title: Drosophila E-cadherin is required for the maintenance of ring canals anchoring to mechanically withstand tissue growth.
abstract: Intercellular bridges called "ring canals" (RCs) resulting from incomplete cytokinesis play an essential role in intercellular communication in somatic and germinal tissues. During Drosophila oogenesis, RCs connect the maturing oocyte to nurse cells supporting its growth. Despite numerous genetic screens aimed at identifying genes involved in RC biogenesis and maturation, how RCs anchor to the plasma membrane (PM) throughout development remains unexplained. In this study, we report that the clathrin adaptor protein 1 (AP-1) complex, although dispensable for the biogenesis of RCs, is required for the maintenance of the anchorage of RCs to the PM to withstand the increased membrane tension associated with the exponential tissue growth at the onset of vitellogenesis. Here we unravel the mechanisms by which AP-1 enables the maintenance of RCs' anchoring to the PM during size expansion. We show that AP-1 regulates the localization of the intercellular adhesion molecule E-cadherin and that loss of AP-1 causes the disappearance of the E-cadherin-containing adhesive clusters surrounding the RCs. E-cadherin itself is shown to be required for the maintenance of the RCs' anchorage, a function previously unrecognized because of functional compensation by N-cadherin. Scanning block-face EM combined with transmission EM analyses reveals the presence of interdigitated, actin- and Moesin-positive, microvilli-like structures wrapping the RCs. Thus, by modulating E-cadherin trafficking, we show that the sustained E-cadherin-dependent adhesion organizes the microvilli meshwork and ensures the proper attachment of RCs to the PM, thereby counteracting the increasing membrane tension induced by exponential tissue growth.
authors.affiliation: CNRS, UMR 6290, F-35000 Rennes, France; Institut de Génétique et Développement de Rennes, Université Rennes 1, F-35000 Rennes, France; Equipe Labellisée Ligue Nationale Contre le Cancer, F-35000 Rennes, France;
authors.forename: Nicolas
authors.initials: N
authors.lastname: Loyer
authors.affiliation: CNRS, UMR 6290, F-35000 Rennes, France; Institut de Génétique et Développement de Rennes, Université Rennes 1, F-35000 Rennes, France; Equipe Labellisée Ligue Nationale Contre le Cancer, F-35000 Rennes, France; CNRS, Structure Fédérative de Recherche BIOSIT, Microscopy Rennes Imaging Center-Electron Microscopy Facility, F-35000 Rennes, France.
authors.forename: Irina
authors.initials: I
authors.lastname: Kolotuev
authors.affiliation: CNRS, UMR 6290, F-35000 Rennes, France; Institut de Génétique et Développement de Rennes, Université Rennes 1, F-35000 Rennes, France; Equipe Labellisée Ligue Nationale Contre le Cancer, F-35000 Rennes, France;
authors.forename: Mathieu
authors.initials: M
authors.lastname: Pinot
authors.affiliation: CNRS, UMR 6290, F-35000 Rennes, France; Institut de Génétique et Développement de Rennes, Université Rennes 1, F-35000 Rennes, France; Equipe Labellisée Ligue Nationale Contre le Cancer, F-35000 Rennes, France; roland.leborgne@univ-rennes1.fr.
authors.forename: Roland
authors.initials: R
authors.lastname: Le Borgne
mesh_terms: D033961:Adaptor Protein Complex 1 / Q000235:genetics / Q000378:metabolism; D000818:Animals; D015820:Cadherins / Q000235:genetics / Q000378:metabolism*; D002462:Cell Membrane / Q000235:genetics / Q000378:metabolism*; D029721:Drosophila Proteins / Q000235:genetics / Q000378:metabolism*; D004331:Drosophila melanogaster; D005260:Female; D009866:Oogenesis / Q000502:physiology*
chemical_list: D033961:Adaptor Protein Complex 1; D015820:Cadherins; D029721:Drosophila Proteins
keywords: E-cadherin; membrane tension; ring canals; tissue growth; trafficking