STRIPAK–PP2A regulates Hippo-Yorkie signaling to suppress retinal fate in the Drosophila eye disc peripodial epithelium

Scott J. Neal; Qingxiang Zhou; Francesca Pignoni

doi:10.1242/jcs.237834

Broad-complex, but not ecdysone receptor, is required for progression of the morphogenetic furrow in the Drosophila eye

Development ◽

10.1242/dev.128.1.1 ◽

2001 ◽

Vol 128 (1) ◽

pp. 1-11 ◽

Cited By ~ 6

Author(s):

C.A. Brennan ◽

T.R. Li ◽

M. Bender ◽

F. Hsiung ◽

K. Moses

Keyword(s):

Zinc Finger ◽

Receptor Gene ◽

Ecdysone Receptor ◽

Morphogenetic Furrow ◽

Response Gene ◽

Ecdysteroid Receptor ◽

Receptor Isoforms ◽

Eye Disc ◽

Drosophila Eye ◽

Broad Complex

The progression of the morphogenetic furrow in the developing Drosophila eye is an early metamorphic, ecdysteroid-dependent event. Although Ecdysone receptor-encoded nuclear receptor isoforms are the only known ecdysteroid receptors, we show that the Ecdysone receptor gene is not required for furrow function. DHR78, which encodes another candidate ecdysteroid receptor, is also not required. In contrast, zinc finger-containing isoforms encoded by the early ecdysone response gene Broad-complex regulate furrow progression and photoreceptor specification. br-encoded Broad-complex subfunctions are required for furrow progression and proper R8 specification, and are antagonized by other subfunctions of Broad-complex. There is a switch from Broad complex Z2 to Z1 zinc-finger isoform expression at the furrow which requires Z2 expression and responds to Hedgehog signals. These results suggest that a novel hormone transduction hierarchy involving an uncharacterized receptor operates in the eye disc.

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Role of the morphogenetic furrow in establishing polarity in the Drosophila eye

Development ◽

10.1242/dev.121.12.4085 ◽

1995 ◽

Vol 121 (12) ◽

pp. 4085-4094 ◽

Cited By ~ 12

Author(s):

F. Chanut ◽

U. Heberlein

Keyword(s):

Ectopic Expression ◽

Morphogenetic Furrow ◽

Eye Disc ◽

Drosophila Eye ◽

Retinal Epithelium ◽

Anteroposterior Polarity ◽

Crystalline Array

The Drosophila retina is a crystalline array of 800 ommatidia whose organization and assembly suggest polarization of the retinal epithelium along anteroposterior and dorsoventral axes. The retina develops by a stepwise process following the posterior-to-anterior progression of the morphogenetic furrow across the eye disc. Ectopic expression of hedgehog or local removal of patched function generates ectopic furrows that can progress in any direction across the disc leaving in their wake differentiating fields of ectopic ommatidia. We have studied the effect of these ectopic furrows on the polarity of ommatidial assembly and rotation. We find that the anteroposterior asymmetry of ommatidial assembly parallels the progression of ectopic furrows, regardless of their direction. In addition, ommatidia developing behind ectopic furrows rotate coordinately, forming equators in various regions of the disc. Interestingly, the expression of a marker normally restricted to the equator is induced in ectopic ommatidial fields. Ectopic equators are stable as they persist to adulthood, where they can coexist with the normal equator. Our results suggest that ectopic furrows can impart polarity to the disc epithelium, regarding the direction of both assembly and rotation of ommatidia. We propose that these processes are polarized as a consequence of furrow propagation, while more global determinants of dorsoventral and anteroposterior polarity may act less directly by determining the site of furrow initiation.

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Lobe mediates Notch signaling to control domain-specific growth in the Drosophila eye disc

Development ◽

10.1242/dev.129.17.4005 ◽

2002 ◽

Vol 129 (17) ◽

pp. 4005-4013 ◽

Cited By ~ 2

Author(s):

Joshua J. Chern ◽

Kwang-Wook Choi

Keyword(s):

Mirror Symmetry ◽

Tissue Loss ◽

Domain Specific ◽

Eye Growth ◽

Proliferative Effect ◽

Eye Disc ◽

Drosophila Eye ◽

Domain Loss ◽

Necessary And Sufficient ◽

Novel Protein

Notch (N) activation at the dorsoventral (DV) boundary of the Drosophila eye is required for early eye primordium growth. Despite the apparent DV mirror symmetry, some mutations cause a preferential loss of the ventral domain, suggesting that the growth of individual domains is asymmetrically regulated. We show that the Lobe (L) gene is required non-autonomously for ventral growth but not dorsal growth, and that it mediates the proliferative effect of midline N signaling in a ventral-specific manner. L encodes a novel protein with a conserved domain. Loss of L suppresses the overproliferation phenotype of constitutive N activation in the ventral, but not in the dorsal eye, and gain of L rescues ventral tissue loss in N mutant background. Furthermore, L is necessary and sufficient for the ventral expression of a N ligand, Serrate (Ser), which affects ventral growth. Our data suggest that the control of ventral Ser expression by L represents a molecular mechanism that governs asymmetrical eye growth.

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Integrins Regulate Apical Constriction via Microtubule Stabilization in the Drosophila Eye Disc Epithelium

Cell Reports ◽

10.1016/j.celrep.2014.11.041 ◽

2014 ◽

Vol 9 (6) ◽

pp. 2043-2055 ◽

Cited By ~ 13

Author(s):

Vilaiwan M. Fernandes ◽

Kasandra McCormack ◽

Lindsay Lewellyn ◽

Esther M. Verheyen

Keyword(s):

Apical Constriction ◽

Microtubule Stabilization ◽

Eye Disc ◽

Drosophila Eye

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Drosophila eye disc margin is a center for organizing long-range planar polarity

genesis ◽

10.1002/gene.20022 ◽

2004 ◽

Vol 39 (1) ◽

pp. 26-37 ◽

Cited By ~ 8

Author(s):

Janghoo Lim ◽

Kwang-Wook Choi

Keyword(s):

Long Range ◽

Planar Polarity ◽

Eye Disc ◽

Drosophila Eye

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Ommatidial development in Drosophila eye disc fragments

Developmental Biology ◽

10.1016/0012-1606(86)90335-0 ◽

1986 ◽

Vol 117 (2) ◽

pp. 663-671 ◽

Cited By ~ 32

Author(s):

Richard M. Lebovitz ◽

Donald F. Ready

Keyword(s):

Eye Disc ◽

Drosophila Eye

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A Model of the Spatio-temporal Dynamics of Drosophila Eye Disc Development

PLoS Computational Biology ◽

10.1371/journal.pcbi.1005052 ◽

2016 ◽

Vol 12 (9) ◽

pp. e1005052 ◽

Cited By ~ 10

Author(s):

Patrick Fried ◽

Máximo Sánchez-Aragón ◽

Daniel Aguilar-Hidalgo ◽

Birgitta Lehtinen ◽

Fernando Casares ◽

...

Keyword(s):

Temporal Dynamics ◽

Eye Disc ◽

Drosophila Eye ◽

Spatio Temporal

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Hedgehog is an indirect regulator of morphogenetic furrow progression in the Drosophila eye disc

Development ◽

10.1242/dev.124.17.3233 ◽

1997 ◽

Vol 124 (17) ◽

pp. 3233-3240 ◽

Cited By ~ 11

Author(s):

D.I. Strutt ◽

M. Mlodzik

Keyword(s):

Pattern Formation ◽

Imaginal Disc ◽

Morphogenetic Furrow ◽

Anterior Edge ◽

Eye Disc ◽

Drosophila Eye ◽

Eye Imaginal Disc ◽

Inductive Signal ◽

Rate Of Movement

Pattern formation in the eye imaginal disc of Drosophila occurs in a wave that moves from posterior to anterior. The anterior edge of this wave is marked by a contracted band of cells known as the morphogenetic furrow, behind which photoreceptors differentiate. The movement of the furrow is dependent upon the secretion of the signalling protein Hedgehog (Hh) by more posterior cells, and it has been suggested that Hh acts as an inductive signal to induce cells to enter a furrow fate and begin differentiation. To further define the role of Hh in this process, we have analysed clones of cells lacking the function of the smoothened (smo) gene, which is required for transduction of the Hh signal and allows the investigation of the autonomous requirement for hh signalling. These experiments demonstrate that the function of hh in furrow progression is indirect. Cells that cannot receive/transduce the Hh signal are still capable of entering a furrow fate and differentiating normally. However, hh is required to promote furrow progression and regulate its rate of movement across the disc, since the furrow is significantly delayed in smo clones.

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Ommatidial polarity in the Drosophila eye is determined by the direction of furrow progression and local interactions

Development ◽

10.1242/dev.121.12.4247 ◽

1995 ◽

Vol 121 (12) ◽

pp. 4247-4256 ◽

Cited By ~ 10

Author(s):

D.I. Strutt ◽

M. Mlodzik

Keyword(s):

Mirror Image ◽

Hedgehog Pathway ◽

Ordered Structure ◽

Local Interactions ◽

Eye Disc ◽

Drosophila Eye

The adult eye of Drosophila is a highly ordered structure. It is composed of about 800 ommatidia, each displaying precise polarity. The ommatidia are arranged about an axis of mirror image symmetry, the equator, which lies along the dorsoventral midline of the eye. We use hedgehog pathway mutants to induce ectopic morphogenetic furrows and use these as a tool to investigate the establishment of ommatidial polarity. Our results show that ommatidial clusters are self-organising units whose polarity in one axis is determined by the direction of furrow progression, and which can independently define the position of an equator without reference to the global coordinates of the eye disc.

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The role of Wingless signaling in establishing the anteroposterior and dorsoventral axes of the eye disc

Development ◽

10.1242/dev.128.9.1519 ◽

2001 ◽

Vol 128 (9) ◽

pp. 1519-1529 ◽

Cited By ~ 3

Author(s):

J.D. Lee ◽

J.E. Treisman

Keyword(s):

Signaling Molecules ◽

Morphogenetic Furrow ◽

Wild Type ◽

Dorsoventral Axis ◽

Eye Disc ◽

Wingless Signaling ◽

Drosophila Eye ◽

Ectopic Activation ◽

Lateral Margins

The posteriorly expressed signaling molecules Hedgehog and Decapentaplegic drive photoreceptor differentiation in the Drosophila eye disc, while at the anterior lateral margins Wingless expression blocks ectopic differentiation. We show here that mutations in axin prevent photoreceptor differentiation and lead to tissue overgrowth and that both these effects are due to ectopic activation of the Wingless pathway. In addition, ectopic Wingless signaling causes posterior cells to take on an anterior identity, reorienting the direction of morphogenetic furrow progression in neighboring wild-type cells. We also show that signaling by Decapentaplegic and Hedgehog normally blocks the posterior expression of anterior markers such as Eyeless. Wingless signaling is not required to maintain anterior Eyeless expression and in combination with Decapentaplegic signaling can promote its downregulation, suggesting that additional molecules contribute to anterior identity. Along the dorsoventral axis of the eye disc, Wingless signaling is sufficient to promote dorsal expression of the Iroquois gene mirror, even in the absence of the upstream factor pannier. However, Wingless signaling does not lead to ventral mirror expression, implying the existence of ventral repressors.

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