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Coordinate regulation of ribosomal protein gene transcription mediates embryonic secretory cell growth

ABSTRACT: Cell growth is well defined for the late (post-embryonic) stages of development, but evidence for early (embryonic) cell growth during post-mitotic morphogenesis is quite limited. Here, we identify early cell growth as a key characteristic of Drosophila embryonic salivary gland (SG) tubulogenesis. A BTB/POZ domain nuclear factor, Ribbon (Rib), mediates early cell growth without affecting endoreplication. Rib binds the transcription start site of nearly every SG-expressed ribosomal protein gene (RPG), and is required for full expression of all RPGs tested. Rib binding to RPG enhancers is, however, weak and not sequence-specific, suggesting that specificity is achieved through co-factor interactions. We demonstrate Rib’s ability to physically interact with each of the three known activators of RPG transcription. Surprisingly, Rib-dependent early cell growth in another tubular organ—the embryonic trachea—is not mediated by direct RPG transcription. Our results support a model for tissue-specific transcriptional regulation in early cell growth programs.

ORGANISM(S): Drosophila melanogaster

PROVIDER: GSE181361 | GEO | 2022/02/15

REPOSITORIES: GEO

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Project description:Transcription factors, which regulate the spatiotemporal patterns of gene expression during organogenesis, often regulate 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 changes 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 abnormal cell/organ shape in rib mutants occurred without compromising epithelial-specific morphological attributes such as apicobasal polarity and junctional integrity. To identify the genes regulated by Rib that control cell and organ shape, we performed ChIP-seq analysis in embryos driving rib expression specifically in the SGs. To learn if the Rib binding sites identified in the ChIP-seq analysis were linked to changes in gene expression through transcriptional activation, repression, or both, 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 of bound Rib most 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 shape change in the Drosophila salivary gland via a diverse array of targets through both transcriptional activation and repression. Furthermore, our results suggest that a critical component of the SG morphogenetic gene network involving Rib is its autoregulation. Three independent collections of stage 11 â 16 rib1/ribP7 embryos and three of wild-type embryos were used for hybridization to Drosophila Genome 2.0 Chips. Scanned intensity values were normalized using RMA (Partek software) and statistical analysis analyses were performed using the Spotfire software package (TIBCO). Target genes were identified as those that were upregulated/downregulated (1.5-fold change cutoff, P < 0.05) in rib1/ribP7 embryos when compared with Oregon R controls.

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Coordinate regulation of ribosomal protein gene transcription mediates embryonic secretory cell growth

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