Global analysis of patterns of gene expression during Drosophilaembryogenesis

Tomančák, Pavel; Berman, Benjamin P.; Beaton, Amy; Weiszmann, Richard; Kwan, Elaine; Hartenstein, Volker; Celniker, S; Rubin, Gerald M.

doi:10.1186/gb-2007-8-7-r145

Cited by 557 publications

(724 citation statements)

References 41 publications

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“…1B). There are significant differences in the expression and functions of genes in the active, stalled or no Pol II classes based on in situ expression patterns (ImaGO) 27 and functional annotations (GO)28 (Fig. 4).…”

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confidence: 99%

RNA polymerase stalling at developmental control genes in the Drosophila melanogaster embryo

et al. 2007

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It is widely assumed that the key rate-limiting step in gene activation is the recruitment of RNA polymerase II (Pol II) to the core promoter 2 . Although there are well-documented examples where Pol II is recruited to a gene but stalls3 -14, a general role for Pol II stalling in development has not been established. We have performed comprehensive Pol II ChIP-chip assays in Drosophila embryos and identified three distinct Pol II binding behaviors: active (uniform binding across the entire transcription unit), no binding, and stalled (binding at the transcription start site). The striking feature of the ~10% genes that are stalled is that they are highly enriched for developmental control genes that are repressed at the time of analysis or poised for activation during subsequent stages of development. We propose that Pol II stalling facilitates rapid temporal and spatial changes in gene activity during development.Pol II stalling is probably best studied at heat shock genes in Drosophila, where Pol II engages in transcription but pauses immediately downstream of the transcriptional start site 3,4,22 . Upon activation by heat shock, Pol II is able to rapidly transcribe these genes. Regulation of Pol II activity after recruitment has also been described in bacteria 23 , yeast 13 and mammalian cell lines 3,[6][7][8][9][10][11][12] , and includes instances where Pol II is found in an inactive pre-initiation complex 24,25 . We will collectively refer to inactive Pol II near the transcription start site as stalled Pol II.To determine at which genes Pol II stalling occurs during development, we analyzed global Pol II occupancy in whole Drosophila embryos. While this is one of the few systems where The results show that many genes known to be repressed in Toll 10b embryos display strikingly high levels of Pol II near the transcription start site (Fig.1A-D). In some cases the prominent Pol II peak is tightly restricted to the promoter region (e.g. at the tup gene in Fig. 1A), while at other genes Pol II is also found at low levels throughout the transcription unit (e.g. the sog and brk genes Fig. 1C,D). This is consistent with previous evidence that some genes such as sog are transiently activated but then repressed at later stages 26 , while other genes such as tup are never activated in Toll 10b mutants 19,20 .The Pol II profile of repressed genes is clearly distinct from those of active genes ( Fig. 1E, F). For example, the Hbr gene, which encodes an FGF receptor specifically expressed in mesodermal precursors ( Fig. 1E), and ribosomal genes such as RpL3 (Fig.1F), show uniformly high levels of Pol II throughout the transcription unit. Furthermore, genes that are silent in the early embryo simply lack Pol II binding altogether ( Fig. 1G, H). Thus, there appears to be three distinct classes of genes: those with Pol II distributed throughout the transcription unit, those genes with preferential enrichment of Pol II at the transcription site, and genes that lack Pol II binding altogether.To further characterize t...

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confidence: 99%

RNA polymerase stalling at developmental control genes in the Drosophila melanogaster embryo

et al. 2007

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“…The expression patterns of all four Drosophila RBCC/TRIMs (DPLD, BRAT, MEI-26, and ABBA) have been partially characterized during embryogenesis (Tomancak et al, 2002), and the expression pattern of brat has been extensively documented in developing adult tissues (Arama et al, 2000;Sonoda and Wharton, 2001;Frank et al, 2002). The four RBCC/TRIM paralogs have very different zygotic transcription patterns, the only exception being an overlap between brat and dpld, which are coexpressed in the developing embryonic central nervous system (CNS; Tomancak et al, 2002).…”

Section: Abba and Dpld Are Expressed In Different Tissues During Devementioning

confidence: 99%

“…The four RBCC/TRIM paralogs have very different zygotic transcription patterns, the only exception being an overlap between brat and dpld, which are coexpressed in the developing embryonic central nervous system (CNS; Tomancak et al, 2002). To gain a better understanding of the potential functions of those less-characterized Drosophila family members, abba and dpld, we performed in situ hybridization (ISH) on a variety of tissues at various developmental stages.…”

Section: Abba and Dpld Are Expressed In Different Tissues During Devementioning

confidence: 99%

Regulation of the Drosophila lin‐41 homologue dappled by let‐7 reveals conservation of a regulatory mechanism within the LIN‐41 subclade

O’Farrell

Esfahani

Engström

et al. 2007

Developmental Dynamics

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Drosophila Dappled (DPLD) is a member of the RBCC/TRIM superfamily, a protein family involved in numerous diverse processes such as developmental timing and asymmetric cell divisions. DPLD belongs to the LIN-41 subclade, several members of which are micro RNA (miRNA) regulated. We re-examined the LIN-41 subclade members and their relation to other RBCC/TRIMs and dpld paralogs, and identified a new Drosophila muscle specific RBCC/TRIM: Another B-Box Affiliate, ABBA. In silico predictions of candidate miRNA regulators of dpld identified let-7 as the strongest candidate. Overexpression of dpld led to abnormal eye development, indicating that strict regulation of dpld mRNA levels is crucial for normal eye development. This phenotype was sensitive to let-7 dosage, suggesting let-7 regulation of dpld in the eye disc. A cell-based assay verified let-7 miRNA down-regulation of dpld expression by means of its 3 -untranslated region. Thus, dpld seems also to be miRNA regulated, suggesting that miRNAs represent an ancient mechanism of LIN-41 regulation. Developmental Dynamics 237:196 -208, 2008.

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“…For example, in model organism specific databases ZFin (Sprague et al, 2003), Wormbase (Rogers et al, 2008), MEPD (Henrich et al, 2005), Geisha (Bell et al, 2004;Darnell et al, 2007), GXD (Ringwald et al, 1997;Smith et al, 2007), BDGP (Tomancak et al, 2007), and Xenbase (Bowes et al, 2008), and across multiple species in VisiGene (Kuhn et al, 2007), 4DX-press (Haudry et al, 2008), and quickImage (Gilchrist et al, 2008). The general areas of bioimage informatics and related topics are covered in a recent review (Peng, 2008).…”

Section: Introductionmentioning

confidence: 99%

“…Anatomy-based annotation is exemplified in zebrafish by the heroic efforts of Bernard Thisse and others, visualized through the Zfin database (Sprague et al, 2003), and a similar approach has been used both for mouse brains in the Allen Brain Atlas (Lein et al, 2007) and for fruit fly embryos in the BDGP database (Tomancak et al, 2007). This is essentially a manual annotation process.…”

Section: Introductionmentioning

confidence: 99%

Database of queryable gene expression patterns for Xenopus

Gilchrist

Christensen

Bronchain

et al. 2009

Developmental Dynamics

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The precise localization of gene expression within the developing embryo, and how it changes over time, is one of the most important sources of information for elucidating gene function. As a searchable resource, this information has up until now been largely inaccessible to the Xenopus community. Here, we present a new database of Xenopus gene expression patterns, queryable by specific location or region in the embryo. Pattern matching can be driven either from an existing in situ image, or from a user-defined pattern based on development stage schematic diagrams. The data are derived from the work of a group of 21 Xenopus researchers over a period of 4 days. We used a novel, rapid manual annotation tool, XenMARK, which exploits the ability of the human brain to make the necessary distortions in transferring data from the in situ images to the standard schematic geometry.

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Global analysis of patterns of gene expression during Drosophilaembryogenesis

Cited by 557 publications

References 41 publications

RNA polymerase stalling at developmental control genes in the Drosophila melanogaster embryo

RNA polymerase stalling at developmental control genes in the Drosophila melanogaster embryo

Regulation of the Drosophila lin‐41 homologue dappled by let‐7 reveals conservation of a regulatory mechanism within the LIN‐41 subclade

Database of queryable gene expression patterns for Xenopus

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