Identification of protein complexes that bind to histone H3 combinatorial modifications using super-SILAC and weighted correlation network analysis

Nucleic Acids Research

Volumn 43, Issue 3, 2015, Pages 1418-1432

  Kunowska, Natalia ^a   Rotival, Maxime ^a   Yu, Lu ^b   Choudhary, Jyoti ^b   Dillon, Niall ^a  

^a HAMMERSMITH HOSPITAL   (United Kingdom)

^b WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H3; HISTONE; PROTEIN;

ACCURACY; ANIMAL CELL; ARTICLE; BINDING SITE; COMPLEX FORMATION; CONTROLLED STUDY; HIGH THROUGHPUT SCREENING; HISTONE MODIFICATION; INTERMETHOD COMPARISON; INVESTIGATIVE PROCEDURES; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; SILAC METHOD; VALIDATION PROCESS; WEIGHTED CORRELATION NETWORK ANALYSIS; ANIMAL; COMBINATORIAL CHEMISTRY; MASS SPECTROMETRY; METABOLISM; TUMOR CELL LINE; VALIDATION STUDY;

EUKARYOTA;

ANIMALS; CELL LINE, TUMOR; COMBINATORIAL CHEMISTRY TECHNIQUES; HISTONES; MASS SPECTROMETRY; MICE; PROTEINS;

EID: 84936757664     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku1350     Document Type: Article

References (66)

1. Rando,O.J. (2012) Combinatorial complexity in chromatin structure and function: revisiting the histone code. Curr. Opin. Genet. Dev., 22, 148-155.
2. Gehani,S.S., Agrawal-Singh,S., Dietrich,N., Christophersen,N.S., Helin,K. and Hansen,K. (2010) Polycomb group protein displacement and gene activation through MSK-dependent H3K27me3S28 phosphorylation. Mol. Cell, 39, 886-900.
3. Sabbattini,P., Sjoberg,M., Nikic,S., Frangini,A., Holmqvist,P.H., Kunowska,N., Carroll,T., Brookes,E., Arthur,S.J., Pombo,A. et al. (2014) An H3K9/S10 methyl-phospho switch modulates Polycomb and Pol II binding at repressed genes during differentiation. Mol. Biol. Cell, 25, 904-915.
4. Geiger,T., Cox,J., Ostasiewicz,P., Wisniewski,J.R. and Mann,M. (2010) Super-SILAC mix for quantitative proteomics of human tumor tissue. Nat. Methods, 7, 383-385.
5. Langfelder,P. and Horvath,S. (2008) WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics, 9, 559.
6. Zhang,B. and Horvath,S. (2005) A general framework for weighted gene co-expression network analysis. Stat. Appl. Genet. Mol. Biol., 4, Article17.
7. Durocher,Y., Perret,S. and Kamen,A. (2002) High-level and high-throughput recombinant protein production by transient transfection of suspension-growing human 293-EBNA1 cells. Nucleic Acids Res., 30, e9.
8. Wysocka,J. (2006) Identifying novel proteins recognizing histone modifications using peptide pull-down assay. Methods, 40, 339-343.
9. 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.
10. Shirasaki,D.I., Greiner,E.R., Al-Ramahi,I., Gray,M., Boontheung,P., Geschwind,D.H., Botas,J., Coppola,G., Horvath,S., Loo,J.A. et al. (2012) Network organization of the huntingtin proteomic interactome in mammalian brain. Neuron, 75, 41-57.
11. Nozawa,R.S., Nagao,K., Masuda,H.T., Iwasaki,O., Hirota,T., Nozaki,N., Kimura,H. and Obuse,C. (2010) Human POGZ modulates dissociation of HP1alpha from mitotic chromosome arms through Aurora B activation. Nat. Cell. Biol., 12, 719-727.
12. Nikolov,M., Stutzer,A., Mosch,K., Krasauskas,A., Soeroes,S., Stark,H., Urlaub,H. and Fischle,W. (2011) Chromatin affinity purification and quantitative mass spectrometry defining the interactome of histone modification patterns. Mol. Cell. Proteomics, 10, M110 005371.
13. Macdonald,N., Welburn,J.P., Noble,M.E., Nguyen,A., Yaffe,M.B., Clynes,D., Moggs,J.G., Orphanides,G., Thomson,S., Edmunds,J.W. et al. (2005) Molecular basis for the recognition of phosphorylated and phosphoacetylated histone H3 by 14-3-3. Mol. Cell, 20, 199-211.
14. Winter,S., Fischle,W. and Seiser,C. (2008) Modulation of 14-3-3 interaction with phosphorylated histone H3 by combinatorial modification patterns. Cell Cycle, 7, 1336-1342.
15. Eustermann,S., Yang,J.C., Law,M.J., Amos,R., Chapman,L.M., Jelinska,C., Garrick,D., Clynes,D., Gibbons,R.J., Rhodes,D. et al. (2011) Combinatorial readout of histone H3 modifications specifies localization of ATRX to heterochromatin. Nat. Struct. Mol. Biol., 18, 777-782.
16. Allen,J.D., Xie,Y., Chen,M., Girard,L. and Xiao,G. (2012) Comparing statistical methods for constructing large scale gene networks. PLoS One, 7, e29348.
17. Boyer,L.A., Latek,R.R. and Peterson,C.L. (2004) The SANT domain: a unique histone-tail-binding module? Nat. Rev. Mol. Cell. Biol., 5, 158-163.
18. Boyer,L.A., Langer,M.R., Crowley,K.A., Tan,S., Denu,J.M. and Peterson,C.L. (2002) Essential role for the SANT domain in the functioning of multiple chromatin remodeling enzymes. Mol. Cell, 10, 935-942.
19. Schaniel,C., Ang,Y.S., Ratnakumar,K., Cormier,C., James,T., Bernstein,E., Lemischka,I.R. and Paddison,P.J. (2009) Smarcc1/Baf155 couples self-renewal gene repression with changes in chromatin structure in mouse embryonic stem cells. Stem Cells, 27, 2979-2991.
20. Nielsen,A.L., Sanchez,C., Ichinose,H., Cervino,M., Lerouge,T., Chambon,P. and Losson,R. (2002) Selective interaction between the chromatin-remodeling factor BRG1 and the heterochromatin-associated protein HP1alpha. EMBO J., 21, 5797-5806.
21. Iwase,S., Xiang,B., Ghosh,S., Ren,T., Lewis,P.W., Cochrane,J.C., Allis,C.D., Picketts,D.J., Patel,D.J., Li,H. et al. (2011) ATRX ADD domain links an atypical histone methylation recognition mechanism to human mental-retardation syndrome. Nat. Struct. Mol. Biol., 18, 769-776.
22. Bandyopadhyay,S., Chiang,C.Y., Srivastava,J., Gersten,M., White,S., Bell,R., Kurschner,C., Martin,C.H., Smoot,M., Sahasrabudhe,S. et al. (2010) A human MAP kinase interactome. Nat. Methods, 7, 801-805.
23. Rowbotham,S.P., Barki,L., Neves-Costa,A., Santos,F., Dean,W., Hawkes,N., Choudhary,P., Will,W.R., Webster,J., Oxley,D. et al. (2011) Maintenance of silent chromatin through replication requires SWI/SNF-like chromatin remodeler SMARCAD1. Mol. Cell, 42, 285-296.
24. Nozawa,R.S., Nagao,K., Igami,K.T., Shibata,S., Shirai,N., Nozaki,N., Sado,T., Kimura,H. and Obuse,C. (2013) Human inactive X chromosome is compacted through a PRC2-independent SMCHD1-HBiX1 pathway. Nat. Struct. Mol. Biol., 20, 566-573.
25. Rosnoblet,C., Vandamme,J., Volkel,P. and Angrand,P.O. (2011) Analysis of the human HP1 interactome reveals novel binding partners. Biochem. Biophys. Res. Commun., 413, 206-211.
26. Vassallo,M.F. and Tanese,N. (2002) Isoform-specific interaction of HP1 with human TAFII130. Proc. Natl. Acad. Sci. U.S.A., 99, 5919-5924.
27. Prasanth,S.G., Shen,Z., Prasanth,K.V. and Stillman,B. (2010) Human origin recognition complex is essential for HP1 binding to chromatin and heterochromatin organization. Proc. Natl. Acad. Sci. U.S.A., 107, 15093-15098.
28. Das,C., Gadad,S.S. and Kundu,T.K. (2010) Human positive coactivator 4 controls heterochromatinization and silencing of neural gene expression by interacting with REST/NRSF and CoREST. J. Mol. Biol., 397, 1-12.
29. Bawa-Khalfe,T., Lu,L.S., Zuo,Y., Huang,C., Dere,R., Lin,F.M. and Yeh,E.T. (2012) Differential expression of SUMO-specific protease 7 variants regulates epithelial-mesenchymal transition. Proc. Natl. Acad. Sci. U.S.A., 109, 17466-17471.
30. Lin,C.H., Li,B., Swanson,S., Zhang,Y., Florens,L., Washburn,M.P., Abmayr,S.M. and Workman,J.L. (2008) Heterochromatin protein 1a stimulates histone H3 lysine 36 demethylation by the Drosophila KDM4A demethylase. Mol. Cell, 32, 696-706.
31. Cao,Q., Wang,X., Zhao,M., Yang,R., Malik,R., Qiao,Y., Poliakov,A., Yocum,A.K., Li,Y., Chen,W. et al. (2014) The central role of EED in the orchestration of polycomb group complexes. Nat. Commun., 5, 3127.
32. Frescas,D., Guardavaccaro,D., Kuchay,S.M., Kato,H., Poleshko,A., Basrur,V., Elenitoba-Johnson,K.S., Katz,R.A. and Pagano,M. (2008) KDM2A represses transcription of centromeric satellite repeats and maintains the heterochromatic state. Cell Cycle, 7, 3539-3547.
33. Illingworth,R.S., Botting,C.H., Grimes,G.R., Bickmore,W.A. and Eskeland,R. (2012) PRC1 and PRC2 are not required for targeting of H2A.Z to developmental genes in embryonic stem cells. PLoS One, 7, e34848.
34. Franz,H., Mosch,K., Soeroes,S., Urlaub,H. and Fischle,W. (2009) Multimerization and H3K9me3 binding are required for CDYL1b heterochromatin association. J. Biol. Chem., 284, 35049-35059.
35. Zhang,J., Gao,Q., Li,P., Liu,X., Jia,Y., Wu,W., Li,J., Dong,S., Koseki,H. and Wong,J. (2011) S phase-dependent interaction with DNMT1 dictates the role of UHRF1 but not UHRF2 in DNA methylation maintenance. Cell Res., 21, 1723-1739.
36. Kokura,K., Sun,L., Bedford,M.T. and Fang,J. (2010) Methyl-H3K9-binding protein MPP8 mediates E-cadherin gene silencing and promotes tumour cell motility and invasion. EMBO J., 29, 3673-3687.
37. Eberl,H.C., Spruijt,C.G., Kelstrup,C.D., Vermeulen,M. and Mann,M. (2013) A map of general and specialized chromatin readers in mouse tissues generated by label-free interaction proteomics. Mol. Cell, 49, 368-378.
38. He,C., Li,F., Zhang,J., Wu,J. and Shi,Y. (2013) The methyltransferase NSD3 has chromatin-binding motifs, PHD5-C5HCH, that are distinct from other NSD (nuclear receptor SET domain) family members in their histone H3 recognition. J. Biol. Chem., 288, 4692-4703.
39. Trojer,P., Cao,A.R., Gao,Z., Li,Y., Zhang,J., Xu,X., Li,G., Losson,R., Erdjument-Bromage,H., Tempst,P. et al. (2011) L3MBTL2 protein acts in concert with PcG protein-mediated monoubiquitination of H2A to establish a repressive chromatin structure. Mol. Cell, 42, 438-450.
40. Wu,M., Wang,L., Li,Q., Li,J., Qin,J. and Wong,J. (2013) The MTA family proteins as novel histone H3 binding proteins. Cell Biosci., 3, 1.
41. Schmitges,F.W., Prusty,A.B., Faty,M., Stutzer,A., Lingaraju,G.M., Aiwazian,J., Sack,R., Hess,D., Li,L., Zhou,S. et al. (2011) Histone methylation by PRC2 is inhibited by active chromatin marks. Mol. Cell, 42, 330-341.
42. Audebert,M., Salles,B. and Calsou,P. (2004) Involvement of poly(ADP-ribose) polymerase-1 and XRCC1/DNA ligase III in an alternative route for DNA double-strand breaks rejoining. J. Biol. Chem., 279, 55117-55126.
43. Wang,H., Rosidi,B., Perrault,R., Wang,M., Zhang,L., Windhofer,F. and Iliakis,G. (2005) DNA ligase III as a candidate component of backup pathways of nonhomologous end joining. Cancer Res., 65, 4020-4030.
44. Rosidi,B., Wang,M., Wu,W., Sharma,A., Wang,H. and Iliakis,G. (2008) Histone H1 functions as a stimulatory factor in backup pathways of NHEJ. Nucleic Acids Res., 36, 1610-1623.
45. Pinnola,A., Naumova,N., Shah,M. and Tulin,A.V. (2007) Nucleosomal core histones mediate dynamic regulation of poly(ADP-ribose) polymerase 1 protein binding to chromatin and induction of its enzymatic activity. J. Biol. Chem., 282, 32511-32519.
46. Dantzer,F. and Santoro,R. (2013) The expanding role of PARPs in the establishment and maintenance of heterochromatin. FEBS J., 280, 3508-3518.
47. Lodhi,N., Kossenkov,A.V. and Tulin,A.V. (2014) Bookmarking promoters in mitotic chromatin: poly(ADP-ribose)polymerase-1 as an epigenetic mark. Nucleic Acids Res., 7028-7038.
48. Margueron,R., Justin,N., Ohno,K., Sharpe,M.L., Son,J., Drury,W.J. III, Voigt,P., Martin,S.R., Taylor,W.R., De Marco,V. et al. (2009) Role of the polycomb protein EED in the propagation of repressive histone marks. Nature, 461, 762-767.
49. Xu,C., Bian,C., Yang,W., Galka,M., Ouyang,H., Chen,C., Qiu,W., Liu,H., Jones,A.E., MacKenzie,F. et al. (2010) Binding of different histone marks differentially regulates the activity and specificity of polycomb repressive complex 2 (PRC2). Proc. Natl. Acad. Sci. U.S.A., 107, 19266-19271.
50. Mozzetta,C., Pontis,J., Fritsch,L., Robin,P., Portoso,M., Proux,C., Margueron,R. and Ait-Si-Ali,S. (2014) The histone H3 lysine 9 methyltransferases G9a and GLP regulate polycomb repressive complex 2-mediated gene silencing. Mol. Cell, 53, 277-289.
51. Babbio,F., Pistore,C., Curti,L., Castiglioni,I., Kunderfranco,P., Brino,L., Oudet,P., Seiler,R., Thalman,G.N., Roggero,E. et al. (2012) The SRA protein UHRF1 promotes epigenetic crosstalks and is involved in prostate cancer progression. Oncogene, 31, 4878-4887.
52. Cerutti,H. and Casas-Mollano,J.A. (2009) Histone H3 phosphorylation: universal code or lineage specific dialects? Epigenetics, 4, 71-75.
53. DiLeo,M.V., Strahan,G.D., den Bakker,M. and Hoekenga,O.A. (2011) Weighted correlation network analysis (WGCNA) applied to the tomato fruit metabolome. PLoS One, 6, e26683.
54. Presson,A.P., Yoon,N.K., Bagryanova,L., Mah,V., Alavi,M., Maresh,E.L., Rajasekaran,A.K., Goodglick,L., Chia,D. and Horvath,S. (2011) Protein expression based multimarker analysis of breast cancer samples. BMC Cancer, 11, 230.
55. Yaffe,M.B., Rittinger,K., Volinia,S., Caron,P.R., Aitken,A., Leffers,H., Gamblin,S.J., Smerdon,S.J. and Cantley,L.C. (1997) The structural basis for 14-3-3:phosphopeptide binding specificity. Cell, 91, 961-971.
56. Fu,H., Subramanian,R.R. and Masters,S.C. (2000) 14-3-3 proteins: structure, function, and regulation. Annu. Rev. Pharmacol. Toxicol., 40, 617-647.
57. McDowell,T.L., Gibbons,R.J., Sutherland,H., O'Rourke,D.M., Bickmore,W.A., Pombo,A., Turley,H., Gatter,K., Picketts,D.J., Buckle,V.J. et al. (1999) Localization of a putative transcriptional regulator (ATRX) at pericentromeric heterochromatin and the short arms of acrocentric chromosomes. Proc Natl Acad Sci U.S.A., 96, 13983-13988.
58. Fischle,W., Tseng,B.S., Dormann,H.L., Ueberheide,B.M., Garcia,B.A., Shabanowitz,J., Hunt,D.F., Funabiki,H. and Allis,C.D. (2005) Regulation of HP1-chromatin binding by histone H3 methylation and phosphorylation. Nature, 438, 1116-1122.
59. Chan,D.W., Wang,Y., Wu,M., Wong,J., Qin,J. and Zhao,Y. (2009) Unbiased proteomic screen for binding proteins to modified lysines on histone H3. Proteomics, 9, 2343-2354.
60. Xi,Q., Wang,Z., Zaromytidou,A.I., Zhang,X.H., Chow-Tsang,L.F., Liu,J.X., Kim,H., Barlas,A., Manova-Todorova,K., Kaartinen,V. et al. (2011) A poised chromatin platform for TGF-beta access to master regulators. Cell, 147, 1511-1524.
61. Baumann,C., Viveiros,M.M. and De La Fuente,R. (2010) Loss of maternal ATRX results in centromere instability and aneuploidy in the mammalian oocyte and pre-implantation embryo. PLoS Genet., 6, e1001137.
62. Morozov,V.M., Gavrilova,E.V., Ogryzko,V.V. and Ishov,A.M. (2012) Dualistic function of Daxx at centromeric and pericentromeric heterochromatin in normal and stress conditions. Nucleus, 3, 276-285.
63. Drane,P., Ouararhni,K., Depaux,A., Shuaib,M. and Hamiche,A. (2010) The death-associated protein DAXX is a novel histone chaperone involved in the replication-independent deposition of H3.3. Genes Dev., 24, 1253-1265.
64. Lewis,P.W., Elsaesser,S.J., Noh,K.M., Stadler,S.C. and Allis,C.D. (2010) Daxx is an H3.3-specific histone chaperone and cooperates with ATRX in replication-independent chromatin assembly at telomeres. Proc. Natl. Acad. Sci. U.S.A., 107, 14075-14080.
65. Okada,M., Okawa,K., Isobe,T. and Fukagawa,T. (2009) CENP-H-containing complex facilitates centromere deposition of CENP-A in cooperation with FACT and CHD1. Mol. Biol. Cell, 20, 3986-3995.
66. Vizcaino,J.A., Deutsch,E.W., Wang,R., Csordas,A., Reisinger,F., Rios,D., Dianes,J.A., Sun,Z., Farrah,T., Bandeira,N. et al. (2014) ProteomeXchange provides globally coordinated proteomics data submission and dissemination. Nat. Biotechnol., 32, 223-226.