Skip to main content
SpringerLink
Log in

Propagation of histone marks and epigenetic memory during normal and interrupted DNA replication

  • Review
  • Published:
Cellular and Molecular Life Sciences Aims and scope Submit manuscript

Abstract

Although all nucleated cells within a multicellular organism contain a complete copy of the genome, cell identity relies on the expression of a specific subset of genes. Therefore, when cells divide they must not only copy their genome to their daughters, but also ensure that the pattern of gene expression present before division is restored. While the carrier of this epigenetic memory has been a topic of much research and debate, post-translational modifications of histone proteins have emerged in the vanguard of candidates. In this paper we examine the mechanisms by which histone post-translational modifications are propagated through DNA replication and cell division, and we critically examine the evidence that they can also act as vectors of epigenetic memory. Finally, we consider ways in which epigenetic memory might be disrupted by interfering with the mechanisms of DNA replication.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Luger K, Mader AW, Richmond RK, Sargent DF, Richmond TJ (1997) Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389(6648):251–260

    Article  PubMed  CAS  Google Scholar 

  2. Happel N, Doenecke D (2009) Histone H1 and its isoforms: contribution to chromatin structure and function. Gene 431(1–2):1–12

    Article  PubMed  CAS  Google Scholar 

  3. Bassett A, Cooper S, Wu C, Travers A (2009) The folding and unfolding of eukaryotic chromatin. Curr Opin Genet Dev 19(2):159–165

    Article  PubMed  CAS  Google Scholar 

  4. Holliday R (1987) The inheritance of epigenetic defects. Science 238(4824):163–170

    Article  PubMed  CAS  Google Scholar 

  5. Grewal SI, Elgin SC (2007) Transcription and RNA interference in the formation of heterochromatin. Nature 447(7143):399–406

    Article  PubMed  CAS  Google Scholar 

  6. Bird A (2002) DNA methylation patterns and epigenetic memory. Genes Dev 16(1):6–21

    Article  PubMed  CAS  Google Scholar 

  7. Turner BM (2005) Reading signals on the nucleosome with a new nomenclature for modified histones. Nat Struct Mol Biol 12(2):110–112

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  9. Turner BM (1993) Decoding the nucleosome. Cell 75(1):5–8

    PubMed  CAS  Google Scholar 

  10. Strahl BD, Allis CD (2000) The language of covalent histone modifications. Nature 403(6765):41–45

    Article  PubMed  CAS  Google Scholar 

  11. Turner BM (2007) Defining an epigenetic code. Nat Cell Biol 9(1):2–6

    Article  PubMed  CAS  Google Scholar 

  12. Ringrose L, Paro R (2004) Epigenetic regulation of cellular memory by the Polycomb and Trithorax group proteins. Annu Rev Genet 38:413–443

    Article  PubMed  CAS  Google Scholar 

  13. Lewis EB (1978) A gene complex controlling segmentation in Drosophila. Nature 276(5688):565–570

    Article  PubMed  CAS  Google Scholar 

  14. Ingham PW (1985) A clonal analysis of the requirement for the trithorax gene in the diversification of segments in Drosophila. J Embryol Exp Morphol 89:349–365

    PubMed  CAS  Google Scholar 

  15. Cao R, Wang L, Wang H, Xia L, Erdjument-Bromage H, Tempst P, Jones RS, Zhang Y (2002) Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science 298(5595):1039–1043

    Article  PubMed  CAS  Google Scholar 

  16. Czermin B, Melfi R, McCabe D, Seitz V, Imhof A, Pirrotta V (2002) Drosophila enhancer of Zeste/ESC complexes have a histone H3 methyltransferase activity that marks chromosomal Polycomb sites. Cell 111(2):185–196

    Article  PubMed  CAS  Google Scholar 

  17. Muller J, Hart CM, Francis NJ, Vargas ML, Sengupta A, Wild B, Miller EL, O’Connor MB, Kingston RE, Simon JA (2002) Histone methyltransferase activity of a Drosophila Polycomb group repressor complex. Cell 111(2):197–208

    Article  PubMed  CAS  Google Scholar 

  18. Kuzmichev A, Nishioka K, Erdjument-Bromage H, Tempst P, Reinberg D (2002) Histone methyltransferase activity associated with a human multiprotein complex containing the Enhancer of Zeste protein. Genes Dev 16(22):2893–2905

    Article  PubMed  CAS  Google Scholar 

  19. Beisel C, Imhof A, Greene J, Kremmer E, Sauer F (2002) Histone methylation by the Drosophila epigenetic transcriptional regulator Ash1. Nature 419(6909):857–862

    Article  PubMed  CAS  Google Scholar 

  20. Byrd KN, Shearn A (2003) ASH1, a Drosophila trithorax group protein, is required for methylation of lysine 4 residues on histone H3. Proc Natl Acad Sci USA 100(20):11535–11540

    Article  PubMed  CAS  Google Scholar 

  21. Hansen K, Bracken A, Pasini D, Dietrich N, Gehani S, Monrad A, Rappsilber J, Lerdrup M, Helin K (2008) A model for transmission of the H3K27me3 epigenetic mark. Nat Cell Biol 10(11):1291–1300

    Article  PubMed  CAS  Google Scholar 

  22. Müller HJ (1930) Types of visible variations induced by X-rays in Drosophila. J Genetics 22:299–334

    Article  Google Scholar 

  23. Schultz J (1936) Variegation in Drosophila and the inert chromosome regions. Proc Natl Acad Sci USA 22(1):27–33

    Article  PubMed  CAS  Google Scholar 

  24. Fodor BD, Shukeir N, Reuter G, Jenuwein T (2010) Mammalian Su(var) genes in chromatin control. Annu Rev Cell Dev Biol 26:471–501

    Article  PubMed  CAS  Google Scholar 

  25. Bannister AJ, Zegerman P, Partridge JF, Miska EA, Thomas JO, Allshire RC, Kouzarides T (2001) Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 410(6824):120–124

    Article  PubMed  CAS  Google Scholar 

  26. Lachner M, O’Carroll D, Rea S, Mechtler K, Jenuwein T (2001) Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410(6824):116–120

    Article  PubMed  CAS  Google Scholar 

  27. Nakayama J, Rice JC, Strahl BD, Allis CD, Grewal SI (2001) Role of histone H3 lysine 9 methylation in epigenetic control of heterochromatin assembly. Science 292(5514):110–113

    Article  PubMed  CAS  Google Scholar 

  28. Haber JE (1998) Mating-type gene switching in Saccharomyces cerevisiae. Annu Rev Genet 32:561–599

    Article  PubMed  CAS  Google Scholar 

  29. Klar AJ (2007) Lessons learned from studies of fission yeast mating-type switching and silencing. Annu Rev Genet 41:213–236

    Article  PubMed  CAS  Google Scholar 

  30. Pillus L, Rine J (1989) Epigenetic inheritance of transcriptional states in S. cerevisiae. Cell 59(4):637–647

    Article  PubMed  CAS  Google Scholar 

  31. Grewal SI, Klar AJ (1996) Chromosomal inheritance of epigenetic states in fission yeast during mitosis and meiosis. Cell 86(1):95–101

    Article  PubMed  CAS  Google Scholar 

  32. Thon G, Friis T (1997) Epigenetic inheritance of transcriptional silencing and switching competence in fission yeast. Genetics 145(3):685–696

    PubMed  CAS  Google Scholar 

  33. Thon G, Cohen A, Klar AJ (1994) Three additional linkage groups that repress transcription and meiotic recombination in the mating-type region of Schizosaccharomyces pombe. Genetics 138(1):29–38

    PubMed  CAS  Google Scholar 

  34. Ekwall K, Ruusala T (1994) Mutations in rik1, clr2, clr3 and clr4 genes asymmetrically derepress the silent mating-type loci in fission yeast. Genetics 136(1):53–64

    PubMed  CAS  Google Scholar 

  35. Lorentz A, Heim L, Schmidt H (1992) The switching gene swi6 affects recombination and gene expression in the mating-type region of Schizosaccharomyces pombe. Mol Gen Genet 233(3):436–442

    Article  PubMed  CAS  Google Scholar 

  36. Furuyama T, Banerjee R, Breen TR, Harte PJ (2004) SIR2 is required for polycomb silencing and is associated with an E(Z) histone methyltransferase complex. Curr Biol 14(20):1812–1821

    Article  PubMed  CAS  Google Scholar 

  37. Dodd IB, Micheelsen MA, Sneppen K, Thon G (2007) Theoretical analysis of epigenetic cell memory by nucleosome modification. Cell 129(4):813–822

    Article  PubMed  CAS  Google Scholar 

  38. Muramoto T, Muller I, Thomas G, Melvin A, Chubb JR (2010) Methylation of H3K4 Is required for inheritance of active transcriptional states. Curr Biol 20(5):397–406

    Article  PubMed  CAS  Google Scholar 

  39. Ye X, Franco A, Santos H, Nelson D, Kaufman P, Adams P (2003) Defective S phase chromatin assembly causes DNA damage, activation of the S phase checkpoint, and S phase arrest. Mol Cell 11(2):341–351

    Article  PubMed  CAS  Google Scholar 

  40. Loyola A, Bonaldi T, Roche D, Imhof A, Almouzni G (2006) PTMs on H3 variants before chromatin assembly potentiate their final epigenetic state. Mol Cell 24(2):309–316

    Article  PubMed  CAS  Google Scholar 

  41. Campos EI, Fillingham J, Li G, Zheng H, Voigt P, Kuo WH, Seepany H, Gao Z, Day LA, Greenblatt JF, Reinberg D (2010) The program for processing newly synthesized histones H3.1 and H4. Nat Struct Mol Biol 17(11):1343–1351

    Article  PubMed  CAS  Google Scholar 

  42. Chicoine LG, Schulman IG, Richman R, Cook RG, Allis CD (1986) Nonrandom utilization of acetylation sites in histones isolated from Tetrahymena. Evidence for functionally distinct H4 acetylation sites. J Biol Chem 261(3):1071–1076

    PubMed  CAS  Google Scholar 

  43. Sobel RE, Cook RG, Perry CA, Annunziato AT, Allis CD (1995) Conservation of deposition-related acetylation sites in newly synthesized histones H3 and H4. Proc Natl Acad Sci USA 92(4):1237–1241

    Article  PubMed  CAS  Google Scholar 

  44. Masumoto H, Hawke D, Kobayashi R, Verreault A (2005) A role for cell-cycle-regulated histone H3 lysine 56 acetylation in the DNA damage response. Nature 436(7048):294–298

    Article  PubMed  CAS  Google Scholar 

  45. Driscoll R, Hudson A, Jackson SP (2007) Yeast Rtt109 promotes genome stability by acetylating histone H3 on lysine 56. Science 315(5812):649–652

    Article  PubMed  CAS  Google Scholar 

  46. Schneider J, Bajwa P, Johnson FC, Bhaumik SR, Shilatifard A (2006) Rtt109 is required for proper H3K56 acetylation: a chromatin mark associated with the elongating RNA polymerase II. J Biol Chem 281(49):37270–37274

    Article  PubMed  CAS  Google Scholar 

  47. Li Q, Zhou H, Wurtele H, Davies B, Horazdovsky B, Verreault A, Zhang Z (2008) Acetylation of histone H3 lysine 56 regulates replication-coupled nucleosome assembly. Cell 134(2):244–255

    Article  PubMed  CAS  Google Scholar 

  48. Jasencakova Z, Scharf AN, Ask K, Corpet A, Imhof A, Almouzni G, Groth A (2010) Replication stress interferes with histone recycling and predeposition marking of new histones. Mol Cell 37(5):736–743

    Article  PubMed  CAS  Google Scholar 

  49. Sogo JM, Ness PJ, Widmer RM, Parish RW, Koller T (1984) Psoralen-crosslinking of DNA as a probe for the structure of active nucleolar chromatin. J Mol Biol 178(4):897–919

    Article  PubMed  CAS  Google Scholar 

  50. Sogo JM, Stahl H, Koller T, Knippers R (1986) Structure of replicating simian virus 40 minichromosomes. The replication fork, core histone segregation and terminal structures. J Mol Biol 189(1):189–204

    Article  PubMed  CAS  Google Scholar 

  51. Jackson V, Chalkley R (1985) Histone segregation on replicating chromatin. Biochemistry 24(24):6930–6938

    Article  PubMed  CAS  Google Scholar 

  52. 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 

  53. Vestner B, Waldmann T, Gruss C (2000) Histone octamer dissociation is not required for in vitro replication of simian virus 40 minichromosomes. J Biol Chem 275(11):8190–8195

    Article  PubMed  CAS  Google Scholar 

  54. Annunziato AT, Schindler RK, Riggs MG, Seale RL (1982) Association of newly synthesized histones with replicating and nonreplicating regions of chromatin. J Biol Chem 257(14):8507–8515

    PubMed  CAS  Google Scholar 

  55. 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 

  56. Park YJ, Luger K (2008) Histone chaperones in nucleosome eviction and histone exchange. Curr Opin Struct Biol 18(3):282–289

    Article  PubMed  CAS  Google Scholar 

  57. Smith S, Stillman B (1989) Purification and characterization of CAF-I, a human cell factor required for chromatin assembly during DNA replication in vitro. Cell 58(1):15–25

    Article  PubMed  CAS  Google Scholar 

  58. Stillman B (1986) Chromatin assembly during SV40 DNA replication in vitro. Cell 45(4):555–565

    Article  PubMed  CAS  Google Scholar 

  59. Kaufman PD, Kobayashi R, Stillman B (1997) Ultraviolet radiation sensitivity and reduction of telomeric silencing in Saccharomyces cerevisiae cells lacking chromatin assembly factor-I. Genes Dev 11(3):345–357

    Article  PubMed  CAS  Google Scholar 

  60. Kaufman PD, Kobayashi R, Kessler N, Stillman B (1995) The p150 and p60 subunits of chromatin assembly factor I: a molecular link between newly synthesized histones and DNA replication. Cell 81(7):1105–1114

    Article  PubMed  CAS  Google Scholar 

  61. Takami Y, Ono T, Fukagawa T, Shibahara K, Nakayama T (2007) Essential role of chromatin assembly factor-1-mediated rapid nucleosome assembly for DNA replication and cell division in vertebrate cells. Mol Biol Cell 18(1):129–141

    Article  PubMed  CAS  Google Scholar 

  62. Nabatiyan A, Krude T (2004) Silencing of chromatin assembly factor 1 in human cells leads to cell death and loss of chromatin assembly during DNA synthesis. Mol Cell Biol 24(7):2853–2862

    Article  PubMed  CAS  Google Scholar 

  63. Gerard A, Koundrioukoff S, Ramillon V, Sergere JC, Mailand N, Quivy JP, Almouzni G (2006) The replication kinase Cdc7-Dbf4 promotes the interaction of the p150 subunit of chromatin assembly factor 1 with proliferating cell nuclear antigen. EMBO Rep 7(8):817–823

    PubMed  CAS  Google Scholar 

  64. Shibahara K, Stillman B (1999) Replication-dependent marking of DNA by PCNA facilitates CAF-1-coupled inheritance of chromatin. Cell 96(4):575–585

    Article  PubMed  CAS  Google Scholar 

  65. Zhang Z, Shibahara K, Stillman B (2000) PCNA connects DNA replication to epigenetic inheritance in yeast. Nature 408(6809):221–225

    Article  PubMed  CAS  Google Scholar 

  66. Gaillard PH, Martini EM, Kaufman PD, Stillman B, Moustacchi E, Almouzni G (1996) Chromatin assembly coupled to DNA repair: a new role for chromatin assembly factor I. Cell 86(6):887–896

    Article  PubMed  CAS  Google Scholar 

  67. Moggs JG, Grandi P, Quivy JP, Jonsson ZO, Hubscher U, Becker PB, Almouzni G (2000) A CAF-1-PCNA-mediated chromatin assembly pathway triggered by sensing DNA damage. Mol Cell Biol 20(4):1206–1218

    Article  PubMed  CAS  Google Scholar 

  68. Green CM, Almouzni G (2003) Local action of the chromatin assembly factor CAF-1 at sites of nucleotide excision repair in vivo. EMBO J 22(19):5163–5174

    Article  PubMed  CAS  Google Scholar 

  69. Smith S, Stillman B (1991) Stepwise assembly of chromatin during DNA replication in vitro. EMBO J 10(4):971–980

    PubMed  CAS  Google Scholar 

  70. 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 

  71. Talbert PB, Henikoff S (2010) Histone variants—ancient wrap artists of the epigenome. Nat Rev Mol Cell Biol 11(4):264–275

    Article  PubMed  CAS  Google Scholar 

  72. Polo S, Roche D, Almouzni G (2006) New histone incorporation marks sites of UV repair in human cells. Cell 127(3):481–493

    Article  PubMed  CAS  Google Scholar 

  73. Malik HS, Henikoff S (2003) Phylogenomics of the nucleosome. Nat Struct Biol 10(11):882–891

    Article  PubMed  CAS  Google Scholar 

  74. Kaufman PD, Cohen JL, Osley MA (1998) Hir proteins are required for position-dependent gene silencing in Saccharomyces cerevisiae in the absence of chromatin assembly factor I. Mol Cell Biol 18(8):4793–4806

    PubMed  CAS  Google Scholar 

  75. Verreault A, Kaufman PD, Kobayashi R, Stillman B (1996) Nucleosome assembly by a complex of CAF-1 and acetylated histones H3/H4. Cell 87(1):95–104

    Article  PubMed  CAS  Google Scholar 

  76. Shibahara K, Verreault A, Stillman B (2000) The N-terminal domains of histones H3 and H4 are not necessary for chromatin assembly factor-1-mediated nucleosome assembly onto replicated DNA in vitro. Proc Natl Acad Sci USA 97(14):7766–7771

    Article  PubMed  CAS  Google Scholar 

  77. Le S, Davis C, Konopka JB, Sternglanz R (1997) Two new S-phase-specific genes from Saccharomyces cerevisiae. Yeast 13(11):1029–1042

    Article  PubMed  CAS  Google Scholar 

  78. Tyler JK, Adams CR, Chen SR, Kobayashi R, Kamakaka RT, Kadonaga JT (1999) The RCAF complex mediates chromatin assembly during DNA replication and repair. Nature 402(6761):555–560

    Article  PubMed  CAS  Google Scholar 

  79. Sanematsu F, Takami Y, Barman HK, Fukagawa T, Ono T, Shibahara K, Nakayama T (2006) Asf1 is required for viability and chromatin assembly during DNA replication in vertebrate cells. J Biol Chem 281(19):13817–13827

    Article  PubMed  CAS  Google Scholar 

  80. Groth A, Ray-Gallet D, Quivy JP, Lukas J, Bartek J, Almouzni G (2005) Human Asf1 regulates the flow of S phase histones during replicational stress. Mol Cell 17(2):301–311

    Article  PubMed  CAS  Google Scholar 

  81. Franco AA, Lam WM, Burgers PM, Kaufman PD (2005) Histone deposition protein Asf1 maintains DNA replisome integrity and interacts with replication factor C. Genes Dev 19(11):1365–1375

    Article  PubMed  CAS  Google Scholar 

  82. Groth A, Corpet A, Cook A, Roche D, Bartek J, Lukas J, Almouzni G (2007) Regulation of replication fork progression through histone supply and demand. Science 318(5858):1928–1931

    Article  PubMed  CAS  Google Scholar 

  83. Adkins MW, Tyler JK (2004) The histone chaperone Asf1p mediates global chromatin disassembly in vivo. J Biol Chem 279(50):52069–52074

    Article  PubMed  CAS  Google Scholar 

  84. Korber P, Barbaric S, Luckenbach T, Schmid A, Schermer UJ, Blaschke D, Horz W (2006) The histone chaperone Asf1 increases the rate of histone eviction at the yeast PHO5 and PHO8 promoters. J Biol Chem 281(9):5539–5545

    Article  PubMed  CAS  Google Scholar 

  85. Tyler JK, Collins KA, Prasad-Sinha J, Amiott E, Bulger M, Harte PJ, Kobayashi R, Kadonaga JT (2001) Interaction between the Drosophila CAF-1 and ASF1 chromatin assembly factors. Mol Cell Biol 21(19):6574–6584

    Article  PubMed  CAS  Google Scholar 

  86. 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 

  87. Mirkin E, Mirkin S (2007) Replication fork stalling at natural impediments. Microbiol Mol Biol Rev 71(1):13–35

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  89. Papp B, Muller J (2006) Histone trimethylation and the maintenance of transcriptional ON and OFF states by trxG and PcG proteins. Genes Dev 20(15):2041–2054

    Article  PubMed  CAS  Google Scholar 

  90. Francis NJ, Follmer NE, Simon MD, Aghia G, Butler JD (2009) Polycomb proteins remain bound to chromatin and DNA during DNA replication in vitro. Cell 137(1):110–122

    Article  PubMed  CAS  Google Scholar 

  91. Byvoet P, Shepherd GR, Hardin JM, Noland BJ (1972) The distribution and turnover of labeled methyl groups in histone fractions of cultured mammalian cells. Arch Biochem Biophys 148(2):558–567

    Article  PubMed  CAS  Google Scholar 

  92. Jenuwein T, Allis C (2001) Translating the histone code. Science 293(5532):1074–1080

    Article  PubMed  CAS  Google Scholar 

  93. Zee BM, Levin RS, Dimaggio PA, Garcia BA (2010) Global turnover of histone post-translational modifications and variants in human cells. Epigenetics Chromatin 3(1):22

    Article  PubMed  CAS  Google Scholar 

  94. Pray-Grant MG, Daniel JA, Schieltz D, Yates JR III, Grant PA (2005) Chd1 chromodomain links histone H3 methylation with SAGA- and SLIK-dependent acetylation. Nature 433(7024):434–438

    Article  PubMed  CAS  Google Scholar 

  95. Hoppmann V, Thorstensen T, Kristiansen PE, Veiseth SV, Rahman MA, Finne K, Aalen RB, Aasland R (2011) The CW domain, a new histone recognition module in chromatin proteins. EMBO J 30(10):1939–1952

    Article  PubMed  CAS  Google Scholar 

  96. Carmen AA, Milne L, Grunstein M (2002) Acetylation of the yeast histone H4 N terminus regulates its binding to heterochromatin protein SIR3. J Biol Chem 277(7):4778–4781

    Article  PubMed  CAS  Google Scholar 

  97. Lan F, Collins RE, De Cegli R, Alpatov R, Horton JR, Shi X, Gozani O, Cheng X, Shi Y (2007) Recognition of unmethylated histone H3 lysine 4 links BHC80 to LSD1-mediated gene repression. Nature 448(7154):718–722

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  99. David-Rus D, Mukhopadhyay S, Lebowitz JL, Sengupta AM (2009) Inheritance of epigenetic chromatin silencing. J Theor Biol 258(1):112–120

    Article  PubMed  CAS  Google Scholar 

  100. Pokholok DK, Harbison CT, Levine S, Cole M, Hannett NM, Lee TI, Bell GW, Walker K, Rolfe PA, Herbolsheimer E, Zeitlinger J, Lewitter F, Gifford DK, Young RA (2005) Genome-wide map of nucleosome acetylation and methylation in yeast. Cell 122(4):517–527

    Article  PubMed  CAS  Google Scholar 

  101. Ng SS, Yue WW, Oppermann U, Klose RJ (2009) Dynamic protein methylation in chromatin biology. Cell Mol Life Sci 66(3):407–422

    Article  PubMed  CAS  Google Scholar 

  102. Agger K, Cloos PA, Christensen J, Pasini D, Rose S, Rappsilber J, Issaeva I, Canaani E, Salcini AE, Helin K (2007) UTX and JMJD3 are histone H3K27 demethylases involved in HOX gene regulation and development. Nature 449(7163):731–734

    Article  PubMed  CAS  Google Scholar 

  103. Klose RJ, Yamane K, Bae Y, Zhang D, Erdjument-Bromage H, Tempst P, Wong J, Zhang Y (2006) The transcriptional repressor JHDM3A demethylates trimethyl histone H3 lysine 9 and lysine 36. Nature 442(7100):312–316

    Article  PubMed  CAS  Google Scholar 

  104. Mellor J (2006) Dynamic nucleosomes and gene transcription. Trends Genet 22(6):320–329

    Article  PubMed  CAS  Google Scholar 

  105. Radman-Livaja M, Liu CL, Friedman N, Schreiber SL, Rando OJ (2010) Replication and active demethylation represent partially overlapping mechanisms for erasure of H3K4me3 in budding yeast. PLoS Genet 6(2):e1000837

    Article  PubMed  CAS  Google Scholar 

  106. Ingvarsdottir K, Edwards C, Lee MG, Lee JS, Schultz DC, Shilatifard A, Shiekhattar R, Berger SL (2007) Histone H3 K4 demethylation during activation and attenuation of GAL1 transcription in Saccharomyces cerevisiae. Mol Cell Biol 27(22):7856–7864

    Article  PubMed  CAS  Google Scholar 

  107. 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(1):97–108

    Article  PubMed  CAS  Google Scholar 

  108. Dion MF, Kaplan T, Kim M, Buratowski S, Friedman N, Rando OJ (2007) Dynamics of replication-independent histone turnover in budding yeast. Science 315(5817):1405–1408

    Article  PubMed  CAS  Google Scholar 

  109. Hodges C, Bintu L, Lubkowska L, Kashlev M, Bustamante C (2009) Nucleosomal fluctuations govern the transcription dynamics of RNA polymerase II. Science 325(5940):626–628

    Article  PubMed  CAS  Google Scholar 

  110. Clapier CR, Cairns BR (2009) The biology of chromatin remodeling complexes. Annu Rev Biochem 78:273–304

    Article  PubMed  CAS  Google Scholar 

  111. Mito Y, Henikoff JG, Henikoff S (2005) Genome-scale profiling of histone H3.3 replacement patterns. Nat Genet 37(10):1090–1097

    Article  PubMed  CAS  Google Scholar 

  112. Deal RB, Henikoff JG, Henikoff S (2010) Genome-wide kinetics of nucleosome turnover determined by metabolic labeling of histones. Science 328(5982):1161–1164

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  114. Ng RK, Gurdon JB (2008) Epigenetic memory of an active gene state depends on histone H3.3 incorporation into chromatin in the absence of transcription. Nat Cell Biol 10(1):102–109

    Article  PubMed  CAS  Google Scholar 

  115. Jin C, Felsenfeld G (2007) Nucleosome stability mediated by histone variants H3.3 and H2A.Z. Genes Dev 21(12):1519–1529

    Article  PubMed  CAS  Google Scholar 

  116. Lewis PW, Elsaesser SJ, Noh KM, Stadler SC, Allis CD (2010) Daxx is an H3.3-specific histone chaperone and cooperates with ATRX in replication-independent chromatin assembly at telomeres. Proc Natl Acad Sci USA 107(32):14075–14080

    Article  PubMed  CAS  Google Scholar 

  117. Chuang LS, Ian HI, Koh TW, Ng HH, Xu G, Li BF (1997) Human DNA-(cytosine-5) methyltransferase-PCNA complex as a target for p21WAF1. Science 277(5334):1996–2000

    Article  PubMed  CAS  Google Scholar 

  118. Esteve PO, Chin HG, Smallwood A, Feehery GR, Gangisetty O, Karpf AR, Carey MF, Pradhan S (2006) Direct interaction between DNMT1 and G9a coordinates DNA and histone methylation during replication. Genes Dev 20(22):3089–3103

    Article  PubMed  CAS  Google Scholar 

  119. Murzina N, Verreault A, Laue E, Stillman B (1999) Heterochromatin dynamics in mouse cells: interaction between chromatin assembly factor 1 and HP1 proteins. Mol Cell 4(4):529–540

    Article  PubMed  CAS  Google Scholar 

  120. Filion GJ, van Bemmel JG, Braunschweig U, Talhout W, Kind J, Ward LD, Brugman W, de Castro IJ, Kerkhoven RM, Bussemaker HJ, van Steensel B (2010) Systematic protein location mapping reveals five principal chromatin types in Drosophila cells. Cell 143(2):212–224

    Article  PubMed  CAS  Google Scholar 

  121. Hand R (1978) Eucaryotic DNA: organization of the genome for replication. Cell 15(2):317–325

    Article  PubMed  CAS  Google Scholar 

  122. Hiratani I, Ryba T, Itoh M, Yokochi T, Schwaiger M, Chang CW, Lyou Y, Townes TM, Schubeler D, Gilbert DM (2008) Global reorganization of replication domains during embryonic stem cell differentiation. PLoS Biol 6(10):e245

    Article  PubMed  CAS  Google Scholar 

  123. McNairn AJ, Gilbert DM (2003) Epigenomic replication: linking epigenetics to DNA replication. BioEssays News Rev Mol Cell Dev Biol 25(7):647–656

    CAS  Google Scholar 

  124. Lande-Diner L, Zhang J, Cedar H (2009) Shifts in replication timing actively affect histone acetylation during nucleosome reassembly. Mol Cell 34(6):767–774

    Article  PubMed  CAS  Google Scholar 

  125. Gilbert DM (2002) Replication timing and transcriptional control: beyond cause and effect. Curr Opin Cell Biol 14(3):377–383

    Article  PubMed  CAS  Google Scholar 

  126. Hiratani I, Takebayashi S, Lu J, Gilbert DM (2009) Replication timing and transcriptional control: beyond cause and effect—part II. Curr Opin Genet Dev 19(2):142–149

    Article  PubMed  CAS  Google Scholar 

  127. Reik A, Telling A, Zitnik G, Cimbora D, Epner E, Groudine M (1998) The locus control region is necessary for gene expression in the human beta-globin locus but not the maintenance of an open chromatin structure in erythroid cells. Mol Cell Biol 18(10):5992–6000

    PubMed  CAS  Google Scholar 

  128. Goren A, Tabib A, Hecht M, Cedar H (2008) DNA replication timing of the human beta-globin domain is controlled by histone modification at the origin. Genes Dev 22(10):1319–1324

    Article  PubMed  CAS  Google Scholar 

  129. Prioleau MN, Gendron MC, Hyrien O (2003) Replication of the chicken beta-globin locus: early-firing origins at the 5’ HS4 insulator and the rho- and betaA-globin genes show opposite epigenetic modifications. Mol Cell Biol 23(10):3536–3549

    Article  PubMed  CAS  Google Scholar 

  130. Almouzni G, Mechali M, Wolffe AP (1991) Transcription complex disruption caused by a transition in chromatin structure. Mol Cell Biol 11(2):655–665

    PubMed  CAS  Google Scholar 

  131. Maizels N (2006) Dynamic roles for G4 DNA in the biology of eukaryotic cells. Nat Struct Mol Biol 13(12):1055–1059

    Article  PubMed  CAS  Google Scholar 

  132. Lipps HJ, Rhodes D (2009) G-quadruplex structures: in vivo evidence and function. Trends Cell Biol 19(8):414–422

    Article  PubMed  CAS  Google Scholar 

  133. Sarkies P, Reams C, Simpson LJ, Sale JE (2010) Epigenetic instability due to defective replication of structured DNA. Mol Cell 40(5):703–713

    Article  PubMed  CAS  Google Scholar 

  134. Edmunds CE, Simpson LJ, Sale JE (2008) PCNA ubiquitination and REV1 define temporally distinct mechanisms for controlling translesion synthesis in the avian cell line DT40. Mol Cell 30(4):519–529

    Article  PubMed  CAS  Google Scholar 

  135. Jansen J, Tsaalbi-Shtylik A, Hendriks G, Gali H, Hendel A, Johansson F, Erixon K, Livneh Z, Mullenders L, Haracska L, de Wind N (2009) Separate domains of Rev1 mediate two modes of DNA damage bypass in mammalian cells. Mol Cell Biol 29(11):3113–3123

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We would like to thank members of the lab for discussions and comments on the manuscript. Work in the lab is supported by the Medical Research Council, Association for International Cancer Research and the Fanconi Anemia Research Fund.

Conflict of interest

The authors declare that they have no conflicts of interest.

Author information

Authors and Affiliations

  1. Division of Protein and Nucleic Acid Chemistry, Medical Research Council Laboratory of Molecular Biology, Hills Road, Cambridge, CB2 0QH, UK

    Peter Sarkies & Julian E. Sale

Authors
  1. Peter Sarkies
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Julian E. Sale
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Peter Sarkies or Julian E. Sale.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sarkies, P., Sale, J.E. Propagation of histone marks and epigenetic memory during normal and interrupted DNA replication. Cell. Mol. Life Sci. 69, 697–716 (2012). https://doi.org/10.1007/s00018-011-0824-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00018-011-0824-1

Keywords

Search

Navigation