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      The Wg and Dpp morphogens regulate gene expression by modulating the frequency of transcriptional bursts

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          Abstract

          Morphogen signaling contributes to the patterned spatiotemporal expression of genes during development. One mode of regulation of signaling-responsive genes is at the level of transcription. Single-cell quantitative studies of transcription have revealed that transcription occurs intermittently, in bursts. Although the effects of many gene regulatory mechanisms on transcriptional bursting have been studied, it remains unclear how morphogen gradients affect this dynamic property of downstream genes. Here we have adapted single molecule fluorescence in situ hybridization (smFISH) for use in the Drosophila wing imaginal disc in order to measure nascent and mature mRNA of genes downstream of the Wg and Dpp morphogen gradients. We compared our experimental results with predictions from stochastic models of transcription, which indicated that the transcription levels of these genes appear to share a common method of control via burst frequency modulation. Our data help further elucidate the link between developmental gene regulatory mechanisms and transcriptional bursting.

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          Most cited references 63

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          Exact stochastic simulation of coupled chemical reactions

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            Wnt/β-catenin signaling and disease.

            The WNT signal transduction cascade controls myriad biological phenomena throughout development and adult life of all animals. In parallel, aberrant Wnt signaling underlies a wide range of pathologies in humans. In this Review, we provide an update of the core Wnt/β-catenin signaling pathway, discuss how its various components contribute to disease, and pose outstanding questions to be addressed in the future. Copyright © 2012 Elsevier Inc. All rights reserved.
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              Regulation of chromatin by histone modifications.

              Chromatin is not an inert structure, but rather an instructive DNA scaffold that can respond to external cues to regulate the many uses of DNA. A principle component of chromatin that plays a key role in this regulation is the modification of histones. There is an ever-growing list of these modifications and the complexity of their action is only just beginning to be understood. However, it is clear that histone modifications play fundamental roles in most biological processes that are involved in the manipulation and expression of DNA. Here, we describe the known histone modifications, define where they are found genomically and discuss some of their functional consequences, concentrating mostly on transcription where the majority of characterisation has taken place.
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                Author and article information

                Contributors
                Role: Reviewing Editor
                Role: Senior Editor
                Journal
                eLife
                Elife
                eLife
                eLife
                eLife Sciences Publications, Ltd
                2050-084X
                22 June 2020
                2020
                : 9
                Affiliations
                [1 ]Department of Molecular Biosciences, Northwestern University EvanstonUnited States
                [2 ]NSF-Simons Center for Quantitative Biology, Northwestern University EvanstonUnited States
                [3 ]Department of Engineering Sciences and Applied Mathematics, Northwestern University EvanstonUnited States
                Baylor College of Medicine United States
                University of California, Los Angeles United States
                Baylor College of Medicine United States
                Article
                56076
                10.7554/eLife.56076
                7340504
                32568073
                © 2020, Bakker et al

                This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

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                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/100000002, National Institutes of Health;
                Award ID: R35GM118144
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000002, National Institutes of Health;
                Award ID: T32CA080621
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000001, National Science Foundation;
                Award ID: 1764421
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000893, Simons Foundation;
                Award ID: 597491
                Award Recipient :
                The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
                Categories
                Research Article
                Developmental Biology
                Custom metadata
                Experimental results in Drosophila support a model in which gene expression is fundamentally controlled by morphogens tuning the same transcription parameter for genes that are expressed in highly diverse patterns.

                Life sciences

                d. melanogaster, burst frequency, morphogen, wing disc

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