Abstract
Chromatin within eukaryotic cell nuclei accommodates many complex activities that require at least partial disassembly and reassembly of nucleosomes. This disassembly/reassembly is thought to be somewhat localized when associated with processes such as site-specific DNA repair but likely occurs over extended regions during processive processes such as DNA replication or transcription. Here we review data addressing the effect of transcription elongation on nucleosome disassembly/reassembly, specifically focusing on the issue of transcription-dependent exchange of H2A/H2B dimers and H3/H4 tetramers. We suggest a model whereby passage of a polymerase through a nucleosome induces displacement of H2A/H2B dimers with a much higher probability than displacement of H3/H4 tetramers such that the extent of tetramer replacement is relatively low and proportional to polymerase density on any particular gene.
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Adkins MW, Howar SR, Tyler JK (2004) Chromatin disassembly mediated by the histone chaperone Asf1 is essential for transcriptional activation of the yeast PHO5 and PHO8 genes. Mol Cell 14:657–666
Ahmad K, Henikoff S (2002) The histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly. Mol Cell 9:1191–1200
Alilat M, Sivolob A, Revet B, Prunell A (1999) Nucleosome dynamics. Protein and DNA contributions in the chiral transition of the tetrasome, the histone (H3-H4)2 tetramer-DNA particle. J Mol Biol 291:815–841
Allfrey VG, Faulkner R, Mirsky AE (1964) Acetylation and Methylation of Histones and Their Possible Role in the Regulation of Rna Synthesis. Proc Natl Acad Sci USA 51:786–794
Annunziato AA, Frado L-LY, Seale RL, Woodcock CLF (1988) Treatment with sodium butyrate inhibits the complete condensation of interphase chromatin. Chromosoma 96:132–138
Belotserkovskaya R, Oh S, Bondarenko VA, Orphanides G, Studitsky VM, Reinberg D (2003) FACT facilitates transcription-dependent nucleosome alteration. Science 301:1090–1093
Boeger H, Griesenbeck J, Strattan JS, Kornberg RD (2003) Nucleosomes unfold completely at a transcriptionally active promoter. Mol Cell 11:1587–1598
Boyer LA, Logie C, Bonte E, Becker PB, Wade PA, Wolffe AP, Wu C, Imbalzano AN, Peterson CL (2000) Functional delineation of three groups of the ATP-dependent family of chromatin remodeling enzymes. J Biol Chem 275:18864–18870
Brownell JE, Zhou J, Ranalli T, Kobayashi R, Edmondson DG, Roth SY, Allis CD (1996) Tetrahymena histone acetyltransferase A: a homolog to yeast Gcn5p linking histone acetylation to gene activation. Cell 84:843–851
Chang CH, Luse DS (1997) The H3/H4 tetramer blocks transcript elongation by RNA polymerase II in vitro. J Biol Chem 272:23427–23434
Clark DJ, Felsenfeld G (1992) A nucleosome core is transferred out of the path of a transcribing polymerase. Cell 71:11–22
Cosma MP (2002) Ordered recruitment: gene-specific mechanism of transcription activation. Mol Cell 10:227–236
de la Cruz X, Lois S, Sanchez-Molina S, Martinez-Balbas M (2005) Do protein motifs read the histone code? Bioessays 27:164–175
Felsenfeld G, Clark D, Studitsky V (2000) Transcription through nucleosomes. Biophys Chem 86:231–237
Giaever GN, Wang JC (1988) Supercoiling of intracellular DNA can occur in eukaryotic cells. Cell 55:849–856
Grunstein M (1997) Histone acetylation in chromatin structure and transcription. Nature 389:349–352
Hake SB, Garcia BA, Duncan EM, Kauer M, Dellaire G, Shabanowitz J, Bazett-Jones DP, Allis CD, Hunt DF (2005) Expression patterns and post-translational modifications associated with mammalian histone H3 variants. J Biol Chem
Hansen JC (2002) Conformational Dynamics of the Chromatin Fiber in Solution: Determinants, Mechanisms, and Functions. Annu Rev Biophys Biomol Struct 31:361–392
Hendzel MJ, Davie JR (1990) Nucleosomal histones of transcriptionally active/competent chromatin preferentially exchange with newly synthesized histones in quiescent chicken erythrocytes. Biochem J 271:67–73
Huang RC, Bonner J (1962) Histone, a suppressor of chromosomal RNA synthesis. Proc Natl Acad Sci USA 48:1216–1222
Izban MG, Luse DS (1991) Transcription on nucleosomal templates by RNA polymerase II in vitro: inhibition of elongation with enhancement of sequence-specific pausing. Genes Dev 5:683–696
Jackson V, Chalkley R (1985) Histone synthesis and deposition in the G1 and S phases of hepatoma tissue culture cells. Biochemistry 24:6921–6930
Jackson V, Marshall S, Chalkley R (1981) The sites of deposition of newly synthesized histone. Nucleic Acids Res 9:4563–4581
Janicki SM, Tsukamoto T, Salghetti SE, Tansey WP, Sachidanandam R, Prasanth KV, Ried T, Shav-Tal Y, Bertrand E, Singer RH, Spector DL (2004) From silencing to gene expression: real-time analysis in single cells. Cell 116:683–698
Kimura H, Cook PR (2001) Kinetics of core histones in living human cells: little exchange of H3 and H4 and some rapid exchange of H2B. J Cell Biol 153:1341–1353
Kireeva ML, Hancock B, Cremona GH, Walter W, Studitsky VM, Kashlev M (2005) Nature of the nucleosomal barrier to RNA polymerase II. Mol Cell 18:97–108
Kireeva ML, Walter W, Tchernajenko V, Bondarenko V, Kashlev M, Studitsky VM (2002) Nucleosome remodeling induced by RNA polymerase II: loss of the H2A/H2B dimer during transcription. Mol Cell 9:541–552
Knezetic JA, Luse DS (1986) The Presence of Nucleosomes on a DNA Template Prevents Initiation by RNA Polymerase II In vitro. Cell 45:95–104
Lee CK, Shibata Y, Rao B, Strahl BD, Lieb JD (2004) Evidence for nucleosome depletion at active regulatory regions genome-wide. Nat Genet 36:900–905
Levchenko V, Jackson B, Jackson V (2005) Histone release during transcription: displacement of the two H2A-H2B dimers in the nucleosome is dependent on different levels of transcription-induced positive stress. Biochemistry 44:5357–5372
Louters L, Chalkley R (1985) Exchange of histones H1, H2A, and H2B in vivo. Biochemistry 24:3080–3085
McKittrick E, Gafken PR, Ahmad K, Henikoff S (2004) Histone H3.3 is enriched in covalent modifications associated with active chromatin. Proc Natl Acad Sci USA 101:1525–1530
Mito Y, Henikoff JG, Henikoff S (2005) Genome-scale profiling of histone H3.3 replacement patterns. Nat Genet 37:1090–1097
Orphanides G, LeRoy G, Chang CH, Luse DS, Reinberg D (1998) FACT, a factor that facilitates transcript elongation through nucleosomes. Cell 92:105–116
Perry CA, Dadd CA, Allis CD, Annunziato AT (1993) Analysis of nucleosome assembly and histone exchange using antibodies specific for acetylated H4. Biochemistry 32:13605–13614
Peterson CL (2000) ATP-dependent chromatin remodeling: going mobile. FEBS Lett 476:68–72
Peterson CL, Laniel MA (2004) Histones and histone modifications. Curr Biol 14:R546–R551
Reinke H, Horz W (2003) Histones are first hyperacetylated and then lose contact with the activated PHO5 promoter. Mol Cell 11:1599–1607
Sathyanarayana UG, Freeman LA, Lee MS, Garrard WT (1999) RNA polymerase-specific nucleosome disruption by transcription in vivo. J Biol Chem 274:16431–16436
Saunders A, Werner J, Andrulis ED, Nakayama T, Hirose S, Reinberg D, Lis JT (2003) Tracking FACT and the RNA polymerase II elongation complex through chromatin in vivo. Science 301:1094–1096
Schwabish MA, Struhl K (2004) Evidence for eviction and rapid deposition of histones upon transcriptional elongation by RNA polymerase II. Mol Cell Biol 24:10111–10117
Silverman B, Mirsky AE (1973) Accessibility of DNA in chromatin to DNA polymerase and RNA polymerase. Proc Natl Acad Sci USA 70:1326–1330
Strahl BD, Allis CD (2000) The language of covalent histone modifications. Nature 403:41–45
Studitsky VM, Clark DJ, Felsenfeld G (1994) A histone octamer can step around a transcribing polymerase without leaving the template. Cell 76:371–382
Studitsky VM, Clark DJ, Felsenfeld G (1995) Overcoming a nucleosomal barrier to transcription. Cell 83:19–27
Studitsky VM, Kassavetis GA, Geiduschek EP, Felsenfeld G (1997) Mechanism of transcription through the nucleosome by eukaryotic RNA polymerase. Science 278:1960–1963
Studitsky VM, Walter W, Kireeva M, Kashlev M, Felsenfeld G (2004) Chromatin remodeling by RNA polymerases. Trends Biochem Sci 29:127–135
Thatcher TH, MacGaffey J, Bowen J, Horowitz S, Shapiro DL, Gorovsky MA (1994) Independent evolutionary origin of histone H3.3-like variants of animals and Tetrahymena. Nucleic Acids Res 22:180–186
Thiriet C, Hayes JJ (2005) Replication-independent core histone dynamics at transcriptionally active loci in vivo. Genes Dev 19:677–682
Tsao YP, Wu HY, Liu LF (1989) Transcription-driven supercoiling of DNA: direct biochemical evidence from in vitro studies. Cell 56:111–118
Wirbelauer C, Bell O, Schubeler D (2005) Variant histone H3.3 is deposited at sites of nucleosomal displacement throughout transcribed genes while active histone modifications show a promoter-proximal bias. Genes Dev 19:1761–1766
Wolffe AP, Kurumizaka H (1998) The nucleosome: a powerful regulator of transcription. Prog Nucleic Acid Res Mol Biol 61:379–422
Woodcock CL, Dimitrov S (2001) Higher-order structure of chromatin and chromosomes. Curr Opin Genet Dev 11:130–135
Wu C (1980) The 5′ends of Drosophila heat shock genes in chromatin are hypersensitive to DNase I. Nature 286:854–860
Wu C, Wong YC, Elgin SC (1979) The chromatin structure of specific genes: II. Disruption of chromatin structure during gene activity. Cell 16:807–814
Yu L, Gorovsky MA (1997) Constitutive expression, not a particular primary sequence, is the important feature of the H3 replacement variant hv2 in Tetrahymena thermophila. Mol Cell Biol 17:6303–6310
Zhang Y, Reinberg D (2001) Transcription regulation by histone methylation: interplay between different covalent modifications of the core histone tails. Genes Dev. 15:2343–2360
Zheng C, Hayes JJ (2003) Structures and interactions of the core histone tail domains. Biopolymers 68:539–546
Acknowledgments
This work was supported by NIH grant GM52426 and NSF grant MCB-0317935. We thank Drs. Anthony Annunziato and Vasily Studitsky for a critical reading of the manuscript.
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Thiriet, C., Hayes, J.J. Histone Dynamics During Transcription: Exchange of H2A/H2B Dimers and H3/H4 Tetramers During Pol II Elongation. In: Laurent, B.C. (eds) Chromatin Dynamics in Cellular Function. Results and Problems in Cell Differentiation, vol 41. Springer, Berlin, Heidelberg. https://doi.org/10.1007/400_009
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DOI: https://doi.org/10.1007/400_009
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