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.
Bantignies
Frédéric
F
Institute of Human Genetics, Centre National de la Recherche Scientifique, 34396 Montpellier 5, France.
Grimaud
Charlotte
C
Lavrov
Sergey
S
Gabut
Mathieu
M
Cavalli
Giacomo
G
D000818:Animals; D030801:Animals, Genetically Modified; D002467:Cell Nucleus / Q000235:genetics; D002843:Chromatin / Q000235:genetics; D002875:Chromosomes / Q000235:genetics*; D004268:DNA-Binding Proteins / Q000235:genetics; D004330:Drosophila / Q000196:embryology / Q000235:genetics*; D029721:Drosophila Proteins / Q000235:genetics*; D004625:Embryo, Nonmammalian; D005260:Female; D018507:Gene Expression Regulation, Developmental; D020868:Gene Silencing; D018398:Homeodomain Proteins / Q000235:genetics; D008297:Male; D008540:Meiosis; D008938:Mitosis; D063150:Polycomb Repressive Complex 1; D012045:Regulatory Sequences, Nucleic Acid; D014157:Transcription Factors; D014960:X Chromosome
C062393:Abd-B proteins, Drosophila; D002843:Chromatin; D004268:DNA-Binding Proteins; D029721:Drosophila Proteins; D018398:Homeodomain Proteins; C066770:Pc protein, Drosophila; D014157:Transcription Factors; C063460:Trl protein, Drosophila; D063150:Polycomb Repressive Complex 1