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PMID: 11604507 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

The gypsy insulator can act as a promoter-specific transcriptional stimulator.

Molecular and cellular biology ·Vol. 21 ·No. 22 ·2001-11-00 ·Pages 7714-20

Wei W, Brennan MD

Abstract

Insulators define chromosomal domains such that an enhancer in one domain cannot activate a promoter in a different domain. We show that the Drosophila gypsy insulator behaves as a cis-stimulatory element in the larval fat body. Transcriptional stimulation by the insulator is distance dependent, as expected for a promoter element as opposed to an enhancer. Stimulation of a test alcohol dehydrogenase promoter requires a binding site for a GATA transcription factor, suggesting that the insulator may be facilitating access of this DNA binding protein to the promoter. Short-range stimulation requires both the Suppressor of Hairy-wing protein and the Mod(mdg4)-62.7 protein encoded by the trithorax group gene mod(mdg4). In the absence of interaction with Mod(mdg4)-62.7, the insulator is converted into a short-range transcriptional repressor but retains some cis-stimulatory activity over longer distances. These results indicate that insulator and promoter sequences share important characteristics and are not entirely distinct. We propose that the gypsy insulator can function as a promoter element and may be analogous to promoter-proximal regulatory modules that integrate input from multiple distal enhancer sequences.

MeSH Terms
Alcohol Dehydrogenase/genetics Animals DNA-Binding Proteins/genetics,metabolism Drosophila/genetics Drosophila Proteins Gene Expression Regulation Genes, Insect Nuclear Proteins/genetics,metabolism Promoter Regions, Genetic Recombinant Proteins/genetics,metabolism Repressor Proteins/genetics,metabolism Retroelements Transcription Factors/genetics,metabolism Transcription, Genetic
Chemicals
DNA-Binding Proteins Drosophila Proteins Nuclear Proteins Recombinant Proteins Repressor Proteins Retroelements Transcription Factors mdg4 protein (gypsy) su(Hw) protein, Drosophila Alcohol Dehydrogenase
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Wei W
Department of Biochemistry and Molecular Biology, University of Louisville, Kentucky 40202, USA.
Brennan M D
References (60)
60 references, click to expand
  1. Transcriptional repression mediated by polycomb group proteins and other chromatin-associated repressors is selectively blocked by insulators.
    J Biol Chem. 2000 Jan 7;275(1):697-704 PMID: 10617669
  2. Interactions between the Su(Hw) and Mod(mdg4) proteins required for gypsy insulator function.
    EMBO J. 2001 May 15;20(10):2518-27 PMID: 11350941
  3. Genetic and molecular complexity of the position effect variegation modifier mod(mdg4) in Drosophila.
    Genetics. 2000 May;155(1):141-57 PMID: 10790390
  4. Deletion of an insulator element by the mutation facet-strawberry in Drosophila melanogaster.
    Genetics. 2000 Jul;155(3):1297-311 PMID: 10880489
  5. Functional studies of the BTB domain in the Drosophila GAGA and Mod(mdg4) proteins.
    Nucleic Acids Res. 2000 Oct 15;28(20):3864-70 PMID: 11024164
  6. Differences in insulator properties revealed by enhancer blocking assays on episomes.
    EMBO J. 2000 Nov 1;19(21):5864-74 PMID: 11060037
  7. Complex developmental regulation of the Drosophila affinidisjuncta alcohol dehydrogenase gene in Drosophila melanogaster.
    Dev Biol. 1988 Jan;125(1):64-74 PMID: 3119402
  8. The Drosophila su(Hw) gene, which controls the phenotypic effect of the gypsy transposable element, encodes a putative DNA-binding protein.
    Genes Dev. 1988 Oct;2(10):1205-15 PMID: 2462523
  9. The Drosophila melanogaster suppressor of Hairy-wing protein binds to specific sequences of the gypsy retrotransposon.
    Genes Dev. 1988 Nov;2(11):1414-23 PMID: 2850261
  10. Novel genes influencing the expression of the yellow locus and mdg4 (gypsy) in Drosophila melanogaster.
    Mol Gen Genet. 1989 Dec;220(1):121-6 PMID: 2558282
  11. A position-effect assay for boundaries of higher order chromosomal domains.
    Cell. 1991 Mar 8;64(5):941-50 PMID: 1848159
  12. Repression of hsp70 heat shock gene transcription by the suppressor of hairy-wing protein of Drosophila melanogaster.
    Mol Cell Biol. 1991 Apr;11(4):1894-900 PMID: 1900919
  13. A Drosophila Adh gene can be activated in trans by an enhancer.
    Nucleic Acids Res. 1991 Oct 25;19(20):5713-7 PMID: 1945848
  14. A group of scs elements function as domain boundaries in an enhancer-blocking assay.
    Mol Cell Biol. 1992 May;12(5):2424-31 PMID: 1569958
  15. Sequence of scs and scs' Drosophila DNA fragments with boundary function in the control of gene expression.
    Nucleic Acids Res. 1992 May 25;20(10):2604 PMID: 1598225
  16. The suppressor of Hairy-wing binding region is required for gypsy mutagenesis.
    Mol Gen Genet. 1992 May;233(1-2):65-70 PMID: 1318501
  17. DNA position-specific repression of transcription by a Drosophila zinc finger protein.
    Genes Dev. 1992 Oct;6(10):1865-73 PMID: 1327958
  18. The su(Hw) protein insulates expression of the Drosophila melanogaster white gene from chromosomal position-effects.
    EMBO J. 1993 Feb;12(2):435-42 PMID: 8382607
  19. A 5' element of the chicken beta-globin domain serves as an insulator in human erythroid cells and protects against position effect in Drosophila.
    Cell. 1993 Aug 13;74(3):505-14 PMID: 8348617
  20. Distance-independent inactivation of an enhancer by the suppressor of Hairy-wing DNA-binding protein of Drosophila.
    Genetics. 1993 Aug;134(4):1135-44 PMID: 8375652
  21. A leucine zipper domain of the suppressor of Hairy-wing protein mediates its repressive effect on enhancer function.
    Genes Dev. 1993 Oct;7(10):1966-78 PMID: 7916729
  22. The enhancer of position-effect variegation of Drosophila, E(var)3-93D, codes for a chromatin protein containing a conserved domain common to several transcriptional regulators.
    Proc Natl Acad Sci U S A. 1993 Dec 1;90(23):11376-80 PMID: 8248257
  23. Transcriptional activation: a complex puzzle with few easy pieces.
    Cell. 1994 Apr 8;77(1):5-8 PMID: 8156597
  24. 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 Jul;21(14):4807-17 PMID: 11416154
  25. A chromatin insulator determines the nuclear localization of DNA.
    Mol Cell. 2000 Nov;6(5):1025-35 PMID: 11106742
  26. Drosophila melanogaster mutations suppressible by the suppressor of Hairy-wing are insertions of a 7.3-kilobase mobile element.
    Proc Natl Acad Sci U S A. 1983 Mar;80(6):1678-82 PMID: 6300868
  27. Construction of improved M13 vectors using oligodeoxynucleotide-directed mutagenesis.
    Gene. 1983 Dec;26(1):101-6 PMID: 6323249
  28. Introduction of a functional P element into the germ-line of Drosophila hawaiiensis.
    Cell. 1984 Aug;38(1):147-51 PMID: 6088059
  29. The 87A7 chromomere. Identification of novel chromatin structures flanking the heat shock locus that may define the boundaries of higher order domains.
    J Mol Biol. 1985 Sep 20;185(2):341-58 PMID: 2997449
  30. On the molecular mechanism of gypsy-induced mutations at the yellow locus of Drosophila melanogaster.
    EMBO J. 1986 Oct;5(10):2657-62 PMID: 3096713
  31. Redundant cis-acting elements control expression of the Drosophila affinidisjuncta Adh gene in the larval fat body.
    Nucleic Acids Res. 1994 Apr 11;22(7):1257-64 PMID: 8165141
  32. 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 U S A. 1994 Oct 25;91(22):10717-21 PMID: 7938017
  33. The suppressor of Hairy-wing protein regulates the tissue-specific expression of the Drosophila gypsy retrotransposon.
    Genetics. 1995 Jan;139(1):215-28 PMID: 7705625
  34. A transcriptional role for conserved footprinting sequences within the larval promoter of a Drosophila alcohol dehydrogenase gene.
    J Mol Biol. 1995 Jun 2;249(2):259-69 PMID: 7783192
  35. 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
  36. The BTB/POZ domain: a new protein-protein interaction motif common to DNA- and actin-binding proteins.
    Cell Growth Differ. 1995 Sep;6(9):1193-8 PMID: 8519696
  37. ISWI, a member of the SWI2/SNF2 ATPase family, encodes the 140 kDa subunit of the nucleosome remodeling factor.
    Cell. 1995 Dec 15;83(6):1021-6 PMID: 8521502
  38. The DNA-binding and enhancer-blocking domains of the Drosophila suppressor of Hairy-wing protein.
    Mol Cell Biol. 1996 Jul;16(7):3381-92 PMID: 8668153
  39. Boundary and insulator elements in chromosomes.
    Curr Opin Genet Dev. 1996 Apr;6(2):185-92 PMID: 8722175
  40. Genetic and molecular analysis of the gypsy chromatin insulator of Drosophila.
    Proc Natl Acad Sci U S A. 1996 Sep 3;93(18):9378-83 PMID: 8790337
  41. Interaction between mutations in the suppressor of Hairy wing and modifier of mdg4 genes of Drosophila melanogaster affecting the phenotype of gypsy-induced mutations.
    Genetics. 1996 Feb;142(2):425-36 PMID: 8852842
  42. Fab-7 functions as a chromatin domain boundary to ensure proper segment specification by the Drosophila bithorax complex.
    Genes Dev. 1996 Dec 15;10(24):3202-15 PMID: 8985188
  43. Characterization of functional domains of the su(Hw) protein that mediate the silencing effect of mod(mdg4) mutations.
    Genetics. 1997 Jan;145(1):153-61 PMID: 9017397
  44. The gypsy insulator can function as a promoter-specific silencer in the Drosophila embryo.
    EMBO J. 1997 Apr 1;16(7):1732-41 PMID: 9130717
  45. The role of insulator elements in defining domains of gene expression.
    Curr Opin Genet Dev. 1997 Apr;7(2):242-8 PMID: 9115431
  46. Polycomb group repression is blocked by the Drosophila suppressor of Hairy-wing [su(Hw)] insulator.
    Genetics. 1998 Jan;148(1):331-9 PMID: 9475743
  47. Chromatin domain boundaries in the Bithorax complex.
    Cell Mol Life Sci. 1998 Jan;54(1):60-70 PMID: 9487387
  48. Polycomb and trithorax group proteins mediate the function of a chromatin insulator.
    Cell. 1998 Feb 20;92(4):511-21 PMID: 9491892
  49. Genomic cis-regulatory logic: experimental and computational analysis of a sea urchin gene.
    Science. 1998 Mar 20;279(5358):1896-902 PMID: 9506933
  50. Chromatin remodeling mediated by Drosophila GAGA factor and ISWI activates fushi tarazu gene transcription in vitro.
    Mol Cell Biol. 1998 May;18(5):2455-61 PMID: 9566866
  51. Going the distance: a current view of enhancer action.
    Science. 1998 Jul 3;281(5373):60-3 PMID: 9679020
  52. Cis-acting sequences contributing to expression of the Drosophila affinidisjuncta Adh gene in both larvae and adults.
    Insect Biochem Mol Biol. 1998 Nov;28(11):869-73 PMID: 9818387
  53. Distant liaisons: long-range enhancer-promoter interactions in Drosophila.
    Curr Opin Genet Dev. 1999 Oct;9(5):505-14 PMID: 10508687
  54. Enhancer blocking by the Drosophila gypsy insulator depends upon insulator anatomy and enhancer strength.
    Genetics. 1999 Oct;153(2):787-98 PMID: 10511558
  55. Polarity of transcriptional enhancement revealed by an insulator element.
    Proc Natl Acad Sci U S A. 2000 Dec 19;97(26):14518-23 PMID: 11114171
  56. The iab-7 polycomb response element maps to a nucleosome-free region of chromatin and requires both GAGA and pleiohomeotic for silencing activity.
    Mol Cell Biol. 2001 Feb;21(4):1311-8 PMID: 11158316
  57. Effects of cis arrangement of chromatin insulators on enhancer-blocking activity.
    Science. 2001 Jan 19;291(5503):493-5 PMID: 11161205
  58. Loss of insulator activity by paired Su(Hw) chromatin insulators.
    Science. 2001 Jan 19;291(5503):495-8 PMID: 11161206
  59. The GAGA factor of Drosophila interacts with SAP18, a Sin3-associated polypeptide.
    EMBO Rep. 2000 Sep;1(3):253-9 PMID: 11256608
  60. The genome sequence of Drosophila melanogaster.
    Science. 2000 Mar 24;287(5461):2185-95 PMID: 10731132
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
2001-11-00
Pages
7714-20
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC99942
Subset
IM
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