Keratinization in crocodilian scales and avian epidermis: evolutionary implications for the origin of avian apteric epidermis

Terminal differentiation of keratinocytes of avian apteric epidermis occurs with the accumulation of little keratin and much lipids so that a soft and elastic corneous layer is produced. The distribution of keratins and some proteins associated with cornification has been studied in crocodilian scales, in ratite and zebrafinch apteric epidermis by means of light and ultrastructural immunocytochemistry. Soft (alpha)keratinization in apteric epidermis of birds resembled the process occurring in hinge regions of crocodilian scales where the stratum corneum was thin and beta(hard)-keratin disappeared. Acidic and basic alpha-keratins were seen in living pre-corneous layers. Instead, keratins typical for cornification, loricrine, transglutaminase, and sometimes filaggrin-like immunoreactivities, were present in the transitional and lowermost corneous layer of crocodilian hinge and apteric avian epidermis. Trichohyalin, involucrin, and iso-peptide bond immunoreactivities were absent. Loricrine-like and transglutaminase labelling were generally absent in the corneous layer, but were weakly present among keratin bundles and lipids in the transitional layer of apteric epidermis. Transglutaminase immunolabelling was present in condensing nuclear chromatin of transitional corneocytes of apteric epidermis, suggesting that these cells undergo terminal differentiation or even apoptosis. Sulfydryl groups in keratins, or specific sulfur-rich proteins of loricrin-type, were scarce in apteric epidermis. This suggests that the cornified cell envelope of avian keratinocytes is more simplified than that of mammalian keratinocytes. In the latter, numerous proteins concentrate along the corneous cell envelope to enhance mechanical and chemical resistance of the stratum corneum. This mechanism probably is more simplified in apteric epidermis of birds, and the mechanical protection of the epidermis is taken over by the plumage, while apteric epidermis has mainly a role as barrier against water loss. It is speculated that avian interfollicular and apteric epidermis has evolved from interscale hinge regions of proto-avian archosaurian ancestors.