Histone H4 acetylation dynamics determined by stable isotope labeling with amino acids in cell culture and mass spectrometry

Analytical Biochemistry

Volumn 363, Issue 1, 2007, Pages 22-34

  Su, Xiaodan ^a   Zhang, Liwen ^a   Lucas, David M ^a   Davis, Melanie E ^a   Knapp, Amy R ^a   Green Church, Kari B ^a   Marcucci, Guido ^a   Parthun, Mark R ^a   Byrd, John C ^a   Freitas, Michael A ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

Acetylation; Chromatin; Histone; Histone deacetylase inhibitor; Mass spectrometry; Quantitative proteomics

Indexed keywords

ACETYLATION; AMINO ACIDS; CELL CULTURE; CELLS; DESORPTION; ELECTROPHORESIS; INDUCTIVELY COUPLED PLASMA; ISOTOPES; MASS SPECTROMETRY; PROTEOMICS; UREA;

CHROMATIN; EPIGENETIC REGULATION; HISTONE; HISTONE DEACETYLASE INHIBITOR; MATRIX-ASSISTED LASER DESORPTION/IONIZATION-TIME-OF-FLIGHT MASS SPECTROMETRY; POLYACRYLAMIDE GEL ELECTROPHORESIS; QUANTITATIVE PROTEOMICS; STABLE-ISOTOPE LABELING;

PROTEINS;

ACETIC ACID; AMINO ACID; DEPSIPEPTIDE; DEUTERIUM; HISTONE DEACETYLASE; HISTONE DEACETYLASE INHIBITOR; HISTONE H4; TRYPSIN; UREA;

ACETYLATION; AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ARTICLE; CELL CULTURE; CELL LINE; CELL SEPARATION; CONTROLLED STUDY; CULTURE MEDIUM; DYNAMICS; ENZYME ACTIVITY; HUMAN; HUMAN CELL; ISOTOPE LABELING; KINETICS; LYMPHOBLAST; MASS SPECTROMETRY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; QUANTITATIVE ASSAY;

EID: 33847368080     PISSN: 00032697     EISSN: 10960309     Source Type: Journal    
DOI: 10.1016/j.ab.2006.12.031     Document Type: Article

References (46)

1. Lindner H., Sarg B., Meraner C., and Helliger W. Separation of acetylated core histones by hydrophilic-interaction liquid chromatography. J. Chromatogr. A 743 (1996) 137-144
2. Freitas M.A., Sklenar A.R., and Parthun M.R. Application of mass spectrometry to the identification and quantification of histone post-translational modifications. J. Cell Biochem. 92 (2004) 691-700
3. Marks P.A., Richon V.M., and Rifkind R.A. Histone deacetylase inhibitors: inducers of differentiation or apoptosis of transformed cells. J. Natl. Cancer Inst. 92 (2000) 1210-1216
4. Arts J., de Schepper S., and Van Emelen K. Histone deacetylase inhibitors: from chromatin remodeling to experimental cancer therapeutics. Curr. Med. Chem. 10 (2003) 2343-2350
5. Richon V.M., Sandhoff T.W., Rifkind R.A., and Marks P.A. Histone deacetylase inhibitor selectively induces p21waf1 expression and gene-associated histone acetylation. Proc. Natl. Acad. Sci. USA 97 (2000) 10014-10019
6. Zhang L., Freitas M.A., Wickman J., Parthun M.R., Klisovic M.I., Marcucci G., and Byrd J.C. Differential expression of histone post-translational modifications in acute myeloid and chronic lymphocytic leukemia determined by high-pressure liquid chromatography and mass spectrometry. J. Am. Soc. Mass Spectrom. 15 (2004) 77-86
7. Allfrey V.G., Faulkner R., and Mirsky A.E. Acetylation and methylation of histones and their possible role in the regulation of rna synthesis. Proc. Natl. Acad. Sci. USA 51 (1964) 786-794
8. Mei S., Ho A.D., and Mahlknecht U. Role of histone deacetylase inhibitors in the treatment of cancer (review). Int. J. Oncol. 25 (2004) 1509-1519
9. Chiurazzi P., and Neri G. Reactivation of silenced genes and transcriptional therapy. Cytogenet. Genome Res. 100 (2003) 56-64
10. Kwon H.J., Owa T., Hassig C.A., Shimada J., and Schreiber S.L. Depudecin induces morphological reversion of transformed fibroblasts via the inhibition of histone deacetylase. Proc. Natl. Acad. Sci. USA 95 (1998) 3356-3361
11. Yoshida M., Kijima M., Akita M., and Beppu T. Potent and specific inhibition of mammalian histone deacetylase both in vivo and in vitro by trichostatin a. J. Biol. Chem. 265 (1990) 17174-17179
12. Kijima M., Yoshida M., Sugita K., Horinouchi S., and Beppu T. Trapoxin, an antitumor cyclic tetrapeptide, is an irreversible inhibitor of mammalian histone deacetylase. J. Biol. Chem. 268 (1993) 22429-22435
13. Newmark H.L., Lupton J.R., and Young C.W. Butyrate as a differentiating agent: pharmacokinetics, analogues and current status. Cancer Lett. 78 (1994) 1-5
14. Aron J.L., Parthun M.R., Marcucci G., Kitada S., Mone A.P., Davis M.E., Shen T., Murphy T., Wickham J., Kanakry C., Lucas D.M., Reed J.C., Grever M.R., and Byrd J.C. Depsipeptide (fr901228) induces histone acetylation and inhibition of histone deacetylase in chronic lymphocytic leukemia cells concurrent with activation of caspase 8-mediated apoptosis and down-regulation of c-flip protein. Blood 102 (2003) 652-658
15. Byrd J.C., Shinn C., Ravi R., Willis C.R., Waselenko J.K., Flinn I.W., Dawson N.A., and Grever M.R. Depsipeptide (fr901228): a novel therapeutic agent with selective, in vitro activity against human b-cell chronic lymphocytic leukemia cells. Blood 94 (1999) 1401-1408
16. Wang Y.K., Ma Z., Quinn D.F., and Fu E.W. Inverse 18o labeling mass spectrometry for the rapid identification of marker/target proteins. Anal. Chem. 73 (2001) 3742-3750
17. Waterborg J.H. Dynamics of histone acetylation in vivo. A function for acetylation turnover?. Biochem. Cell Biol. 80 (2002) 363-378
18. Smith C.M., Gafken P.R., Zhang Z., Gottschling D.E., Smith J.B., and Smith D.L. Mass spectrometric quantification of acetylation at specific lysines within the amino-terminal tail of histone h4. Anal. Biochem. 316 (2003) 23-33
19. Smith C.M. Quantification of acetylation at proximal lysine residues using isotopic labeling and tandem mass spectrometry. Methods 36 (2005) 395-403
20. Ong S.E., Blagoev B., Kratchmarova I., Kristensen D.B., Steen H., Pandey A., and Mann M. Stable isotope labeling by amino acids in cell culture, silac, as a simple and accurate approach to expression proteomics. Mol. Cell. Proteomics 1 (2002) 376-386
21. Ong S.E., Foster L.J., and Mann M. Mass spectrometric-based approaches in quantitative proteomics. Methods 29 (2003) 124-130
22. Pan S., Gu S., Bradbury E.M., and Chen X. Single peptide-based protein identification in human proteome through MALDI-TOF MS coupled with amino acids coded mass tagging. Anal. Chem. 75 (2003) 1316-1324
23. Gu S., Pan S., Bradbury E.M., and Chen X. Use of deuterium-labeled lysine for efficient protein identification and peptide de novo sequencing. Anal. Chem. 74 (2002) 5774-5785
24. Gu S., Pan S., Bradbury E.M., and Chen X. Precise peptide sequencing and protein quantification in the human proteome through in vivo lysine-specific mass tagging. J. Am. Soc. Mass Spectrom. 14 (2003) 1-7
25. Zhu H., Hunter T.C., Pan S., Yau P.M., Bradbury E.M., and Chen X. Residue-specific mass signatures for the efficient detection of protein modifications by mass spectrometry. Anal. Chem. 74 (2002) 1687-1694
26. Zhu H., Pan S., Gu S., Bradbury E.M., and Chen X. Amino acid residue specific stable isotope labeling for quantitative proteomics. Rapid Commun. Mass Spectrom. 16 (2002) 2115-2123
27. Miyashita T., and Reed J.C. Bcl-2 oncoprotein blocks chemotherapy-induced apoptosis in a human leukemia cell line. Blood 81 (1993) 151-157
28. Vermes I., Haanen C., Steffens-Nakken H., and Reutelingsperger C. A novel assay for apoptosis. Flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labelled annexin v. J. Immunol. Methods 184 (1995) 39-51
29. Panyim S., and Chalkley R. High resolution acrylamide gel electrophoresis of histones. Arch. Biochem. Biophys. 130 (1969) 337-346
30. Pastink A., Berkhout T.A., Mager W.H., and Planta R.J. Analysis of histones from the yeast Saccharomyces carlsbergensis. Biochem. J. 177 (1979) 917-923
31. Waterborg J.H., and Harrington R.E. Western blotting of histones from acid-urea-triton- and sodium dodecyl sulfate-polyacrylamide gels. Anal. Biochem. 162 (1987) 430-434
32. MacCoss M.J., Wu C.C., Liu H., Sadygov R., and Yates III J.R. A correlation algorithm for the automated quantitative analysis of shotgun proteomics data. Anal. Chem. 75 (2003) 6912-6921
33. Ong S.E., Kratchmarova I., and Mann M. Properties of 13c-substituted arginine in stable isotope labeling by amino acids in cell culture (silac). J. Proteome Res. 2 (2003) 173-181
34. Nilsson I., and Heijne G.V. A signal peptide with a proline next to the cleavage site inhibits leader pepdidase when present in a sec-independent protein. Fed. Eur. Biochem. Soc. 299 (1992) 243-246
35. Kieliszewski M.J., Leykam J.F., and Lamport D.T. Trypsin cleaves lysylproline in a hydroxyproline-rich glycoprotein from zea mays. Pept. Res. 2 (1989) 246-248
36. Lucas D.M., Davis M.E., Parthun M.R., Mone A.P., Kitada S., Cunningham K.D., Flax E.L., Wickham J., Reed J.C., Byrd J.C., and Grever M.R. The histone deacetylase inhibitor ms-275 induces caspase-dependent apoptosis in b-cell chronic lymphocytic leukemia cells. Leukemia 18 (2004) 1207-1214
37. Tang C., Willingham M.C., Reed J.C., Miyashita T., Ray S., Ponnathpur V., Huang Y., Mahoney M.E., Bullock G., and Bhalla K. High levels of p26bcl-2 oncoprotein retard taxol-induced apoptosis in human pre-b leukemia cells. Leukemia 8 (1994) 1960-1969
38. Schotta G., Lachner M., Peters A.H., and Jenuwein T. The indexing potential of histone lysine methylation. Novartis Found. Symp. 259 (2004) 22-37 discussion 37-47, 163-9
39. Zhang Y., and Reinberg D. Transcription regulation by histone methylation: Interplay between different covalent modifications of the core histone tails. Genes Dev. 15 (2001) 2343-2360
40. Bannister A.J., Schneider R., and Kouzarides T. Histone methylation: dynamic or static?. Cell 109 (2002) 801-806
41. Zhang L., Eugeni E.E., Parthun M.R., and Freitas M.A. Identification of novel histone post-translational modifications by peptide mass fingerprinting. Chromosoma 112 (2003) 77-86
42. Zhang K., Williams K.E., Huang L., Yau P., Siino J.S., Bradbury E.M., Jones P.R., Minch M.J., and Burlingame A.L. Histone acetylation and deacetylation: identification of acetylation and methylation sites of hela histone h4 by mass spectrometry. Mol. Cell. Proteomics 1 (2002) 500-508
43. Ren C., Zhang L., Freitas M.A., Ghoshal K., Parthun M.R., and Jacob S.T. Peptide mass mapping of acetylated isoforms of histone h4 from mouse lymphosarcoma cells treated with histone deacetylase (hdacs) inhibitors. J. Am. Soc. Mass Spectrom. 16 (2005) 1641-1653
44. Ip Y.T., Jackson V., Meier J., and Chalkley R. The separation of transcriptionally engaged genes. J. Biol. Chem. 263 (1988) 14044-14052
45. Zhang D.E., and Nelson D.A. Histone acetylation in chicken erythrocytes. Rates of acetylation and evidence that histones in both active and potentially active chromatin are rapidly modified. Biochem. J. 250 (1988) 233-240
46. Cousens L.S., and Alberts B.M. Accessibility of newly synthesized chromatin to histone acetylase. J. Biol. Chem. 257 (1982) 3945-3949