Quantitative Single-Embryo Profile of<i>Drosophila</i>Genome Activation and the Dorsal–Ventral Patterning Network

Sandler, Jeremy E.; Stathopoulos, Angelike

doi:10.1534/genetics.116.186783

Cited by 43 publications

(70 citation statements)

References 25 publications

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“…This coordinated increase occurs at the same time for all six mesoderm genes included in the NanoString study ( twi, mes3, sna, hbr, NetA , and htl ), and coincides with the time of high dynamic change between NCs 14A and 14B. In contrast, target genes of Bicoid expressed along the anterior-posterior (AP) axis, such as hb and otd , show no signs of a coordinated increase in expression between NCs 14A and 14B, or any other time point [45]. The AP targets of Bicoid increase gradually during the time course without a rapid change in expression strength.…”

Section: Possible Roles For Step-wise Progression Of Embryonic Gene Ementioning

confidence: 81%

“…gene expression) is assayed with fine temporal resolution. Use of the NanoString technology has supported generation of a time-series from carefully staged, individual Drosophila embryo fixed samples [45]. From these data, dynamic trends within gene regulatory networks can be inferred such as identification of gene expression cohorts and specific, temporal roles for transcription factors [64].…”

Section: Resultsmentioning

confidence: 99%

“…The recent quantitative analysis of gene expression in Drosophila embryos has highlighted activation of genes expressed along the DV axis occurs in a step-wise manner [13, 45]. We contend this step-wise activation program is instrumental for DV patterning and suggest three ideas regarding its roles, below.…”

Section: Possible Roles For Step-wise Progression Of Embryonic Gene Ementioning

confidence: 98%

“…An assay of gene expression dynamics was performed recently using NanoString nCounter technology (Box 2) to measure the levels of expression for ~70 genes in the early Drosophila embryo, focusing on those expressed along the DV axis and providing further insight into the dynamics of genes expressed in the early embryo [45, 46]. Ten time points spanning nuclear cycles (NC) 10 through 14 and also including gastrulation were investigated through assay of gene expression within individual, carefully-staged Drosophila embryos (Figure 1, Key Figure).…”

Section: A Temporally Fine-scale Quantitative Assay Of Gene Expressimentioning

confidence: 99%

“…This bimodal profile may relate to temporal increases in Dorsal levels and/or to the additive effect of a second factor joining a feed forward loop (Figure 2). When twi is mutated so it can no longer bind to DNA and mutant embryos are assayed by NanoString, the rapid increase in transcription usually observed in NC 14 does not occur, and the slower rate of transcription observed in NCs 10–13 is maintained [45]. This difference in transcription rate demonstrates the additive nature of feed forward loops; at NC 14, Dorsal alone is able to activate its targets at a moderate level, but the input of Twist is able to provide an additional boost transcription that is added to the input of Dorsal to support high level expression.…”

Section: A Temporally Fine-scale Quantitative Assay Of Gene Expressimentioning

confidence: 99%

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Stepwise Progression of Embryonic Patterning

Sandler

Stathopoulos

2016

Trends in Genetics

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It is long established that the graded distribution of Dorsal transcription factor influences spatial domains of gene expression along the dorsoventral axis of Drosophila melanogaster embryos.However, the more recent realization that Dorsal levels also change in time raises the question of whether these dynamics are instructive. Here, an overview of dorsoventral axis patterning is provided focusing on new insights identified through quantitative analysis of temporal changes in Dorsal target gene expression from one nuclear cycle to the next ('steps'). Possible roles for the step-wise progression of this patterning program are discussed including (i) tight, temporal regulation of signaling pathway activation, (ii) control of gene expression cohorts, and (iii) to ensure irreversibility of the patterning and cell fate specification process. KeywordsDorsal transcription factor; Drosophila embryo; dorsal-ventral patterning; dynamics; morphogen gradients; spatiotemporal gene expression Transcription factor dynamics regulate target gene expressionSubdividing the embryo into distinct domains of gene expression by combinatorial control of transcription factors is an important function of regulatory networks acting in early embryos including those of Drosophila [1][2][3][4][5]. These early patterning events influence the activation of signaling pathways to support tissue differentiation and also control cell movements required for the generation of a multilayered embryo; the developmental actions that encompass gastrulation [6,7]. To study these events at the transcriptional level in Drosophila embryos, previous studies of early zygotic gene expression have considered one or two time-points spanning the first four hours of early embryo development [8][9][10][11], and yet recent studies suggest gene expression patterns change on the order of minutes rather than hours [e.g. 12, 13, 14]. Furthermore, only recently has it come to light that transcription factors in the early embryo exhibit changes in levels over time [15][16][17][18]. At least in part these dynamics relate to the fast nuclear divisions that encompass Drosophila early embryonic * Correspondence: angelike@caltech.edu (A. Stathopoulos). Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. HHS Public Access Author ManuscriptAuthor Manuscript Author ManuscriptAuthor Manuscript development and result in oscillatory inputs to target genes. Transcription factor dynamics appear to be a general mechanism of regulating gene expression [19,20] and highlight the need to study temporal regulation of developmental gene expression...

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Section: Possible Roles For Step-wise Progression Of Embryonic Gene Ementioning

confidence: 81%

Section: Resultsmentioning

confidence: 99%

Section: Possible Roles For Step-wise Progression Of Embryonic Gene Ementioning

confidence: 98%

Section: A Temporally Fine-scale Quantitative Assay Of Gene Expressimentioning

confidence: 99%

Section: A Temporally Fine-scale Quantitative Assay Of Gene Expressimentioning

confidence: 99%

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Stepwise Progression of Embryonic Patterning

Sandler

Stathopoulos

2016

Trends in Genetics

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Spatiotemporal control of gene expression boundaries using a feedforward loop

Bandodkar

Asafen

Reeves

2020

Developmental Dynamics

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Background A feedforward loop (FFL) is commonly observed in several biological networks. The FFL network motif has been mostly studied with respect to variation of the input signal in time, with only a few studies of FFL activity in a spatially distributed system such as morphogen‐mediated tissue patterning. However, most morphogen gradients also evolve in time. Results We studied the spatiotemporal behavior of a coherent FFL in two contexts: (a) a generic, oscillating morphogen gradient and (b) the dorsal‐ventral patterning of the early Drosophila embryo by a gradient of the NF‐κB homolog dorsal with its early target Twist. In both models, we found features in the dynamics of the intermediate node—phase difference and noise filtering—that were largely independent of the parameterization of the models, and thus were functions of the structure of the FFL itself. In the dorsal gradient model, we also found that proper target gene expression was not possible without including the effect of maternal pioneer factor Zelda. Conclusions An FFL buffers fluctuation to changes in the morphogen signal ensuring stable gene expression boundaries.

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Link of Zygotic Genome Activation and Cell Cycle Control

Liu

Großhans

2017

Methods in Molecular Biology

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The activation of the zygotic genome and onset of transcription in blastula embryos is linked to changes in cell behavior and remodeling of the cell cycle and constitutes a transition from exclusive maternal to zygotic control of development. This step in development is referred to as mid-blastula transition and has served as a paradigm for the link between developmental program and cell behavior and morphology. Here, we discuss the mechanism and functional relationships between the zygotic genome activation and cell cycle control during mid-blastula transition with a focus on Drosophila embryos.

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

Cited by 43 publications

References 25 publications

Stepwise Progression of Embryonic Patterning

Stepwise Progression of Embryonic Patterning

Spatiotemporal control of gene expression boundaries using a feedforward loop

Link of Zygotic Genome Activation and Cell Cycle Control

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