Skip to main content

Histone Dynamics During Transcription: Exchange of H2A/H2B Dimers and H3/H4 Tetramers During Pol II Elongation

  • Chapter
  • First Online:

Part of the book series: Results and Problems in Cell Differentiation ((RESULTS,volume 41))

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.

This is a preview of subscription content, log in via an institution.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 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

    Article  CAS  PubMed  Google Scholar 

  2. Ahmad K, Henikoff S (2002) The histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly. Mol Cell 9:1191–1200

    Article  CAS  PubMed  Google Scholar 

  3. 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

    Article  CAS  PubMed  Google Scholar 

  4. 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

    Article  CAS  PubMed  Google Scholar 

  5. 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

    Article  CAS  PubMed  Google Scholar 

  6. Belotserkovskaya R, Oh S, Bondarenko VA, Orphanides G, Studitsky VM, Reinberg D (2003) FACT facilitates transcription-dependent nucleosome alteration. Science 301:1090–1093

    Article  CAS  PubMed  Google Scholar 

  7. Boeger H, Griesenbeck J, Strattan JS, Kornberg RD (2003) Nucleosomes unfold completely at a transcriptionally active promoter. Mol Cell 11:1587–1598

    Article  CAS  PubMed  Google Scholar 

  8. 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

    Article  CAS  PubMed  Google Scholar 

  9. 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

    Article  CAS  PubMed  Google Scholar 

  10. Chang CH, Luse DS (1997) The H3/H4 tetramer blocks transcript elongation by RNA polymerase II in vitro. J Biol Chem 272:23427–23434

    Article  CAS  PubMed  Google Scholar 

  11. Clark DJ, Felsenfeld G (1992) A nucleosome core is transferred out of the path of a transcribing polymerase. Cell 71:11–22

    Article  CAS  PubMed  Google Scholar 

  12. Cosma MP (2002) Ordered recruitment: gene-specific mechanism of transcription activation. Mol Cell 10:227–236

    Article  CAS  PubMed  Google Scholar 

  13. de la Cruz X, Lois S, Sanchez-Molina S, Martinez-Balbas M (2005) Do protein motifs read the histone code? Bioessays 27:164–175

    Article  PubMed  CAS  Google Scholar 

  14. Felsenfeld G, Clark D, Studitsky V (2000) Transcription through nucleosomes. Biophys Chem 86:231–237

    Article  CAS  PubMed  Google Scholar 

  15. Giaever GN, Wang JC (1988) Supercoiling of intracellular DNA can occur in eukaryotic cells. Cell 55:849–856

    Article  CAS  PubMed  Google Scholar 

  16. Grunstein M (1997) Histone acetylation in chromatin structure and transcription. Nature 389:349–352

    Article  CAS  PubMed  Google Scholar 

  17. 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

    Google Scholar 

  18. Hansen JC (2002) Conformational Dynamics of the Chromatin Fiber in Solution: Determinants, Mechanisms, and Functions. Annu Rev Biophys Biomol Struct 31:361–392

    Article  CAS  PubMed  Google Scholar 

  19. 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

    CAS  PubMed  Google Scholar 

  20. Huang RC, Bonner J (1962) Histone, a suppressor of chromosomal RNA synthesis. Proc Natl Acad Sci USA 48:1216–1222

    Article  CAS  PubMed  Google Scholar 

  21. 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

    Article  CAS  PubMed  Google Scholar 

  22. Jackson V, Chalkley R (1985) Histone synthesis and deposition in the G1 and S phases of hepatoma tissue culture cells. Biochemistry 24:6921–6930

    Article  CAS  PubMed  Google Scholar 

  23. Jackson V, Marshall S, Chalkley R (1981) The sites of deposition of newly synthesized histone. Nucleic Acids Res 9:4563–4581

    Article  CAS  PubMed  Google Scholar 

  24. 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

    Article  CAS  PubMed  Google Scholar 

  25. 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

    Article  CAS  PubMed  Google Scholar 

  26. 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

    Article  CAS  PubMed  Google Scholar 

  27. 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

    Article  CAS  PubMed  Google Scholar 

  28. 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

    Article  CAS  PubMed  Google Scholar 

  29. 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

    Article  CAS  PubMed  Google Scholar 

  30. 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

    Article  CAS  PubMed  Google Scholar 

  31. Louters L, Chalkley R (1985) Exchange of histones H1, H2A, and H2B in vivo. Biochemistry 24:3080–3085

    Article  CAS  PubMed  Google Scholar 

  32. 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

    Article  CAS  PubMed  Google Scholar 

  33. Mito Y, Henikoff JG, Henikoff S (2005) Genome-scale profiling of histone H3.3 replacement patterns. Nat Genet 37:1090–1097

    Article  CAS  PubMed  Google Scholar 

  34. Orphanides G, LeRoy G, Chang CH, Luse DS, Reinberg D (1998) FACT, a factor that facilitates transcript elongation through nucleosomes. Cell 92:105–116

    Article  CAS  PubMed  Google Scholar 

  35. 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

    Article  CAS  PubMed  Google Scholar 

  36. Peterson CL (2000) ATP-dependent chromatin remodeling: going mobile. FEBS Lett 476:68–72

    Article  CAS  PubMed  Google Scholar 

  37. Peterson CL, Laniel MA (2004) Histones and histone modifications. Curr Biol 14:R546–R551

    Article  CAS  PubMed  Google Scholar 

  38. Reinke H, Horz W (2003) Histones are first hyperacetylated and then lose contact with the activated PHO5 promoter. Mol Cell 11:1599–1607

    Article  CAS  PubMed  Google Scholar 

  39. Sathyanarayana UG, Freeman LA, Lee MS, Garrard WT (1999) RNA polymerase-specific nucleosome disruption by transcription in vivo. J Biol Chem 274:16431–16436

    Article  CAS  PubMed  Google Scholar 

  40. 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

    Article  CAS  PubMed  Google Scholar 

  41. 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

    Article  CAS  PubMed  Google Scholar 

  42. Silverman B, Mirsky AE (1973) Accessibility of DNA in chromatin to DNA polymerase and RNA polymerase. Proc Natl Acad Sci USA 70:1326–1330

    Article  CAS  PubMed  Google Scholar 

  43. Strahl BD, Allis CD (2000) The language of covalent histone modifications. Nature 403:41–45

    Article  CAS  PubMed  Google Scholar 

  44. Studitsky VM, Clark DJ, Felsenfeld G (1994) A histone octamer can step around a transcribing polymerase without leaving the template. Cell 76:371–382

    Article  CAS  PubMed  Google Scholar 

  45. Studitsky VM, Clark DJ, Felsenfeld G (1995) Overcoming a nucleosomal barrier to transcription. Cell 83:19–27

    Article  CAS  PubMed  Google Scholar 

  46. Studitsky VM, Kassavetis GA, Geiduschek EP, Felsenfeld G (1997) Mechanism of transcription through the nucleosome by eukaryotic RNA polymerase. Science 278:1960–1963

    Article  CAS  PubMed  Google Scholar 

  47. Studitsky VM, Walter W, Kireeva M, Kashlev M, Felsenfeld G (2004) Chromatin remodeling by RNA polymerases. Trends Biochem Sci 29:127–135

    Article  CAS  PubMed  Google Scholar 

  48. 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

    Article  CAS  PubMed  Google Scholar 

  49. Thiriet C, Hayes JJ (2005) Replication-independent core histone dynamics at transcriptionally active loci in vivo. Genes Dev 19:677–682

    Article  CAS  PubMed  Google Scholar 

  50. Tsao YP, Wu HY, Liu LF (1989) Transcription-driven supercoiling of DNA: direct biochemical evidence from in vitro studies. Cell 56:111–118

    Article  CAS  PubMed  Google Scholar 

  51. 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

    Article  CAS  PubMed  Google Scholar 

  52. Wolffe AP, Kurumizaka H (1998) The nucleosome: a powerful regulator of transcription. Prog Nucleic Acid Res Mol Biol 61:379–422

    Article  CAS  Google Scholar 

  53. Woodcock CL, Dimitrov S (2001) Higher-order structure of chromatin and chromosomes. Curr Opin Genet Dev 11:130–135

    Article  CAS  PubMed  Google Scholar 

  54. Wu C (1980) The 5′ends of Drosophila heat shock genes in chromatin are hypersensitive to DNase I. Nature 286:854–860

    Article  CAS  PubMed  Google Scholar 

  55. 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

    Article  CAS  PubMed  Google Scholar 

  56. 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

    CAS  PubMed  Google Scholar 

  57. 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

    Article  CAS  PubMed  Google Scholar 

  58. Zheng C, Hayes JJ (2003) Structures and interactions of the core histone tail domains. Biopolymers 68:539–546

    Article  CAS  PubMed  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jeffrey J. Hayes .

Editor information

Brehon C. Laurent

Rights and permissions

Reprints and permissions

About this chapter

Cite this chapter

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

Download citation

Publish with us

Policies and ethics