Cdt1-binding protein GRWD1 is a novel histone-binding protein that facilitates MCM loading through its influence on chromatin architecture

Nucleic Acids Research

Volumn 43, Issue 12, 2015, Pages 5898-5911

  Sugimoto, Nozomi ^a   Maehara, Kazumitsu ^b   Yoshida, Kazumasa ^a   Yasukouchi, Shuhei ^a   Osano, Satoko ^c   Watanabe, Shinya ^a   Aizawa, Masahiro ^a   Yugawa, Takashi ^c   Kiyono, Tohru ^c   Kurumizaka, Hitoshi ^d   Ohkawa, Yasuyuki ^b   Fujita, Masatoshi ^a  

^a KYUSHU UNIVERSITY   (Japan)

^b KYUSHU UNIVERSITY   (Japan)

^c NATIONAL CANCER CENTER RESEARCH INSTITUTE   (Japan)

^d WASEDA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; CELL CYCLE PROTEIN 6; GLUTAMATE RICH WD40 REPEAT CONTAINING 1 BINDING PROTEIN; MINICHROMOSOME MAINTENANCE PROTEIN; REPLICATION LICENSING FACTOR CDT1; UNCLASSIFIED DRUG; CARRIER PROTEIN; CDC6 PROTEIN, HUMAN; CDT1 PROTEIN, HUMAN; CELL CYCLE PROTEIN; CHROMATIN; GRWD1 PROTEIN, HUMAN; HISTONE; LAMIN B; LAMIN B2; MCM4 PROTEIN, HUMAN; MINICHROMOSOME MAINTENANCE PROTEIN 4; NUCLEAR PROTEIN;

ARTICLE; CELL CYCLE G1 PHASE; CHROMATIN IMMUNOPRECIPITATION; CHROMATIN STRUCTURE; CONTROLLED STUDY; HIGH THROUGHPUT SEQUENCING; HUMAN; HUMAN CELL; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REGULATORY MECHANISM; CELL CYCLE; CELL NUCLEUS; CHEMISTRY; CHROMATIN; DNA REPLICATION; DNA REPLICATION ORIGIN; GENETICS; HEK293 CELL LINE; HELA CELL LINE; METABOLISM; PHYSIOLOGY;

CARRIER PROTEINS; CELL CYCLE; CELL CYCLE PROTEINS; CELL NUCLEUS; CHROMATIN; DNA REPLICATION; HEK293 CELLS; HELA CELLS; HISTONES; HUMANS; LAMIN TYPE B; MINICHROMOSOME MAINTENANCE COMPLEX COMPONENT 4; MINICHROMOSOME MAINTENANCE PROTEINS; NUCLEAR PROTEINS; REPLICATION ORIGIN;

EID: 84942155704     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv509     Document Type: Article

References (98)

1. Arias, E.E. and Walter, J.C. (2007) Strength in numbers: preventing rereplication via multiple mechanisms in eukaryotic cells. Genes Dev., 21, 497-518.
2. Diffley, J.F. (2004) Regulation of early events in chromosome replication. Curr. Biol., 14, R778-R786.
3. Masai, H., Matsumoto, S., You, Z., Yoshizawa-Sugata, N. and Oda, M. (2010) Eukaryotic chromosome DNA replication: Where, when, and how? Annu. Rev. Biochem., 79, 89-130.
4. Sugimoto, N., Yoshida, K., Tatsumi, Y., Yugawa, T., Narisawa-Saito, M., Waga, S., Kiyono, T. and Fujita, M. (2009) Redundant and differential regulation of multiple licensing factors ensures prevention of re-replication in normal human cells. J. Cell. Sci., 122, 1184-1191.
5. Vaziri, C., Saxena, S., Jeon, Y., Lee, C., Murata, K., Machida, Y., Wagle, N., Hwang, D.S. and Dutta, A. (2003) A p53-dependent checkpoint pathway prevents rereplication. Mol. Cell, 11, 997-1008.
6. Sugimoto, N., Kitabayashi, I., Osano, S., Tatsumi, Y., Yugawa, T., Narisawa-Saito, M., Matsukage, A., Kiyono, T. and Fujita, M. (2008) Identification of novel human Cdt1-binding proteins by a proteomics approach: proteolytic regulation by APC/CCdh1. Mol. Biol. Cell, 19, 1007-1021.
7. Ge, X.Q., Jackson, D.A. and Blow, J.J. (2007) Dormant origins licensed by excess Mcm2-7 are required for human cells to survive replicative stress. Genes Dev., 21, 3331-3341.
8. Tsao, C.C., Geisen, C. and Abraham, R.T. (2004) Interaction between human MCM7 and Rad17 proteins is required for replication checkpoint signaling. Embo j., 23, 4660-4669.
9. Woodward, A.M., Gohler, T., Luciani, M.G., Oehlmann, M., Ge, X., Gartner, A., Jackson, D.A. and Blow, J.J. (2006) Excess Mcm2-7 license dormant origins of replication that can be used under conditions of replicative stress. J. Cell Biol., 173, 673-683.
10. Shima, N., Alcaraz, A., Liachko, I., Buske, T.R., Andrews, C.A., Munroe, R.J., Hartford, S.A., Tye, B.K. and Schimenti, J.C. (2007) A viable allele of Mcm4 causes chromosome instability and mammary adenocarcinomas in mice. Nat. Genet., 39, 93-98.
11. Pruitt, S.C., Bailey, K.J. and Freeland, A. (2007) Reduced Mcm2 expression results in severe stem/progenitor cell deficiency and cancer. Stem Cells, 25, 3121-3132.
12. Iizuka, M., Matsui, T., Takisawa, H. and Smith, M.M. (2006) Regulation of replication licensing by acetyltransferase Hbo1. Mol. Cell. Biol., 26, 1098-1108.
13. Miotto, B. and Struhl, K. (2008) HBO1 histone acetylase is a coactivator of the replication licensing factor Cdt1. Genes Dev., 22, 2633-2638.
14. Miotto, B. and Struhl, K. (2010) HBO1 histone acetylase activity is essential for DNA replication licensing and inhibited by geminin. Mol. Cell, 37, 57-66.
15. Sugimoto, N., Yugawa, T., Iizuka, M., Kiyono, T. and Fujita, M. (2011) Chromatin remodeler sucrose nonfermenting 2 homolog (SNF2H) is recruited onto DNA replication origins through interaction with Cdc10 protein-dependent transcript 1 (Cdt1) and promotes pre-replication complex formation. J. Biol. Chem., 286, 39200-39210.
16. Burgess, R.J. and Zhang, Z. (2013) Histone chaperones in nucleosome assembly and human disease. Nat. Struct. Mol. Biol., 20, 14-22.
17. De Koning, L., Corpet, A., Haber, J.E. and Almouzni, G. (2007) Histone chaperones: an escort network regulating histone traffic. Nat. Struct. Mol. Biol., 14, 997-1007.
18. Gratenstein, K., Heggestad, A.D., Fortun, J., Notterpek, L., Pestov, D.G. and Fletcher, B.S. (2005) The WD-repeat protein GRWD1: potential roles in myeloid differentiation and ribosome biogenesis. Genomics, 85, 762-773.
19. Iouk, T.L., Aitchison, J.D., Maguire, S. and Wozniak, R.W. (2001) Rrb1p, a yeast nuclear WD-repeat protein involved in the regulation of ribosome biosynthesis. Mol. Cell. Biol., 21, 1260-1271.
20. Killian, A., Le Meur, N., Sesboue, R., Bourguignon, J., Bougeard, G., Gautherot, J., Bastard, C., Frebourg, T. and Flaman, J.M. (2004) Inactivation of the RRB1-pescadillo pathway involved in ribosome biogenesis induces chromosomal instability. Oncogene, 23, 8597-8602.
21. Schaper, S., Fromont-Racine, M., Linder, P., de la Cruz, J., Namane, A. and Yaniv, M. (2001) A yeast homolog of chromatin assembly factor 1 is involved in early ribosome assembly. Curr. Biol., 11, 1885-1890.
22. Du, Y.C. and Stillman, B. (2002) Yph1p, an ORC-interacting protein: potential links between cell proliferation control, DNA replication, and ribosome biogenesis. Cell, 109, 835-848.
23. He, Y.J., McCall, C.M., Hu, J., Zeng, Y. and Xiong, Y. (2006) DDB1 functions as a linker to recruit receptor WD40 proteins to CUL4-ROC1 ubiquitin ligases. Genes Dev., 20, 2949-2954.
24. Higa, L.A., Wu, M., Ye, T., Kobayashi, R., Sun, H. and Zhang, H. (2006) CUL4-DDB1 ubiquitin ligase interacts with multiple WD40-repeat proteins and regulates histone methylation. Nat. Cell Biol., 8, 1277-1283.
25. Harada, A., Okada, S., Konno, D., Odawara, J., Yoshimi, T., Yoshimura, S., Kumamaru, H., Saiwai, H., Tsubota, T., Kurumizaka, H. et al. (2012) Chd2 interacts with H3.3 to determine myogenic cell fate. Embo j., 31, 2994-3007.
26. Maehara, K., Odawara, J., Harada, A., Yoshimi, T., Nagao, K., Obuse, C., Akashi, K., Tachibana, T., Sakata, T. and Ohkawa, Y. (2013) A co-localization model of paired ChIP-seq data using a large ENCODE data set enables comparison of multiple samples. Nucleic Acids Res., 41, 54-62.
27. Mortazavi, A., Williams, B.A., McCue, K., Schaeffer, L. and Wold, B. (2008) Mapping and quantifying mammalian transcriptomes by RNA-seq. Nat. Methods, 5, 621-628.
28. Yoshida, K., Sugimoto, N., Iwahori, S., Yugawa, T., Narisawa-Saito, M., Kiyono, T. and Fujita, M. (2010) CDC6 interaction with ATR regulates activation of a replication checkpoint in higher eukaryotic cells. J. Cell. Sci., 123, 225-235.
29. Hiraiwa, A., Fujita, M., Nagasaka, T., Adachi, A., Ohashi, M. and Ishibashi, M. (1997) Immunolocalization of hCDC47 protein in normal and neoplastic human tissues and its relation to growth. Int. J. Cancer, 74, 180-184.
30. Tatsumi, Y., Sugimoto, N., Yugawa, T., Narisawa-Saito, M., Kiyono, T. and Fujita, M. (2006) Deregulation of Cdt1 induces chromosomal damage without rereplication and leads to chromosomal instability. J. Cell. Sci., 119, 3128-3140.
31. Williams, G.H., Romanowski, P., Morris, L., Madine, M., Mills, A.D., Stoeber, K., Marr, J., Laskey, R.A. and Coleman, N. (1998) Improved cervical smear assessment using antibodies against proteins that regulate DNA replication. Proc. Natl. Acad. Sci. U.S.A., 95, 14932-14937.
32. Sato, K., Ishiai, M., Toda, K., Furukoshi, S., Osakabe, A., Tachiwana, H., Takizawa, Y., Kagawa, W., Kitao, H., Dohmae, N. et al. (2012) Histone chaperone activity of fanconi anemia proteins, FANCD2 and FANCI, is required for DNA crosslink repair. EMBO J., 31, 3524-3536.
33. Tachiwana, H., Osakabe, A., Kimura, H. and Kurumizaka, H. (2008) Nucleosome formation with the testis-specific histone H3 variant, H3t, by human nucleosome assembly proteins in vitro. Nucleic Acids Res., 36, 2208-2218.
34. Cayrou, C., Coulombe, P., Vigneron, A., Stanojcic, S., Ganier, O., Peiffer, I., Rivals, E., Puy, A., Laurent-Chabalier, S., Desprat, R. et al. (2011) Genome-scale analysis of metazoan replication origins reveals their organization in specific but flexible sites defined by conserved features. Genome Res., 21, 1438-1449.
35. Karnani, N., Taylor, C.M., Malhotra, A. and Dutta, A. (2010) Genomic study of replication initiation in human chromosomes reveals the influence of transcription regulation and chromatin structure on origin selection. Mol. Biol. Cell, 21, 393-404.
36. MacAlpine, H.K., Gordan, R., Powell, S.K., Hartemink, A.J. and MacAlpine, D.M. (2010) Drosophila ORC localizes to open chromatin and marks sites of cohesin complex loading. Genome Res., 20, 201-211.
37. Papior, P., Arteaga-Salas, J.M., Gunther, T., Grundhoff, A. and Schepers, A. (2012) Open chromatin structures regulate the efficiencies of pre-RC formation and replication initiation in epstein-barr virus. J. Cell Biol., 198, 509-528.
38. Sequeira-Mendes, J., Diaz-Uriarte, R., Apedaile, A., Huntley, D., Brockdorff, N. and Gomez, M. (2009) Transcription initiation activity sets replication origin efficiency in mammalian cells. PLoS Genet., 5, e1000446.
39. Besnard, E., Babled, A., Lapasset, L., Milhavet, O., Parrinello, H., Dantec, C., Marin, J.M. and Lemaitre, J.M. (2012) Unraveling cell type-specific and reprogrammable human replication origin signatures associated with G-quadruplex consensus motifs. Nat. Struct. Mol. Biol., 19, 837-844.
40. Norio, P. and Schildkraut, C.L. (2001) Visualization of DNA replication on individual epstein-barr virus episomes. Science, 294, 2361-2364.
41. Norio, P. and Schildkraut, C.L. (2004) Plasticity of DNA replication initiation in epstein-barr virus episomes. PLoS Biol., 2, e152.
42. Giresi, P.G., Kim, J., McDaniell, R.M., Iyer, V.R. and Lieb, J.D. (2007) FAIRE (formaldehyde-assisted isolation of regulatory elements) isolates active regulatory elements from human chromatin. Genome Res., 17, 877-885.
43. Simon, J.M., Giresi, P.G., Davis, I.J. and Lieb, J.D. (2012) Using formaldehyde-assisted isolation of regulatory elements (FAIRE) to isolate active regulatory DNA. Nat. Protoc., 7, 256-267.
44. Song, L., Zhang, Z., Grasfeder, L.L., Boyle, A.P., Giresi, P.G., Lee, B.K., Sheffield, N.C., Graf, S., Huss, M., Keefe, D. et al. (2011) Open chromatin defined by DNaseI and FAIRE identifies regulatory elements that shape cell-type identity. Genome Res., 21, 1757-1767.
45. Yoshida, K., Bacal, J., Desmarais, D., Padioleau, I., Tsaponina, O., Chabes, A., Pantesco, V., Dubois, E., Parrinello, H., Skrzypczak, M. et al. (2014) The histone deacetylases sir2 and rpd3 act on ribosomal DNA to control the replication program in budding yeast. Mol. Cell, 54, 691-697.
46. Beall, E.L., Manak, J.R., Zhou, S., Bell, M., Lipsick, J.S. and Botchan, M.R. (2002) Role for a drosophila myb-containing protein complex in site-specific DNA replication. Nature, 420, 833-837.
47. Bosco, G., Du, W. and Orr-Weaver, T.L. (2001) DNA replication control through interaction of E2F-RB and the origin recognition complex. Nat. Cell Biol., 3, 289-295.
48. Dominguez-Sola, D., Ying, C.Y., Grandori, C., Ruggiero, L., Chen, B., Li, M., Galloway, D.A., Gu, W., Gautier, J. and Dalla-Favera, R. (2007) Non-transcriptional control of DNA replication by c-myc. Nature, 448, 445-451.
49. Shen, Z., Sathyan, K.M., Geng, Y., Zheng, R., Chakraborty, A., Freeman, B., Wang, F., Prasanth, K.V. and Prasanth, S.G. (2010) A WD-repeat protein stabilizes ORC binding to chromatin. Mol. Cell, 40, 99-111.
50. Arias, E.E. and Walter, J.C. (2007) Strength in numbers: preventing rereplication via multiple mechanisms in eukaryotic cells. Genes Dev., 21, 497-518.
51. Diffley, J.F. (2004) Regulation of early events in chromosome replication. Curr. Biol., 14, R778-R786.
52. Masai, H., Matsumoto, S., You, Z., Yoshizawa-Sugata, N. and Oda, M. (2010) Eukaryotic chromosome DNA replication: Where, when, and how? Annu. Rev. Biochem., 79, 89-130.
53. Sugimoto, N., Yoshida, K., Tatsumi, Y., Yugawa, T., Narisawa-Saito, M., Waga, S., Kiyono, T. and Fujita, M. (2009) Redundant and differential regulation of multiple licensing factors ensures prevention of re-replication in normal human cells. J. Cell. Sci., 122, 1184-1191.
54. Vaziri, C., Saxena, S., Jeon, Y., Lee, C., Murata, K., Machida, Y., Wagle, N., Hwang, D.S. and Dutta, A. (2003) A p53-dependent checkpoint pathway prevents rereplication. Mol. Cell, 11, 997-1008.
55. Sugimoto, N., Kitabayashi, I., Osano, S., Tatsumi, Y., Yugawa, T., Narisawa-Saito, M., Matsukage, A., Kiyono, T. and Fujita, M. (2008) Identification of novel human Cdt1-binding proteins by a proteomics approach: proteolytic regulation by APC/CCdh1. Mol. Biol. Cell, 19, 1007-1021.
56. Ge, X.Q., Jackson, D.A. and Blow, J.J. (2007) Dormant origins licensed by excess Mcm2-7 are required for human cells to survive replicative stress. Genes Dev., 21, 3331-3341.
57. Tsao, C.C., Geisen, C. and Abraham, R.T. (2004) Interaction between human MCM7 and Rad17 proteins is required for replication checkpoint signaling. Embo j., 23, 4660-4669.
58. Woodward, A.M., Gohler, T., Luciani, M.G., Oehlmann, M., Ge, X., Gartner, A., Jackson, D.A. and Blow, J.J. (2006) Excess Mcm2-7 license dormant origins of replication that can be used under conditions of replicative stress. J. Cell Biol., 173, 673-683.
59. Shima, N., Alcaraz, A., Liachko, I., Buske, T.R., Andrews, C.A., Munroe, R.J., Hartford, S.A., Tye, B.K. and Schimenti, J.C. (2007) A viable allele of Mcm4 causes chromosome instability and mammary adenocarcinomas in mice. Nat. Genet., 39, 93-98.
60. Pruitt, S.C., Bailey, K.J. and Freeland, A. (2007) Reduced Mcm2 expression results in severe stem/progenitor cell deficiency and cancer. Stem Cells, 25, 3121-3132.
61. Iizuka, M., Matsui, T., Takisawa, H. and Smith, M.M. (2006) Regulation of replication licensing by acetyltransferase Hbo1. Mol. Cell. Biol., 26, 1098-1108.
62. Miotto, B. and Struhl, K. (2008) HBO1 histone acetylase is a coactivator of the replication licensing factor Cdt1. Genes Dev., 22, 2633-2638.
63. Miotto, B. and Struhl, K. (2010) HBO1 histone acetylase activity is essential for DNA replication licensing and inhibited by geminin. Mol. Cell, 37, 57-66.
64. Sugimoto, N., Yugawa, T., Iizuka, M., Kiyono, T. and Fujita, M. (2011) Chromatin remodeler sucrose nonfermenting 2 homolog (SNF2H) is recruited onto DNA replication origins through interaction with Cdc10 protein-dependent transcript 1 (Cdt1) and promotes pre-replication complex formation. J. Biol. Chem., 286, 39200-39210.
65. Burgess, R.J. and Zhang, Z. (2013) Histone chaperones in nucleosome assembly and human disease. Nat. Struct. Mol. Biol., 20, 14-22.
66. De Koning, L., Corpet, A., Haber, J.E. and Almouzni, G. (2007) Histone chaperones: an escort network regulating histone traffic. Nat. Struct. Mol. Biol., 14, 997-1007.
67. Gratenstein, K., Heggestad, A.D., Fortun, J., Notterpek, L., Pestov, D.G. and Fletcher, B.S. (2005) The WD-repeat protein GRWD1: potential roles in myeloid differentiation and ribosome biogenesis. Genomics, 85, 762-773.
68. Iouk, T.L., Aitchison, J.D., Maguire, S. and Wozniak, R.W. (2001) Rrb1p, a yeast nuclear WD-repeat protein involved in the regulation of ribosome biosynthesis. Mol. Cell. Biol., 21, 1260-1271.
69. Killian, A., Le Meur, N., Sesboue, R., Bourguignon, J., Bougeard, G., Gautherot, J., Bastard, C., Frebourg, T. and Flaman, J.M. (2004) Inactivation of the RRB1-pescadillo pathway involved in ribosome biogenesis induces chromosomal instability. Oncogene, 23, 8597-8602.
70. Schaper, S., Fromont-Racine, M., Linder, P., de la Cruz, J., Namane, A. and Yaniv, M. (2001) A yeast homolog of chromatin assembly factor 1 is involved in early ribosome assembly. Curr. Biol., 11, 1885-1890.
71. Du, Y.C. and Stillman, B. (2002) Yph1p, an ORC-interacting protein: potential links between cell proliferation control, DNA replication, and ribosome biogenesis. Cell, 109, 835-848.
72. He, Y.J., McCall, C.M., Hu, J., Zeng, Y. and Xiong, Y. (2006) DDB1 functions as a linker to recruit receptor WD40 proteins to CUL4-ROC1 ubiquitin ligases. Genes Dev., 20, 2949-2954.
73. Higa, L.A., Wu, M., Ye, T., Kobayashi, R., Sun, H. and Zhang, H. (2006) CUL4-DDB1 ubiquitin ligase interacts with multiple WD40-repeat proteins and regulates histone methylation. Nat. Cell Biol., 8, 1277-1283.
74. Harada, A., Okada, S., Konno, D., Odawara, J., Yoshimi, T., Yoshimura, S., Kumamaru, H., Saiwai, H., Tsubota, T., Kurumizaka, H. et al. (2012) Chd2 interacts with H3.3 to determine myogenic cell fate. Embo j., 31, 2994-3007.
75. Maehara, K., Odawara, J., Harada, A., Yoshimi, T., Nagao, K., Obuse, C., Akashi, K., Tachibana, T., Sakata, T. and Ohkawa, Y. (2013) A co-localization model of paired ChIP-seq data using a large ENCODE data set enables comparison of multiple samples. Nucleic Acids Res., 41, 54-62.
76. Mortazavi, A., Williams, B.A., McCue, K., Schaeffer, L. and Wold, B. (2008) Mapping and quantifying mammalian transcriptomes by RNA-seq. Nat. Methods, 5, 621-628.
77. Yoshida, K., Sugimoto, N., Iwahori, S., Yugawa, T., Narisawa-Saito, M., Kiyono, T. and Fujita, M. (2010) CDC6 interaction with ATR regulates activation of a replication checkpoint in higher eukaryotic cells. J. Cell. Sci., 123, 225-235.
78. Hiraiwa, A., Fujita, M., Nagasaka, T., Adachi, A., Ohashi, M. and Ishibashi, M. (1997) Immunolocalization of hCDC47 protein in normal and neoplastic human tissues and its relation to growth. Int. J. Cancer, 74, 180-184.
79. Tatsumi, Y., Sugimoto, N., Yugawa, T., Narisawa-Saito, M., Kiyono, T. and Fujita, M. (2006) Deregulation of Cdt1 induces chromosomal damage without rereplication and leads to chromosomal instability. J. Cell. Sci., 119, 3128-3140.
80. Williams, G.H., Romanowski, P., Morris, L., Madine, M., Mills, A.D., Stoeber, K., Marr, J., Laskey, R.A. and Coleman, N. (1998) Improved cervical smear assessment using antibodies against proteins that regulate DNA replication. Proc. Natl. Acad. Sci. U.S.A., 95, 14932-14937.
81. Sato, K., Ishiai, M., Toda, K., Furukoshi, S., Osakabe, A., Tachiwana, H., Takizawa, Y., Kagawa, W., Kitao, H., Dohmae, N. et al. (2012) Histone chaperone activity of fanconi anemia proteins, FANCD2 and FANCI, is required for DNA crosslink repair. EMBO J., 31, 3524-3536.
82. Tachiwana, H., Osakabe, A., Kimura, H. and Kurumizaka, H. (2008) Nucleosome formation with the testis-specific histone H3 variant, H3t, by human nucleosome assembly proteins in vitro. Nucleic Acids Res., 36, 2208-2218.
83. Cayrou, C., Coulombe, P., Vigneron, A., Stanojcic, S., Ganier, O., Peiffer, I., Rivals, E., Puy, A., Laurent-Chabalier, S., Desprat, R. et al. (2011) Genome-scale analysis of metazoan replication origins reveals their organization in specific but flexible sites defined by conserved features. Genome Res., 21, 1438-1449.
84. Karnani, N., Taylor, C.M., Malhotra, A. and Dutta, A. (2010) Genomic study of replication initiation in human chromosomes reveals the influence of transcription regulation and chromatin structure on origin selection. Mol. Biol. Cell, 21, 393-404.
85. MacAlpine, H.K., Gordan, R., Powell, S.K., Hartemink, A.J. and MacAlpine, D.M. (2010) Drosophila ORC localizes to open chromatin and marks sites of cohesin complex loading. Genome Res., 20, 201-211.
86. Papior, P., Arteaga-Salas, J.M., Gunther, T., Grundhoff, A. and Schepers, A. (2012) Open chromatin structures regulate the efficiencies of pre-RC formation and replication initiation in epstein-barr virus. J. Cell Biol., 198, 509-528.
87. Sequeira-Mendes, J., Diaz-Uriarte, R., Apedaile, A., Huntley, D., Brockdorff, N. and Gomez, M. (2009) Transcription initiation activity sets replication origin efficiency in mammalian cells. PLoS Genet., 5, e1000446.
88. Besnard, E., Babled, A., Lapasset, L., Milhavet, O., Parrinello, H., Dantec, C., Marin, J.M. and Lemaitre, J.M. (2012) Unraveling cell type-specific and reprogrammable human replication origin signatures associated with G-quadruplex consensus motifs. Nat. Struct. Mol. Biol., 19, 837-844.
89. Norio, P. and Schildkraut, C.L. (2001) Visualization of DNA replication on individual epstein-barr virus episomes. Science, 294, 2361-2364.
90. Norio, P. and Schildkraut, C.L. (2004) Plasticity of DNA replication initiation in epstein-barr virus episomes. PLoS Biol., 2, e152.
91. Giresi, P.G., Kim, J., McDaniell, R.M., Iyer, V.R. and Lieb, J.D. (2007) FAIRE (formaldehyde-assisted isolation of regulatory elements) isolates active regulatory elements from human chromatin. Genome Res., 17, 877-885.
92. Simon, J.M., Giresi, P.G., Davis, I.J. and Lieb, J.D. (2012) Using formaldehyde-assisted isolation of regulatory elements (FAIRE) to isolate active regulatory DNA. Nat. Protoc., 7, 256-267.
93. Song, L., Zhang, Z., Grasfeder, L.L., Boyle, A.P., Giresi, P.G., Lee, B.K., Sheffield, N.C., Graf, S., Huss, M., Keefe, D. et al. (2011) Open chromatin defined by DNaseI and FAIRE identifies regulatory elements that shape cell-type identity. Genome Res., 21, 1757-1767.
94. Yoshida, K., Bacal, J., Desmarais, D., Padioleau, I., Tsaponina, O., Chabes, A., Pantesco, V., Dubois, E., Parrinello, H., Skrzypczak, M. et al. (2014) The histone deacetylases sir2 and rpd3 act on ribosomal DNA to control the replication program in budding yeast. Mol. Cell, 54, 691-697.
95. Beall, E.L., Manak, J.R., Zhou, S., Bell, M., Lipsick, J.S. and Botchan, M.R. (2002) Role for a drosophila myb-containing protein complex in site-specific DNA replication. Nature, 420, 833-837.
96. Bosco, G., Du, W. and Orr-Weaver, T.L. (2001) DNA replication control through interaction of E2F-RB and the origin recognition complex. Nat. Cell Biol., 3, 289-295.
97. Dominguez-Sola, D., Ying, C.Y., Grandori, C., Ruggiero, L., Chen, B., Li, M., Galloway, D.A., Gu, W., Gautier, J. and Dalla-Favera, R. (2007) Non-transcriptional control of DNA replication by c-myc. Nature, 448, 445-451.
98. Shen, Z., Sathyan, K.M., Geng, Y., Zheng, R., Chakraborty, A., Freeman, B., Wang, F., Prasanth, K.V. and Prasanth, S.G. (2010) A WD-repeat protein stabilizes ORC binding to chromatin. Mol. Cell, 40, 99-111.