Decapentaplegic head capsule mutations disrupt novel peripodial expression controlling the morphogenesis of the Drosophila ventral head

Stultz, Brian G.; Lee, Heuijung; Ramon, Karolyn; Hursh, Deborah A.

doi:10.1016/j.ydbio.2006.05.034

Cited by 24 publications

(50 citation statements)

References 51 publications

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“…The ventral margin of the eye-antennal disc may be particularly susceptible to ectopic photoreceptor differentiation because of the high level of Dpp signaling there. A 5Ј enhancer element has been shown to direct dpp expression specifically in the ventral marginal peripodial epithelium of the eye-antennal disc (Stultz et al, 2006). The ability of Dpp and Ey to synergize to drive retinal differentiation (Chen et al, 1999) therefore makes it critical to repress Ey in this region, which is fated to form head capsule.…”

Section: Distinct Mechanisms Control Dorsal and Ventral Head Differenmentioning

confidence: 99%

The transcriptional co-factor Chip acts with LIM-homeodomain proteins to set the boundary of the eye field in Drosophila

et al. 2010

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SUMMARYDevelopment involves the establishment of boundaries between fields specified to differentiate into distinct tissues. The Drosophila larval eye-antennal imaginal disc must be subdivided into regions that differentiate into the adult eye, antenna and head cuticle. We have found that the transcriptional co-factor Chip is required for cells at the ventral eye-antennal disc border to take on a head cuticle fate; clones of Chip mutant cells in this region instead form outgrowths that differentiate into ectopic eye tissue. Chip acts independently of the transcription factor Homothorax, which was previously shown to promote head cuticle development in the same region. Chip and its vertebrate CLIM homologues have been shown to form complexes with LIM-homeodomain transcription factors, and the domain of Chip that mediates these interactions is required for its ability to suppress the eye fate. We show that two LIM-homeodomain proteins, Arrowhead and Lim1, are expressed in the region of the eye-antennal disc affected in Chip mutants, and that both require Chip for their ability to suppress photoreceptor differentiation when misexpressed in the eye field. Loss-of-function studies support the model that Arrowhead and Lim1 act redundantly, using Chip as a co-factor, to prevent retinal differentiation in regions of the eye disc destined to become ventral head tissue.

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Section: Distinct Mechanisms Control Dorsal and Ventral Head Differenmentioning

confidence: 99%

The transcriptional co-factor Chip acts with LIM-homeodomain proteins to set the boundary of the eye field in Drosophila

et al. 2010

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“…It most accurately reflects the dpp expression in the lateral peripodial epithelium of the eye/antennal disc ( Fig. 4A) that is responsible for the role of dpp in ventral head formation (Stultz et al, 2006). In genotypes in which opa was removed postembryonically, using opa ts125 at non-permissive temperature, we observe a reduction in reporter expression, indicating that opa is a positive regulator of dpp expression in this location (Fig.…”

Section: Research Articlementioning

confidence: 78%

“…Scanning electron microscopy was carried out using standard method as described (Stultz et al, 2006).…”

Section: Scanning Electron Microscopymentioning

confidence: 99%

“…dpp expression responsible for the formation of the ventral head capsule is limited to the lateral peripodial epithelium of the eye/antennal disc (Stultz et al, 2006) (Fig. 4A; Fig.…”

Section: Research Articlementioning

confidence: 99%

“…dpp is the Drosophila homolog of Bone morphogenetic proteins (BMPs) 2 and 4, and the major TGF␤-like protein in the fruitfly. The enhancer elements disrupted in these mutations direct expression of Dpp in the lateral peripodial epithelium of eye/antennal discs, and loss of this expression in third instar eye/antennal discs results in defects in the ventral head capsule (Stultz et al, 2006). We carried out an extensive genetic screen to recover genes that interact with dpp to form the ventral adult head (D.A.H., unpublished).…”

Section: Introductionmentioning

confidence: 99%

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The Zic family member,odd-paired, regulates theDrosophilaBMP,decapentaplegic, during adult head development

2007

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The eye/antennal discs of Drosophila form most of the adult head capsule. We are analyzing the role of the BMP family member decapentaplegic (dpp) in the process of head formation, as we have identified a class of cis-regulatory dpp mutations (dpp s-hc ) that specifically disrupts expression in the lateral peripodial epithelium of eye/antennal discs and is required for ventral head formation. Here we describe the recovery of mutations in odd-paired (opa), a zinc finger transcription factor related to the vertebrate Zic family, as dominant enhancers of this dpp head mutation. A single loss-of-function opa allele in combination with a single copy of a dpp s-hc produces defects in the ventral adult head. Furthermore, postembryonic loss of opa expression alone causes head defects identical to loss of dpp, and dpp hc /+;opa/+ mutant combinations. opa is required for dpp expression in the lateral peripodial epithelium, but not other areas of the eye/antennal disc. Thus a pathway that includes opa and dpp expression in the peripodial epithelium is crucial to the formation of the ventral adult head. Zic proteins and members of the BMP pathway are crucial for vertebrate head development, as mutations in them are associated with midline defects of the head. The interaction of these genes in the morphogenesis of the fruitfly head suggests that the regulation of head formation may be conserved across metazoans.

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Signaling in the third dimension: The peripodial epithelium in eye disc development

Atkins¹,

Mardon²

2009

Developmental Dynamics

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The eye-antennal imaginal disc of Drosophila melanogaster has often been described as an epithelial monolayer with complex signaling events playing out in two dimensions. However, the imaginal disc actually comprises two opposing epithelia (the peripodial epithelium, or PE, and the disc proper, or DP) separated by a lumen to form a sac-like structure. Recent studies expose complex molecular interactions between the PE and the DP, and reveal dynamic communication between the two tissues. Further findings suggest the PE makes important contributions to DP development by acting as a source of signaling molecules as well as cells. Here we summarize those findings and highlight implications for further research.

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Decapentaplegic head capsule mutations disrupt novel peripodial expression controlling the morphogenesis of the Drosophila ventral head

Cited by 24 publications

References 51 publications

The transcriptional co-factor Chip acts with LIM-homeodomain proteins to set the boundary of the eye field in Drosophila

The transcriptional co-factor Chip acts with LIM-homeodomain proteins to set the boundary of the eye field in Drosophila

The Zic family member,odd-paired, regulates theDrosophilaBMP,decapentaplegic, during adult head development

Signaling in the third dimension: The peripodial epithelium in eye disc development

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