Early Eye Development: Specification and Determination

Mishra, Abhishek Kumar; Sprecher, Simon G.

doi:10.1007/978-3-030-42246-2_1

Cited by 5 publications

(9 citation statements)

References 261 publications

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“…At the genetic level, the very early stages of eye specification involve a deeply conserved transcriptional network (Gehring, 2001;Kumar, 2001;Hsiung and Moses, 2002;Mishra and Sprecher, 2020) comprising the Pax6 "master regulator of eye development" and its downstream retinal determination gene network (RDGN). The latter is contributed to by sine oculis (so), eyes absent (eya), and dachshund (dac), which were originally identified during D. melanogaster eye mutant screening (Bonini et al, 1993;Cheyette et al, 1994;Serikaku and O'Tousa, 1994).…”

Section: Introductionmentioning

confidence: 99%

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: Introductionmentioning

confidence: 99%

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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“…Drosophila eye begins from approximately 20 eye‐antennal primordial cells that are set aside during embryogenesis (Garcia‐Bellido & Merriam, 1969; Held, 2002; Poulson, 1950). These eye‐antennal primordial cells undergo proliferation during first‐ and second‐ instar stages of larval development, followed by differentiation during late second or early third instar of larval development, which give rise to the adult compound eye, antenna and head cuticle (Atkins & Mardon, 2009; Gogia, Puli, et al, 2020; Kumar, 2011, 2020b; Mishra & Sprecher, 2020; Ready, Hanson, & Benzer, 1976; Tare, Puli Roy, & Singh, 2013).…”

Section: Introductionmentioning

confidence: 99%

“…During Drosophila eye development, a core cascade of genes, referred to as the retinal determination (RD) gene network, which comprises of PAX‐6 homolog eyeless (ey) , twin of eyeless (toy) , eye gone (eyg) , twin of eyegone (toe) , eyes absent (eya) , sine oculis (so) , and dachshund (dac) are required to form an adult eye (Gogia, Puli, et al, 2020; Jang et al, 2003; Kango‐Singh, Singh, & Sun, 2003; Mishra & Sprecher, 2020; Singh, Lim, & Choi, 2005; Tare, Puli Roy, & Singh, 2013). Most of the core members of RD gene network except Eya, a tyrosine phosphatase, are transcription factors.…”

Section: Introductionmentioning

confidence: 99%

“…Most of the core members of RD gene network except Eya, a tyrosine phosphatase, are transcription factors. These RD genes are necessary and sufficient for the normal development of the eye, and have capability to induce ectopic eyes in other imaginal discs like wing and leg imaginal discs (Halder et al, 1998; Kango‐Singh et al, 2003; Kumar, 2011; Mishra & Sprecher, 2020). In first instar eye primordial cells, ey is expressed in the entire eye disc and its expression is activated by Toy (Czerny et al, 1999).…”

Section: Introductionmentioning

confidence: 99%

“…In first instar eye primordial cells, ey is expressed in the entire eye disc and its expression is activated by Toy (Czerny et al, 1999). Ey expression is downregulated at the MF as well as in the cells posterior to the MF (Czerny et al, 1999), which in turn activates the expression of downstream genes eya , so , and dac to promote retinal differentiation (Bui, Zimmerman, Liu, & Bonini, 2000; Halder et al, 1998; Kango‐Singh et al, 2003; Mishra & Sprecher, 2020; Niimi, Seimiya, Kloter, Flister, & Gehring, 1999; Serikaku & O'Tousa, 1994).…”

Section: Introductionmentioning

confidence: 99%

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An E3 ubiquitin ligase, cullin‐4 regulates retinal differentiation in Drosophila eye

Tare

Chimata

Gogia

et al. 2020

Genesis

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During organogenesis, cell proliferation is followed by the differentiation of specific cell types to form an organ. Any aberration in differentiation can result in developmental defects, which can result in a partial to a near-complete loss of an organ. We employ the Drosophila eye model to understand the genetic and molecular mechanisms involved in the process of differentiation. In a forward genetic screen, we identified, cullin-4 (cul-4), which encodes an E3 ubiquitin ligase, to play an important role in retinal differentiation. During development, cul-4 is known to be involved in protein degradation, regulation of genomic stability, and regulation of cell cycle. Previously, we have reported that cul-4 regulates cell death during eye development by downregulating Wingless (Wg)/Wnt signaling pathway. We found that loss-offunction of cul-4 results in a reduced eye phenotype, which can be due to onset of cell death. However, we found that loss-of-function of cul-4 also affects retinal development by downregulating retinal determination (RD) gene expression. Early markers of retinal differentiation are dysregulated in cul-4 loss of function conditions, indicating that cul-4 is necessary for differentiation. Furthermore, loss-of-function of cul-4 ectopically induces expression of negative regulators of eye development like Wg and Homothorax (Hth). During eye development, Wg is known to block the progression of a synchronous wave of differentiation referred to as Morphogenetic furrow (MF). In cul-4 loss-of-function background, expression of dpp-lacZ, a MF marker, is significantly downregulated. Our data suggest a new role of cul-4 in retinal differentiation. These studies may have significant bearings on our understanding of early eye development.

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Motif 1 Binding Protein suppresses wingless to promote eye fate in Drosophila

Raj

Chimata

Singh

2020

Sci Rep

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The phenomenon of RNA polymerase II (Pol II) pausing at transcription start site (TSS) is one of the key rate-limiting steps in regulating genome-wide gene expression. In Drosophila embryo, Pol II pausing is known to regulate the developmental control genes expression, however, the functional implication of Pol II pausing during later developmental time windows remains largely unknown. A highly conserved zinc finger transcription factor, Motif 1 Binding Protein (M1BP), is known to orchestrate promoter-proximal pausing. We found a new role of M1BP in regulating Drosophila eye development. Downregulation of M1BP function suppresses eye fate resulting in a reduced eye or a “no-eye” phenotype. The eye suppression function of M1BP has no domain constraint in the developing eye. Downregulation of M1BP results in more than two-fold induction of wingless (wg) gene expression along with robust induction of Homothorax (Hth), a negative regulator of eye fate. The loss-of-eye phenotype of M1BP downregulation is dependent on Wg upregulation as downregulation of both M1BP and wg, by using wgRNAi, shows a significant rescue of a reduced eye or a “no-eye” phenotype, which is accompanied by normalizing of wg and hth expression levels in the eye imaginal disc. Ectopic induction of Wg is known to trigger developmental cell death. We found that upregulation of wg as a result of downregulation of M1BP also induces apoptotic cell death, which can be significantly restored by blocking caspase-mediated cell death. Our data strongly imply that transcriptional regulation of wg by Pol II pausing factor M1BP may be one of the important regulatory mechanism(s) during Drosophila eye development.

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Early Eye Development: Specification and Determination

Cited by 5 publications

References 261 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

An E3 ubiquitin ligase, cullin‐4 regulates retinal differentiation in Drosophila eye

Motif 1 Binding Protein suppresses wingless to promote eye fate in Drosophila

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