BMP-dependent gene repression cascade in Drosophila eggshell patterning

Charbonnier, Enrica; Fuchs, Alisa; Cheung, Lily S.; Chayengia, Mrinal; Veikkolainen, Ville; Seyfferth, Janine; Shvartsman, Stanislav Y.; Pyrowolakis, George

doi:10.1016/j.ydbio.2015.02.004

Cited by 10 publications

(17 citation statements)

References 43 publications

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“…Brk is expressed in most follicle cells and is required for Br expression. Since brk expression is directly repressed by Dpp signaling in the anterior-most follicle cells, Br cannot be expressed in these cells (Charbonnier et al, 2015; Chen and Schüpbach, 2006; Shravage et al, 2007). …”

Section: Patterningmentioning

confidence: 99%

Epithelial Patterning, Morphogenesis, and Evolution: Drosophila Eggshell as a Model

2017

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Summary Understanding the mechanisms driving tissue and organ formation requires knowledge across scales. How do signaling pathways specify distinct tissue types? How does the patterning system control morphogenesis? How do these processes evolve? The Drosophila egg chamber, where EGF and BMP signaling intersect to specify unique cell types that construct epithelial tubes for specialized eggshell structures, has provided a tractable system to ask these questions. Work there has elucidated connections between scales of development, including across evolutionary scales, and fostered the development of quantitative modeling tools. These tools and general principles can be applied towards understanding other developmental processes across organisms.

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Section: Patterningmentioning

confidence: 99%

Epithelial Patterning, Morphogenesis, and Evolution: Drosophila Eggshell as a Model

2017

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“…In most cases, Dpp signaling directly accounts for the distribution of Brk by negatively regulating its transcription. Dpp-dependent repression of brk transcription requires the repressor Schnurri (Shn) and short DNA sequences, the silencer elements (SEs), present in the regulatory region of brk (Charbonnier et al, 2015;Marty et al, 2000;Müller et al, 2003;Pyrowolakis et al, 2004;Torres-Vazquez et al, 2001;Yao et al, 2008). Upon signal activation, Smad trimers consisting of two pMad and one Medea molecule bind directly to the SE, which comprises three minimal Smad-binding sites (GNC; N, any nucleotide) organized in the consensus GNCGNC(N) 5 GTCT (minimal Smad-binding sites in bold; Fig.…”

Section: Introductionmentioning

confidence: 99%

Sequence environment of BMP-dependent activating elements controls transcriptional responses to Dpp signaling in Drosophila

et al. 2019

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Intercellular signaling pathways activate transcription factors, which, along with tissue-specific co-factors, regulate expression of target genes. Responses to TGFβ/BMP signals are mediated by Smad proteins, which form complexes and accumulate in the nucleus to directly bind and regulate enhancers of BMP targets upon signaling. In Drosophila, gene activation by BMP signaling often requires, in addition to direct input by Smads, the signal-dependent removal of the transcriptional repressor Brk. Previous studies on enhancers of BMP-activated genes have defined a BMP-responsive motif, the AE, which integrates activatory and repressive input by the Smad complex and Brk, respectively. Here, we address whether sequence variations within the core AE sequences might endow the motif with additional properties accounting for qualitative and quantitative differences in BMP responses, including tissue specificity of transcriptional activation and differential sensitivity to Smad and Brk inputs. By analyzing and cross-comparing three distinct BMPresponsive enhancers from the genes wit and Dad in two different epithelia, the wing imaginal disc and the follicular epithelium, we demonstrate that differences in the AEs contribute neither to the observed tissue-restriction of BMP responses nor to differences in the utilization of the Smad and Brk branches for transcriptional activation. Rather, our results suggest that the cis-environment of the BMPresponse elements not only dictates tissue specificity but also differential sensitivity to the two BMP mediators.

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“…These effects are mediated by two distinct repression events, which are separated both in time and in space. The anterior repression depends on the anterior gradient of DPP signaling (2,17,23), which controls br through a two-tier cascade that involves repression of BRK, a direct target of DPP in multiple stages of Drosophila development (24)(25)(26). The posterior repression of br relies on the earlier phase of EGFR signaling, when the oocyte nucleus is located at the posterior of the oocyte.…”

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confidence: 99%

“…The DPP pathway controls only the late phase of br expression within the appendage primordia. The net effect of DPP is repressive and is fully dependent on BRK (23). Specifically, the DPP pathway directly represses brk in the anterior follicle cells, by acting through a well-characterized direct mechanism (Fig.…”

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Gene regulation during Drosophila eggshell patterning

Pyrowolakis

Veikkolainen

Yakoby

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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A common path to the formation of complex 3D structures starts with an epithelial sheet that is patterned by inductive cues that control the spatiotemporal activities of transcription factors. These activities are then interpreted by the cis-regulatory regions of the genes involved in cell differentiation and tissue morphogenesis. Although this general strategy has been documented in multiple developmental contexts, the range of experimental models in which each of the steps can be examined in detail and evaluated in its effect on the final structure remains very limited. Studies of the Drosophila eggshell patterning provide unique insights into the multiscale mechanisms that connect gene regulation and 3D epithelial morphogenesis. Here we review the current understanding of this system, emphasizing how the recent identification of cis-regulatory regions of genes within the eggshell patterning network enables mechanistic analysis of its spatiotemporal dynamics and evolutionary diversification. It appears that cis-regulatory changes can account for only some aspects of the morphological diversity of Drosophila eggshells, such as the prominent differences in the number of the respiratory dorsal appendages. Other changes, such as the appearance of the respiratory eggshell ridges, are caused by changes in the spatial distribution of inductive signals. Both types of mechanisms are at play in this rapidly evolving system, which provides an excellent model of developmental patterning and morphogenesis.enhancer | network | evolution | signal | dynamics

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BMP-dependent gene repression cascade in Drosophila eggshell patterning

Cited by 10 publications

References 43 publications

Epithelial Patterning, Morphogenesis, and Evolution: Drosophila Eggshell as a Model

Epithelial Patterning, Morphogenesis, and Evolution: Drosophila Eggshell as a Model

Sequence environment of BMP-dependent activating elements controls transcriptional responses to Dpp signaling in Drosophila

Gene regulation during Drosophila eggshell patterning

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