Dynamic changes in the genomic localization of DNA replication-related element binding factor during the cell cycle

Cell Cycle

Volumn 12, Issue 10, 2013, Pages 1605-1615

  Gurudatta, B V ^a   Yang, Jingping ^a   Van Bortle, Kevin ^a   Donlin Asp, Paul G ^a   Corces, Victor G ^a  

^a EMORY UNIVERSITY   (United States)

Author keywords

Cell cycle; Chromatin; Epigenetics; Mitosis; Replication; Transcription

Indexed keywords

BOUNDARY ELEMENT ASSOCIATED FACTOR 32; CENTROSOMAL PROTEIN 190; DNA BINDING PROTEIN; DNA REPLICATION RELATED ELEMENT BINDING FACTOR; DROSOPHILA PROTEIN; TRANSCRIPTION FACTOR CTCF; UNCLASSIFIED DRUG; BEAF-32 PROTEIN, DROSOPHILA; CHROMATIN; CP190 PROTEIN, DROSOPHILA; DREF PROTEIN, DROSOPHILA; EYE PROTEIN; MCM2 PROTEIN, DROSOPHILA; MICROTUBULE ASSOCIATED PROTEIN; MINICHROMOSOME MAINTENANCE PROTEIN; NUCLEAR PROTEIN; ORC2 PROTEIN, DROSOPHILA; ORIGIN RECOGNITION COMPLEX; TRANSCRIPTION FACTOR;

ARTICLE; CELL CYCLE; CELL GROWTH; CELL PROLIFERATION; CHROMATIN; CHROMOSOME STRUCTURE; CONTROLLED STUDY; DNA REPLICATION; DROSOPHILA; GENE LOCATION; INSULATOR ELEMENT; INTERPHASE; MITOSIS; NONHUMAN; PROTEIN BINDING; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; ANIMAL; CELL CULTURE; GENETICS; GENOME; METABOLISM; MUTATION;

ANIMALS; CELL PROLIFERATION; CELLS, CULTURED; CHROMATIN; DNA-BINDING PROTEINS; DROSOPHILA; DROSOPHILA PROTEINS; EYE PROTEINS; GENOME; INSULATOR ELEMENTS; INTERPHASE; MICROTUBULE-ASSOCIATED PROTEINS; MINICHROMOSOME MAINTENANCE PROTEINS; MITOSIS; MUTATION; NUCLEAR PROTEINS; ORIGIN RECOGNITION COMPLEX; TRANSCRIPTION FACTORS;

EID: 84877934795     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.24742     Document Type: Article

References (63)

1. Matsukage A, Hirose F, Yoo MA, Yamaguchi M. The DRE/DREF transcriptional regulatory system: a master key for cell proliferation. Biochim Biophys Acta 2008; 1779:81-9; PMID:18155677; http://dx.doi.org/10.1016/j.bbagrm.2007.11.011
2. Hochheimer A, Tjian R. Diversified transcription initiation complexes expand promoter selectivity and tissuespecific gene expression. Genes Dev 2003; 17:1309-20; PMID:12782648; http://dx.doi.org/10.1101/gad.1099903
3. Isogai Y, Keles S, Prestel M, Hochheimer A, Tjian R. Transcription of histone gene cluster by differential core-promoter factors. Genes Dev 2007; 21:2936-49; PMID:17978101; http://dx.doi.org/10.1101/gad.1608807
4. Hirose F, Yamaguchi M, Matsukage A. Targeted expression of the DNA binding domain of DRE-binding factor, a Drosophila transcription factor, attenuates DNA replication of the salivary gland and eye imaginal disc. Mol Cell Biol 1999; 19:6020-8; PMID:10454549
5. Hyun J, Jasper H, Bohmann D. DREF is required for efficient growth and cell cycle progression in Drosophila imaginal discs. Mol Cell Biol 2005; 25:5590-8; PMID:15964814; http://dx.doi.org/10.1128/MCB.25.13.5590-5598.2005
6. Hirose F, Yamaguchi M, Handa H, Inomata Y, Matsukage A. Novel 8-base pair sequence (Drosophila DNA replication-related element) and specific binding factor involved in the expression of Drosophila genes for DNA polymerase alpha and proliferating cell nuclear antigen. J Biol Chem 1993; 268:2092-9; PMID:8093616
7. Yamaguchi M, Hayashi Y, Nishimoto Y, Hirose F, Matsukage A. A nucleotide sequence essential for the function of DRE, a common promoter element for Drosophila DNa replication-related genes. J Biol Chem 1995; 270:15808-14; PMID:7797583; http://dx.doi.org/10.1074/jbc.270.26.15808
8. Sawado T, Hirose F, Takahashi Y, Sasaki T, Shinomiya T, Sakaguchi K, et al. The DNA replication-related element (DRE)/DRE-binding factor system is a transcriptional regulator of the Drosophila E2F gene. J Biol Chem 1998; 273:26042-51; PMID:9748283; http://dx.doi.org/10.1074/jbc.273.40.26042
9. Ohno K, Hirose F, Sakaguchi K, Nishida Y, Matsukage A. Transcriptional regulation of the Drosophila CycA gene by the DNA replication-related element (DRE) and DRE binding factor (DREF). Nucleic Acids Res 1996; 24:3942-6; PMID:8918795; http://dx.doi.org/10.1093/nar/24.20.3942
10. Nakamura K, Ida H, Yamaguchi M. Transcriptional regulation of the Drosophila moira and osa genes by the DREF pathway. Nucleic Acids Res 2008; 36:3905-15; PMID:18511465; http://dx.doi.org/10.1093/nar/gkn291
11. Park JS, Kim YS, Kim JG, Lee SH, Park SY, Yamaguchi M, et al. Regulation of the Drosophila p38b gene by transcription factor DREF in the adult midgut. Biochim Biophys Acta 2010; 1799:510-9; PMID:20346429; http://dx.doi.org/10.1016/ j.bbagrm.2010.03.001
12. Trong-Tue N, Thao DT, Yamaguchi M. Role of DREF in transcriptional regulation of the Drosophila p53 gene. Oncogene 2010; 29:2060-9; PMID:20101238; http://dx.doi.org/10.1038/onc.2009.483
13. Yoshida H, Kwon E, Hirose F, Otsuki K, Yamada M, Yamaguchi M. DREF is required for EGFR signalling during Drosophila wing vein development. Genes Cells 2004; 9:935-44; PMID:15461664; http://dx.doi.org/10.1111/j.1365-2443.2004. 00775.x
14. Phillips JE, Corces VG. CTCF: master weaver of the genome. Cell 2009; 137:1194-211; PMID:19563753; http://dx.doi.org/10.1016/j.cell.2009.06.001
15. Phillips-Cremins JE, Corces VG. CTCF: Linking genome organization to cellular function. Mol Cell 2013; In press
16. Cremer T, Cremer M, Dietzel S, Müller S, Solovei I, Fakan S. Chromosome territories - a functional nuclear landscape. Curr Opin Cell Biol 2006; 18:307-16; PMID:16687245; http://dx.doi.org/10.1016/j.ceb.2006.04.007
17. van Driel R, Fransz PF, Verschure PJ. The eukaryotic genome: a system regulated at different hierarchical levels. J Cell Sci 2003; 116:4067-75; PMID:12972500; http://dx.doi.org/10.1242/jcs.00779
18. Chambeyron S, Bickmore WA. Chromatin decondensation and nuclear reorganization of the HoxB locus upon induction of transcription. Genes Dev 2004; 18:1119-30; PMID:15155579; http://dx.doi.org/10.1101/gad.292104
19. Lomvardas S, Barnea G, Pisapia DJ, Mendelsohn M, Kirkland J, Axel R. Interchromosomal interactions and olfactory receptor choice. Cell 2006; 126:403-13; PMID:16873069; http://dx.doi.org/10.1016/j.cell.2006.06.035
20. Spilianakis CG, Lalioti MD, Town T, Lee GR, Flavell RA. Interchromosomal associations between alternatively expressed loci. Nature 2005; 435:637-45; PMID:15880101; http://dx.doi.org/10.1038/nature03574
21. Li T, Hu JF, Qiu X, Ling J, Chen H, Wang S, et al. CTCF regulates allelic expression of Igf2 by orchestrating a promoter-polycomb repressive complex 2 intrachromosomal loop. Mol Cell Biol 2008; 28:6473-82; PMID:18662993; http://dx.doi.org/10.1128/MCB.00204-08
22. Hou C, Li L, Qin ZS, Corces VG. Gene density, transcription, and insulators contribute to the partition of the Drosophila genome into physical domains. Mol Cell 2012; 48:471-84; PMID:23041285; http://dx.doi.org/10.1016/j. molcel.2012.08.031
23. Dixon JR, Selvaraj S, Yue F, Kim A, Li Y, Shen Y, et al. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 2012; 485:376-80; PMID:22495300; http://dx.doi.org/10.1038/nature11082
24. Nora EP, Lajoie BR, Schulz EG, Giorgetti L, Okamoto I, Servant N, et al. Spatial partitioning of the regulatory landscape of the X-inactivation centre. Nature 2012; 485:381-5; PMID:22495304; http://dx.doi.org/10.1038/nature11049
25. Sexton T, Yaffe E, Kenigsberg E, Bantignies F, Leblanc B, Hoichman M, et al. Three-dimensional folding and functional organization principles of the Drosophila genome. Cell 2012; 148:458-72; PMID:22265598; http://dx.doi.org/10. 1016/j.cell.2012.01.010
26. Gerasimova TI, Lei EP, Bushey AM, Corces VG. Coordinated control of dCTCF and gypsy chromatin insulators in Drosophila. Mol Cell 2007; 28:761-72; PMID:18082602; http://dx.doi.org/10.1016/j.molcel.2007.09.024
27. Moon H, Filippova G, Loukinov D, Pugacheva E, Chen Q, Smith ST, et al. CTCF is conserved from Drosophila to humans and confers enhancer blocking of the Fab-8 insulator. EMBO Rep 2005; 6:165-70; PMID:15678159; http://dx.doi.org/10. 1038/sj.embor.7400334
28. Parkhurst SM, Harrison DA, Remington MP, Spana C, Kelley RL, Coyne RS, et al. The Drosophila su(Hw) gene, which controls the phenotypic effect of the gypsy transposable element, encodes a putative DNA-binding protein. Genes Dev 1988; 2:1205-15; PMID:2462523; http://dx.doi.org/10.1101/gad.2.10.1205
29. Zhao K, Hart CM, Laemmli UK. Visualization of chromosomal domains with boundary element-associated factor BEAF-32. Cell 1995; 81:879-89; PMID:7781065; http://dx.doi.org/10.1016/0092-8674(95)90008-X
30. Belozerov VE, Majumder P, Shen P, Cai HN. A novel boundary element may facilitate independent gene regulation in the Antennapedia complex of Drosophila. EMBO J 2003; 22:3113-21; PMID:12805225; http://dx.doi.org/10.1093/ emboj/cdg297
31. Gaszner M, Vazquez J, Schedl P. The Zw5 protein, a component of the scs chromatin domain boundary, is able to block enhancer-promoter interaction. Genes Dev 1999; 13:2098-107; PMID:10465787; http://dx.doi.org/10.1101/gad.13.16.2098
32. Pai CY, Lei EP, Ghosh D, Corces VG. The centrosomal protein CP190 is a component of the gypsy chromatin insulator. Mol Cell 2004; 16:737-48; PMID:15574329; http://dx.doi.org/10.1016/j.molcel.2004.11.004
33. Gause M, Morcillo P, Dorsett D. Insulation of enhancer-promoter communication by a gypsy transposon insert in the Drosophila cut gene: cooperation between suppressor of hairy-wing and modifier of mdg4 proteins. Mol Cell Biol 2001; 21:4807-17; PMID:11416154; http://dx.doi.org/10.1128/MCB.21.14. 4807-4817.2001
34. Ghosh D, Gerasimova TI, Corces VG. Interactions between the Su(Hw) and Mod(mdg4) proteins required for gypsy insulator function. EMBO J 2001; 20:2518-27; PMID:11350941; http://dx.doi.org/10.1093/emboj/20.10.2518
35. Wood AM, Van Bortle K, Ramos E, Takenaka N, Rohrbaugh M, Jones BC, et al. Regulation of chromatin organization and inducible gene expression by a Drosophila insulator. Mol Cell 2011; 44:29-38; PMID:21981916; http://dx.doi.org/10.1016/j.molcel.2011.07.035
36. Bushey AM, Ramos E, Corces VG. Three subclasses of a Drosophila insulator show distinct and cell type-specific genomic distributions. Genes Dev 2009; 23:1338-50; PMID:19443682; http://dx.doi.org/10.1101/gad.1798209
37. Nègre N, Brown CD, Shah PK, Kheradpour P, Morrison CA, Henikoff JG, et al. A comprehensive map of insulator elements for the Drosophila genome. PLoS Genet 2010; 6:e1000814; PMID:20084099; http://dx.doi.org/10.1371/journal. pgen.1000814
38. Jiang N, Emberly E, Cuvier O, Hart CM. Genome-wide mapping of boundary element-associated factor (BEAF) binding sites in Drosophila melanogaster links BEAF to transcription. Mol Cell Biol 2009; 29:3556-68; PMID:19380483; http://dx.doi.org/10.1128/MCB.01748-08
39. Yang J, Ramos E, Corces VG. The BEAF-32 insulator coordinates genome organization and function during the evolution of Drosophila species. Genome Res 2012; 22:2199-207; PMID:22895281; http://dx.doi.org/10.1101/gr.142125.112
40. Van Bortle K, Ramos E, Takenaka N, Yang J, Wahi JE, Corces VG. Drosophila CTCF tandemly aligns with other insulator proteins at the borders of H3K27me3 domains. Genome Res 2012; 22:2176-87; PMID:22722341; http://dx.doi.org/10.1101/ gr.136788.111
41. Hou C, Corces VG. Throwing transcription for a loop: expression of the genome in the 3D nucleus. Chromosoma 2012; 121:107-16; PMID:22094989; http://dx.doi.org/10.1007/s00412-011-0352-7
42. Hart CM, Cuvier O, Laemmli UK. Evidence for an antagonistic relationship between the boundary element-associated factor BEAF and the transcription factor DREF. Chromosoma 1999; 108:375-83; PMID:10591997; http://dx.doi.org/10.1007/ s004120050389
43. Hart CM, Zhao K, Laemmli UK. The scs' boundary element: characterization of boundary element-associated factors. Mol Cell Biol 1997; 17:999-1009; PMID:9001253
44. Whitfield ML, Sherlock G, Saldanha AJ, Murray JI, Ball CA, Alexander KE, et al. Identification of genes periodically expressed in the human cell cycle and their expression in tumors. Mol Biol Cell 2002; 13:1977-2000; PMID:12058064; http://dx.doi.org/10.1091/mbc.02-02-0030.
45. Young DW, Hassan MQ, Pratap J, Galindo M, Zaidi SK, Lee SH, et al. Mitotic occupancy and lineage-specific transcriptional control of rRNA genes by Runx2. Nature 2007; 445:442-6; PMID:17251981; http://dx.doi.org/10.1038/ nature05473
46. Gurudatta BV, Ramos E, Corces VG. The BEAF insulator regulates genes involved in cell polarity and neoplastic growth. Dev Biol 2012; 369:124-32; PMID:22743648; http://dx.doi.org/10.1016/j.ydbio.2012.06.013
47. Yang J, Sung E, Donlin-Asp PG, Corces VG. A subset of Drosophila Myc sites remain associated with mitotic chromosomes co-localized with insulator proteins. Nat Commun 2013; 4:1464; PMID:23403565; http://dx.doi.org/10.1038/ ncomms2469
48. Machanick P, Bailey TL. MEME-ChIP: motif analysis of large DNA datasets. Bioinformatics 2011; 27:1696-7; PMID:21486936; http://dx.doi.org/10.1093/ bioinformatics/btr189
49. MacAlpine HK, Gordân R, Powell SK, Hartemink AJ, MacAlpine DM. Drosophila ORC localizes to open chromatin and marks sites of cohesin complex loading. Genome Res 2010; 20:201-11; PMID:19996087; http://dx.doi.org/10.1101/ gr.097873.109
50. Araki M, Yu H, Asano M. A novel motif governs APC-dependent degradation of Drosophila ORC1 in vivo. Genes Dev 2005; 19:2458-65; PMID:16195415; http://dx.doi.org/10.1101/gad.1361905
51. Baldinger T, Gossen M. Binding of Drosophila ORC proteins to anaphase chromosomes requires cessation of mitotic cyclin-dependent kinase activity. Mol Cell Biol 2009; 29:140-9; PMID:18955499; http://dx.doi.org/10.1128/MCB.00981-08
52. Zaidi SK, Young DW, Montecino MA, Lian JB, van Wijnen AJ, Stein JL, et al. Mitotic bookmarking of genes: a novel dimension to epigenetic control. Nat Rev Genet 2010; 11:583-9; PMID:20628351; http://dx.doi.org/10.1038/nrg2827
53. Blobel GA, Kadauke S, Wang E, Lau AW, Zuber J, Chou MM, et al. A reconfigured pattern of MLL occupancy within mitotic chromatin promotes rapid transcriptional reactivation following mitotic exit. Mol Cell 2009; 36:970-83; PMID:20064463; http://dx.doi.org/10.1016/j.molcel.2009.12.001
54. Dey A, Nishiyama A, Karpova T, McNally J, Ozato K. Brd4 marks select genes on mitotic chromatin and directs postmitotic transcription. Mol Biol Cell 2009; 20:4899-909; PMID:19812244; http://dx.doi.org/10.1091/mbc.E09-05-0380
55. Gurudatta BV, Corces VG. Chromatin insulators: lessons from the fly. Brief Funct Genomic Proteomic 2009; 8:276-82; PMID:19752045; http://dx.doi.org/10.1093/bfgp/elp032
56. Van Bortle K, Corces VG. Nuclear organization and genome function. Annu Rev Cell Dev Biol 2012; 28:163-87; PMID:22905954; http://dx.doi.org/10.1146/ annurev-cellbio-101011-155824
57. Young DW, Hassan MQ, Yang XQ, Galindo M, Javed A, Zaidi SK, et al. Mitotic retention of gene expression patterns by the cell fate-determining transcription factor Runx2. Proc Natl Acad Sci USA 2007; 104:3189-94; PMID:17360627; http://dx.doi.org/10.1073/pnas.0611419104
58. Sarge KD, Park-Sarge OK. Mitotic bookmarking of formerly active genes: keeping epigenetic memories from fading. Cell Cycle 2009; 8:818-23; PMID:19221503; http://dx.doi.org/10.4161/cc.8.6.7849
59. Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 2009; 10:R25; PMID:19261174; http://dx.doi.org/10.1186/gb-2009-10-3-r25
60. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol 2008; 9:R137; PMID:18798982; http://dx.doi.org/10.1186/gb-2008-9-9-r137
61. Goecks J, Nekrutenko A, Taylor J; Galaxy Team. Galaxy: a comprehensive approach for supporting accessible, reproducible, and transparent computational research in the life sciences. Genome Biol 2010; 11:R86; PMID:20738864; http://dx.doi.org/10.1186/gb-2010-11-8-r86
62. Huang W, Sherman BT, Tan Q, Collins JR, Alvord WG, Roayaei J, et al. The DAVID Gene Functional Classification Tool: a novel biological module-centric algorithm to functionally analyze large gene lists. Genome Biol 2007; 8:R183; PMID:17784955; http://dx.doi.org/10.1186/gb-2007-8-9-r183
63. Hoover KK, Chien AJ, Corces VG. Effects of transposable elements on the expression of the forked gene of Drosophila melanogaster. Genetics 1993; 135:507-26; PMID:8244011