Inheritance of Polycomb-dependent chromosomal interactions in Drosophila

• Published in: Genes & development 2003-10, Vol.17 (19), p.2406-2420
• Main Authors: Bantignies, Frédéric, Grimaud, Charlotte, Lavrov, Sergey, Gabut, Mathieu, Cavalli, Giacomo
• Format: Article
• Language: English
• Subjects: Abdominal-B gene; Animals; Animals, Genetically Modified; Cell Nucleus - genetics; Chromatin - genetics; Chromosomes - genetics; DNA-Binding Proteins - genetics; Drosophila; Drosophila - embryology; Drosophila - genetics; Drosophila Proteins - genetics; Embryo, Nonmammalian; epigenetics; Fab-7 gene; Female; Gene Expression Regulation, Developmental; Gene Silencing; Homeodomain Proteins - genetics; Male; Meiosis; Mitosis; polycomb group proteins; Polycomb Repressive Complex 1; Regulatory Sequences, Nucleic Acid; Research Papers; Transcription Factors; X Chromosome
• ISSN: 0890-9369; 1549-5477
• DOI: 10.1101/gad.269503

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.