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The Differentiation of Epidermis II

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The Differentiation of Epidermis II /. Embryol. exp. Morph., Vol. 17, 1, pp. 107-117, February 1967 107 With 4 plates Printed in Great Britain The differentiation of epidermis II. Alternative pathways of differentiation of embryonic chicken epidermis in organ culture ByJ. W. DODSON1 From the Strangeways Research Laboratory, Cambridge INTRODUCTION In the present study, two series of experiments have been made to investigate the role of the dermis in determining alternative pathways of differentiation in the epidermis. Previous work has shown that the scaly metatarsal epidermis of 12-day chicken embryos, when isolated in culture on a plasma clot or various other substrata, fails to develop normally and undergoes a characteristic sequence of differentiative and degenerative changes (McLoughlin, 1961a; Wessells, 1962;Dodson, 1963,1966). On the other hand, the separated epidermis, when cultivated in combination with either its own dermis or a gel of collagen, survives and forms a stratum corneum (Dodson, 1963, 1966). The questions arise of whether the changes produced in the epidermis by growth in isolation can be reversed by subsequent recombination of the epithelium with the dermis, and if so at what stage the degeneration becomes irreversible. Accordingly, in the first series of experiments, epidermis was cultivated in isolation for various periods of time, then recombined with dermis and cultivated further; the explants were examined histologically for signs of a keratinizing epithelium. In a similar experiment, Wessells (1963) found that proliferating columnar basal cells appeared in epidermis isolated for 10 or 24 h, then recombined with dermis for a further 1 or 2 days, but longer periods of segregation were not tested, nor was further differentiation described. The differentiation of the epidermis of embryonic chicken skin in culture can also be altered profoundly by treatment with excess of vitamin A (Fell & Mellanby, 1953; Fell, 1957). When the whole skin of 7-, 13-, or 18-day embryos was treated, keratinization was inhibited and a mucous metaplasia was in- duced; the latter change, however, was less extensive and less frequent in the oldest skin. Originally it was not known whether this action of the vitamin was directly on the epidermis or whether it was mediated through changes produced in the dermis. McLoughlin (1961a) noted, however, that in isolated limb 1 Author's address: Department of Zoology, University of Bristol, Bristol, U.K. 108 J. W. DODSON epidermis from 5-day chicken embryos, squamous changes associated with slight keratinization in control explants were inhibited by the vitamin and in the treated explants a thin layer of mucus appeared; this result indicated that in this very young material the changes were due to a primary action of the vitamin on the epithelium. The second series of experiments recorded in the present paper was made to determine whether the vitamin also acts directly on the partly differentiated epidermis of older embryos and whether the isolated epithelium from such embryos can undergo a full mucous metaplasia when grown on a collagen gel in the presence of excess of vitamin A. MATERIALS AND METHODS Epidermis was separated from dermis after Versene treatment of the scaly skin of the anterior tarso-metatarsal region of 12-day chicken embryos (stages 37^-38^ of Hamburger & Hamilton, 1951). The techniques of separation, cultivation, and histological examination have been described in a previous paper (Dodson, 1966). Sheets of separated epidermis were spread over either rayon-acetate rafts (Schaflfer, 1956) or pieces of Millipore filter, type HA (Millipore Filter Corp., Bedford, Mass.); they were then cultivated for 12-48 h at 37-5 °C by the watch-glass technique of Fell & Robison (1929) on clots made of 12 drops of fowl plasma and 8 drops of embryo extract. The pieces of separated dermis were placed on rayon rafts on clots and kept at room temperature (18-20 °C) until required for recombination, except that when epidermis was isolated for 48 h, dermis was prepared freshly immediately before recombination. After incubation the epidermis was carefully removed from the raft or filter and was placed on the inner surface of a piece of dermis (i.e. the surface not bearing the basement membrane) on a raft; a second piece of dermis was then placed over the epithelium, again with its inner surface next to the latter tissue. This 'sandwich' technique obviated the necessity of determining the basal surface of the twisted sheet of isolated epidermis, and placing the inner surface of the dermis next to the epithelium prevented the extant basement membrane on the dermis from being confused with any newly formed basement membrane next to the epidermis. The recombined tissues were cultivated on a clot as before, for periods ranging from 3 h to 7 days. For the experiments on the effect of vitamin A, gels of collagen from acetic acid-extracted rat tail tendon were prepared as described in the previous paper. Vitamin A alcohol was dissolved in ethanol and added to fresh fowl plasma to give a concentration of either 2-4 or 9 i.u. per ml in the final plasma-embryo extract clot. The medium for control explants contained the same amount of ethanol (0-1 %). Pieces of collagen gel were soaked in clot exudate (H. B. Fell, personal communication) containing either vitamin A or ethanol alone, and freshly separated epidermis was spread on them; the explants mounted on the Differentiation of epidermis in culture 109 collagen gel were then placed on a clot and incubated at 37-5 °C for 2-12 days. All explants were subcultured on to fresh clots every 2 days, and after fixation were examined histologically. RESULTS 1. Epidermis grown alone, then recombined with dermis Epidermis grown in isolation on a raft developed as described previously (Dodson, 1966). The basal cells very rapidly became flattened, the epithelium thickened, and the cells lost their regular, layered arrangement; some cells showed signs of differentiation, but by 2 days in culture most nuclei were pycnotic (Plate 1, figs. A-D). On Millipore filter the results were variable, some explants developing as above while others became attached to the filter and sometimes formed a layered arrangement. The latter grew slightly differently after recombination and are described separately; the main description refers to epidermis isolated on rafts or unattached to Millipore filter. Thirty-three explants of epidermis were grown in isolation for 24 h, then recombined with dermis. The epidermis was thickened and there were two or three layers of flattened cells at the basal surface. Mitosis had ceased, but the cytoplasm was still basophilic. The periderm, which had migrated round to the lower surface at the edges of some explants, had begun to develop its charac- teristic granules (Plate 1, fig. A). Within 3 h of the recombination, the epidermis was enveloped by dermal cells, which made close and continuous contact with the basal layer, but not with the periderm. A new periodic acid-Schiff (PAS)- positive and aniline blue-staining basement membrane first appeared under some areas of basal cells at about 10 h after recombination (Plate 2, fig. E), but it was not present under the whole basal layer until 20-27 h. Closely associated with the appearance of the basement membrane were reorientation and division of the basal cells. Although nearly all these elements were flattened at 10 h, after 15 h many were cuboidal and by 20 h most were cuboidal or even columnar (Plate 2, fig. F); flattened cells persisted in some regions, however, even after 4 and 5 days. Mitosis, which had ceased in the isolated epidermis, reappeared in both flattened and cuboidal basal cells at 10-15 h after recombination. The s. basale, re-formed 10-20 h after recombination, pushed up layers of differentiating cells which, together with the layers of flattened cells that de- veloped during isolation, formed a s. spinosum. Meanwhile the upper parts of the epidermis continued to develop as though still isolated and many of the cells became pycnotic, although the lower cells, immediately above the regene- rating epithelium, retained their basophilia longer and tended to differentiate further than the more distal cells. Cornified cells first appeared in the regenerating epithelium after 2-3 days (Plate 2, fig. G) and by 5 days a well-arranged kera- tinizing epithelium had been formed. In the most healthy explants the re- generated epidermis extended over the inner surface of the surrounding dermis, so that a keratinizing pearl was formed, in the centre of which were the remains 110 J. W. DODSON of the upper parts of the isolated epidermis. The dermis, both above and below the epithelium, underwent the normal development found in culture: the cells were healthy and produced more intercellular material; the basement mem- branes remaining on the outer surfaces were sometimes seen, even after 2 days in vitro, but often were not detected. When isolated for 30 h, the histological appearance of the epidermis was similar to that at 24 h, but of thirteen explants isolated for this time, only five redeveloped a viable epithelium when recombined with dermis for 2 days; some cuboidal, dividing basal cells, a few layers of s. spinosum, and a basement membrane were present (Plate 3, fig. H). In the other explants there were occasional small groups of living basal cells on a basement membrane, but there was no continuous s. basale and no stratified arrangement. Except for these basal cells, the rest of the epidermis continued to behave as though still isolated. Although a basement membrane was present after 2 days' recombination, the earliest time of its appearance was not determined. After 36 h of isolation, many epidermal cells, including those that were unoriented between the whorls and also those that were flattened on the lower surface, resembled cells of the lower s.
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