Dachsous-Dependent Asymmetric Localization of Spiny-Legs Determines Planar Cell Polarity Orientation in Drosophila

In Drosophila, planar cell polarity (PCP) molecules such as Dachsous (Ds) may function as global directional cues directing the asymmetrical localization of PCP core proteins such as Frizzled (Fz). However, the relationship between Ds asymmetry and Fz localization in the eye is opposite to that in t...

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Main Authors: Tomonori Ayukawa, Masakazu Akiyama, Jennifer L. Mummery-Widmer, Thomas Stoeger, Junko Sasaki, Juergen A. Knoblich, Haruki Senoo, Takehiko Sasaki, Masakazu Yamazaki
Format: Article
Language:English
Published: Elsevier 2014-07-01
Series:Cell Reports
Online Access:http://www.sciencedirect.com/science/article/pii/S221112471400477X
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spelling doaj-8afbad580a384e989ba6a5480a30bd112020-11-25T02:35:54ZengElsevierCell Reports2211-12472014-07-018261062110.1016/j.celrep.2014.06.009Dachsous-Dependent Asymmetric Localization of Spiny-Legs Determines Planar Cell Polarity Orientation in DrosophilaTomonori Ayukawa0Masakazu Akiyama1Jennifer L. Mummery-Widmer2Thomas Stoeger3Junko Sasaki4Juergen A. Knoblich5Haruki Senoo6Takehiko Sasaki7Masakazu Yamazaki8Research Center for Biosignal, Akita University, Akita 010-8543, JapanResearch Institute for Electronic Science, Hokkaido University, Hokkaido 060-0812, JapanInstitute of Molecular Biotechnology of the Austrian Academy of Sciences (IMBA), Vienna 1030, AustriaInstitute of Molecular Biotechnology of the Austrian Academy of Sciences (IMBA), Vienna 1030, AustriaDepartment of Medical Biology, Akita University Graduate School of Medicine, Akita 010-8543, JapanInstitute of Molecular Biotechnology of the Austrian Academy of Sciences (IMBA), Vienna 1030, AustriaDepartment of Cell Biology and Morphology, Akita University Graduate School of Medicine, Akita 010-8543, JapanResearch Center for Biosignal, Akita University, Akita 010-8543, JapanResearch Center for Biosignal, Akita University, Akita 010-8543, JapanIn Drosophila, planar cell polarity (PCP) molecules such as Dachsous (Ds) may function as global directional cues directing the asymmetrical localization of PCP core proteins such as Frizzled (Fz). However, the relationship between Ds asymmetry and Fz localization in the eye is opposite to that in the wing, thereby causing controversy regarding how these two systems are connected. Here, we show that this relationship is determined by the ratio of two Prickle (Pk) isoforms, Pk and Spiny-legs (Sple). Pk and Sple form different complexes with distinct subcellular localizations. When the amount of Sple is increased in the wing, Sple induces a reversal of PCP using the Ds-Ft system. A mathematical model demonstrates that Sple is the key regulator connecting Ds and the core proteins. Our model explains the previously noted discrepancies in terms of the differing relative amounts of Sple in the eye and wing.http://www.sciencedirect.com/science/article/pii/S221112471400477X
collection DOAJ
language English
format Article
sources DOAJ
author Tomonori Ayukawa
Masakazu Akiyama
Jennifer L. Mummery-Widmer
Thomas Stoeger
Junko Sasaki
Juergen A. Knoblich
Haruki Senoo
Takehiko Sasaki
Masakazu Yamazaki
spellingShingle Tomonori Ayukawa
Masakazu Akiyama
Jennifer L. Mummery-Widmer
Thomas Stoeger
Junko Sasaki
Juergen A. Knoblich
Haruki Senoo
Takehiko Sasaki
Masakazu Yamazaki
Dachsous-Dependent Asymmetric Localization of Spiny-Legs Determines Planar Cell Polarity Orientation in Drosophila
Cell Reports
author_facet Tomonori Ayukawa
Masakazu Akiyama
Jennifer L. Mummery-Widmer
Thomas Stoeger
Junko Sasaki
Juergen A. Knoblich
Haruki Senoo
Takehiko Sasaki
Masakazu Yamazaki
author_sort Tomonori Ayukawa
title Dachsous-Dependent Asymmetric Localization of Spiny-Legs Determines Planar Cell Polarity Orientation in Drosophila
title_short Dachsous-Dependent Asymmetric Localization of Spiny-Legs Determines Planar Cell Polarity Orientation in Drosophila
title_full Dachsous-Dependent Asymmetric Localization of Spiny-Legs Determines Planar Cell Polarity Orientation in Drosophila
title_fullStr Dachsous-Dependent Asymmetric Localization of Spiny-Legs Determines Planar Cell Polarity Orientation in Drosophila
title_full_unstemmed Dachsous-Dependent Asymmetric Localization of Spiny-Legs Determines Planar Cell Polarity Orientation in Drosophila
title_sort dachsous-dependent asymmetric localization of spiny-legs determines planar cell polarity orientation in drosophila
publisher Elsevier
series Cell Reports
issn 2211-1247
publishDate 2014-07-01
description In Drosophila, planar cell polarity (PCP) molecules such as Dachsous (Ds) may function as global directional cues directing the asymmetrical localization of PCP core proteins such as Frizzled (Fz). However, the relationship between Ds asymmetry and Fz localization in the eye is opposite to that in the wing, thereby causing controversy regarding how these two systems are connected. Here, we show that this relationship is determined by the ratio of two Prickle (Pk) isoforms, Pk and Spiny-legs (Sple). Pk and Sple form different complexes with distinct subcellular localizations. When the amount of Sple is increased in the wing, Sple induces a reversal of PCP using the Ds-Ft system. A mathematical model demonstrates that Sple is the key regulator connecting Ds and the core proteins. Our model explains the previously noted discrepancies in terms of the differing relative amounts of Sple in the eye and wing.
url http://www.sciencedirect.com/science/article/pii/S221112471400477X
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