Home LiteratureArticle Details
PMID: 18560994 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

The nuclear organization of Polycomb/Trithorax group response elements in larval tissues of Drosophila melanogaster.

Fedorova E, Sadoni N, Dahlsveen IK, Koch J, Kremmer E, Eick D, Paro R, Zink D

Abstract

We analysed the nuclear organization of the Polycomb/Trithorax group response element (PRE/TRE) Fab-7 and of other PRE/TREs in larval tissues of D. melanogaster. The results show that pairing/clustering of transgenic and endogenous Fab-7 elements and of other endogenous PRE/TREs occurs only to a limited degree in a highly locus-specific and tissue-specific manner. However, transgenic Fab-7 elements as well as the Fab-7-regulated Abd-B gene and other endogenous loci preferentially occupied defined nuclear regions. Preferred association with the nuclear periphery was observed in the inactive state. However, also in the active state, Fab-7 was often found associated with the nuclear periphery as well as with the boundary of heterochromatin in a fly line- and tissue-specific manner. The boundary between heterochromatin and euchromatin revealed a highly complex architecture in the three-dimensional nuclear space with a close juxtaposition of active and repressed domains. The results suggest that such complex architectures create nuclear microenvironments sustaining specific states of activity of defined PRE/TREs. However, the data also show that the positional behaviour of the transgenic Fab-7 element does not apply to PRE/TREs in general. Altogether, this finding and the highly locus-, tissue-, and fly line-specific behaviour with regard to nuclear positioning and pairing/clustering suggest that the relationships between nuclear organization and functional regulation of PRE/TREs are highly complex and that simple models making general predictions might not be appropriate.

MeSH Terms
Animals Binding Sites Cell Nucleus/genetics Chromosomal Proteins, Non-Histone/genetics Drosophila Proteins/genetics,metabolism Drosophila melanogaster/genetics Epidermal Cells Green Fluorescent Proteins/metabolism Heterochromatin/metabolism Histones/metabolism In Situ Hybridization, Fluorescence Larva/genetics Nuclear Lamina/metabolism Polycomb-Group Proteins RNA Polymerase II/metabolism Repressor Proteins/genetics Response Elements/genetics Transgenes
Chemicals
Chromosomal Proteins, Non-Histone Drosophila Proteins Heterochromatin Histones Polycomb-Group Proteins Repressor Proteins enhanced green fluorescent protein trx protein, Drosophila Green Fluorescent Proteins RNA Polymerase II
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Fedorova Elena
Department Biologie II, Ludwig-Maximilians-Universität München, Grosshaderner Str. 2, 82152, Planegg-Martinsried, Germany.
Sadoni Nicolas
Dahlsveen Ina K
Koch Jeannette
Kremmer Elisabeth
Eick Dirk
Paro Renato
Zink Daniele
References (71)
71 references, click to expand
  1. Role of histone H3 lysine 27 methylation in Polycomb-group silencing.
    Science. 2002 Nov 1;298(5595):1039-43 PMID: 12351676
  2. Characterization of the Drosophila melanogaster genome at the nuclear lamina.
    Nat Genet. 2006 Sep;38(9):1005-14 PMID: 16878134
  3. Trithorax and dCBP acting in a complex to maintain expression of a homeotic gene.
    Science. 2001 Nov 9;294(5545):1331-4 PMID: 11701926
  4. The human polycomb group complex associates with pericentromeric heterochromatin to form a novel nuclear domain.
    J Cell Biol. 1998 Aug 24;142(4):887-98 PMID: 9722603
  5. The distribution of polycomb-group proteins during cell division and development in Drosophila embryos: impact on models for silencing.
    J Cell Biol. 1998 Apr 20;141(2):469-81 PMID: 9548724
  6. Nuclear distribution of transcription factors in relation to sites of transcription and RNA polymerase II.
    J Cell Sci. 1997 Aug;110 ( Pt 15):1781-91 PMID: 9264465
  7. Developmentally induced changes in transcriptional program alter spatial organization across chromosomes.
    Genes Dev. 2005 May 15;19(10):1188-98 PMID: 15905407
  8. Perinuclear localization of chromatin facilitates transcriptional silencing.
    Nature. 1998 Aug 6;394(6693):592-5 PMID: 9707122
  9. 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
  10. In vivo binding pattern of a trans-regulator of homoeotic genes in Drosophila melanogaster.
    Nature. 1989 Feb 2;337(6206):468-71 PMID: 2563569
  11. Mapping Polycomb-repressed domains in the bithorax complex using in vivo formaldehyde cross-linked chromatin.
    Cell. 1993 Dec 17;75(6):1187-98 PMID: 7903220
  12. Chromatin boundaries in budding yeast: the nuclear pore connection.
    Cell. 2002 May 31;109(5):551-62 PMID: 12062099
  13. Spatial positioning; a new dimension in genome function.
    Cell. 2004 Oct 15;119(2):153-6 PMID: 15479633
  14. The Drosophila trithorax protein binds to specific chromosomal sites and is co-localized with Polycomb at many sites.
    EMBO J. 1995 May 1;14(9):2056-65 PMID: 7744011
  15. Central role of Drosophila SU(VAR)3-9 in histone H3-K9 methylation and heterochromatic gene silencing.
    EMBO J. 2002 Mar 1;21(5):1121-31 PMID: 11867540
  16. The polyhomeotic gene of Drosophila encodes a chromatin protein that shares polytene chromosome-binding sites with Polycomb.
    Genes Dev. 1992 Feb;6(2):223-32 PMID: 1346609
  17. Genome-wide prediction of Polycomb/Trithorax response elements in Drosophila melanogaster.
    Dev Cell. 2003 Nov;5(5):759-71 PMID: 14602076
  18. Probes of chromatin accessibility in the Drosophila bithorax complex respond differently to Polycomb-mediated repression.
    EMBO J. 1996 Feb 1;15(3):569-80 PMID: 8599940
  19. Transvection and chromosomal trans-interaction effects.
    Biochim Biophys Acta. 1999 Jul 29;1424(1):M1-8 PMID: 10456029
  20. Binding of trithorax and Polycomb proteins to the bithorax complex: dynamic changes during early Drosophila embryogenesis.
    EMBO J. 1998 Sep 1;17(17):5141-50 PMID: 9724650
  21. Nup-PI: the nucleopore-promoter interaction of genes in yeast.
    Mol Cell. 2006 Feb 3;21(3):379-91 PMID: 16455493
  22. Polycomb/Trithorax response elements and epigenetic memory of cell identity.
    Development. 2007 Jan;134(2):223-32 PMID: 17185323
  23. Polycomb and polyhomeotic are constituents of a multimeric protein complex in chromatin of Drosophila melanogaster.
    EMBO J. 1992 Aug;11(8):2941-50 PMID: 1353445
  24. Neural induction promotes large-scale chromatin reorganisation of the Mash1 locus.
    J Cell Sci. 2006 Jan 1;119(Pt 1):132-40 PMID: 16371653
  25. Inheritance of Polycomb-dependent chromosomal interactions in Drosophila.
    Genes Dev. 2003 Oct 1;17(19):2406-20 PMID: 14522946
  26. Gene inactivation in Drosophila mediated by the Polycomb gene product or by position-effect variegation does not involve major changes in the accessibility of the chromatin fibre.
    Mol Gen Genet. 1994 May 25;243(4):453-62 PMID: 7911223
  27. Transcriptional silencing by the Polycomb protein in Drosophila embryos.
    EMBO J. 1995 Mar 15;14(6):1209-20 PMID: 7720711
  28. Polycomb group protein complexes exchange rapidly in living Drosophila.
    Development. 2005 Sep;132(17):3963-76 PMID: 16079157
  29. Chromatin and epigenetics in development: blending cellular memory with cell fate plasticity.
    Development. 2006 Jun;133(11):2089-94 PMID: 16672331
  30. Nuclear pore association confers optimal expression levels for an inducible yeast gene.
    Nature. 2006 Jun 8;441(7094):774-8 PMID: 16760983
  31. Epigenetic regulation of cellular memory by the Polycomb and Trithorax group proteins.
    Annu Rev Genet. 2004;38:413-43 PMID: 15568982
  32. The nuclear distribution of Polycomb during Drosophila melanogaster development shown with a GFP fusion protein.
    Chromosoma. 1999 May;108(2):83-94 PMID: 10382070
  33. Histone methyltransferase activity of a Drosophila Polycomb group repressor complex.
    Cell. 2002 Oct 18;111(2):197-208 PMID: 12408864
  34. Mapping functional domains of the polycomb protein of Drosophila melanogaster.
    Chromosome Res. 1995 Sep;3(6):351-60 PMID: 7551550
  35. Histone methyltransferase activity associated with a human multiprotein complex containing the Enhancer of Zeste protein.
    Genes Dev. 2002 Nov 15;16(22):2893-905 PMID: 12435631
  36. Related chromosome binding sites for zeste, suppressors of zeste and Polycomb group proteins in Drosophila and their dependence on Enhancer of zeste function.
    EMBO J. 1993 Apr;12(4):1513-22 PMID: 8467801
  37. Stabilization of chromatin structure by PRC1, a Polycomb complex.
    Cell. 1999 Jul 9;98(1):37-46 PMID: 10412979
  38. Genome-wide localization of the nuclear transport machinery couples transcriptional status and nuclear organization.
    Cell. 2004 May 14;117(4):427-39 PMID: 15137937
  39. The DNA-binding polycomb group protein pleiohomeotic mediates silencing of a Drosophila homeotic gene.
    Development. 1999 Sep;126(17):3905-13 PMID: 10433918
  40. SAGA and a novel Drosophila export complex anchor efficient transcription and mRNA export to NPC.
    EMBO J. 2007 Dec 12;26(24):4956-65 PMID: 18034162
  41. Drosophila enhancer of Zeste/ESC complexes have a histone H3 methyltransferase activity that marks chromosomal Polycomb sites.
    Cell. 2002 Oct 18;111(2):185-96 PMID: 12408863
  42. Association of transcriptionally silent genes with Ikaros complexes at centromeric heterochromatin.
    Cell. 1997 Dec 12;91(6):845-54 PMID: 9413993
  43. Chromatin unfolds.
    Cell. 1996 Jul 12;86(1):13-9 PMID: 8689680
  44. Chromatin multiprotein complexes involved in the maintenance of transcription patterns.
    Curr Opin Genet Dev. 1995 Apr;5(2):174-9 PMID: 7613086
  45. The Mcp element mediates stable long-range chromosome-chromosome interactions in Drosophila.
    Mol Biol Cell. 2006 May;17(5):2158-65 PMID: 16495335
  46. Structural basis for specific binding of Polycomb chromodomain to histone H3 methylated at Lys 27.
    Genes Dev. 2003 Aug 1;17(15):1823-8 PMID: 12897052
  47. Discrete Polycomb-binding sites in each parasegmental domain of the bithorax complex.
    Development. 1995 Jun;121(6):1681-9 PMID: 7600985
  48. Mechanisms of heritable gene repression during development of Drosophila.
    Curr Opin Cell Biol. 1993 Dec;5(6):999-1005 PMID: 7907493
  49. The mcp element from the Drosophila melanogaster bithorax complex mediates long-distance regulatory interactions.
    Genetics. 1999 Nov;153(3):1333-56 PMID: 10545463
  50. The Drosophila Fab-7 chromosomal element conveys epigenetic inheritance during mitosis and meiosis.
    Cell. 1998 May 15;93(4):505-18 PMID: 9604927
  51. In situ dissection of the Fab-7 region of the bithorax complex into a chromatin domain boundary and a Polycomb-response element.
    Development. 1997 May;124(9):1809-20 PMID: 9165128
  52. Histone methylation by the Drosophila epigenetic transcriptional regulator Ash1.
    Nature. 2002 Oct 24;419(6909):857-62 PMID: 12397363
  53. Histone trimethylation and the maintenance of transcriptional ON and OFF states by trxG and PcG proteins.
    Genes Dev. 2006 Aug 1;20(15):2041-54 PMID: 16882982
  54. Modulation of heat shock gene expression by the TAC1 chromatin-modifying complex.
    Nat Cell Biol. 2004 Feb;6(2):162-7 PMID: 14730313
  55. Transcription-dependent spatial arrangements of CFTR and adjacent genes in human cell nuclei.
    J Cell Biol. 2004 Sep 13;166(6):815-25 PMID: 15364959
  56. Transvection in the iab-5,6,7 region of the bithorax complex of Drosophila: homology independent interactions in trans.
    Genetics. 1995 Feb;139(2):815-33 PMID: 7713434
  57. From genetics to epigenetics: the tale of Polycomb group and trithorax group genes.
    Chromosome Res. 2006;14(4):363-75 PMID: 16821133
  58. ASH1, a Drosophila trithorax group protein, is required for methylation of lysine 4 residues on histone H3.
    Proc Natl Acad Sci U S A. 2003 Sep 30;100(20):11535-40 PMID: 13679578
  59. Molecular basis for the discrimination of repressive methyl-lysine marks in histone H3 by Polycomb and HP1 chromodomains.
    Genes Dev. 2003 Aug 1;17(15):1870-81 PMID: 12897054
  60. RNAi components are required for nuclear clustering of Polycomb group response elements.
    Cell. 2006 Mar 10;124(5):957-71 PMID: 16530043
  61. 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
  62. Genetic modification of heterochromatic association and nuclear organization in Drosophila.
    Nature. 1996 Jun 6;381(6582):529-31 PMID: 8632827
  63. The histone methyltransferases Trithorax and Ash1 prevent transcriptional silencing by Polycomb group proteins.
    EMBO Rep. 2004 Apr;5(4):373-7 PMID: 15031712
  64. The scalloped gene encodes a novel, evolutionarily conserved transcription factor required for sensory organ differentiation in Drosophila.
    Genes Dev. 1992 Mar;6(3):367-79 PMID: 1547938
  65. The Drosophila ash1 gene product, which is localized at specific sites on polytene chromosomes, contains a SET domain and a PHD finger.
    Genetics. 1996 Jun;143(2):913-28 PMID: 8725238
  66. Chromatin insulator elements block the silencing of a target gene by the Drosophila polycomb response element (PRE) but allow trans interactions between PREs on different chromosomes.
    Genetics. 1997 Sep;147(1):209-21 PMID: 9286681
  67. Perturbation of nuclear architecture by long-distance chromosome interactions.
    Cell. 1996 May 31;85(5):745-59 PMID: 8646782
  68. Chromatin complexes regulating gene expression in Drosophila.
    Curr Opin Genet Dev. 1995 Aug;5(4):466-72 PMID: 7580138
  69. Transcriptional silencing of homeotic genes in Drosophila.
    Bioessays. 1995 Sep;17(9):775-84 PMID: 8763830
  70. SAGA interacting factors confine sub-diffusion of transcribed genes to the nuclear envelope.
    Nature. 2006 Jun 8;441(7094):770-3 PMID: 16760982
  71. Mammalian WDR12 is a novel member of the Pes1-Bop1 complex and is required for ribosome biogenesis and cell proliferation.
    J Cell Biol. 2005 Aug 1;170(3):367-78 PMID: 16043514
Article Info
Journal
Chromosome research : an international journal on the molecular, supramolecular and evolutionary aspects of chromosome biology
Abbr.
Chromosome Res
ISSN
0967-3849
Published
2008-00-00
Epub
2008-00-03
Pages
649-73
Language
English
Region
Netherlands
NLM ID
9313452
Subset
IM
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