Combining genomic and proteomic approaches for epigenetics research

Papers of special note have been highlighted as: ▪ of interest ▪▪ of considerable interest

References

• 1  Esteller M. Epigenetics in cancer. N. Engl. J. Med.358,1148–1159 (2008).
  Medline CASGoogle Scholar
• 2  Berger SL, Kouzarides T, Shiekhattar R, Shilatifard A. An operational definition of epigenetics. Gene Dev.23,781–783 (2009).
  Medline CASGoogle Scholar
• 3  Suzuki MM, Bird A. DNA methylation landscapes: provocative insights from epigenomics. Nat. Rev. Genet.9,465–476 (2008).
  Medline CASGoogle Scholar
• 4  Goldberg AD, Allis CD, Bernstein E. Epigenetics: a landscape takes shape. Cell128,635 (2007).
  Medline CASGoogle Scholar
• 5  Nakao M. Epigenetics: interaction of DNA methylation and chromatin. Gene278,25–31 (2001).
  Medline CASGoogle Scholar
• 6  Sajan SA, Hawkins RD. Methods for identification of higher-order chromatin structure. Annu. Rev. Genomics Hum. Genet.13,59–82 (2012).
  Medline CASGoogle Scholar
• 7  Kornberg RD. Chromatin structure: a repeating unit of histones and DNA. Science184,868 (1974).
  Medline CASGoogle Scholar
• 8  Grunstein M. Histone acetylation in chromatin structure and transcription. Nature389,349–352 (1997).
  Medline CASGoogle Scholar
• 9  Weinhold B. Epigenetics: the science of change. Environ. Health Persp.114,A160 (2006).
  MedlineGoogle Scholar
• 10  Jones PA. Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat. Rev. Genet.13,484–492 (2012).▪ Describes how the function of DNA methylation is intrinsically linked to the mechanisms for establishing, maintaining and removing the methyl group.
  Medline CASGoogle Scholar
• 11  Bird AP, Wolffe AP. Methylation-induced repression – belts, braces, and chromatin. Cell99,451–454 (1999).
  Medline CASGoogle Scholar
• 12  Dodge JE, Okano M, Dick F et al. Inactivation of Dnmt3b in mouse embryonic fibroblasts results in DNA hypomethylation, chromosomal instability, and spontaneous immortalization. J. Biol. Chem.280,17986–17991 (2005).
  Medline CASGoogle Scholar
• 13  Hammoud SS, Cairns BR, Carrell DT. Analysis of gene-specific and genome-wide sperm DNA methylation. Methods Mol. Biol.927,451–458 (2013).
  Medline CASGoogle Scholar
• 14  Surani MA. Imprinting and the initiation of gene silencing in the germ line. Cell93,309–312 (1998).
  Medline CASGoogle Scholar
• 15  Ng HH, Adrian B. DNA methylation and chromatin modification. Curr. Opin. Genet. Dev.9,158–163 (1999).
  Medline CASGoogle Scholar
• 16  Weber M, Davies JJ, Wittig D et al. Chromosome-wide and promoter-specific analyses identify sites of differential DNA methylation in normal and transformed human cells. Nat. Genet.37,853–862 (2005).
  Medline CASGoogle Scholar
• 17  Chen Z, Wang L, Wang Q, Li W. Histone modifications and chromatin organization in prostate cancer. Epigenomics2,551–560 (2010).
  CASGoogle Scholar
• 18  Strahl BD, Allis CD. The language of covalent histone modifications. Nature403,41–45 (2000).
  Medline CASGoogle Scholar
• 19  Ruthenburg AJ, Li H, Patel DJ, Allis CD. Multivalent engagement of chromatin modifications by linked binding modules. Nat. Rev. Mol. Cell Biol.8,983–994 (2007).
  Medline CASGoogle Scholar
• 20  Tan M, Luo H, Lee S et al. Identification of 67 histone marks and histone lysine crotonylation as a new type of histone modification. Cell146,1016–1028 (2011).
  Medline CASGoogle Scholar
• 21  Jenuwein T, Allis CD. Translating the histone code. Science293,1074–1080 (2001).
  Medline CASGoogle Scholar
• 22  Turner BM. Cellular memory and the histone code. Cell111,285–291 (2002).
  Medline CASGoogle Scholar
• 23  Bannister AJ, Kouzarides T. Regulation of chromatin by histone modifications. Cell Res.21,381–395 (2011).
  Medline CASGoogle Scholar
• 24  Cedar H, Bergman Y. Linking DNA methylation and histone modification: patterns and paradigms. Nat. Rev. Genet.10,295–304 (2009).
  Medline CASGoogle Scholar
• 25  Bird A. DNA methylation patterns and epigenetic memory. Gene Dev.16,6–21 (2002).
  Medline CASGoogle Scholar
• 26  Fuks F. DNA methylation and histone modifications: teaming up to silence genes. Curr. Opin. Genet. Dev.15,490–495 (2005).
  Medline CASGoogle Scholar
• 27  Esteller M. Cancer epigenomics: DNA methylomes and histone-modification maps. Nat. Rev. Genet.8,286–298 (2007).
  Medline CASGoogle Scholar
• 28  Alelu-Paz R, Ashour N, Gonzalez-Corpas A, Ropero S. DNA methylation, histone modifications, and signal transduction pathways: a close relationship in malignant gliomas pathophysiology. J. Signal. Trans.2012,956–958 (2012).
  Google Scholar
• 29  Harris RA, Wang T, Coarfa C et al. Comparison of sequencing-based methods to profile DNA methylation and identification of monoallelic epigenetic modifications. Nat. Biotechnol.28,1097–1105 (2010).
  Medline CASGoogle Scholar
• 30  Bock C, Tomazou EM, Brinkman AB et al. Quantitative comparison of genome-wide DNA methylation mapping technologies. Nat. Biotechnol.28,1106–1114 (2010).▪ Describes several methods that have been developed to map DNA methylation on a genomic scale. Most of these methods combine DNA analysis by microarrays or high-throughput sequencing with one of four ways of translating DNA methylation patterns into DNA sequence information or library enrichment.
  Medline CASGoogle Scholar
• 31  Laird PW. Principles and challenges of genomewide DNA methylation analysis. Nat. Rev. Genet.11,191–203 (2010).
  Medline CASGoogle Scholar
• 32  Zilberman D, Henikoff S. Genome-wide analysis of DNA methylation patterns. Development134,3959–3965 (2007).
  Medline CASGoogle Scholar
• 33  Brunner AL, Johnson DS, Kim SW et al. Distinct DNA methylation patterns characterize differentiated human embryonic stem cells and developing human fetal liver. Genome Res.19,1044–1056 (2009).
  Medline CASGoogle Scholar
• 34  Oda M, Glass JL, Thompson RF et al. High-resolution genome-wide cytosine methylation profiling with simultaneous copy number analysis and optimization for limited cell numbers. Nucleic Acids Res.37,3829–3839 (2009).
  Medline CASGoogle Scholar
• 35  Down TA, Rakyan VK, Turner DJ et al. A Bayesian deconvolution strategy for immunoprecipitation-based DNA methylome analysis. Nat. Biotechnol.26,779–785 (2008).
  Medline CASGoogle Scholar
• 36  Coverdale LE, Martin CC. Epigenomics – genome wide modifications of cytosine and new dimensions in our understanding of differentiation and disease. Curr. Genomics6,491–500 (2005).
  CASGoogle Scholar
• 37  Brinkman AB, Simmer F, Ma K, Kaan A, Zhu J, Stunnenberg HG. Whole-genome DNA methylation profiling using methylCap-seq. Methods52,232–236 (2010).
  Medline CASGoogle Scholar
• 38  Serre D, Lee BH, Ting AH. MBD-isolated genome sequencing provides a high-throughput and comprehensive survey of DNA methylation in the human genome. Nucleic Acids Res.38,391–399 (2010).
  Medline CASGoogle Scholar
• 39  Meissner A, Mikkelsen TS, Gu H et al. Genome-scale DNA methylation maps of pluripotent and differentiated cells. Nature454,766–770 (2008).
  Medline CASGoogle Scholar
• 40  Eckhardt F, Lewin J, Cortese R et al. DNA methylation profiling of human chromosomes 6, 20 and 22. Nat. Genet.38,1378–1385 (2006).
  Medline CASGoogle Scholar
• 41  Laird PW. The power and the promise of DNA methylation markers. Nat. Rev. Cancer3,253–266 (2003).
  Medline CASGoogle Scholar
• 42  Pomraning KR, Smith KM, Freitag M. Genome-wide high throughput analysis of DNA methylation in eukaryotes. Methods47,142–150 (2009).
  Medline CASGoogle Scholar
• 43  Sørensen AL, Collas P. Immunoprecipitation of methylated DNA. Methods Mol. Biol.567,249–262 (2009).
  MedlineGoogle Scholar
• 44  Maunakea AK, Nagarajan RP, Bilenky M et al. Conserved role of intragenic DNA methylation in regulating alternative promoters. Nature466,253–257 (2010).
  Medline CASGoogle Scholar
• 45  Lister R, Pelizzola M, Dowen RH et al. Human DNA methylomes at base resolution show widespread epigenomic differences. Nature462,315–322 (2009).
  Medline CASGoogle Scholar
• 46  Meissner A, Gnirke A, Bell GW, Ramsahoye B, Lander ES, Jaenisch R. Reduced representation bisulfite sequencing for comparative high-resolution DNA methylation analysis. Nucleic Acids Res.33,5868–5877 (2005).
  Medline CASGoogle Scholar
• 47  Gu H, Smith ZD, Bock C, Boyle P, Gnirke A, Meissner A. Preparation of reduced representation bisulfite sequencing libraries for genome-scale DNA methylation profiling. Nat. Protoc.6,468–481 (2011).
  Medline CASGoogle Scholar
• 48  Cokus SJ, Feng S, Zhang X et al. Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature452,215–219 (2008).
  Medline CASGoogle Scholar
• 49  Kouzarides T. Chromatin modifications and their function. Cell128,693 (2007).
  Medline CASGoogle Scholar
• 50  Li B, Carey M, Workman JL. The role of chromatin during transcription. Cell128,707–719 (2007).
  Medline CASGoogle Scholar
• 51  Schones DE, Zhao K. Genome-wide approaches to studying chromatin modifications. Nat. Rev. Genet.9,179–191 (2008).
  Medline CASGoogle Scholar
• 52  Iyer VR, Horak CE, Scafe CS, Botstein D, Snyder M, Brown PO. Genomic binding sites of the yeast cell-cycle transcription factors SBF and MBF. Nature409,533–538 (2001).
  Medline CASGoogle Scholar
• 53  Ren B, Robert F, Wyrick JJ et al. Genome-wide location and function of DNA binding proteins. Science290,2306–2309 (2000).
  Medline CASGoogle Scholar
• 54  Zhang Z, Pugh BF. High-resolution genome-wide mapping of the primary structure of chromatin. Cell144,175–186 (2011).
  Medline CASGoogle Scholar
• 55  Zhou VW, Goren A, Bernstein BE. Charting histone modifications and the functional organization of mammalian genomes. Nat. Rev. Genet.12,7–18 (2011).
  MedlineGoogle Scholar
• 56  Wang Z, Zang C, Rosenfeld JA et al. Combinatorial patterns of histone acetylations and methylations in the human genome. Nat. Genet.40,897–903 (2008).
  Medline CASGoogle Scholar
• 57  Vega VB, Cheung E, Palanisamy N, Sung WK. Inherent signals in sequencing-based chromatin-immunoprecipitation control libraries. PLoS One4,e5241 (2009).
  MedlineGoogle Scholar
• 58  Roh T, Zhao K. High-resolution, genome-wide mapping of chromatin modifications by GMAT. Methods Mol. Biol.387,95 (2008).
  Medline CASGoogle Scholar
• 59  Ng P, Tan JJ, Ooi HS et al. Multiplex sequencing of paired-end ditags (MS-PET): a strategy for the ultra-high-throughput analysis of transcriptomes and genomes. Nucleic Acids Res.34,e84–e84 (2006).
  MedlineGoogle Scholar
• 60  Buck MJ, Lieb JD. ChIP-chip: considerations for the design, analysis, and application of genome-wide chromatin immunoprecipitation experiments. Genomics83,349–360 (2004).
  Medline CASGoogle Scholar
• 61  Park PJ. ChIP-seq: advantages and challenges of a maturing technology. Nat. Rev. Genet.10,669–680 (2009).
  Medline CASGoogle Scholar
• 62  Li KK, Luo C, Wang D, Jiang H, Zheng YG. Chemical and biochemical approaches in the study of histone methylation and demethylation. Med. Res. Rev.32,815–867 (2012).
  Medline CASGoogle Scholar
• 63  Heintzman ND, Stuart RK, Hon G et al. Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat. Genet.39,311–318 (2007).
  Medline CASGoogle Scholar
• 64  Kirmizis A, Bartley SM, Kuzmichev A et al. Silencing of human polycomb target genes is associated with methylation of histone H3 Lys 27. Gene Dev.18,1592–1605 (2004).
  Medline CASGoogle Scholar
• 65  Viré E, Brenner C, Deplus R et al. The polycomb group protein EZH2 directly controls DNA methylation. Nature439,871–874 (2005).
  MedlineGoogle Scholar
• 66  Peters AH, Schübeler D. Methylation of histones: playing memory with DNA. Curr. Opin. Cell Biol.17,230–238 (2005).
  Medline CASGoogle Scholar
• 67  Irvine RA, Hsieh CL. Q-PCR in combination with ChIP assays to detect changes in chromatin acetylation. Methods Mol. Biol.287,45–52 (2004).
  Medline CASGoogle Scholar
• 68  Barski A, Cuddapah S, Cui K et al. High-resolution profiling of histone methylations in the human genome. Cell129,823–837 (2007).
  Medline CASGoogle Scholar
• 69  Garcia BA, Pesavento JJ, Mizzen CA, Kelleher NL. Pervasive combinatorial modification of histone H3 in human cells. Nat. Methods4,487–489 (2007).
  Medline CASGoogle Scholar
• 70  Vermeulen M, Eberl HC, Matarese F et al. Quantitative interaction proteomics and genome-wide profiling of epigenetic histone marks and their readers. Cell142,967–980 (2010).
  Medline CASGoogle Scholar
• 71  Vasilescu J, Figeys D. Mapping protein–protein interactions by mass spectrometry. Curr. Opin. Biotech.17,394 (2006).▪▪ Overview of developments in protein interaction mapping by mass spectrometry (MS) and MS-based methods that employ novel affinity purification strategies and affinity tags, as well as a description of in vivo and in vitro chemical crosslinking.
  Medline CASGoogle Scholar
• 72  Ethier M, Lambert JP, Vasilescu J, Figeys D. Analysis of protein interaction networks using mass spectrometry compatible techniques. Anal. Chim. Acta564,10–18 (2006).
  Medline CASGoogle Scholar
• 73  Bauer A, Kuster B. Affinity purification-mass spectrometry. Eur. J. Biochem.270,570–578 (2003).
  Medline CASGoogle Scholar
• 74  Roque A, Lowe C. Affinity chromatography: history, perspectives, limitations and prospects. Methods Mol. Biol.421,1–21 (2008).
  Medline CASGoogle Scholar
• 75  Dunham WH, Mullin M, Gingras AC. Affinity-purification coupled to mass spectrometry: basic principles and strategies. Proteomics12,1576–1590 (2012).
  Medline CASGoogle Scholar
• 76  Puig O, Caspary F, Rigaut G et al. The tandem affinity purification (TAP) method: a general procedure of protein complex purification. Methods24,218–229 (2001).
  Medline CASGoogle Scholar
• 77  Li Y. The tandem affinity purification technology: an overview. Biotechnol. Lett.33,1487–1499 (2011).
  Medline CASGoogle Scholar
• 78  Trinkle-Mulcahy L. Resolving protein interactions and complexes by affinity purification followed by label-based quantitative mass spectrometry. Proteomics12,1623–1638 (2012).
  Medline CASGoogle Scholar
• 79  Galan JA, Paris LL, Zhang HJ, Adler J, Geahlen RL, Tao WA. Proteomic studies of Syk-interacting proteins using a novel amine-specific isotope tag and GFP nanotrap. J. Am. Soc. Mass Spectrom.22,319–328 (2011).
  Medline CASGoogle Scholar
• 80  Oeffinger M. Two steps forward – one step back: advances in affinity purification mass spectrometry of macromolecular complexes. Proteomics12,1591–1608 (2012).
  Medline CASGoogle Scholar
• 81  Breitkreutz A, Choi H, Sharom JR et al. A global protein kinase and phosphatase interaction network in yeast. Science328,1043–1046 (2010).
  Medline CASGoogle Scholar
• 82  Poser I, Sarov M, Hutchins JR et al. BAC TransgeneOmics: a high-throughput method for exploration of protein function in mammals. Nat. Methods5,409–415 (2008).
  Medline CASGoogle Scholar
• 83  Tang X, Bruce JE. Chemical crosslinking for protein–protein interaction studies. Methods Mol. Biol.492,283–293 (2009).
  Medline CASGoogle Scholar
• 84  Sinz A. Chemical crosslinking and mass spectrometry to map three-dimensional protein structures and protein–protein interactions. Mass Spectrom. Rev.25,663–682 (2006).
  Medline CASGoogle Scholar
• 85  Leitner A, Walzthoeni T, Kahraman A et al. Probing native protein structures by chemical crosslinking, mass spectrometry, and bioinformatics. Mol. Cell Proteomics9,1634–1649 (2010).
  Medline CASGoogle Scholar
• 86  Byrum SD, Taverna SD, Tackett AJ. Quantitative analysis of histone exchange for transcriptionally active chromatin. J. Clin. Bioinforma.1,17 (2011).
  Medline CASGoogle Scholar
• 87  Byrum S, Mackintosh SG, Edmondson RD, Cheung WL, Taverna SD, Tackett AJ. Analysis of histone exchange during chromatin purification. J. Integr. OMICS1,61–65 (2011).
  MedlineGoogle Scholar
• 88  Northrup DL, Zhao K. Application of ChIP-seq and related techniques to the study of immune function. Immunity34,830–842 (2011).
  Medline CASGoogle Scholar
• 89  Das PM, Ramachandran K, Vanwert J, Singal R. Chromatin immunoprecipitation assay. Biotechniques37,961–969 (2004).
  Medline CASGoogle Scholar
• 90  O’Neill LP, Turner BM. Immunoprecipitation of native chromatin: NChIP. Methods31,76–82 (2003).
  MedlineGoogle Scholar
• 91  Krogan NJ, Cagney G, Yu H et al. Global landscape of protein complexes in the yeast Saccharomyces cerevisiae. Nature440,637–643 (2006).
  Medline CASGoogle Scholar
• 92  Stunnenberg HG, Vermeulen M. Towards cracking the epigenetic code using a combination of high-throughput epigenomics and quantitative mass spectrometry-based proteomics. Bioessays33,547–551 (2011).
  Medline CASGoogle Scholar
• 93  Dawson MA, Kouzarides T. Cancer epigenetics: from mechanism to therapy. Cell150,12–27 (2012).
  Medline CASGoogle Scholar
• 94  Ueberheide BM, Mollah S. Deciphering the histone code using mass spectrometry. Int. J. Mass Spectrom.259,46–56 (2007).
  CASGoogle Scholar
• 95  Bartke T, Borgel J, Dimaggio PA. Proteomics in epigenetics: new perspectives for cancer research. Brief Funct. Genomics12(3),205–218 (2013).▪▪ Overview of the applications of MS-based proteomics in studying various aspects of chromatin biology, the use of MS in the discovery and mapping of histone modifications and how novel proteomic approaches are being utilized to identify and study chromatin-associated proteins and multisubunit complexes.
  Medline CASGoogle Scholar
• 96  Young NL, Dimaggio PA, Garcia BA. The significance, development and progress of high-throughput combinatorial histone code analysis. Cell Mol. Life Sci.67,3983–4000 (2010).
  Medline CASGoogle Scholar
• 97  Yates JR, Ruse CI, Nakorchevsky A. Proteomics by mass spectrometry: approaches, advances, and applications. Annu. Rev. Biomed. Eng.11,49–79 (2009).
  Medline CASGoogle Scholar
• 98  Zee BM, Garcia BA. Validation of protein acetylation by mass spectrometry. Methods Mol. Biol.981,1–11 (2013).
  Medline CASGoogle Scholar
• 99  Sidoli S, Cheng L, Jensen ON. Proteomics in chromatin biology and epigenetics: Elucidation of post-translational modifications of histone proteins by mass spectrometry. J. Proteomics75,3419–3433 (2012).
  Medline CASGoogle Scholar
• 100  Lin S, Garcia BA. Examining histone posttranslational modification patterns by high-resolution mass spectrometry. Methods Enzymol.512,3–28 (2012).
  Medline CASGoogle Scholar
• 101  Siuti N, Kelleher NL. Decoding protein modifications using top-down mass spectrometry. Nat. Methods4,817–821 (2007).
  Medline CASGoogle Scholar
• 102  Macek B, Waanders LF, Olsen JV, Mann M. Top-down protein sequencing and MS3 on a hybrid linear quadrupole ion trap-orbitrap mass spectrometer. Mol. Cell Proteomics5,949–958 (2006).
  Medline CASGoogle Scholar
• 103  Pesavento JJ, Kim YB, Taylor GK, Kelleher NL. Shotgun annotation of histone modifications: a new approach for streamlined characterization of proteins by top down mass spectrometry. J. Am. Chem. Soc.126,3386–3387 (2004).
  Medline CASGoogle Scholar
• 104  Thomas CE, Kelleher NL, Mizzen CA. Mass spectrometric characterization of human histone H3: a bird’s eye view. J. Proteome Res.5,240–247 (2006).
  Medline CASGoogle Scholar
• 105  Young NL, Dimaggio PA, Plazas-Mayorca MD, Baliban RC, Floudas CA, Garcia BA. High throughput characterization of combinatorial histone codes. Mol. Cell Proteomics8,2266–2284 (2009).
  Medline CASGoogle Scholar
• 106  Boyne MT 2nd, Pesavento JJ, Mizzen CA, Kelleher NL. Precise characterization of human histones in the H2A gene family by top down mass spectrometry. J. Proteome Res.5,248–253 (2006).
  Medline CASGoogle Scholar
• 107  Soldi M, Bonaldi T. The proteomic investigation of chromatin functional domains reveals novel synergisms among distinct heterochromatin components. Mol. Cell Proteomics12,764–780 (2013).▪ Overview of affinity-interaction assays using different baits in conjunction with SILAC-based proteomics and the development of a global, quantitative proteomic strategy named ‘chromatin proteomics’ to analyze the protein component characterizing distinct chromatin regions.
  Medline CASGoogle Scholar
• 108  Pokholok DK, Harbison CT, Levine S et al. Genome-wide map of nucleosome acetylation and methylation in yeast. Cell122,517–527 (2005).
  Medline CASGoogle Scholar
• 109  Nelson EA, Walker SR, Alvarez JV, Frank DA. Isolation of unique STAT5 targets by chromatin immunoprecipitation-based gene identification. J. Biol. Chem.279,54724–54730 (2004).
  Medline CASGoogle Scholar
• 110  Voigt P, Leroy G, Drury WJ 3rd et al. Asymmetrically modified nucleosomes. Cell151,181–193 (2012).
  Medline CASGoogle Scholar
• 111  Vinckevicius A, Chakravarti D. Chromatin immunoprecipitation: advancing analysis of nuclear hormone signaling. J. Mol. Endocrinol.49,R113–R123 (2012).
  Medline CASGoogle Scholar
• 112  Nelson JD, Denisenko O, Bomsztyk K. Protocol for the fast chromatin immunoprecipitation (ChIP) method. Nat. Protoc.1,179–185 (2006).
  Medline CASGoogle Scholar
• 113  Collas P, Dahl JA. Chop it, ChIP it, check it: the current status of chromatin immunoprecipitation. Front. Biosci.13,929–943 (2008).
  Medline CASGoogle Scholar
• 114  Collas P. The current state of chromatin immunoprecipitation. Mol. Biotechnol.45,87–100 (2010).▪ Describes recent developments in the chromatin immunoprecipitation field that have led to the emergence of protocols aiming to reduce cell numbers.
  Medline CASGoogle Scholar
• 115  Garcia BA, Shabanowitz J, Hunt DF. Characterization of histones and their post-translational modifications by mass spectrometry. Curr. Opin. Chem. Biol.11(1),66–73 (2007).
  Medline CASGoogle Scholar
• 116  Beck HC. Mass spectrometry in epigenetic research. Methods Mol. Biol.593,263–282 (2010).
  Medline CASGoogle Scholar
• 117  Hardison RC, Taylor J. Genomic approaches towards finding cis-regulatory modules in animals. Nat. Rev. Genet.13,469–483 (2012).
  Medline CASGoogle Scholar
• 118  Leroy G, Chepelev I, Dimaggio PA et al. Proteogenomic characterization and mapping of nucleosomes decoded by Brd and HP1 proteins. Genome Biol.13,R68 (2012).
  MedlineGoogle Scholar
• 119  Wang CI, Alekseyenko AA, Leroy G et al. Chromatin proteins captured by ChIP-mass spectrometry are linked to dosage compensation in Drosophila. Nat. Struct. Mol. Biol.20,202–209 (2013).
  Medline CASGoogle Scholar
• 120  Price CM, Cech TR. Telomeric DNA–protein interactions of oxytricha macronuclear DNA. Gene Dev.1,783–793 (1987).
  Medline CASGoogle Scholar
• 121  Lambert JP, Mitchell L, Rudner A, Baetz K, Figeys D. A novel proteomics approach for the discovery of chromatin-associated protein networks. Mol. Cell Proteomics8,870–882 (2009).
  Medline CASGoogle Scholar
• 122  Wood A, Schneider J, Dover J, Johnston M, Shilatifard A. The Bur1/Bur2 complex is required for histone H2B monoubiquitination by Rad6/Bre1 and histone methylation by COMPASS. Mol. Cell20,589–599 (2005).
  Medline CASGoogle Scholar
• 123  Chu DS, Liu H, Nix P et al. Sperm chromatin proteomics identifies evolutionarily conserved fertility factors. Nature443,101–105 (2006).
  Medline CASGoogle Scholar
• 124  Griesenbeck J, Boeger H, Strattan JS, Kornberg RD. Affinity purification of specific chromatin segments from chromosomal loci in yeast. Mol. Cell Biol.23,9275–9282 (2003).
  Medline CASGoogle Scholar
• 125  Rusk N. Reverse ChIP. Nat. Methods6,187–187 (2009).
  CASGoogle Scholar
• 126  Byrum SD, Raman A, Taverna SD, Tackett AJ. ChAP–MS: a method for identification of proteins and histone posttranslational modifications at a single genomic locus. Cell Reports2(1),198–205 (2012).
  Medline CASGoogle Scholar
• 127  Déjardin J, Kingston RE. Purification of proteins associated with specific genomic Loci. Cell136,175–186 (2009).
  Medline CASGoogle Scholar
• 128  Wu CH, Chen S, Shortreed MR et al. Sequence-specific capture of protein–DNA complexes for mass spectrometric protein identification. PLoS One6,e26217 (2011).
  Medline CASGoogle Scholar
• 129  Fujita T, Fujii H. Direct identification of insulator components by insertional chromatin immunoprecipitation. PLoS One6,e26109 (2011).
  Medline CASGoogle Scholar
• 130  Fujita T, Fujii H. Locus-specific biochemical epigenetics/chromatin biochemistry by insertional chromatin immunoprecipitation. ISRN Biochem.2013,913273 (2013).
  MedlineGoogle Scholar
• 131  Agelopoulos M, Mckay DJ, Mann RS. Developmental regulation of chromatin conformation by Hox proteins in Drosophila. Cell Rep.1,350–359 (2012).
  Medline CASGoogle Scholar
• 132  Eberl HC, Mann M, Vermeulen M. Quantitative proteomics for epigenetics. Chembiochem12,224–234 (2011).
  Medline CASGoogle Scholar
• 133  Cox J, Mann M. Quantitative, high-resolution proteomics for data-driven systems biology. Annu. Rev. Biochem.80,273–299 (2011).
  Medline CASGoogle Scholar
• 134  Vermeulen M, Mulder KW, Denissov S et al. Selective anchoring of TFIID to nucleosomes by trimethylation of histone H3 lysine 4. Cell131,58–69 (2007).
  Medline CASGoogle Scholar
• 135  Katan-Khaykovich Y, Struhl K. Splitting of H3–H4 tetramers at transcriptionally active genes undergoing dynamic histone exchange. Proc. Natl Acad. Sci. USA108,1296–1301 (2011).
  Medline CASGoogle Scholar
• 136  Greer EL, Shi Y. Histone methylation: a dynamic mark in health, disease and inheritance. Nat. Rev. Genet.13,343–357 (2012).
  Medline CASGoogle Scholar
• 137  Bartke T, Vermeulen M, Xhemalce B, Robson SC, Mann M, Kouzarides T. Nucleosome-interacting proteins regulated by DNA and histone methylation. Cell143,470–484 (2010).
  Medline CASGoogle Scholar
• 138  Li X, Foley EA, Molloy KR, Li Y, Chait BT, Kapoor TM. Quantitative chemical proteomics approach to identify post-translational modification-mediated protein–protein interactions. J. Am. Chem. Soc.134,1982–1985 (2012).
  Medline CASGoogle Scholar
• 139  Bogdanovic O, Veenstra GJ. Affinity-based enrichment strategies to assay methyl-CpG binding activity and DNA methylation in early Xenopus embryos. BMC Res. Notes4,300 (2011).
  Medline CASGoogle Scholar
• 140  Mittler G, Butter F, Mann M. A SILAC-based DNA protein interaction screen that identifies candidate binding proteins to functional DNA elements. Genome Res.19,284–293 (2009).
  Medline CASGoogle Scholar
• 141  Spruijt CG, Gnerlich F, Smits AH et al. Dynamic readers for 5-(hydroxy)methylcytosine and its oxidized derivatives. Cell152,1146–1159 (2013).
  Medline CASGoogle Scholar
• 142  O’Neill LP, Vermilyea MD, Turner BM. Epigenetic characterization of the early embryo with a chromatin immunoprecipitation protocol applicable to small cell populations. Nat. Genet.38,835–841 (2006).
  MedlineGoogle Scholar
• 143  Dahl JA, Collas P. Q2ChIP, a quick and quantitative chromatin immunoprecipitation assay, unravels epigenetic dynamics of developmentally regulated genes in human carcinoma cells. Stem Cells25,1037–1046 (2007).
  Medline CASGoogle Scholar
• 144  Dahl JA, Collas P. MicroChIP – a rapid micro chromatin immunoprecipitation assay for small cell samples and biopsies. Nucleic Acids Res.36,e15 (2008).
  MedlineGoogle Scholar
• 145  Dahl JA, Collas P. A rapid micro chromatin immunoprecipitation assay (microChIP). Nat. Protoc.3,1032–1045 (2008).
  Medline CASGoogle Scholar
• 146  Flanagin S, Nelson JD, Castner DG, Denisenko O, Bomsztyk K. Microplate-based chromatin immunoprecipitation method, Matrix ChIP: a platform to study signaling of complex genomic events. Nucleic Acids Res.36,e17 (2008).
  MedlineGoogle Scholar