Home LiteratureArticle Details
PMID: 19443682 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

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

Genes & development ·Vol. 23 ·No. 11 ·2009-06-01 ·Pages 1338-50

Bushey AM, Ramos E, Corces VG

Abstract

Insulators are protein-bound DNA elements that are thought to play a role in chromatin organization and the regulation of gene expression by mediating intra- and interchromosomal interactions. Suppressor of Hair-wing [Su(Hw)] and Drosophila CTCF (dCTCF) insulators are found at distinct loci throughout the Drosophila melanogaster genome and function by recruiting an additional protein, Centrosomal Protein 190 (CP190). We performed chromatin immunoprecipitation (ChIP) and microarray analysis (ChIP-chip) experiments with whole-genome tiling arrays to compare Su(Hw), dCTCF, boundary element-associated factor (BEAF), and CP190 localization on DNA in two different cell lines and found evidence that BEAF is a third subclass of CP190-containing insulators. The DNA-binding proteins Su(Hw), dCTCF, and BEAF show unique distribution patterns with respect to the location and expression level of genes, suggesting diverse roles for these three subclasses of insulators in genome organization. Notably, cell line-specific localization sites for all three DNA-binding proteins as well as CP190 indicate multiple levels at which insulators can be regulated to affect gene expression. These findings suggest a model in which insulator subclasses may have distinct functions that together organize the genome in a cell type-specific manner, resulting in differential regulation of gene expression.

MeSH Terms
Animals CCCTC-Binding Factor Chromatin Immunoprecipitation DNA-Binding Proteins Drosophila Proteins Drosophila melanogaster/cytology,genetics,growth & development,metabolism Gene Expression Regulation Genome, Insect/genetics Insulator Elements/genetics Microtubule-Associated Proteins Nuclear Proteins Protein Array Analysis Protein Transport Repressor Proteins
Chemicals
CCCTC-Binding Factor CP190 protein, Drosophila CTCF protein, Drosophila DNA-Binding Proteins Drosophila Proteins Microtubule-Associated Proteins Nuclear Proteins Repressor Proteins su(Hw) protein, Drosophila
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Bushey Ashley M
Department of Biology, Emory University, Atlanta, Georgia 30322, USA.
Ramos Edward
Corces Victor G
References (51)
51 references, click to expand
  1. Poly(ADP-ribosyl)ation and epigenetics. Is CTCF PARt of the plot?
    Cell Cycle. 2005 Jan;4(1):96-101 PMID: 15655363
  2. Coordinated control of dCTCF and gypsy chromatin insulators in Drosophila.
    Mol Cell. 2007 Dec 14;28(5):761-72 PMID: 18082602
  3. Interaction between differentially methylated regions partitions the imprinted genes Igf2 and H19 into parent-specific chromatin loops.
    Nat Genet. 2004 Aug;36(8):889-93 PMID: 15273689
  4. We gather together: insulators and genome organization.
    Curr Opin Genet Dev. 2007 Oct;17(5):400-7 PMID: 17913488
  5. The ubiquitin ligase dTopors directs the nuclear organization of a chromatin insulator.
    Mol Cell. 2005 Oct 7;20(1):105-16 PMID: 16209949
  6. Fitting a mixture model by expectation maximization to discover motifs in biopolymers.
    Proc Int Conf Intell Syst Mol Biol. 1994;2:28-36 PMID: 7584402
  7. Polycomb and trithorax group proteins mediate the function of a chromatin insulator.
    Cell. 1998 Feb 20;92(4):511-21 PMID: 9491892
  8. DNA position-specific repression of transcription by a Drosophila zinc finger protein.
    Genes Dev. 1992 Oct;6(10):1865-73 PMID: 1327958
  9. CTCF mediates methylation-sensitive enhancer-blocking activity at the H19/Igf2 locus.
    Nature. 2000 May 25;405(6785):486-9 PMID: 10839547
  10. SUMO conjugation attenuates the activity of the gypsy chromatin insulator.
    EMBO J. 2006 May 3;25(9):1906-14 PMID: 16628226
  11. A Drosophila protein that imparts directionality on a chromatin insulator is an enhancer of position-effect variegation.
    Cell. 1995 Aug 25;82(4):587-97 PMID: 7664338
  12. CTCF tethers an insulator to subnuclear sites, suggesting shared insulator mechanisms across species.
    Mol Cell. 2004 Jan 30;13(2):291-8 PMID: 14759373
  13. Analysis of the H19ICR insulator.
    Mol Cell Biol. 2007 May;27(9):3499-510 PMID: 17339341
  14. An endogenous Su(Hw) insulator separates the yellow gene from the Achaete-scute gene complex in Drosophila.
    Development. 2003 Jul;130(14):3249-58 PMID: 12783795
  15. BioProspector: discovering conserved DNA motifs in upstream regulatory regions of co-expressed genes.
    Pac Symp Biocomput. 2001;:127-38 PMID: 11262934
  16. The scs' boundary element: characterization of boundary element-associated factors.
    Mol Cell Biol. 1997 Feb;17(2):999-1009 PMID: 9001253
  17. Protein:protein interactions and the pairing of boundary elements in vivo.
    Genes Dev. 2003 Mar 1;17(5):664-75 PMID: 12629048
  18. Insulators: exploiting transcriptional and epigenetic mechanisms.
    Nat Rev Genet. 2006 Sep;7(9):703-13 PMID: 16909129
  19. Identification of genomic sites that bind the Drosophila suppressor of Hairy-wing insulator protein.
    Mol Cell Biol. 2006 Aug;26(16):5983-93 PMID: 16880510
  20. BEAF regulates cell-cycle genes through the controlled deposition of H3K9 methylation marks into its conserved dual-core binding sites.
    PLoS Biol. 2008 Dec 23;6(12):2896-910 PMID: 19108610
  21. An endogenous suppressor of hairy-wing insulator separates regulatory domains in Drosophila.
    Proc Natl Acad Sci U S A. 2003 Nov 11;100(23):13436-41 PMID: 14597701
  22. SCOPE: a web server for practical de novo motif discovery.
    Nucleic Acids Res. 2007 Jul;35(Web Server issue):W259-64 PMID: 17485471
  23. DAVID: Database for Annotation, Visualization, and Integrated Discovery.
    Genome Biol. 2003;4(5):P3 PMID: 12734009
  24. 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. 2004 Apr;24(8):3497-504 PMID: 15060168
  25. Methylation of a CTCF-dependent boundary controls imprinted expression of the Igf2 gene.
    Nature. 2000 May 25;405(6785):482-5 PMID: 10839546
  26. CTCF-dependent enhancer-blocking by alternative chromatin loop formation.
    Proc Natl Acad Sci U S A. 2008 Dec 23;105(51):20398-403 PMID: 19074263
  27. Induction of acetylcholinesterase activity by beta-ecdysone in a Drosophila cell line.
    Science. 1977 Jul 15;197(4300):275-7 PMID: 877552
  28. Malignant neoplasms of genetic origin in Drosophila melanogaster.
    Science. 1978 Jun 30;200(4349):1448-59 PMID: 96525
  29. Global analysis of the insulator binding protein CTCF in chromatin barrier regions reveals demarcation of active and repressive domains.
    Genome Res. 2009 Jan;19(1):24-32 PMID: 19056695
  30. Identification of a class of chromatin boundary elements.
    Mol Cell Biol. 1998 Dec;18(12):7478-86 PMID: 9819433
  31. The enhancer-blocking activity of the Fab-7 boundary from the Drosophila bithorax complex requires GAGA-factor-binding sites.
    Genetics. 2004 Nov;168(3):1371-84 PMID: 15579691
  32. Poly(ADP-ribosyl)ation regulates CTCF-dependent chromatin insulation.
    Nat Genet. 2004 Oct;36(10):1105-10 PMID: 15361875
  33. Active promoters and insulators are marked by the centrosomal protein 190.
    EMBO J. 2009 Apr 8;28(7):877-88 PMID: 19229299
  34. Visualization of chromosomal domains with boundary element-associated factor BEAF-32.
    Cell. 1995 Jun 16;81(6):879-89 PMID: 7781065
  35. Genomic mapping of Suppressor of Hairy-wing binding sites in Drosophila.
    Genome Biol. 2007;8(8):R167 PMID: 17705839
  36. Making connections: boundaries and insulators in Drosophila.
    Curr Opin Genet Dev. 2007 Oct;17(5):394-9 PMID: 17904351
  37. CTCF mediates long-range chromatin looping and local histone modification in the beta-globin locus.
    Genes Dev. 2006 Sep 1;20(17):2349-54 PMID: 16951251
  38. Study of the functional interaction between Mcp insulators from the Drosophila bithorax complex: effects of insulator pairing on enhancer-promoter communication.
    Mol Cell Biol. 2007 Apr;27(8):3035-43 PMID: 17283051
  39. Genomic organization of gypsy chromatin insulators in Drosophila melanogaster.
    Genetics. 2006 Apr;172(4):2337-49 PMID: 16452134
  40. Analysis of the vertebrate insulator protein CTCF-binding sites in the human genome.
    Cell. 2007 Mar 23;128(6):1231-45 PMID: 17382889
  41. New properties of Drosophila fab-7 insulator.
    Genetics. 2007 Sep;177(1):113-21 PMID: 17890362
  42. CTCF genomic binding sites in Drosophila and the organisation of the bithorax complex.
    PLoS Genet. 2007 Jul;3(7):e112 PMID: 17616980
  43. Visualization of chromatin domains created by the gypsy insulator of Drosophila.
    J Cell Biol. 2003 Aug 18;162(4):565-74 PMID: 12925706
  44. The Drosophila insulator proteins CTCF and CP190 link enhancer blocking to body patterning.
    EMBO J. 2007 Oct 3;26(19):4203-14 PMID: 17805343
  45. 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. 2005 May;25(9):3682-9 PMID: 15831473
  46. The centrosomal protein CP190 is a component of the gypsy chromatin insulator.
    Mol Cell. 2004 Dec 3;16(5):737-48 PMID: 15574329
  47. Weeder Web: discovery of transcription factor binding sites in a set of sequences from co-regulated genes.
    Nucleic Acids Res. 2004 Jul 1;32(Web Server issue):W199-203 PMID: 15215380
  48. RNA interference machinery influences the nuclear organization of a chromatin insulator.
    Nat Genet. 2006 Aug;38(8):936-41 PMID: 16862159
  49. Cutting edge: developmental stage-specific recruitment of cohesin to CTCF sites throughout immunoglobulin loci during B lymphocyte development.
    J Immunol. 2009 Jan 1;182(1):44-8 PMID: 19109133
  50. 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 U S A. 2006 Jul 11;103(28):10684-9 PMID: 16815976
  51. Functional interaction between the Fab-7 and Fab-8 boundaries and the upstream promoter region in the Drosophila Abd-B gene.
    Mol Cell Biol. 2008 Jun;28(12):4188-95 PMID: 18426914
Article Info
Journal
Genes & development
Abbr.
Genes Dev
ISSN
1549-5477
Published
2009-06-01
Epub
2009-00-14
Pages
1338-50
Language
English
Region
United States
NLM ID
8711660
PMCID
PMC2701583
Subset
IM
Grants
NCI NIH HHS · K01 CA133106 · United States
NIGMS NIH HHS · R01 GM035463 · United States
NIGMS NIH HHS · GM35463 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com