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

Tomonori Ayukawa; Masakazu Akiyama; Jennifer L. Mummery-Widmer; Thomas Stoeger; Junko Sasaki; Juergen A. Knoblich; Haruki Senoo; Takehiko Sasaki; Masakazu Yamazaki

doi:10.1016/j.celrep.2014.06.009

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

Tomonori Ayukawa, Masakazu Akiyama, Jennifer L. Mummery-Widmer, Thomas Stoeger, Junko Sasaki, Juergen A. Knoblich, Haruki Senoo, Takehiko Sasaki, Masakazu Yamazaki^*

^*Corresponding author for this work

Medicine, Pulmonary Division

Research output: Contribution to journal › Article › peer-review

54 Scopus citations

Abstract

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.

Original language	English (US)
Pages (from-to)	610-621
Number of pages	12
Journal	Cell reports
Volume	8
Issue number	2
DOIs	https://doi.org/10.1016/j.celrep.2014.06.009
State	Published - Jul 24 2014

Funding

We thank D. Gubb, P. Adler, K. Irvine, D. Strutt, T. Uemura, F. Wirtz-Peitz, the Kyoto Stock Center, the Vienna Drosophila RNAi Center, the Bloomington Drosophila Stock Center, Drosophila Genomics Resource Center, Transgenic RNAi Project (TRiP), Developmental Studies of Hybridoma Bank (DSHB), and Addgene for fly stocks, antibodies, and plasmids and N. Odaka, M. Suzuki, and A. Kato for technical assistance. We thank Jeffrey D. Axelrod for communicating results before publication. This work was supported by Grant-in-Aid for Scientific Research on Innovative Areas from the Ministry of Education, Culture, Sports and Technology of Japan (MEXT); the Japan Society for the Promotion of Science (JSPS); Takeda Science Foundation; and The Uehara Memorial Foundation (to M.Y.). T.A. is supported by MEXT. Work in J.A.K.’s lab is supported by the Austrian Academy of Sciences, the Austrian Science Fund (FWF; grants I_552-B19 and Z_153_B09), and an advanced grant of the European Research Council (ERC). T. Sasaki is supported by MEXT, JSPS, and the Takeda Science Foundation and NEXT program. T. Sasaki and M.Y. were supported by the Global COE Program of MEXT.

ASJC Scopus subject areas

General Biochemistry, Genetics and Molecular Biology

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10.1016/j.celrep.2014.06.009

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title = "Dachsous-Dependent Asymmetric Localization of Spiny-Legs Determines Planar Cell Polarity Orientation in Drosophila",

abstract = "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.",

author = "Tomonori Ayukawa and Masakazu Akiyama and Mummery-Widmer, \{Jennifer L.\} and Thomas Stoeger and Junko Sasaki and Knoblich, \{Juergen A.\} and Haruki Senoo and Takehiko Sasaki and Masakazu Yamazaki",

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AU - Ayukawa, Tomonori

AU - Akiyama, Masakazu

AU - Mummery-Widmer, Jennifer L.

AU - Stoeger, Thomas

AU - Sasaki, Junko

AU - Knoblich, Juergen A.

AU - Senoo, Haruki

AU - Sasaki, Takehiko

AU - Yamazaki, Masakazu

PY - 2014/7/24

Y1 - 2014/7/24

N2 - 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.

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

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