Dynamics of the higher-order structure of chromatin

Abstract

Eukaryotic DNA is hierarchically packaged into chromatin to fit inside the nucleus. Dynamics of the chromatin structure plays a critical role in transcriptional regulation and other biological processes that involve DNA, such as DNA replication and DNA repair. Many factors, including histone variants, histone modification, DNA methylation and the binding of non-histone architectural proteins regulate the structure of chromatin. Although the structure of nucleosomes, the fundamental repeating unit of chromatin, is clear, there is still much discussion on the higher-order levels of chromatin structure. Identifying the structural details and dynamics of higher-order chromatin fibers is therefore very important for understanding the organization and regulation of gene activities. Here, we review studies on the dynamics of chromatin higher-order structure and its relationship with gene transcription.

Keywords

chromatin / higher-order structure / dynamics / transcriptional regulation

References

[1] Angelov, D., Verdel, A., An, W., Bondarenko, V., Hans, F., Doyen, C.M., Studitsky, V.M., Hamiche, A., Roeder, R.G., Bouvet, P., . (2004). SWI/SNF remodeling and p300-dependent transcription of histone variant H2ABbd nucleosomal arrays. EMBO J 23 , 3815–3824 .10.1038/sj.emboj.7600400
[2] Bannister, A.J., Zegerman, P., Partridge, J.F., Miska, E.A., Thomas, J.O., Allshire, R.C., and Kouzarides, T. (2001). Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 410, 120–124 .10.1038/35065138
[3] Bussiek, M., Tóth, K., Schwarz, N., and Langowski, J. (2006). Trinucleosome compaction studied by fluorescence energy transfer and scanning force microscopy. Biochemistry 45, 10838–10846 .10.1021/bi060807p
[4] Catez, F., Ueda, T., and Bustin, M. (2006). Determinants of histone H1 mobility and chromatin binding in living cells. Nat Struct Mol Biol 13, 305–310 .10.1038/nsmb1077
[5] 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
[6] Eltsov, M., Maclellan, K.M., Maeshima, K., Frangakis, A.S., and Dubochet, J. (2008). Analysis of cryo-electron microscopy images does not support the existence of 30-nm chromatin fibers in mitotic chromosomes in situ. Proc Natl Acad Sci U S A 105, 19732–19737 .10.1073/pnas.0810057105
[7] Fan, J.Y., Rangasamy, D., Luger, K., and Tremethick, D.J. (2004). H2A.Z alters the nucleosome surface to promote HP1alpha-mediated chromatin fiber folding. Mol Cell 16, 655–66 .10.1016/j.molcel.2004.10.023
[8] Francis, N.J., Kingston, R.E., and Woodcock, C.L. (2004). Chromatin compaction by a polycomb group protein complex. Science 306, 1574–1577 .10.1126/science.1100576
[9] Gansen, A., Valeri, A., Hauger, F., Felekyan, S., Kalinin, S., Tóth, K., Langowski, J., and Seidel, C.A. (2009). Nucleosome disassembly intermediates characterized by single-molecule FRET. Proc Natl Acad Sci U S A 106, 15308–15313 .10.1073/pnas.0903005106
[10] Hendzel, M.J., Lever, M.A., Crawford, E., and Th’ng, J.P. (2004). The C-terminal domain is the primary determinant of histone H1 binding to chromatin in vivo. J Biol Chem 279, 20028–20034 .10.1074/jbc.M400070200
[11] 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
[12] Li, G., Margueron, R., Hu, G., Stokes, D., Wang, Y.H., and Reinberg, D. (2010). Highly compacted chromatin formed in vitro reflects the dynamics of transcription activation in vivo. Mol Cell 38, 41–53 .10.1016/j.molcel.2010.01.042
[13] Llères, D., James, J., Swift, S., Norman, D.G., and Lamond, A.I. (2009). Quantitative analysis of chromatin compaction in living cells using FLIM-FRET. J Cell Biol 187, 481–496 .10.1083/jcb.200907029
[14] Luger, K., M?der, 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
[15] 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
[16] 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
[17] Robinson, P.J., Fairall, L., Huynh, V.A., and Rhodes, D. (2006). EM measurements define the dimensions of the “30-nm” chromatin fiber: evidence for a compact, interdigitated structure. Proc Natl Acad Sci U S A 103, 6506–6511 .10.1073/pnas.0601212103
[18] Robinson, P.J., and Rhodes, D. (2006). Structure of the ‘30 nm’ chromatin fibre: a key role for the linker histone. Curr Opin Struct Biol 16, 336–343 .10.1016/j.sbi.2006.05.007
[19] 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
[20] 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
[21] 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
[22] Strick, R., Strissel, P.L., Gavrilov, K., and Levi-Setti, R. (2001). Cation-chromatin binding as shown by ion microscopy is essential for the structural integrity of chromosomes. J Cell Biol 155, 899–910 .10.1083/jcb.200105026
[23] Thoma, F., Koller, T., and Klug, A. (1979). Involvement of histone H1 in the organization of the nucleosome and of the salt-dependent superstructures of chromatin. J Cell Biol 83, 403–427 .10.1083/jcb.83.2.403
[24] Trojer, P., Li, G., Sims, R.J. 3rd, Vaquero, A., Kalakonda, N., Boccuni, P., Lee, D., Erdjument-Bromage, H., Tempst, P., Nimer, S.D., . (2007). L3MBTL1, a histone-methylation-dependent chromatin lock. Cell 129, 915–928 .
[25] Watanabe, S., Resch, M., Lilyestrom, W., Clark, N., Hansen, J.C., Peterson, C., and Luger, K. (2010). Structural characterization of H3K56Q nucleosomes and nucleosomal arrays. Biochim Biophys Acta 1799, 480–486 .
[26] Widom, J., and Klug, A. (1985). Structure of the 300A chromatin filament: X-ray diffraction from oriented samples. Cell 43, 207–213 .
[27] Williams, S.P., Athey, B.D., Muglia, L.J., Schappe, R.S., Gough, A.H., and Langmore, J.P. (1986). Chromatin fibers are left-handed double helices with diameter and mass per unit length that depend on linker length. Biophys J 49, 233–248 .10.1016/S0006-3495(86)83637-2
[28] Woodcock, C.L., Frado, L.L., and Rattner, J.B. (1984). The higher-order structure of chromatin: evidence for a helical ribbon arrangement. J Cell Biol 99, 42–52 .10.1083/jcb.99.1.42
[29] Zlatanova, J., Caiafa, P., and Van Holde, K. (2000). Linker histone binding and displacement: versatile mechanism for transcriptional regulation. FASEB J 14, 1697–1704 .10.1096/fj.99-0869rev