Retinal determination genes function along with cell‐cell signals to regulate <i>Drosophila</i> eye development

Baker, Nicholas E.; Firth, Lucy C.

doi:10.1002/bies.201000131

Cited by 19 publications

(16 citation statements)

References 62 publications

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“…For example, enhancer E controls early eya expression while enhancer 1 is responsible for the bulk of late eya transcription (Fig 3). Having separate cis-regulatory elements control eya expression at different times during development is consistent with the idea that RD genes are dynamically regulated temporally and spatially to insure distinct expression patterns necessary for the differentiation of specific retinal cell types over the course of eye development [40]. …”

Section: Discussionsupporting

confidence: 68%

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Retinal Expression of the Drosophila eyes absent Gene Is Controlled by Several Cooperatively Acting Cis-regulatory Elements

Weasner

Neuman

et al. 2016

PLoS Genet

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The eyes absent (eya) gene of the fruit fly, Drosophila melanogaster, is a member of an evolutionarily conserved gene regulatory network that controls eye formation in all seeing animals. The loss of eya leads to the complete elimination of the compound eye while forced expression of eya in non-retinal tissues is sufficient to induce ectopic eye formation. Within the developing retina eya is expressed in a dynamic pattern and is involved in tissue specification/determination, cell proliferation, apoptosis, and cell fate choice. In this report we explore the mechanisms by which eya expression is spatially and temporally governed in the developing eye. We demonstrate that multiple cis-regulatory elements function cooperatively to control eya transcription and that spacing between a pair of enhancer elements is important for maintaining correct gene expression. Lastly, we show that the loss of eya expression in sine oculis (so) mutants is the result of massive cell death and a progressive homeotic transformation of retinal progenitor cells into head epidermis.

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Section: Discussionsupporting

confidence: 68%

“…As such their regulation and gene expression is often highly temporally and spatially dynamic allowing for the proper differentiation of the multiple cell types necessary for the proper function of the compound eye [40]. eyes absent is a core member of this network and provides a key example of this type of complex gene expression.…”

Section: Discussionmentioning

confidence: 99%

Retinal Expression of the Drosophila eyes absent Gene Is Controlled by Several Cooperatively Acting Cis-regulatory Elements

Weasner

Neuman

et al. 2016

PLoS Genet

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“…It has been shown that signaling pathways activated in the morphogenetic furrow increase levels of Eya, So and Dac; furthermore, it is proposed that this upregulation alters their targets, creating an embedded loop within the circuitry governing retinal development and allowing signaling events to indirectly regulate targets through the RD network [26], [28], [61]. The identification of ey regulation by So posterior to the morphogenetic furrow represents a direct target consistent with this model.…”

Section: Discussionmentioning

confidence: 61%

Dynamic Rewiring of the Drosophila Retinal Determination Network Switches Its Function from Selector to Differentiation

Atkins¹,

Jiang²,

Sansores-García³

et al. 2013

PLoS Genet

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Organ development is directed by selector gene networks. Eye development in the fruit fly Drosophila melanogaster is driven by the highly conserved selector gene network referred to as the “retinal determination gene network,” composed of approximately 20 factors, whose core comprises twin of eyeless (toy), eyeless (ey), sine oculis (so), dachshund (dac), and eyes absent (eya). These genes encode transcriptional regulators that are each necessary for normal eye development, and sufficient to direct ectopic eye development when misexpressed. While it is well documented that the downstream genes so, eya, and dac are necessary not only during early growth and determination stages but also during the differentiation phase of retinal development, it remains unknown how the retinal determination gene network terminates its functions in determination and begins to promote differentiation. Here, we identify a switch in the regulation of ey by the downstream retinal determination genes, which is essential for the transition from determination to differentiation. We found that central to the transition is a switch from positive regulation of ey transcription to negative regulation and that both types of regulation require so. Our results suggest a model in which the retinal determination gene network is rewired to end the growth and determination stage of eye development and trigger terminal differentiation. We conclude that changes in the regulatory relationships among members of the retinal determination gene network are a driving force for key transitions in retinal development.

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“…ato is first expressed in all cells in a stripe just anterior to the morphogenetic furrow, but it rapidly resolves more posteriorly into regularly spaced groups of cells and then into single cells, the future R8 photoreceptors (Figure (b)). Its initial expression is driven by a 3′ enhancer region that contains essential binding sites for Ey and So, suggesting that the input from Hh and Dpp signaling may be mediated by these eye determination factors . A 5′ enhancer that responds to Ato autoregulation and to the zinc finger transcription factor Roughened eye mediates its later expression .…”

Section: Progressive Photoreceptor Differentiation Is Driven By Autormentioning

confidence: 99%

Retinal differentiation in Drosophila

Treisman

2012

WIREs Developmental Biology

119

113

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Drosophila eye development has been extensively studied, due to the ease of genetic screens for mutations disrupting this process. The eye imaginal disc is specified during embryonic and larval development by the Pax6 homolog Eyeless and a network of downstream transcription factors. Expression of these factors is regulated by signaling molecules and also indirectly by growth of the eye disc. Differentiation of photoreceptor clusters initiates in the third larval instar at the posterior of the eye disc and progresses anteriorly, driven by the secreted protein Hedgehog. Within each cluster, the combined activities of Hedgehog signaling and Notch-mediated lateral inhibition induce and refine the expression of the transcription factor Atonal, which specifies the founding R8 photoreceptor of each ommatidium. Seven additional photoreceptors, followed by cone and pigment cells, are successively recruited by the signaling molecules Spitz, Delta, and Bride of sevenless. Combinations of these signals and of intrinsic transcription factors give each ommatidial cell its specific identity. During the pupal stages, Rhodopsins are expressed, and the photoreceptors and accessory cells take on their final positions and morphologies to form the adult retina. Over the past few decades, the genetic analysis of this small number of cell types arranged in a repetitive structure has allowed a remarkably detailed understanding of the basic mechanisms controlling cell differentiation and morphological rearrangement.

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Retinal determination genes function along with cell‐cell signals to regulate Drosophila eye development

Cited by 19 publications

References 62 publications

Retinal Expression of the Drosophila eyes absent Gene Is Controlled by Several Cooperatively Acting Cis-regulatory Elements

Retinal Expression of the Drosophila eyes absent Gene Is Controlled by Several Cooperatively Acting Cis-regulatory Elements

Dynamic Rewiring of the Drosophila Retinal Determination Network Switches Its Function from Selector to Differentiation

Retinal differentiation in Drosophila

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