The Invading Anchor Cell Induces Lateral Membrane Constriction during Vulval Lumen Morphogenesis in C. elegans

Abstract

During epithelial tube morphogenesis, linear arrays of cells are converted into tubular structures through actomyosin-generated intracellular forces that induce tissue invagination and lumen formation. We have investigated lumen morphogenesis in the C. elegans vulva. The first discernible event initiating lumen formation is the apical constriction of the two innermost primary cells (VulF). The VulF cells thereafter constrict their lateral membranes along the apicobasal axis to extend the lumen dorsally. Lateral, but not apical, VulF constriction requires the prior invasion of the anchor cell (AC). The invading AC extends actin-rich protrusions toward VulF, resulting in the formation of a direct AC-VulF interface. The recruitment of the F-BAR-domain protein TOCA-1 to the AC-VulF interface induces the accumulation of force-generating actomyosin, causing a switch from apical to lateral membrane constriction and the dorsal extension of the lumen. Invasive cells may induce shape changes in adjacent cells to penetrate their target tissues.

A multi-layered and dynamic apical extracellular matrix shapes the vulva lumen inCaenorhabditis elegans

“…Apical matrix may generate, counteract and distribute multiple forces during lumen shaping Prior work showed that the vulva is expanded by a combination of pushing forces by chondroitin GAGs and actin-myosin constriction by 2˚ cells, which may then focus the GAG-dependent forces dorsally (Yang, Roiz, Mereu, Daube, & Hajnal, 2017). The data here suggest that GAGs not only inflate the lumen, but also play other roles.…”

A multi-layered and dynamic apical extracellular matrix shapes the vulva lumen in Caenorhabditis elegans

“…Prior work showed that the vulva is expanded by a combination of pushing forces by chondroitin GAGs ( Hwang et al, 2003a ) and actin-myosin constriction by 2° cells, which may then focus the GAG-dependent forces dorsally ( Yang et al, 2017a ). The data here suggest that GAGs not only inflate the lumen, but also play other roles.…”

C. elegans Apical Extracellular Matrices Shape Epithelia

“…It is comprised of twenty-two cells of seven different types derived from either Ras-dependent (primary) or Notch-dependent (secondary) vulva precursor cells [76] ( Figure 3F). During L4 stage, the vulva first expands dramatically from a simple invagination to a large lumen via the action of chondroitin glycosaminoglycans and actin-myosin constriction [77][78][79][80][81][82]. Next, the vulva tube is shaped into a narrow, slit-like channel via further cell shape changes, rearrangements, and the action of its pre-cuticular aECM ( Figure 3G) [48,83].…”