Horse hooves and bird feathers: Two model systems for studying the structure and development of highly adapted integumentary accessory organs--the role of the dermo-epidermal interface for the micro-architecture of complex epidermal structures

Accessory organs of the integument are locally modified parts of the potentially feather-bearing skin in birds (e.g., the rhamphotheca, claws, or scales), and of the potentially hairy skin in mammals (e.g., the rhinarium, nails, claws, or hooves). These special parts of the integument are characterised by a modified structure of their epidermal, dermal and subcutaneous layers. The developmental processes of these various integumentary structures in birds and mammals show both similarities and differences. For example, the development of the specialised epidermal structures of both feathers and the hoof capsule is influenced by the local three-dimensional configuration of the dermis. However, in feathers, in contrast to hooves, the arrangement of the corneous cells is only partially a direct result of the particular arrangement and shape of the dermal surface of the papillary body. Whereas the diameter of the feather papilla, as well as the number, length, and width of dermal ridges on the surface of the feather papilla influence the three-dimensional architecture of the feather rami, there is no apparent direct correlation between the dermo-epidermal interface and the development of the highly ordered architecture of the radii and hamuli in the feather vane. In order to elucidate this morphogenic problem and the problem of locally different processes of keratinisation and cornification, the structure and development of feathers in birds are compared to those of the hoof capsule in horses. The equine hoof is the most complex mammalian integumentary structure, which is determined directly by the dermal surface of the papillary body. Perspectives for further research on the development of modified integumentary structures, such as the role of the dermal microangioarchitecture and the selective adhesion and various differentiation pathways of epidermal cells, are discussed.     

Fine structure of the dorsal lingual epithelium of the Japanese monkey Macaca fuscata fuscata.

Filiform papillae, which were densely distributed all over the dorsal surface of the lingual body, were crown-shaped, with a central, circular area that sloped in the anterior direction and several branches that surrounded it in a semicircle from the back of the central area. Dome-shaped, fungiform papillae were scattered among these filiform papillae. At the posterior end of the lingual body, there were four circumvallate papillae. Prominent microridges and elevated intercellular borders were widely distributed in the central area of the filiform papillae and the interpapillar region. On the surface of the branches of the filiform papillae, microridges were rarely seen. On the surface of the fungiform papillae, indistinct microridges were observed. Histologically, the dorsal lingual epithelium revealed three different regions: the epithelium on the anterior side of the filiform papillae, the epithelium on the posterior side of the filiform papillae and the interpapillar epithelium. Whereas the basal and suprabasal cells are similar throughout, differences characterize the intermediate and surface layers. Keratohyalin granules appear predominantly in the intermediate layer in the epithelium on the anterior side of filiform papillae. In the epithelium on the posterior side of the filiform papillae, no keratohyalin granules occur and, instead, tonofibrils are prominent. The cells become significantly flattened. In the interpapillar epithelium, no keratohyalin granules are visible, and the tonofilaments occupy almost the entire cytoplasm of most cells in the intermediate and surface layers. The cells are larger in volume in these layers.     

Three-dimensional and surface structures of rat filiform papillae

The three-dimensional and surface structures of the simple conical papillae of the rat tongue have been demonstrated with scanning electron microscopy. The papillary projection was organized into the anterior, posterior and central core cell populations, whereas the basal region of the papilla which consisted of circularly arranged cells showed no differentiation into three autonomic cell populations. It is considered that the anterior and posterior cell populations around the central core tend to be mutually attached at the bilateral sides, and that the posterior and core cell contacts are rather close than the anterior one. The anterior papillary cells showed relatively smooth surface with little micropits and without microridges. The reticular microridges on the basal cell surface of the posterior papillary cells appear to later develop the micropits and linear microridges on the tip cell surface. These suggest that the anterior cell surface is more highly keratinized than the posterior one. The microridges or micropits on the outer cell surface and the microprojections on the inner cell surface organizing filiform papilla are considered to be the structures for the purpose of cell adhesion.     

Scanning-electron-microscopic study of the dorsal lingual surface of the squirrel monkey

The structure of the lingual papillae and the ultrastructure of the surface of the lingual dorsal epithelial cells of squirrel monkeys were observed by scanning electron microscopy. Filiform papillae were distributed over the entire dorsal surface of the tongue, except for the radix zone. Fungiform papillae were scattered among these filiform papillae. In the middle of the posterior end of the lingual body, a single vallate papilla was located. Higher magnification of the lingual dorsal epithelium revealed that prominent microridges and elevated intercellular borders occurred widely in the basofrontal area of the filiform papillae, interpapillar area and lingual radix zone. On the surface of the upper part of the filiform papillae, fine pits and hollows were observed. Indistinct microridges were distributed over the surface of the fungiform papillae.     

The three-dimensional microanatomy of Meissner corpuscles in monkey palmar skin

The Meissner corpuscle is a rapidly-adapting mechanoreceptor in the dermal papillae of digital skin. For an analysis of how the sensory endings detect tissue deformations, an examination of their fine structure and relationships with dermal collagen was carried out in the Japanese monkey, Macaca fuscata, using a combination of three methods: SEM of cell architecture denuded by 6N sodium hydroxide maceration, SEM of collagen networks exposed by a mild alkaline corrosion, and TEM according to a conventional procedure. Observations showed the sensory corpuscles to be represented by a stack of discoid components consisting of flattened axon terminals sandwiched between Schwann cell lamellae, as reported previously. Each corpuscle was entirely covered by a connective tissue capsule, which was linked with the basal aspect of the epidermis by dermal collagen fibers. Margins of the discoid components of the corpuscles were serrated with numerous fine projections of lamellar Schwann cells, which tightly held collagen trabeculae on the inner aspect of the pericorpuscular capsule. Central portions of the discoids, on the other hand, displayed extremely smooth surfaces, which were covered by a thick layer of basal lamina-like matrix. The former portions of the discoids appear susceptible to mechanical deformations of surrounding tissues, while the latter may follow the tissue movements rather slowly because of their indirect linkage with the dermal collagen network. The resulting distortions of the axon endings during dynamic phases of the tissue deformations will be in favor of the generation of rapidly adapting receptor potentials in the sensory corpuscle.     

Scanning electron microscopic study on the structure of the lingual papillae of the Saanen goat

The morphology of lingual papillae of the ten male mature Saanen goats (11 months old, approximately 42 kg in weight and of a known pedigree) was examined by scanning electron microscopy. Tissues were taken from the dorsal and ventral surfaces of the apex, body and root of the tongue, and were prepared accordingly and observed under the scanning electron microscope. On the dorsal and ventro-lateral surfaces of the lingual mucosa, three types of mechanical papillae (filiform, lenticular, and conical) and two types of gustatory papillae (vallate and fungiform) were observed. The structure and density of the filiform papillae differentiated on the anterior, posterior and ventro-lateral aspects of the tongue. Two types of lenticular papillae, both possessing a prominent surrounding papillary groove, were determined. The pyramidal-shaped type I lenticular papilla had a pointed apex while the round-shaped type II lenticular papilla possessed a blunt apex. Certain number of the type I lenticular papillae had double apices. The larger conical papillae were hollow structures, differing structurally from the filiform papillae with their larger size, a tip without projections and lack of the secondary papillae. The vallate papillae were present on both rims of the torus linguae, were encircled by a prominent gustatory furrow which was also surrounded by a thick annular fold. The fungiform papillae were scattered among the filiform papillae in the anterior two-thirds of the dorsal and lateral surfaces, and each of them was highly protected by surrounding filiform papillae, yet encircled by a papillary groove. Our findings indicate that Saanen goat have profuse distribution of papillae on the tongue displaying morphological features characteristic of mechanical function.     

The dynamics of hoof growth of the primitive Konik horses (Equus caballus gmelini Ant.) in an annual cycle

The annual growth rate of the horny wall of the hoof was investigated in 38 horses—31 mares and seven stallions. Experimental subjects were Konik horses kept in a conservative breeding herd. The horses hooves of both limbs: the right fore limb and the right hind limb were measured and next growth rate of the horny wall was analysed at five points of the hoof capsule. On the basis of Principal Component Analysis it was found that the subjects needed to be considered in three groups: three-year old mares, older mares and stallions. Next the growth increments were averaged in each investigated group and compared. The dynamics of hoof horn growth turned out to be the highest in the group of young mares, followed by the group of stallions and the group of adult mares. In the winter months the lowest growth increment of the hoof horn was observed in all the analysed groups. In the period of the elongating solar day, i.e. from May to July, the growth was rapid and reached the highest values. Starting from August the growth of the hoof horn decreased.     

Comparative studies of the dorsal surface of the tongue in three mammalian species by scanning electron microscopy

Comparative features of the dorsal tongue epithelia in musk shrews, mongooses and rats were described. The shapes of the filiform papillae were different in each of the species. The distribution pattern of filiform papillae was similar both in the musk shrews and mongoose, in that the form of filiform papillae changed gradually from the lingual apex to the posterior part of the lingual body. By contrast, the different types of filiform papillae were distributed on definite areas of the dorsal lingual surface in the rat. Microridges on the interpapillar surface in the musk shrew and mongoose presented a clear outline, but those of the rat were not so distinct. In all species, the upper surface of filiform papillae did not show any distinct microridges.     

Cuttlefish skin papilla morphology suggests a muscular hydrostatic function for rapid changeability

Coleoid cephalopods adaptively change their body patterns (color, contrast, locomotion, posture, and texture) for camouflage and signaling. Benthic octopuses and cuttlefish possess the capability, unique in the animal kingdom, to dramatically and quickly change their skin from smooth and flat to rugose and three‐dimensional. The organs responsible for this physical change are the skin papillae, whose biomechanics have not been investigated. In this study, small dorsal papillae from cuttlefish (Sepia officinalis) were preserved in their retracted or extended state, and examined with a variety of histological techniques including brightfield, confocal, and scanning electron microscopy. Analyses revealed that papillae are composed of an extensive network of dermal erector muscles, some of which are arranged in concentric rings while others extend across each papilla's diameter. Like cephalopod arms, tentacles, and suckers, skin papillae appear to function as muscular hydrostats. The collective action of dermal erector muscles provides both movement and structural support in the absence of rigid supporting elements. Specifically, concentric circular dermal erector muscles near the papilla's base contract and push the overlying tissue upward and away from the mantle surface, while horizontally arranged dermal erector muscles pull the papilla's perimeter toward its center and determine its shape. Each papilla has a white tip, which is produced by structural light reflectors (leucophores and iridophores) that lie between the papilla's muscular core and the skin layer that contains the pigmented chromatophores. In extended papillae, the connective tissue layer appeared thinner above the papilla's apex than in surrounding areas. This result suggests that papilla extension might create tension in the overlying connective tissue and chromatophore layers, storing energy for elastic retraction. Numerous, thin subepidermal muscles form a meshwork between the chromatophore layer and the epidermis and putatively provide active papillary retraction. J. Morphol., 2013. © 2013 Wiley Periodicals, Inc.     

A scanning electron microscopic study of secondary lamellae and chloride cells of rainbow trout (Salmo gairdneri)

Summary Scanning electron micrographs of gill tissue from rainbow trout fixed with 50% glutaraldehyde revealed the presence of microridges on surfaces of epithelial cells of the secondary lamellae. These microridges vary in length from 1 to 7 , with a mean height of 0.75 . Calculations show that they increase the total lamellar epithelial surface area approximately 2.5 fold. Mucus secreting cells are present on the body of the filament and on secondary lamellae. Chloride cells are located primarily in the interlamellae filamental epithelium and on the basal area of lamellae. Extensions of the chloride cell epithelium are microvillous in nature and their height is only slightly greater than that of the microridges of typical lamellar epithelial cells. A reduction in number or complete absence of microvilli on chloride cells appeared to be related to degenerative changes in these cells observed in transmission electron micrographs. Non secretory interlamellae filamental epithelial cells have microridges of very attenuated lengths.This research was supported by EPA Grant R-801034, USPHS Training Grant HL-05873, the Mich. Agr. Exp. Sta., Proj. 122 (Journal Article No. 5801), and OWRR Grant A-064. Acknowledgements: The authors wish to express their gratitude to Mrs. J. Mack and Mr. Wm. McAffe for their technical assistance with the electron microscopes.     

Anatomical and scanning electron microscopic characteristics of the oropharyngeal cavity (tongue,palate and laryngeal entrance) in the southern lapwing (Charadriidae: Vanellus chilensis,Molina 1782)

This investigation aimed to determine the morphological characteristics of the tongue, palate and laryngeal entrance of southern lapwing by gross anatomy and scanning electron microscopy. For this purpose, the organs of three birds were used as material. Numerous densely distributed acicular projections were found on the lingual apex. Papillary crest consisting of sharp conical papillae were observed between the body and root of the tongue. Conical papillae of the lateral border of the papillary crest were triangular in form, and other conical papillae of the papillary crest were shorter in form. There were no papillary projections or papillae on the smooth surfaces of the lingual body and radix. On the median part of the palate, larger conical papillae, which were directed caudally, also surrounded entrance of the choanal cleft. The transversal papillary rows of conical papillae were observed between the rostral and caudal parts of the choanal cleft and on the caudal border of the infundibular cleft. The laryngeal entrance was surrounded by smooth mucosa without conical papillae. However, in the caudal border of the glottic fissure, there was a conical papillary row formed by numerous conical papillae. There were no anatomical differences between female and male birds.     

An ultrastructural study of the dorsal lingual epithelium of the crab-eating frog,Rana cancrivora

The amphibian tongue contains two types of papilla which are believed to function in gustation and in the secretion of salivary fluid. Scanning electron microscopy reveals that columnar, filiform papillae are compactly distributed over nearly the entire dorsal surface of the tongue of the frog, Rana cancrivora, and fungiform papillae are scattered among the filiform papillae. Microridges and microvilli are distributed on the epithelial cell surface of the extensive area of the filiform papillae. Light microscopy shows that the apex of each filiform papilla is composed of stratified columnar and/or cuboidal epithelium and its base is composed of simple columnar epithelium. Transmission electron microscopy reveals that most of the epithelium of the filiform papillae is composed of cells that contain numerous round electron-dense granules 1–3 μm in diameter. Cellular interdigitation is well developed between adjacent cells. On the free-surface of epithelial cells, microridges or microvilli are frequently seen. Between these granular cells, a small number of ciliated cells, mitochondria-rich cells and electron-lucent cells are inserted. In some cases, electron-dense granules are present in the ciliated cells. At higher magnification, the electron-dense granules appear to be covered with patterns of spots and tubules. Overall, the morphology and ultrastructure of the lingual epithelium of the three species of Rana that have been studied are quite similar, but they can be easily distinguished from those of Bufo japonicus. Therefore, it appears that lingual morphology is phylogenetically constrained among members of the predominantly freshwater genus Rana to produce uniformity of papillary structure and this morphology persists in Rana cancrivora despite the distinct saline environment in which it lives. © 1993 Wiley-Liss, Inc.     

Roles for PDGF-A and sonic hedgehog in development of mesenchymal components of the hair follicle.

Skin appendages, such as hair, develop as a result of complex reciprocal signaling between epithelial and mesenchymal cells. These interactions are not well understood at the molecular level. Platelet-derived growth factor-A (PDGF-A) is expressed in the developing epidermis and hair follicle epithelium, and its receptor PDGF-Ralpha is expressed in associated mesenchymal structures. Here we have characterized the skin and hair phenotypes of mice carrying a null mutation in the PDGF-A gene. Postnatal PDGF-A-/- mice developed thinner dermis, misshapen hair follicles, smaller dermal papillae, abnormal dermal sheaths and thinner hair, compared with wild-type siblings. BrdU labeling showed reduced cell proliferation in the dermis and in the dermal sheaths of PDGF-A-/- skin. PDGF-A-/- skin transplantation to nude mice led to abnormal hair formation, reproducing some of the features of the skin phenotype of PDGF-A-/- mice. Taken together, expression patterns and mutant phenotypes suggest that epidermal PDGF-A has a role in stimulating the proliferation of dermal mesenchymal cells that may contribute to the formation of dermal papillae, mesenchymal sheaths and dermal fibroblasts. Finally, we show that sonic hedgehog (shh)-/- mouse embryos have disrupted formation of dermal papillae. Such embryos fail to form pre-papilla aggregates of postmitotic PDGF-Ralpha-positive cells, suggesting that shh has a critical role in the assembly of the dermal papilla.     

A scanning electron microscope study of the gills of the air-breathing catfish, Clarias batrachus L.

Using the scanning electron microscope, the gills of the air-breathing catfish, Clarias batrachus , have been studied. The overall morphology of the gills are similar to other teleosts. In contrast to water-breathing species, however, microridges are absent from the surfaces of the secondary lamellae and only short microvilli are present. Long, convoluted microridges are present on the epithelial cells of the gill filaments. The possible roles of these structures in relation to water flow are discussed.     

人胎儿真皮乳头和皮纹发生的研究

本文用扫描电镜法研究了入胎儿的皮纹发生过程,包括初级真皮嵴、次级真皮嵴、真皮乳头和表皮隆线的发生。为研究人皮纹的发生和皮肤的异常提供了皮肤正常发育的形态学依据。共观察111例从第6周到第9个月胎儿的皮纹区皮肤,表明第3个月末胎儿开始形成初级真皮嵴,以后逐渐加深,至第16周嵴的顶端中央产生纵沟形成两条平行的次级真皮嵴;自19周后,次级真皮嵴局部隆起,由波浪形逐渐形成乳头。至30周乳头呈犬牙状。表皮隆线于第4—5月形成,随真皮乳头的增高而渐趋明显。至第6个月,全部皮纹图样已可辨认。本文还讨论了真皮乳头发生的过程。     

A whole lamella perspective on the origin of the epidermal free margin of Anolis (Reptilia: Dactyloidae) toe pads

Anoline lamellae terminate in an epidermal free margin carrying the majority of its setae. How the free margin is extruded from the body of the scale is not well understood. Two hypotheses have been advanced to account for it, one advocating distal migration of the outer epidermal layers relative to the body of the lamella, and the other proposing regression of the dermal core. Available evidence provides partial support for both. We assembled a series of specimens of Anolis grahami representing all shedding cycle stages, and prepared histological sections of the toe pads to allow measurement of appropriate lamellar components through the shedding cycle. Through its proliferative phases the lamellae increase markedly in length, with the distance between the distal tip of the dermal core and that of the lamella accounting for most of this, indicating that epidermal extrusion is responsible for production of the new free margin. The dermal core showed no evidence of regression. Concomitant with epidermal extrusion, the lacunar cells on the inner lamellar face hypertrophy and keep pace with the increasing thickness of the outer lamellar face resulting from the lengthening of the replacement setae. The integrated changes observed are consistent with continuity of functioning and alignment of the exposed setal carpet of the outer epidermal generation while ensuring that the new setal carpet is fully aligned and functional immediately after shedding. At shedding the original proportions of the lamellae are restored. Development of the new free margin results from a combination of distal displacement of Oberhäutchen cells along with arrested maturation of the epidermis in this region. Changes in length of the lamellae during the proliferative stages may impact the overall size of the adhesive toe pad, which may have consequences for assessments of the relationship between whole animal clinging ability and adhesive pad area. J. Morphol. 278:360–368, 2017. © 2017 Wiley Periodicals, Inc.     

Development of mechanical papillae of the tongue in the domestic goose (<Emphasis Type="Italic">Anser anser f. domestica</Emphasis>) during the embryonic period

Three types of mechanical papillae, i.e., conical, filiform, and hair-like papillae, are present on the tongue in the domestic goose. Within conical papillae, we distinguish three categories: large and small conical papillae on the body and conical papillae on the lingual prominence. The arrangement of mechanical papillae on the tongue in Anseriformes is connected functionally with different feeding mechanisms such as grazing and filter-feeding. The present work aims to determine whether morphology of three types of mechanical papillae in goose at the time of hatching is the same as in an adult bird and if the tongue is prepared to fulfill feeding function. Our results revealed that the primordia of the large conical papillae start to develop during the differentiation stage. The primordia of the small conical papillae and conical papillae of the lingual papillae start to develop during the growth stage. At the end of the growth stage, only large conical papillae, three pairs of small conical papillae, and conical papillae of the lingual prominence have similar arrangement as in an adult bird. The shape and arrangement of the remaining small conical papillae probably will be changed after hatching. During embryonic period, the filiform papillae and hair-like papillae are not formed. The embryonic epithelium that covered the mechanical papillae undergoes transformation leading to the formation of multilayered epithelium. During prehatching stage, epithelium becomes orthokeratinized epithelium. In conclusion, the tongue of the domestic goose after hatching is well prepared only for grazing. The filtration of food from water is limited due to the lack of filiform papillae.     

Gross structure of the respiratory organs and dimensions of the gill in the mud–skipper, Periophthalmodon schlosseri (Bleeker)

In Periopkrlialnwdon scldosseri the respiratory organs consist of the gills, the suprabranchial and opercular chambers. The gills are more suited for aerial than aquatic respiration as is shown by the presence of the vascular papillae, blood sinusesand dilated blood vessels in their lamellae. The gill lamellae possess a surface coat of sulphated mucopolysaccharides that prevents water loss during exposure to the air. The filaments of the outer hemibranchs in the first gill arch are reduced to nearly one quarter of those of its posterior hemibranch. The gill area in relation to body weight shows a high slope value ( b =0·93).     

Comparative morphology of changeable skin papillae in octopus and cuttlefish

A major component of cephalopod adaptive camouflage behavior has rarely been studied: their ability to change the three‐dimensionality of their skin by morphing their malleable dermal papillae. Recent work has established that simple, conical papillae in cuttlefish (Sepia officinalis) function as muscular hydrostats; that is, the muscles that extend a papilla also provide its structural support. We used brightfield and scanning electron microscopy to investigate and compare the functional morphology of nine types of papillae of different shapes, sizes and complexity in six species: S. officinalis small dorsal papillae, Octopus vulgaris small dorsal and ventral eye papillae, Macrotritopus defilippi dorsal eye papillae, Abdopus aculeatus major mantle papillae, O. bimaculoides arm, minor mantle, and dorsal eye papillae, and S. apama face ridge papillae. Most papillae have two sets of muscles responsible for extension: circular dermal erector muscles arranged in a concentric pattern to lift the papilla away from the body surface and horizontal dermal erector muscles to pull the papilla's perimeter toward its core and determine shape. A third set of muscles, retractors, appears to be responsible for pulling a papilla's apex down toward the body surface while stretching out its base. Connective tissue infiltrated with mucopolysaccharides assists with structural support. S. apama face ridge papillae are different: the contraction of erector muscles perpendicular to the ridge causes overlying tissues to buckle. In this case, mucopolysaccharide‐rich connective tissue provides structural support. These six species possess changeable papillae that are diverse in size and shape, yet with one exception they share somewhat similar functional morphologies. Future research on papilla morphology, biomechanics and neural control in the many unexamined species of octopus and cuttlefish may uncover new principles of actuation in soft, flexible tissue. J. Morphol. 275:371–390, 2014. © 2013 Wiley Periodicals, Inc.     

Nerves and nerve endings in the skin of tropical cattle.

The nerves and nerve endings in the skin of tropical cattle were studied using histological and histochemical techniques. Many nerve trunks and fibres were present in the reticular and papillary dermis in both hairy and non-hairy skin sites. In non-hairy skin locations such as the muzzle and lower lip, encapsulated endings akin to Krause and Ruffini end bulbs, which arise from myelinated nerve trunks situated lower down the dermis were observed at the upper papillary layer level. Some fibre trunks seen at this level extended upwards to terminate within dermal papillae as bulb-shaped longitudinally lamellated Pacinian-type endings, while other onion-shaped lamellated nerve structures were located either within dermal papillae or near the dermo-epidermal area. Intraepidermal free-ending nerve fibres, appearing non-myelinated were observed in areas with thick epidermis. Intraepidermal free-ending nerve fibres, appearing non-myelinated were observed in areas with thick epidermis. On hairy skin sites, however, organized nerve endings or intraepidermal nerve endings were not readily identifiable.