Game of Tissues: How the Epidermis Thrones C. elegans Shape

Abstract

The versatility of epithelial cell structure is universally exploited by organisms in multiple contexts. Epithelial cells can establish diverse polarized axes within their tridimensional structure which enables them to flexibly communicate with their neighbors in a 360° range. Hence, these cells are central to multicellularity, and participate in diverse biological processes such as organismal development, growth or immune response and their misfunction ultimately impacts disease. During the development of an organism, the first task epidermal cells must complete is the formation of a continuous sheet, which initiates its own morphogenic process. In this review, we will focus on the C. elegans embryonic epithelial morphogenesis. We will describe how its formation, maturation, and spatial arrangements set the final shape of the nematode C. elegans. Special importance will be given to the tissue-tissue interactions, regulatory tissue-tissue feedback mechanisms and the players orchestrating the process.

A genetic screen for temperature-sensitive morphogenesis-defective Caenorhabditis elegans mutants

“…The body plan of C. elegans is relatively simple, and elongation of the initially ovoid embryo into a vermiform larva is driven largely by epidermal cell morphogenesis. This elongation comprises three epidermal cell morphogenetic events: dorsal intercalation, ventral enclosure, and seam cell elongation ( Sulston et al 1983 ; Priess and Hirsh 1986 ; Chin-Sang and Chisholm 2000 ; Simske and Hardin 2001 ; Chisholm and Hardin 2005 ; Hall and Altun 2008 ; Carvalho and Broday 2020 ).…”

“…Enclosure completes when the pocket cells meet and fuse at the ventral midline, likely by a “purse-string” mechanism utilizing an actomyosin cable similar to Drosophila dorsal closure ( Williams-Masson et al 1997 ; Gilbert et al 2020 ). The movement of the ventral epidermal cells also requires the underlying neuroblasts; loss of the ephrin receptor VAB-1 in neuroblasts results in the lack of neuroblast ventral cleft closure and the subsequent nonautonomous halting of epidermal leading cell migration ( George et al 1998 ; Chin-Sang et al 1999 ; Carvalho and Broday 2020 ).…”

A Genetic Screen for Temperature-sensitive Morphogenesis-defectiveCaenorhabditis elegansMutants

“…The body plan of C. elegans is relatively simple, and elongation of the initially ovoid embryo into a vermiform larva is driven largely by epidermal cell morphogenesis. This elongation comprises three epidermal cell morphogenetic events: dorsal intercalation, ventral enclosure, and seam cell elongation (Carvalho and Broday, 2020;Chin-Sang and Chisholm, 2000;Chisholm and Ventral enclosure begins as dorsal intercalation ends and serves to cover the posterior ventral surface of the embryo with a layer of epidermal cells. In the first step, two pairs of leading cells, V0 and V18 on the left side and V1 and V19 on the right side ( Figure 1A), extend actin-rich filopodia towards the ventral midline until they meet and form stable adherens junctions.…”

“…The movement of the ventral epidermal cells also requires the underlying neuroblasts; loss of the ephrin receptor VAB-1 in neuroblasts results in the lack of neuroblast ventral cleft closure and the subsequent non-autonomous halting of epidermal leading cell migration (Carvalho and Broday, 2020;Chin-Sang et al, 1999;George et al, 1998).…”

“…Elongation is divided into two stages. The second stage, which we will not discuss at length here, requires muscle twitching to elongate the embryo from 2-fold to 4-fold (Carvalho and Broday, 2020;Chisholm and Hardin, 2005). The first stage, however, is driven largely by epidermal seam cell shape changes that elongate the embryo from the bean stage to 2-fold in length.…”