Chromatin replication and epigenome maintenance

Nature Reviews Molecular Cell Biology

Volumn 13, Issue 3, 2012, Pages 153-167

  Alabert, Constance ^a   Groth, Anja ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; HISTONE;

CHROMATIN; DNA REPLICATION; DNA SYNTHESIS; EPIGENETICS; GENOME; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW;

ANIMALS; CELL DIVISION; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA REPLICATION; EPIGENESIS, GENETIC; EPIGENOMICS; GENOMIC INSTABILITY; HISTONES; HUMANS; MULTIPROTEIN COMPLEXES; REPLICATION ORIGIN;

EID: 84857430552     PISSN: 14710072     EISSN: 14710080     Source Type: Journal    
DOI: 10.1038/nrm3288     Document Type: Review

References (201)

1. Probst, A. V., Dunleavy, E & Almouzni G. Epigenetic inheritance during the cell cycle. Nature Rev. Mol. Cell Biol. 10, 192-206 (2009).
2. Groth, A., Rocha, W., Verreault, A. & Almouzni, G. Chromatin challenges during DNA replication and repair. Cell 128, 721-733 (2007). (Pubitemid 46273574)
3. Meister, P., Mango, S. E. & Gasser, S. M. Locking the genome: nuclear organization and cell fate. Curr. Opin. Genet. Dev. 21, 167-174 (2011).
4. Blow, J. J., Ge, X. Q. & Jackson, D. A. How dormant origins promote complete genome replication. Trends Biochem. Sci. 36, 405-414 (2011).
5. Branzei, D. & Foiani, M. Maintaining genome stability at the replication fork. Nature Rev. Mol. Cell Biol. 11, 208-219 (2010).
6. Halazonetis, T. D., Gorgoulis, V. G. & Bartek, J. An oncogene-induced DNA damage model for cancer development. Science 319, 1352-1355 (2008). (Pubitemid 351354863)
7. Sharma, S., Kelly, T. K. & Jones, P. A. Epigenetics in cancer. Carcinogenesis 31, 27-36 (2010).
8. Jasencakova, Z. & Groth, A. Replication stress, a source of epigenetic aberrations in cancer? Bioessays 32, 847-855 (2010).
9. Kouzarides, T. Chromatin modifications and their function. Cell 128, 693-705 (2007). (Pubitemid 46273577)
10. Mechali, M. Eukaryotic DNA replication origins: many choices for appropriate answers. Nature Rev. Mol. Cell Biol. 11, 728-738 (2010).
11. Remus, D. & Diffley, J. F. Eukaryotic DNA replication control: lock and load, then fire. Curr. Opin. Cell Biol. 21, 771-777 (2009).
12. Letessier, A. et al. Cell type specific replication initiation programs set fragility of the FRA3B fragile site. Nature 470, 120-123 (2011).
13. MacAlpine, H. K., Gordan, R., Powell, S. K., Hartemink, A. J. & MacAlpine, D. M. Drosophila ORC localizes to open chromatin and marks sites of cohesin complex loading. Genome Res. 20, 201-211 (2010).
14. Lubelsky, Y. et al. Pre-replication complex proteins assemble at regions of low nucleosome occupancy within the Chinese hamster dihydrofolate reductase initiation zone. Nucleic Acids Res. 39, 3141-3155 (2011).
15. Cayrou, C. et al. Genome-scale analysis of metazoan replication origins reveals their organization in specific but flexible sites defined by conserved features. Genome Res.12, 1438-1449 (2011).
16. Thomae, A. W. et al. Interaction between HMGA1a and the origin recognition complex creates site-specific replication origins. Proc. Natl Acad. Sci. USA 105, 1692-1697 (2008). (Pubitemid 351346576)
17. Atanasiu, C., Deng, Z., Wiedmer, A., Norseen, J. & Lieberman, P. M. ORC binding to TRF2 stimulates OriP replication. EMBO Rep. 7, 716-721 (2006). (Pubitemid 43986269)
18. Schwaiger, M., Kohler, H., Oakeley, E. J., Stadler, M. B. & Schubeler, D. Heterochromatin protein 1 (HP1) modulates replication timing of the Drosophila genome. Genome Res. 20, 771-780 (2010).
19. Tardat, M. et al. The histone H4 Lys 20 methyltransferase PRSet7 regulates replication origins in mammalian cells. Nature Cell Biol. 12, 1086-1093 (2010).
20. Jorgensen, S. et al. SET8 is degraded via PCNA-coupled CRL4(CDT2) ubiquitylation in S phase and after UV irradiation. J. Cell Biol. 192, 43-54 (2011).
21. Centore, R. C. et al. CRL4(Cdt2)-mediated destruction of the histone methyltransferase Set8 prevents premature chromatin compaction in S phase. Mol. Cell 40, 22-33 (2010).
22. Rice, J. C. et al. Mitotic-specific methylation of histone H4 Lys 20 follows increased PRSet7 expression and its localization to mitotic chromosomes. Genes Dev. 16, 2225-2230 (2002). (Pubitemid 35013085)
23. Miotto, B. & Struhl, K. HBO1 histone acetylase activity is essential for DNA replication licensing and inhibited by Geminin. Mol. Cell 37, 57-66 (2010).
24. Miotto, B. & Struhl, K. HBO1 histone acetylase is a coactivator of the replication licensing factor Cdt1. Genes Dev. 22, 2633-2638 (2008).
25. Iizuka, M., Matsui, T., Takisawa, H. & Smith, M. M. Regulation of replication licensing by acetyltransferase Hbo1. Mol. Cell. Biol. 26, 1098-1108 (2006). (Pubitemid 43146501)
26. Remus, D. et al. Concerted loading of Mcm2-7 double hexamers around DNA during DNA replication origin licensing. Cell 139, 719-730 (2009).
27. Gambus, A. et al. GINS maintains association of Cdc45 with MCM in replisome progression complexes at eukaryotic DNA replication forks. Nature Cell Biol. 8, 358-366 (2006).
28. Ge, X. Q., Jackson, D. A. & Blow, J. J. Dormant origins licensed by excess Mcm2-7 are required for human cells to survive replicative stress. Genes Dev. 21, 3331-3341 (2007). (Pubitemid 350277759)
29. Ibarra, A., Schwob, E. & Mendez, J. Excess MCM proteins protect human cells from replicative stress by licensing backup origins of replication. Proc. Natl Acad. Sci. USA 105, 8956-8961 (2008).
30. Courbet, S. et al. Replication fork movement sets chromatin loop size and origin choice in mammalian cells. Nature 455, 557-560 (2008).
31. Jackson, D. A. & Pombo, A. Replicon clusters are stable units of chromosome structure: evidence that nuclear organization contributes to the efficient activation and propagation of S phase in human cells. J. Cell Biol. 140, 1285-1295 (1998). (Pubitemid 28152979)
32. Gillespie, P. J. & Blow, J. J. Clusters, factories and domains: the complex structure of S-phase comes into focus. Cell Cycle 9, 3218-3226 (2010).
33. Buongiorno-Nardelli, M., Micheli, G., Carri, M. T. & Marilley, M. A relationship between replicon size and supercoiled loop domains in the eukaryotic genome. Nature 298, 100-102 (1982). (Pubitemid 12087493)
34. Guillou, E. et al. Cohesin organizes chromatin loops at DNA replication factories. Genes Dev. 24, 2812-2822 (2010).
35. Gilbert, D. M. et al. Space and time in the nucleus: developmental control of replication timing and chromosome architecture. Cold Spring Harb. Symp. Quant. Biol. 75, 143-153 (2010).
36. Hiratani, I. et al. Global reorganization of replication domains during embryonic stem cell differentiation. PLoS Biol. 6, 2220-2236 (2008).
37. Filion, G. J. et al. Systematic protein location mapping reveals five principal chromatin types in Drosophila cells. Cell 143, 212-224 (2010).
38. Bell, O. et al. Accessibility of the Drosophila genome discriminates PcG repression, H4K16 acetylation and replication timing. Nature Struct. Mol. Biol. 17, 894-900 (2010).
39. Hansen, R. S. et al. Sequencing newly replicated DNA reveals widespread plasticity in human replication timing. Proc. Natl Acad. Sci. USA 107, 139-144 (2010).
40. Schwaiger, M. et al. Chromatin state marks cell-type and gender-specific replication of the Drosophila genome. Genes Dev. 23, 589-601 (2009).
41. Lieberman-Aiden, E. et al. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326, 289-293 (2009).
42. Ryba, T. et al. Evolutionarily conserved replication timing profiles predict long-range chromatin interactions and distinguish closely related cell types. Genome Res. 20, 761-770 (2010).
43. De, S. & Michor, F. DNA replication timing and long-range DNA interactions predict mutational landscapes of cancer genomes. Nature Biotech. 29, 1103-1108 (2011).
44. Francis, N. J., Follmer, N. E., Simon, M. D., Aghia, G. & Butler, J. D. Polycomb proteins remain bound to chromatin and DNA during DNA replication in vitro. Cell 137, 110-122 (2009).
45. Kuipers, M. A. et al. Highly stable loading of Mcm proteins onto chromatin in living cells requires replication to unload. J. Cell Biol. 192, 29-41 (2011).
46. Alexandrow, M. G. & Hamlin, J. L. Chromatin decondensation in S-phase involves recruitment of Cdk2 by Cdc45 and histone H1 phosphorylation. J. Cell Biol. 168, 875-886 (2005). (Pubitemid 40397002)
47. Thomson, A. M., Gillespie, P. J. & Blow, J. J. Replication factory activation can be decoupled from the replication timing program by modulating Cdk levels. J. Cell Biol. 188, 209-221 (2010).
48. Contreras, A. et al. The dynamic mobility of histone H1 is regulated by cyclin/CDK phosphorylation. Mol. Cell. Biol. 23, 8626-8636 (2003). (Pubitemid 37433367)
49. Thiriet, C. & Hayes, J. J. Linker histone phosphorylation regulates global timing of replication origin firing. J. Biol. Chem. 284, 2823-2829 (2009).
50. Cardoso, M. C., Leonhardt, H. & Nadal-Ginard, B. Reversal of terminal differentiation and control of DNA replication: cyclin A and Cdk2 specifically localize at subnuclear sites of DNA replication. Cell 74, 979-992 (1993). (Pubitemid 23289456)
51. Koundrioukoff, S. et al. A direct interaction between proliferating cell nuclear antigen (PCNA) and Cdk2 targets PCNA-interacting proteins for phosphorylation. J. Biol. Chem. 275, 22882-22887 (2000). (Pubitemid 30646174)
52. Chibazakura, T. et al. Cyclin A promotes S-phase entry via interaction with the replication licensing factor Mcm7. Mol. Cell Biol. 31, 248-255 (2011).
53. Katsuno, Y. et al. Cyclin A-Cdk1 regulates the origin firing program in mammalian cells. Proc. Natl Acad. Sci. USA 106, 3184-3189 (2009).
54. Sogo, J. M., Stahl, H., Koller, T. & Knippers, R. Structure of replicating simian virus 40 minichromosomes. The replication fork, core histone segregation and terminal structures. J. Mol. Biol. 189, 189-204 (1986). (Pubitemid 16063831)
55. Gasser, R., Koller, T. & Sogo, J. M. The stability of nucleosomes at the replication fork. J. Mol. Biol. 258, 224-239 (1996). (Pubitemid 26131727)
56. Groth, A. Replicating chromatin: a tale of histones. Biochem. Cell Biol. 87, 51-63 (2009).
57. Xu, M. et al. Partitioning of histone H3H4 tetramers during DNA replication-dependent chromatin assembly. Science 328, 94-98 (2010).
58. Jackson, V. & Chalkley, R. A re-evaluation of new histone deposition on replicating chromatin. J. Biol. Chem. 256, 5095-5103 (1981).
59. Radman-Livaja, M. et al. Patterns and mechanisms of ancestral histone protein inheritance in budding yeast. PLoS Biol. 9, e1001075 (2011).
60. Ishimi, Y., Ichinose, S., Omori, A., Sato, K. & Kimura, H. Binding of human minichromosome maintenance proteins with histone H3. J. Biol. Chem. 271, 24115-24122 (1996). (Pubitemid 26327393)
61. Ramsperger, U. & Stahl, H. Unwinding of chromatin by the SV40 large T antigen DNA helicase. EMBO J. 14, 3215-3225 (1995).
62. Groth, A. et al. Regulation of replication fork progression through histone supply and demand. Science 318, 1928-1931 (2007).
63. Jasencakova, Z. et al. Replication stress interferes with histone recycling and predeposition marking of new histones. Mol. Cell 37, 736-743 (2010).
64. English, C. M., Adkins, M. W., Carson, J. J., Churchill, M. E. & Tyler, J. K. Structural basis for the histone chaperone activity of Asf1. Cell 127, 495-508 (2006). (Pubitemid 44647420)
65. Natsume, R. et al. Structure and function of the histone chaperone CIA/ASF1 complexed with histones H3 and H4. Nature 446, 338-341 (2007). (Pubitemid 46437114)
66. Duro, E. et al. Identification of the MMS22L-TONSL complex that promotes homologous recombination. Mol. Cell 40, 632-644 (2010).
67. Tan, B. C., Chien, C. T., Hirose, S. & Lee, S. C. Functional cooperation between FACT and MCM helicase facilitates initiation of chromatin DNA replication. EMBO J. 25, 3975-3985 (2006). (Pubitemid 44338740)
68. VanDemark, A. P. et al. The structure of the yFACT Pob3-M domain, its interaction with the DNA replication factor RPA, and a potential role in nucleosome deposition. Mol. Cell 22, 363-374 (2006).
69. Wittmeyer, J. & Formosa, T. The Saccharomyces cerevisiae DNA polymerase α catalytic subunit interacts with Cdc68/Spt16 and with Pob3, a protein similar to an HMG1-like protein. Mol. Cell. Biol. 17, 4178-4190 (1997). (Pubitemid 27281894)
70. Formosa, T. The role of FACT in making and breaking nucleosomes. Biochim. Biophys. Acta 23 Jul 2011 (doi:10.1016/j.bbagrm.2011.07.009).
71. Abe, T. et al. The histone chaperone FACT maintains normal replication fork rates. J. Biol. Chem. 286, 30504-30512 (2011).
72. Winkler, D. D., Muthurajan, U. M., Hieb, A. R. & Luger, K. Histone chaperone FACT coordinates nucleosome interaction through multiple synergistic binding events. J. Biol. Chem. 286, 41883-41892 (2011).
73. Marzluff, W. F., Wagner, E. J. & Duronio, R. J. Metabolism and regulation of canonical histone mRNAs: life without a poly(A) tail. Nature Rev. Genet. 9, 843-854 (2008).
74. Annunziato, A. T. Assembling chromatin: the long and winding road. Biochim. Biophys. Acta 18 Jul 2011 (doi:10.1016/j.bbagrm.2011.07.005).
75. Smith, S. & Stillman, B. Purification and characterization of CAFI, a human cell factor required for chromatin assembly during DNA replication in vitro. Cell 58, 15-25 (1989). (Pubitemid 19180075)
76. Campos, E. I. et al. The program for processing newly synthesized histones H3.1 and H4. Nature Struct. Mol. Biol. 17, 1343-1351 (2010).
77. Alvarez, F. et al. Sequential establishment of marks on soluble histones h3 and h4. J. Biol. Chem. 286, 17714-17721 (2011).
78. Cook, A. J., Gurard-Levin, Z. A., Vassias, I. & Almouzni, G. A specific function for the histone chaperone NASP to fine-tune a reservoir of soluble H3H4 in the histone supply chain. Mol. Cell 44, 918-927 (2011).
79. Sobel, R. E., Cook, R. G., Perry, C. A., Annunziato, A. T. & Allis, C. D. Conservation of deposition-related acetylation sites in newly synthesized histones H3 and H4. Proc. Natl Acad. Sci. USA 92, 1237-1241 (1995).
80. Loyola, A., Bonaldi, T., Roche, D., Imhof, A. & Almouzni, G. PTMs on H3 variants before chromatin assembly potentiate their final epigenetic state. Mol. Cell 24, 309-316 (2006). (Pubitemid 44557123)
81. Tyler, J. K. et al. The RCAF complex mediates chromatin assembly during DNA replication and repair. Nature 402, 555-560 (1999).
82. Mello, J. A. et al. Human Asf1 and CAF1 interact and synergize in a repair-coupled nucleosome assembly pathway. EMBO Rep. 3, 329-334 (2002). (Pubitemid 34467602)
83. Hu, H. et al. Structure of a CENP-A-histone H4 heterodimer in complex with chaperone HJURP. Genes Dev. 25, 901-906 (2011).
84. Tagami, H., Ray-Gallet, D., Almouzni, G. & Nakatani, Y. Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis. Cell 116, 51-61 (2004). (Pubitemid 38156183)
85. Groth, A. et al. Human Asf1 regulates the flow of S phase histones during replicational stress. Mol. Cell 17, 301-311 (2005). (Pubitemid 40138623)
86. Ray-Gallet, D. et al. Dynamics of histone h3 deposition in vivo reveal a nucleosome gap-filling mechanism for h3.3 to maintain chromatin integrity. Mol. Cell 44, 928-941 (2011).
87. Ahmad, K. & Henikoff, S. The histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly. Mol. Cell 9, 1191-1200 (2002). (Pubitemid 34722299)
88. Kang, B. et al. Phosphorylation of H4 Ser 47 promotes HIRA-mediated nucleosome assembly. Genes Dev. 25, 1359-1364 (2011).
89. Masumoto, H., Hawke, D., Kobayashi, R. & Verreault, A. A role for cell-cycle-regulated histone H3 lysine 56 acetylation in the DNA damage response. Nature 436, 294-298 (2005). (Pubitemid 41021284)
90. Burgess, R. J., Zhou, H., Han, J. & Zhang, Z. A role for Gcn5 in replication-coupled nucleosome assembly. Mol. Cell 37, 469-480 (2010).
91. Li, Q. et al. Acetylation of histone H3 lysine 56 regulates replication-coupled nucleosome assembly. Cell 134, 244-255 (2008). (Pubitemid 352010333)
92. Das, C., Lucia, M. S., Hansen, K. C. & Tyler, J. K. CBP/p300-mediated acetylation of histone H3 on lysine 56. Nature 459, 113-117 (2009).
93. Loyola, A. et al. The HP1α-CAF1-SetDB1-containing complex provides H3K9me1 for Suv39-mediated K9me3 in pericentric heterochromatin. EMBO Rep. 10, 769-775 (2009).
94. Quivy, J. P., Gerard, A., Cook, A. J., Roche, D. & Almouzni, G. The HP1p150/CAF1 interaction is required for pericentric heterochromatin replication and S-phase progression in mouse cells. Nature Struct. Mol. Biol. 15, 972-979 (2008).
95. Murzina, N., Verreault, A., Laue, E. & Stillman, B. Heterochromatin dynamics in mouse cells: interaction between chromatin assembly factor 1 and HP1 proteins. Mol. Cell 4, 529-540 (1999). (Pubitemid 29531133)
96. Probst, A. V. & Almouzni, G. Heterochromatin establishment in the context of genome-wide epigenetic reprogramming. Trends Genet. 27, 177-185 (2011).
97. Margueron, R. & Reinberg, D. Chromatin structure and the inheritance of epigenetic information. Nature Rev. Genet. 11, 285-296 (2010).
98. Johnson, A. & O'Donnell, M. Cellular DNA replicases: components and dynamics at the replication fork. Annu. Rev. Biochem. 74, 283-315 (2005). (Pubitemid 40995509)
99. Shibahara, K. & Stillman, B. Replication-dependent marking of DNA by PCNA facilitates CAF-1-coupled inheritance of chromatin. Cell 96, 575-585 (1999). (Pubitemid 29106844)
100. Moggs, J. G. et al. A CAF-1-PCNA-mediated chromatin assembly pathway triggered by sensing DNA damage. Mol. Cell Biol. 20, 1206-1218 (2000). (Pubitemid 30069241)
101. Chafin, D. R., Vitolo, J. M., Henricksen, L. A., Bambara, R. A. & Hayes, J. J. Human DNA ligase I efficiently seals nicks in nucleosomes. EMBO J. 19, 5492-5501 (2000).
102. Huggins, C. F. et al. Flap endonuclease 1 efficiently cleaves base excision repair and DNA replication intermediates assembled into nucleosomes. Mol. Cell 10, 1201-1211 (2002). (Pubitemid 35453836)
103. Beattie, T. R. & Bell, S. D. The role of the DNA sliding clamp in Okazaki fragment maturation in archaea and eukaryotes. Biochem. Soc. Trans. 39, 70-76 (2011).
104. Andrews, A. J., Chen, X., Zevin, A., Stargell, L. A. & Luger, K. The histone chaperone Nap1 promotes nucleosome assembly by eliminating nonnucleosomal histone DNA interactions. Mol. Cell 37, 834-842 (2010).
105. Nasmyth, K. Cohesin: a catenase with separate entry and exit gates? Nature Cell Biol. 13, 1170-1177 (2011).
106. Lengronne, A. et al. Establishment of sister chromatid cohesion at the S. cerevisiae replication fork. Mol. Cell 23, 787-799 (2006). (Pubitemid 44344523)
107. Bermudez, V. P. et al. The alternative Ctf18-Dcc1-Ctf8-replication factor C complex required for sister chromatid cohesion loads proliferating cell nuclear antigen onto DNA. Proc. Natl Acad. Sci. USA 100, 10237-10242 (2003). (Pubitemid 37071862)
108. Terret, M. E., Sherwood, R., Rahman, S., Qin, J. & Jallepalli, P. V. Cohesin acetylation speeds the replication fork. Nature 462, 231-234 (2009).
109. Sporbert, A., Gahl, A., Ankerhold, R., Leonhardt, H. & Cardoso, M. C. DNA polymerase clamp shows little turnover at established replication sites but sequential de novo assembly at adjacent origin clusters. Mol. Cell 10, 1355-1365 (2002). (Pubitemid 36050877)
110. Nakano, S., Stillman, B. & Horvitz, H. R. Replication-coupled chromatin assembly generates a neuronal bilateral asymmetry in C. elegans. Cell 147, 1525-1536 (2011).
111. Annunziato, A. T. & Seale, R. L. Histone deacetylation is required for the maturation of newly replicated chromatin. J. Biol. Chem. 258, 12675-12684 (1983).
112. Fisher, D. & Mechali, M. Vertebrate HoxB gene expression requires DNA replication. EMBO J. 22, 3737-3748 (2003). (Pubitemid 36898350)
113. Kloc, A., Zaratiegui, M., Nora, E. & Martienssen, R. RNA interference guides histone modification during the S phase of chromosomal replication. Curr. Biol. 18, 490-495 (2008).
114. Chen, E. S. et al. Cell cycle control of centromeric repeat transcription and heterochromatin assembly. Nature 451, 734-737 (2008). (Pubitemid 351220568)
115. Perry, C. A. & Annunziato, A. T. Influence of histone acetylation on the solubility, H1 content and DNase I sensitivity of newly assembled chromatin. Nucleic Acids Res. 17, 4275-4291 (1989). (Pubitemid 19153427)
116. Taddei, A., Maison, C., Roche, D. & Almouzni, G. Reversible disruption of pericentric heterochromatin and centromere function by inhibiting deacetylases. Nature Cell Biol. 3, 114-120 (2001). (Pubitemid 32118363)
117. Conti, C. et al. Inhibition of histone deacetylase in cancer cells slows down replication forks, activates dormant origins, and induces DNA damage. Cancer Res. 70, 4470-4480 (2010).
118. Bhaskara, S. et al. Hdac3 is essential for the maintenance of chromatin structure and genome stability. Cancer Cell 18, 436-447 (2010).
119. Sirbu, B. M. et al. Analysis of protein dynamics at active, stalled, and collapsed replication forks. Genes Dev. 25, 1320-1327 (2011).
120. Milutinovic, S., Zhuang, Q. & Szyf, M. Proliferating cell nuclear antigen associates with histone deacetylase activity, integrating DNA replication and chromatin modification. J. Biol. Chem. 277, 20974-20978 (2002). (Pubitemid 34967408)
121. Rowbotham, S. P. et al. Maintenance of silent chromatin through replication requires SWI/SNF-like chromatin remodeler SMARCAD1. Mol. Cell 42, 285-296 (2011).
122. Taddei, A., Roche, D., Sibarita, J. B., Turner, B. M. & Almouzni, G. Duplication and maintenance of heterochromatin domains. J. Cell Biol. 147, 1153-1166 (1999). (Pubitemid 30012803)
123. Lande-Diner, L., Zhang, J. & Cedar, H. Shifts in replication timing actively affect histone acetylation during nucleosome reassembly. Mol. Cell 34, 767-774 (2009).
124. Jones, P. A. & Liang, G. Rethinking how DNA methylation patterns are maintained. Nature Rev. Genet. 10, 805-811 (2009).
125. Egger, G. et al. Identification of DNMT1 (DNA methyltransferase 1) hypomorphs in somatic knockouts suggests an essential role for DNMT1 in cell survival. Proc. Natl Acad. Sci. USA 103, 14080-14085 (2006). (Pubitemid 44452983)
126. Schermelleh, L. et al. Dynamics of Dnmt1 interaction with the replication machinery and its role in postreplicative maintenance of DNA methylation. Nucleic Acids Res. 35, 4301-4312 (2007). (Pubitemid 47244584)
127. Wu, H. & Zhang, Y. Mechanisms and functions of Tet protein-mediated 5-methylcytosine oxidation. Genes Dev. 25, 2436-2452 (2011).
128. Poot, R. A. et al. The Williams syndrome transcription factor interacts with PCNA to target chromatin remodelling by ISWI to replication foci. Nature Cell Biol. 6, 1236-1244 (2004). (Pubitemid 39625123)
129. Scharf, A. N., Barth, T. K. & Imhof, A. Establishment of histone modifications after chromatin assembly. Nucleic Acids Res. 37, 5032-5040 (2009).
130. Xu, M., Wang, W., Chen, S. & Zhu, B. A model for mitotic inheritance of histone lysine methylation. EMBO Rep. 13, 60-67 (2011).
131. Esteve, P. O. et al. Direct interaction between DNMT1 and G9a coordinates DNA and histone methylation during replication. Genes Dev. 20, 3089-3103 (2006).
132. Sarraf, S. A. & Stancheva, I. Methyl-CpG binding protein MBD1 couples histone H3 methylation at lysine 9 by SETDB1 to DNA replication and chromatin assembly. Mol. Cell 15, 595-605 (2004). (Pubitemid 39141786)
133. Raynaud, C. et al. Two cell-cycle regulated SET-domain proteins interact with proliferating cell nuclear antigen (PCNA) in Arabidopsis. Plant J. 47, 395-407 (2006). (Pubitemid 44036408)
134. Jacob, Y. et al. Regulation of heterochromatic DNA replication by histone H3 lysine 27 methyltransferases. Nature 466, 987-991 (2010).
135. Zaratiegui, M. et al. RNAi promotes heterochromatic silencing through replication-coupled release of RNA Pol II. Nature 479, 135-138 (2011).
136. Li, F., Martienssen, R. & Cande, W. Z. Coordination of DNA replication and histone modification by the Rik1-Dos2 complex. Nature 475, 244-248 (2011).
137. Pesavento, J. J., Yang, H., Kelleher, N. L. & Mizzen, C. A. Certain and progressive methylation of histone H4 at lysine 20 during the cell cycle. Mol. Cell. Biol. 28, 468-486 (2008).
138. Lanzuolo, C., Lo Sardo, F., Diamantini, A. & Orlando, V. PcG complexes set the stage for epigenetic inheritance of gene silencing in early S phase before replication. PLoS Genet. 7, e1002370 (2011).
139. Dodd, I. B., Micheelsen, M. A., Sneppen, K. & Thon, G. Theoretical analysis of epigenetic cell memory by nucleosome modification. Cell 129, 813-822 (2007). (Pubitemid 46802381)
140. Aagaard, L. et al. Functional mammalian homologues of the Drosophila PEV-modifier Su(var)3-9 encode centromere-associated proteins which complex with the heterochromatin component M31. EMBO J. 18, 1923-1938 (1999). (Pubitemid 29158536)
141. Hansen, K. H. et al. A model for transmission of the H3K27me3 epigenetic mark. Nature Cell Biol. 10, 1291-1300 (2008).
142. Margueron, R. et al. Role of the polycomb protein EED in the propagation of repressive histone marks. Nature 461, 762-767 (2009).
143. De Vos, D. et al. Progressive methylation of ageing histones by Dot1 functions as a timer. EMBO Rep. 12, 956-962 (2011).
144. Sweet, S. M., Li, M., Thomas, P. M., Durbin, K. R. & Kelleher, N. L. Kinetics of re-establishing H3K79 methylation marks in global human chromatin. J. Biol. Chem. 285, 32778-32786 (2010).
145. Xu, G. L. et al. Chromosome instability and immunodeficiency syndrome caused by mutations in a DNA methyltransferase gene. Nature 402, 187-191 (1999).
146. Peters, A. H. et al. Loss of the Suv39h histone methyltransferases impairs mammalian heterochromatin and genome stability. Cell 107, 323-337 (2001). (Pubitemid 33049976)
147. Gaudet, F. et al. Induction of tumors in mice by genomic hypomethylation. Science 300, 489-492 (2003). (Pubitemid 36444330)
148. Hansen, K. D. et al. Increased methylation variation in epigenetic domains across cancer types. Nature Genet. 43, 768-775 (2011).
149. Fraga, M. F. et al. Loss of acetylation at Lys16 and trimethylation at Lys20 of histone H4 is a common hallmark of human cancer. Nature Genet. 37, 391-400 (2005).
150. Wen, B., Wu, H., Shinkai, Y., Irizarry, R. A. & Feinberg, A. P. Large histone H3 lysine 9 dimethylated chromatin blocks distinguish differentiated from embryonic stem cells. Nature Genet. 41, 246-250 (2009).
151. Clemente-Ruiz, M. & Prado, F. Chromatin assembly controls replication fork stability. EMBO Rep. 10, 790-796 (2009).
152. Myung, K., Pennaneach, V., Kats, E. S. & Kolodner, R. D. Saccharomyces cerevisiae chromatin-assembly factors that act during DNA replication function in the maintenance of genome stability. Proc. Natl Acad. Sci. USA 100, 6640-6645 (2003). (Pubitemid 36666634)
153. Prado, F., Cortes-Ledesma, F. & Aguilera, A. The absence of the yeast chromatin assembly factor Asf1 increases genomic instability and sister chromatid exchange. EMBO Rep. 5, 497-502 (2004). (Pubitemid 38745041)
154. Yang, J. H. & Freudenreich, C. H. The Rtt109 histone acetyltransferase facilitates error-free replication to prevent CAG/CTG repeat contractions. DNA Repair (Amst.) 9, 414-420 (2010).
155. Feser, J. et al. Elevated histone expression promotes life span extension. Mol. Cell 39, 724-735 (2010).
156. O'Sullivan, R. J., Kubicek, S., Schreiber, S. L. & Karlseder, J. Reduced histone biosynthesis and chromatin changes arising from a damage signal at telomeres. Nature Struct. Mol. Biol. 17, 1218-1225 (2010).
157. Sanchez-Molina, S. et al. Role for hACF1 in the G2/M damage checkpoint. Nucleic Acids Res. 39, 8445-8456 (2011).
158. Bester, A. C. et al. Nucleotide deficiency promotes genomic instability in early stages of cancer development. Cell 145, 435-446 (2011).
159. Sarkies, P., Reams, C., Simpson, L. J. & Sale, J. E. Epigenetic instability due to defective replication of structured DNA. Mol. Cell 40, 703-713 (2010).
160. Nyce, J., Liu, L. & Jones, P. A. Variable effects of DNA-synthesis inhibitors upon DNA methylation in mammalian cells. Nucleic Acids Res. 14, 4353-4367 (1986). (Pubitemid 17189635)
161. Lopes, M., Foiani, M. & Sogo, J. M. Multiple mechanisms control chromosome integrity after replication fork uncoupling and restart at irreparable UV lesions. Mol. Cell 21, 15-27 (2006). (Pubitemid 43017845)
162. Daigaku, Y., Davies, A. A. & Ulrich, H. D. Ubiquitin-dependent DNA damage bypass is separable from genome replication. Nature 465, 951-955 (2010).
163. Polo, S. E., Roche, D. & Almouzni, G. New histone incorporation marks sites of UV repair in human cells. Cell 127, 481-493 (2006). (Pubitemid 44647423)
164. Singh, G. & Klar, A. J. Mutations in deoxyribonucleotide biosynthesis pathway cause spreading of silencing across heterochromatic barriers at the mating-type region of the fission yeast. Yeast 25, 117-128 (2008). (Pubitemid 351279441)
165. Zaratiegui, M. et al. CENP-B preserves genome integrity at replication forks paused by retrotransposon LTR. Nature 469, 112-115 (2011).
166. Dubarry, M., Loiodice, I., Chen, C. L., Thermes, C. & Taddei, A. Tight protein-DNA interactions favor gene silencing. Genes Dev. 25, 1365-1370 (2011).
167. Saveliev, A., Everett, C., Sharpe, T., Webster, Z. & Festenstein, R. DNA triplet repeats mediate heterochromatin-protein-1-sensitive variegated gene silencing. Nature 422, 909-913 (2003). (Pubitemid 36520045)
168. Mirkin, S. M. Expandable DNA repeats and human disease. Nature 447, 932-940 (2007). (Pubitemid 46975760)
169. Di Micco, R. et al. Interplay between oncogene-induced DNA damage response and heterochromatin in senescence and cancer. Nature Cell Biol. 13, 292-302 (2011).
170. Shimada, K. et al. Ino80 chromatin remodeling complex promotes recovery of stalled replication forks. Curr. Biol. 18, 566-575 (2008).
171. Falbo, K. B. et al. Involvement of a chromatin remodeling complex in damage tolerance during DNA replication. Nature Struct. Mol. Biol. 16, 1167-1172 (2009).
172. Papamichos-Chronakis, M. & Peterson, C. L. The Ino80 chromatin-remodeling enzyme regulates replisome function and stability. Nature Struct. Mol. Biol. 15, 338-345 (2008). (Pubitemid 351483399)
173. O'Donnell, L. et al. The MMS22L-TONSL complex mediates recovery from replication stress and homologous recombination. Mol. Cell 40, 619-631 (2010).
174. O'Connell, B. C. et al. A genome-wide camptothecin sensitivity screen identifies a mammalian MMS22L-NFKBIL2 complex required for genomic stability. Mol. Cell 40, 645-657 (2010).
175. Piwko, W. et al. RNAi-based screening identifies the Mms22L-Nfkbil2 complex as a novel regulator of DNA replication in human cells. EMBO J. 29, 4210-4222 (2010).
176. Takeda, S. et al. BRU1, a novel link between responses to DNA damage and epigenetic gene silencing in Arabidopsis. Genes Dev. 18, 782-793 (2004). (Pubitemid 38480890)
177. Kliszczak, A. E., Rainey, M. D., Harhen, M., Boisvert, F. M. & Santocanale, C. DNA mediated chromatin pull-down for the study of chromatin replication. Scientific Reports 1, 95 (2011).
178. Bochman, M. L. & Schwacha, A. The Mcm complex: unwinding the mechanism of a replicative helicase. Microbiol. Mol. Biol. Rev. 73, 652-683 (2009).
179. Costa, A. et al. The structural basis for MCM2-7 helicase activation by GINS and Cdc45. Nature Struct. Mol. Biol. 18, 471-477 (2011).
180. Fu, Y. V. et al. Selective bypass of a lagging strand roadblock by the eukaryotic replicative DNA helicase. Cell 146, 931-941 (2011).
181. Errico, A. & Costanzo, V. Differences in the DNA replication of unicellular eukaryotes and metazoans: known unknowns. EMBO Rep. 11, 270-278 (2010).
182. Pak, D. T. et al. Association of the origin recognition complex with heterochromatin and HP1 in higher eukaryotes. Cell 91, 311-323 (1997). (Pubitemid 27467962)
183. Prasanth, S. G., Shen, Z., Prasanth, K. V. & Stillman, B. Human origin recognition complex is essential for HP1 binding to chromatin and heterochromatin organization. Proc. Natl Acad. Sci. USA 107, 15093-15098 (2010).
184. Triolo, T. & Sternglanz, R. Role of interactions between the origin recognition complex and SIR1 in transcriptional silencing. Nature 381, 251-253 (1996). (Pubitemid 26148036)
185. Iizuka, M. & Stillman, B. Histone acetyltransferase HBO1 interacts with the ORC1 subunit of the human initiator protein. J. Biol. Chem. 274, 23027-23034 (1999).
186. Burke, T. W., Cook, J. G., Asano, M. & Nevins, J. R. Replication factors MCM2 and ORC1 interact with the histone acetyltransferase HBO1. J. Biol. Chem. 276, 15397-15408 (2001).
187. Shen, Z. et al. A WD-repeat protein stabilizes ORC binding to chromatin. Mol. Cell 40, 99-111 (2010).
188. Dhar, S. K. et al. Replication from oriP of Epstein-Barr virus requires human ORC and is inhibited by geminin. Cell 106, 287-296 (2001). (Pubitemid 32772613)
189. Li, P. C., Chretien, L., Cote, J., Kelly, T. J. & Forsburg, S. L. S. pombe replication protein Cdc18 (Cdc6) interacts with Swi6 (HP1) heterochromatin protein: region specific effects and replication timing in the centromere. Cell Cycle 10, 323-336 (2011).
190. Doyon, Y. et al. ING tumor suppressor proteins are critical regulators of chromatin acetylation required for genome expression and perpetuation. Mol. Cell 21, 51-64 (2006). (Pubitemid 43017848)
191. Ryu, M. J. et al. Direct interaction between cohesin complex and DNA replication machinery. Biochem. Biophys. Res. Commun. 341, 770-775 (2006).
192. Franco, A. A., Lam, W. M., Burgers, P. M. & Kaufman, P. D. Histone deposition protein Asf1 maintains DNA replisome integrity and interacts with replication factor C. Genes Dev. 19, 1365-1375 (2005). (Pubitemid 41003025)
193. Chuang, L. S. et al. Human DNA-(cytosine-5) methyltransferase-PCNA complex as a target for p21WAF1. Science 277, 1996-2000 (1997). (Pubitemid 27449142)
194. Shumaker, D. K. et al. The highly conserved nuclear lamin Ig-fold binds to PCNA: its role in DNA replication. J. Cell Biol. 181, 269-280 (2008). (Pubitemid 351574552)
195. Moldovan, G. L., Pfander, B. & Jentsch, S. PCNA controls establishment of sister chromatid cohesion during S phase. Mol. Cell 23, 723-732 (2006). (Pubitemid 44292556)
196. Huen, M. S., Sy, S. M., van Deursen, J. M. & Chen, J. Direct interaction between SET8 and proliferating cell nuclear antigen couples H4K20 methylation with DNA replication. J. Biol. Chem. 283, 11073-11077 (2008).
197. Jorgensen, S. et al. The histone methyltransferase SET8 is required for S-phase progression. J. Cell Biol. 179, 1337-1345 (2007).
198. Liang, Z., Diamond, M., Smith, J. A., Schnell, M. & Daniel, R. Proliferating cell nuclear antigen is required for loading of the SMCX/KMD5C histone demethylase onto chromatin. Epigenetics Chromatin 4, 18 (2011).
199. Hasan, S., Hassa, P. O., Imhof, R. & Hottiger, M. O. Transcription coactivator p300 binds PCNA and may have a role in DNA repair synthesis. Nature 410, 387-391 (2001). (Pubitemid 32246058)
200. Hasan, S. et al. Regulation of human flap endonuclease1 activity by acetylation through the transcriptional coactivator p300. Mol. Cell 7, 1221-1231 (2001). (Pubitemid 32607356)
201. Balakrishnan, L., Stewart, J., Polaczek, P., Campbell, J. L. & Bambara, R. A. Acetylation of Dna2 endonuclease/helicase and flap endonuclease 1 by p300 promotes DNA stability by creating long flap intermediates. J. Biol. Chem. 285, 4398-4404 (2010).