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Planar cell polarity: the orientation of larval denticles in Drosophila appears to depend on gradients of Dachsous and Fat.

ABSTRACT: The larval ventral belts of Drosophila consist of six to seven rows of denticles that are oriented, some pointing forwards, some backwards. We present evidence that denticle orientation is determined almost entirely by Dachsous and Fat, one of two planar cell polarity systems. If we change the distribution of Dachsous we can alter the polarity of denticles. We suggest that the orientation of the individual denticle rows, in both the anterior compartment (which mostly point backwards) and the posterior compartment (which point forwards), is determined by the opposing slopes of a Dachsous/Fat gradient. We show, by altering the concentration gradients of Dachsous during development, that we can change the polarity of the denticles made by larval cells as they progress between the first and third larval instars without mitosis.

SUBMITTER: Repiso A

PROVIDER: S-EPMC2947754 | biostudies-literature | 2010 Oct

REPOSITORIES: biostudies-literature

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Planar cell polarity: the orientation of larval denticles in Drosophila appears to depend on gradients of Dachsous and Fat.

Repiso Ada A Saavedra Pedro P Casal José J Lawrence Peter A PA

Development (Cambridge, England) 20100908 20

The larval ventral belts of Drosophila consist of six to seven rows of denticles that are oriented, some pointing forwards, some backwards. We present evidence that denticle orientation is determined almost entirely by Dachsous and Fat, one of two planar cell polarity systems. If we change the distribution of Dachsous we can alter the polarity of denticles. We suggest that the orientation of the individual denticle rows, in both the anterior compartment (which mostly point backwards) and the pos ...[more]

PMID: 20826534

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Project description:Planar Cell Polarity (PCP) is an evolutionarily conserved characteristic of animal tissues marked by coordinated polarization of cells or structures in the plane of a tissue. In insect wing epithelium, for instance, PCP is characterized by en masse orientation of hairs orthogonal to its apical-basal axis and pointing along the proximal-distal axis of the organ. Directional cue for PCP has been proposed to be generated by complex sets of interactions amongst three proteins - Fat (Ft), Dachsous (Ds) and Four-jointed (Fj). Ft and Ds are two atypical cadherins, which are phosphorylated by Fj, a Golgi kinase. Ft and Ds from adjacent cells bind heterophilically via their tandem cadherin repeats, and their binding affinities are regulated by Fj. Further, in the wing epithelium, sub-cellular levels of Ft-Ds heterodimers are seen to be elevated at the distal edges of individual cells, prefiguring their PCP. Mechanisms generating this sub-cellular asymmetry of Ft-Ds heterodimer in proximal and distal edges of cells, however, have not been resolved yet. Using a mathematical modeling approach, here we provide a framework for generation of this sub-cellular asymmetry of Ft-Ds heterodimer. First, we explain how the known interactions within Ft-Ds-Fj system translate into sub-cellular asymmetry of Ft-Ds heterodimer. Second, we show that this asymmetric localization of Ft-Ds heterodimer is lost when tissue-level gradient of Fj is flattened, or when phosphorylation of Ft by Fj is abolished, but not when tissue-level gradient of Ds is flattened or when phosphorylation of Ds is abrogated. Finally, we show that distal enrichment of Ds also amplifies Ft-Ds asymmetry. These observations reveal that gradient of Fj expression, phosphorylation of Ft by Fj and sub-cellular distal accumulation of Ds are three critical elements required for generating sub-cellular asymmetry of Ft-Ds heterodimer. Our model integrates the known experimental data and presents testable predictions for future studies.

Dataset Information

Planar cell polarity: the orientation of larval denticles in Drosophila appears to depend on gradients of Dachsous and Fat.

Publications

Planar cell polarity: the orientation of larval denticles in Drosophila appears to depend on gradients of Dachsous and Fat.

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