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Van Gogh and Frizzled act redundantly in the Drosophila sensory organ precursor cell to orient its asymmetric division.

Gomes JE, Corado M, Schweisguth F - PLoS ONE (2009)

Bottom Line: Here, we investigate the relative contributions of Vang, Fz and Dishevelled (Dsh), a membrane-associated protein acting downstream of Fz, in orienting SOP polarity.Additionally, we find that the activity of Vang is dispensable for the non-autonomous polarizing activity of fz.These observations indicate that both Vang and Fz act as cues for downstream effectors orienting the planar polarity axis of dividing SOPs.

View Article: PubMed Central - PubMed

Affiliation: Ecole Normale Supérieure, CNRS UMR8542, Paris, France.

ABSTRACT
Drosophila sensory organ precursor cells (SOPs) divide asymmetrically along the anterior-posterior (a-p) body axis to generate two different daughter cells. Planar Cell Polarity (PCP) regulates the a-p orientation of the SOP division. The localization of the PCP proteins Van Gogh (Vang) and Frizzled (Fz) define anterior and posterior apical membrane domains prior to SOP division. Here, we investigate the relative contributions of Vang, Fz and Dishevelled (Dsh), a membrane-associated protein acting downstream of Fz, in orienting SOP polarity. Genetic and live imaging analyses suggest that Dsh restricts the localization of a centrosome-attracting activity to the anterior cortex and that Vang is a target of Dsh in this process. Using a clone border assay, we provide evidence that the Vang and fz genes act redundantly in SOPs to orient its polarity axis in response to extrinsic local PCP cues. Additionally, we find that the activity of Vang is dispensable for the non-autonomous polarizing activity of fz. These observations indicate that both Vang and Fz act as cues for downstream effectors orienting the planar polarity axis of dividing SOPs.

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Related in: MedlinePlus

Fz and Vang are individually dispensable to orient the SOP polarity axis.The orientation of SOP division was studied along the border of wild-type control (A–B′), Vangstbm6c mutant (C–D′) and fz(RNAi) (E–F′) clones. SOPs were identified using Sens (red in A, B, E and F) in fixed tissues and GFP-PonLD (green in C and D) in living tissues. Orientation of the division was determined using Pins (blue in A, B, E and F) or GFP-PonLD (green in C and D). We used nls-GFP (in green) as a clone marker. (A–B′) wild-type SOPs inside (GFP− in A) and outside (GFP+ in B) control clones. (C–D′) Vangstbm6c mutant (GFP− in C) and wild-type (GFP+ in D) SOPs. (E–F′) fz(RNAi) (GFP− in E) and wild-type (GFP+ in F) SOPs. The orientation of SOP division was measured as an angle between the axis of SOP polarity oriented towards Pins and Pon and a line corresponding to the clone border at the position of the dividing SOPs (see A′ for a graphic representation). Angle values corresponding to the genotypes studied in top panels are plotted in the bottom panels. The orientation of the asymmetry axis, relative to the clone margin, was divided in four categories, corresponding to four 90° quadrants of the circumference (see A′). Statistical differences between genotypes were evaluated by comparing the number of SOPs per quadrant using a Fischer exact test (4×2 contingency table). No statistically significant difference was seen in the orientation of wild-type control SOPs located outside (A′) and inside (B′) the clone. However, the orientation of SOPs located along Vangstbm6c mutant and fz(RNAi) clone borders (C′,D′,E′ and F′) was significantly different from wild-type control distribution.
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pone-0004485-g003: Fz and Vang are individually dispensable to orient the SOP polarity axis.The orientation of SOP division was studied along the border of wild-type control (A–B′), Vangstbm6c mutant (C–D′) and fz(RNAi) (E–F′) clones. SOPs were identified using Sens (red in A, B, E and F) in fixed tissues and GFP-PonLD (green in C and D) in living tissues. Orientation of the division was determined using Pins (blue in A, B, E and F) or GFP-PonLD (green in C and D). We used nls-GFP (in green) as a clone marker. (A–B′) wild-type SOPs inside (GFP− in A) and outside (GFP+ in B) control clones. (C–D′) Vangstbm6c mutant (GFP− in C) and wild-type (GFP+ in D) SOPs. (E–F′) fz(RNAi) (GFP− in E) and wild-type (GFP+ in F) SOPs. The orientation of SOP division was measured as an angle between the axis of SOP polarity oriented towards Pins and Pon and a line corresponding to the clone border at the position of the dividing SOPs (see A′ for a graphic representation). Angle values corresponding to the genotypes studied in top panels are plotted in the bottom panels. The orientation of the asymmetry axis, relative to the clone margin, was divided in four categories, corresponding to four 90° quadrants of the circumference (see A′). Statistical differences between genotypes were evaluated by comparing the number of SOPs per quadrant using a Fischer exact test (4×2 contingency table). No statistically significant difference was seen in the orientation of wild-type control SOPs located outside (A′) and inside (B′) the clone. However, the orientation of SOPs located along Vangstbm6c mutant and fz(RNAi) clone borders (C′,D′,E′ and F′) was significantly different from wild-type control distribution.

Mentions: Figure 3:


Van Gogh and Frizzled act redundantly in the Drosophila sensory organ precursor cell to orient its asymmetric division.

Gomes JE, Corado M, Schweisguth F - PLoS ONE (2009)

Fz and Vang are individually dispensable to orient the SOP polarity axis.The orientation of SOP division was studied along the border of wild-type control (A–B′), Vangstbm6c mutant (C–D′) and fz(RNAi) (E–F′) clones. SOPs were identified using Sens (red in A, B, E and F) in fixed tissues and GFP-PonLD (green in C and D) in living tissues. Orientation of the division was determined using Pins (blue in A, B, E and F) or GFP-PonLD (green in C and D). We used nls-GFP (in green) as a clone marker. (A–B′) wild-type SOPs inside (GFP− in A) and outside (GFP+ in B) control clones. (C–D′) Vangstbm6c mutant (GFP− in C) and wild-type (GFP+ in D) SOPs. (E–F′) fz(RNAi) (GFP− in E) and wild-type (GFP+ in F) SOPs. The orientation of SOP division was measured as an angle between the axis of SOP polarity oriented towards Pins and Pon and a line corresponding to the clone border at the position of the dividing SOPs (see A′ for a graphic representation). Angle values corresponding to the genotypes studied in top panels are plotted in the bottom panels. The orientation of the asymmetry axis, relative to the clone margin, was divided in four categories, corresponding to four 90° quadrants of the circumference (see A′). Statistical differences between genotypes were evaluated by comparing the number of SOPs per quadrant using a Fischer exact test (4×2 contingency table). No statistically significant difference was seen in the orientation of wild-type control SOPs located outside (A′) and inside (B′) the clone. However, the orientation of SOPs located along Vangstbm6c mutant and fz(RNAi) clone borders (C′,D′,E′ and F′) was significantly different from wild-type control distribution.
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Related In: Results  -  Collection

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pone-0004485-g003: Fz and Vang are individually dispensable to orient the SOP polarity axis.The orientation of SOP division was studied along the border of wild-type control (A–B′), Vangstbm6c mutant (C–D′) and fz(RNAi) (E–F′) clones. SOPs were identified using Sens (red in A, B, E and F) in fixed tissues and GFP-PonLD (green in C and D) in living tissues. Orientation of the division was determined using Pins (blue in A, B, E and F) or GFP-PonLD (green in C and D). We used nls-GFP (in green) as a clone marker. (A–B′) wild-type SOPs inside (GFP− in A) and outside (GFP+ in B) control clones. (C–D′) Vangstbm6c mutant (GFP− in C) and wild-type (GFP+ in D) SOPs. (E–F′) fz(RNAi) (GFP− in E) and wild-type (GFP+ in F) SOPs. The orientation of SOP division was measured as an angle between the axis of SOP polarity oriented towards Pins and Pon and a line corresponding to the clone border at the position of the dividing SOPs (see A′ for a graphic representation). Angle values corresponding to the genotypes studied in top panels are plotted in the bottom panels. The orientation of the asymmetry axis, relative to the clone margin, was divided in four categories, corresponding to four 90° quadrants of the circumference (see A′). Statistical differences between genotypes were evaluated by comparing the number of SOPs per quadrant using a Fischer exact test (4×2 contingency table). No statistically significant difference was seen in the orientation of wild-type control SOPs located outside (A′) and inside (B′) the clone. However, the orientation of SOPs located along Vangstbm6c mutant and fz(RNAi) clone borders (C′,D′,E′ and F′) was significantly different from wild-type control distribution.
Mentions: Figure 3:

Bottom Line: Here, we investigate the relative contributions of Vang, Fz and Dishevelled (Dsh), a membrane-associated protein acting downstream of Fz, in orienting SOP polarity.Additionally, we find that the activity of Vang is dispensable for the non-autonomous polarizing activity of fz.These observations indicate that both Vang and Fz act as cues for downstream effectors orienting the planar polarity axis of dividing SOPs.

View Article: PubMed Central - PubMed

Affiliation: Ecole Normale Supérieure, CNRS UMR8542, Paris, France.

ABSTRACT
Drosophila sensory organ precursor cells (SOPs) divide asymmetrically along the anterior-posterior (a-p) body axis to generate two different daughter cells. Planar Cell Polarity (PCP) regulates the a-p orientation of the SOP division. The localization of the PCP proteins Van Gogh (Vang) and Frizzled (Fz) define anterior and posterior apical membrane domains prior to SOP division. Here, we investigate the relative contributions of Vang, Fz and Dishevelled (Dsh), a membrane-associated protein acting downstream of Fz, in orienting SOP polarity. Genetic and live imaging analyses suggest that Dsh restricts the localization of a centrosome-attracting activity to the anterior cortex and that Vang is a target of Dsh in this process. Using a clone border assay, we provide evidence that the Vang and fz genes act redundantly in SOPs to orient its polarity axis in response to extrinsic local PCP cues. Additionally, we find that the activity of Vang is dispensable for the non-autonomous polarizing activity of fz. These observations indicate that both Vang and Fz act as cues for downstream effectors orienting the planar polarity axis of dividing SOPs.

Show MeSH
Related in: MedlinePlus