Quantitative Interaction Proteomics and Genome-wide Profiling of Epigenetic Histone Marks and Their Readers

Cell

Volumn 142, Issue 6, 2010, Pages 967-980

  Vermeulen, Michiel ^a   Eberl, H Christian ^a   Matarese, Filomena ^b   Marks, Hendrik ^b   Denissov, Sergei ^b   Butter, Falk ^a   Lee, Kenneth K ^c   Olsen, Jesper V ^a,e   Hyman, Anthony A ^d   Stunnenberg, Henk G ^b   Mann, Matthias ^a  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^c STOWERS INSTITUTE FOR MEDICAL RESEARCH   (United States)

^d MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

^e University of Copenhagen   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE; HISTONE H3; LYSINE; CHROMATIN; HISTONE ACETYLTRANSFERASE;

ARTICLE; BINDING SITE; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENOME; HUMAN; MASS SPECTROMETRY; METHYLATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION; PROTEOMICS; GENE EXPRESSION REGULATION; GENETIC ASSOCIATION; GENETIC EPIGENESIS; HELA CELL LINE; HISTONE CODE; METABOLISM; PROCEDURES;

CHROMATIN; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION; GENOME-WIDE ASSOCIATION STUDY; HELA CELLS; HISTONE ACETYLTRANSFERASES; HISTONE CODE; HUMANS; LYSINE; MASS SPECTROMETRY; METHYLATION; PROTEOMICS;

EID: 77956643239     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2010.08.020     Document Type: Article

References (56)

1. Butter F., Kappei D., Buchholz F., Vermeulen M., Mann M. A domesticated transposon mediates the effects of a single-nucleotide polymorphism responsible for enhanced muscle growth. EMBO Rep. 2010, 11:305-311.
2. Cloos P.A., Christensen J., Agger K., Helin K. Erasing the methyl mark: histone demethylases at the center of cellular differentiation and disease. Genes Dev. 2008, 22:1115-1140.
3. 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.
4. Denissov S., van Driel M., Voit R., Hekkelman M., Hulsen T., Hernandez N., Grummt I., Wehrens R., Stunnenberg H. Identification of novel functional TBP-binding sites and general factor repertoires. EMBO J. 2007, 26:944-954.
5. Fejes A.P., Robertson G., Bilenky M., Varhol R., Bainbridge M., Jones S.J. FindPeaks 3.1: a tool for identifying areas of enrichment from massively parallel short-read sequencing technology. Bioinformatics 2008, 24:1729-1730.
6. Fischle W., Wang Y., Allis C.D. Binary switches and modification cassettes in histone biology and beyond. Nature 2003, 425:475-479.
7. Fischle W., Wang Y., Jacobs S.A., Kim Y., Allis C.D., Khorasanizadeh S. Molecular basis for the discrimination of repressive methyl-lysine marks in histone H3 by Polycomb and HP1 chromodomains. Genes Dev. 2003, 17:1870-1881.
8. Fischle W., Tseng B.S., Dormann H.L., Ueberheide B.M., Garcia B.A., Shabanowitz J., Hunt D.F., Funabiki H., Allis C.D. Regulation of HP1-chromatin binding by histone H3 methylation and phosphorylation. Nature 2005, 438:1116-1122.
9. Fischle W., Franz H., Jacobs S.A., Allis C.D., Khorasanizadeh S. Specificity of the chromodomain Y chromosome family of chromodomains for lysine-methylated ARK(S/T) motifs. J. Biol. Chem. 2008, 283:19626-19635.
10. Franz H., Mosch K., Soeroes S., Urlaub H., Fischle W. Multimerization and H3K9me3 binding are required for CDYL1b heterochromatin association. J. Biol. Chem. 2009, 284:35049-35059.
11. Garcia B.A., Shabanowitz J., Hunt D.F. Characterization of histones and their post-translational modifications by mass spectrometry. Curr. Opin. Chem. Biol. 2007, 11:66-73.
12. Horton J.R., Upadhyay A.K., Qi H.H., Zhang X., Shi Y., Cheng X. Enzymatic and structural insights for substrate specificity of a family of jumonji histone lysine demethylases. Nat. Struct. Mol. Biol. 2010, 17:38-43.
13. Huang Y., Fang J., Bedford M.T., Zhang Y., Xu R.M. Recognition of histone H3 lysine-4 methylation by the double tudor domain of JMJD2A. Science 2006, 312:748-751.
14. Hubner N.C., Bird A.W., Cox J., Splettstoesser B., Bandilla P., Poser I., Hyman A., Mann M. Quantitative proteomics combined with BAC TransgeneOmics reveals in vivo protein interactions. J. Cell Biol. 2010, 189:739-754.
15. Hughes-Davies L., Huntsman D., Ruas M., Fuks F., Bye J., Chin S.F., Milner J., Brown L.A., Hsu F., Gilks B., et al. EMSY links the BRCA2 pathway to sporadic breast and ovarian cancer. Cell 2003, 115:523-535.
16. Huisinga K.L., Pugh B.F. A genome-wide housekeeping role for TFIID and a highly regulated stress-related role for SAGA in Saccharomyces cerevisiae. Mol. Cell 2004, 13:573-585.
17. Hurd P.J., Bannister A.J., Halls K., Dawson M.A., Vermeulen M., Olsen J.V., Ismail H., Somers J., Mann M., Owen-Hughes T., et al. Phosphorylation of histone H3 Thr-45 is linked to apoptosis. J. Biol. Chem. 2009, 284:16575-16583.
18. Ikura T., Ogryzko V.V., Grigoriev M., Groisman R., Wang J., Horikoshi M., Scully R., Qin J., Nakatani Y. Involvement of the TIP60 histone acetylase complex in DNA repair and apoptosis. Cell 2000, 102:463-473.
19. Jenuwein T., Allis C.D. Translating the histone code. Science 2001, 293:1074-1080.
20. Kouzarides T. Chromatin modifications and their function. Cell 2007, 128:693-705.
21. Lechner M.S., Schultz D.C., Negorev D., Maul G.G., Rauscher F.J. The mammalian heterochromatin protein 1 binds diverse nuclear proteins through a common motif that targets the chromoshadow domain. Biochem. Biophys. Res. Commun. 2005, 331:929-937.
22. Lee K.K., Workman J.L. Histone acetyltransferase complexes: one size doesn't fit all. Nat. Rev. Mol. Cell Biol. 2007, 8:284-295.
23. Lee N., Erdjument-Bromage H., Tempst P., Jones R.S., Zhang Y. The H3K4 Demethylase Lid Associates with and Inhibits Histone Deacetylase Rpd3. Mol. Cell. Biol. 2009, 29:1401-1410.
24. Li H., Ruan J., Durbin R. Mapping short DNA sequencing reads and calling variants using mapping quality scores. Genome Res. 2008, 18:1851-1858.
25. Mandel S., Rechavi G., Gozes I. Activity-dependent neuroprotective protein (ADNP) differentially interacts with chromatin to regulate genes essential for embryogenesis. Dev. Biol. 2007, 303:814-824.
26. Margueron R., Justin N., Ohno K., Sharpe M.L., Son J., Drury W.J., Voigt P., Martin S.R., Taylor W.R., De Marco V., et al. Role of the polycomb protein EED in the propagation of repressive histone marks. Nature 2009, 461:762-767.
27. Martens J.H., O'Sullivan R.J., Braunschweig U., Opravil S., Radolf M., Steinlein P., Jenuwein T. The profile of repeat-associated histone lysine methylation states in the mouse epigenome. EMBO J. 2005, 24:800-812.
28. Mateescu B., England P., Halgand F., Yaniv M., Muchardt C. Tethering of HP1 proteins to chromatin is relieved by phosphoacetylation of histone H3. EMBO Rep. 2004, 5:490-496.
29. Maurer-Stroh S., Dickens N.J., Hughes-Davies L., Kouzarides T., Eisenhaber F., Ponting C.P. The Tudor domain " Royal Family": Tudor, plant Agenet, Chromo, PWWP and MBT domains. Trends Biochem. Sci. 2003, 28:69-74.
30. Moshkin Y.M., Kan T.W., Goodfellow H., Bezstarosti K., Maeda R.K., Pilyugin M., Karch F., Bray S.J., Demmers J.A., Verrijzer C.P. Histone chaperones ASF1 and NAP1 differentially modulate removal of active histone marks by LID-RPD3 complexes during NOTCH silencing. Mol. Cell 2009, 35:782-793.
31. Nagy Z., Tora L. Distinct GCN5/PCAF-containing complexes function as co-activators and are involved in transcription factor and global histone acetylation. Oncogene 2007, 26:5341-5357.
32. Nagy Z., Riss A., Fujiyama S., Krebs A., Orpinell M., Jansen P., Cohen A., Stunnenberg H.G., Kato S., Tora L. The metazoan ATAC and SAGA coactivator HAT complexes regulate different sets of inducible target genes. Cell. Mol. Life Sci. 2010, 67:611-628.
33. Olsen J.V., Ong S.E., Mann M. Trypsin cleaves exclusively C-terminal to arginine and lysine residues. Mol. Cell. Proteomics 2004, 3:608-614.
34. Olsen J.V., Vermeulen M., Santamaria A., Kumar C., Miller M.L., Jensen L.J., Gnad F., Cox J., Jensen T.S., Nigg E.A., et al. Quantitative phosphoproteomics reveals widespread full phosphorylation site occupancy during mitosis. Sci. Signal. 2010, 3:ra3.
35. 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.
36. Poser I., Sarov M., Hutchins J.R., Heriche J.K., Toyoda Y., Pozniakovsky A., Weigl D., Nitzsche A., Hegemann B., Bird A.W., et al. BAC TransgeneOmics: a high-throughput method for exploration of protein function in mammals. Nat. Methods 2008, 5:409-415.
37. Prasanth S.G., Prasanth K.V., Siddiqui K., Spector D.L., Stillman B. Human Orc2 localizes to centrosomes, centromeres and heterochromatin during chromosome inheritance. EMBO J. 2004, 23:2651-2663.
38. Pray-Grant M.G., Daniel J.A., Schieltz D., Yates J.R., Grant P.A. Chd1 chromodomain links histone H3 methylation with SAGA- and SLIK-dependent acetylation. Nature 2005, 433:434-438.
39. Ringrose L., Ehret H., Paro R. Distinct contributions of histone H3 lysine 9 and 27 methylation to locus-specific stability of polycomb complexes. Mol. Cell 2004, 16:641-653.
40. Shilatifard A. Chromatin modifications by methylation and ubiquitination: implications in the regulation of gene expression. Annu. Rev. Biochem. 2006, 75:243-269.
41. Sims R.J., Chen C.F., Santos-Rosa H., Kouzarides T., Patel S.S., Reinberg D. Human but not yeast CHD1 binds directly and selectively to histone H3 methylated at lysine 4 via its tandem chromodomains. J. Biol. Chem. 2005, 280:41789-41792.
42. Squatrito M., Gorrini C., Amati B. Tip60 in DNA damage response and growth control: many tricks in one HAT. Trends Cell Biol. 2006, 16:433-442.
43. Taverna S.D., Li H., Ruthenburg A.J., Allis C.D., Patel D.J. How chromatin-binding modules interpret histone modifications: lessons from professional pocket pickers. Nat. Struct. Mol. Biol. 2007, 14:1025-1040.
44. Tyteca S., Vandromme M., Legube G., Chevillard-Briet M., Trouche D. Tip60 and p400 are both required for UV-induced apoptosis but play antagonistic roles in cell cycle progression. EMBO J. 2006, 25:1680-1689.
45. van Oevelen C., Wang J., Asp P., Yan Q., Kaelin W.G., Kluger Y., Dynlacht B.D. A role for mammalian Sin3 in permanent gene silencing. Mol. Cell 2008, 32:359-370.
46. Vermeulen M., Selbach M. Quantitative proteomics: a tool to assess cell differentiation. Curr. Opin. Cell Biol. 2009, 21:761-766.
47. Vermeulen M., Mulder K.W., Denissov S., Pijnappel W.W., van Schaik F.M., Varier R.A., Baltissen M.P., Stunnenberg H.G., Mann M., Timmers H.T. Selective anchoring of TFIID to nucleosomes by trimethylation of histone H3 lysine 4. Cell 2007, 131:58-69.
48. Vermeulen M., Hubner N.C., Mann M. High confidence determination of specific protein-protein interactions using quantitative mass spectrometry. Curr. Opin. Biotechnol. 2008, 19:331-337.
49. Vezzoli A., Bonadies N., Allen M.D., Freund S.M., Santiveri C.M., Kvinlaug B.T., Huntly B.J., Gottgens B., Bycroft M. Molecular basis of histone H3K36me3 recognition by the PWWP domain of Brpf1. Nat. Struct. Mol. Biol. 2010, 17:617-619.
50. Wang G.G., Song J., Wang Z., Dormann H.L., Casadio F., Li H., Luo J.L., Patel D.J., Allis C.D. Haematopoietic malignancies caused by dysregulation of a chromatin-binding PHD finger. Nature 2009, 459:847-851.
51. Wang Y., Reddy B., Thompson J., Wang H., Noma K., Yates J.R., Jia S. Regulation of Set9-mediated H4K20 methylation by a PWWP domain protein. Mol. Cell 2009, 33:428-437.
52. Wang Z., Zang C., Cui K., Schones D.E., Barski A., Peng W., Zhao K. Genome-wide mapping of HATs and HDACs reveals distinct functions in active and inactive genes. Cell 2009, 138:1019-1031.
53. Winter S., Fischle W., Seiser C. Modulation of 14-3-3 interaction with phosphorylated histone H3 by combinatorial modification patterns. Cell Cycle 2008, 7:1336-1342.
54. Wisniewski J.R., Zougman A., Nagaraj N., Mann M. Universal sample preparation method for proteome analysis. Nat. Methods 2009, 6:359-362.
55. Wysocka J., Swigut T., Xiao H., Milne T.A., Kwon S.Y., Landry J., Kauer M., Tackett A.J., Chait B.T., Badenhorst P., et al. A PHD finger of NURF couples histone H3 lysine 4 trimethylation with chromatin remodelling. Nature 2006, 442:86-90.
56. Zhang Y., Buchholz F., Muyrers J.P., Stewart A.F. A new logic for DNA engineering using recombination in Escherichia coli. Nat. Genet. 1998, 20:123-128.