Skip to main content
SpringerLink
Log in

Split decision: why it matters?

  • Review
  • Published:
Frontiers in Biology

Abstract

The establishment and faithful maintenance of epigenetic information in the context of chromatin are crucial for a great number of biologic phenomena, including position effect variegation, Polycomb silencing, X-chromosome inactivation and genomic imprinting. However, mechanisms by which that the correct histone modification patterns propagate into daughter cells during mitotic divisions remain to be elucidated. The partitioning pattern of parental histone H3–H4 tetramers is a critical question toward our understanding of the epigenetic inheritance. In this review, we discuss why the histone H3–H4 tetramer split decision matters.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Ahmad K, Henikoff S (2002). The histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly. Mol Cell, 9(6): 1191–1200

    Article  PubMed  CAS  Google Scholar 

  • Allis C D, Jenuwein T, Reinberg D (2006). Epigenetics. New York, Cold Spring Harbor, Cold Spring Harbor Laboratory Press

    Google Scholar 

  • Annunziato A T (2005). Split decision: what happens to nucleosomes during DNA replication? J Biol Chem, 280(13): 12065–12068

    Article  PubMed  CAS  Google Scholar 

  • Annunziato A T, Schindler R K, Riggs M G, Seale R L (1982). Association of newly synthesized histones with replicating and nonreplicating regions of chromatin. J Biol Chem, 257(14): 8507–8515

    PubMed  CAS  Google Scholar 

  • Baxevanis A D, Godfrey J E, Moudrianakis E N (1991). Associative behavior of the histone (H3–H4)2 tetramer: dependence on ionic environment. Biochemistry, 30(36): 8817–8823

    Article  PubMed  CAS  Google Scholar 

  • Benson L J, Gu Y, Yakovleva T, Tong K, Barrows C, Strack C L, Cook R G, Mizzen C A, Annunziato A T (2006). Modifications of H3 and H4 during chromatin replication, nucleosome assembly, and histone exchange. J Biol Chem, 281(14): 9287–9296

    Article  PubMed  CAS  Google Scholar 

  • Chuang L S, Ian H I, Koh T W, Ng H H, Xu G, Li B F (1997). Human DNA-(cytosine-5) methyltransferase-PCNA complex as a target for p21WAF1. Science, 277(5334): 1996–2000

    Article  PubMed  CAS  Google Scholar 

  • English C M, Adkins M W, Carson J J, Churchill M E, Tyler J K (2006). Structural basis for the histone chaperone activity of Asf1. Cell, 127(3): 495–508

    Article  PubMed  CAS  Google Scholar 

  • English C M, Maluf N K, Tripet B, Churchill M E, Tyler J K (2005). ASF1 binds to a heterodimer of histones H3 and H4: a two-step mechanism for the assembly of the H3–H4 heterotetramer on DNA. Biochemistry, 44(42): 13673–13682

    Article  PubMed  CAS  Google Scholar 

  • Franklin S G, Zweidler A (1977). Non-allelic variants of histones 2a, 2b and 3 in mammals. Nature, 266(5599): 273–275

    Article  PubMed  CAS  Google Scholar 

  • Groth A, Rocha W, Verreault A, Almouzni G (2007). Chromatin challenges during DNA replication and repair. Cell, 128(4): 721–733

    Article  PubMed  CAS  Google Scholar 

  • Grunstein M (1997). Histone acetylation in chromatin structure and transcription. Nature, 389(6649): 349–352

    Article  PubMed  CAS  Google Scholar 

  • Hake S B, Allis C D (2006). Histone H3 variants and their potential role in indexing mammalian genomes: the “H3 barcode hypothesis”. Proc Natl Acad Sci U S A, 103(17): 6428–6435

    Article  PubMed  CAS  Google Scholar 

  • Henikoff S (2008). Nucleosome destabilization in the epigenetic regulation of gene expression. Nat Rev Genet, 9(1): 15–26

    Article  PubMed  CAS  Google Scholar 

  • Henikoff S, Furuyama T, Ahmad K (2004). Histone variants, nucleosome assembly and epigenetic inheritance. Trends Genet, 20(7): 320–326

    Article  PubMed  CAS  Google Scholar 

  • Hermann A, Goyal R, Jeltsch A (2004). The Dnmt1 DNA-(cytosine-C5)-methyltransferase methylates DNA processively with high preference for hemimethylated target sites. J Biol Chem, 279(46): 48350–48359

    Article  PubMed  CAS  Google Scholar 

  • Isenberg I (1979). Histones. Annu Rev Biochem, 48: 159–191

    Article  PubMed  CAS  Google Scholar 

  • Jackson V (1988). Deposition of newly synthesized histones: hybrid nucleosomes are not tandemly arranged on daughter DNA strands. Biochemistry, 27(6): 2109–2120

    Article  PubMed  CAS  Google Scholar 

  • Jackson V (1990). In vivo studies on the dynamics of histone-DNA interaction: evidence for nucleosome dissolution during replication and transcription and a low level of dissolution independent of both. Biochemistry, 29(3): 719–731

    Article  PubMed  CAS  Google Scholar 

  • Jackson V, Chalkley R (1981). A new method for the isolation of replicative chromatin: selective deposition of histone on both new and old DNA. Cell, 23(1): 121–134

    Article  PubMed  CAS  Google Scholar 

  • Jaenisch R (1997). DNA methylation and imprinting: why bother? Trends Genet, 13(8): 323–329

    Article  PubMed  CAS  Google Scholar 

  • Jones P A, Takai D (2001). The role of DNA methylation in mammalian epigenetics. Science, 293(5532): 1068–1070

    Article  PubMed  CAS  Google Scholar 

  • Kimura H, Cook P R (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(7): 1341–1353

    Article  PubMed  CAS  Google Scholar 

  • Kornberg R D (1974). Chromatin structure: a repeating unit of histones and DNA. Science, 184(139): 868–871

    Article  PubMed  CAS  Google Scholar 

  • Kornberg R D, Thomas J O (1974). Chromatin structure; oligomers of the histones. Science, 184(139): 865–868

    Article  PubMed  CAS  Google Scholar 

  • Kouzarides T (2007). Chromatin modifications and their function. Cell, 128(4): 693–705

    Article  PubMed  CAS  Google Scholar 

  • Lee M G, Villa R, Trojer P, Norman J, Yan K P, Reinberg D, Di Croce L, Shiekhattar R (2007). Demethylation of H3K27 regulates polycomb recruitment and H2A ubiquitination. Science, 318(5849): 447–450

    Article  PubMed  CAS  Google Scholar 

  • Leffak IM, Grainger R, Weintraub H (1977). Conservative assembly and segregation of nucleosomal histones. Cell, 12(3): 837–845

    Article  PubMed  CAS  Google Scholar 

  • Li E, Bestor T H, Jaenisch R (1992). Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell, 69(6): 915–926

    Article  PubMed  CAS  Google Scholar 

  • Luger K, Mäder A W, Richmond R K, Sargent D F, Richmond T J (1997). Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature, 389(6648): 251–260

    Article  PubMed  CAS  Google Scholar 

  • Margueron R, Justin N, Ohno K, Sharpe M L, Son J, Drury W J 3rd, Voigt P, Martin S R, Taylor W R, De Marco V, Pirrotta V, Reinberg D, Gamblin S J (2009). Role of the polycomb protein EED in the propagation of repressive histone marks. Nature, 461(7265): 762–767

    Article  PubMed  CAS  Google Scholar 

  • Margueron R, Trojer P, Reinberg D (2005). The key to development: interpreting the histone code? Curr Opin Genet Dev, 15(2): 163–176

    Article  PubMed  CAS  Google Scholar 

  • Martin C, Zhang Y (2005). The diverse functions of histone lysine methylation. Nat Rev Mol Cell Biol, 6(11): 838–849

    Article  PubMed  CAS  Google Scholar 

  • Martin C, Zhang Y (2007). Mechanisms of epigenetic inheritance. Curr Opin Cell Biol, 19(3): 266–272

    Article  PubMed  CAS  Google Scholar 

  • Nakatani Y, Ray-Gallet D, Quivy J P, Tagami H, Almouzni G (2004). Two distinct nucleosome assembly pathways: dependent or independent of DNA synthesis promoted by histone H3.1 and H3.3 complexes. Cold Spring Harb Symp Quant Biol, 69: 273–280

    Article  PubMed  CAS  Google Scholar 

  • Nakayama J, Rice J C, Strahl B D, Allis C D, Grewal S I (2001). Role of histone H3 lysine 9 methylation in epigenetic control of heterochromatin assembly. Science, 292(5514): 110–113

    Article  PubMed  CAS  Google Scholar 

  • Natsume R, Eitoku M, Akai Y, Sano N, Horikoshi M, Senda T (2007). Structure and function of the histone chaperone CIA/ASF1 complexed with histones H3 and H4. Nature, 446(7133): 338–341

    Article  PubMed  CAS  Google Scholar 

  • Olins A L, Olins D E (1974). Spheroid chromatin units (v bodies). Science, 183(4122): 330–332

    Article  PubMed  CAS  Google Scholar 

  • Ong S E, Blagoev B, Kratchmarova I, Kristensen D B, Steen H, Pandey A, Mann M (2002). Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol Cell Proteomics, 1(5): 376–386

    Article  PubMed  CAS  Google Scholar 

  • Prior C P, Cantor C R, Johnson E M, Allfrey V G (1980). Incorporation of exogenous pyrene-labeled histone into Physarum chromatin: a system for studying changes in nucleosomes assembled in vivo. Cell, 20(3): 597–608

    Article  PubMed  CAS  Google Scholar 

  • Probst A V, Dunleavy E, Almouzni G (2009). Epigenetic inheritance during the cell cycle. Nat Rev Mol Cell Biol, 10(3): 192–206

    Article  PubMed  CAS  Google Scholar 

  • Ray-Gallet D, Almouzni G (2010). Molecular biology. Mixing or not mixing. Science, 328(5974): 56–57 PMID:20360101

    Article  PubMed  CAS  Google Scholar 

  • Riggs A D, Martiennssen R A, Russo V E A (1996). Epigenetic Mechanisms of Gene Regulation. New York: Cold Spring Harbor Laboratory Press

    Google Scholar 

  • Russev G, Hancock R (1981). Formation of hybrid nucleosomes cantaining new and old histones. Nucleic Acids Res, 9(16): 4129–4137

    Article  PubMed  CAS  Google Scholar 

  • Seale R L (1976). Studies on the mode of segregation of histone nu bodies during replication in HeLa cells. Cell, 9(3): 423–429

    Article  PubMed  CAS  Google Scholar 

  • Sharif J, Muto M, Takebayashi S, Suetake I, Iwamatsu A, Endo T A, Shinga J, Mizutani-Koseki Y, Toyoda T, Okamura K, Tajima S, Mitsuya K, Okano M, Koseki H (2007). The SRA protein Np95 mediates epigenetic inheritance by recruiting Dnmt1 to methylated DNA. Nature, 450(7171): 908–912

    Article  PubMed  CAS  Google Scholar 

  • Shi Y, Lan F, Matson C, Mulligan P, Whetstine J R, Cole P A, Casero R A, Shi Y (2004). Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell, 119(7): 941–953

    Article  PubMed  CAS  Google Scholar 

  • Tagami H, Ray-Gallet D, Almouzni G, Nakatani Y (2004). Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis. Cell, 116(1): 51–61

    Article  PubMed  CAS  Google Scholar 

  • Weintraub H, Worcel A, Alberts B (1976). A model for chromatin based upon two symmetrically paired half-nucleosomes. Cell, 9(3): 409–417

    Article  PubMed  CAS  Google Scholar 

  • Wu R S, Tsai S, Bonner W M (1982). Patterns of histone variant synthesis can distinguish G0 from G1 cells. Cell, 31(2 Pt 1): 367–374

    Article  PubMed  CAS  Google Scholar 

  • Xu M, Long C, Chen X, Huang C, Chen S, Zhu B (2010). Partitioning of histone H3–H4 tetramers during DNA replication-dependent chromatin assembly. Science, 328(5974): 94–98

    Article  PubMed  CAS  Google Scholar 

  • Yamasu K, Senshu T (1990). Conservative segregation of tetrameric units of H3 and H4 histones during nucleosome replication. J Biochem, 107(1): 15–20

    PubMed  CAS  Google Scholar 

  • Zee B M, Levin R S, Xu B, LeRoy G, Wingreen N S, Garcia B A (2010). In vivo residue-specific histone methylation dynamics. J Biol Chem, 285(5): 3341–3350

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Graduate School, Chinese Academy of Medical Sciences & Peking Union Medical College, Beijing, 100730, China

    Hui Wu

  2. National Institute of Biological Sciences, Beijing, 102206, China

    Hui Wu & Bing Zhu

Authors
  1. Hui Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bing Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Bing Zhu.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wu, H., Zhu, B. Split decision: why it matters?. Front. Biol. 6, 88–92 (2011). https://doi.org/10.1007/s11515-011-1040-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11515-011-1040-y

Keywords

Search

Navigation