Chromatin Insulator Factors Involved in Long-Range DNA Interactions and Their Role in the Folding of the Drosophila Genome

PLoS Genetics

Volumn 10, Issue 8, 2014, Pages

  Vogelmann, Jutta ^a,b,c   Le Gall, Antoine ^a,b,c   Dejardin, Stephanie ^a,b,c   Allemand, Frederic ^a,b,c   Gamot, Adrien ^d   Labesse, Gilles ^a,b,c   Cuvier, Olivier ^d   Nègre, Nicolas ^e   Cohen Gonsaud, Martin ^a,b,c   Margeat, Emmanuel ^a,b,c   Nöllmann, Marcelo ^a,b,c  

^a CNRS   (France)

^b CENTRE DE BIOCHIMIE STRUCTURALE   (France)

^c UNIV MONTPELLIER   (France)

^d UNIVERSITÉ DE TOULOUSE   (France)

^e University of Montpellier II   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; CHROMATOR; PROTEIN BEAF32; PROTEIN CP190; UNCLASSIFIED DRUG; BEAF-32 PROTEIN, DROSOPHILA; CHROMATIN; CHROMATOR PROTEIN, DROSOPHILA; CP190 PROTEIN, DROSOPHILA; DNA; DNA BINDING PROTEIN; DROSOPHILA PROTEIN; EYE PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; NUCLEAR MATRIX PROTEIN; NUCLEAR PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; BIOCHEMICAL COMPOSITION; CARBOXY TERMINAL SEQUENCE; CELL DIVISION; CHROMATIN INSULATOR; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DIMERIZATION; DNA BINDING; FLUORESCENCE ANALYSIS; IN VITRO STUDY; INSULATOR ELEMENT; LONG RANGE DNA INTERACTION; MOLECULAR INTERACTION; MOLECULAR MODEL; PROTEIN DOMAIN; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; STRUCTURE ANALYSIS; ANIMAL; CHROMATIN; DROSOPHILA MELANOGASTER; GENE REGULATORY NETWORK; GENETICS; INSECT GENOME;

ANIMALS; CHROMATIN; DNA; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EYE PROTEINS; GENE REGULATORY NETWORKS; GENOME, INSECT; INSULATOR ELEMENTS; MICROTUBULE-ASSOCIATED PROTEINS; NUCLEAR MATRIX-ASSOCIATED PROTEINS; NUCLEAR PROTEINS;

EID: 84925548299     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004544     Document Type: Article

References (91)

1. Chang HY, Cuvier O, Dekker J, (2009) Gene dates, parties and galas. Symposium on Chromatin Dynamics and Higher Order Organization. EMBO Rep 10: 689–693 doi:10.1038/embor.2009.136
2. Elgin SC, Grewal SI, (2003) Heterochromatin: silence is golden. Curr Biol 13: R895–R898.
3. Mechali M, (2010) Eukaryotic DNA replication origins: many choices for appropriate answers. Nat Rev Mol Cell Biol 11: 728–738 doi:10.1038/nrm2976
4. Probst AV, Dunleavy E, Almouzni G, (2009) Epigenetic inheritance during the cell cycle. Nat Rev Mol Cell Biol 10: 192–206 doi:10.1038/nrm2640
5. Sexton T, Bantignies F, Cavalli G, (2009) Genomic interactions: chromatin loops and gene meeting points in transcriptional regulation. Semin Cell Dev Biol 20: 849–855 doi:10.1016/j.semcdb.2009.06.004
6. Misteli T, (2007) Beyond the sequence: cellular organization of genome function. Cell 128: 787–800 doi:10.1016/j.cell.2007.01.028
7. Gaszner M, Felsenfeld G, (2006) Insulators: exploiting transcriptional and epigenetic mechanisms. Nat Rev Genet 7: 703–713 doi:10.1038/nrg1925
8. Negre N, Brown CD, Ma L, Bristow CA, Miller SW, et al. (2011) A cis-regulatory map of the Drosophila genome. Nature 471: 527–531 doi:10.1038/nature09990
9. Vogelmann J, Valeri A, Guillou E, Cuvier O, Nollmann M, (2011) Roles of chromatin insulator proteins in higher-order chromatin organization and transcription regulation. Nucleus 2: 358–369 doi:10.4161/nucl.2.5.17860
10. Bushey AM, Ramos E, Corces VG, (2009) Three subclasses of a Drosophila insulator show distinct and cell type-specific genomic distributions. Genes Dev 23: 1338–1350 doi:10.1101/gad.1798209
11. Emberly E, Blattes R, Schuettengruber B, Hennion M, Jiang N, et al. (2008) BEAF regulates cell-cycle genes through the controlled deposition of H3K9 methylation marks into its conserved dual-core binding sites. PLoS Biol 6: 2896–2910 doi:10.1371/journal.pbio.0060327
12. Hou C, Li L, Qin Z, Corces V, (2012) Gene density, transcription, and insulators contribute to the partition of the Drosophila genome into physical domains. Mol Cell 48: 471–484 doi:10.1016/j.molcel.2012.08.031
13. Sexton T, Yaffe E, Kenigsberg E, Bantignies FDR, Leblanc B, et al. (2012) Three-dimensional folding and functional organization principles of the Drosophila genome. Cell 148: 458–472 doi:10.1016/j.cell.2012.01.010
14. Geyer PK, Corces VG, (1992) DNA position-specific repression of transcription by a Drosophila zinc finger protein. Genes Dev 6: 1865–1873.
15. Zhao K, Hart CM, Laemmli UK, (1995) Visualization of chromosomal domains with boundary element-associated factor BEAF-32. Cell 81: 879–889.
16. Gaszner M, Vazquez J, Schedl P, (1999) The Zw5 protein, a component of the scs chromatin domain boundary, is able to block enhancer-promoter interaction. Genes Dev 13: 2098–2107.
17. Maeda RK, Karch F, (2007) Making connections: boundaries and insulators in Drosophila. Curr Opin Genet Dev 17: 394–399 doi:10.1016/j.gde.2007.08.002
18. Moon H, Filippova G, Loukinov D, Pugacheva E, Chen Q, et al. (2005) CTCF is conserved from Drosophila to humans and confers enhancer blocking of the Fab-8 insulator. EMBO Rep 6: 165–170 doi:10.1038/sj.embor.7400334
19. Cuvier O, Hart CM, Laemmli UK, (1998) Identification of a class of chromatin boundary elements. Mol Cell Biol 18: 7478–7486.
20. Roy S, Gilbert MK, Hart CM, (2007) Characterization of BEAF mutations isolated by homologous recombination in Drosophila. Genetics 176: 801–813 doi:10.1534/genetics.106.068056
21. Pai CY, Lei EP, Ghosh D, Corces VG, (2004) The centrosomal protein CP190 is a component of the gypsy chromatin insulator. Mol Cell 16: 737–748 doi:10.1016/j.molcel.2004.11.004
22. Oegema K, Whitfield WG, Alberts B, (1995) The cell cycle-dependent localization of the CP190 centrosomal protein is determined by the coordinate action of two separable domains. J Cell Biol 131: 1261–1273.
23. Akbari OS, Oliver D, Eyer K, Pai CY, (2009) An Entry/Gateway cloning system for general expression of genes with molecular tags in Drosophila melanogaster. BMC Cell Biol 10: 8 doi:10.1186/1471-2121-10-8
24. Golovnin A, Mazur A, Kopantseva M, Kurshakova M, Gulak PV, et al. (2007) Integrity of the Mod(mdg4)-67.2 BTB domain is critical to insulator function in Drosophila melanogaster. Mol Cell Biol 27: 963–974 doi:10.1128/MCB.00795-06
25. Negre N, Brown CD, Shah PK, Kheradpour P, Morrison CA, et al. (2010) A comprehensive map of insulator elements for the Drosophila genome. PLoS Genet 6: e1000814 doi:10.1371/journal.pgen.1000814
26. Van Bortle K, Ramos E, Takenaka N, Yang J, Wahi JE, et al. (2012) Drosophila CTCF tandemly aligns with other insulator proteins at the borders of H3K27me3 domains. Genome Res 22: 2176–2187 doi:10.1101/gr.136788.111
27. Blanton J, Gaszner M, Schedl P, (2003) Protein:protein interactions and the pairing of boundary elements in vivo. Genes Dev 17: 664–675 doi:10.1101/gad.1052003
28. Degner SC, Verma-Gaur J, Wong TP, Bossen C, Iverson GM, et al. (2011) CCCTC-binding factor (CTCF) and cohesin influence the genomic architecture of the Igh locus and antisense transcription in pro-B cells. Proc Natl Acad Sci USA 108: 9566–9571 doi:10.1073/pnas.1019391108
29. Kurukuti S, Tiwari VK, Tavoosidana G, Pugacheva E, Murrell A, et al. (2006) CTCF binding at the H19 imprinting control region mediates maternally inherited higher-order chromatin conformation to restrict enhancer access to Igf2. Proc Natl Acad Sci USA 103: 10684–10689 doi:10.1073/pnas.0600326103
30. Mishiro T, Ishihara K, Hino S, Tsutsumi S, Aburatani H, et al. (2009) Architectural roles of multiple chromatin insulators at the human apolipoprotein gene cluster. EMBO J 28: 1234–1245 doi:10.1038/emboj.2009.81
31. Phillips-Cremins JE, Sauria ME, Sanyal A, Gerasimova TI, Lajoie BR, et al. (2013) Architectural protein subclasses shape 3D organization of genomes during lineage commitment. Cell 153: 1281–1295 doi:10.1016/j.cell.2013.04.053
32. Wendt KS, Yoshida K, Itoh T, Bando M, Koch B, et al. (2008) Cohesin mediates transcriptional insulation by CCCTC-binding factor. Nature 451: 796–801 doi:10.1038/nature06634
33. Wood AM, Van Bortle K, Ramos E, Takenaka N, Rohrbaugh M, et al. (2011) Regulation of chromatin organization and inducible gene expression by a Drosophila insulator. Mol Cell 44: 29–38 doi:10.1016/j.molcel.2011.07.035
34. Yusufzai TM, Tagami H, Nakatani Y, Felsenfeld G, (2004) CTCF tethers an insulator to subnuclear sites, suggesting shared insulator mechanisms across species. Mol Cell 13: 291–298.
35. Cavalli G, (2007) Chromosome kissing. Curr Opin Genet Dev 17: 443–450 doi:10.1016/j.gde.2007.08.013
36. Fraser P, Bickmore W, (2007) Nuclear organization of the genome and the potential for gene regulation. Nature 447: 413–417 doi:10.1038/nature05916
37. Yu W, Ginjala V, Pant V, Chernukhin I, Whitehead J, et al. (2004) Poly(ADP-ribosyl)ation regulates CTCF-dependent chromatin insulation. Nat Genet 36: 1105–1110 doi:10.1038/ng1426
38. Bartkuhn M, Straub T, Herold M, Herrmann M, Rathke C, et al. (2009) Active promoters and insulators are marked by the centrosomal protein 190. EMBO J 28: 877–888 doi:10.1038/emboj.2009.34
39. Gerasimova TI, Lei EP, Bushey AM, Corces VG, (2007) Coordinated control of dCTCF and gypsy chromatin insulators in Drosophila. Mol Cell 28: 761–772 doi:10.1016/j.molcel.2007.09.024
40. Yang J, Corces VG, (2012) Insulators, long-range interactions, and genome function. Curr Opin Genet Dev 22: 86–92 doi:10.1016/j.gde.2011.12.007
41. Rath U, Ding Y, Deng H, Qi H, Bao X, et al. (2006) The chromodomain protein, Chromator, interacts with JIL-1 kinase and regulates the structure of Drosophila polytene chromosomes. J Cell Sci 119: 2332–2341 doi:10.1242/jcs.02960
42. Gortchakov AA, Eggert H, Gan M, Mattow J, Zhimulev IF, et al. (2005) Chriz, a chromodomain protein specific for the interbands of Drosophila melanogaster polytene chromosomes. Chromosoma 114: 54–66 doi:10.1007/s00412-005-0339-3
43. Rath U, Wang D, Ding Y, Xu YZ, Qi H, et al. (2004) Chromator, a novel and essential chromodomain protein interacts directly with the putative spindle matrix protein skeletor. J Cell Biochem 93: 1033–1047 doi:10.1002/jcb.20243
44. Mendjan S, Taipale M, Kind J, Holz H, Gebhardt P, et al. (2006) Nuclear pore components are involved in the transcriptional regulation of dosage compensation in Drosophila. Mol Cell 21: 811–823 doi:10.1016/j.molcel.2006.02.007
45. Yao C, Ding Y, Cai W, Wang C, Girton J, et al. (2012) The chromodomain-containing NH(2)-terminus of Chromator interacts with histone H1 and is required for correct targeting to chromatin. Chromosoma 121: 209–220 doi:10.1007/s00412-011-0355-4
46. Lakowicz JR (2006) Principles of Fluorescence Spectroscopy. New York: Springer.
47. Schwartz YB, Linder-Basso D, Kharchenko PV, Tolstorukov MY, Kim M, et al. (2012) Nature and function of insulator protein binding sites in the Drosophila genome. Genome Res 22: 2188–2198 doi:10.1101/gr.138156.112
48. Kharchenko PV, Alekseyenko AA, Schwartz YB, Minoda A, Riddle NC, et al. (2011) Comprehensive analysis of the chromatin landscape in Drosophila melanogaster. Nature 471: 480–485 doi:10.1038/nature09725
49. Kim SA, Heinze KG, Bacia K, Waxham MN, Schwille P, (2005) Two-photon cross-correlation analysis of intracellular reactions with variable stoichiometry. Biophys J 88: 4319–4336 doi:10.1529/biophysj.104.055319
50. Schwille P, Meyer-Almes FJ, Rigler R, (1997) Dual-color fluorescence cross-correlation spectroscopy for multicomponent diffusional analysis in solution. Biophys J 72: 1878–1886 doi:10.1016/S0006-3495(97)78833-7
51. Bacia K, Kim SA, Schwille P, (2006) Fluorescence cross-correlation spectroscopy in living cells. Nat Methods 3: 83–89 doi:10.1038/nmeth822
52. Muller BK, Zaychikov E, Brauchle C, Lamb DC, (2005) Pulsed interleaved excitation. Biophys J 89: 3508–3522 doi:10.1529/biophysj.105.064766
53. Olofsson L, Margeat E, (2013) Pulsed interleaved excitation fluorescence spectroscopy with a supercontinuum source. Opt Express 21: 3370–3378.
54. Perez-Torrado R, Yamada D, Defossez PA, (2006) Born to bind: the BTB protein-protein interaction domain. Bioessays 28: 1194–1202 doi:10.1002/bies.20500
55. Stogios PJ, Downs GS, Jauhal JJ, Nandra SK, Prive GG, (2005) Sequence and structural analysis of BTB domain proteins. Genome Biol 6: R82 doi:10.1186/gb-2005-6-10-r82
56. Krissinel E, Henrick K, (2007) Inference of macromolecular assemblies from crystalline state. J Mol Biol 372: 774–797 doi:10.1016/j.jmb.2007.05.022
57. Ashkenazy H, Erez E, Martz E, Pupko T, Ben-Tal N, (2010) ConSurf 2010: calculating evolutionary conservation in sequence and structure of proteins and nucleic acids. Nucleic Acids Research 38: W529–W533 doi:10.1093/nar/gkq399
58. Oliver D, Sheehan B, South H, Akbari O, Pai CY, (2010) The chromosomal association/dissociation of the chromatin insulator protein Cp190 of Drosophila melanogaster is mediated by the BTB/POZ domain and two acidic regions. BMC Cell Biol 11: 101 doi:10.1186/1471-2121-11-101
59. Dean A, (2011) In the loop: long range chromatin interactions and gene regulation. Brief Funct Genomics 10: 3–10 doi:10.1093/bfgp/elq033
60. Kyrchanova O, Chetverina D, Maksimenko O, Kullyev A, Georgiev P, (2008) Orientation-dependent interaction between Drosophila insulators is a property of this class of regulatory elements. Nucleic Acids Research 36: 7019–7028 doi:10.1093/nar/gkn781
61. Mukhopadhyay S, Schedl P, Studitsky VM, Sengupta AM, (2011) Theoretical analysis of the role of chromatin interactions in long-range action of enhancers and insulators. Proc Natl Acad Sci USA 108: 19919–19924 doi:10.1073/pnas.1103845108
62. Wallace JA, Felsenfeld G, (2007) We gather together: insulators and genome organization. Curr Opin Genet Dev 17: 400–407 doi:10.1016/j.gde.2007.08.005
63. Bardwell VJ, Treisman R, (1994) The POZ domain: a conserved protein-protein interaction motif. Genes Dev 8: 1664–1677.
64. Lours C, Bardot O, Godt D, Laski FA, Couderc JL, (2003) The Drosophila melanogaster BTB proteins bric a brac bind DNA through a composite DNA binding domain containing a pipsqueak and an AT-Hook motif. Nucleic Acids Research 31: 5389–5398.
65. Zollman S, Godt D, Prive GG, Couderc JL, Laski FA, (1994) The BTB domain, found primarily in zinc finger proteins, defines an evolutionarily conserved family that includes several developmentally regulated genes in Drosophila. Proc Natl Acad Sci USA 91: 10717–10721.
66. Bonchuk A, Denisov S, Georgiev P, Maksimenko O, (2011) Drosophila BTB/POZ domains of “ttk group” can form multimers and selectively interact with each other. J Mol Biol 412: 423–436 doi:10.1016/j.jmb.2011.07.052
67. Mohan M, Bartkuhn M, Herold M, Philippen A, Heinl N, et al. (2007) The Drosophila insulator proteins CTCF and CP190 link enhancer blocking to body patterning. EMBO J 26: 4203–4214 doi:10.1038/sj.emboj.7601851
68. Ong CT, Van Bortle K, Ramos E, Corces VG, (2013) Poly(ADP-ribosyl)ation Regulates Insulator Function and Intrachromosomal Interactions in Drosophila. Cell 155: 148–159 doi:10.1016/j.cell.2013.08.052
69. Lei EP, Corces VG, (2006) RNA interference machinery influences the nuclear organization of a chromatin insulator. Nat Genet 38: 936–941 doi:10.1038/ng1850
70. Brayer KJ, Segal DJ, (2008) Keep your fingers off my DNA: protein-protein interactions mediated by C2H2 zinc finger domains. Cell Biochem Biophys 50: 111–131 doi:10.1007/s12013-008-9008-5
71. Ahmad KF, Melnick A, Lax S, Bouchard D, Liu J, et al. (2003) Mechanism of SMRT corepressor recruitment by the BCL6 BTB domain. Mol Cell 12: 1551–1564.
72. Ghetu AF, Corcoran CM, Cerchietti L, Bardwell VJ, Melnick A, et al. (2008) Structure of a BCOR corepressor peptide in complex with the BCL6 BTB domain dimer. Mol Cell 29: 384–391 doi:10.1016/j.molcel.2007.12.026
73. Gurudatta BV, Corces VG, (2009) Chromatin insulators: lessons from the fly. Brief Funct Genomic Proteomic 8: 276–282 doi:10.1093/bfgp/elp032
74. Li Y, Cai W, Wang C, Yao C, Bao X, et al. (2013) Domain Requirements of the JIL-1 Tandem Kinase for Histone H3 Serine 10 Phosphorylation and Chromatin Remodeling in Vivo. J Biol Chem 288: 19441–19449 doi:10.1074/jbc.M113.464271
75. Regnard C, Straub T, Mitterweger A, Dahlsveen IK, Fabian V, et al. (2011) Global analysis of the relationship between JIL-1 kinase and transcription. PLoS Genet 7: e1001327 doi:10.1371/journal.pgen.1001327
76. Wang C, Cai W, Li Y, Deng H, Bao X, et al. (2011) The epigenetic H3S10 phosphorylation mark is required for counteracting heterochromatic spreading and gene silencing in Drosophila melanogaster. J Cell Sci 124: 4309–4317 doi:10.1242/jcs.092585
77. Jiang N, Emberly E, Cuvier O, Hart CM, (2009) Genome-wide mapping of boundary element-associated factor (BEAF) binding sites in Drosophila melanogaster links BEAF to transcription. Mol Cell Biol 29: 3556–3568 doi:10.1128/MCB.01748-08
78. Filippova GN, Fagerlie S, Klenova EM, Myers C, Dehner Y, et al. (1996) An exceptionally conserved transcriptional repressor, CTCF, employs different combinations of zinc fingers to bind diverged promoter sequences of avian and mammalian c-myc oncogenes. Mol Cell Biol 16: 2802–2813.
79. Yang J, Sung E, Donlin-Asp PG, Corces VG, (2013) A subset of Drosophila Myc sites remain associated with mitotic chromosomes colocalized with insulator proteins. Nat Commun 4: 1464 doi:10.1038/ncomms2469
80. Gurudatta BV, Yang J, Van Bortle K, Donlin-Asp PG, Corces VG, (2013) Dynamic changes in the genomic localization of DNA replication-related element binding factor during the cell cycle. Cell Cycle 12: 1605–1615 doi:10.4161/cc.24742
81. Ptacin JL, Nollmann M, Becker EC, Cozzarelli NR, Pogliano K, et al. (2008) Sequence-directed DNA export guides chromosome translocation during sporulation in Bacillus subtilis. Nat Struct Mol Biol 15: 485–493 doi:10.1038/nsmb.1412
82. Hart CM, Cuvier O, Laemmli UK, (1999) Evidence for an antagonistic relationship between the boundary element-associated factor BEAF and the transcription factor DREF. Chromosoma 108: 375–383.
83. Jee J, Rozowsky J, Yip KY, Lochovsky L, Bjornson R, et al. (2011) ACT: aggregation and correlation toolbox for analyses of genome tracks. Bioinformatics 27: 1152–1154 doi:10.1093/bioinformatics/btr092
84. Roy S, Ernst J, Kharchenko PV, Kheradpour P, Negre N, et al. (2010) Identification of functional elements and regulatory circuits by Drosophila modENCODE. Science 330: 1787–1797 doi:10.1126/science.1198374
85. Quinlan AR, Hall IM, (2010) BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26: 841–842 doi:10.1093/bioinformatics/btq033
86. Winn MD, Ballard CC, Cowtan KD, Dodson EJ, Emsley P, et al. (2011) Overview of the CCP4 suite and current developments. Acta Crystallogr D Biol Crystallogr 67: 235–242 doi:10.1107/S0907444910045749
87. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, et al. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66: 213–221 doi:10.1107/S0907444909052925
88. Pons JL, Labesse G, (2009) TOME-2: a new pipeline for comparative modeling of protein-ligand complexes. Nucleic Acids Research 37: W485–W491 doi:10.1093/nar/gkp368
89. Emsley P, Cowtan K, (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126–2132 doi:10.1107/S0907444904019158
90. Hac AE, Seeger HM, Fidorra M, Heimburg T, (2005) Diffusion in two-component lipid membranes–a fluorescence correlation spectroscopy and monte carlo simulation study. Biophys J 88: 317–333 doi:10.1529/biophysj.104.040444
91. Sacksteder CA, Whittier JE, Xiong Y, Li J, Galeva NA, et al. (2006) Tertiary structural rearrangements upon oxidation of Methionine145 in calmodulin promotes targeted proteasomal degradation. Biophys J 91: 1480–1493 doi:10.1529/biophysj.106.086033