Trunk-specific modulation of Wingless signalling in Drosophila by Teashirt binding to Armadillo

Abstract

Background: One function of the Wingless signal cascade is to determine the ‘naked’ cuticle cell-fate choice instead of the denticled one in Drosophila larvae. Wingless stabilises cytoplasmic Armadillo, which may act in a transcriptional activator complex with the DNA-binding protein T-cell factor (also known as Pangolin). As these components are critical for all Wingless-dependent patterning events, the problem arises as to how specific outputs are achieved.Results: The Teashirt zinc finger protein was found to be necessary for a subset of late Wingless-dependent functions in the embryonic trunk segments where the teashirt gene is expressed. Teashirt was found to be required for the maintenance of the late Wingless signalling target gene wingless but not for an earlier one, engrailed. Armadillo and Teashirt proteins showed similar Wingless-dependent modulation patterns in homologous parts of each trunk segment in embryos, with high levels of nuclear Teashirt and intracellular Armadillo within cells destined to form naked cuticle. We found that Teashirt associates with, and requires, Armadillo in a complex for its function.Conclusions: Teashirt binds to, and requires, Armadillo for the naked cell-fate choice in the larval trunk. Teashirt is required for trunk segment identity, suggesting that Teashirt provides a region-specific output to Armadillo activity. Further modulation of Wingless is achieved in homologous parts of each trunk segment where Wingless and Teashirt are especially active. Our results provide a novel, cell-intrinsic mechanism to explain the modulation of the activity of the Wingless signalling pathway.