Methylation of Histone H3 on Lysine 79 Associates with a Group of Replication Origins and Helps Limit DNA Replication Once per Cell Cycle

PLoS Genetics

Volumn 9, Issue 6, 2013, Pages

  Fu, Haiqing ^a   Maunakea, Alika K ^b   Martin, Melvenia M ^a   Huang, Liang ^a   Zhang, Ya ^a   Ryan, Michael ^c   Kim, RyangGuk ^c   Lin, Chii Meil ^a   Zhao, Keji ^b   Aladjem, Mirit I ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^c In Silico Solutions   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEMOGLOBIN BETA CHAIN; HISTONE H3; HISTONE H3 LYSINE 79; HISTONE LYSINE METHYLTRANSFERASE; NUCLEAR PROTEIN; PROTEIN DOT1L; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE REGULATION; CELL CYCLE S PHASE; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CHROMATIN; COMBINATORIAL CHEMISTRY; CONTROLLED STUDY; DNA HISTONE INTERACTION; DNA REPLICATION; DNA SEQUENCE; GENE CONTROL; GENE FREQUENCY; GENETIC ASSOCIATION; GENOME ANALYSIS; GENOMIC INSTABILITY; HISTONE METHYLATION; HUMAN; HUMAN CELL; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION;

CELL CYCLE; CHROMATIN; DNA REPLICATION; GENOME, HUMAN; GENOMIC INSTABILITY; HISTONE DEMETHYLASES; HISTONES; HUMANS; METHYLATION; METHYLTRANSFERASES; REPLICATION ORIGIN; S PHASE;

MAMMALIA;

EID: 84879610545     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003542     Document Type: Article

References (51)

1. Gomez M, Brockdorff N, (2004) Heterochromatin on the inactive X chromosome delays replication timing without affecting origin usage. Proc Natl Acad Sci U S A 101: 6923-6928.
2. Antequera F, (2004) Genomic specification and epigenetic regulation of eukaryotic DNA replication origins. EMBO J 23: 4365-4370.
3. Martin MM, Ryan M, Kim R, Zakas AL, Fu H, et al. (2011) Genome-wide depletion of replication initiation events in highly transcribed regions. Genome Res 21: 1822-32.
4. Besnard E, Babled A, Lapasset L, Milhavet O, Parrinello H, et al. (2012) Unraveling cell type-specific and reprogrammable human replication origin signatures associated with G-quadruplex consensus motifs. Nat Struct Mol Biol 19: 837-844.
5. Cayrou C, Coulombe P, Vigneron A, Stanojcic S, Ganier O, 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.
6. Aladjem MI, (2007) Replication in context: dynamic regulation of DNA replication patterns in metazoans. Nat Rev Genet 8: 588-600.
7. Mechali M, (2010) Eukaryotic DNA replication origins: many choices for appropriate answers. Nat Rev Mol Cell Biol 11: 728-738.
8. Aladjem MI, Groudine M, Brody LL, Dieken ES, Fournier RE, et al. (1995) Participation of the human beta-globin locus control region in initiation of DNA replication. Science 270: 815-819.
9. Kalejta RF, Li X, Mesner LD, Dijkwel PA, Lin HB, et al. (1998) Distal sequences, but not ori-beta/OBR-1, are essential for initiation of DNA replication in the Chinese hamster DHFR origin. Molecular Cell 2: 797-806.
10. Hayashida T, Oda M, Ohsawa K, Yamaguchi A, Hosozawa T, et al. (2006) Replication initiation from a novel origin identified in the Th2 cytokine cluster locus requires a distant conserved noncoding sequence. J Immunol 176: 5446-5454.
11. Feng YQ, Desprat R, Fu H, Olivier E, Lin CM, et al. (2006) DNA methylation supports intrinsic epigenetic memory in mammalian cells. PLoS Genet 2: e65.
12. Huang L, Fu H, Lin CM, Conner AL, Zhang Y, et al. (2011) Prevention of transcriptional silencing by a replicator-binding complex consisting of SWI/SNF, MeCP1, and hnRNP C1/C2. Mol Cell Biol 31: 3472-3484.
13. Ryba T, Hiratani I, Lu J, Itoh M, Kulik M, et al. (2010) Evolutionarily conserved replication timing profiles predict long-range chromatin interactions and distinguish closely related cell types. Genome Res 20: 761-770.
14. Gilbert DM, (2012) Replication origins run (ultra) deep. Nat Struct Mol Biol 19: 740-742.
15. Lacoste N, Utley RT, Hunter JM, Poirier GG, Cote J, (2002) Disruptor of telomeric silencing-1 is a chromatin-specific histone H3 methyltransferase. J Biol Chem 277: 30421-30424.
16. Frederiks F, Tzouros M, Oudgenoeg G, van Welsem T, Fornerod M, et al. (2008) Nonprocessive methylation by Dot1 leads to functional redundancy of histone H3K79 methylation states. Nat Struct Mol Biol 15: 550-557.
17. Schulze JM, Jackson J, Nakanishi S, Gardner JM, Hentrich T, et al. (2009) Linking cell cycle to histone modifications: SBF and H2B monoubiquitination machinery and cell-cycle regulation of H3K79 dimethylation. Mol Cell 35: 626-641.
18. Zhou H, Madden BJ, Muddiman DC, Zhang Z, (2006) Chromatin assembly factor 1 interacts with histone H3 methylated at lysine 79 in the processes of epigenetic silencing and DNA repair. Biochemistry 45: 2852-2861.
19. Im H, Park C, Feng Q, Johnson KD, Kiekhaefer CM, et al. (2003) Dynamic regulation of histone H3 methylated at lysine 79 within a tissue-specific chromatin domain. J Biol Chem 278: 18346-18352.
20. Mohan M, Herz HM, Takahashi YH, Lin C, Lai KC, et al. (2010) Linking H3K79 trimethylation to Wnt signaling through a novel Dot1-containing complex (DotCom). Genes Dev 24: 574-589.
21. Jones B, Su H, Bhat A, Lei H, Bajko J, et al. (2008) The histone H3K79 methyltransferase Dot1L is essential for mammalian development and heterochromatin structure. PLoS Genet 4: e1000190.
22. Onder TT, Kara N, Cherry A, Sinha AU, Zhu N, et al. (2012) Chromatin-modifying enzymes as modulators of reprogramming. Nature 483: 598-602.
23. Giannattasio M, Lazzaro F, Plevani P, Muzi-Falconi M, (2005) The DNA damage checkpoint response requires histone H2B ubiquitination by Rad6-Bre1 and H3 methylation by Dot1. J Biol Chem 280: 9879-9886.
24. Huyen Y, Zgheib O, Ditullio RA Jr, Gorgoulis VG, Zacharatos P, et al. (2004) Methylated lysine 79 of histone H3 targets 53BP1 to DNA double-strand breaks. Nature 432: 406-411.
25. Tatum D, Li S, (2011) Evidence that the histone methyltransferase Dot1 mediates global genomic repair by methylating histone H3 on lysine 79. J Biol Chem 286: 17530-17535.
26. Jacinto FV, Ballestar E, Esteller M, (2009) Impaired recruitment of the histone methyltransferase DOT1L contributes to the incomplete reactivation of tumor suppressor genes upon DNA demethylation. Oncogene 28: 4212-4224.
27. Bernt KM, Zhu N, Sinha AU, Vempati S, Faber J, et al. (2011) MLL-Rearranged Leukemia Is Dependent on Aberrant H3K79 Methylation by DOT1L. Cancer Cell 20: 66-78.
28. Chang MJ, Wu H, Achille NJ, Reisenauer MR, Chou CW, et al. (2011) Histone H3 lysine 79 methyltransferase Dot1 is required for immortalization by MLL oncogenes. Cancer Res 70: 10234-10242.
29. Wang P, Lin C, Smith ER, Guo H, Sanderson BW, et al. (2009) Global analysis of H3K4 methylation defines MLL family member targets and points to a role for MLL1-mediated H3K4 methylation in the regulation of transcriptional initiation by RNA polymerase II. Mol Cell Biol 29: 6074-6085.
30. Okada Y, Feng Q, Lin Y, Jiang Q, Li Y, et al. (2005) hDOT1L links histone methylation to leukemogenesis. Cell 121: 167-178.
31. Aladjem MI, Rodewald LW, Kolman JL, Wahl GM, (1998) Genetic dissection of a mammalian replicator in the human beta-globin locus. Science 281: 1005-1009.
32. Kitsberg D, Selig S, Keshet I, Cedar H, (1993) Replication structure of the human beta-globin gene domain. Nature 366: 588-590.
33. Wang L, Lin CM, Brooks S, Cimbora D, Groudine M, et al. (2004) The human beta-globin replication initiation region consists of two modular independent replicators. Mol Cell Biol 24: 3373-3386.
34. Wang L, Lin CM, Lopreiato JO, Aladjem MI, (2006) Cooperative sequence modules determine replication initiation sites at the human beta-globin locus. Hum Mol Genet 15: 2613-2622.
35. Forrester WC, Epner E, Driscoll MC, Enver T, Brice M, et al. (1990) A deletion of the human beta-globin locus activation region causes a major alteration in chromatin structure and replication across the entire beta-globin locus. Genes Dev 4: 1637-1649.
36. Groudine M, Kohwi-Shigematsu T, Gelinas R, Stamatoyannopoulos G, Papayannopoulou T, (1983) Human fetal to adult hemoglobin switching: changes in chromatin structure of the beta-globin gene locus. Proc Natl Acad Sci U S A 80: 7551-7555.
37. Fu H, Wang L, Lin CM, Singhania S, Bouhassira EE, et al. (2006) Preventing gene silencing with human replicators. Nat Biotechnol 24: 572-576.
38. Tardat M, Brustel J, Kirsh O, Lefevbre C, Callanan M, et al. (2010) The histone H4 Lys 20 methyltransferase PR-Set7 regulates replication origins in mammalian cells. Nat Cell Biol 12: 1086-1093.
39. Dellino GI, Cittaro D, Piccioni R, Luzi L, Banfi S, et al. (2013) Genome-wide mapping of human DNA-replication origins: levels of transcription at ORC1 sites regulate origin selection and replication timing. Genome Res 23: 1-11.
40. Kuo AJ, Song J, Cheung P, Ishibe-Murakami S, Yamazoe S, et al. (2012) The BAH domain of ORC1 links H4K20me2 to DNA replication licensing and Meier-Gorlin syndrome. Nature 484: 115-119.
41. Klose RJ, Gardner KE, Liang G, Erdjument-Bromage H, Tempst P, et al. (2007) Demethylation of histone H3K36 and H3K9 by Rph1: a vestige of an H3K9 methylation system in Saccharomyces cerevisiae? Mol Cell Biol 27: 3951-3961.
42. Arias EE, Walter JC, (2007) Strength in numbers: preventing rereplication via multiple mechanisms in eukaryotic cells. Genes Dev 21: 497-518.
43. DePamphilis ML, Blow JJ, Ghosh S, Saha T, Noguchi K, et al. (2006) Regulating the licensing of DNA replication origins in metazoa. Curr Opin Cell Biol 18: 231-239.
44. Gassen A, Brechtefeld D, Schandry N, Arteaga-Salas JM, Israel L, et al. (2012) DOT1A-dependent H3K76 methylation is required for replication regulation in Trypanosoma brucei. Nucleic Acids Res 40: 10302-10311.
45. Raynaud C, Sozzani R, Glab N, Domenichini S, Perennes C, et al. (2006) Two cell-cycle regulated SET-domain proteins interact with proliferating cell nuclear antigen (PCNA) in Arabidopsis. Plant J 47: 395-407.
46. Jacob Y, Stroud H, Leblanc C, Feng S, Zhuo L, et al. (2010) Regulation of heterochromatic DNA replication by histone H3 lysine 27 methyltransferases. Nature 466: 987-991.
47. Conti C, Caburet S, Schurra C, Bensimon A, (2001) Molecular combing. Curr Protoc Cytom Chapter 8: Unit 8 10.
48. Conti C, Leo E, Eichler GS, Sordet O, Martin MM, et al. (2010) Inhibition of histone deacetylase in cancer cells slows down replication forks, activates dormant origins, and induces DNA damage. Cancer Res 70: 4470-4480.
49. Langmead B, Schatz MC, Lin J, Pop M, Salzberg SL, (2009) Searching for SNPs with cloud computing. Genome Biol 10: R134.
50. Robinson JT, Thorvaldsdottir H, Winckler W, Guttman M, Lander ES, et al. (2011) Integrative genomics viewer. Nat Biotechnol 29: 24-26.
51. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B, (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5: 621-628.