Dorsal-Ventral Gene Expression in the Drosophila Embryo Reflects the Dynamics and Precision of the Dorsal Nuclear Gradient

Reeves, Gregory T.; Trisnadi, Nathanie; Truong, Thai V.; Nahmad, Marcos; Katz, Sophie; Stathopoulos, Angelike

doi:10.1016/j.devcel.2011.12.007

Cited by 113 publications

(239 citation statements)

References 42 publications

(75 reference statements)

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“…It has been previously shown that Dorsal, a maternal morphogen that is required for twist transcription, is active in a gradient along the ventral-lateral axis with highest nuclear levels in the most ventral cells (Kanodia et al, 2009;Reeves et al, 2012). twist expression levels have previously been described as being uniform across the central region of the ventral furrow with a gradient of twist at the edge of the furrow, where cells stretch (Leptin, 1991).…”

Section: An Upstream Regulator Of Contractility T48 Exists In a Gramentioning

confidence: 99%

Actomyosin-based tissue folding requires a multicellular myosin gradient

Heer

Miller

Chanet

et al. 2017

Journal of Cell Science

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Tissue folding promotes three-dimensional (3D) form during development. In many cases, folding is associated with myosin accumulation at the apical surface of epithelial cells, as seen in the vertebrate neural tube and the Drosophila ventral furrow. This type of folding is characterized by constriction of apical cell surfaces, and the resulting cell shape change is thought to cause tissue folding. Here, we use quantitative microscopy to measure the pattern of transcription, signaling, myosin activation and cell shape in the Drosophila mesoderm. We found that cells within the ventral domain accumulate different amounts of active apical non-muscle myosin 2 depending on the distance from the ventral midline. This gradient in active myosin depends on a newly quantified gradient in upstream signaling proteins. A 3D continuum model of the embryo with induced contractility demonstrates that contractility gradients, but not contractility per se, promote changes to surface curvature and folding. As predicted by the model, experimental broadening of the myosin domain in vivo disrupts tissue curvature where myosin is uniform. Our data argue that apical contractility gradients are important for tissue folding.

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Section: An Upstream Regulator Of Contractility T48 Exists In a Gramentioning

confidence: 99%

Actomyosin-based tissue folding requires a multicellular myosin gradient

Heer

Miller

Chanet

et al. 2017

Journal of Cell Science

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“…The nuclear concentration of Bicoid during the final five nuclear cycles remains mostly constant during each nuclear cycle, indicating that Bicoid itself activates transcription of AP genes at a constant rate through these nuclear cycles (Gregor et al 2007). In contrast, the protein product of the maternal gene dorsal, found in a DV gradient, increases in concentration within nuclei during each of the final five nuclear cycles (Reeves et al 2012). This increase in nuclear Dorsal concentration suggests that the DV network is activated differently at each nuclear cycle, both by Dorsal itself, and by a network of transcription factors that respond to different levels of Dorsal.…”

mentioning

confidence: 98%

“…In Drosophila melanogaster, the MZT takes place within the first 3 hr of development, during the late syncytial nuclear divisions and ending at the cellular blastoderm stage with gastrulation (Foe and Alberts 1983;Pritchard and Schubiger 1996;Tadros and Lipshitz 2009). Gene expression during the MZT is highly dynamic, with patterns of zygotic genes first being established and changing between and within nuclear cycles (Stathopoulos and Levine 2005;Reeves et al 2012). It is clear, therefore, that each syncytial nuclear cycle can be treated as a single, or even multiple developmental time points.…”

mentioning

confidence: 99%

Quantitative Single-Embryo Profile ofDrosophilaGenome Activation and the Dorsal–Ventral Patterning Network

Sandler¹,

Stathopoulos

2016

Genetics

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During embryonic development of Drosophila melanogaster, the maternal-to-zygotic transition (MZT) marks a significant and rapid turning point when zygotic transcription begins and control of development is transferred from maternally deposited transcripts. Characterizing the sequential activation of the genome during the MZT requires precise timing and a sensitive assay to measure changes in expression. We utilized the NanoString nCounter instrument, which directly counts messenger RNA transcripts without reverse transcription or amplification, to study .70 genes expressed along the dorsal-ventral (DV) axis of early Drosophila embryos, dividing the MZT into 10 time points. Transcripts were quantified for every gene studied at all time points, providing the first dataset of absolute numbers of transcripts during Drosophila development. We found that gene expression changes quickly during the MZT, with early nuclear cycle 14 (NC14) the most dynamic time for the embryo. twist is one of the most abundant genes in the entire embryo and we use mutants to quantitatively demonstrate how it cooperates with Dorsal to activate transcription and is responsible for some of the rapid changes in transcription observed during early NC14. We also uncovered elements within the gene regulatory network that maintain precise transcript levels for sets of genes that are spatiotemporally cotranscribed within the presumptive mesoderm or dorsal ectoderm. Using these new data, we show that a fine-scale, quantitative analysis of temporal gene expression can provide new insights into developmental biology by uncovering trends in gene networks, including coregulation of target genes and specific temporal input by transcription factors.

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“…In both Drosophila and Tribolium, Toll signalling leads to the formation of a ventral-to-dorsal nuclear gradient of the NF-κB transcription factor Dorsal. The NF-κB/Dorsal gradient is fairly stable in Drosophila and patterns the DV axis by activating or repressing target genes in a concentration-dependent manner (Hong et al, 2008;Ozdemir et al, 2014;Reeves and Stathopoulos, 2009;Reeves et al, 2012;Roth et al, 1989;Rushlow et al, 1989;Steward, 1989). Among the targets of NF-κB/Dorsal are transcription factors directly involved in cell fate specification such as twist (twi), as well as components of other signalling pathways which indirectly specify subregions along the DV axis.…”

Section: Introductionmentioning

confidence: 99%

Genome wide identification ofTriboliumdorsoventral patterning genes

et al. 2016

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The gene regulatory network controlling dorsoventral axis formation in insects has undergone drastic evolutionary changes. In Drosophila, a stable long-range gradient of Toll signalling specifies ventral cell fates and restricts BMP signalling to the dorsal half of the embryo. In Tribolium, however, Toll signalling is transient and only indirectly controls BMP signalling. In order to gain unbiased insights into the Tribolium network, we performed comparative transcriptome analyses of embryos with various dorsoventral pattering defects produced by parental RNAi for Toll and BMP signalling components. We also included embryos lacking the mesoderm ( produced by Tctwist RNAi) and characterized similarities and differences between Drosophila and Tribolium twist loss-of-function phenotypes. Using stringent conditions, we identified over 750 differentially expressed genes and analysed a subset with altered expression in more than one knockdown condition. We found new genes with localized expression and showed that conserved genes frequently possess earlier and stronger phenotypes than their Drosophila orthologues. For example, the leucine-rich repeat (LRR) protein Tartan, which has only a minor influence on nervous system development in Drosophila, is essential for early neurogenesis in Tribolium and the Tc-zinc-finger homeodomain protein 1 (Tc-zfh1), the orthologue of which plays a minor role in Drosophila muscle development, is essential for maintaining early Tc-twist expression, indicating an important function for mesoderm specification.

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Dorsal-Ventral Gene Expression in the Drosophila Embryo Reflects the Dynamics and Precision of the Dorsal Nuclear Gradient

Cited by 113 publications

References 42 publications

Actomyosin-based tissue folding requires a multicellular myosin gradient

Actomyosin-based tissue folding requires a multicellular myosin gradient

Quantitative Single-Embryo Profile ofDrosophilaGenome Activation and the Dorsal–Ventral Patterning Network

Genome wide identification ofTriboliumdorsoventral patterning genes

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