Contradictions in Modern Data on the Structure and Function of Dog Hepatoid Circumanal Glands1

Since the 1950s, an erroneous viewpoint has gained a foothold in the special and reference literature that dog hepatoid circumanal glands have an abortive nature, lack efferent ducts, and show no signs of secretory activity. Nevertheless, most modern researchers indicate that these glands are actively functioning structures differentiated to exercise some function according to their histological pattern; however, no one has managed to define this function. The latest international publication (Atoji et al., 1998) considers dog circumanal hepatoid glands as a circumanal body similar to epidermis rather than glands. We discuss strong and weak points of the data on dog hepatoid circumanal glands published in 1950s–1990s in comparison with those obtained in our purposeful long-term investigation of various hepatoid glands. We strongly disagree with the viewpoint of Atoji et al. (1998); hepatoid circumanal glands of dog and other canids should be considered as odor glands, their abundant protein secretion covers the skin surface in the circumanal region, it is preserved on fecal marks, and its smell is perceived during mutual nosing of the anal region.     

Detection of Hepatoid Glands and Distinctive Features of the Hepatoid Acinus

In the 1920s–1930s, skin glands of a new type, hepatoid glands, were described in 13 mammal species (Rodentia, Canidae, and Bovidae). The hepatoid glands resemble sebaceous glands in their morphology, bur radically differ from them in specific structure of the acinus and another type of secretion. Later, these data either could not be confirmed or were considered insignificant and the hepatoid glands were described as modified sebaceous glands, glands with uncertain function, or modifications of epidermis. Based on the studies of various hepatoid glands in 22 species of Carniviora and Artiodactyla, the authors described in detail the characteristic features of the hepatoid acinus, which allow a precise discrimination of hepatoid and sebaceous glands. Extracellular secretory canaliculi have been described in the hepatoid glands, as well as the richness of hepatoid glands in protein, distribution of hydrophobic lipids in certain hepatoid glands, and formation of excretory ducts and cysts. The hepatoid glands are a source of great amounts of protein secreted in the merocrine way; the secretory substance of some of these glands has a strong odor.     

The morphogenesis of mammalian cutaneous glands in evolutionary perspective

The morphogenesis of mammalian cutaneous glands is considered based on the analysis of the literature and our own original data with the focus on the issues of gland polymorphism and specific features in postnatal development (from the case study of circumanal hepatoid glands of newborn domestic dogs), including the features reflecting the evolutionary relationships of various types of cutaneous glands. The hepatoid glands are a component of the glandular complex of the hair follicle, which also includes sebaceous and sweat glands; have a specific structure; and produce protein secretion by a merocrine pathway. Characteristic of these glands are wide polymorphism, sex- and age-related differences in the degree of development, occurrence in only a few phylogenetically related mammalian taxa (even-toed ungulates and carnivores); and a signaling type of their secretion. The data support the “generative concept,” relying on the idea of a separate and independent origination of diverse derivatives of the external integuments.     

Microstructure of skin derivatives as a reflection of phylogenesis of vertebrates

The possibility of using separate signs of microstructure of skin derivatives to understand phylogenesis processes at various hierarchical levels on the example of elasmoid scale of bony fish, feathers of Paleognathae birds, hepatoid glands, and mammal hair was demonstrated and discussed. It was shown that (1) the presence of toothed sclerite growths on the surface of the elasmoid scale of bony fish provided with a central canal can serve as a proof of the evolutional relation of placoid and elasmoid scales; (2) particularities of the microstructure of feathers of Paleognathae birds accord with the branching of their phylogenetic tree; (3) the development of hepatoid glands suggests a phylogenetic relatedness of ancestor forms of cavicorns, Canidae, and Felidae; (4) the subtle construction of horse hair shows the succession of the ancient E. lenensis and northern aborigine breeds of the domestic horse, the direction of the historical process of horse domestication and adaptation of these animals to environmental conditions; (5) similarities in the microstructure of hair of the giant and red panda and bears indicate their evolutional links with Ursidae rather than raccoons.     

Comparative Morphological Analysis of Different Hepatoid Glands: Histological Variants and the Morphofunctional Unit

Three groups can be recognized among hepatoid glands: glands synthesizing protein alone, glands synthesizing protein and hydrophobic lipids and/or melanin, and intermediate glands. Histological variants (seven in total) can be recognized within each group. Different possible combinations of hepatoid glands with other derivatives of hair follicles are considered. The first definition of the morphofunctional unit of hepatoid glands is proposed.__________Translated from Izvestiya Akademii Nauk, Seriya Biologicheskaya, No. 4, 2005, pp. 428–434.Original Russian Text Copyright © 2005 by Shabadash, Zelikina.     

The Tail Gland of Canids

The tail gland of canids is a hepatoid glandular organ surrounded and penetrated by powerful hair erector muscles squeezing out its lipoprotein secretion onto the skin surface. The gland is most developed in solitary species (Arctic, red, and corsac foxes) where it is represented by powerful glandular layer with large secretion containers—cisterns. It is less developed in the jackal; there are cisterns but glandular lobes do not merge into a layer. In the raccoon dog, wolf, and domestic dog the gland is composed of small lobes without cisterns. Hepatoid glands of the tail gland are represented by two histological variants distinguished by the presence or absence of hydrophobic lipids in the secretory cells. The excretory ducts are formed by lipid transformation of the cellular bands.     

The histological and histochemical characteristics of the hepatoid circumanal glands in the dog: the features of similarity and difference with the skin glands of other types

Three types of skin glands, the derivatives of the outer root sheath of the hair follicle, have been compared, which are represented by hepatoid, sebaceous and apocrine sweat glands. There are three characteristic properties inherent to hepatoid glands, existence of a network of intercellular secretory tubules, lysis of some secretory cells during the duct formation which is not the fatty transformation and cyst formation.     

The development of the sweat and sebaceous glands in the skin of the one-humped camel (Camelus dromedarius)

The sweat gland primordium appeared as a solid bud from the ental side of the epithelial cords of the growing hair follicles in the CRL 36 cm-fetus from the primary hair follicles and in the CRL 64 cm-fetus from the secondary ones. In the CRL 68 cm-fetus the glands were tubular with a slight curving of their lower third, which became convoluted at the CRL 83 cm-stage. At the latter age, clear myoepithelial cells were observed in the secretory portion as also in the duct. The buds of the sebaceous glands could be observed in the CRL 45 cm-fetus from the primary hair follicles and in the CRL 68 cm-fetus from the secondary ones. At the CRL 83 cm-fetal stage, the branched glands were elongated in shape and opened into the follicles by two separated ducts, united at the hair canal. The glands were in function nearly from its early development.     

The skin of primates. XL. The skin of the cottontop pinché Saguinus (=Oedipomidas) oedipus

The skin of Saguinus (= Oedipomidas) oedipus Linnaeus, is basically similar to that of the red-mantled tamarin, Saguinus (= Tamarinus) fuscicollis Spix; it has several peculiarities: (1) a circumscribed tuft of vibrissae on the ulnar aspect of the wrist; (2) an accumulation of apocrine glands over the sternum; and (3) an extensive posterior abdominal field of gigantic sebaceous glands admixed with large apocrine glands, better developed in the female. The epidermis, dermis, hair follicles, sebaceous ducts, and apocrine excretory ducts are all heavily pigmented. Hairs are arranged in linear perfect sets; the epithelial sac of quiescent follicles is devoid of glycogen and phosphorylase. Eccrine sweat glands are restricted to the volar friction surfaces and contain no glycogen. Only the coiled excretory ducts of the eccrine glands contain phosphorylase. All cutaneous nerve fibers are more reactive for acetylthan butyrylcholinesterase.     

The complete mitochondrial genome of dhole <Emphasis Type="Italic">Cuon alpinus</Emphasis>: phylogenetic analysis and dating evolutionary divergence within canidae

The dhole (Cuon alpinus) is the only existent species in the genus Cuon (Carnivora: Canidae). In the present study, the complete mitochondrial genome of the dhole was sequenced. The total length is 16672 base pairs which is the shortest in Canidae. Sequence analysis revealed that most mitochondrial genomic functional regions were highly consistent among canid animals except the CSB domain of the control region. The difference in length among the Canidae mitochondrial genome sequences is mainly due to the number of short segments of tandem repeated in the CSB domain. Phylogenetic analysis was progressed based on the concatenated data set of 14 mitochondrial genes of 8 canid animals by using maximum parsimony (MP), maximum likelihood (ML) and Bayesian (BI) inference methods. The genera Vulpes and Nyctereutes formed a sister group and split first within Canidae, followed by that in the Cuon. The divergence in the genus Canis was the latest. The divarication of domestic dogs after that of the Canis lupus laniger is completely supported by all the three topologies. Pairwise sequence divergence data of different mitochondrial genes among canid animals were also determined. Except for the synonymous substitutions in protein-coding genes, the control region exhibits the highest sequence divergences. The synonymous rates are approximately two to six times higher than those of the non-synonymous sites except for a slightly higher rate in the non-synonymous substitution between Cuon alpinus and Vulpes vulpes. 16S rRNA genes have a slightly faster sequence divergence than 12S rRNA and tRNA genes. Based on nucleotide substitutions of tRNA genes and rRNA genes, the times since divergence between dhole and other canid animals, and between domestic dogs and three subspecies of wolves were evaluated. The result indicates that Vulpes and Nyctereutes have a close phylogenetic relationship and the divergence of Nyctereutes is a little earlier. The Tibetan wolf may be an archaic pedigree within wolf subspecies. The genetic distance between wolves and domestic dogs is less than that among different subspecies of wolves. The domestication of dogs was about 1.56–1.92 million years ago or even earlier.     

Morphologic diversity of the minor salivary glands of the rat: fertile ground for studies in gene function and proteomics

In this article the locations and histologic and ultrastructural features of all of the minor salivary glands of the rat are presented; similarities and differences among them are highlighted. These glands are almost as diverse morphologically as the major salivary glands of the rat. The acini of von Ebner's glands are serous; those of the anterior and posterior buccal glands and minor sublingual glands are mucous; and those of the glossopalatal, palatal, and Weber's glands are mucous with serous demilunes. The anterior buccal, minor sublingual and von Ebner's glands have striated and stratified columnar ducts, while only the minor sublingual and von Ebner's glands have intercalated ducts. The glossopalatal, palatal, posterior buccal and Weber's glands have none of these ducts; the tubulo-acini drain abruptly into short terminal ducts composed of stratified squamous epithelium. All of the mucous acini react with an antibody to a mucin (Muc19) of the rat major sublingual gland, but in some of the glands the reaction varies in intensity among the acinar cells. Ultrastructurally, the mucous secretory granules of the anterior buccal, glossopalatal, palatal and Weber's glands are biphasic, while those of the minor sublingual and posterior buccal glands are monophasic. Although there is a considerable body of literature concerning the development, innervation, physiology and proteomics of von Ebner's glands, investigation of the other minor salivary glands of the rat ranges from modest to nearly nonexistent.     

Rapid changes in weight and growth potential during childhood

The close resemblance between the skin of Goeldi's marmoset (Callimico goeldii) and that of the genus Saguinus (Hoffmannsegg) suggests that C. goeldii be placed in the family Callithricidae (Thomas, '03) as originally proposed by Pocock in 1920 and not in the family Cebidae (Swainson, 1835). Recent karyological evidence supports this point of view. The skin is characterized by (1) a melanin-laden epidermis and aggregates of melanocytes in the upper dermis; (2) nonglandular skin in the gular region distinguished by a sparsely haired, pebbly, granular surface; (3) cholinesterase-positive Meissner corpuscles and papillary nerve end-organs; (4) groups of 3 to 5 hair follicles in linear perfect sets; (5) sinus hairs on the ventral ulnar wrist; (6) manubrial, sternal, genitopubic, and circumanal sebaceous-apocrine glandular concentrations rich in phosphorylase and alkaline phosphatase; (7) eccrine glands, restricted to volar friction surfaces, whose clear and dark secretory cells contain phosphorylase but no glycogen; and (8) eccrine glomeruli surrounded by many acetyl- but few butyrylcholinesterase-reactive nerves.     

Kallikrein-like activity in salivary glands using a new tripeptide substrate, including preliminary secretory studies and observations on mast cells

Summary The tripeptide substrated-val-leu-arg-4-methoxy-2-naphthylamine gave a precise localization of reaction product in cryostat sections of aldehyde-fixed salivary glands from a number of species, with Fast Blue B as the capture reagent. In submandibular glands, there was strong staining of the granules in granular tubules of rats and hamsters and somewhat less in mice. Submandibular striated ducts showed variable periluminal staining in a finer granular form; it was abundant in guinea-pigs, strong in cats but somewhat less pronounced in dogs. Parotid glands contained less reactivity with none detectable in hamsters and guinea-pigs. In the rabbit, neither gland showed any reaction. Mast cells were densely stained in glands from cats and dogs; they were less reactive in rats and unstained in the other species.The closely related 7-amino-4-trifluoromethylcoumarin derivative of the tripeptide has been found highly satisfactory for assessing activity in submandibular saliva from cats. Preliminary functional studies indicate that an extensive rapid secretion of enzyme occurs into saliva on sympathetic stimulation, with a corresponding depletion of reactive material from the striated ducts in tissue sections. Far less mobilization of enzyme occurs into saliva on parasympathetic stimulation with no obvious change in the histochemical reaction of striated ducts. The possible significance of these findings in cats is discussed.Extensive qualitative and quantitative studies are required to evaluate enzyme and substrate specificities in each species. Nevertheless, derivatives ofd-val-leu-arg offer great promise for the functional testing of kallikrein-like reactivity both by histochemical means on cells and biochemically in their secretions.     

Two atavistic characters of some Lumbriculidae and their importance for the classification of Oligochaeta

The rudimentary atria, and the posterior sperm funnels and sperm ducts, which occur in some species of the Lumbriculidae, are discussed. It is shown that the posterior location of funnels and sperm ducts is the result of a forward shift of the atria, which refutes Stephenson's supposition that the Lumbriculidae is the most archaic family of the present-day Oligochaeta.     

Ultrastructure of bovine parotid glands

Bovine parotid glands exhibit outstanding structural differences when compared with those of non-ruminant mammals. The acini are tortuous, branched and lined with cells of different heights, imparting a scalloped appearance to acinar lumina. Numerous microvilli, ca. 1.5 μ in length, extend into the lumina and intercellular canaliculi. Intercellular canaliculi measure ca. 3 μ in diameter and interweave in close association with intercellular tissue spaces. Intercellular tissue spaces are separated from the extraacinar spaces across a basal lamina only, whereas junctional complexes guard canaliculi from direct continuity with tissue spaces and/or extraacinar spaces. Flattened cytoplasmic lamellae extend from adjacent acinar cells and loosely interdigitate with one another across the tissue spaces. Acinar cells contain more mitochondria and less granular endoplasmic reticulum than parotid glands of non-ruminant mammals. Two types of secretory material, in the form of inclusions which vary in size and electron density, are present in the acinar cells. Intercalated ducts connect acini with striated ducts which in turn, empty into collecting ducts located between gland lobules. In terms of frequency of “basal infoldings” and numbers of mitochondria, striated ducts of calf parotid glands are not as well developed as those of certain other salivary glands. Myoepithelial cells are most often present at junctions of acini and intercalated ducts where they may attach to both acinar and ductal epithelium. Nerve “terminals” were not observed on the epithelial side of basement membranes in relation to the secretory cells.     

Morphologic diversity of the minor salivary glands of the rat: fertile ground for studies in gene function and proteomics

In this article the locations and histologic and ultrastructural features of all of the minor salivary glands of the rat are presented; similarities and differences among them are highlighted. These glands are almost as diverse morphologically as the major salivary glands of the rat. The acini of von Ebner's glands are serous; those of the anterior and posterior buccal glands and minor sublingual glands are mucous; and those of the glossopalatal, palatal, and Weber's glands are mucous with serous demilunes. The anterior buccal, minor sublingual and von Ebner's glands have striated and stratified columnar ducts, while only the minor sublingual and von Ebner's glands have intercalated ducts. The glossopalatal, palatal, posterior buccal and Weber's glands have none of these ducts; the tubulo-acini drain abruptly into short terminal ducts composed of stratified squamous epithelium. All of the mucous acini react with an antibody to a mucin (Muc19) of the rat major sublingual gland, but in some of the glands the reaction varies in intensity among the acinar cells. Ultrastructurally, the mucous secretory granules of the anterior buccal, glossopalatal, palatal and Weber's glands are biphasic, while those of the minor sublingual and posterior buccal glands are monophasic. Although there is a considerable body of literature concerning the development, innervation, physiology and proteomics of von Ebner's glands, investigation of the other minor salivary glands of the rat ranges from modest to nearly nonexistent.     

Occurrence and morphometry of the hypopharyngeal glands inScaptotrigona postica Lat. (Hymenoptera, Apidae, Meliponinae)

As compared toApis mellifera where only workers have hypopharyngeal glands, inScaptotrigona postica, these glands occur in workers, queens and males. They are composed of two long axial ducts with many unicellular secretory alveoli interconnected by secretory canaliculi. The axial ducts are longer in males than in workers, but the alveolar areas of queens and males are generally smaller. In workers the alveoli have their greatest size in the nurses or middle-aged individuals while in queens and males they are larger in newly emerged individuals. The results indicate that the glands in workers may produce food for the brood as inA. mellifera, since they are well developed in the nurse workers. However, the function of the glands in queens and males remains to be clarified since these individuals have no part in brood care.     

The anatomy of the circumgenital scent gland of Saguinus fuscicollis (Callitrichidae, Primates)

In the adult male Saguinus fuscicollis , the scrotal skin and the area above the root of the penis are raised in a sharply defined cushion, which extends cranially into a rectangular suprapubic pad. The circumgenital area of the adult female resembles that of the male, except that the suprapubic pad is relatively and absolutely larger. A complex glandular organ, composed of holocrine and apocrine glands, is located beneath the epidermis of the circumgenital skin. In males, specialized holocrine glands associated with hair follicles predominate. They form a layer, 2-3 mm deep beneath the epidermis. These holocrine glands have a complex alveolar structure and possess numerously branched excretory ducts. Each group of glands empties into a common duct which enters the hair follicle. In males, the apocrine glands are located predominantly at the periphery of the glandular pad and between the scrotal and perineal areas. The excretory ducts of most apocrine glands empty on to the skin surface in close spatial association with hair follicles. However, independent openings were also observed. In females, the specialized holocrine glands resemble those of males but are more frequently interspersed with apocrine glands. The apocrine glands are larger and much more numerous than in males, especially in the region of the labia majora. Gonadectomy of an adult male and female resulted in a reduction in the size of the holocrine glands but had much less effect on the apocrine glands of the scent organ. In addition, the sexual dimorphism in gland histology was retained years after castration.     

Microscopic observations of skin and lymphoid organs in the hairless dog derived from the Mexican hairless

The skin and lymphoid organs of Mexican hairless dogs and their hairless offspring were examined histologically. The hairless dogs lacked most hairs except for sparse hairs on the head, tail and feet. The skin of newborn pups consisted of a thick epidermis with epidermal ingrowths forming the rudiments of hair follicles. In older dogs more than 2 months of age, however, the epidermis was thin and the ingrowths were few. Neither hair follicles nor skin glands were present. The hairy skin of the head and tail had hair follicles with sebaceous glands. Regarding the lymphoid organs, the newborn pups possessed a thymus like haired pups. But in the older dogs more than 2 months of age, the thymus was atrophied and the lymphocyte population was too sparse to demarcate the cortex and the medulla. Lymphocyte accumulation in older dogs was also poor in the spleen and mesenteric lymph nodes. The present findings indicate that the hairlessness of the Mexican hairless dogs and their descendants is accompanied by early atrophy of the thymus after birth, and is followed by poor accumulation of lymphocytes in the thymus-dependent area of the spleen and the mesenteric lymph nodes. The defect of the thymus in the hairless dog seems to be different from that in athymic nude mice and rats. Further studies are needed to elucidate the immunological response and function in hairless dogs.