Form and function of the apical extracellular matrix: new insights from Caenorhabditis elegans, Drosophila melanogaster, and the vertebrate inner ear

Abstract

Apical extracellular matrices (aECMs) are the extracellular layers on the apical sides of epithelia. aECMs form the outer layer of the skin in most animals and line the luminal surface of internal tubular epithelia. Compared to the more conserved basal ECMs (basement membranes), aECMs are highly diverse between tissues and between organisms and have been more challenging to understand at mechanistic levels. Studies in several genetic model organisms are revealing new insights into aECM composition, biogenesis, and function and have begun to illuminate common principles and themes of aECM organization. There is emerging evidence that, in addition to mechanical or structural roles, aECMs can participate in reciprocal signaling with associated epithelia and other cell types. Studies are also revealing mechanisms underlying the intricate nanopatterns exhibited by many aECMs. In this review, we highlight recent findings from well-studied model systems, including the external cuticle and ductal aECMs of Caenorhabditis elegans, Drosophila melanogaster, and other insects and the internal aECMs of the vertebrate inner ear.

Keywords: chitin; collagens; epithelia; tubulogenesis; zona pellucida domain.

Figure 1.. Apical extracellular matrices of Caenorhabditis elegans, Drosophila melanogaster, and the vertebrate inner ear.

a. Cartoon of adult C. elegans cuticle, longitudinal section. The cuticle consists of an outer surface coat (gold), a lipid-rich epicuticle (red), collagenous cuticle proper (divided into cortical [blue], medial [gray], fibrous [purple], and basal [navy] layers). The cuticle is secreted by the underlying cellular epidermis (green), internal to which is a basement membrane (burgundy). b. Cartoon of D. melanogaster cuticle, consisting of an outer lipid-rich envelope (red), glycoprotein-rich epicuticle (yellow), and the chitinous procuticle (blue), formed in the assembly zone at the apical surface of the underlying epidermis (green). Pore canals form channels through the cuticle layers to the surface. c. Cartoon of D. melanogaster mature tracheal cuticle, showing taenidial folds (blue). Envelope and epicuticle are not shown for simplicity. d. The vertebrate tectorial membrane (blue) is shown in cross section, attached to the underlying epithelial ridge of the organ of Corti at its medial edge and to the stereocilia of the outer hair cells at its lateral edge. The underlying basement membrane is known as the basilar membrane.