Apical and Basal Matrix Remodeling Control Epithelial Morphogenesis

Abstract

SummaryEpithelial 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.

broadcontrols leg imaginal disc morphogenesis in Drosophila via regulation of cell shape changes and remodeling of extracellular matrix

“…Here we show that cell shape changes and cell rearrangements fail to occur normally in br 5 mutant prepupae. In addition, consistent with previous work demonstrating that the ECM provides a constraining force and must be degraded to allow disc elongation (Pastor-Pareja and Xu, 2011; Diaz-de-la-Loza et al ., 2018; Maria-del-Carmen et al ., 2018), we show that the basal ECM protein Collagen IV is not substantially degraded in leg imaginal discs from amorphic br 5 mutant animals as old as 8 hours after puparium formation (APF). In this study, we also use this allele to identify specific genes regulated by br in the leg discs at the onset of metamorphosis through an RNA sequencing-based approach.…”

“…In this study, we have demonstrated that Br is required for many of the tissue-level events required for leg morphogenesis during the first several hours of metamorphosis in Drosophila , and have identified a collection of genes regulated by br that may help explain this developmental process. Many previous studies have demonstrated that leg morphogenesis requires ecdysone signaling (Mandaron, 1971; Fristrom et al ., 1973), cell shape changes and rearrangements (Condic et al ., 1991), and proteolysis of the ECM (Diaz-de-la-Loza et al ., 2018). Here we show that leg discs in br 5 mutant animals fail to fully degrade their ECM (Fig.…”

“…Imaginal discs are diploid tissues found within the larva that give rise to the adult integument during metamorphosis (Willis, 1974; Csaba, 1977; Fristrom, 1988). Both classical experiments and more recent live imaging studies (De las Heras et al ., 2018; Diaz-de-la-Loza et al ., 2018) have revealed requirements for cell shape changes and rearrangements, as well as for remodeling of the extracellular matrix (ECM) in imaginal disc morphogenesis during metamorphosis. These experiments also demonstrate the key role that 20-hydroxyecdysone (hereafter referred to as ecdysone) plays in directing these processes.…”

Decoupling from yolk sac is required for extraembryonic tissue spreading in the scuttle fly Megaselia abdita

“…In D. melanogaster, modulation of tissue-tissue adhesion as well as complete tissue-tissue decoupling has been previously associated with Matrix metalloprotease 1 (Mmp1) activity (Diaz-de-la-Loza et al, 2018;Glasheen et al, 2010;LaFever et al, 2017;Srivastava et al, 2007). To test whether activity of this matrix metalloprotease was involved in mechanical decoupling of serosa and yolk sac, we cloned the M. abdita orthologue of Mmp1 (Mab-Mmp1) and found it expressed in yolk sac nuclei ( Figure 5A).…”

Optogenetic control of morphogenesis goes 3D

“…The basal surfaces of many different epithelia experience dynamic changes in locally generated actomyosin contractile forces (He et al , 2010; Sherrard et al , 2010; Sun et al , 2017; Huebner & Wallingford, 2018) as well as in the constraining force of the basal extracellular matrix (Haigo & Bilder, 2011; Diaz‐de‐la‐Loza et al , 2018). Thus, a full understanding of epithelial morphogenesis will require moving from 2D analysis of the apical surface towards 3D analysis of tissue mechanics at both the apical and basal surface of epithelia.…”