20 of histone H4 is a common hallmark of human cancer. Nat Genet 37: 391-400.
8. Masumoto H, Hawke D, Kobayashi R, Verreault A, (2005) A role for cell-cycle-regulated histone H3 lysine 56 acetylation in the DNA damage response. Nature 436: 294-298.
9. Jenuwein T, Allis CD, (2001) Translating the histone code. Science 293: 1074-1080.
10. Oliver SS, Denu JM, (2011) Dynamic interplay between histone H3 modifications and protein interpreters: emerging evidence for a "histone language". ChemBioChem 12: 299-307.
11. Schiltz RL, Mizzen CA, Vassilev A, Cook RG, Allis CD, et al. (1999) Overlapping but distinct patterns of histone acetylation by the human coactivators p300 and PCAF within nucleosomal substrates. J Biol Chem 274: 1189-1192.
12. Lau OD, Courtney AD, Vassilev A, Marzilli LA, Cotter RJ, et al. (2000) p300/CBP-associated factor histone acetyltransferase processing of a peptide substrate. J Biol Chem 275: 21953-21959.
13. Trievel RC, Li FY, Marmorstein R, (2000) Application of a fluorescent histone acetyltransferase assay to probe the substrate specificity of the human p300/CBP-associated factor. Anal Biochem 287: 319-328.
14. Jiang L, Smith JN, Anderson SL, Ma P, Mizzen CA, et al. (2007) Global assessment of combinatorial post-translational modification of core histones in yeast using contemporary mass spectrometry: LYS4 trimethylation correlates with degree of acetylation on the same H3 tail. J Biol Chem 282: 27923-27934.
15. Berndsen CE, Denu JM, (2008) Catalysis and substrate selection by histone/protein lysine acetyltransferases. Curr Opin Struct Biol 18: 682-689.
16. Li TT, Du YP, Wang LK, Huang L, Li WL, et al. (2012) Characterization and prediction of lysine (K)-acetyl-transferase specific acetylation sites. Mol Cell Proteomics 11.1.
17. Kuo MH, Brownell JE, Sobel RE, Ranalli TA, Cook RG, et al. (1996) Transcription-linked acetylation by Gcn5p of histones H3 and H4 at specific lysines. Nature 383: 269-272.
18. Wellen KE, Hatzivassiliou G, Sachdeva UM, Bui TV, Cross JR, et al. (2009) ATP-citrate lyase links cellular metabolism to histone acetylation. Science 324: 1076-1080.
19. Neumann H, Peak-Chew SY, Chin JW, (2008) Genetically encoding N-epsilon-acetyllysine in recombinant proteins. Nat Chem Biol 4: 232-234.
20. Andrews AJ, Chen X, Zevin A, Stargell LA, Luger K, (2010) The histone chaperone Nap1 promotes nucleosome assembly by eliminating nonnucleosomal histone DNA interactions. Mol Cell 37: 834-842.
21. Rüchel R, (1981) Properties of a purified proteinase from the yeast Candida albicans. Biochim Biophys Acta 659: 99-113.
22. Hudgin RL, Pricer WE, Ashwell G, Stockert RJ, Morell AG, (1974) Isolation and properties of a rabbit liver binding-protein specific for asialoglycoproteins. J Biol Chem 249: 5536-5543.
23. Kim SC, Chen Y, Mirza S, Xu Y, Lee J, et al. (2006) A clean, more efficient method for in-solution digestion of protein mixtures without detergent or urea. J Proteome Res 5: 3446-3452.
24. Garcia BA, Mollah S, Ueberheide BM, Busby SA, Muratore TL, et al. (2007) Chemical derivatization of histones for facilitated analysis by mass spectrometry. Nature Protocols 2: 933-938.
25. Paik WK, Pearson D, Lee HW, Kim S, (1970) Nonenzymatic acetylation of histones with acetyl-CoA. Biochim Biophys Acta 213: 513-522.
26. Liu B, Lin YH, Darwanto A, Song XH, Xu GL, et al. (2009) Identification and Characterization of Propionylation at Histone H3 Lysine 23 in Mammalian Cells. J Biol Chem 284: 32288-32295.
27. Schneider TD, Arteaga-Salas JM, Mentele E, David R, Nicetto D, et al. (2011) Stage-specific histone modification profiles reveal global transitions in the xenopus embryonic epigenome. Plos One 6: e22548.
28. Kim Y, Tanner KG, Denu JM, (2000) A continuous, nonradioactive assay for histone acetyltransferases. Anal Biochem 280: 308-314.
29. Zhang LW, Eugeni EE, Parthun MR, Freitas MA, (2003) Identification of novel histone post-translational modifications by peptide mass fingerprinting. Chromosoma 112: 77-86.
30. McKittrick E, Gaften PR, Ahmad K, Henikoff S, (2004) Histone H3.3 is enriched in covalent modifications associated with active chromatin. Proc Natl Acad Sci U S A 101: 1525-1530.
31. Johnson L, Mollah S, Garcia BA, Muratore TL, Shabanowitz J, et al. (2004) Mass spectrometry analysis of Arabidopsis histone H3 reveals distinct combinations of post-translational modifications. Nucleic Acids Res 32: 6511-6518.
32. Garcia BA, Busby SA, Shabanowitz J, Hunt DF, Mishra N, (2005) Resetting the epigenetic histone code in the MRL-lpr/lpr mouse model of lupus by histone deacetylase inhibition. J Proteome Res 4: 2032-2042.
33. Hake SB, Garcia BA, Duncan EM, Kauer M, Dellaire G, et al. (2006) Expression patterns and post-translational modifications associated with mammalian histone H3 variants. J Biol Chem 281: 559-568.
34. Grant PA, Eberharter A, John S, Cook RG, Turner BM, et al. (1999) Expanded lysine acetylation specificity of Gcn5 in native complexes. J Biol Chem 274: 5895-5900.
35. Morris SA, Rao B, Garcia BA, Hake SB, Diaz RL, et al. (2007) Identification of histone H3 lysine 36 acetylation as a highly conserved histone modification. J Biol Chem 282: 7632-7640.
36. Kikuchi H, Takami Y, Nakayama T, (2005) GCN5: a supervisor in all-inclusive control of vertebrate cell cycle progression through transcription regulation of various cell cycle-related genes. Gene 347: 83-97.
37. Jin QH, Yu LR, Wang LF, Zhang ZJ, Kasper LH, et al. (2011) Distinct roles of GCN5/PCAF-mediated H3K9ac and CBP/p300-mediated H3K18/27ac in nuclear receptor transactivation. EMBO J 30: 249-262.
38. Cornish-Bowden A, Cardenas ML, (2010) Specificity of non-Michaelis-Menten enzymes: necessary information for analyzing metabolic pathways. J Phys Chem B 114: 16209-16213.
39. Brot FE, Bender ML, (1969) Use of the specificity constant of alpha-chymotrypsin. J Am Chem Soc 91: 7187-7191.
40. Bosshard HR, (1976) Theories of enzyme specificity and their application to proteases and aminoacyl-transfer RNA synthetases. Cell Mol Life Sci 32: 949-963.
41. Hedstrom L (2001) Enzyme Specificity and Selectivity. In: eLS. John Wiley & Sons, Ltd, Chichester.
42. Bender ML, Kezdy FJ, (1965) Mechanism of action of proteolytic enzymes. Annu Rev Biochem 34: 49-76.
43. Radzicka A, Wolfenden R, (1995) A proficient enzyme. Science 267: 90-93.
44. Wolfenden R, (2006) Degrees of difficulty of water-consuming reactions in the absence of enzymes. Chem Rev 106: 3379-3396.
45. Truscott RJW, Mizdrak J, Friedrich MG, Hooi MY, Lyons B, et al. (2012) Is protein methylation in the human lens a result of non-enzymatic methylation by S-adenosylmethionine? Exp Eye Res 99: 48-54.
46. Commerford SL, Carsten AL, Cronkite EP, (1982) Histone turnover within nonproliferating cells. Proc Natl Acad Sci U S A 79: 1163-1165.
47. Wu RS, Panusz HT, Hatch CL, Bonner WM, (1986) Histones and their modifications. CRC Crit Rev Biochem 20: 201-263.
48. Schwer B, Eckersdorff M, Li Y, Silva JC, Fermin D, et al. (2009) Calorie restriction alters mitochondrial protein acetylation. Aging Cell 8: 604-606.
49. Wagner GR, Payne RM (2011) Mitochondrial acetylation and diseases of aging. J Aging Res 2011: Article ID 234875.
50. Deng LW, Wang D, de la Fuente C, Wang L, Li H, et al. (2001) Enhancement of the p300 HAT activity by HIV-1 Tat on chromatin DNA. Virology 289: 312-326.
51. Kuo MH, vom Baur E, Struhl K, Allis CD, (2000) Gcn4 activator targets Gcn5 histone acetyltransferase to specific promoters independently of transcription. Mol Cell 6: 1309-1320.
52. Cai L, Sutter BM, Li B, Tu BP, (2011) Acetyl-CoA induces cell growth and proliferation by promoting the acetylation of histones at growth genes. Mol Cell 42: 426-437.
53. Tanner KG, Trievel RC, Kuo MH, Howard RM, Berger SL, et al. (1999) Catalytic mechanism and function of invariant glutamic acid 173 from the histone acetyltransferase GCN5 transcriptional coactivator. J Biol Chem 274: 18157-18160.
54. Davey CA, Sargent DF, Luger K, Maeder AW, Richmond TJ, (2002) Solvent mediated interactions in the structure of the nucleosome core particle at 1.9 angstrom resolution. J Mol Biol. 319: 1097-1113.