Inheritance of Polycomb-dependent chromosomal interactions in Drosophila.

Maintenance of cell identity is a complex task that involves multiple layers of regulation, acting at all levels of chromatin packaging, from nucleosomes to folding of chromosomal domains in the cell nucleus. Polycomb-group (PcG) and trithorax-group (trxG) proteins maintain memory of chromatin states through binding at cis-regulatory elements named PcG response elements or cellular memory modules. Fab-7 is a well-defined cellular memory module involved in regulation of the homeotic gene Abdominal-B (Abd-B). In addition to its action in cis, we show here by three-dimensional FISH that the Fab-7 element leads to association of transgenes with each other or with the endogenous Fab-7, even when inserted in different chromosomes. These long-distance interactions enhance PcG-mediated silencing. They depend on PcG proteins, on DNA sequence homology, and on developmental progression. Once long-distance pairing is abolished by removal of the endogenous Fab-7, the derepressed chromatin state induced at the transgene locus can be transmitted through meiosis into a large fraction of the progeny, even after reintroduction of the endogenous Fab-7. Strikingly, meiotic inheritance of the derepressed state involves loss of pairing between endogenous and transgenic Fab-7. This suggests that transmission of nuclear architecture through cell division might contribute to inheritance of chromatin states in eukaryotes.

[1]  D. Tautz,et al.  A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback , 1989, Chromosoma.

[2]  G. Reuter,et al.  Isolation of dominant suppressor mutations for position-effect variegation in Drosophila melanogaster , 2004, Molecular and General Genetics MGG.

[3]  Roland Eils,et al.  Global Chromosome Positions Are Transmitted through Mitosis in Mammalian Cells , 2003, Cell.

[4]  V. Orlando.  Polycomb, Epigenomes, and Control of Cell Identity , 2003, Cell.

[5]  Thomas Cremer,et al.  Chromosome order in HeLa cells changes during mitosis and early G1, but is stably maintained during subsequent interphase stages , 2003, The Journal of cell biology.

[6]  W. Bickmore,et al.  Considering Nuclear Compartmentalization in the Light of Nuclear Dynamics , 2003, Cell.

[7]  R. Paro,et al.  Transcription through Intergenic Chromosomal Memory Elements of the Drosophila Bithorax Complex Correlates with an Epigenetic Switch , 2002, Molecular and Cellular Biology.

[8]  Christian Beisel,et al.  Histone methylation by the Drosophila epigenetic transcriptional regulator Ash1 , 2002, Nature.

[9]  R. Paro,et al.  A cellular memory module conveys epigenetic inheritance of hedgehog expression during Drosophila wing imaginal disc development. , 2002, Genes & development.

[10]  V. Pirrotta.  Silence in the Germ , 2002, Cell.

[11]  Tom Misteli,et al.  Chromosome positioning in the interphase nucleus. , 2002, Trends in cell biology.

[12]  Giacomo Cavalli.  Chromatin as a eukaryotic template of genetic information. , 2002, Current opinion in cell biology.

[13]  T. Mahmoudi,et al.  GAGA can mediate enhancer function in trans by linking two separate DNA molecules , 2002, The EMBO journal.

[14]  J. Birchler,et al.  RNAi related mechanisms affect both transcriptional and posttranscriptional transgene silencing in Drosophila. , 2002, Molecular cell.

[15]  J. Kassis.  Pairing-sensitive silencing, polycomb group response elements, and transposon homing in Drosophila. , 2002, Advances in genetics.

[16]  Gregory J. Hannon,et al.  Insight Review Articles , 2022 .

[17]  C. Croce,et al.  Trithorax and dCBP Acting in a Complex to Maintain Expression of a Homeotic Gene , 2001, Science.

[18]  R. Kingston,et al.  A Drosophila Polycomb group complex includes Zeste and dTAFII proteins , 2001, Nature.

[19]  V. Orlando,et al.  General transcription factors bind promoters repressed by Polycomb group proteins , 2001, Nature.

[20]  T. Cremer,et al.  Chromosome territories, nuclear architecture and gene regulation in mammalian cells , 2001, Nature Reviews Genetics.

[21]  S. Gasser,et al.  Positions of Potential:Nuclear Organization and Gene Expression , 2001, Cell.

[22]  V. Orlando,et al.  Drosophila chromosome condensation proteins Topoisomerase II and Barren colocalize with Polycomb and maintain Fab-7 PRE silencing. , 2001, Molecular cell.

[23]  N. Dillon,et al.  Transcription Factor Dosage Affects Changes in Higher Order Chromatin Structure Associated with Activation of a Heterochromatic Gene , 2000, Cell.

[24]  S. Grewal,et al.  A Chromodomain Protein, Swi6, Performs Imprinting Functions in Fission Yeast during Mitosis and Meiosis , 2000, Cell.

[25]  Phillip D. Zamore,et al.  RNA Interference , 2000, Science.

[26]  T. Kornberg,et al.  GFP-tagged balancer chromosomes for Drosophila melanogaster , 1999, Mechanisms of Development.

[27]  V. Pirrotta,et al.  The mcp element from the Drosophila melanogaster bithorax complex mediates long-distance regulatory interactions. , 1999, Genetics.

[28]  R. Paro,et al.  Epigenetic inheritance of active chromatin after removal of the main transactivator. , 1999, Science.

[29]  Mark Groudine,et al.  A Functional Enhancer Suppresses Silencing of a Transgene and Prevents Its Localization Close to Centromeric Heterochromatin , 1999, Cell.

[30]  M. Fujioka,et al.  Trithorax- and Polycomb-Group Response Elements within an Ultrabithorax Transcription Maintenance Unit Consist of Closely Situated but Separable Sequences , 1999, Molecular and Cellular Biology.

[31]  P. Verveer,et al.  Homologous association of the Bithorax-Complex during embryogenesis: consequences for transvection in Drosophila melanogaster. , 1998, Development.

[32]  R. Paro,et al.  Binding of Trithorax and Polycomb proteins to the bithorax complex: dynamic changes during early Drosophila embryogenesis , 1998, The EMBO journal.

[33]  P. Freemont,et al.  The Human Polycomb Group Complex Associates with Pericentromeric Heterochromatin to Form a Novel Nuclear Domain , 1998, The Journal of cell biology.

[34]  R. Paro,et al.  The Drosophila Fab-7 Chromosomal Element Conveys Epigenetic Inheritance during Mitosis and Meiosis , 1998, Cell.

[35]  S. Henikoff,et al.  Trans-Sensing Effects: The Ups and Downs of Being Together , 1998, Cell.

[36]  H. Strutt,et al.  The Distribution of Polycomb-Group Proteins During Cell Division and Development in Drosophila Embryos: Impact on Models for Silencing , 1998, The Journal of cell biology.

[37]  B. Turner,et al.  Transient Inhibition of Histone Deacetylation Alters the Structural and Functional Imprint at Fission Yeast Centromeres , 1997, Cell.

[38]  Matthias Merkenschlager,et al.  Association of Transcriptionally Silent Genes with Ikaros Complexes at Centromeric Heterochromatin , 1997, Cell.

[39]  A. Murray,et al.  Interphase chromosomes undergo constrained diffusional motion in living cells , 1997, Current Biology.

[40]  C. Sigrist,et al.  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. , 1997, Genetics.

[41]  J. Birchler,et al.  Cosuppression in Drosophila: Gene Silencing of Alcohol dehydrogenase by white-Adh Transgenes Is Polycomb Dependent , 1997, Cell.

[42]  P. Schedl,et al.  A Polycomb and GAGA dependent silencer adjoins the Fab-7 boundary in the Drosophila bithorax complex. , 1997, Genetics.

[43]  R. Paro,et al.  Co‐localization of Polycomb protein and GAGA factor on regulatory elements responsible for the maintenance of homeotic gene expression , 1997, The EMBO journal.

[44]  Tom Misteli,et al.  The dynamics of a pre-mRNA splicing factor in living cells , 1997, Nature.

[45]  F. Karch,et al.  In situ dissection of the Fab-7 region of the bithorax complex into a chromatin domain boundary and a Polycomb-response element. , 1997, Development.

[46]  P. Cook.  The transcriptional basis of chromosome pairing. , 1997, Journal of cell science.

[47]  Mark J Alkema,et al.  Identification of Bmi1-interacting proteins as constituents of a multimeric mammalian polycomb complex. , 1997, Genes & development.

[48]  P. Schedl,et al.  Fab-7 functions as a chromatin domain boundary to ensure proper segment specification by the Drosophila bithorax complex. , 1996, Genes & development.

[49]  M. Levine,et al.  The Fab-7 element of the bithorax complex attenuates enhancer-promoter interactions in the Drosophila embryo. , 1996, Genes & development.

[50]  S. Henikoff,et al.  Genetic modification of heterochromatic association and nuclear organization in Drosophila , 1996, Nature.

[51]  D. Arndt-Jovin,et al.  FISH in whole‐mount Drosophila embryos. RNA: activation of a transcriptional locus, DNA: gene architecture and expression , 1996 .

[52]  D. Agard,et al.  Perturbation of Nuclear Architecture by Long-Distance Chromosome Interactions , 1996, Cell.

[53]  R. Paro,et al.  Drosophila Polycomb‐group regulated chromatin inhibits the accessibility of a trans‐activator to its target DNA. , 1995, The EMBO journal.

[54]  V. Pirrotta,et al.  White gene expression, repressive chromatin domains and homeotic gene regulation in Drosophila , 1994, BioEssays : news and reviews in molecular, cellular and developmental biology.

[55]  V. Pirrotta,et al.  A Polycomb response element in the Ubx gene that determines an epigenetically inherited state of repression. , 1994, The EMBO journal.

[56]  M. Fauvarque,et al.  polyhomeotic regulatory sequences induce developmental regulator-dependent variegation and targeted P-element insertions in Drosophila. , 1993, Genes & development.

[57]  M. Palazzolo,et al.  The scalloped gene encodes a novel, evolutionarily conserved transcription factor required for sensory organ differentiation in Drosophila. , 1992, Genes & development.

[58]  F. Karch,et al.  A new homeotic mutation in the Drosophila bithorax complex removes a boundary separating two domains of regulation. , 1990, The EMBO journal.

[59]  D. Kuhn,et al.  Paternal imprinting of inversion Uab1 causes homeotic transformations in Drosophila. , 1988, Genetics.