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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.


Influence of Ds-Fat PCP on hair polarity in abdominal pleura.Hair polarity in pleura revealed by F-actin (phalloidin staining) in ft8/ftG-rv (A), dGC13/d210 (B), dGC13 ft8/dGC13 ftG-rv (C), ft8 sple1/ftG-rv sple1 (D), ds36D/dsUA071 (E), dGC13 ds36D/dGC13 dsUA071 (F), ft8 pk30/ftG-rv pk30 (G), ft8 pk-sple14/ftG-rv pk-sple14 (H), dGC13 pk30 (I) and dGC13 sple1 (J) mutant animals. Yellow asterisk indicates the position of the spiracle. Yellow arrows indicate the region where hair orientation is normal, and red arrows indicate the region where hair orientation is disrupted. Dashed yellow lines mark approximate boundaries between regions with normal and abnormal polarity.DOI:http://dx.doi.org/10.7554/eLife.09946.017
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fig9: Influence of Ds-Fat PCP on hair polarity in abdominal pleura.Hair polarity in pleura revealed by F-actin (phalloidin staining) in ft8/ftG-rv (A), dGC13/d210 (B), dGC13 ft8/dGC13 ftG-rv (C), ft8 sple1/ftG-rv sple1 (D), ds36D/dsUA071 (E), dGC13 ds36D/dGC13 dsUA071 (F), ft8 pk30/ftG-rv pk30 (G), ft8 pk-sple14/ftG-rv pk-sple14 (H), dGC13 pk30 (I) and dGC13 sple1 (J) mutant animals. Yellow asterisk indicates the position of the spiracle. Yellow arrows indicate the region where hair orientation is normal, and red arrows indicate the region where hair orientation is disrupted. Dashed yellow lines mark approximate boundaries between regions with normal and abnormal polarity.DOI:http://dx.doi.org/10.7554/eLife.09946.017

Mentions: In fat or ds mutants, hair polarity is disturbed in much of the A and P compartments, although a small region at the front of the A compartment exhibits normal hair polarity (Figures 9A,E, 10A,E) (Casal et al., 2002). To determine whether the abnormal polarity could be explained by mis-localization of Dachs and/or Ds, and a consequent mis-localization of Sple and/or Pk, we assessed both genetic interactions and protein localization. The disruption of polarity within A compartments in fat or ds mutants was correlated with mis-localization of Dachs throughout the A compartment (mostly uniform Dachs in fat mutants, and randomized Dachs in ds mutants, Figures 6D, 8A,K), and mis-localization of Sple everywhere except the most anterior region of the A compartment (Figure 6E,H, 8B). Moreover, mutation of dachs suppressed the hair polarity phenotypes of fat and ds in A compartments (Figures 9C,F, 10C,G) (Mao et al., 2006), and also suppressed the mis-localization of Sple (Figures 6F,H, 8D). These observations suggest that ds and fat polarity phenotypes in the anterior abdomen can be accounted for by a Dachs-dependent mis-localization of Sple, as we had observed in the wing. Mutation of dachs alone does not disrupt polarity in A compartments (Figures 9B, 10B). It could be that in the absence of Dachs and Ds, Sple is localized by the same cues that localize Pk, as Pk localization remained normal within A compartments of ft or ds mutants (Figure 8E,F,K).10.7554/eLife.09946.017Figure 9.Influence of Ds-Fat PCP on hair polarity in abdominal pleura.


Coordination of planar cell polarity pathways through Spiny-legs.

Ambegaonkar AA, Irvine KD - Elife (2015)

Influence of Ds-Fat PCP on hair polarity in abdominal pleura.Hair polarity in pleura revealed by F-actin (phalloidin staining) in ft8/ftG-rv (A), dGC13/d210 (B), dGC13 ft8/dGC13 ftG-rv (C), ft8 sple1/ftG-rv sple1 (D), ds36D/dsUA071 (E), dGC13 ds36D/dGC13 dsUA071 (F), ft8 pk30/ftG-rv pk30 (G), ft8 pk-sple14/ftG-rv pk-sple14 (H), dGC13 pk30 (I) and dGC13 sple1 (J) mutant animals. Yellow asterisk indicates the position of the spiracle. Yellow arrows indicate the region where hair orientation is normal, and red arrows indicate the region where hair orientation is disrupted. Dashed yellow lines mark approximate boundaries between regions with normal and abnormal polarity.DOI:http://dx.doi.org/10.7554/eLife.09946.017
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Related In: Results  -  Collection

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fig9: Influence of Ds-Fat PCP on hair polarity in abdominal pleura.Hair polarity in pleura revealed by F-actin (phalloidin staining) in ft8/ftG-rv (A), dGC13/d210 (B), dGC13 ft8/dGC13 ftG-rv (C), ft8 sple1/ftG-rv sple1 (D), ds36D/dsUA071 (E), dGC13 ds36D/dGC13 dsUA071 (F), ft8 pk30/ftG-rv pk30 (G), ft8 pk-sple14/ftG-rv pk-sple14 (H), dGC13 pk30 (I) and dGC13 sple1 (J) mutant animals. Yellow asterisk indicates the position of the spiracle. Yellow arrows indicate the region where hair orientation is normal, and red arrows indicate the region where hair orientation is disrupted. Dashed yellow lines mark approximate boundaries between regions with normal and abnormal polarity.DOI:http://dx.doi.org/10.7554/eLife.09946.017
Mentions: In fat or ds mutants, hair polarity is disturbed in much of the A and P compartments, although a small region at the front of the A compartment exhibits normal hair polarity (Figures 9A,E, 10A,E) (Casal et al., 2002). To determine whether the abnormal polarity could be explained by mis-localization of Dachs and/or Ds, and a consequent mis-localization of Sple and/or Pk, we assessed both genetic interactions and protein localization. The disruption of polarity within A compartments in fat or ds mutants was correlated with mis-localization of Dachs throughout the A compartment (mostly uniform Dachs in fat mutants, and randomized Dachs in ds mutants, Figures 6D, 8A,K), and mis-localization of Sple everywhere except the most anterior region of the A compartment (Figure 6E,H, 8B). Moreover, mutation of dachs suppressed the hair polarity phenotypes of fat and ds in A compartments (Figures 9C,F, 10C,G) (Mao et al., 2006), and also suppressed the mis-localization of Sple (Figures 6F,H, 8D). These observations suggest that ds and fat polarity phenotypes in the anterior abdomen can be accounted for by a Dachs-dependent mis-localization of Sple, as we had observed in the wing. Mutation of dachs alone does not disrupt polarity in A compartments (Figures 9B, 10B). It could be that in the absence of Dachs and Ds, Sple is localized by the same cues that localize Pk, as Pk localization remained normal within A compartments of ft or ds mutants (Figure 8E,F,K).10.7554/eLife.09946.017Figure 9.Influence of Ds-Fat PCP on hair polarity 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.