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Coordination of planar cell polarity pathways through Spiny-legs.

Ambegaonkar AA, Irvine KD - Elife (2015)

Bottom Line: Two different components of the Dachsous-Fat system, Dachsous and Dachs, can each independently interact with Spiny-legs and direct its localization in vivo.Through characterization of the contributions of Prickle, Spiny-legs, Dachsous, Fat, and Dachs to PCP in the Drosophila wing, eye, and abdomen, we define where Dachs-Spiny-legs and Dachsous-Spiny-legs interactions contribute to PCP, and provide a new understanding of the orientation of polarity and the basis of PCP phenotypes.Our results support the direct linkage of PCP systems through Sple in specific locales, while emphasizing that cells can be subject to and must ultimately resolve distinct, competing PCP signals.

View Article: PubMed Central - PubMed

Affiliation: Howard Hughes Medical Institute, Rutgers University, Piscataway, United States.

ABSTRACT
Morphogenesis and physiology of tissues and organs requires planar cell polarity (PCP) systems that orient and coordinate cells and their behaviors, but the relationship between PCP systems has been controversial. We have characterized how the Frizzled and Dachsous-Fat PCP systems are connected through the Spiny-legs isoform of the Prickle-Spiny-legs locus. Two different components of the Dachsous-Fat system, Dachsous and Dachs, can each independently interact with Spiny-legs and direct its localization in vivo. Through characterization of the contributions of Prickle, Spiny-legs, Dachsous, Fat, and Dachs to PCP in the Drosophila wing, eye, and abdomen, we define where Dachs-Spiny-legs and Dachsous-Spiny-legs interactions contribute to PCP, and provide a new understanding of the orientation of polarity and the basis of PCP phenotypes. Our results support the direct linkage of PCP systems through Sple in specific locales, while emphasizing that cells can be subject to and must ultimately resolve distinct, competing PCP signals.

No MeSH data available.


Related in: MedlinePlus

Gradients influencing PCP in the abdomen.(A) Schematic illustrating the orientation of hairs and approximate gradients of Ds, Fj and Hh expression in the abdomen (Casal et al., 2002; Struhl et al., 1997). (B) Rose plots depicting polarization of GFP:Sple or GFP:Pk in pleural cells of the indicated genotypes. Additional wild-type analysis is for comparison to mutants shown in Figure 6; anterior polarization is to the left and posterior polarization is to the right. For GFP:Sple the anterior compartment was subdivided into a front region (A1, anterior-most 8 cells), and the remainder of the A compartment (A*). For GFP:Pk the A compartment was subdivided into a front region of 5 cells (Af), a back region of 10 cells (Ab), and a middle region comprising the rest of the compartment (Am). (C) Pleura of dGC13 sple1/ dGC13 sple1 pupa with clones of cells expressing GFP:Pk (green). Posterior compartments are marked by hh-Gal4 UAS-mCD8-RFP (red). Anterior-posterior body axis is indicated at top.DOI:http://dx.doi.org/10.7554/eLife.09946.014
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fig6s1: Gradients influencing PCP in the abdomen.(A) Schematic illustrating the orientation of hairs and approximate gradients of Ds, Fj and Hh expression in the abdomen (Casal et al., 2002; Struhl et al., 1997). (B) Rose plots depicting polarization of GFP:Sple or GFP:Pk in pleural cells of the indicated genotypes. Additional wild-type analysis is for comparison to mutants shown in Figure 6; anterior polarization is to the left and posterior polarization is to the right. For GFP:Sple the anterior compartment was subdivided into a front region (A1, anterior-most 8 cells), and the remainder of the A compartment (A*). For GFP:Pk the A compartment was subdivided into a front region of 5 cells (Af), a back region of 10 cells (Ab), and a middle region comprising the rest of the compartment (Am). (C) Pleura of dGC13 sple1/ dGC13 sple1 pupa with clones of cells expressing GFP:Pk (green). Posterior compartments are marked by hh-Gal4 UAS-mCD8-RFP (red). Anterior-posterior body axis is indicated at top.DOI:http://dx.doi.org/10.7554/eLife.09946.014

Mentions: Hairs in the Drosophila abdomen point posteriorly; this orientation is influenced by components of both the Fz and Ds-Fat PCP pathways (Casal et al., 2002; 2006; Lawrence et al., 2004). In analyzing the relationship between PCP pathways in the abdomen, we focused on the pleural cells, which form in lateral and ventral regions, but have also examined polarity in tergites, which form on the dorsal side of the abdomen. As the subcellular localizations of Dachs, Sple and Pk within pupal abdominal cells have not been described, we first characterized their distributions in pleural cells of wild-type animals at pupal stages, with posterior compartments marked using hh-Gal4 and UAS-RFP transgenes. Dachs:GFP and Sple:GFP were polarized towards the anterior sides of cells within A compartments, and towards the posterior sides of cells within P compartments (Figure 6A,B,H). This is consistent with their being polarized in response to the Ds and Fj gradients, as the Fj and Ds gradients are oriented oppositely within anterior (A) versus posterior (P) compartments of each segment (Figure 6—figure supplement 1) (Casal et al., 2002), and Dachs and Sple accumulate on the sides of cells that face towards lower Ds levels and higher Fj levels. Pk:GFP, by contrast, was polarized towards the anterior sides of cells within both A and P compartments (Figure 6C,H). Thus, in A compartments Pk:GFP and Sple:GFP polarize in the same direction, whereas in P compartments they polarize in opposite directions.10.7554/eLife.09946.013Figure 6.Localization of Dachs, Sple and Pk in abdominal pleura.


Coordination of planar cell polarity pathways through Spiny-legs.

Ambegaonkar AA, Irvine KD - Elife (2015)

Gradients influencing PCP in the abdomen.(A) Schematic illustrating the orientation of hairs and approximate gradients of Ds, Fj and Hh expression in the abdomen (Casal et al., 2002; Struhl et al., 1997). (B) Rose plots depicting polarization of GFP:Sple or GFP:Pk in pleural cells of the indicated genotypes. Additional wild-type analysis is for comparison to mutants shown in Figure 6; anterior polarization is to the left and posterior polarization is to the right. For GFP:Sple the anterior compartment was subdivided into a front region (A1, anterior-most 8 cells), and the remainder of the A compartment (A*). For GFP:Pk the A compartment was subdivided into a front region of 5 cells (Af), a back region of 10 cells (Ab), and a middle region comprising the rest of the compartment (Am). (C) Pleura of dGC13 sple1/ dGC13 sple1 pupa with clones of cells expressing GFP:Pk (green). Posterior compartments are marked by hh-Gal4 UAS-mCD8-RFP (red). Anterior-posterior body axis is indicated at top.DOI:http://dx.doi.org/10.7554/eLife.09946.014
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Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4764577&req=5

fig6s1: Gradients influencing PCP in the abdomen.(A) Schematic illustrating the orientation of hairs and approximate gradients of Ds, Fj and Hh expression in the abdomen (Casal et al., 2002; Struhl et al., 1997). (B) Rose plots depicting polarization of GFP:Sple or GFP:Pk in pleural cells of the indicated genotypes. Additional wild-type analysis is for comparison to mutants shown in Figure 6; anterior polarization is to the left and posterior polarization is to the right. For GFP:Sple the anterior compartment was subdivided into a front region (A1, anterior-most 8 cells), and the remainder of the A compartment (A*). For GFP:Pk the A compartment was subdivided into a front region of 5 cells (Af), a back region of 10 cells (Ab), and a middle region comprising the rest of the compartment (Am). (C) Pleura of dGC13 sple1/ dGC13 sple1 pupa with clones of cells expressing GFP:Pk (green). Posterior compartments are marked by hh-Gal4 UAS-mCD8-RFP (red). Anterior-posterior body axis is indicated at top.DOI:http://dx.doi.org/10.7554/eLife.09946.014
Mentions: Hairs in the Drosophila abdomen point posteriorly; this orientation is influenced by components of both the Fz and Ds-Fat PCP pathways (Casal et al., 2002; 2006; Lawrence et al., 2004). In analyzing the relationship between PCP pathways in the abdomen, we focused on the pleural cells, which form in lateral and ventral regions, but have also examined polarity in tergites, which form on the dorsal side of the abdomen. As the subcellular localizations of Dachs, Sple and Pk within pupal abdominal cells have not been described, we first characterized their distributions in pleural cells of wild-type animals at pupal stages, with posterior compartments marked using hh-Gal4 and UAS-RFP transgenes. Dachs:GFP and Sple:GFP were polarized towards the anterior sides of cells within A compartments, and towards the posterior sides of cells within P compartments (Figure 6A,B,H). This is consistent with their being polarized in response to the Ds and Fj gradients, as the Fj and Ds gradients are oriented oppositely within anterior (A) versus posterior (P) compartments of each segment (Figure 6—figure supplement 1) (Casal et al., 2002), and Dachs and Sple accumulate on the sides of cells that face towards lower Ds levels and higher Fj levels. Pk:GFP, by contrast, was polarized towards the anterior sides of cells within both A and P compartments (Figure 6C,H). Thus, in A compartments Pk:GFP and Sple:GFP polarize in the same direction, whereas in P compartments they polarize in opposite directions.10.7554/eLife.09946.013Figure 6.Localization of Dachs, Sple and Pk in abdominal pleura.

Bottom Line: Two different components of the Dachsous-Fat system, Dachsous and Dachs, can each independently interact with Spiny-legs and direct its localization in vivo.Through characterization of the contributions of Prickle, Spiny-legs, Dachsous, Fat, and Dachs to PCP in the Drosophila wing, eye, and abdomen, we define where Dachs-Spiny-legs and Dachsous-Spiny-legs interactions contribute to PCP, and provide a new understanding of the orientation of polarity and the basis of PCP phenotypes.Our results support the direct linkage of PCP systems through Sple in specific locales, while emphasizing that cells can be subject to and must ultimately resolve distinct, competing PCP signals.

View Article: PubMed Central - PubMed

Affiliation: Howard Hughes Medical Institute, Rutgers University, Piscataway, United States.

ABSTRACT
Morphogenesis and physiology of tissues and organs requires planar cell polarity (PCP) systems that orient and coordinate cells and their behaviors, but the relationship between PCP systems has been controversial. We have characterized how the Frizzled and Dachsous-Fat PCP systems are connected through the Spiny-legs isoform of the Prickle-Spiny-legs locus. Two different components of the Dachsous-Fat system, Dachsous and Dachs, can each independently interact with Spiny-legs and direct its localization in vivo. Through characterization of the contributions of Prickle, Spiny-legs, Dachsous, Fat, and Dachs to PCP in the Drosophila wing, eye, and abdomen, we define where Dachs-Spiny-legs and Dachsous-Spiny-legs interactions contribute to PCP, and provide a new understanding of the orientation of polarity and the basis of PCP phenotypes. Our results support the direct linkage of PCP systems through Sple in specific locales, while emphasizing that cells can be subject to and must ultimately resolve distinct, competing PCP signals.

No MeSH data available.


Related in: MedlinePlus