Asymmetric Notch activation specifies photoreceptors R3 and R4 and planar polarity in the Drosophila eye

Manolis Fanto; Marek Mlodzik

doi:10.1038/17389

Faculty Opinions recommendation of The atypical cadherin Flamingo links Frizzled and Notch signaling in planar polarity establishment in the Drosophila eye.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.1006606.82106 ◽

2002 ◽

Author(s):

Jeffrey Axelrod

Keyword(s):

Notch Signaling ◽

Planar Polarity ◽

Drosophila Eye ◽

Polarity Establishment

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The Atypical Cadherin Flamingo Links Frizzled and Notch Signaling in Planar Polarity Establishment in the Drosophila Eye

Developmental Cell ◽

10.1016/s1534-5807(02)00147-8 ◽

2002 ◽

Vol 2 (5) ◽

pp. 655-666 ◽

Cited By ~ 76

Author(s):

Gishnu Das ◽

Jessica Reynolds-Kenneally ◽

Marek Mlodzik

Keyword(s):

Notch Signaling ◽

Planar Polarity ◽

Drosophila Eye ◽

Polarity Establishment

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Jun mediates Frizzled-induced R3/R4 cell fate distinction and planar polarity determination in the Drosophila eye

Development ◽

10.1242/dev.127.16.3619 ◽

2000 ◽

Vol 127 (16) ◽

pp. 3619-3629 ◽

Cited By ~ 6

Author(s):

U. Weber ◽

N. Paricio ◽

M. Mlodzik

Keyword(s):

Cell Fate ◽

Genetic Interaction ◽

Function Analysis ◽

Loss Of Function ◽

Planar Polarity ◽

Jnk Signaling ◽

Drosophila Eye ◽

Polarity Determination ◽

Signaling Components

Jun acts as a signal-regulated transcription factor in many cellular decisions, ranging from stress response to proliferation control and cell fate induction. Genetic interaction studies have suggested that Jun and JNK signaling are involved in Frizzled (Fz)-mediated planar polarity generation in the Drosophila eye. However, simple loss-of-function analysis of JNK signaling components did not show comparable planar polarity defects. To address the role of Jun and JNK in Fz signaling, we have used a combination of loss- and gain-of-function studies. Like Fz, Jun affects the bias between the R3/R4 photoreceptor pair that is critical for ommatidial polarity establishment. Detailed analysis of jun(−) clones reveals defects in R3 induction and planar polarity determination, whereas gain of Jun function induces the R3 fate and associated polarity phenotypes. We find also that affecting the levels of JNK signaling by either reduction or overexpression leads to planar polarity defects. Similarly, hypomorphic allelic combinations and overexpression of the negative JNK regulator Puckered causes planar polarity eye phenotypes, establishing that JNK acts in planar polarity signaling. The observation that Dl transcription in the early R3/R4 precursor cells is deregulated by Jun or Hep/JNKK activation, reminiscent of the effects seen with Fz overexpression, suggests that Jun is one of the transcription factors that mediates the effects of fz in planar polarity generation.

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Epithelial planar polarity in the developing Drosophila eye

Development ◽

10.1242/dev.121.8.2451 ◽

1995 ◽

Vol 121 (8) ◽

pp. 2451-2459 ◽

Cited By ~ 15

Author(s):

M. Wehrli ◽

A. Tomlinson

Keyword(s):

Positional Information ◽

Reverse Direction ◽

Local Orientation ◽

Planar Polarity ◽

Drosophila Eye ◽

Retinal Epithelium

Experiments with the insect ectoderm have suggested that planar polarity in epithelia results from the local orientation of cells to the slope of a gradient of positional information. Here we show that planar polarity in the Drosophila eye is inverted when the morphogenetic wave that sweeps through the presumptive retinal epithelium is induced to move in the reverse direction. We suggest that the movement of the morphogenetic wave may be causal in establishing the planar polarity of this epithelium.

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Nuclear signaling by Rac and Rho GTPases is required in the establishment of epithelial planar polarity in the Drosophila eye

Current Biology ◽

10.1016/s0960-9822(00)00645-x ◽

2000 ◽

Vol 10 (16) ◽

pp. 979-S1 ◽

Cited By ~ 112

Author(s):

Manolis Fanto ◽

Ursula Weber ◽

David I. Strutt ◽

Marek Mlodzik

Keyword(s):

Rho Gtpases ◽

Planar Polarity ◽

Nuclear Signaling ◽

Drosophila Eye

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Decoding vectorial information from a gradient: sequential roles of the receptors Frizzled and Notch in establishing planar polarity in the Drosophila eye

Development ◽

10.1242/dev.126.24.5725 ◽

1999 ◽

Vol 126 (24) ◽

pp. 5725-5738 ◽

Cited By ~ 10

Author(s):

A. Tomlinson ◽

G. Struhl

Keyword(s):

High Activity ◽

Cell Fate ◽

Photoreceptor Cells ◽

The Other ◽

Cell Fate Decision ◽

Planar Polarity ◽

Genetic Mosaics ◽

Polar Cell ◽

Drosophila Eye ◽

Fate Decision

The Drosophila eye is composed of several hundred ommatidia that can exist in either of two chiral forms, depending on position: ommatidia in the dorsal half of the eye adopt one chiral form, whereas ommatidia in the ventral half adopt the other. Chirality appears to be specified by a polarizing signal with a high activity at the interface between the two halves (the ‘equator’), which declines in opposite directions towards the dorsal and ventral poles. Here, using genetic mosaics, we show that this polarizing signal is decoded by the sequential use of two receptor systems. The first depends on the seven-transmembrane receptor Frizzled (Fz) and distinguishes between the two members of the R3/R4 pair of presumptive photoreceptor cells, predisposing the cell that is located closer to the equator and having higher Fz activity towards the R3 photoreceptor fate and the cell further away towards the R4 fate. This bias is then amplified by subsequent interactions between the two cells mediated by the receptor Notch (N) and its ligand Delta (Dl), ensuring that the equatorial cell becomes the R3 photoreceptor while the polar cell becomes the R4 photoreceptor. As a consequence of this reciprocal cell fate decision, the R4 cell moves asymmetrically relative to the R3 cell, initiating the appropriate chiral pattern of the remaining cells of the ommatidium.

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Notch signalling and the initiation of neural development in the Drosophila eye

Development ◽

10.1242/dev.128.20.3889 ◽

2001 ◽

Vol 128 (20) ◽

pp. 3889-3898 ◽

Cited By ~ 3

Author(s):

Antonio Baonza ◽

Matthew Freeman

Keyword(s):

Neural Development ◽

Notch Signalling ◽

The Other ◽

Signalling Pathways ◽

Notch Signalling Pathway ◽

Drosophila Eye ◽

Dependent Signal ◽

Notch Activation ◽

Number Of Cells

Neural determination in the Drosophila eye occurs progressively. A diffusible signal, Dpp, causes undetermined cells first to adopt a ‘pre-proneural’ state in which they are primed to start differentiating. A second signal is required to trigger the activation of the transcription factor Atonal, which causes the cells to initiate overt photoreceptor neurone differentiation. Both Dpp and the second signal are dependent on Hedgehog (Hh) signalling. Previous work has shown that the Notch signalling pathway also has a proneural role in the eye (as well as a later, opposite function when it restricts the number of cells becoming photoreceptors – a process of lateral inhibition). It is not clear how the early proneural role of Notch integrates with the other signalling pathways involved. We provide evidence that Notch activation by its ligand Delta is the second Hh-dependent signal required for neural determination. Notch activity normally only triggers Atonal expression in cells that have adopted the pre-proneural state induced by Dpp. We also report that Notch drives the transition from pre-proneural to proneural by downregulating two repressors of Atonal: Hairy and Extramacrochaetae.

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