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Two frizzled planar cell polarity signals in the Drosophila wing are differentially organized by the Fat/Dachsous pathway.

Hogan J, Valentine M, Cox C, Doyle K, Collier S - PLoS Genet. (2011)

Bottom Line: There is strong evidence that the Fz PCP pathway signals twice during wing development, and we have previously presented a Bidirectional-Biphasic Fz PCP signaling model which proposes that the Early and Late Fz PCP signals are in different directions and employ different isoforms of the Prickle protein.The goal of this study was to investigate the role of the Ft/Ds pathway in the context of our Fz PCP signaling model.Our results allow us to draw the following conclusions: (1) The Early Fz PCP signals are in opposing directions in the anterior and posterior wing and converge precisely at the site of the L3 wing vein. (2) Increased or decreased expression of Ft/Ds pathway genes can alter the direction of the Early Fz PCP signal without affecting the Late Fz PCP signal. (3) Lowfat, a Ft/Ds pathway regulator, is required for the normal orientation of the Early Fz PCP signal but not the Late Fz PCP signal. (4) At the time of the Early Fz PCP signal there are symmetric gradients of dachsous (ds) expression centered on the L3 wing vein, suggesting Ds activity gradients may orient the Fz signal. (5) Localized knockdown or over-expression of Ft/Ds pathway genes shows that boundaries/gradients of Ft/Ds pathway gene expression can redirect the Early Fz PCP signal specifically. (6) Altering the timing of ds knockdown during wing development can separate the role of the Ft/Ds pathway in wing morphogenesis from its role in Early Fz PCP signaling.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Sciences, Marshall University, Huntington, West Virginia, United States of America.

ABSTRACT
The regular array of distally pointing hairs on the mature Drosophila wing is evidence for the fine control of Planar Cell Polarity (PCP) during wing development. Normal wing PCP requires both the Frizzled (Fz) PCP pathway and the Fat/Dachsous (Ft/Ds) pathway, although the functional relationship between these pathways remains under debate. There is strong evidence that the Fz PCP pathway signals twice during wing development, and we have previously presented a Bidirectional-Biphasic Fz PCP signaling model which proposes that the Early and Late Fz PCP signals are in different directions and employ different isoforms of the Prickle protein. The goal of this study was to investigate the role of the Ft/Ds pathway in the context of our Fz PCP signaling model. Our results allow us to draw the following conclusions: (1) The Early Fz PCP signals are in opposing directions in the anterior and posterior wing and converge precisely at the site of the L3 wing vein. (2) Increased or decreased expression of Ft/Ds pathway genes can alter the direction of the Early Fz PCP signal without affecting the Late Fz PCP signal. (3) Lowfat, a Ft/Ds pathway regulator, is required for the normal orientation of the Early Fz PCP signal but not the Late Fz PCP signal. (4) At the time of the Early Fz PCP signal there are symmetric gradients of dachsous (ds) expression centered on the L3 wing vein, suggesting Ds activity gradients may orient the Fz signal. (5) Localized knockdown or over-expression of Ft/Ds pathway genes shows that boundaries/gradients of Ft/Ds pathway gene expression can redirect the Early Fz PCP signal specifically. (6) Altering the timing of ds knockdown during wing development can separate the role of the Ft/Ds pathway in wing morphogenesis from its role in Early Fz PCP signaling.

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A model for PCP specification in the Drosophila wing.At 18 hours a.p.f., there are symmetric gradients of Ds expression that peak at the site of the L3 vein. The resulting Ds activity gradients are opposed by gradients of Ft and Fj activity. The Ft/Ds pathway organizes the direction of the Early Fz PCP signal, which points up the Ds activity gradient towards the site of the L3 vein. This Early Fz PCP signal employs the Sple isoform of the Prickle protein and determines the orientation of posterior wing ridges, which are specified orthogonal to the direction of Fz signaling. The outcome of the Early Fz PCP signal can be modified by the differentiation of wing veins, possibly due to EGF signaling. A second Fz signal occurs prior to wing hair initiation at 32 hours a.p.f. and employs the Pk isoform of the Prickle protein. The Late Fz PCP signal points distally and determines the orientation of hairs and also anterior ridges, which are specified orthogonal to the Fz activity gradient. The Late Fz PCP signal points down the contemporaneous Ds expression gradient and up a Fj expression gradient. However, it is likely that other factors are involved in controlling the direction of the Late Fz PCP signal.
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pgen-1001305-g009: A model for PCP specification in the Drosophila wing.At 18 hours a.p.f., there are symmetric gradients of Ds expression that peak at the site of the L3 vein. The resulting Ds activity gradients are opposed by gradients of Ft and Fj activity. The Ft/Ds pathway organizes the direction of the Early Fz PCP signal, which points up the Ds activity gradient towards the site of the L3 vein. This Early Fz PCP signal employs the Sple isoform of the Prickle protein and determines the orientation of posterior wing ridges, which are specified orthogonal to the direction of Fz signaling. The outcome of the Early Fz PCP signal can be modified by the differentiation of wing veins, possibly due to EGF signaling. A second Fz signal occurs prior to wing hair initiation at 32 hours a.p.f. and employs the Pk isoform of the Prickle protein. The Late Fz PCP signal points distally and determines the orientation of hairs and also anterior ridges, which are specified orthogonal to the Fz activity gradient. The Late Fz PCP signal points down the contemporaneous Ds expression gradient and up a Fj expression gradient. However, it is likely that other factors are involved in controlling the direction of the Late Fz PCP signal.

Mentions: The data presented in this report allow us to refine our Bid-Bip Fz PCP signaling model (Figure 1), particularly the nature of the proposed Early Fz(Sple) signal. We find that the Early Fz(Sple) signal is in opposing directions in the anterior and posterior wing and converges precisely at the site of the L3 vein. The site of the L3 vein, therefore, represents a discontinuity in Early Fz(Sple) signaling that we have called the PCP-D (see Figure 9). However, it is clear that physical differentiation of the L3 vein is not required for the formation of the PCP-D. The correspondence of the PCP-D with the site of the L3 vein is perhaps surprising as the compartment boundary (a barrier to clonal growth that runs a few cells anterior to the L4 vein) appears a more obvious boundary between the anterior and posterior wing. However, the L3 vein has been defined as a specific region of low Hedgehog signaling within the wing [39], suggesting this region has the molecular autonomy needed to function as a signaling centre. In addition, recently published work from the Eaton lab has also identified the L3 vein as the boundary between oppositely polarized cells in the anterior and posterior of early pupal wings [40].


Two frizzled planar cell polarity signals in the Drosophila wing are differentially organized by the Fat/Dachsous pathway.

Hogan J, Valentine M, Cox C, Doyle K, Collier S - PLoS Genet. (2011)

A model for PCP specification in the Drosophila wing.At 18 hours a.p.f., there are symmetric gradients of Ds expression that peak at the site of the L3 vein. The resulting Ds activity gradients are opposed by gradients of Ft and Fj activity. The Ft/Ds pathway organizes the direction of the Early Fz PCP signal, which points up the Ds activity gradient towards the site of the L3 vein. This Early Fz PCP signal employs the Sple isoform of the Prickle protein and determines the orientation of posterior wing ridges, which are specified orthogonal to the direction of Fz signaling. The outcome of the Early Fz PCP signal can be modified by the differentiation of wing veins, possibly due to EGF signaling. A second Fz signal occurs prior to wing hair initiation at 32 hours a.p.f. and employs the Pk isoform of the Prickle protein. The Late Fz PCP signal points distally and determines the orientation of hairs and also anterior ridges, which are specified orthogonal to the Fz activity gradient. The Late Fz PCP signal points down the contemporaneous Ds expression gradient and up a Fj expression gradient. However, it is likely that other factors are involved in controlling the direction of the Late Fz PCP signal.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3040658&req=5

pgen-1001305-g009: A model for PCP specification in the Drosophila wing.At 18 hours a.p.f., there are symmetric gradients of Ds expression that peak at the site of the L3 vein. The resulting Ds activity gradients are opposed by gradients of Ft and Fj activity. The Ft/Ds pathway organizes the direction of the Early Fz PCP signal, which points up the Ds activity gradient towards the site of the L3 vein. This Early Fz PCP signal employs the Sple isoform of the Prickle protein and determines the orientation of posterior wing ridges, which are specified orthogonal to the direction of Fz signaling. The outcome of the Early Fz PCP signal can be modified by the differentiation of wing veins, possibly due to EGF signaling. A second Fz signal occurs prior to wing hair initiation at 32 hours a.p.f. and employs the Pk isoform of the Prickle protein. The Late Fz PCP signal points distally and determines the orientation of hairs and also anterior ridges, which are specified orthogonal to the Fz activity gradient. The Late Fz PCP signal points down the contemporaneous Ds expression gradient and up a Fj expression gradient. However, it is likely that other factors are involved in controlling the direction of the Late Fz PCP signal.
Mentions: The data presented in this report allow us to refine our Bid-Bip Fz PCP signaling model (Figure 1), particularly the nature of the proposed Early Fz(Sple) signal. We find that the Early Fz(Sple) signal is in opposing directions in the anterior and posterior wing and converges precisely at the site of the L3 vein. The site of the L3 vein, therefore, represents a discontinuity in Early Fz(Sple) signaling that we have called the PCP-D (see Figure 9). However, it is clear that physical differentiation of the L3 vein is not required for the formation of the PCP-D. The correspondence of the PCP-D with the site of the L3 vein is perhaps surprising as the compartment boundary (a barrier to clonal growth that runs a few cells anterior to the L4 vein) appears a more obvious boundary between the anterior and posterior wing. However, the L3 vein has been defined as a specific region of low Hedgehog signaling within the wing [39], suggesting this region has the molecular autonomy needed to function as a signaling centre. In addition, recently published work from the Eaton lab has also identified the L3 vein as the boundary between oppositely polarized cells in the anterior and posterior of early pupal wings [40].

Bottom Line: There is strong evidence that the Fz PCP pathway signals twice during wing development, and we have previously presented a Bidirectional-Biphasic Fz PCP signaling model which proposes that the Early and Late Fz PCP signals are in different directions and employ different isoforms of the Prickle protein.The goal of this study was to investigate the role of the Ft/Ds pathway in the context of our Fz PCP signaling model.Our results allow us to draw the following conclusions: (1) The Early Fz PCP signals are in opposing directions in the anterior and posterior wing and converge precisely at the site of the L3 wing vein. (2) Increased or decreased expression of Ft/Ds pathway genes can alter the direction of the Early Fz PCP signal without affecting the Late Fz PCP signal. (3) Lowfat, a Ft/Ds pathway regulator, is required for the normal orientation of the Early Fz PCP signal but not the Late Fz PCP signal. (4) At the time of the Early Fz PCP signal there are symmetric gradients of dachsous (ds) expression centered on the L3 wing vein, suggesting Ds activity gradients may orient the Fz signal. (5) Localized knockdown or over-expression of Ft/Ds pathway genes shows that boundaries/gradients of Ft/Ds pathway gene expression can redirect the Early Fz PCP signal specifically. (6) Altering the timing of ds knockdown during wing development can separate the role of the Ft/Ds pathway in wing morphogenesis from its role in Early Fz PCP signaling.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Sciences, Marshall University, Huntington, West Virginia, United States of America.

ABSTRACT
The regular array of distally pointing hairs on the mature Drosophila wing is evidence for the fine control of Planar Cell Polarity (PCP) during wing development. Normal wing PCP requires both the Frizzled (Fz) PCP pathway and the Fat/Dachsous (Ft/Ds) pathway, although the functional relationship between these pathways remains under debate. There is strong evidence that the Fz PCP pathway signals twice during wing development, and we have previously presented a Bidirectional-Biphasic Fz PCP signaling model which proposes that the Early and Late Fz PCP signals are in different directions and employ different isoforms of the Prickle protein. The goal of this study was to investigate the role of the Ft/Ds pathway in the context of our Fz PCP signaling model. Our results allow us to draw the following conclusions: (1) The Early Fz PCP signals are in opposing directions in the anterior and posterior wing and converge precisely at the site of the L3 wing vein. (2) Increased or decreased expression of Ft/Ds pathway genes can alter the direction of the Early Fz PCP signal without affecting the Late Fz PCP signal. (3) Lowfat, a Ft/Ds pathway regulator, is required for the normal orientation of the Early Fz PCP signal but not the Late Fz PCP signal. (4) At the time of the Early Fz PCP signal there are symmetric gradients of dachsous (ds) expression centered on the L3 wing vein, suggesting Ds activity gradients may orient the Fz signal. (5) Localized knockdown or over-expression of Ft/Ds pathway genes shows that boundaries/gradients of Ft/Ds pathway gene expression can redirect the Early Fz PCP signal specifically. (6) Altering the timing of ds knockdown during wing development can separate the role of the Ft/Ds pathway in wing morphogenesis from its role in Early Fz PCP signaling.

Show MeSH