Positioning of centrioles is a conserved readout of Frizzled planar cell polarity signalling

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Abstract

Planar cell polarity (PCP) signalling is a well-conserved developmental pathway regulating cellular orientation during development. An evolutionarily conserved pathway readout is not established and, moreover, it is thought that PCP mediated cellular responses are tissue-specific. A key PCP function in vertebrates is to regulate coordinated centriole/cilia positioning, a function that has not been associated with PCP in Drosophila. Here we report instructive input of Frizzled-PCP (Fz/PCP) signalling into polarized centriole positioning in Drosophila wings. We show that centrioles are polarized in pupal wing cells as a readout of PCP signalling, with both gain and loss-of-function Fz/PCP signalling affecting centriole polarization. Importantly, loss or gain of centrioles does not affect Fz/PCP establishment, implicating centriolar positioning as a conserved PCP-readout, likely downstream of PCP-regulated actin polymerization. Together with vertebrate data, these results suggest a unifying model of centriole/cilia positioning as a common downstream effect of PCP signalling from flies to mammals.

Abstract

Planar cell polarity (PCP) contributes to cellular orientation during development but how this is regulated in Drosophila is unclear. Here, the authors identify Frizzled-PCP signalling as regulating polarised centriole positioning in the wing disc.

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Most cited references 53

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Randomization of left-right asymmetry due to loss of nodal cilia generating leftward flow of extraembryonic fluid in mice lacking KIF3B motor protein.

Shigenori Nonaka, Yosuke Tanaka, Yasushi Okada … (1998)

Microtubule-dependent motor, murine KIF3B, was disrupted by gene targeting. The null mutants did not survive beyond midgestation, exhibiting growth retardation, pericardial sac ballooning, and neural tube disorganization. Prominently, the left-right asymmetry was randomized in the heart loop and the direction of embryonic turning. lefty-2 expression was either bilateral or absent. Furthermore, the node lacked monocilia while the basal bodies were present. Immunocytochemistry revealed KIF3B localization in wild-type nodal cilia. Video microscopy showed that these cilia were motile and generated a leftward flow. These data suggest that KIF3B is essential for the left-right determination through intraciliary transportation of materials for ciliogenesis of motile primary cilia that could produce a gradient of putative morphogen along the left-right axis in the node.

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The ciliopathies: an emerging class of human genetic disorders.

Jose L Badano, Norimasa Mitsuma, Phil Beales … (2006)

Cilia and flagella are ancient, evolutionarily conserved organelles that project from cell surfaces to perform diverse biological roles, including whole-cell locomotion; movement of fluid; chemo-, mechano-, and photosensation; and sexual reproduction. Consistent with their stringent evolutionary conservation, defects in cilia are associated with a range of human diseases, such as primary ciliary dyskinesia, hydrocephalus, polycystic liver and kidney disease, and some forms of retinal degeneration. Recent evidence indicates that ciliary defects can lead to a broader set of developmental and adult phenotypes, with mutations in ciliary proteins now associated with nephronophthisis, Bardet-Biedl syndrome, Alstrom syndrome, and Meckel-Gruber syndrome. The molecular data linking seemingly unrelated clinical entities are beginning to highlight a common theme, where defects in ciliary structure and function can lead to a predictable phenotypic pattern that has potentially predictive and therapeutic value.

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Cell flow reorients the axis of planar polarity in the wing epithelium of Drosophila.

Benoît Aigouy, Reza Farhadifar, Douglas B Staple … (2010)

Planar cell polarity (PCP) proteins form polarized cortical domains that govern polarity of external structures such as hairs and cilia in both vertebrate and invertebrate epithelia. The mechanisms that globally orient planar polarity are not understood, and are investigated here in the Drosophila wing using a combination of experiment and theory. Planar polarity arises during growth and PCP domains are initially oriented toward the well-characterized organizer regions that control growth and patterning. At pupal stages, the wing hinge contracts, subjecting wing-blade epithelial cells to anisotropic tension in the proximal-distal axis. This results in precise patterns of oriented cell elongation, cell rearrangement and cell division that elongate the blade proximo-distally and realign planar polarity with the proximal-distal axis. Mutation of the atypical Cadherin Dachsous perturbs the global polarity pattern by altering epithelial dynamics. This mechanism utilizes the cellular movements that sculpt tissues to align planar polarity with tissue shape. Copyright 2010 Elsevier Inc. All rights reserved.

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Author and article information

Journal

Journal ID (nlm-ta): Nat Commun

Journal ID (iso-abbrev): Nat Commun

Title: Nature Communications

Publisher: Nature Publishing Group

ISSN (Electronic): 2041-1723

Publication date (Electronic): 29 March 2016

Publication date Collection: 2016

Volume: 7

Electronic Location Identifier: 11135

Affiliations

[1 ]Department of Developmental & Regenerative Biology, Tisch Cancer Institute, and Graduate School of Biomedical Sciences, Icahn School of Medicine at Mount Sinai , One Gustave L. Levy Place, New York, New York 10029, USA

[2 ]Champalimaud Neuroscience Programme , Avenida de Brasilia, Lisbon 1400-038, Portugal

Author notes

[a ] jmcarvaj@ 123456unex.es

[b ] marek.mlodzik@ 123456mssm.edu

[*]

Present address: Departamento de Bioquímica y Biología Molecular, Facultad de Ciencias, Universidad de Extremadura, Badajoz 06071, Spain.

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Publisher Item ID: ncomms11135

DOI: 10.1038/ncomms11135

PMC ID: 4820615

PubMed ID: 27021213

SO-VID: 05e2ebab-7129-4dff-94cf-105718922b82

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Positioning of centrioles is a conserved readout of Frizzled planar cell polarity signalling

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Stress signalling in stem cells

Most cited references 53

Randomization of left-right asymmetry due to loss of nodal cilia generating leftward flow of extraembryonic fluid in mice lacking KIF3B motor protein.

The ciliopathies: an emerging class of human genetic disorders.

Cell flow reorients the axis of planar polarity in the wing epithelium of Drosophila.

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