Planar cell polarity and tissue design: Shaping the Drosophila wing membrane

Valentine, Meagan E.; Collier, Simon

doi:10.4161/fly.5.4.15836

Cited by 8 publications

(10 citation statements)

References 26 publications

(38 reference statements)

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“…Collier and colleagues discovered that the fly wing has parallel cuticular ridges that and that their orientation is under the control of the fz/stan and ds/ft pathways (Fig 5EFG) (Valentine and Collier, 2011). Interestingly, the ridges are oriented differently in the anterior and posterior parts of the wing and this appears to be related to differences between two phases of fz signaling that utilize different pk isoforms (Doyle et al, 2008; Hogan et al, 2011; Valentine and Collier, 2011). Their data also argues that the early phase is dependent on ds/ft while the latter is not.…”

Section: The Cellular Basis For Pcpmentioning

confidence: 99%

The frizzled/stan Pathway and Planar Cell Polarity in the Drosophila Wing

Adler

2012

Current Topics in Developmental Biology

127

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Drosophila has been the key model system for studies on Planar Cell Polarity (PCP). The rich morphology of the insect exoskeleton contains many structures that display PCP. Among these are the trichomes (cuticular hairs) that cover much of the exoskeleton, sensory bristles and ommatidia. Many genes have been identified that must function for the development of normal PCP. Among these are the genes that comprise the frizzled/starry night (fz/stan) and dachsous/fat pathways. The mechanisms that underlie the function of the fz/stan pathway are best understood. All of the protein products of these genes accumulate asymmetrically in wing cells and there is good evidence that this involves local intercellular signaling between protein complexes on the distal edge of one cell and the juxtaposed proximal edge of its neighbor. It is thought that a feedback system, directed transport and stabilizing protein-protein interactions mediate the formation of distal and proximal protein complexes. These complexes appear to recruit downstream proteins that function to spatially restrict the activation of the cytoskeleton in wing cells. This leads to the formation of the array of distally pointing hairs found on wings.

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Section: The Cellular Basis For Pcpmentioning

confidence: 99%

The frizzled/stan Pathway and Planar Cell Polarity in the Drosophila Wing

Adler

2012

Current Topics in Developmental Biology

127

180

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“…It has been suggested that the pk pk and pk sple mutant phenotypes are due to specific roles for the two isoforms in interpreting global cues in different tissues [17], [18]. In particular, gradients of Ft/Ds activity have been proposed to orient core protein complexes containing Sple, but to have little influence on Pk-containing complexes [19].…”

Section: Introductionmentioning

confidence: 99%

Strabismus Promotes Recruitment and Degradation of Farnesylated Prickle in Drosophila melanogaster Planar Polarity Specification

2013

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The core planar polarity proteins are required to specify the orientation of structures that are polarised in the plane of the epithelium. In the Drosophila melanogaster wing, the core proteins localise asymmetrically at either proximal or distal cell edges. Asymmetric localisation is thought to be biased by long-range cues, causing asymmetric complexes to become aligned with the tissue axes. Core proteins are then thought to participate in feedback interactions that are necessary to amplify asymmetry, and in order for such feedback interactions to operate correctly, the levels of the core proteins at junctions must be tightly regulated. We have investigated regulation of the core protein Prickle (Pk) in the pupal wing. The core protein Strabismus (Stbm) is required to recruit Pk into asymmetric complexes at proximal cell ends, and we report here that it also promotes proteasomal degradation of excess Pk, probably via a Cullin-1 dependent process. We also show for the first time that Pk is farnesylated in vivo, and this is essential for Pk function in the wing. Notably, farnesylation of Pk is necessary for it to be recruited into asymmetric complexes and function in feedback amplification, probably by reinforcing weak direct interactions between Stbm and Pk. Furthermore, farnesylation is also required for Stbm to promote proteasomal degradation of Pk. We propose that Stbm recruits farnesylated Pk into asymmetric complexes, but also promotes degradation of excess Pk that would otherwise perturb feedback amplification.

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“…Our observations in Dipterans and Hymenopterans have led us to propose a Master-Slave model for insect wing membrane development [Figure 4 and see (Valentine and Collier 2011)]. In the model, rigid cuticle, secreted by the dorsal wing epithelium, acts a mold to shape more flexible cuticle secreted by the ventral wing epithelium.…”

Section: Resultsmentioning

confidence: 99%

“…A Master-Slave model for insect membrane development adapted from Valentine and Collier (2011). (A) Dorsal and ventral pupal wing epithelia are attached at their basal surfaces.…”

Section: Resultsmentioning

confidence: 99%

“…In addition, the membrane itself can have a characteristic topography that also may contribute to wing flexibility. For example, we have previously shown that the Drosophila wing membrane is characterized by parallel ridges that are the equivalent of one epithelial cell in width (approximately 10 μm), and multiple cells in length wing [see Figure 1, B−D (Doyle et al 2008; Valentine and Collier 2011)]. These ridges have an anteroposterior orientation in the anterior wing and a proximodistal orientation in the posterior wing.…”

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confidence: 98%

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Insect Wing Membrane Topography Is Determined by the Dorsal Wing Epithelium

Belalcazar

Doyle

Hogan

et al. 2013

G3 Genes|Genomes|Genetics

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The Drosophila wing consists of a transparent wing membrane supported by a network of wing veins. Previously, we have shown that the wing membrane cuticle is not flat but is organized into ridges that are the equivalent of one wing epithelial cell in width and multiple cells in length. These cuticle ridges have an anteroposterior orientation in the anterior wing and a proximodistal orientation in the posterior wing. The precise topography of the wing membrane is remarkable because it is a fusion of two independent cuticle contributions from the dorsal and ventral wing epithelia. Here, through morphological and genetic studies, we show that it is the dorsal wing epithelium that determines wing membrane topography. Specifically, we find that wing hair location and membrane topography are coordinated on the dorsal, but not ventral, surface of the wing. In addition, we find that altering Frizzled Planar Cell Polarity (i.e., Fz PCP) signaling in the dorsal wing epithelium alone changes the membrane topography of both dorsal and ventral wing surfaces. We also examined the wing morphology of two model Hymenopterans, the honeybee Apis mellifera and the parasitic wasp Nasonia vitripennis. In both cases, wing hair location and wing membrane topography are coordinated on the dorsal, but not ventral, wing surface, suggesting that the dorsal wing epithelium also controls wing topography in these species. Because phylogenomic studies have identified the Hymenotera as basal within the Endopterygota family tree, these findings suggest that this is a primitive insect character.

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Planar cell polarity and tissue design: Shaping the Drosophila wing membrane

Cited by 8 publications

References 26 publications

The frizzled/stan Pathway and Planar Cell Polarity in the Drosophila Wing

The frizzled/stan Pathway and Planar Cell Polarity in the Drosophila Wing

Strabismus Promotes Recruitment and Degradation of Farnesylated Prickle in Drosophila melanogaster Planar Polarity Specification

Insect Wing Membrane Topography Is Determined by the Dorsal Wing Epithelium

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