Limits...
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.

Show MeSH

Related in: MedlinePlus

A Bidirectional-Biphasic (Bid-Bip) model for Fz PCP signaling in the Drosophila wing.The model proposes two distinct Fz PCP signals that differ both in direction and in use of the Prickle protein isoforms, Pk and Sple. An Early Fz(Sple) signal along the A-P axis organizes posterior ridge orientation. A Late Fz(Pk) signal along the P-D axis organizes anterior ridge orientation and hair polarity. (a.p.f. = after pupal formation).
© Copyright Policy
Related In: Results  -  Collection


getmorefigures.php?uid=PMC3040658&req=5

pgen-1001305-g001: A Bidirectional-Biphasic (Bid-Bip) model for Fz PCP signaling in the Drosophila wing.The model proposes two distinct Fz PCP signals that differ both in direction and in use of the Prickle protein isoforms, Pk and Sple. An Early Fz(Sple) signal along the A-P axis organizes posterior ridge orientation. A Late Fz(Pk) signal along the P-D axis organizes anterior ridge orientation and hair polarity. (a.p.f. = after pupal formation).

Mentions: In an earlier paper we showed that, in addition to organizing wing hair polarity, the Fz PCP pathway is required for the integrity and orientation of cuticle ridges that traverse the adult wing membrane [12]. However, although wing hairs have a common orientation across the wing, ridges are aligned with the anteroposterior (A-P) axis in the anterior wing and with the P-D axis in the posterior wing. Consequently, hair and ridge orientation are approximately orthogonal in the anterior wing, but are closely matched in the posterior wing. This presents the problem of how Fz PCP signaling can lead to these two distinct outcomes in anterior and posterior wing cells. Data from our work, and from other labs, has led us to propose a Bidirectional-Biphasic (Bid-Bip) model in which two distinct Fz PCP signaling events occur along different axes of the wing (Figure 1 and [12]). In the model, there is an Early Fz PCP signal aligned with the A-P axis that is approximately symmetric in the anterior and posterior wing. This is followed by a Late Fz PCP signal aligned with the P-D axis. For the model, the direction of Fz PCP signaling is defined as the hair polarity that would be specified by the signal.


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 Bidirectional-Biphasic (Bid-Bip) model for Fz PCP signaling in the Drosophila wing.The model proposes two distinct Fz PCP signals that differ both in direction and in use of the Prickle protein isoforms, Pk and Sple. An Early Fz(Sple) signal along the A-P axis organizes posterior ridge orientation. A Late Fz(Pk) signal along the P-D axis organizes anterior ridge orientation and hair polarity. (a.p.f. = after pupal formation).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3040658&req=5

pgen-1001305-g001: A Bidirectional-Biphasic (Bid-Bip) model for Fz PCP signaling in the Drosophila wing.The model proposes two distinct Fz PCP signals that differ both in direction and in use of the Prickle protein isoforms, Pk and Sple. An Early Fz(Sple) signal along the A-P axis organizes posterior ridge orientation. A Late Fz(Pk) signal along the P-D axis organizes anterior ridge orientation and hair polarity. (a.p.f. = after pupal formation).
Mentions: In an earlier paper we showed that, in addition to organizing wing hair polarity, the Fz PCP pathway is required for the integrity and orientation of cuticle ridges that traverse the adult wing membrane [12]. However, although wing hairs have a common orientation across the wing, ridges are aligned with the anteroposterior (A-P) axis in the anterior wing and with the P-D axis in the posterior wing. Consequently, hair and ridge orientation are approximately orthogonal in the anterior wing, but are closely matched in the posterior wing. This presents the problem of how Fz PCP signaling can lead to these two distinct outcomes in anterior and posterior wing cells. Data from our work, and from other labs, has led us to propose a Bidirectional-Biphasic (Bid-Bip) model in which two distinct Fz PCP signaling events occur along different axes of the wing (Figure 1 and [12]). In the model, there is an Early Fz PCP signal aligned with the A-P axis that is approximately symmetric in the anterior and posterior wing. This is followed by a Late Fz PCP signal aligned with the P-D axis. For the model, the direction of Fz PCP signaling is defined as the hair polarity that would be specified by the signal.

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
Related in: MedlinePlus