Abstract
Epithelia are bound by both basal and apical extracellular matrices (ECM). Although the composition and function of the former have been intensively investigated, less is known about the latter. The embryonic sheath, the ECM apical to the Caenorhabditis elegans embryonic epidermis, has been suggested to promote elongation of the embryo. In an RNAi screen for the components of the sheath, we identified the zona pellucida domain proteins NOAH-1 and NOAH-2. We found that these proteins act in the same pathway, and in parallel to three other putative sheath proteins, the leucine-rich repeat proteins SYM-1, LET-4 and FBN-1/Fibrillin, to ensure embryonic integrity and promote elongation. Laser nano-ablation experiments to map the stress field show that NOAH-1 and NOAH-2, together with PAK-1/p21-activated kinase, maintain and relay the actomyosin-dependent stress generated within the lateral epidermis before muscles become active. Subsequently, loss-of-function experiments show that apical ECM proteins are essential for muscle anchoring and for relaying the mechanical input from muscle contractions, which are essential for elongation. Hence, the apical ECM contributes to morphogenesis by maintaining embryonic integrity and relaying mechanical stress.
Highlights
The extracellular matrix (ECM) is a specialized structure providing mechanical support for tissue assembly and organ shape
We identified potential embryonic sheath (ES) proteins based on two assumptions: they should be essential for embryonic integrity during elongation; they are secreted or transmembraneous
We found that the stress in wild-type, noah2(RNAi), and pak-1(ok448) embryos was higher in the DV direction compared to the AP direction, whereas it was nearly isotropic in pak-1(ok448); noah-2(RNAi) embryos (Fig. 8C-D)
Summary
The extracellular matrix (ECM) is a specialized structure providing mechanical support for tissue assembly and organ shape. It is mainly constituted of secreted or transmembrane fibrous proteins and polysaccharides, forming an organized meshwork closely associated with the cell membrane (Alberts, 2014). The role of the basal ECM has been widely explored, whereas less is known about the apical ECM (aECM) (Labouesse, 2012; Alberts, 2014). As for the basal ECM, aECM components mediate numerous functions, since they have been linked to fertility, hearing, renal and vascular diseases, cancers and morphogenesis (Jovine et al, 2005; Plaza et al, 2010).
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