ZLocal induction of patterning and programmed cell death in the developing <i>Drosophila</i> retina

Miller, David T.; Cagan, Ross L.

doi:10.1242/dev.125.12.2327

Cited by 159 publications

(8 citation statements)

References 46 publications

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“…Although the output of our model does not achieve the same level of precision in regard to the regularity of the ommatidial units, it does achieve a good approximation of the typical hexagonal arrangement (Johnson, 2021). Additional factors (that are not currently implemented in the program) are known to play important roles in achieving the level of precision manifested in D. melanogaster, including proper adhesion between cells (Bao et al, 2010), precise levels of cell size (Kim et al, 2016), and appropriate elimination of excess cells (Wolff and Ready, 1991a;Miller and Cagan, 1998;Rusconi et al, 2000;Monserrate and Brachmann, 2007). However, less-regular compound eyes have been observed for other insects, such as in the Madagascar hissing cockroach (Gromphadorhina portentosa) (Mishra and Meyer-Rochow, 2008) or in the ventral portion of certain male butterflies (Uchiyama et al, 2013), suggesting that imperfect organization from the default parameters may be relevant to some (including more ancestral) compound eyes.…”

Section: Recreating the Eye Layout Of D Melanogastermentioning

confidence: 90%

“…In D. melanogaster, eye unit borders are refined by eliminating any remaining unspecified cells through programmed cell death (apoptosis) (Wolff and Ready, 1991a;Miller and Cagan, 1998;Rusconi et al, 2000;Monserrate and Brachmann, 2007). In EyeVolve, the timing and speed of cell death are set using the input parameters "distance from furrow" and "death chance", which is the probability that each cell will die.…”

Section: Cell Deathmentioning

confidence: 99%

“…In the D. melanogaster compound eye, once all necessary cells have differentiated, apoptosis of the remaining cells fine tunes the final ommatidial layout. This process is regulated by a precise interplay between Notch (promoting apoptosis (Cagan and Ready, 1989a;Parks et al, 1995)) and Ras (impeding apoptosis (Miller and Cagan, 1998)) pathways. These phenotypes suggest that the rate of apoptosis is another important parameter that could mediate evolutionary differences in eye unit organization.…”

Section: The Apoptosis Rate Of Remaining Cells Molds the Final Eye La...mentioning

confidence: 99%

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EyeVolve, a modular PYTHON based model for simulating developmental eye type diversification

Lavin

Rathore

Bauer

et al. 2022

Front. Cell Dev. Biol.

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Vision is among the oldest and arguably most important sensory modalities for animals to interact with their external environment. Although many different eye types exist within the animal kingdom, mounting evidence indicates that the genetic networks required for visual system formation and function are relatively well conserved between species. This raises the question as to how common developmental programs are modified in functionally different eye types. Here, we approached this issue through EyeVolve, an open-source PYTHON-based model that recapitulates eye development based on developmental principles originally identified in Drosophila melanogaster. Proof-of-principle experiments showed that this program’s animated timeline successfully simulates early eye tissue expansion, neurogenesis, and pigment cell formation, sequentially transitioning from a disorganized pool of progenitor cells to a highly organized lattice of photoreceptor clusters wrapped with support cells. Further, tweaking just five parameters (precursor pool size, founder cell distance and placement from edge, photoreceptor subtype number, and cell death decisions) predicted a multitude of visual system layouts, reminiscent of the varied eye types found in larval and adult arthropods. This suggests that there are universal underlying mechanisms that can explain much of the existing arthropod eye diversity. Thus, EyeVolve sheds light on common principles of eye development and provides a new computational system for generating specific testable predictions about how development gives rise to diverse visual systems from a commonly specified neuroepithelial ground plan.

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Section: Recreating the Eye Layout Of D Melanogastermentioning

confidence: 90%

Section: Cell Deathmentioning

confidence: 99%

Section: The Apoptosis Rate Of Remaining Cells Molds the Final Eye La...mentioning

confidence: 99%

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EyeVolve, a modular PYTHON based model for simulating developmental eye type diversification

Lavin

Rathore

Bauer

et al. 2022

Front. Cell Dev. Biol.

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“…Our results imply that this latency is a consequence of protection conferred by EGFR signalling. The EGFR has multiple functions in the developing eye, including a protective effect against cell death in normal development (Domínguez et al ., 1998; Miller and Cagan, 1998). Furthermore, a strong genetic interaction has been observed between the cell death‐inducing factor Hid and Ras1 signalling in the eye, and the latter apparently promotes cell survival by downregulating Hid directly at the transcriptional and post‐transcriptional level (Bergmann et al ., 1998; Kurada and White, 1998).…”

Section: Discussionmentioning

confidence: 99%

EGF receptor/Rolled MAP kinase signalling protects cells against activated Armadillo in the Drosophila eye

Freeman

Bienz

2001

EMBO Reports

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β-catenin/Armadillo are transcriptional co-activators that mediate Wnt signalling in normal development. Activated forms of β-catenin are oncogenic. We have constructed mutant forms of Drosophila Armadillo which correspond to common human oncogenic mutations, and find them to activate Armadillo constitutively. When expressed in the Drosophila eye, these eventually induce apoptosis in all cell types. Intriguingly, cells in the eye are resistant to the effects of activated Armadillo for a long period prior to the onset of cell death at the mid-pupal stage. This latency is conferred by EGF receptor (EGFR)/MAP kinase signalling, which prevents activated Armadillo from inducing apoptosis; when EGFR signalling naturally ceases, the cells rapidly die. Nemo, the Drosophila homologue of NLK in mice and LIT-1 in Caenorhabditis elegans, does not antagonize activated Armadillo, suggesting that the Nemo-like MAP kinases may not generally interact with Armadillo/β-catenin. Thus, our results show that activated Armadillo is subject to a specific negative control by EGFR/Rolled MAP kinase signalling.

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“…Yet posterior progenitor cells do not carry on with further fate transitions until the anterior ommatidia complete the initial induction of R cells and cone cells (Cagan and Ready, 1989). It is only then, that progenitor cells resume undergoing RTK-induced fate transitions – forming the pigment cells (Freeman, 1996; Miller and Cagan, 1998). We suggest that Yan and Pnt are shut off after the R-cell specification phase in order to create a multi-hour gap in progenitor competence that separates the two phases of fate specification.…”

Section: Discussionmentioning

confidence: 99%

Ratiometric sensing of Pnt and Yan transcription factor levels confers ultrasensitivity to photoreceptor fate transitions in Drosophila

Sm¹,

Peláez

et al. 2018

Preprint

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Cells must reliably respond to changes in transcription factor levels in order to execute cell state transitions in the correct time and place. These transitions are typically thought to be triggered by changes in the absolute nuclear concentrations of relevant transcription factors. We have identified a developmental context in which cell fate transitions depend on changes in the relative concentrations of two transcription factors. Here, we quantify the in vivo expression dynamics of Yan and Pointed, two essential E-twenty-six (ETS) proteins that regulate transcription during eye development in Drosophila. These two factors exert opposing influences; one impedes transcription of gene targets required for differentiation while the other promotes it. We show that both proteins are transiently co-expressed in eye progenitor cells and also during photoreceptor specification. To decide whether to undergo state transitions, cells respond to the ratio of the two protein concentrations rather than changes in the absolute abundance of either transcription factor. We show that a simple model based on the statistical physics of protein-DNA binding illustrates how this ratiometric sensing of transcription factor concentrations could occur. Gene dosage experiments reveal that progenitor cells stabilize the ratio against fluctuations in the absolute concentration of either protein. We further show that signaling inputs via the Notch and Receptor Tyrosine Kinase (RTK) pathways set the ratio in progenitor cells, priming them for either transit to differentiation or for continued multipotency. A sustained change in the ratio accompanies the transit to differentiation This novel mechanism allows for distributed control of developmental transitions by multiple transcription factors, making the system robust to fluctuating genetic or environmental conditions.

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ZLocal induction of patterning and programmed cell death in the developing Drosophila retina

Cited by 159 publications

References 46 publications

EyeVolve, a modular PYTHON based model for simulating developmental eye type diversification

EyeVolve, a modular PYTHON based model for simulating developmental eye type diversification

EGF receptor/Rolled MAP kinase signalling protects cells against activated Armadillo in the Drosophila eye

Ratiometric sensing of Pnt and Yan transcription factor levels confers ultrasensitivity to photoreceptor fate transitions in Drosophila

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