Proteomics to study DNA-bound and chromatin-associated gene regulatory complexes

Human Molecular Genetics

Volumn 25, Issue R2, 2016, Pages R106-R114

  Wierer, Michael ^a   Mann, Matthias ^a  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; HISTONE; PROTEOME; TRANSCRIPTION FACTOR;

CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; EPIGENETICS; GENE CONTROL; GENE EXPRESSION REGULATION; GENE LOCUS; HISTONE MODIFICATION; HUMAN; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEOMICS; REVIEW;

EID: 84994153091     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddw208     Document Type: Review

References (93)

1. Altelaar, A.F., Munoz, J., and Heck, A.J. (2013) Next-generation proteomics: towards an integrative view of proteome dynamics. Nat. Rev. Genet., 14, 35-48.
2. Gingras, A.C., Gstaiger, M., Raught, B., and Aebersold, R. (2007) Analysis of protein complexes using mass spectrometry. Nat. Rev. Mol. Cell Biol., 8, 645-654.
3. Dunham, W.H., Mullin, M., and Gingras, A.C. (2012) Affinitypurification coupled to mass spectrometry: basic principles and strategies. Proteomics, 12, 1576-1590.
4. Ong, S.E., and Mann, M. (2007) Stable isotope labeling by amino acids in cell culture for quantitative proteomics. Methods Mol. Biol., 359, 37-52.
5. Cox, J., Hein, M.Y., Luber, C.A., Paron, I., Nagaraj, N., and Mann, M. (2014) Accurate proteome-wide label-free quantification by delayed normalization and maximal peptide ratio extraction, termed MaxLFQ. Mol. Cell. Proteomics, 13, 2513-2526.
6. Cappadona, S., Baker, P.R., Cutillas, P.R., Heck, A.J., and van Breukelen, B. (2012) Current challenges in software solutions for mass spectrometry-based quantitative proteomics. Amino Acids, 43, 1087-1108.
7. Krogan, N.J., Cagney, G., Yu, H., Zhong, G., Guo, X., Ignatchenko, A., Li, J., Pu, S., Datta, N., Tikuisis, A.P., et al. (2006) Global landscape of protein complexes in the yeast Saccharomyces cerevisiae. Nature, 440, 637-643.
8. Havugimana, P.C., Hart, G.T., Nepusz, T., Yang, H., Turinsky, A.L., Li, Z., Wang, P.I., Boutz, D.R., Fong, V., Phanse, S., et al. (2012) A census of human soluble protein complexes. Cell, 150, 1068-1081.
9. Hein, M.Y., Hubner, N.C., Poser, I., Cox, J., Nagaraj, N., Toyoda, Y., Gak, I.A., Weisswange, I., Mansfeld, J., Buchholz, F., et al. (2015) A human interactome in three quantitative dimensions organized by stoichiometries and abundances. Cell, 163, 712-723.
10. Huttlin, E.L., Ting, L., Bruckner, R.J., Gebreab, F., Gygi, M.P., Szpyt, J., Tam, S., Zarraga, G., Colby, G., Baltier, K., et al. (2015) The BioPlex Network: A Systematic Exploration of the Human Interactome. Cell, 162, 425-440.
11. Huang, H., Lin, S., Garcia, B.A., and Zhao, Y. (2015) Quantitative proteomic analysis of histone modifications. Chem. Rev., 115, 2376-2418.
12. Lange, M., Demajo, S., Jain, P., and Di Croce, L. (2011) Combinatorial assembly and function of chromatin regulatory complexes. Epigenomics, 3, 567-580.
13. Dasgupta, S., Lonard, D.M., and O'Malley, B.W. (2014) Nuclear receptor coactivators: master regulators of human health and disease. Ann. Rev. Med., 65, 279-292.
14. Chou, D.M., Adamson, B., Dephoure, N.E., Tan, X., Nottke, A.C., Hurov, K.E., Gygi, S.P., Colaiacovo, M.P., and Elledge, S.J. (2010) A chromatin localization screen reveals poly (ADP ribose)-regulated recruitment of the repressive polycomb and NuRD complexes to sites of DNA damage. Proc. Natl. Acad. Sci. U S A., 107, 18475-18480.
15. Kim, D.R., Gidvani, R.D., Ingalls, B.P., Duncker, B.P., and McConkey, B.J. (2011) Differential chromatin proteomics of the MMS-induced DNA damage response in yeast. Proteome Science, 9, 62.
16. Raschle, M., Smeenk, G., Hansen, R.K., Temu, T., Oka, Y., Hein, M.Y., Nagaraj, N., Long, D.T., Walter, J.C., Hofmann, K., et al. (2015) DNA repair. Proteomics reveals dynamic assembly of repair complexes during bypass of DNA cross-links. Science, 348, 1253671.
17. Khoudoli, G.A., Gillespie, P.J., Stewart, G., Andersen, J.S., Swedlow, J.R., and Blow, J.J. (2008) Temporal profiling of the chromatin proteome reveals system-wide responses to replication inhibition. Curr. Biol., 18, 838-843.
18. Kubota, T., Hiraga, S., Yamada, K., Lamond, A.I., and Donaldson, A.D. (2011) Quantitative proteomic analysis of chromatin reveals that Ctf18 acts in the DNA replication checkpoint. Mol. Cell. Proteomics, 10, M110 005561.
19. Sirbu, B.M., Couch, F.B., and Cortez, D. (2012) Monitoring the spatiotemporal dynamics of proteins at replication forks and in assembled chromatin using isolation of proteins on nascent DNA. Nat. Protoc., 7, 594-605.
20. Alabert, C., Bukowski-Wills, J.C., Lee, S.B., Kustatscher, G., Nakamura, K., de Lima Alves, F., Menard, P., Mejlvang, J., Rappsilber, J., and Groth, A. (2014) Nascent chromatin capture proteomics determines chromatin dynamics during DNA replication and identifies unknown fork components. Nat. Cell Biol., 16, 281-293.
21. Ohta, S., Bukowski-Wills, J.C., Sanchez-Pulido, L., Alves Fde, L., Wood, L., Chen, Z.A., Platani, M., Fischer, L., Hudson, D.F., Ponting, C.P., et al. (2010) The protein composition of mitotic chromosomes determined using multiclassifier combinatorial proteomics. Cell, 142, 810-821.
22. Campos, E.I., Smits, A.H., Kang, Y.H., Landry, S., Escobar, T.M., Nayak, S., Ueberheide, B.M., Durocher, D., Vermeulen, M., Hurwitz, J., et al. (2015) Analysis of the Histone H3.1 Interactome: A Suitable Chaperone for the Right Event. Mol. Cell, 60, 697-709.
23. Shiio, Y., Eisenman, R.N., Yi, E.C., Donohoe, S., Goodlett, D.R., and Aebersold, R. (2003) Quantitative proteomic analysis of chromatin-associated factors. J. Am. Soc. Mass. Spectrom., 14, 696-703.
24. Torrente, M.P., Zee, B.M., Young, N.L., Baliban, R.C., LeRoy, G., Floudas, C.A., Hake, S.B., and Garcia, B.A. (2011) Proteomic interrogation of human chromatin. PloS One, 6, e24747.
25. Alajem, A., Biran, A., Harikumar, A., Sailaja, B.S., Aaronson, Y., Livyatan, I., Nissim-Rafinia, M., Sommer, A.G., Mostoslavsky, G., Gerbasi, V.R., et al. (2015) Differential association of chromatin proteins identifies BAF60a/SMARCD1 as a regulator of embryonic stem cell differentiation. Cell Rep., 10, 2019-2031.
26. Kustatscher, G., Hegarat, N., Wills, K.L., Furlan, C., Bukowski-Wills, J.C., Hochegger, H., and Rappsilber, J. (2014) Proteomics of a fuzzy organelle: interphase chromatin. EMBO J., 33, 648-664.
27. Kustatscher, G., Wills, K.L., Furlan, C., and Rappsilber, J. (2014) Chromatin enrichment for proteomics. Nat. Protoc., 9, 2090-2099.
28. Strahl, B.D., and Allis, C.D. (2000) The language of covalent histone modifications. Nature, 403, 41-45.
29. Wysocka, J., Swigut, T., Milne, T.A., Dou, Y., Zhang, X., Burlingame, A.L., Roeder, R.G., Brivanlou, A.H., and Allis, C.D. (2005) WDR5 associates with histone H3 methylated at K4 and is essential for H3 K4 methylation and vertebrate development. Cell, 121, 859-872.
30. 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. (2006) A PHD finger of NURF couples histone H3 lysine 4 trimethylation with chromatin remodelling. Nature, 442, 86-90.
31. 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., and Timmers, H.T. (2007) Selective anchoring of TFIID to nucleosomes by trimethylation of histone H3 lysine 4. Cell, 131, 58-69.
32. Vermeulen, M., Eberl, H.C., Matarese, F., Marks, H., Denissov, S., Butter, F., Lee, K.K., Olsen, J.V., Hyman, A.A., Stunnenberg, H.G., et al. (2010) Quantitative interaction proteomics and genome-wide profiling of epigenetic histone marks and their readers. Cell, 142, 967-980.
33. Migliori, V., Muller, J., Phalke, S., Low, D., Bezzi, M., Mok, W.C., Sahu, S.K., Gunaratne, J., Capasso, P., Bassi, C., et al. (2012) Symmetric dimethylation of H3R2 is a newly identified histone mark that supports euchromatin maintenance. Nat. Struct. Mol. Biol., 19, 136-144.
34. 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.
35. Bluhm, A., Casas-Vila, N., Scheibe, M., and Butter, F. (2015) Reader interactome of epigenetic histone marks in birds. Proteomics, 16:427-436.
36. 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.
37. Shema-Yaacoby, E., Nikolov, M., Haj-Yahya, M., Siman, P., Allemand, E., Yamaguchi, Y., Muchardt, C., Urlaub, H., Brik, A., Oren, M., et al. (2013) Systematic identification of proteins binding to chromatin-embedded ubiquitylated H2B reveals recruitment of SWI/SNF to regulate transcription. Cell Rep., 4, 601-608.
38. Bartke, T., Vermeulen, M., Xhemalce, B., Robson, S.C., Mann, M., and Kouzarides, T. (2010) Nucleosome-interacting proteins regulated by DNA and histone methylation. Cell, 143, 470-484.
39. Bannister, A.J., and Kouzarides, T. (2011) Regulation of chromatin by histone modifications. Cell Res., 21, 381-395.
40. Park, P.J. (2009) ChIP-seq: advantages and challenges of a maturing technology. Nat. Rev. Genet., 10, 669-680.
41. Furey, T.S. (2012) ChIP-seq and beyond: new and improved methodologies to detect and characterize protein-DNA interactions. Nat. Rev., Genet., 13, 840-852.
42. Wang, C.I., Alekseyenko, A.A., LeRoy, G., Elia, A.E., Gorchakov, A.A., Britton, L.M., Elledge, S.J., Kharchenko, P.V., Garcia, B.A., and Kuroda, M.I. (2013) Chromatin proteins captured by ChIP-mass spectrometry are linked to dosage compensation in Drosophila. Nat. Struct. Mol. Biol., 20, 202-209.
43. Won, K.J., Choi, I., LeRoy, G., Zee, B.M., Sidoli, S., Gonzales-Cope, M., and Garcia, B.A. (2015) Proteogenomics analysis reveals specific genomic orientations of distal regulatory regions composed by non-canonical histone variants. Epigenetics Chromatin, 8, 13.
44. Soldi, M., and Bonaldi, T. (2013) The proteomic investigation of chromatin functional domains reveals novel synergisms among distinct heterochromatin components. Mol. Cell. Proteomics, 12, 764-780.
45. Soldi, M., and Bonaldi, T. (2014) The ChroP approach combines ChIP and mass spectrometry to dissect locus-specific proteomic landscapes of chromatin. J. Vis. Exp., doi: 10.3791/51220.
46. Lambert, J.P., Mitchell, L., Rudner, A., Baetz, K., and Figeys, D. (2009) A novel proteomics approach for the discovery of chromatin-associated protein networks. Mol. Cell. Proteomics, 8, 870-882.
47. Lambert, J.P., Fillingham, J., Siahbazi, M., Greenblatt, J., Baetz, K., and Figeys, D. (2010) Defining the budding yeast chromatin-associated interactome. Mol. Syst. Biol., 6, 448.
48. Mohammed, H., D'Santos, C., Serandour, A.A., Ali, H.R., Brown, G.D., Atkins, A., Rueda, O.M., Holmes, K.A., Theodorou, V., Robinson, J.L., et al. (2013) Endogenous purification reveals GREB1 as a key estrogen receptor regulatory factor. Cell Rep., 3, 342-349.
49. Mohammed, H., Russell, I.A., Stark, R., Rueda, O.M., Hickey, T.E., Tarulli, G.A., Serandour, A.A., Birrell, S.N., Bruna, A., Saadi, A., et al. (2015) Progesterone receptor modulates ERalpha action in breast cancer. Nature, 523, 313-317.
50. Mohammed, H., Taylor, C., Brown, G.D., Papachristou, E.K., Carroll, J.S., and D'Santos, C.S. (2016) Rapid immunoprecipitation mass spectrometry of endogenous proteins (RIME) for analysis of chromatin complexes. Nat. Protoc., 11, 316-326.
51. Ji, X., Dadon, D.B., Abraham, B.J., Lee, T.I., Jaenisch, R., Bradner, J.E., and Young, R.A. (2015) Chromatin proteomic profiling reveals novel proteins associated with histonemarked genomic regions. Proc. Natl. Acad. Sci. U S A, 112, 3841-3846.
52. Engelen, E., Brandsma, J.H., Moen, M.J., Signorile, L., Dekkers, D.H., Demmers, J., Kockx, C.E., Ozgur, Z., van, I.W.F., van den Berg, D.L., et al. (2015) Proteins that bind regulatory regions identified by histone modification chromatin immunoprecipitations and mass spectrometry. Nat. Commun., 6, 7155.
53. Alekseyenko, A.A., McElroy, K.A., Kang, H., Zee, B.M., Kharchenko, P.V., and Kuroda, M.I. (2015) BioTAP-XL: Crosslinking/Tandem Affinity Purification to Study DNA Targets, RNA, and Protein Components of Chromatin-Associated Complexes. Current Protocols in Molecular Biology/Edited by Frederick M. Ausubel. [et al.], 109, 21 30-32. 21.
54. Zee, B.M., Alekseyenko, A.A., McElroy, K.A., and Kuroda, M.I. (2016) Streamlined discovery of cross-linked chromatin complexes and associated histone modifications by mass spectrometry. Proc. Natl. Acad. Sci. U S A, 113, 1784-1789.
55. Alekseyenko, A.A., Gorchakov, A.A., Kharchenko, P.V., and Kuroda, M.I. (2014) Reciprocal interactions of human C10orf12 and C17orf96 with PRC2 revealed by BioTAP-XL cross-linking and affinity purification. Proc. Natl. Acad. Sci. U S A, 111, 2488-2493.
56. Alekseyenko, A.A., Gorchakov, A.A., Zee, B.M., Fuchs, S.M., Kharchenko, P.V., and Kuroda, M.I. (2014) Heterochromatinassociated interactions of Drosophila HP1a with dADD1, HIPP1, and repetitive RNAs. Genes & Dev., 28, 1445-1460.
57. Mitchell, L., Huard, S., Cotrut, M., Pourhanifeh-Lemeri, R., Steunou, A.L., Hamza, A., Lambert, J.P., Zhou, H., Ning, Z., Basu, A., et al. (2013) mChIP-KAT-MS, a method to map protein interactions and acetylation sites for lysine acetyltransferases. Proc. Natl. Acad. Sci. U S A, 110, E1641-E1650.
58. Rinn, J.L., and Chang, H.Y. (2012) Genome regulation by long noncoding RNAs. Ann. Rev. Biochem., 81, 145-166.
59. Quinodoz, S., and Guttman, M. (2014) Long noncoding RNAs: an emerging link between gene regulation and nuclear organization. Trends Cell Biol., 24, 651-663.
60. Chu, C., Qu, K., Zhong, F.L., Artandi, S.E., and Chang, H.Y. (2011) Genomic maps of long noncoding RNA occupancy reveal principles of RNA-chromatin interactions. Mol. Cell, 44, 667-678.
61. Chu, C., Zhang, Q.C., da Rocha, S.T., Flynn, R.A., Bharadwaj, M., Calabrese, J.M., Magnuson, T., Heard, E., and Chang, H.Y. (2015) Systematic discovery of Xist RNA binding proteins. Cell, 161, 404-416.
62. McHugh, C.A., Chen, C.K., Chow, A., Surka, C.F., Tran, C., McDonel, P., Pandya-Jones, A., Blanco, M., Burghard, C., Moradian, A., et al. (2015) The Xist lncRNA interacts directly with SHARP to silence transcription through HDAC3. Nature, 521, 232-236.
63. Mittler, G., Butter, F., and Mann, M. (2009) A SILAC-based DNA protein interaction screen that identifies candidate binding proteins to functional DNA elements. Genome Res., 19, 284-293.
64. Kappei, D., Butter, F., Benda, C., Scheibe, M., Draskovic, I., Stevense, M., Novo, C.L., Basquin, C., Araki, M., Araki, K., et al. (2013) HOT1 is a mammalian direct telomere repeat-binding protein contributing to telomerase recruitment. EMBO J., 32, 1681-1701.
65. Casas-Vila, N., Scheibe, M., Freiwald, A., Kappei, D., and Butter, F. (2015) Identification of TTAGGG-binding proteins in Neurospora crassa, a fungus with vertebrate-like telomere repeats. BMC Genomics, 16, 965.
66. Bejerano, G., Pheasant, M., Makunin, I., Stephen, S., Kent, W.J., Mattick, J.S., and Haussler, D. (2004) Ultraconserved elements in the human genome. Science, 304, 1321-1325.
67. Viturawong, T., Meissner, F., Butter, F., and Mann, M. (2013) A DNA-centric protein interaction map of ultraconserved elements reveals contribution of transcription factor binding hubs to conservation. Cell Rep., 5, 531-545.
68. Markljung, E., Jiang, L., Jaffe, J.D., Mikkelsen, T.S., Wallerman, O., Larhammar, M., Zhang, X., Wang, L., Saenz-Vash, V., Gnirke, A., et al. (2009) ZBED6, a novel transcription factor derived from a domesticated DNA transposon regulates IGF2 expression and muscle growth. PLoS Biol., 7, e1000256.
69. Butter, F., Kappei, D., Buchholz, F., Vermeulen, M., and Mann, M. (2010) A domesticated transposon mediates the effects of a single-nucleotide polymorphism responsible for enhanced muscle growth. EMBO Rep., 11, 305-311.
70. Butter, F., Davison, L., Viturawong, T., Scheibe, M., Vermeulen, M., Todd, J.A., and Mann, M. (2012) Proteomewide analysis of disease-associated SNPs that show allelespecific transcription factor binding. PLoS Genet., 8, e1002982.
71. Makowski, M.M., Willems, E., Fang, J., Choi, J., Zhang, T., Jansen, P.W., Brown, K.M., and Vermeulen, M. (2015) An interaction proteomics survey of transcription factor binding at recurrent TERT promoter mutations. Proteomics, 16:417-426.
72. Horn, S., Figl, A., Rachakonda, P.S., Fischer, C., Sucker, A., Gast, A., Kadel, S., Moll, I., Nagore, E., Hemminki, K., et al. (2013) TERT promoter mutations in familial and sporadic melanoma. Science, 339, 959-961.
73. Huang, F.W., Hodis, E., Xu, M.J., Kryukov, G.V., Chin, L., and Garraway, L.A. (2013) Highly recurrent TERT promoter mutations in human melanoma. Science, 339, 957-959.
74. Bell, R.J., Rube, H.T., Kreig, A., Mancini, A., Fouse, S.D., Nagarajan, R.P., Choi, S., Hong, C., He, D., Pekmezci, M., et al. (2015) Cancer. The transcription factor GABP selectively binds and activates the mutant TERT promoter in cancer. Science, 348, 1036-1039.
75. Hubner, N.C., Nguyen, L.N., Hornig, N.C., and Stunnenberg, H.G. (2015) A quantitative proteomics tool to identify DNAprotein interactions in primary cells or blood. J. Proteome Res., 14, 1315-1329.
76. Bartels, S.J., Spruijt, C.G., Brinkman, A.B., Jansen, P.W., Vermeulen, M., and Stunnenberg, H.G. (2011) A SILAC-based screen for Methyl-CpG binding proteins identifies RBP-J as a DNA methylation and sequence-specific binding protein. PloS One, 6, e25884.
77. Spruijt, C.G., Gnerlich, F., Smits, A.H., Pfaffeneder, T., Jansen, P.W., Bauer, C., Munzel, M., Wagner, M., Muller, M., Khan, F., et al. (2013) Dynamic readers for 5-(hydroxy)methylcytosine and its oxidized derivatives. Cell, 152, 1146-1159.
78. Vasanthakumar, A., and Godley, L.A. (2015) 5-hydroxymethylcytosine in cancer: significance in diagnosis and therapy. Cancer Genet., 208, 167-177.
79. Dejardin, J., and Kingston, R.E. (2009) Purification of proteins associated with specific genomic Loci. Cell, 136, 175-186.
80. Antao, J.M., Mason, J.M., Dejardin, J., and Kingston, R.E. (2012) Protein landscape at Drosophila melanogaster telomereassociated sequence repeats. Mol. Cell. Biol., 32, 2170-2182.
81. Byrum, S.D., Raman, A., Taverna, S.D., and Tackett, A.J. (2012) ChAP-MS: a method for identification of proteins and histone posttranslational modifications at a single genomic locus. Cell Rep., 2, 198-205.
82. Fujita, T., and Fujii, H. (2011) Direct identification of insulator components by insertional chromatin immunoprecipitation. PloS One, 6, e26109.
83. Pourfarzad, F., Aghajanirefah, A., de Boer, E., Ten Have, S., Bryn van Dijk, T., Kheradmandkia, S., Stadhouders, R., Thongjuea, S., Soler, E., Gillemans, N., et al. (2013) Locusspecific proteomics by TChP: targeted chromatin purification. Cell Rep., 4, 589-600.
84. Bogdanove, A.J., and Voytas, D.F. (2011) TAL effectors: customizable proteins for DNA targeting. Science, 333, 1843-1846.
85. Byrum, S.D., Taverna, S.D., and Tackett, A.J. (2013) Purification of a specific native genomic locus for proteomic analysis. Nucleic Acids Res., 41, e195.
86. Fujita, T., Asano, Y., Ohtsuka, J., Takada, Y., Saito, K., Ohki, R., and Fujii, H. (2013) Identification of telomereassociated molecules by engineered DNA-binding moleculemediated chromatin immunoprecipitation (enChIP). Sci. Rep., 3, 3171.
87. Sander, J.D., and Joung, J.K. (2014) CRISPR-Cas systems for editing, regulating and targeting genomes. Nat. Biotechnol., 32, 347-355.
88. Gilbert, L.A., Horlbeck, M.A., Adamson, B., Villalta, J.E., Chen, Y., Whitehead, E.H., Guimaraes, C., Panning, B., Ploegh, H.L., Bassik, M.C., et al. (2014) Genome-Scale CRISPR-Mediated Control of Gene Repression and Activation. Cell, 159, 647-661.
89. Gilbert, L.A., Larson, M.H., Morsut, L., Liu, Z., Brar, G.A., Torres, S.E., Stern-Ginossar, N., Brandman, O., Whitehead, E.H., Doudna, J.A., et al. (2013) CRISPR-mediated modular RNA-guided regulation of transcription in eukaryotes. Cell, 154, 442-451.
90. Waldrip, Z.J., Byrum, S.D., Storey, A.J., Gao, J., Byrd, A.K., Mackintosh, S.G., Wahls, W.P., Taverna, S.D., Raney, K.D., and Tackett, A.J. (2014) A CRISPR-based approach for proteomic analysis of a single genomic locus. Epigenetics, 9, 1207-1211.
91. Fujita, T., and Fujii, H. (2013) Efficient isolation of specific genomic regions and identification of associated proteins by engineered DNA-binding molecule-mediated chromatin immunoprecipitation (enChIP) using CRISPR. Biochem. Biophys. Res. Commun., 439, 132-136.
92. Wu, X., Scott, D.A., Kriz, A.J., Chiu, A.C., Hsu, P.D., Dadon, D.B., Cheng, A.W., Trevino, A.E., Konermann, S., Chen, S., et al. (2014) Genome-wide binding of the CRISPR endonuclease Cas9 in mammalian cells. Nat. Biotechnol., 32, 670-676.
93. Horlbeck, M.A., Witkowsky, L.B., Guglielmi, B., Replogle, J.M., Gilbert, L.A., Villalta, J.E., Torigoe, S.E., Tjian, R., and Weissman, J.S. (2016) Nucleosomes impede Cas9 access to DNA in vivo and in vitro. eLife, 5, pii: e12677.