Dynamic Chromatin Regulation from a Single Molecule Perspective

ACS Chemical Biology

Volumn 11, Issue 3, 2016, Pages 609-620

  Fierz, Beat ^a  

^a EPFL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE; CHROMATIN; PROTEIN BINDING;

CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; GENE CONTROL; IN VITRO STUDY; NUCLEOSOME; PRIORITY JOURNAL; PROMOTER REGION; REGULATORY MECHANISM; REVIEW; ANIMAL; GENETIC EPIGENESIS; HUMAN; PHYSIOLOGY; PROTEIN PROCESSING; SIGNAL TRANSDUCTION;

ANIMALS; CHROMATIN; EPIGENESIS, GENETIC; HUMANS; PROTEIN BINDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; SIGNAL TRANSDUCTION;

EID: 84961815192     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/acschembio.5b00832     Document Type: Review

References (121)

1. Smith, E. and Shilatifard, A. (2010) The Chromatin Signaling Pathway: Diverse Mechanisms of Recruitment of Histone-Modifying Enzymes and Varied Biological Outcomes Mol. Cell 40, 689-701 10.1016/j.molcel.2010.11.031
2. van Holde, K. (1989) Chromatin, Springer, New York.
3. Clapier, C. R. and Cairns, B. R. (2009) The Biology of Chromatin Remodeling Complexes Annu. Rev. Biochem. 78, 273-304 10.1146/annurev.biochem.77.062706.153223
4. Bell, O., Tiwari, V. K., Thoma, N. H., and Schubeler, D. (2011) Determinants and dynamics of genome accessibility Nat. Rev. Genet. 12, 554-564 10.1038/nrg3017
5. Moazed, D. (2011) Mechanisms for the inheritance of chromatin states Cell 146, 510-518 10.1016/j.cell.2011.07.013
6. Cedar, H. and Bergman, Y. (2012) Programming of DNA methylation patterns Annu. Rev. Biochem. 81, 97-117 10.1146/annurev-biochem-052610-091920
7. Allis, C. D., Jenuwein, T., and Reinberg, D. (2007) Epigenetics, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
8. Roy, S., Ernst, J., Kharchenko, P. V., Kheradpour, P., Negre, N., Eaton, M. L., Landolin, J. M., Bristow, C. A., Ma, L. J., Lin, M. F., Washietl, S., Arshinoff, B. I., Ay, F., Meyer, P. E., Robine, N., Washington, N. L., Di Stefano, L., Berezikov, E., Brown, C. D., Candeias, R., Carlson, J. W., Carr, A., Jungreis, I., Marbach, D., Sealfon, R., Tolstorukov, M. Y., Will, S., Alekseyenko, A. A., Artieri, C., Booth, B. W., Brooks, A. N., Dai, Q., Davis, C. A., Duff, M. O., Feng, X., Gorchakov, A. A., Gu, T. T., Henikoff, J. G., Kapranov, P., Li, R. H., MacAlpine, H. K., Malone, J., Minoda, A., Nordman, J., Okamura, K., Perry, M., Powell, S. K., Riddle, N. C., Sakai, A., Samsonova, A., Sandler, J. E., Schwartz, Y. B., Sher, N., Spokony, R., Sturgill, D., van Baren, M., Wan, K. H., Yang, L., Yu, C., Feingold, E., Good, P., Guyer, M., Lowdon, R., Ahmad, K., Andrews, J., Berger, B., Brenner, S. E., Brent, M. R., Cherbas, L., Elgin, S. C. R., Gingeras, T. R., Grossman, R., Hoskins, R. A., Kaufman, T. C., Kent, W., Kuroda, M. I., Orr-Weaver, T., Perrimon, N., Pirrotta, V., Posakony, J. W., Ren, B., Russell, S., Cherbas, P., Graveley, B. R., Lewis, S., Micklem, G., Oliver, B., Park, P. J., Celniker, S. E., Henikoff, S., Karpen, G. H., Lai, E. C., MacAlpine, D. M., Stein, L. D., White, K. P., Kellis, M., and Consortium, m. et al. 2010, Identification of Functional Elements and Regulatory Circuits by Drosophila modENCODE Science 330, 1787-1797 10.1126/science.1198374
9. Kharchenko, P. V., Alekseyenko, A. A., Schwartz, Y. B., Minoda, A., Riddle, N. C., Ernst, J., Sabo, P. J., Larschan, E., Gorchakov, A. A., Gu, T., Linder-Basso, D., Plachetka, A., Shanower, G., Tolstorukov, M. Y., Luquette, L. J., Xi, R., Jung, Y. L., Park, R. W., Bishop, E. P., Canfield, T. K., Sandstrom, R., Thurman, R. E., MacAlpine, D. M., Stamatoyannopoulos, J. A., Kellis, M., Elgin, S. C., Kuroda, M. I., Pirrotta, V., Karpen, G. H., and Park, P. J. (2011) Comprehensive analysis of the chromatin landscape in Drosophila melanogaster Nature 471, 480-485 10.1038/nature09725
10. Ernst, J., Kheradpour, P., Mikkelsen, T. S., Shoresh, N., Ward, L. D., Epstein, C. B., Zhang, X., Wang, L., Issner, R., Coyne, M., Ku, M., Durham, T., Kellis, M., and Bernstein, B. E. (2011) Mapping and analysis of chromatin state dynamics in nine human cell types Nature 473, 43-49 10.1038/nature09906
11. Steffen, P. A., Fonseca, J. P., and Ringrose, L. (2012) Epigenetics meets mathematics: towards a quantitative understanding of chromatin biology BioEssays 34, 901-913 10.1002/bies.201200076
12. Cheutin, T., McNairn, A. J., Jenuwein, T., Gilbert, D. M., Singh, P. B., and Misteli, T. (2003) Maintenance of stable heterochromatin domains by dynamic HP1 binding Science 299, 721-725 10.1126/science.1078572
13. Muller, K. P., Erdel, F., Caudron-Herger, M., Marth, C., Fodor, B. D., Richter, M., Scaranaro, M., Beaudouin, J., Wachsmuth, M., and Rippe, K. (2009) Multiscale analysis of dynamics and interactions of heterochromatin protein 1 by fluorescence fluctuation microscopy Biophys. J. 97, 2876-2885 10.1016/j.bpj.2009.08.057
14. Deal, R. B. and Henikoff, S. (2010) Capturing the dynamic epigenome Genome biology 11, 218 10.1186/gb-2010-11-10-218
15. Pick, H., Kilic, S., and Fierz, B. (2014) Engineering chromatin states: chemical and synthetic biology approaches to investigate histone modification function Biochim. Biophys. Acta, Gene Regul. Mech. 1839, 644-656 10.1016/j.bbagrm.2014.04.016
16. Kornberg, R. D. and Lorch, Y. (1991) Irresistible force meets immovable object: transcription and the nucleosome Cell 67, 833-836 10.1016/0092-8674(91)90354-2
17. Li, G. and Widom, J. (2004) Nucleosomes facilitate their own invasion Nat. Struct. Mol. Biol. 11, 763-769 10.1038/nsmb801
18. Polach, K. J. and Widom, J. (1995) Mechanism of protein access to specific DNA-sequences in chromatin-a dynamic equilibrium-model for gene-regulation J. Mol. Biol. 254, 130-149 10.1006/jmbi.1995.0606
19. Li, G., Levitus, M., Bustamante, C., and Widom, J. (2005) Rapid spontaneous accessibility of nucleosomal DNA Nat. Struct. Mol. Biol. 12, 46-53 10.1038/nsmb869
20. Koopmans, W. J., Brehm, A., Logie, C., Schmidt, T., and van Noort, J. (2007) Single-pair FRET microscopy reveals mononucleosome dynamics J. Fluoresc. 17, 785-795 10.1007/s10895-007-0218-9
21. Koopmans, W. J. A., Buning, R., Schmidt, T., and van Noort, J. (2009) spFRET Using Alternating Excitation and FCS Reveals Progressive DNA Unwrapping in Nucleosomes Biophys. J. 97, 195-204 10.1016/j.bpj.2009.04.030
22. Wei, S., Falk, S. J., Black, B. E., and Lee, T. H. (2015) A novel hybrid single molecule approach reveals spontaneous DNA motion in the nucleosome Nucleic Acids Res. 43, e111 10.1093/nar/gkv549
23. Bohm, V., Hieb, A. R., Andrews, A. J., Gansen, A., Rocker, A., Toth, K., Luger, K., and Langowski, J. (2011) Nucleosome accessibility governed by the dimer/tetramer interface Nucleic Acids Res. 39, 3093-3102 10.1093/nar/gkq1279
24. Ngo, T. T. and Ha, T. (2015) Nucleosomes undergo slow spontaneous gaping Nucleic Acids Res. 43, 3964-3971 10.1093/nar/gkv276
25. Gemmen, G. J., Sim, R., Haushalter, K. A., Ke, P. C., Kadonaga, J. T., and Smith, D. E. (2005) Forced unraveling of nucleosomes assembled on heterogeneous DNA using core histones, NAP-1, and ACF J. Mol. Biol. 351, 89-99 10.1016/j.jmb.2005.05.058
26. Cui, Y. and Bustamante, C. (2000) Pulling a single chromatin fiber reveals the forces that maintain its higher-order structure Proc. Natl. Acad. Sci. U. S. A. 97, 127-132 10.1073/pnas.97.1.127
27. Brower-Toland, B. D., Smith, C. L., Yeh, R. C., Lis, J. T., Peterson, C. L., and Wang, M. D. (2002) Mechanical disruption of individual nucleosomes reveals a reversible multistage release of DNA Proc. Natl. Acad. Sci. U. S. A. 99, 1960-1965 10.1073/pnas.022638399
28. Bennink, M. L., Leuba, S. H., Leno, G. H., Zlatanova, J., de Grooth, B. G., and Greve, J. (2001) Unfolding individual nucleosomes by stretching single chromatin fibers with optical tweezers Nat. Struct. Biol. 8, 606-610 10.1038/89646
29. Pope, L. H., Bennink, M. L., van Leijenhorst-Groener, K. A., Nikova, D., Greve, J., and Marko, J. F. (2005) Single chromatin fiber stretching reveals physically distinct populations of disassembly events Biophys. J. 88, 3572-3583 10.1529/biophysj.104.053074
30. Hall, M. A., Shundrovsky, A., Bai, L., Fulbright, R. M., Lis, J. T., and Wang, M. D. (2009) High-resolution dynamic mapping of histone-DNA interactions in a nucleosome Nat. Struct. Mol. Biol. 16, 124-129 10.1038/nsmb.1526
31. Park, Y. J., Dyer, P. N., Tremethick, D. J., and Luger, K. (2004) A new fluorescence resonance energy transfer approach demonstrates that the histone variant H2AZ. stabilizes the histone octamer within the nucleosome J. Biol. Chem. 279, 24274-24282 10.1074/jbc.M313152200
32. Chen, P., Zhao, J., Wang, Y., Wang, M., Long, H., Liang, D., Huang, L., Wen, Z., Li, W., Li, X., Feng, H., Zhao, H., Zhu, P., Li, M., Wang, Q. F., and Li, G. (2013) H3.3 actively marks enhancers and primes gene transcription via opening higher-ordered chromatin Genes Dev. 27, 2109-2124 10.1101/gad.222174.113
33. Dechassa, M. L., Wyns, K., Li, M., Hall, M. A., Wang, M. D., and Luger, K. (2011) Structure and Scm3-mediated assembly of budding yeast centromeric nucleosomes Nat. Commun. 2, 313 10.1038/ncomms1320
34. Widom, J. (2001) Role of DNA sequence in nucleosome stability and dynamics Q. Rev. Biophys. 34, 269-324 10.1017/S0033583501003699
35. Ngo, T. T., Zhang, Q., Zhou, R., Yodh, J. G., and Ha, T. (2015) Asymmetric unwrapping of nucleosomes under tension directed by DNA local flexibility Cell 160, 1135-1144 10.1016/j.cell.2015.02.001
36. Luger, K., Mader, A. W., Richmond, R. K., Sargent, D. F., and Richmond, T. J. (1997) Crystal structure of the nucleosome core particle at 2.8 A resolution Nature 389, 251-260 10.1038/38444
37. Hagerman, P. J. (1990) Sequence-directed curvature of DNA Annu. Rev. Biochem. 59, 755-781 10.1146/annurev.bi.59.070190.003543
38. Lowary, P. T. and Widom, J. (1998) New DNA sequence rules for high affinity binding to histone octamer and sequence-directed nucleosome positioning J. Mol. Biol. 276, 19-42 10.1006/jmbi.1997.1494
39. Zabel, U. and Baeuerle, P. A. (1990) Purified human I kappa B can rapidly dissociate the complex of the NF-kappa B transcription factor with its cognate DNA Cell 61, 255-265 10.1016/0092-8674(90)90806-P
40. McNally, J. G., Muller, W. G., Walker, D., Wolford, R., and Hager, G. L. (2000) The glucocorticoid receptor: rapid exchange with regulatory sites in living cells Science 287, 1262-1265 10.1126/science.287.5456.1262
41. Luo, Y., North, J. A., Rose, S. D., and Poirier, M. G. (2014) Nucleosomes accelerate transcription factor dissociation Nucleic Acids Res. 42, 3017-3027 10.1093/nar/gkt1319
42. Sing, C. E., Olvera de la Cruz, M., and Marko, J. F. (2014) Multiple-binding-site mechanism explains concentration-dependent unbinding rates of DNA-binding proteins Nucleic Acids Res. 42, 3783-3791 10.1093/nar/gkt1327
43. Graham, J., Johnson, R., and Marko, J. (2011) Concentration-dependent exchange accelerates turnover of proteins bound to double-stranded DNA Nucleic Acids Res. 39, 2249-2259 10.1093/nar/gkq1140
44. Ha, T. (2013) Single-molecule approaches embrace molecular cohorts Cell 154, 723-726 10.1016/j.cell.2013.07.012
45. Kim, S., Brostromer, E., Xing, D., Jin, J., Chong, S., Ge, H., Wang, S., Gu, C., Yang, L., Gao, Y. Q., Su, X. D., Sun, Y., and Xie, X. S. (2013) Probing allostery through DNA Science 339, 816-819 10.1126/science.1229223
46. Segal, E., Fondufe-Mittendorf, Y., Chen, L., Thastrom, A., Field, Y., Moore, I. K., Wang, J. P., and Widom, J. (2006) A genomic code for nucleosome positioning Nature 442, 772-778 10.1038/nature04979
47. Cairns, B. R. (2007) Chromatin remodeling: insights and intrigue from single-molecule studies Nat. Struct. Mol. Biol. 14, 989-996 10.1038/nsmb1333
48. Zhang, Y., Smith, C. L., Saha, A., Grill, S. W., Mihardja, S., Smith, S. B., Cairns, B. R., Peterson, C. L., and Bustamante, C. (2006) DNA translocation and loop formation mechanism of chromatin remodeling by SWI/SNF and RSC Mol. Cell 24, 559-568 10.1016/j.molcel.2006.10.025
49. Blosser, T. R., Yang, J. G., Stone, M. D., Narlikar, G. J., and Zhuang, X. (2009) Dynamics of nucleosome remodelling by individual ACF complexes Nature 462, 1022-1027 10.1038/nature08627
50. Deindl, S., Hwang, W. L., Hota, S. K., Blosser, T. R., Prasad, P., Bartholomew, B., and Zhuang, X. (2013) ISWI remodelers slide nucleosomes with coordinated multi-base-pair entry steps and single-base-pair exit steps Cell 152, 442-452 10.1016/j.cell.2012.12.040
51. Li, M., Hada, A., Sen, P., Olufemi, L., Hall, M. A., Smith, B. Y., Forth, S., McKnight, J. N., Patel, A., Bowman, G. D., Bartholomew, B., and Wang, M. D. (2015) Dynamic regulation of transcription factors by nucleosome remodeling, eLife, 4, DOI: 10.7554/eLife.06249.
52. Choy, J. S., Wei, S., Lee, J. Y., Tan, S., Chu, S., and Lee, T. H. (2010) DNA methylation increases nucleosome compaction and rigidity J. Am. Chem. Soc. 132, 1782-1783 10.1021/ja910264z
53. Taverna, S. D., Li, H., Ruthenburg, A. J., Allis, C. D., and Patel, D. J. (2007) How chromatin-binding modules interpret histone modifications: lessons from professional pocket pickers Nat. Struct. Mol. Biol. 14, 1025-1040 10.1038/nsmb1338
54. Grunstein, M. (1997) Histone acetylation in chromatin structure and transcription Nature 389, 349-352 10.1038/38664
55. Martin, C. and Zhang, Y. (2005) The diverse functions of histone lysine methylation Nat. Rev. Mol. Cell Biol. 6, 838-849 10.1038/nrm1761
56. Toth, K., Brun, N., and Langowski, J. (2006) Chromatin compaction at the mononucleosome level Biochemistry 45, 1591-1598 10.1021/bi052110u
57. Gansen, A., Toth, K., Schwarz, N., and Langowski, J. (2009) Structural variability of nucleosomes detected by single-pair Forster resonance energy transfer: histone acetylation, sequence variation, and salt effects J. Phys. Chem. B 113, 2604-2613 10.1021/jp7114737
58. Lee, J. Y., Wei, S., and Lee, T. H. (2011) Effects of histone acetylation by Piccolo NuA4 on the structure of a nucleosome and the interactions between two nucleosomes J. Biol. Chem. 286, 11099-11109 10.1074/jbc.M110.192047
59. Davey, C. A., Sargent, D. F., Luger, K., Maeder, A. W., and Richmond, T. J. (2002) Solvent mediated interactions in the structure of the nucleosome core particle at 1.9 a resolution J. Mol. Biol. 319, 1097-1113 10.1016/S0022-2836(02)00386-8
60. Xu, F., Zhang, K., and Grunstein, M. (2005) Acetylation in histone H3 globular domain regulates gene expression in yeast Cell 121, 375-385 10.1016/j.cell.2005.03.011
61. Masumoto, H., Hawke, D., Kobayashi, R., and Verreault, A. (2005) A role for cell-cycle-regulated histone H3 lysine 56 acetylation in the DNA damage response Nature 436, 294-298 10.1038/nature03714
62. Neumann, H., Hancock, S. M., Buning, R., Routh, A., Chapman, L., Somers, J., Owen-Hughes, T., van Noort, J., Rhodes, D., and Chin, J. W. (2009) A method for genetically installing site-specific acetylation in recombinant histones defines the effects of H3 K56 acetylation Mol. Cell 36, 153-163 10.1016/j.molcel.2009.07.027
63. Neumann, H., Peak-Chew, S. Y., and Chin, J. W. (2008) Genetically encoding N-epsilon-acetyllysine in recombinant proteins Nat. Chem. Biol. 4, 232-234 10.1038/nchembio.73
64. Dawson, P. E., Muir, T. W., Clark-Lewis, I., and Kent, S. B. H. (1994) Synthesis of proteins by native chemical ligation Science 266, 776-779 10.1126/science.7973629
65. Shimko, J. C., North, J. A., Bruns, A. N., Poirier, M. G., and Ottesen, J. J. (2011) Preparation of Fully Synthetic Histone H3 Reveals That Acetyl-Lysine 56 Facilitates Protein Binding Within Nucleosomes J. Mol. Biol. 408, 187-204 10.1016/j.jmb.2011.01.003
66. Simon, M., North, J. A., Shimko, J. C., Forties, R. A., Ferdinand, M. B., Manohar, M., Zhang, M., Fishel, R., Ottesen, J. J., and Poirier, M. G. (2011) Histone fold modifications control nucleosome unwrapping and disassembly Proc. Natl. Acad. Sci. U. S. A. 108, 12711-12716 10.1073/pnas.1106264108
67. North, J. A., Shimko, J. C., Javaid, S., Mooney, A. M., Shoffner, M. A., Rose, S. D., Bundschuh, R., Fishel, R., Ottesen, J. J., and Poirier, M. G. (2012) Regulation of the nucleosome unwrapping rate controls DNA accessibility Nucleic Acids Res. 40, 10215-10227 10.1093/nar/gks747
68. Brehove, M., Wang, T., North, J., Luo, Y., Dreher, S. J., Shimko, J. C., Ottesen, J. J., Luger, K., and Poirier, M. G. (2015) Histone Core Phosphorylation Regulates DNA Accessibility J. Biol. Chem. 290, 22612 10.1074/jbc.M115.661363
69. Luger, K., Dechassa, M. L., and Tremethick, D. J. (2012) New insights into nucleosome and chromatin structure: an ordered state or a disordered affair? Nat. Rev. Mol. Cell Biol. 13, 436-447 10.1038/nrm3382
70. Gall, J. G. (1966) Chromosome fibers studied by a spreading technique Chromosoma 20, 221-233 10.1007/BF00335209
71. Scheffer, M. P., Eltsov, M., and Frangakis, A. S. (2011) Evidence for short-range helical order in the 30-nm chromatin fibers of erythrocyte nuclei Proc. Natl. Acad. Sci. U. S. A. 108, 16992-16997 10.1073/pnas.1108268108
72. Efroni, S., Duttagupta, R., Cheng, J., Dehghani, H., Hoeppner, D. J., Dash, C., Bazett-Jones, D. P., Le Grice, S., McKay, R. D., Buetow, K. H., Gingeras, T. R., Misteli, T., and Meshorer, E. (2008) Global transcription in pluripotent embryonic stem cells Cell Stem Cell 2, 437-447 10.1016/j.stem.2008.03.021
73. Fussner, E., Strauss, M., Djuric, U., Li, R., Ahmed, K., Hart, M., Ellis, J., and Bazett-Jones, D. P. (2012) Open and closed domains in the mouse genome are configured as 10-nm chromatin fibres EMBO Rep. 13, 992 10.1038/embor.2012.139
74. Joti, Y., Hikima, T., Nishino, Y., Kamada, F., Hihara, S., Takata, H., Ishikawa, T., and Maeshima, K. (2012) Chromosomes without a 30-nm chromatin fiber Nucleus 3, 404-410 10.4161/nucl.21222
75. Ricci, M. A., Manzo, C., Garcia-Parajo, M. F., Lakadamyali, M., and Cosma, M. P. (2015) Chromatin fibers are formed by heterogeneous groups of nucleosomes in vivo Cell 160, 1145-1158 10.1016/j.cell.2015.01.054
76. Dorigo, B., Schalch, T., Kulangara, A., Duda, S., Schroeder, R. R., and Richmond, T. J. (2004) Nucleosome arrays reveal the two-start organization of the chromatin fiber Science 306, 1571-1573 10.1126/science.1103124
77. Schalch, T., Duda, S., Sargent, D. F., and Richmond, T. J. (2005) X-ray structure of a tetranucleosome and its implications for the chromatin fibre Nature 436, 138-141 10.1038/nature03686
78. Song, F., Chen, P., Sun, D., Wang, M., Dong, L., Liang, D., Xu, R. M., Zhu, P., and Li, G. (2014) Cryo-EM study of the chromatin fiber reveals a double helix twisted by tetranucleosomal units Science 344, 376-380 10.1126/science.1251413
79. Routh, A., Sandin, S., and Rhodes, D. (2008) Nucleosome repeat length and linker histone stoichiometry determine chromatin fiber structure Proc. Natl. Acad. Sci. U. S. A. 105, 8872-8877 10.1073/pnas.0802336105
80. Grigoryev, S. A., Arya, G., Correll, S., Woodcock, C. L., and Schlick, T. (2009) Evidence for heteromorphic chromatin fibers from analysis of nucleosome interactions Proc. Natl. Acad. Sci. U. S. A. 106, 13317-13322 10.1073/pnas.0903280106
81. Kruithof, M., Chien, F. T., Routh, A., Logie, C., Rhodes, D., and van Noort, J. (2009) Single-molecule force spectroscopy reveals a highly compliant helical folding for the 30-nm chromatin fiber Nat. Struct. Mol. Biol. 16, 534-540 10.1038/nsmb.1590
82. Poirier, M. G., Oh, E., Tims, H. S., and Widom, J. (2009) Dynamics and function of compact nucleosome arrays Nat. Struct. Mol. Biol. 16, 938-944 10.1038/nsmb.1650
83. Dorigo, B., Schalch, T., Bystricky, K., and Richmond, T. J. (2003) Chromatin fiber folding: requirement for the histone H4 N-terminal tail J. Mol. Biol. 327, 85-96 10.1016/S0022-2836(03)00025-1
84. Muir, T. W., Sondhi, D., and Cole, P. A. (1998) Expressed protein ligation: a general method for protein engineering Proc. Natl. Acad. Sci. U. S. A. 95, 6705-6710 10.1073/pnas.95.12.6705
85. Shogren-Knaak, M., Ishii, H., Sun, J. M., Pazin, M. J., Davie, J. R., and Peterson, C. L. (2006) Histone H4-K16 acetylation controls chromatin structure and protein interactions Science 311, 844-847 10.1126/science.1124000
86. Fierz, B., Chatterjee, C., McGinty, R. K., Bar-Dagan, M., Raleigh, D. P., and Muir, T. W. (2011) Histone H2B ubiquitylation disrupts local and higher-order chromatin compaction Nat. Chem. Biol. 7, 113-119 10.1038/nchembio.501
87. Dhall, A., Wei, S., Fierz, B., Woodcock, C. L., Lee, T. H., and Chatterjee, C. (2014) Sumoylated human histone H4 prevents chromatin compaction by inhibiting long-range internucleosomal interactions J. Biol. Chem. 289, 33827-33837 10.1074/jbc.M114.591644
88. Musselman, C., Lalonde, M.-E., Coîté, J., and Kutateladze, T. (2012) Perceiving the epigenetic landscape through histone readers Nat. Struct. Mol. Biol. 19, 1218-1227 10.1038/nsmb.2436
89. Garske, A. L., Oliver, S. S., Wagner, E. K., Musselman, C. A., LeRoy, G., Garcia, B. A., Kutateladze, T. G., and Denu, J. M. (2010) Combinatorial profiling of chromatin binding modules reveals multisite discrimination Nat. Chem. Biol. 6, 283-290 10.1038/nchembio.319
90. Bua, D. J., Kuo, A. J., Cheung, P., Liu, C. L., Migliori, V., Espejo, A., Casadio, F., Bassi, C., Amati, B., Bedford, M. T., Guccione, E., and Gozani, O. (2009) Epigenome Microarray Platform for Proteome-Wide Dissection of Chromatin-Signaling Networks PLoS One 4, e6789 10.1371/journal.pone.0006789
91. Kim, J., Daniel, J., Espejo, A., Lake, A., Krishna, M., Xia, L., Zhang, Y., and Bedford, M. T. (2006) Tudor, MBT and chromo domains gauge the degree of lysine methylation EMBO Rep. 7, 397-403 10.1038/sj.embor.7400625
92. Espejo, A., Cote, J., Bednarek, A., Richard, S., and Bedford, M. T. (2002) A protein-domain microarray identifies novel protein-protein interactions Biochem. J. 367, 697-702 10.1042/bj20020860
93. Stunnenberg, H. G. and Vermeulen, M. (2011) Towards cracking the epigenetic code using a combination of high-throughput epigenomics and quantitative mass spectrometry-based proteomics BioEssays 33, 547-551 10.1002/bies.201100044
94. 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 10.1016/j.cell.2007.08.016
95. 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., and Mann, M. (2010) Quantitative interaction proteomics and genome-wide profiling of epigenetic histone marks and their readers Cell 142, 967-980 10.1016/j.cell.2010.08.020
96. 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 10.1016/j.cell.2010.10.012
97. Spruijt, C., Gnerlich, F., Smits, A., Pfaffeneder, T., Jansen, P., Bauer, C., Münzel, M., Wagner, M., Müller, M., Khan, F., Eberl, H., Mensinga, A., Brinkman, A., Lephikov, K., Müller, U., Walter, J., Boelens, R., van Ingen, H., Leonhardt, H., Carell, T., and Vermeulen, M. (2013) Dynamic readers for 5-(hydroxy)methylcytosine and its oxidized derivatives Cell 152, 1146-1159 10.1016/j.cell.2013.02.004
98. Nguyen, U. T., Bittova, L., Muller, M. M., Fierz, B., David, Y., Houck-Loomis, B., Feng, V., Dann, G. P., and Muir, T. W. (2014) Accelerated chromatin biochemistry using DNA-barcoded nucleosome libraries Nat. Methods 11, 834-840 10.1038/nmeth.3022
99. Kilic, S., Bachmann, A. L., Bryan, L. C., and Fierz, B. (2015) Multivalency governs HP1alpha association dynamics with the silent chromatin state Nat. Commun. 6, 7313 10.1038/ncomms8313
100. Canzio, D., Chang, E. Y., Shankar, S., Kuchenbecker, K. M., Simon, M. D., Madhani, H. D., Narlikar, G. J., and Al-Sady, B. (2011) Chromodomain-mediated oligomerization of HP1 suggests a nucleosome-bridging mechanism for heterochromatin assembly Mol. Cell 41, 67-81 10.1016/j.molcel.2010.12.016
101. Munari, F., Soeroes, S., Zenn, H. M., Schomburg, A., Kost, N., Schroder, S., Klingberg, R., Rezaei-Ghaleh, N., Stutzer, A., Gelato, K. A., Walla, P. J., Becker, S., Schwarzer, D., Zimmermann, B., Fischle, W., and Zweckstetter, M. (2012) Methylation of lysine 9 in histone H3 directs alternative modes of highly dynamic interaction of heterochromatin protein hHP1beta with the nucleosome J. Biol. Chem. 287, 33756-33765 10.1074/jbc.M112.390849
102. 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 10.1038/nature04219
103. Ayoub, N., Jeyasekharan, A. D., Bernal, J. A., and Venkitaraman, A. R. (2008) HP1-beta mobilization promotes chromatin changes that initiate the DNA damage response Nature 453, 682-686 10.1038/nature06875
104. Fazio, T., Visnapuu, M. L., Wind, S., and Greene, E. C. (2008) DNA curtains and nanoscale curtain rods: high-throughput tools for single molecule imaging Langmuir 24, 10524-10531 10.1021/la801762h
105. Visnapuu, M. L. and Greene, E. C. (2009) Single-molecule imaging of DNA curtains reveals intrinsic energy landscapes for nucleosome deposition Nat. Struct. Mol. Biol. 16, 1056-1062 10.1038/nsmb.1655
106. Gorman, J., Plys, A. J., Visnapuu, M. L., Alani, E., and Greene, E. C. (2010) Visualizing one-dimensional diffusion of eukaryotic DNA repair factors along a chromatin lattice Nat. Struct. Mol. Biol. 17, 932-938 10.1038/nsmb.1858
107. Gorman, J., Chowdhury, A., Surtees, J. A., Shimada, J., Reichman, D. R., Alani, E., and Greene, E. C. (2007) Dynamic basis for one-dimensional DNA scanning by the mismatch repair complex Msh2-Msh6 Mol. Cell 28, 359-370 10.1016/j.molcel.2007.09.008
108. Stavreva, D. A., Muller, W. G., Hager, G. L., Smith, C. L., and McNally, J. G. (2004) Rapid glucocorticoid receptor exchange at a promoter is coupled to transcription and regulated by chaperones and proteasomes Mol. Cell. Biol. 24, 2682-2697 10.1128/MCB.24.7.2682-2697.2004
109. Poorey, K., Viswanathan, R., Carver, M. N., Karpova, T. S., Cirimotich, S. M., McNally, J. G., Bekiranov, S., and Auble, D. T. (2013) Measuring chromatin interaction dynamics on the second time scale at single-copy genes Science 342, 369-372 10.1126/science.1242369
110. Lickwar, C. R., Mueller, F., Hanlon, S. E., McNally, J. G., and Lieb, J. D. (2012) Genome-wide protein-DNA binding dynamics suggest a molecular clutch for transcription factor function Nature 484, 251-255 10.1038/nature10985
111. Elf, J., Li, G. W., and Xie, X. S. (2007) Probing transcription factor dynamics at the single-molecule level in a living cell Science 316, 1191-1194 10.1126/science.1141967
112. Abrahamsson, S., Chen, J., Hajj, B., Stallinga, S., Katsov, A. Y., Wisniewski, J., Mizuguchi, G., Soule, P., Mueller, F., Dugast Darzacq, C., Darzacq, X., Wu, C., Bargmann, C. I., Agard, D. A., Dahan, M., and Gustafsson, M. G. (2013) Fast multicolor 3D imaging using aberration-corrected multifocus microscopy Nat. Methods 10, 60-63 10.1038/nmeth.2277
113. Gebhardt, J. C., Suter, D. M., Roy, R., Zhao, Z. W., Chapman, A. R., Basu, S., Maniatis, T., and Xie, X. S. (2013) Single-molecule imaging of transcription factor binding to DNA in live mammalian cells Nat. Methods 10, 421-426 10.1038/nmeth.2411
114. Mazza, D., Abernathy, A., Golob, N., Morisaki, T., and McNally, J. G. (2012) A benchmark for chromatin binding measurements in live cells Nucleic Acids Res. 40, e119 10.1093/nar/gks701
115. Yuan, H., Corbi, N., Basilico, C., and Dailey, L. (1995) Developmental-specific activity of the FGF-4 enhancer requires the synergistic action of Sox2 and Oct-3 Genes Dev. 9, 2635-2645 10.1101/gad.9.21.2635
116. Chen, J., Zhang, Z., Li, L., Chen, B. C., Revyakin, A., Hajj, B., Legant, W., Dahan, M., Lionnet, T., Betzig, E., Tjian, R., and Liu, Z. (2014) Single-molecule dynamics of enhanceosome assembly in embryonic stem cells Cell 156, 1274-1285 10.1016/j.cell.2014.01.062
117. Vigushin, D. M., Ali, S., Pace, P. E., Mirsaidi, N., Ito, K., Adcock, I., and Coombes, R. C. (2001) Trichostatin A is a histone deacetylase inhibitor with potent antitumor activity against breast cancer in vivo Clin. Cancer Res. 7, 971-976
118. Christman, J. K. (2002) 5-Azacytidine and 5-aza-2′-deoxycytidine as inhibitors of DNA methylation: mechanistic studies and their implications for cancer therapy Oncogene 21, 5483-5495 10.1038/sj.onc.1205699
119. Hayashi-Takanaka, Y., Yamagata, K., Wakayama, T., Stasevich, T. J., Kainuma, T., Tsurimoto, T., Tachibana, M., Shinkai, Y., Kurumizaka, H., Nozaki, N., and Kimura, H. (2011) Tracking epigenetic histone modifications in single cells using Fab-based live endogenous modification labeling Nucleic Acids Res. 39, 6475-6488 10.1093/nar/gkr343
120. Stasevich, T. J., Hayashi-Takanaka, Y., Sato, Y., Maehara, K., Ohkawa, Y., Sakata-Sogawa, K., Tokunaga, M., Nagase, T., Nozaki, N., McNally, J. G., and Kimura, H. (2014) Regulation of RNA polymerase II activation by histone acetylation in single living cells Nature 516, 272-275 10.1038/nature13714
121. Los, G. V., Encell, L. P., McDougall, M. G., Hartzell, D. D., Karassina, N., Zimprich, C., Wood, M. G., Learish, R., Ohane, R. F., Urh, M., Simpson, D., Mendez, J., Zimmerman, K., Otto, P., Vidugiris, G., Zhu, J., Darzins, A., Klaubert, D. H., Bulleit, R. F., and Wood, K. V. (2008) HaloTag: A novel protein labeling technology for cell imaging and protein analysis ACS Chem. Biol. 3, 373-382 10.1021/cb800025k