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Force Transmission between Three Tissues Controls Bipolar Planar Polarity Establishment and Morphogenesis

Title: Force Transmission between Three Tissues Controls Bipolar Planar Polarity Establishment and Morphogenesis
Authors: Gillard, Ghislain; Nicolle, Ophélie; Brugière, Thibault; Prigent, Sylvain; Pinot, Mathieu; Michaux, Grégoire
Contributors: Institut de Génétique et Développement de Rennes (IGDR); Université de Rennes (UR)-Centre National de la Recherche Scientifique (CNRS)-Structure Fédérative de Recherche en Biologie et Santé de Rennes (Biosit : Biologie - Santé - Innovation Technologique); Biosit : biologie, santé, innovation technologique (SFR UMS CNRS 3480 - INSERM 018); Université de Rennes (UR)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Structure Fédérative de Recherche en Biologie et Santé de Rennes (Biosit : Biologie - Santé - Innovation Technologique); Plateforme Génomique Santé Biogenouest®
Source: ISSN: 0960-9822.
Publisher Information: HAL CCSD; Elsevier
Publication Year: 2019
Collection: Université de Rennes 1: Publications scientifiques (HAL)
Subject Terms: signaling; C. elegans; mechanotransduction; morphogenesis; planar polarity; [SDV]Life Sciences [q-bio]
Description: International audience ; How tissues from different developmental origins interact to achieve coordinated morphogenesis at the level of a whole organism is a fundamental question in developmental biology. While biochemical signaling pathways controlling morphogenesis have been extensively studied [1-3], morphogenesis of epithelial tissues can also be directed by mechanotransduction pathways physically linking two tissues [4-8]. C. elegans embryonic elongation requires the coordination of three tissues muscles, the dorsal and ventral epidermis, and the lateral epidermis. Elongation starts by cell-shape changes driven by actomyosin contractions in the lateral epidermis [9, 10]. At mid-elongation, muscles become connected to the apical surface of the dorsal and ventral epidermis by molecular tendons formed by muscle integrins, extracellular matrix, and C. elegans hemidesmosomes (CeHDs). The mechanical signal generated by the onset of muscle contractions in the antero-posterior axis from mid-elongation is translated into a biochemical pathway controlling the maturation of CeHDs in the dorsal and ventral epidermis [11]. Consistently, mutations affecting muscle contractions or molecular tendons lead to a mid-elongation arrest [12]. Here, we found that the mechanical force generated by muscle contractions and relayed by molecular tendons is transmitted by adherens junctions to lateral epidermal cells, where it establishes a newly identified bipolar planar polarity of the apical PAR module. The planar polarized PAR module is then required for actin planar organization, thus contributing to the determination of the orientation of cell-shape changes and the elongation axis of the whole embryo. This mechanotransduction pathway is therefore essential to coordinate the morphogenesis of three embryonic tissues.
Document Type: article in journal/newspaper
Language: English
Relation: info:eu-repo/semantics/altIdentifier/pmid/30930039; PUBMED: 30930039
DOI: 10.1016/j.cub.2019.02.059
Availability: https://univ-rennes.hal.science/hal-02119227; https://univ-rennes.hal.science/hal-02119227v1/document; https://univ-rennes.hal.science/hal-02119227v1/file/Gillard-2019-Force%20Transmission%20between%20Three%20Tissues-final.pdf; https://doi.org/10.1016/j.cub.2019.02.059
Rights: info:eu-repo/semantics/OpenAccess
Accession Number: edsbas.F10A4819
Database: BASE