Three subclasses of a Drosophila insulator show distinct and cell type-specific genomic distributions

Genes and Development

Volumn 23, Issue 11, 2009, Pages 1338-1350

  Bushey, Ashley M ^a,b   Ramos, Edward ^a   Corces, Victor G ^a  

^a EMORY UNIVERSITY   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

BEAF; Chromatin organization; CTCF; Gypsy; Insulators

Indexed keywords

CENTROSOMAL PROTEIN 190; DNA; DNA BINDING PROTEIN; MESSENGER RNA; UNCLASSIFIED DRUG; CP190 PROTEIN, DROSOPHILA; CTCF PROTEIN, DROSOPHILA; DROSOPHILA PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; NUCLEAR PROTEIN; REPRESSOR PROTEIN; SU(HW) PROTEIN, DROSOPHILA;

ARTICLE; CELL SPECIFICITY; CELL TYPE; CENTROSOME; CHROMATIN IMMUNOPRECIPITATION; CHROMOSOME; DROSOPHILA MELANOGASTER; GENE EXPRESSION REGULATION; GENOME; MICROARRAY ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN LOCALIZATION; ANIMAL; CYTOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; INSULATOR ELEMENT; METABOLISM; PROTEIN MICROARRAY; PROTEIN TRANSPORT;

DROSOPHILA MELANOGASTER;

ANIMALS; CHROMATIN IMMUNOPRECIPITATION; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION; GENOME, INSECT; INSULATOR ELEMENTS; MICROTUBULE-ASSOCIATED PROTEINS; NUCLEAR PROTEINS; PROTEIN ARRAY ANALYSIS; PROTEIN TRANSPORT; REPRESSOR PROTEINS;

EID: 66149164708     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.1798209     Document Type: Article

References (50)

1. Adryan B, Woerfel G, Birch-Machin I, Gao S, Quick M, Meadows L, Russell S, White R. 2007. Genomic mapping of Suppressor of Hairy-wing binding sites in Drosophila. Genome Biol 8: R167. doi: 10.1186/gb-2007-8-8-r167.
2. Bailey TL, Elkan C. 1994. Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc Int Conf Intell Syst Mol Biol 2: 28-36.
3. Bartkuhn M, Straub T, Herold M, Herrmann M, Rathke C, Saumweber H, Gilfillan GD, Becker PB, Renkawitz R. 2009. Active promoters and insulators are marked by the centrosomal protein 190. EMBO J 28: 877-888.
4. Bell AC, Felsenfeld G. 2000. Methylation of a CTCF-dependent boundary controls imprinted expression of the Igf2 gene. Nature 405: 482-485. (Pubitemid 30367427)
5. Blanton J, Gaszner M, Schedl P. 2003. Protein:protein interactions and the pairing of boundary elements in vivo. Genes & Dev 17: 664-675. (Pubitemid 36307550)
6. Byrd K, Corces VG. 2003. Visualization of chromatin domains created by the gypsy insulator of Drosophila. J Cell Biol 162: 565-574. (Pubitemid 37022935)
7. Capelson M, Corces VG. 2005. The ubiquitin ligase dTopors directs the nuclear organization of a chromatin insulator. Mol Cell 20: 105-116. (Pubitemid 41396566)
8. Capelson M, Corces VG. 2006. SUMO conjugation attenuates the activity of the gypsy chromatin insulator. EMBO J 25: 1906-1914.
9. Carlson JM, Chakravarty A, DeZiel CE, Gross RH. 2007. SCOPE: A Web server for practical de novo motif discovery. Nucleic Acids Res 35: W259-W264. doi: 10.1093/nar/gkm310.
10. Cherbas P, Cherbas L, Williams CM. 1977. Induction of acetylcholinesterase activity by b-ecdysone in a Drosophila cell line. Science 197: 275-277. (Pubitemid 8130442)
11. Cuddapah S, Jothi R, Schones DE, Roh TY, Cui K, Zhao K. 2009. Global analysis of the insulator binding protein CTCF in chromatin barrier regions reveals demarcation of active and repressive domains. Genome Res 19: 24-32.
12. Cuvier O, Hart CM, Laemmli UK. 1998. Identification of a class of chromatin boundary elements. Mol Cell Biol 18: 7478-7486. (Pubitemid 28533066)
13. Degner SC, Wong TP, Jankevicius G, Feeney AJ. 2009. Cutting edge: Developmental stage-specific recruitment of cohesin to CTCF sites throughout immunoglobulin loci during B lymphocyte development. J Immunol 182: 44-48.
14. Dennis G Jr, Sherman BT, Hosack DA, Yang J, Gao W, Lane HC, Lempicki RA. 2003. DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol 4: 3. doi: 10.1186/gb-2003-4-5-p3.
15. Emberly E, Blattes R, Schuettengruber B, Hennion M, Jiang N, Hart CM, Kas E, Cuvier O. 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.
16. Gaszner M, Felsenfeld G. 2006. Insulators: Exploiting transcriptional and epigenetic mechanisms. Nat Rev Genet 7: 703-713. Gateff E. 1978. Malignant neoplasms of genetic origin in Drosophila melanogaster. Science 200: 1448-1459. (Pubitemid 44260006)
17. Gerasimova TI, Corces VG. 1998. Polycomb and trithorax group proteins mediate the function of a chromatin insulator. Cell 92: 511-521. (Pubitemid 28101114)
18. Gerasimova TI, Gdula DA, Gerasimov DV, Simonova O, Corces VG. 1995. A Drosophila protein that imparts directionality on a chromatin insulator is an enhancer of position-effect variegation. Cell 82: 587-597.
19. Gerasimova TI, Lei EP, Bushey AM, Corces VG. 2007. Coordinated control of dCTCF and gypsy chromatin insulators in Drosophila. Mol Cell 28: 761-772. (Pubitemid 350217054)
20. Geyer PK, Corces VG. 1992. DNA position-specific repression of transcription by a Drosophila zinc finger protein. Genes & Dev 6: 1865-1873.
21. Golovnin A, Biryukova I, Romanova O, Silicheva M, Parshikov A, Savitskaya E, Pirrotta V, Georgiev P. 2003. An endogenous Su(Hw) insulator separates the yellow gene from the Achaetescute gene complex in Drosophila. Development 130: 3249-3258. (Pubitemid 36926961)
22. Gruzdeva N, Kyrchanova O, Parshikov A, Kullyev A, Georgiev P. 2005. The Mcp element from the bithorax complex contains an insulator that is capable of pairwise interactions and can facilitate enhancer-promoter communication. Mol Cell Biol 25: 3682-3689. (Pubitemid 40559574)
23. Hark AT, Schoenherr CJ, Katz DJ, Ingram RS, Levorse JM, Tilghman SM. 2000. CTCF mediates methylation-sensitive enhancer-blocking activity at the H19/Igf2 locus. Nature 405: 486-489. (Pubitemid 30367428)
24. Hart CM, Zhao K, Laemmli UK. 1997. The scs' boundary element: Characterization of boundary element-associated factors. Mol Cell Biol 17: 999-1009. (Pubitemid 27044398)
25. Holohan EE, Kwong C, Adryan B, Bartkuhn M, Herold M, Renkawitz R, Russell S, White R. 2007. CTCF genomic binding sites in Drosophila and the organisation of the bithorax complex. PLoS Genet 3: e112. doi: 10.1371/journal.pgen.0030112. (Pubitemid 47203971)
26. Hou C, Zhao H, Tanimoto K, Dean A. 2008. CTCF-dependent enhancer-blocking by alternative chromatin loop formation. Proc Natl Acad Sci 105: 20398-20403.
27. Kim TH, Abdullaev ZK, Smith AD, Ching KA, Loukinov DI, Green RD, Zhang MQ, Lobanenkov VV, Ren B. 2007. Analysis of the vertebrate insulator protein CTCF-binding sites in the human genome. Cell 128: 1231-1245. (Pubitemid 46427876)
28. Klenova E, Ohlsson R. 2005. Poly(ADP-ribosyl)ation and epigenetics. Is CTCF PARt of the plot? Cell Cycle 4: 96-101.
29. Kurukuti S, Tiwari VK, Tavoosidana G, Pugacheva E, Murrell A, Zhao Z, Lobanenkov V, Reik W, Ohlsson R. 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 103: 10684-10689. (Pubitemid 44078037)
30. Kyrchanova O, Toshchakov S, Parshikov A, Georgiev P. 2007. Study of the functional interaction between Mcp insulators from the Drosophila bithorax complex: Effects of insulator pairing on enhancer-promoter communication. Mol Cell Biol 27: 3035-3043. (Pubitemid 46581316)
31. Kyrchanova O, Toshchakov S, Podstreshnaya Y, Parshikov A, Georgiev P. 2008. Functional interaction between the Fab-7 and Fab-8 boundaries and the upstream promoter region in the Drosophila Abd-B gene. Mol Cell Biol 28: 4188-4195.
32. Lei EP, Corces VG. 2006. RNA interference machinery influences the nuclear organization of a chromatin insulator. Nat Genet 38: 936-941. (Pubitemid 44141664)
33. Liu X, Brutlag DL, Liu JS. 2001. BioProspector: Discovering conserved DNA motifs in upstream regulatory regions of coexpressed genes. Pac Symp Biocomput 2001: 127-138.
34. Maeda RK, Karch F. 2007. Making connections: Boundaries and insulators in Drosophila. Curr Opin Genet Dev 17: 394-399. (Pubitemid 350016895)
35. Mohan M, Bartkuhn M, Herold M, Philippen A, Heinl N, Bardenhagen I, Leers J, White RA, Renkawitz-Pohl R, Saumweber H, et al. 2007. The Drosophila insulator proteins CTCF and CP190 link enhancer blocking to body patterning. EMBO J 26: 4203-4214. (Pubitemid 47525162)
36. Murrell A, Heeson S, Reik W. 2004. Interaction between differentially methylated regions partitions the imprinted genes Igf2 and H19 into parent-specific chromatin loops. Nat Genet 36: 889-893. (Pubitemid 39014109)
37. 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. (Pubitemid 39586532)
38. Pant V, Kurukuti S, Pugacheva E, Shamsuddin S, Mariano P, Renkawitz R, Klenova E, Lobanenkov V, Ohlsson R. 2004. Mutation of a single CTCF target site within the H19 imprinting control region leads to loss of Igf2 imprinting and complex patterns of de novo methylation upon maternal inheritance. Mol Cell Biol 24: 3497-3504. (Pubitemid 38452088)
39. Parnell TJ, Viering MM, Skjesol A, Helou C, Kuhn EJ, Geyer PK. 2003. An endogenous suppressor of hairy-wing insulator separates regulatory domains in Drosophila. Proc Natl Acad Sci 100: 13436-13441. (Pubitemid 37444760)
40. Parnell TJ, Kuhn EJ, Gilmore BL, Helou C, Wold MS, Geyer PK. 2006. Identification of genomic sites that bind the Drosophila suppressor of Hairy-wing insulator protein. Mol Cell Biol 26: 5983-5993. (Pubitemid 44204518)
41. Pavesi G, Mereghetti P, Mauri G, Pesole G. 2004. Weeder Web: Discovery of transcription factor binding sites in a set of sequences from co-regulated genes. Nucleic Acids Res 32: W199-W203. doi: 10.1093/nar/gkh465. (Pubitemid 38997329)
42. Ramos E, Ghosh D, Baxter E, Corces VG. 2006. Genomic organization of gypsy chromatin insulators in Drosophila melanogaster. Genetics 172: 2337-2349.
43. Rodin S, Kyrchanova O, Pomerantseva E, Parshikov A, Georgiev P. 2007. New properties of Drosophila fab-7 insulator. Genetics 177: 113-121. (Pubitemid 47555835)
44. Schweinsberg S, Hagstrom K, Gohl D, Schedl P, Kumar RP, Mishra R, Karch F. 2004. The enhancer-blocking activity of the Fab-7 boundary from the Drosophila bithorax complex requires GAGA-factor-binding sites. Genetics 168: 1371-1384. (Pubitemid 40007353)
45. Splinter E, Heath H, Kooren J, Palstra RJ, Klous P, Grosveld F, Galjart N, de Laat W. 2006. CTCF mediates long-range chromatin looping and local histone modification in the b-globin locus. Genes & Dev 20: 2349-2354. (Pubitemid 44320383)
46. Wallace JA, Felsenfeld G. 2007. We gather together: Insulators and genome organization. Curr Opin Genet Dev 17: 400-407. (Pubitemid 350016897)
47. Yoon YS, Jeong S, Rong Q, Park KY, Chung JH, Pfeifer K. 2007. Analysis of the H19ICR insulator. Mol Cell Biol 27: 3499-3510. (Pubitemid 46685224)
48. Yu W, Ginjala V, Pant V, Chernukhin I, Whitehead J, Docquier F, Farrar D, Tavoosidana G, Mukhopadhyay R, Kanduri C, et al. 2004. Poly(ADP-ribosyl)ation regulatesCTCF-dependent chromatin insulation. Nat Genet 36: 1105-1110.
49. 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. (Pubitemid 38183274)
50. Zhao K, Hart CM, Laemmli UK. 1995. Visualization of chromosomal domains with boundary element-associated factor BEAF-32. Cell 81: 879-888.