Apical and Basal Matrix Remodeling Control Epithelial Morphogenesis

• Published in: Developmental cell Vol. 46; no. 1; pp. 23 - 39.e5
• Main Authors: Diaz-de-la-Loza, Maria-del-Carmen, Ray, Robert P., Ganguly, Poulami S., Alt, Silvanus, Davis, John R., Hoppe, Andreas, Tapon, Nic, Salbreux, Guillaume, Thompson, Barry J.
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 02.07.2018; Cell Press
• Subjects: Animals; Body Patterning - physiology; Cell Polarity - physiology; Cell Shape - physiology; Drosophila; Drosophila melanogaster - cytology; Drosophila melanogaster - embryology; Drosophila Proteins - metabolism; Embryo, Nonmammalian - embryology; epithelia; Epithelial Cells - cytology; Epithelium - metabolism; extracellular matrix; Lower Extremity - embryology; Matrix Metalloproteinase 1 - metabolism; Matrix Metalloproteinase 2 - metabolism; Membrane Proteins - metabolism; morphogenesis; Morphogenesis - physiology; Myosin Type II - metabolism; Serine Endopeptidases - metabolism; Wings, Animal - embryology; morphogenesis; epithelia; Drosophila; extracellular matrix
• ISSN: 1534-5807; 1878-1551
• DOI: 10.1016/j.devcel.2018.06.006

Epithelial tissues can elongate in two dimensions by polarized cell intercalation, oriented cell division, or cell shape change, owing to local or global actomyosin contractile forces acting in the plane of the tissue. In addition, epithelia can undergo morphogenetic change in three dimensions. We show that elongation of the wings and legs of Drosophila involves a columnar-to-cuboidal cell shape change that reduces cell height and expands cell width. Remodeling of the apical extracellular matrix by the Stubble protease and basal matrix by MMP1/2 proteases induces wing and leg elongation. Matrix remodeling does not occur in the haltere, a limb that fails to elongate. Limb elongation is made anisotropic by planar polarized Myosin-II, which drives convergent extension along the proximal-distal axis. Subsequently, Myosin-II relocalizes to lateral membranes to accelerate columnar-to-cuboidal transition and isotropic tissue expansion. Thus, matrix remodeling induces dynamic changes in actomyosin contractility to drive epithelial morphogenesis in three dimensions. [Display omitted] •Apical and basal extracellular matrices are degraded to elongate Drosophila limbs•Apical matrix is degraded by the Stubble protease and basal matrix by MMPs•Limbs elongate via convergent extension and cell flattening, driven by Myosin-II•In the haltere, Ultrabithorax prevents matrix remodeling and tissue elongation Diaz-de-la-Loza et al. show that morphogenetic elongation of Drosophila limbs occurs via both convergent extension and columnar-to-cuboidal cell shape change. These processes are spatially organized by Myosin-II and temporally organized by remodeling of the extracellular matrix, including both apical (ZP-domain-containing) and basal (Collagen IV/Laminin/Perlecan-containing) matrices.