title: Patterned Contractile Forces Promote Epidermal Spreading and Regulate Segment Positioning during Drosophila Head Involution.
abstract: Epithelial spreading is a fundamental mode of tissue rearrangement occurring during animal development and wound closure. It has been associated either with the collective migration of cells [1, 2] or with actomyosin-generated forces acting at the leading edge (LE) and pulling the epithelial tissue [3, 4]. During the process of Drosophila head involution (HI), the epidermis spreads anteriorly to envelope the head tissues and fully cover the embryo [5]. This results in epidermal segments of equal width that will give rise to the different organs of the fly [6]. Here we perform a quantitative analysis of tissue spreading during HI. Combining high-resolution live microscopy with laser microsurgery and genetic perturbations, we show that epidermal movement is in part, but not solely, driven by a contractile actomyosin cable at the LE. Additional driving forces are generated within each segment by a gradient of actomyosin-based circumferential tension. Interfering with Hedgehog (Hh) signaling can modulate this gradient, thus suggesting the involvement of polarity genes in the regulation of HI. In particular, we show that disruption of these contractile forces alters segment widths and leads to a mispositioning of segments. Within the framework of a physical description, we confirm that given the geometry of the embryo, a patterned profile of active circumferential tensions can indeed generate propelling forces and control final segment position. Our study thus unravels a mechanism by which patterned tensile forces can regulate spreading and positioning of epithelial tissues.
authors.affiliation: Cell and Developmental Biology Programme, Centre for Genomic Regulation (CRG), The Barcelona Institute of Science and Technology, Doctor Aiguader 88, Barcelona 08003, Spain; Universitat Pompeu Fabra (UPF), Barcelona 08003, Spain.
authors.forename: Natalia Dorota
authors.initials: ND
authors.lastname: Czerniak
authors.affiliation: Cell and Developmental Biology Programme, Centre for Genomic Regulation (CRG), The Barcelona Institute of Science and Technology, Doctor Aiguader 88, Barcelona 08003, Spain; Universitat Pompeu Fabra (UPF), Barcelona 08003, Spain.
authors.forename: Kai
authors.initials: K
authors.lastname: Dierkes
authors.affiliation: Cell and Developmental Biology Programme, Centre for Genomic Regulation (CRG), The Barcelona Institute of Science and Technology, Doctor Aiguader 88, Barcelona 08003, Spain; Universitat Pompeu Fabra (UPF), Barcelona 08003, Spain.
authors.forename: Arturo
authors.initials: A
authors.lastname: D'Angelo
authors.affiliation: Institute for Research in Biomedicine (IRB Barcelona), The Barcelona Institute of Science and Technology, Carrer Baldiri Reixac 10, Barcelona 08028, Spain.
authors.forename: Julien
authors.initials: J
authors.lastname: Colombelli
authors.affiliation: Cell and Developmental Biology Programme, Centre for Genomic Regulation (CRG), The Barcelona Institute of Science and Technology, Doctor Aiguader 88, Barcelona 08003, Spain; Universitat Pompeu Fabra (UPF), Barcelona 08003, Spain. Electronic address: jerome.solon@crg.es.
authors.forename: Jérôme
authors.initials: J
authors.lastname: Solon
mesh_terms: D000818:Animals; D019521:Body Patterning; D004330:Drosophila / Q000196:embryology*; D047108:Embryonic Development; D004817:Epidermis / Q000196:embryology; D004847:Epithelial Cells / Q000166:cytology