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Wingless blocks bristle formation and morphogenetic furrow progression in the eye through repression of Daughterless
Kenneth M Cadigan1, Austin D Jou, Roel Nusse
1Howard Hughes Medical Institute and the Department of Developmental Biology, Stanford University School of Medicine, Beckman Center,Stanford, California 94305, USA. cadigan@umich.edu
Abstract:
In the developing eye, wingless activity represses proneural gene expression (and thus interommatidial bristle formation) and positions the morphogenetic furrow by blocking its initiation in the dorsal and ventral regions of the presumptive eye. We provide evidence that wingless mediates both effects, at least in part, through repression of the basic helix-loop-helix protein Daughterless. daughterless is required for high proneural gene expression and furrow progression. Ectopic expression of wingless blocks Daughterless expression in the proneural clusters. This repression, and that of furrow progression, can be mimicked by an activated form of armadillo and blocked by a dominant negative form of pangolin/TCF. Placing daughterless under the control of a heterologous promoter blocks the ability of ectopic wingless to inhibit bristle formation and furrow progression. hedgehog and decapentapleigic could not rescue the wingless furrow progression block, indicating that wingless acts downstream of these genes. In contrast, Atonal and Scute, which are thought to heterodimerize with Daughterless to promote furrow progression and bristle formation, respectively, can block ectopic wingless action. These results are summarized in a model where daughterless is a major, but probably not the only, target of wingless action in the eye.
Insights
Wingless signaling in developing eyes represses proneural gene expression and eye furrow formation by inhibiting the Daughterless protein. This finding reveals Daughterless as a key target of Wingless during eye development.
Area of Science:
- Developmental biology
- Molecular genetics
- Ophthalmology
Background:
- Wingless signaling is crucial for eye development.
- Proper regulation of proneural gene expression and morphogenetic furrow progression is essential for eye formation.
Purpose of the Study:
- To investigate the molecular mechanisms by which wingless (Wg) signaling controls eye development.
- To identify the downstream targets of Wg signaling in the developing Drosophila eye.
Main Methods:
- Utilized genetic manipulation in Drosophila melanogaster.
- Examined gene expression patterns of proneural genes and furrow progression.
- Assessed the role of Daughterless (Da) protein in Wg signaling pathways.
Main Results:
- Wingless activity represses proneural gene expression and blocks furrow progression, partly by inhibiting Daughterless.
- Ectopic wingless expression reduces Daughterless levels and inhibits furrow progression.
- Daughterless expression under a heterologous promoter rescues wingless-mediated inhibition of bristle formation and furrow progression.
Conclusions:
- Daughterless is a major downstream target of wingless signaling in the developing eye.
- Wingless acts downstream of hedgehog and decapentaplegic signaling pathways.
- Atonal and Scute can counteract ectopic wingless activity, suggesting complex regulatory interactions.