Comparative aspects of the inner root sheath in adult and developing hairs of mammals in relation to the evolution of hairs

The inner root sheath (IRS) allows the exit of hairs through the epidermal surface. The fine structure of monotreme and marsupial IRS and trichohyalin is not known. Using electron microscopy and immunocytochemistry, the localization of trichohyalin and transglutaminase have been studied in monotreme and marsupial hairs, and compared with trichohyalin localization in placental hairs. Trichohyalin in all mammalian species studied here is recognized by a polyclonal antibody against sheep trichohyalin. This generalized immunoreactivity suggests that common epitopes are present in trichohyalin across mammals. In differentiating IRS cells, trichohyalin granules of variable dimensions are composed of an immunolabelled amorphous matrix associated with a network of 10-12-nm-thick keratin filaments. Transglutaminase labelling is present among keratin bundles and trichohyalin granules, and in condensed nuclei of terminally differentiating cells of the inner root sheath. The IRS in monotreme hairs is multistratified but lacks a distinguishable Henle layer. Cornification of IRS determines the sculpturing of the fibre cuticle and later shedding from the follicle for the exit of the hair fibre on the epidermal surface. It is hypothesized that the stratification of IRS in Henle, Huxley and IRS cuticle layers is derived from a simpler organization, like that present in the IRS of monotremes. The IRS is regarded as a localized shedding/sloughing layer needed for the exit of hairs without injury to the epidermis. The formation of the IRS during the evolution of mammalian epidermis allowed the physiological exit of hairs produced inside the skin. The peculiar morphogenesis of hairs in possible primitive skins, such as those of the monotremes (mammals with some reptilian characteristics) or the tails of some rodents (a scaled skin), may elucidate the evolution of hairs. In monotreme and rodent tail skin, the dermal papilla remains localized on the proximal side of the hair peg and forms a hair placode with bilateral symmetry. The papilla is progressively surrounded by the down-growing hair peg until a dermal papilla with radial symmetry is formed. It is speculated that the progressive reduction of the extended dermal papilla of reptilian scales into small and deep papillae of therapsid reptiles produced hairs in mammals.