H3K4me3 demethylation by the histone demethylase KDM5C/JARID1C promotes DNA replication origin firing

Nucleic Acids Research

Volumn 43, Issue 5, 2015, Pages 2560-2574

  Rondinelli, Beatrice ^a,b,d   Schwerer, Hélène ^c   Antonini, Elena ^a   Gaviraghi, Marco ^a,b   Lupi, Alessio ^a,b   Frenquelli, Michela ^a   Cittaro, Davide ^a   Segalla, Simona ^a   Lemaitre, Jean Marc ^c   Tonon, Giovanni ^a  

^a SAN RAFFAELE HOSPITAL   (Italy)

^b VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

^c UNIV MONTPELLIER   (France)

^d DANA FARBER CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE DEMETHYLASE; HISTONE H3; HISTONE H4; PROTEIN JARID1C; UNCLASSIFIED DRUG; CDC45 PROTEIN, HUMAN; CELL CYCLE PROTEIN; CHROMATIN; CYCLINE; HISTONE; KDM5C PROTEIN, HUMAN; LYSINE; N DEMETHYLASE; PROTEIN BINDING;

ACETYLATION; ARTICLE; BINDING AFFINITY; CHROMATIN; CONTROLLED STUDY; DNA REPLICATION; DNA SYNTHESIS; DOWN REGULATION; ENZYME ACTIVITY; HISTONE DEMETHYLATION; HISTONE METHYLATION; PRIORITY JOURNAL; PROTEIN DEPLETION; S PHASE CELL CYCLE CHECKPOINT; CELL CYCLE; DNA REPLICATION ORIGIN; GENETICS; HELA CELL LINE; HUMAN; IMMUNOBLOTTING; METABOLISM; METHYLATION; RNA INTERFERENCE; TIME FACTOR;

MAMMALIA;

CELL CYCLE; CELL CYCLE PROTEINS; CHROMATIN; DNA REPLICATION; HELA CELLS; HISTONES; HUMANS; IMMUNOBLOTTING; LYSINE; METHYLATION; OXIDOREDUCTASES, N-DEMETHYLATING; PROLIFERATING CELL NUCLEAR ANTIGEN; PROTEIN BINDING; REPLICATION ORIGIN; RNA INTERFERENCE; TIME FACTORS;

EID: 84937557285     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv090     Document Type: Article

References (74)

1. Sclafani, R. A. and Holzen, T. M. (2007) Cell cycle regulation of DNA replication. Annu. Rev. Genet., 41, 237-280.
2. Bell, S. P. and Dutta, A. (2002) DNA replication in eukaryotic cells. Annu. Rev. Biochem., 71, 333-374.
3. Mendez, J. and Stillman, B. (2000) Chromatin association of human origin recognition complex, cdc6, and minichromosome maintenance proteins during the cell cycle: assembly of prereplication complexes in late mitosis. Mol. Cell. Biol., 0, 8602-8612.
4. Prasanth, S. G., Mendez, J., Prasanth, K. V. and Stillman, B. (2004) Dynamics of pre-replication complex proteins during the cell division cycle. Philos. Trans. R. Soc. Lond. B Biol. Sci., 359, 7-16.
5. Boos, D., Sanchez-Pulido, L., Rappas, M., Pearl, L. H., Oliver, A. W., Ponting, C. P. and Diffley, J. F. (2011) Regulation of DNA replication through Sld3-Dpb11 interaction is conserved from yeast to humans. Curr. Biol., 21, 1152-1157.
6. Zou, L. and Stillman, B. (2000) Assembly of a complex containing Cdc45p, replication protein A, and Mcm2p at replication origins controlled by S-phase cyclin-dependent kinases and Cdc7p-Dbf4p kinase. Mol. Cell. Biol., 20, 3086-3096.
7. Zou, L. and Stillman, B. (1998) Formation of a preinitiation complex by S-phase cyclin CDK-dependent loading of Cdc45p onto chromatin. Science, 280, 593-596.
8. Hashimoto, Y. and Takisawa, H. (2003) Xenopus Cut5 is essential for a CDK-dependent process in the initiation of DNA replication. EMBO J., 22, 2526-2535.
9. Kubota, Y., Takase, Y., Komori, Y., Hashimoto, Y., Arata, T., Kamimura, Y., Araki, H. and Takisawa, H. (2003) A novel ring-like complex of Xenopus proteins essential for the initiation of DNA replication. Genes Dev., 17, 1141-1152.
10. Aparicio, T., Guillou, E., Coloma, J., Montoya, G. and Mendez, J. (2009) The human GINS complex associates with Cdc45 and MCM and is essential for DNA replication. Nucleic Acids Res., 37, 2087-2095.
11. Kanemaki, M. and Labib, K. (2006) Distinct roles for Sld3 and GINS during establishment and progression of eukaryotic DNA replication forks. EMBO J., 25, 1753-1763.
12. Prelich, G. and Stillman, B. (1988) Coordinated leading and lagging strand synthesis during SV40 DNA replication in vitro requires PCNA. Cell, 53, 117-126.
13. Prelich, G., Tan, C. K., Kostura, M., Mathews, M. B., So, A. G., Downey, K. M. and Stillman, B. (1987) Functional identity of proliferating cell nuclear antigen and a DNA polymerase-delta auxiliary protein. Nature, 326, 517-520.
14. Moldovan, G. L., Pfander, B. and Jentsch, S. (2007) PCNA, the maestro of the replication fork. Cell, 129, 665-679.
15. Mechali, M. (2010) Eukaryotic DNA replication origins: many choices for appropriate answers. Nat. Rev. Mol. Cell Biol., 11, 728-738.
16. Vogelauer, M., Rubbi, L., Lucas, I., Brewer, B. J. and Grunstein, M. (2002) Histone acetylation regulates the time of replication origin firing. Mol. Cell, 10, 1223-1233.
17. 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.
18. Fangman, W. L. and Brewer, B. J. (1992) A question of time: replication origins of eukaryotic chromosomes. Cell, 71, 363-366.
19. Kennedy, B. K., Barbie, D. A., Classon, M., Dyson, N. and Harlow, E. (2000) Nuclear organization of DNA replication in primary mammalian cells. Genes Dev., 14, 2855-2868.
20. Simpson, R. T. (1990) Nucleosome positioning can affect the function of a cis-acting DNA element in vivo. Nature, 343, 387-389.
21. Berbenetz, N. M., Nislow, C. and Brown, G. W. (2010) Diversity of eukaryotic DNA replication origins revealed by genome-wide analysis of chromatin structure. PLoS Genet., 6, e1001092.
22. Crampton, A., Chang, F., Pappas, D. L. Jr., Frisch, R. L. and Weinreich, M. (2008) An ARS element inhibits DNA replication through a SIR2-dependent mechanism. Mol. Cell, 30, 156-166.
23. Aggarwal, B. D. and Calvi, B. R. (2004) Chromatin regulates origin activity in Drosophila follicle cells. Nature, 430, 372-376.
24. Unnikrishnan, A., Gafken, P. R. and Tsukiyama, T. (2010) Dynamic changes in histone acetylation regulate origins of DNA replication. Nat. Struct. Mol. Biol., 17, 430-437.
25. Pryde, F., Jain, D., Kerr, A., Curley, R., Mariotti, F. R. and Vogelauer, M. (2009) H3 k36 methylation helps determine the timing of cdc45 association with replication origins. PLoS One, 4, e5882.
26. Tardat, M., Murr, R., Herceg, Z., Sardet, C. and Julien, E. (2007) PR-Set7-dependent lysine methylation ensures genome replication and stability through S phase. J. Cell Biol, 179, 1413-1426.
27. Tardat, M., Brustel, J., Kirsh, O., Lefevbre, C., Callanan, M., Sardet, C. and Julien, E. (2010) The histone H4 Lys 20 methyltransferase PR-Set7 regulates replication origins in mammalian cells. Nat. Cell Biol, 12, 1086-1093.
28. Jenuwein, T. and Allis, C. D. (2001) Translating the histone code. Science, 293, 1074-1080.
29. Rizzardi, L. F., Dorn, E. S., Strahl, B. D. and Cook, J. G. (2012) DNA replication origin function is promoted by H3K4 di-methylation in Saccharomyces cerevisiae. Genetics, 192, 371-384.
30. Costas, C., de la Paz Sanchez, M., Stroud, H., Yu, Y., Oliveros, J. C., Feng, S., Benguria, A., Lopez-Vidriero, I., Zhang, X., Solano, R. et al (2011) Genome-wide mapping of Arabidopsis thaliana origins of DNA replication and their associated epigenetic marks. Nat. Struct. Mol Biol, 18, 395-400.
31. Valenzuela, M. S., Chen, Y, Davis, S., Yang, F., Walker, R. L., Bilke, S., Lueders, J., Martin, M. M., Aladjem, M. I., Massion, PP et al. (2011) Preferential localization of human origins of DNA replication at the 5'-ends of expressed genes and at evolutionarily conserved DNA sequences. PLoS One, 6, e17308.
32. Radman-Livaja, M., Liu, C. L., Friedman, N., Schreiber, S. L. and Rando, O. J. (2010) Replication and active demethylation represent partially overlapping mechanisms for erasure of H3K4me3 in budding yeast. PLoS Genet., 6, e1000837.
33. Kooistra, S. M. and Helin, K. (2012) Molecular mechanisms and potential functions of histone demethylases. Nat. Rev. Mol. Cell Biol, 13, 297-311.
34. Iwase, S., Lan, F., Bayliss, P., de la Torre-Ubieta, L., Huarte, M., Qi, H. H., Whetstine, J. R., Bonni, A., Roberts, TM. and Shi, Y (2007) The X-linked mental retardation gene SMCX/JARID1C defines a family of histone H3 lysine 4 demethylases. Cell, 128, 1077-1088.
35. Chen, Z., Zang, J., Whetstine, J., Hong, X., Davrazou, F., Kutateladze, TG., Simpson, M., Mao, Q., Pan, C. H., Dai, S. et al. (2006) Structural insights into histone demethylation by JMJD2 family members. Cell, 125, 691-702.
36. Wilsker, D., Patsialou, A., Dallas, PB. and Moran, E. (2002) ARID proteins: a diverse family of DNA binding proteins implicated in the control of cell growth, differentiation, and development. Cell Growth Differ, 13, 95-106.
37. Wu, J., Ellison, J., Salido, E., Yen, P., Mohandas, T and Shapiro, L. J. (1994) Isolation and characterization of XE169, a novel human gene that escapes X-inactivation. Hum. Mol. Genet., 3, 153-160.
38. Jensen, L. R., Amende, M., Gurok, U., Moser, B., Gimmel, V., Tzschach, A., Janecke, A. R., Tariverdian, G., Chelly, J., Fryns, J. P et al. (2005) Mutations in the JARID1C gene, which is involved in transcriptional regulation and chromatin remodeling, cause X-linked mental retardation. Am. J. Hum. Genet., 76, 227-236.
39. Rujirabanjerd, S., Nelson, J., Tarpey, PS., Hackett, A., Edkins, S., Raymond, FL., Schwartz, C. E., Turner, G., Iwase, S., Shi, Y et al. (2010) Identification and characterization of two novel JARID1C mutations: suggestion of an emerging genotype-phenotype correlation. Eur. J. Hum. Genet., 18, 330-335.
40. Tahiliani, M., Mei, P, Fang, R., Leonor, T., Rutenberg, M., Shimizu, F, Li, J., Rao, A. and Shi, Y (2007) The histone H3K4 demethylase SMCX links REST target genes to X-linked mental retardation. Nature, 447, 601-605.
41. Alabert, C, Bukowski-Wills, J. C., Lee, S. B., Kustatscher, G., Nakamura, K., de Lima Alves, F., Menard, P., Mejlvang, J., Rappsilber, J. and Groth, A. (2014) Nascent chromatin capture proteomics determines chromatin dynamics during DNA replication and identifies unknown fork components. Nat. Cell Biol., 16, 281-293.
42. Liang, Z., Diamond, M., Smith, J. A., Schnell, M. and Daniel, R. (2011) Proliferating cell nuclear antigen is required for loading of the SMCX/KMD5C histone demethylase onto chromatin. Epigenet. Chromatin, 4, 18.
43. Groth, A., Corpet, A., Cook, A. J., Roche, D., Bartek, J., Lukas, J. and Almouzni, G (2007) Regulation of replication fork progression through histone supply and demand. Science, 318, 1928-1931.
44. Prieur, A., Besnard, E., Babled, A. and Lemaitre, J. M. (2011) p53 and p16 (INK4A) independent induction of senescence by chromatin-dependent alteration of S-phase progression. Nat. Commun., 2, 473.
45. Cabianca, D. S., Casa, V., Bodega, B., Xynos, A., Ginelli, E., Tanaka, Y. and Gabellini, D. (2012) A long ncRNA links copy number variation to a polycomb/trithorax epigenetic switch in FSHD muscular dystrophy. Cell, 149, 819-831.
46. Bellelli, R., Castellone, M. D., Guida, T., Limongello, R., Dathan, N. A., Merolla, F., Cirafici, A. M., Affuso, A., Masai, H., Costanzo, V. et al. (2014) NCOA4 transcriptional coactivator inhibits activation of DNA replication origins. Mol. Cell, 55, 123-137.
47. Ryba, T., Battaglia, D., Pope, B. D., Hiratani, I. and Gilbert, D. M. (2011) Genome-scale analysis of replication timing: from bench to bioinformatics. Nat. Protoc., 6, 870-895.
48. Ernst, J., Kheradpour, P., Mikkelsen, T. S., Shoresh, N., Ward, L. D., Epstein, C. B., Zhang, X., Wang, L., Issner, R., Coyne, M. et al. (2011) Mapping and analysis of chromatin state dynamics in nine human cell types. Nature, 473, 43-49.
49. Li, H. and Durbin, R. (2010) Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics, 26, 589-595.
50. Walworth, N. C. (2000) Cell-cycle checkpoint kinases: checking in on the cell cycle. Curr. Opin. Cell Biol., 12, 697-704.
51. Falck, J., Mailand, N., Syljuasen, R. G., Bartek, J. and Lukas, J. (2001) The ATM-Chk2-Cdc25A checkpoint pathway guards against radioresistant DNA synthesis. Nature, 410, 842-847.
52. Mailand, N., Falck, J., Lukas, C., Syljuasen, R. G., Welcker, M., Bartek, J. and Lukas, J. (2000) Rapid destruction of human Cdc25A in response to DNA damage. Science, 288, 1425-1429.
53. Feijoo, C., Hall-Jackson, C., Wu, R., Jenkins, D., Leitch, J., Gilbert, D. M. and Smythe, C. (2001) Activation of mammalian Chk1 during DNA replication arrest: a role for Chk1 in the intra-S phase checkpoint monitoring replication origin firing. J Cell Biol, 154, 913-923.
54. Sarkaria, J. N., Busby, E. C., Tibbetts, R. S., Roos, P., Taya, Y., Karnitz, L. M. and Abraham, R. T. (1999) Inhibition of ATM and ATR kinase activities by the radiosensitizing agent, caffeine. Cancer Res., 59, 4375-4382.
55. Nakayasu, H. and Berezney, R. (1989) Mapping replicational sites in the eucaryotic cell nucleus. J. Cell Biol., 108, 1-11.
56. Michalet, X., Ekong, R., Fougerousse, F., Rousseaux, S., Schurra, C., Hornigold, N., van Slegtenhorst, M., Wolfe, J., Povey, S., Beckmann, J. S. et al. (1997) Dynamic molecular combing: stretching the whole human genome for high-resolution studies. Science, 277, 1518-1523.
57. Maya-Mendoza, A., Petermann, E., Gillespie, D. A., Caldecott, K. W. and Jackson, D. A. (2007) Chk1 regulates the density of active replication origins during the vertebrate S phase. EMBO J., 26, 2719-2731.
58. Gibson, D. G., Bell, S. P. and Aparicio, O. M. (2006) Cell cycle execution point analysis of ORC function and characterization of the checkpoint response to ORC inactivation in Saccharomyces cerevisiae. Genes Cells, 11, 557-573.
59. Lengronne, A. and Schwob, E. (2002) The yeast CDK inhibitor Sic1 prevents genomic instability by promoting replication origin licensing in late G (1). Mol. Cell, 9, 1067-1078.
60. Goren, A., Tabib, A., Hecht, M. and Cedar, H. (2008) DNA replication timing of the human beta-globin domain is controlled by histone modification at the origin. Genes Dev., 22, 1319-1324.
61. Miotto, B. and Struhl, K. (2008) HBO1 histone acetylase is a coactivator of the replication licensing factor Cdt1. Genes Dev., 22, 2633-2638.
62. 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.
63. Shreeram, S., Sparks, A., Lane, D. P. and Blow, J. J. (2002) Cell type-specific responses of human cells to inhibition of replication licensing. Oncogene, 21, 6624-6632.
64. Machida, Y. J., Teer, J. K. and Dutta, A. (2005) Acute reduction of an origin recognition complex (ORC) subunit in human cells reveals a requirement of ORC for Cdk2 activation. J. Biol. Chem., 280, 27624-27630.
65. Feng, D., Tu, Z., Wu, W. and Liang, C. (2003) Inhibiting the expression of DNA replication-initiation proteins induces apoptosis in human cancer cells. Cancer Res., 63, 7356-7364.
66. Boos, D., Yekezare, M. and Diffley, J. F. (2013) Identification of a heteromeric complex that promotes DNA replication origin fring in human cells. Science, 340, 981-984.
67. Sansam, C. L., Cruz, N. M., Danielian, P. S., Amsterdam, A., Lau, M. L., Hopkins, N. and Lees, J. A. (2010) A vertebrate gene, ticrr, is an essential checkpoint and replication regulator. Genes Dev., 24, 183-194.
68. Mills, A. A. (2010) Throwing the cancer switch: reciprocal roles of polycomb and trithorax proteins. Nat. Rev. Cancer, 10, 669-682.
69. Calo, E. and Wysocka, J. (2013) Modification of enhancer chromatin: what, how, and why? Mol. Cell, 49, 825-837.
70. Brown, S. J., Stoilov, P. and Xing, Y. (2012) Chromatin and epigenetic regulation of pre-mRNA processing. Hum. Mol. Genet., 21, R90-R96.
71. Ryan, R. J. and Bernstein, B. E. (2012) Molecular biology. Genetic events that shape the cancer epigenome. Science, 336, 1513-1514.
72. Groth, A., Rocha, W., Verreault, A. and Almouzni, G. (2007) Chromatin challenges during DNA replication and repair. Cell, 128, 721-733.
73. Huen, M. S., Sy, S. M., van Deursen, J. M. and Chen, J. (2008) Direct interaction between SET8 and proliferating cell nuclear antigen couples H4-K20 methylation with DNA replication. J. Biol. Chem., 283, 11073-11077.
74. Liu, H., Takeda, S., Kumar, R., Westergard, T. D., Brown, E. J., Pandita, T. K., Cheng, E. H. and Hsieh, J. J. (2010) Phosphorylation of MLL by ATR is required for execution of mammalian S-phase checkpoint. Nature, 467, 343-346.