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PMID: 12750332 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Telomeric associated sequences of Drosophila recruit polycomb-group proteins in vivo and can induce pairing-sensitive repression.

Genetics ·Vol. 164 ·No. 1 ·2003-05-00 ·Pages 195-208

Boivin A, Gally C, Netter S, Anxolabéhère D, Ronsseray S

Abstract

In Drosophila, relocation of a euchromatic gene near centromeric or telomeric heterochromatin often leads to its mosaic silencing. Nevertheless, modifiers of centromeric silencing do not affect telomeric silencing, suggesting that each location requires specific factors. Previous studies suggest that a subset of Polycomb-group (PcG) proteins could be responsible for telomeric silencing. Here, we present the effect on telomeric silencing of 50 mutant alleles of the PcG genes and of their counteracting trithorax-group genes. Several combinations of two mutated PcG genes impair telomeric silencing synergistically, revealing that some of these genes are required for telomeric silencing. In situ hybridization and immunostaining experiments on polytene chromosomes revealed a strict correlation between the presence of PcG proteins and that of heterochromatic telomeric associated sequences (TASs), suggesting that TASs and PcG complexes could be associated at telomeres. Furthermore, lines harboring a transgene containing an X-linked TAS subunit and the mini-white reporter gene can exhibit pairing-sensitive repression of the white gene in an orientation-dependent manner. Finally, an additional binding site for PcG proteins was detected at the insertion site of this type of transgene. Taken together, these results demonstrate that PcG proteins bind TASs in vivo and may be major players in Drosophila telomeric position effect (TPE).

MeSH Terms
Animals DNA-Binding Proteins/genetics,metabolism Drosophila/genetics Drosophila Proteins/genetics,metabolism Gene Expression Regulation Genes, Reporter Polycomb Repressive Complex 1 Telomere Transcription Factors
Chemicals
DNA-Binding Proteins Drosophila Proteins Pc protein, Drosophila Transcription Factors Trl protein, Drosophila Polycomb Repressive Complex 1
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Boivin Antoine
Laboratoire Dynamique du Génome, Institut Jacques Monod UMR 7592, Universités Paris 6 et 7, 75005 Paris, France.
Gally Christelle
Netter Sophie
Anxolabéhère Dominique
Ronsseray Stéphane
References (62)
62 references, click to expand
  1. Epigenetic inheritance of active chromatin after removal of the main transactivator.
    Science. 1999 Oct 29;286(5441):955-8 PMID: 10542150
  2. Analysis of subtelomeric heterochromatin in the Drosophila minichromosome Dp1187 by single P element insertional mutagenesis.
    Genetics. 1992 Nov;132(3):737-53 PMID: 1334894
  3. The genomic silencing of position-effect variegation in Drosophila melanogaster: interaction between the heterochromatin-associated proteins Su(var)3-7 and HP1.
    J Cell Sci. 2000 Dec;113 Pt 23:4253-61 PMID: 11069770
  4. The Polycomb group--no longer an exclusive club?
    Curr Opin Genet Dev. 2001 Apr;11(2):175-81 PMID: 11250141
  5. Maternal expression of genes that regulate the bithorax complex of Drosophila melanogaster.
    Dev Biol. 1986 Dec;118(2):442-56 PMID: 3098596
  6. A complex genetic locus, polyhomeotic, is required for segmental specification and epidermal development in D. melanogaster.
    Cell. 1987 Dec 4;51(5):829-39 PMID: 2890438
  7. A stable genomic source of P element transposase in Drosophila melanogaster.
    Genetics. 1988 Mar;118(3):461-70 PMID: 2835286
  8. Dosage-dependent modifiers of polycomb and antennapedia mutations in Drosophila.
    Proc Natl Acad Sci U S A. 1988 Nov;85(21):8136-40 PMID: 3141923
  9. Maintenance of the engrailed expression pattern by Polycomb group genes in Drosophila.
    Development. 1992 Nov;116(3):805-10 PMID: 1363229
  10. Preferential transposition of Drosophila P elements to nearby chromosomal sites.
    Genetics. 1993 Feb;133(2):347-59 PMID: 8382177
  11. Drosophila melanogaster does not share the telomeric repeat sequence of another invertebrate, Ascaris lumbricoides.
    Mol Gen Genet. 1993 Jan;236(2-3):440-2 PMID: 8437589
  12. Elements of the Drosophila bithorax complex that mediate repression by Polycomb group products.
    Dev Biol. 1993 Jul;158(1):131-44 PMID: 8101171
  13. polyhomeotic regulatory sequences induce developmental regulator-dependent variegation and targeted P-element insertions in Drosophila.
    Genes Dev. 1993 Aug;7(8):1508-20 PMID: 8101825
  14. Maternal repression of the P element promoter in the germline of Drosophila melanogaster: a model for the P cytotype.
    Genetics. 1993 Sep;135(1):149-60 PMID: 8224815
  15. A Polycomb response element in the Ubx gene that determines an epigenetically inherited state of repression.
    EMBO J. 1994 Jun 1;13(11):2553-64 PMID: 7912192
  16. The Trithorax-like gene encodes the Drosophila GAGA factor.
    Nature. 1994 Oct 27;371(6500):806-8 PMID: 7935842
  17. Transposition of the LINE-like retrotransposon TART to Drosophila chromosome termini.
    Proc Natl Acad Sci U S A. 1994 Dec 20;91(26):12510-4 PMID: 7809068
  18. Genetic interactions and dosage effects of Polycomb group genes of Drosophila.
    Mol Gen Genet. 1995 Feb 6;246(3):291-300 PMID: 7854314
  19. Interactions of polyhomeotic with Polycomb group genes of Drosophila melanogaster.
    Genetics. 1994 Dec;138(4):1151-62 PMID: 7896097
  20. Identification of Polycomb and trithorax group responsive elements in the regulatory region of the Drosophila homeotic gene Sex combs reduced.
    Genetics. 1995 Feb;139(2):797-814 PMID: 7713433
  21. Position effect at S. cerevisiae telomeres: reversible repression of Pol II transcription.
    Cell. 1990 Nov 16;63(4):751-62 PMID: 2225075
  22. The unusual telomeres of Drosophila.
    Trends Genet. 1995 Feb;11(2):58-62 PMID: 7716808
  23. A genetic analysis of the Suppressor 2 of zeste complex of Drosophila melanogaster.
    Genetics. 1995 May;140(1):139-81 PMID: 7635282
  24. Mapping functional domains of the polycomb protein of Drosophila melanogaster.
    Chromosome Res. 1995 Sep;3(6):351-60 PMID: 7551550
  25. Regulation of polyhomeotic transcription may involve local changes in chromatin activity in Drosophila.
    Mech Dev. 1995 Aug;52(2-3):343-55 PMID: 8541220
  26. Drosophila Polycomb-group regulated chromatin inhibits the accessibility of a trans-activator to its target DNA.
    EMBO J. 1995 Nov 15;14(22):5660-71 PMID: 8521823
  27. DNA organization and polymorphism of a wild-type Drosophila telomere region.
    Chromosoma. 1995 Dec;104(4):229-41 PMID: 8565699
  28. A P element containing suppressor of hairy-wing binding regions has novel properties for mutagenesis in Drosophila melanogaster.
    Genetics. 1995 Nov;141(3):1061-74 PMID: 8582613
  29. The Drosophila Polycomb group gene Sex comb on midleg (Scm) encodes a zinc finger protein with similarity to polyhomeotic protein.
    Development. 1996 May;122(5):1621-30 PMID: 8625848
  30. Genetic modification of heterochromatic association and nuclear organization in Drosophila.
    Nature. 1996 Jun 6;381(6582):529-31 PMID: 8632827
  31. Perturbation of nuclear architecture by long-distance chromosome interactions.
    Cell. 1996 May 31;85(5):745-59 PMID: 8646782
  32. Keratin 14 and 19 expression in normal, dysplastic and malignant oral epithelia. A study using in situ hybridization and immunohistochemistry.
    J Oral Pathol Med. 1996 Jul;25(6):293-301 PMID: 8887072
  33. PcG complexes and chromatin silencing.
    Curr Opin Genet Dev. 1997 Apr;7(2):249-58 PMID: 9115424
  34. A Polycomb and GAGA dependent silencer adjoins the Fab-7 boundary in the Drosophila bithorax complex.
    Genetics. 1997 Aug;146(4):1365-80 PMID: 9258680
  35. SU(VAR)3-7, a Drosophila heterochromatin-associated protein and companion of HP1 in the genomic silencing of position-effect variegation.
    EMBO J. 1997 Sep 1;16(17):5280-8 PMID: 9311988
  36. A silencer is required for maintenance of transcriptional repression throughout Drosophila development.
    Development. 1997 Nov;124(21):4343-50 PMID: 9334282
  37. The Additional sex combs gene of Drosophila encodes a chromatin protein that binds to shared and unique Polycomb group sites on polytene chromosomes.
    Development. 1998 Apr;125(7):1207-16 PMID: 9477319
  38. The Drosophila Fab-7 chromosomal element conveys epigenetic inheritance during mitosis and meiosis.
    Cell. 1998 May 15;93(4):505-18 PMID: 9604927
  39. Unfolding the mysteries of heterochromatin.
    Curr Opin Genet Dev. 1998 Apr;8(2):147-53 PMID: 9610404
  40. A conserved sequence motif in Polycomb-response elements.
    Mol Cell. 1998 Jun;1(7):1065-6 PMID: 9651590
  41. Expression and properties of wild-type and mutant forms of the Drosophila sex comb on midleg (SCM) repressor protein.
    Genetics. 1998 Oct;150(2):675-86 PMID: 9755199
  42. In vivo chromatin accessibility correlates with gene silencing in Drosophila.
    Genetics. 1998 Dec;150(4):1539-49 PMID: 9832530
  43. The heterochromatin protein 1 prevents telomere fusions in Drosophila.
    Mol Cell. 1998 Nov;2(5):527-38 PMID: 9844626
  44. Directional gene silencing induced by a complex subtelomeric satellite from Drosophila.
    Chromosoma. 1998 Nov;107(5):311-20 PMID: 9880764
  45. Silencing at Drosophila telomeres: nuclear organization and chromatin structure play critical roles.
    EMBO J. 1999 Jul 1;18(13):3724-35 PMID: 10393187
  46. Stabilization of chromatin structure by PRC1, a Polycomb complex.
    Cell. 1999 Jul 9;98(1):37-46 PMID: 10412979
  47. Telomere position effect in human cells.
    Science. 2001 Jun 15;292(5524):2075-7 PMID: 11408657
  48. Terminal retrotransposons activate a subtelomeric white transgene at the 2L telomere in Drosophila.
    Genetics. 2001 Jul;158(3):1111-23 PMID: 11454760
  49. Reconstitution of a functional core polycomb repressive complex.
    Mol Cell. 2001 Sep;8(3):545-56 PMID: 11583617
  50. P-Element repression in Drosophila melanogaster by variegating clusters of P-lacZ-white transgenes.
    Genetics. 2001 Dec;159(4):1631-42 PMID: 11779802
  51. Modifiers of terminal deficiency-associated position effect variegation in Drosophila.
    Genetics. 2002 Mar;160(3):995-1009 PMID: 11901117
  52. Transformation of white locus DNA in drosophila: dosage compensation, zeste interaction, and position effects.
    Cell. 1984 Feb;36(2):469-81 PMID: 6319027
  53. Dosage-dependent modifiers of position effect variegation in Drosophila and a mass action model that explains their effect.
    Genetics. 1988 Sep;120(1):181-98 PMID: 3146523
  54. The ash-1, ash-2 and trithorax genes of Drosophila melanogaster are functionally related.
    Genetics. 1989 Mar;121(3):517-25 PMID: 2497049
  55. Genetic interactions of the suppressor 2 of zeste region genes.
    Dev Genet. 1989;10(3):249-60 PMID: 2500288
  56. Mutations in polycombeotic, a Drosophila polycomb-group gene, cause a wide range of maternal and zygotic phenotypes.
    Genetics. 1990 May;125(1):91-101 PMID: 2341036
  57. Clonal analysis of segmental and compartmental homoeotic transformations in polycomb mutants of Drosophila melanogaster.
    Dev Biol. 1990 Oct;141(2):306-18 PMID: 1976555
  58. Mutation in a heterochromatin-specific chromosomal protein is associated with suppression of position-effect variegation in Drosophila melanogaster.
    Proc Natl Acad Sci U S A. 1990 Dec;87(24):9923-7 PMID: 2124708
  59. Long range repression conferring boundaries of Ultrabithorax expression in the Drosophila embryo.
    EMBO J. 1991 Nov;10(11):3147-55 PMID: 1680676
  60. The Drosophila gene escargot encodes a zinc finger motif found in snail-related genes.
    Mech Dev. 1992 Feb;36(3):117-27 PMID: 1571289
  61. Ten different Polycomb group genes are required for spatial control of the abdA and AbdB homeotic products.
    Development. 1992 Feb;114(2):493-505 PMID: 1350533
  62. The mcp element from the Drosophila melanogaster bithorax complex mediates long-distance regulatory interactions.
    Genetics. 1999 Nov;153(3):1333-56 PMID: 10545463
Article Info
Journal
Genetics
Abbr.
Genetics
ISSN
0016-6731
Published
2003-05-00
Pages
195-208
Language
English
Region
United States
NLM ID
0374636
PMCID
PMC1462534
Subset
IM
Analysis Services
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