The corneal epithelial surface in the eyes of vertebrates: Environmental and evolutionary influences on structure and function

Abstract

The smooth optical surface of the cornea is maintained by a tear film, which adheres to a variety of microprojections. These microprojections increase the cell surface area and are thought to improve the movement of oxygen, nutrients, and metabolic products across the outer cell membranes. However, little is known of these structural adaptations in vertebrates inhabiting different environments. This field emission scanning electron microscopic study examined the cell density and surface structure of corneal epithelial cells across 51 representative species of all vertebrate classes from a large range of habitats (aquatic, amphibious, terrestrial, and aerial). In particular, we wished to extend the range of vertebrates to include agnathans and some uniquely Australian species, such as the Australian lungfish (Neoceratodus forsteri), the Australian galah (Eolophus roseicapillus), the Australian koala (Phascolarctos cinereus), and the rat-tailed dunnart (Sminthopsis crassicaudata). Epithelial cell densities ranged from 28,860 +/- 9,214 cells mm(-2) in the flathead sole Hippoglossoides elassodon (a marine teleost) to 2,126 +/- 713 cells mm(-2) in the Australian koala (a terrestrial mammal), which may indicate a reduction in osmotic stress across the corneal surface. A similar reduction in cell density occurred from marine to estuarine to freshwater species. The structure and occurrence of microholes, microplicae, microridges, and microvilli are also described with respect to the demands placed on the cornea in different environments. All species that spend significant periods out of an aquatic environment possess microvilli and/or microplicae. These include all of our species of Mammalia, Aves, Reptilia, Amphibia, and even one species of Teleostei (Australian lungfish). Well-developed microridges occur only in teleosts in high osmolarity environments such as marine or estuarine habitats. Clear interspecific differences in corneal surface structure suggest a degree of adaptive plasticity, in addition to some phylogenetic trends.

Microridges in Cyprinus carpio scale epidermis

“…The puncta pattern observed here may be indicative of widespread microridge formation as short microridges in these patterns consisted of just a few bright actin puncta (Figure 1b for example). Interestingly a nearly identical honeycomb pattern was seen in the epidermis of yearling coho salmon (Hawkes, 1974) and possibly related patterns observed in vertebrate corneal epithelium (Collin & Collin, 2006) as well. The final microridge configuration identified in this study is that of a honeycomb pattern which is distinctly different from any other pattern observed on koi epidermal cells here.…”

Quantification of Acute Vocal Fold Epithelial Surface Damage with Increasing Time and Magnitude Doses of Vibration Exposure

“…Microprojections assist with stabilizing secretions and facilitating water and metabolic product movement across the cell membrane [9], [13]–[15]. In addition, compromised integrity of this important cell layer may lead to decreased stabilization of secretions and reduced water and metabolic product movement across the outer cell membranes.…”

“…The structure and function of microprojections in other epithelial tissues has been well described. It has been suggested that corneal microprojections enlarge the cell surface area to facilitate nutrient and oxygen absorption, stabilize secretions, and assist with water and metabolic product movement across outer epithelial cell membranes [13], [14]. In comparison to corneal microprojections, the function of vocal fold epithelial microprojections is less understood.…”

Raised intensity phonation compromises vocal fold epithelial barrier integrity

“…The surface of the outermost layer of epithelial cells consists of dense microprojections designed to increase cell surface area. These microprojections provide other important functions, including increasing the absorbance of oxygen and nutrients, and assisting in the movement of water and metabolic products across the cell membrane 1–3. The junctional complex is made up of intercellular tight junction proteins (occludin, zonula occluden (Z0-1), claudin) and subjacent adherens junctions (β-catenin and E-cadherin).…”