title: Ribbon regulates morphogenesis of the Drosophila embryonic salivary gland through transcriptional activation and repression.
abstract: Transcription factors affect spatiotemporal patterns of gene expression often regulating multiple aspects of tissue morphogenesis, including cell-type specification, cell proliferation, cell death, cell polarity, cell shape, cell arrangement and cell migration. In this work, we describe a distinct role for Ribbon (Rib) in controlling cell shape/volume increases during elongation of the Drosophila salivary gland (SG). Notably, the morphogenetic changes in rib mutants occurred without effects on general SG cell attributes such as specification, proliferation and apoptosis. Moreover, the changes in cell shape/volume in rib mutants occurred without compromising epithelial-specific morphological attributes such as apicobasal polarity and junctional integrity. To identify the genes regulated by Rib, we performed ChIP-seq analysis in embryos driving expression of GFP-tagged Rib specifically in the SGs. To learn if the Rib binding sites identified in the ChIP-seq analysis were linked to changes in gene expression, we performed microarray analysis comparing RNA samples from age-matched wild-type and rib null embryos. From the superposed ChIP-seq and microarray gene expression data, we identified 60 genomic sites bound by Rib likely to regulate SG-specific gene expression. We confirmed several of the identified Rib targets by qRT-pCR and/or in situ hybridization. Our results indicate that Rib regulates cell growth and tissue shape in the Drosophila salivary gland via a diverse array of targets through both transcriptional activation and repression. Furthermore, our results suggest that autoregulation of rib expression may be a key component of the SG morphogenetic gene network.
authors.affiliation: Department of Cell Biology, Johns Hopkins University School of Medicine, Baltimore, MD 21205, United States.
authors.forename: Rajprasad
authors.initials: R
authors.lastname: Loganathan
authors.affiliation: Department of Biomedical Sciences, University of Minnesota Medical School, Duluth, MN 55812, United States.
authors.forename: Joslynn S
authors.initials: JS
authors.lastname: Lee
authors.affiliation: Department of Cell Biology, Johns Hopkins University School of Medicine, Baltimore, MD 21205, United States.
authors.forename: Michael B
authors.initials: MB
authors.lastname: Wells
authors.affiliation: Department of Cell Biology, Johns Hopkins University School of Medicine, Baltimore, MD 21205, United States.
authors.forename: Elizabeth
authors.initials: E
authors.lastname: Grevengoed
authors.affiliation: Department of Biomedical Sciences, University of Minnesota Medical School, Duluth, MN 55812, United States.
authors.forename: Matthew
authors.initials: M
authors.lastname: Slattery
authors.affiliation: Department of Cell Biology, Johns Hopkins University School of Medicine, Baltimore, MD 21205, United States. Electronic address: dandrew@jhmi.edu.
authors.forename: Deborah J
authors.initials: DJ
authors.lastname: Andrew
mesh_terms: D000818:Animals; D017209:Apoptosis / Q000235:genetics; D001483:Base Sequence; D001665:Binding Sites; D002455:Cell Division / Q000235:genetics; D016764:Cell Polarity / Q000235:genetics; D047369:Chromatin Immunoprecipitation; D016000:Cluster Analysis; D016384:Consensus Sequence; D003598:Cytoskeletal Proteins / Q000378:metabolism*; D029721:Drosophila Proteins / Q000378:metabolism*; D004331:Drosophila melanogaster / Q000166:cytology / Q000196:embryology / Q000235:genetics*; D004625:Embryo, Nonmammalian / Q000166:cytology / Q000378:metabolism*; D018507:Gene Expression Regulation, Developmental; D063990:Gene Ontology; D008954:Models, Biological; D008969:Molecular Sequence Data; D009024:Morphogenesis / Q000235:genetics*; D009154:Mutation / Q000235:genetics; D059372:Nucleotide Motifs / Q000235:genetics; D020411:Oligonucleotide Array Sequence Analysis; D009929:Organ Size; D011485:Protein Binding; D012097:Repressor Proteins / Q000378:metabolism*; D015203:Reproducibility of Results; D012469:Salivary Glands / Q000166:cytology / Q000196:embryology* / Q000378:metabolism; D017423:Sequence Analysis, RNA; D015533:Transcriptional Activation / Q000235:genetics*
chemical_list: D003598:Cytoskeletal Proteins; D029721:Drosophila Proteins; D012097:Repressor Proteins; C115864:rib protein, Drosophila
keywords: Drosophila; Morphogenesis; Ribbon; Salivary gland; Size control