Epithelial Shaping by Diverse Apical Extracellular Matrices Requires the Nidogen Domain Protein DEX-1 in Caenorhabditis elegans

• Published in: Genetics (Austin) 2019-01, Vol.211 (1), p.185-200
• Main Authors: Cohen, Jennifer D, Flatt, Kristen M, Schroeder, Nathan E, Sundaram, Meera V
• Format: Article
• Language: English
• Subjects: Angiogenesis; Animals; Basement membranes; Caenorhabditis elegans; Caenorhabditis elegans - genetics; Caenorhabditis elegans - growth & development; Caenorhabditis elegans Proteins - genetics; Caenorhabditis elegans Proteins - metabolism; Cell Differentiation; Collagen; Defects; Dendrites; Embryos; Epidermal growth factor; Epithelial Cells - cytology; Epithelial Cells - metabolism; Excretory system; Extracellular matrix; Extracellular Matrix - metabolism; Fat body; Genes; Genetics; Glycoproteins; Glycosaminoglycans; Investigations; Larvae; Lipids; Loss of Function Mutation; Membranes; Morphogenesis; Mutants; Nematodes; Nose; Pharynx; Phenotypes; Proteins; Tissues; Tubes; Vascular system; Worms; Zona pellucida
• ISSN: 1943-2631; 0016-6731; 1943-2631
• DOI: 10.1534/genetics.118.301752

The body's external surfaces and the insides of biological tubes, like the vascular system, are lined by a lipid-, glycoprotein-, and glycosaminoglycan-rich apical extracellular matrix (aECM). aECMs are the body's first line of defense against infectious agents and promote tissue integrity and morphogenesis, but are poorly described relative to basement membranes and stromal ECMs. While some aECM components, such as zona pellucida (ZP) domain proteins, have been identified, little is known regarding the overall composition of the aECM or the mechanisms by which different aECM components work together to shape epithelial tissues. In , external epithelia develop in the context of an ill-defined ZP-containing aECM that precedes secretion of the collagenous cuticle. has 43 genes that encode at least 65 unique ZP proteins, and we show that some of these comprise distinct precuticle aECMs in the embryo. Previously, the nidogen- and EGF-domain protein DEX-1 was shown to anchor dendrites to the nose tip in concert with the ZP protein DYF-7 Here, we identified a new, strong loss-of-function allele of , mutants die as L1 larvae and have a variety of tissue distortion phenotypes, including excretory defects, pharyngeal ingression, alae defects, and a short and fat body shape, that strongly resemble those of genes encoding ZP proteins. DEX-1 localizes to ZP-containing aECMs in the tissues that show defects in mutants. Our studies suggest that DEX-1 is a component of multiple distinct embryonic aECMs that shape developing epithelia, and a potential partner of multiple ZP proteins.