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Dev Cell. 2019 Nov 18;51(4):526-542.e6. doi: 10.1016/j.devcel.2019.10.022.

Dynamic Polarization of the Multiciliated Planarian Epidermis between Body Plan Landmarks.

Author information

1
Max Planck Institute for Molecular Cell Biology and Genetics, Pfotenhauerstrasse 108, 01307 Dresden, Germany.
2
Technische Universität Dresden, Zentrum für Informationsdienste und Hochleistungsrechnen (ZIH), Helmholtzstrasse 10, 01069 Dresden, Germany.
3
Institut Jacques Monod, Bâtiment Buffon, 15 rue Hélène Brion, 75205 Paris CEDEX 13, France.
4
Max Planck Institute for Molecular Cell Biology and Genetics, Pfotenhauerstrasse 108, 01307 Dresden, Germany; Center for Systems Biology Dresden, Pfotenhauerstrasse 108, 01307 Dresden, Germany.
5
Technische Universität Dresden, Zentrum für Informationsdienste und Hochleistungsrechnen (ZIH), Helmholtzstrasse 10, 01069 Dresden, Germany. Electronic address: lutz.brusch@tu-dresden.de.
6
Max Planck Institute for Molecular Cell Biology and Genetics, Pfotenhauerstrasse 108, 01307 Dresden, Germany; Max Planck Institute for Biophysical Chemistry, Am Fassberg 11, 37077 Göttingen, Germany. Electronic address: rink@mpi-cbg.de.

Abstract

Polarity is a universal design principle of biological systems that manifests at all organizational scales, yet its coordination across scales remains poorly understood. Here, we make use of the extreme anatomical plasticity of planarian flatworms to probe the interplay between global body plan polarity and local cell polarity. Our quantitative analysis of ciliary rootlet orientation in the epidermis reveals a dynamic polarity field with head and tail as independent determinants of anteroposterior (A/P) polarization and the body margin as determinant of mediolateral (M/L) polarization. Mathematical modeling rationalizes the global polarity field and its response to experimental manipulations as superposition of separate A/P and M/L fields, and we identify the core PCP and Ft/Ds pathways as their molecular mediators. Overall, our study establishes a framework for the alignment of cellular polarity vectors relative to planarian body plan landmarks and establishes the core PCP and Ft/Ds pathways as evolutionarily conserved 2D-polarization module.

KEYWORDS:

Fat/Dachsous; ciliary rootlet; core PCP; mathematical modeling; multi-ciliated cells; planar cell polarity; planaria

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