A transient apical extracellular matrix relays cytoskeletal patterns to shape permanent acellular ridges on the surface of adult C. elegans

Abstract

Epithelial cells secrete apical extracellular matrices to form protruding structures such as denticles, ridges, scales, or teeth. The mechanisms that shape these structures remain poorly understood. Here, we show how the actin cytoskeleton and a provisional matrix work together to sculpt acellular longitudinal alae ridges in the cuticle of adult C. elegans. Transient assembly of longitudinal actomyosin filaments in the underlying lateral epidermis accompanies deposition of the provisional matrix at the earliest stages of alae formation. Actin is required to pattern the provisional matrix into longitudinal bands that are initially offset from the pattern of longitudinal actin filaments. These bands appear ultrastructurally as alternating regions of adhesion and separation within laminated provisional matrix layers. The provisional matrix is required to establish these demarcated zones of adhesion and separation, which ultimately give rise to alae ridges and their intervening valleys, respectively. Provisional matrix proteins shape the alae ridges and valleys but are not present within the final structure. We propose a morphogenetic mechanism wherein cortical actin patterns are relayed to the laminated provisional matrix to set up distinct zones of matrix layer separation and accretion that shape a permanent and acellular matrix structure.

Meisosomes, folded membrane platforms, link the epidermis to the cuticle inC. elegans

“…Some are involved in the formation of distinct structures, including the circumferential parallel furrows that cover the entire animal (Cox & Hirsh, 1985; Cox et al, 1980; McMahon et al, 2003; Page & Johnstone, 2007; Thein et al, 2003), and the longitudinal lateral alae. The latter have been proposed to be involved in facilitating the traction of C. elegans to its substrate during locomotion, although, notably they are not present from the L2 through the L4 larval stages (Cox et al, 1981; Katz et al, 2022).…”

A sex-specific switch in a single glial cell patterns the apical extracellular matrix

“…We further determined that these sfGFP-GRL-18 rings are transient, forming adjacent to glial endings at the onset of the L4/adult molt and disassembling within ∼1-4 hours as the newly synthesized cuticle is complete and shedding of the old cuticle begins (Figure 4C and Figure S4). The transient localization of GRL-18 is reminiscent of the provisional matrix formed by other C. elegans aECM components during molts to pattern the newly synthesized cuticle (Katz et al, 2022). Provisional matrix components are thought to provide a temporary structural template or scaffold that is critical for patterning newly synthesized aECM, but they are not stably incorporated into the mature structure (Cohen et al, 2020; Gill et al, 2016; Katz et al, 2022; Öztürk-Çolak et al, 2016a).…”

“…The transient localization of GRL-18 is reminiscent of the provisional matrix formed by other C. elegans aECM components during molts to pattern the newly synthesized cuticle (Katz et al, 2022). Provisional matrix components are thought to provide a temporary structural template or scaffold that is critical for patterning newly synthesized aECM, but they are not stably incorporated into the mature structure (Cohen et al, 2020; Gill et al, 2016; Katz et al, 2022; Öztürk-Çolak et al, 2016a). Together, our results suggest that GRL-18 is a novel aECM component that localizes to transient rings at sites where cuticle pores will form (Figure 4D).…”

“…For example, in Drosophila, epidermal cells and olfactory hair cells form tooth-like denticles and peg-like extensions, respectively, that act as molds to sculpt newly secreted matrix proteins, and then retract as the aECM solidifies (Ando et al, 2019; Fernandes et al, 2010). Actin networks also shape aECM pattern through contraction of the cell surface and localized secretion, as in alae of the C. elegans cuticle and taenidia of the Drosophila trachea (Katz et al, 2022; Öztürk-Çolak et al, 2016b). Finally, cellular movements apply mechanical forces that can stretch or fold the aECM during tube morphogenesis (Dong and Hayashi, 2015; Gill et al, 2016).…”

Pathways that affect anterior morphogenesis inC. elegansembryos

“…Moreover, misregulation of fbn-1 is a key factor in causing the Pin phenotype of mec-8; sym double mutants (Kelley et al, 2015). FBN-1 functions as a structural component of the embryonic sheath-a specialized embryonic pre-cuticle-and in the larval cuticle, in which it is required for normal molting (Cohen et al, 2020b;Frand et al, 2005;Katz et al, 2022;. Both the sheath and cuticle are a category of apical extracellular matrix (aECM) that is secreted in large part by the epidermis (Page and Johnstone, 2007).…”