Dampened regulates the activating potency of Bicoid and the embryonic patterning outcome in Drosophila

The Drosophila morphogen gradient of Bicoid (Bcd) initiates anterior–posterior (AP) patterning; however, it is poorly understood how its ability to activate a target gene may have an impact on this process. Here we report an F-box protein, Dampened (Dmpd) as a nuclear cofactor of Bcd that can enhance its activating potency. We establish a quantitative platform to specifically investigate two parameters of a Bcd target gene response, expression amplitude and boundary position. We show that embryos lacking Dmpd have a reduced amplitude of Bcd-activated hunchback (hb) expression at a critical time of development. This is because of a reduced Bcd-dependent transcribing probability. This defect is faithfully propagated further downstream of the AP-patterning network to alter the spatial characteristics of even-skipped (eve) stripes. Thus, unlike another Bcd-interacting F-box protein Fate-shifted (Fsd), which controls AP patterning through regulating the Bcd gradient profile, Dmpd achieves its patterning role through regulating the activating potency of Bcd. The morphogen Bicoid regulates anterior–posterior patterning in the early Drosophila embryo by locally activating its target genes such as hunchback. Here, the authors identify the F-box protein Dampened as a regulator of Bicoid-dependent transcriptional activation of hunchback.

• Publication year

  2013

• Venue

  Nature Communications

• Publication date

  2013-12-16

• Fields of study

  Biology, Medicine

• Identifiers
  DOI 10.1038/ncomms3968PMID 24336107PMCID 3902774
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• Adaptation of the length scale and amplitude of the Bicoid gradient profile to achieve robust patterning in abnormally large Drosophila melanogaster embryos

  2014cited by this paper
• Uncovering a Dynamic Feature of the Transcriptional Regulatory Network for Anterior-Posterior Patterning in the Drosophila Embryo

  2013cited by this paper
• A Spatial Point Pattern Analysis in Drosophila Blastoderm Embryos Evaluating the Potential Inheritance of Transcriptional States

  2013cited by this paper
• Precise developmental gene expression arises from globally stochastic transcriptional activity.

  2013cited by this paper
• Supplemental Information Quantitative Imaging of Transcription in Living Drosophila Embryos Links Polymerase Activity to Patterning

  2013cited by this paper
• Paused Pol II coordinates tissue morphogenesis in the Drosophila embryo.

  2013cited by this paper
• Live Imaging of Bicoid-Depe

  2013cited by this paper
• Ubiquitin and proteasomes in transcription.

  2012cited by this paper
• A system of repressor gradients spatially organizes the boundaries of Bicoid-dependent target genes.

  2012cited by this paper
• Report Precision of Hunchback Expression in the Drosophila Embryo

  2012cited by this paper
• Drosophila Bicoid is a substrate of sumoylation and its activator function is subject to inhibition by this post‐translational modification

  2012cited by this paper
• A systematic phenotypic screen of F-box genes through a tissue-specific RNAi-based approach in Drosophila.

  2012cited by this paper
• Evaluating the Drosophila Bicoid morphogen gradient system through dissecting the noise in transcriptional bursts

  2012cited by this paper
• Insights from studying Bicoid protein degradation

  2011cited by this paper
• Scaling of the Bicoid morphogen gradient by a volume-dependent production rate

  2011cited by this paper
• The snail repressor inhibits release, not elongation, of paused Pol II in the Drosophila embryo.

  2011cited by this paper
• Morphogen gradient formation and action

  2011cited by this paper
• A Multiscale Investigation of Bicoid-Dependent Transcriptional Events in Drosophila Embryos

  2011cited by this paper
• A Two-Dimensional Simulation Model of the Bicoid Gradient in Drosophila

  2010cited by this paper
• Fates-shifted, a novel F-box protein that targets Bicoid for degradation, regulates developmental fate determination in Drosophila embryos

  2010cited by this paper
• The time to measure positional information: maternal Hunchback is required for the synchrony of the Bicoid transcriptional response at the onset of zygotic transcription

  2010cited by this paper
• Morphogen gradient formation.

  2009cited by this paper
• SnapShot: F box proteins I.

  2009cited by this paper
• SnapShot: F Box Proteins II.

  2009cited by this paper
• The F-box Protein β-TrCp1/Fbw1a Interacts with p300 to Enhance β-Catenin Transcriptional Activity*

  2009cited by this paper
• Probing intrinsic properties of a robust morphogen gradient in Drosophila.

  2008cited by this paper
• Precise registration of gene expression boundaries by a repressive morphogen in Drosophila.

  2008cited by this paper
• Gene regulation: boundaries within limits.

  2008cited by this paper
• Pre-Steady-State Decoding of the Bicoid Morphogen Gradient

  2007cited by this paper
• Probing the limits to positional information.

  2007cited by this paper
• F-box proteins: the key to protein degradation.

  2006cited by this paper
• Keeping transcriptional activators under control.

  2006cited by this paper
• The F box protein Dsg1/Mdm30 is a transcriptional coactivator that stimulates Gal4 turnover and cotranscriptional mRNA processing.

  2005cited by this paper
• Bicoid determines sharp and precise target gene expression in the Drosophila embryo.

  2005cited by this paper
• Crossing the line between activation and repression.

  2005cited by this paper
• Seeing Is Believing The Bicoid Morphogen Gradient Matures

  2004cited by this paper
• The SCF ubiquitin ligase: insights into a molecular machine

  2004cited by this paper
• Dynamic control of positional information in the early Drosophila embryo

  2004cited by this paper
• The F-box protein Skp2 participates in c-Myc proteosomal degradation and acts as a cofactor for c-Myc-regulated transcription.

  2003cited by this paper
• Diverse roles for ubiquitin-dependent proteolysis in transcriptional activation

  2003cited by this paper
• Live imaging of endogenous RNA reveals a diffusion and entrapment mechanism for nanos mRNA localization in Drosophila.

  2003cited by this paper
• How the ubiquitin–proteasome system controls transcription

  2003cited by this paper
• Skp2 regulates Myc protein stability and activity.

  2003cited by this paper
• Establishment of developmental precision and proportions in the early Drosophila embryo

  2002cited by this paper
• Emerging Roles of Ubiquitin in Transcription Regulation

  2002cited by this paper
• The activity of the Drosophila morphogenetic protein Bicoid is inhibited by a domain located outside its homeodomain.

  2002cited by this paper
• Drosophila Pin1 prolyl isomerase Dodo is a MAP kinase signal responder during oogenesis

  2001cited by this paper
• Target Selectivity of Bicoid Is Dependent on Nonconsensus Site Recognition and Protein-Protein Interaction

  2000cited by this paper
• Cdc53/cullin and the essential Hrt1 RING-H2 subunit of SCF define a ubiquitin ligase module that activates the E2 enzyme Cdc34.

  1999cited by this paper
• Components of an SCF ubiquitin ligase localize to the centrosome and regulate the centrosome duplication cycle.

  1999cited by this paper
• Bicoid functions without its TATA-binding protein-associated factor interaction domains.

  1999cited by this paper
• SCF and Cullin/Ring H2-based ubiquitin ligases.

  1999cited by this paper
• Recognition of multiple patterns of DNA sites by Drosophila homeodomain protein Bicoid.

  1999cited by this paper
• Localization of ASH1 mRNA particles in living yeast.

  1998cited by this paper
• The eve stripe 2 enhancer employs multiple modes of transcriptional synergy.

  1996cited by this paper
• The Drosophila morphogenetic protein Bicoid binds DNA cooperatively.

  1996cited by this paper
• Posterior stripe expression of hunchback is driven from two promoters by a common enhancer element.

  1995cited by this paper
• Synergy between the hunchback and bicoid morphogens is required for anterior patterning in Drosophila.

  1994cited by this paper
• Control of Drosophila body pattern by the hunchback morphogen gradient.

  1992cited by this paper
• Progression of the cell cycle through mitosis leads to abortion of nascent transcripts.

  1991cited by this paper
• Rescue of bicoid mutant Drosophila embryos by Bicoid fusion proteins containing heterologous activating sequences

  1989cited by this paper
• The gradient morphogen bicoid is a concentration-dependent transcriptional activator.

  1989cited by this paper
• The bicoid protein is a positive regulator of hunchback transcription in the early Drosophila embryo

  1989cited by this paper
• The bicoid protein determines position in the Drosophila embryo in a concentration-dependent manner.

  1988cited by this paper
• The role of localization of bicoid RNA in organizing the anterior pattern of the Drosophila embryo.

  1988cited by this paper
• A gradient of bicoid protein in Drosophila embryos.

  1988cited by this paper
• Identification and expression of the gap segmentation gene hunchback in Drosophila melanogaster.

  1988cited by this paper
• GAL4-VP16 is an unusually potent transcriptional activator

  1988cited by this paper
• Finger protein of novel structure encoded by hunchback, a second member of the gap class of Drosophila segmentation genes

  1987cited by this paper
• Studies of nuclear and cytoplasmic behaviour during the five mitotic cycles that precede gastrulation in Drosophila embryogenesis.

  1983cited by this paper
• Cellular and Molecular Life Sciences REVIEW The gap gene network

  year unknowncited by this paper

• Deep learning-based high-resolution time inference for deciphering dynamic gene regulation from fixed embryos

  2025cites this paper
• Shaping the scaling characteristics of gap gene expression patterns in Drosophila

  2023cites this paper
• Uncovering gene-family founder events during major evolutionary transitions in animals, plants and fungi using GenEra

  2022cites this paper
• Patterning principles of morphogen gradients

  2022cites this paper
• Tonality over a broad frequency range is linked to vocal learning in birds

  2022cites this paper
• Locally correlated kinetics of post-replication DNA methylation reveals processivity and region specificity in DNA methylation maintenance

  2021cites this paper
• Differential regulation of alternative promoters emerges from unified kinetics of enhancer-promoter interaction

  2021cites this paper
• A matter of time: Formation and interpretation of the Bicoid morphogen gradient.

  2020cites this paper
• Enhancer Interactions in Developmental Gene Regulation

  2019cites this paper
• Modularity, criticality, and evolvability of a developmental gene regulatory network

  2018cites this paper
• Dissecting the sharp response of a canonical developmental enhancer reveals multiple sources of cooperativity

  2018cites this paper
• Detection and Quantification of the Bicoid Concentration Gradient in Drosophila Embryos.

  2018cites this paper
• Seeing is believing: the Bicoid protein reveals its path

  2018cites this paper
• Maternal AP determinants in the Drosophila oocyte and embryo

  2016cites this paper
• Time to move on: Modeling transcription dynamics during an embryonic transition away from maternal control

  2016cites this paper
• Probing the impact of temperature on molecular events in a developmental system

  2015cites this paper
• The Presence of Nuclear Cactus in the Early Drosophila Embryo May Extend the Dynamic Range of the Dorsal Gradient

  2015cites this paper
• Modulation of temporal dynamics of gene transcription by activator potency in the Drosophila embryo

  2015cites this paper
• Fundamental origins and limits for scaling a maternal morphogen gradient

  2015cites this paper
• Adaptation of the length scale and amplitude of the Bicoid gradient profile to achieve robust patterning in abnormally large Drosophila melanogaster embryos

  2014cites this paper