Unpaired Ultimobranchial Glands of the African Lungfish, Protopterus dolloi

The ultimobranchial glands of juvenile African lungfish (Protopterus dolloi) (14 individuals; total body length 25-205 mm) were immunohistochemically examined. In individuals larger than 36 mm, one ultimobranchial gland was close to the left afferent branchial arteries. The topography of the ultimobranchial gland was similar to that of salamanders and sharks, but not to teleosts. With body growth, the ultimobranchial gland was vascularized and the parenchymal cells were gradually immunostained with anti-calcitonin antibody. In all individuals examined, the ultimobranchial gland existed only on the left side of the pharynx. These observations are discussed from a phylogenetic viewpoint.     

Innervation of the C cells of chicken ultimobranchial glands studied by immunohistochemistry, fluorescence microscopy, and electron microscopy

Innervation of the ultimobranchial glands in the chicken was investigated by immunohistochemistry, fluorescence microscopy and electron microscopy. The nerve fibers distributed in ultimobranchial glands were clearly visualized by immunoperoxidase staining with antiserum to neurofilament triplet proteins (200K-, 150K- and 68K-dalton) extracted from chicken peripheral nerves. The ultimobranchial glands received numerous nerve fibers originating from both the recurrent laryngeal nerves and direct vagal branches. The left and right sides of the ultimobranchial region were asymmetrical. The left ultimobranchial gland had intimate contact with the vagus nerve trunk, especially with the distal vagal ganglion, but was somewhat separated from the recurrent nerve. The right gland touched the recurrent nerve, the medial edge being frequently penetrated by the nerve, but the gland was separated from the vagal trunk. The left gland was innervated mainly by the branches from the distal vagal ganglion, whereas the right gland received mostly the branches from the recurrent nerve. The carotid body was located cranially near to the ultimobranchial gland. Large nerve bundles in the ultimobranchial gland ran toward and entered into the carotid body. By fluorescence microscopy, nerve fibers in ultimobranchial glands were observed associated with blood vessels. Only a few fluorescent nerve fibers were present in close proximity to C cell groups; the C cells of ultimobranchial glands may receive very few adrenergic sympathetic fibers. By electron microscopy, numerous axons ensheathed with Schwann cell cytoplasm were in close contact with the surfaces of C cells. In addition, naked axons regarded as axon terminals or "en passant" synapses came into direct contact with C cells. The morphology of these axon terminals and synaptic endings suggest that ultimobranchial C cells of chickens are supplied mainly with cholinergic efferent type fibers. In the region where large nerve bundles and complex ramifications of nerve fibers were present, Schwann cell perikarya investing the axons were closely juxtaposed with C cells; long cytoplasmic processes of Schwann cells encompassed large portions of the cell surface. All of these features suggest that C-cell activity, i.e., secretion of hormones and catecholamines, may be regulated by nerve stimuli.     

Analysis of salmon calcitonin I in the ultimobranchial gland and gill filaments during development of rainbow trout, Oncorhynchus mykiss, by in situ hybridization and immunohistochemical staining

We have cloned two distinct cDNAs encoding salmon-type calcitonin (sCT)-I cDNAs from the ultimobranchial gland of rainbow trout, Oncorhynchus mykiss. Both cDNAs were predicted to encode nearly identical sCT-I precursors which consisted of an N-terminal peptide of 80 amino acid residues, a putative cleavage site Lys-Arg, sCT-I, a cleavage and amidation sequence Gly-Lys-Lys-Arg, and a C-terminal peptide of 18 amino acids. Development of sCT-I-expressing cells was then examined by employing conventional histochemical staining, in situ hybridization with a specific cRNA probe, and further immunohistochemistry. The primordium of the ultimobranchial gland was first identified, as two cell masses, in the region between the alimentary canal and sinus venosus behind the heart 17 days postfertilization (dpf; 14 degrees C). However, expression of sCT-I mRNA could not be detected in this gland until one day later, and appeared at 18 dpf. sCT-I immunoreactivity was first observed at 19 dpf (two days before hatching), and the ultimobranchial gland began to assume a follicular structure at 20 dpf (one days before hatching). As ontogeny proceeded, the sCT-I-immunoreactive cells increased in both number and stainability. The sCT-I mRNA was also expressed on the developing gill filaments, but immunoreactive sCT-I was not detected in these sites. These results provide basic data for further research on the organogenesis of the trout ultimobranchial gland.     

Expression and localization of prohormone convertase PC1 in the calcitonin-producing cells of the bullfrog ultimobranchial gland.

We examined the expression and localization of the prohormone convertases, PC1 and PC2, in the ultimobranchial gland of the adult bullfrog using immunohistochemical (IHC) and in situ hybridization (ISH) techniques. In the ultimobranchial gland, PC1-immunoreactive cells were columnar, and were present in the follicular epithelium. When serial sections were immunostained with anti-calcitonin, anti-CGRP, anti-PC1, and anti-PC2 sera, PC1 was found only in the calcitonin/CGRP-producing cells. No PC2-immunopositive cells were detected. In the ISH, PC1 mRNA-positive cells were detected in the follicle cells in the ultimobranchial gland. No PC2 mRNA-positive cells were detected. RT-PCR revealed expression of the mRNAs of PC1 and the PC2 in the ultimobranchial gland. However, very little of the PC2 mRNA is probably translated because no PC2 protein was detected either by IHC staining or by Western blotting analysis. We conclude that the main prohormone convertase that is involved in the proteolytic cleavage of procalcitonin in the bullfrog is PC1.     

Position of ultimobranchial body cysts in the human fetal thyroid gland

In a series of 21 human fetal thyroid glands examined histologically in serial sections, seven ultimobranchial body cysts were found. The position of these cysts correlated well with the distribution of calcitonin-containing cells found by previous investigators in the adult thyroid gland. Ultimobranchial body cysts found external to the thyroid lobes may offer a developmental explanation for the paucity of calcitonin found in some adult thyroid glands. The close developmental relationship between the parathyroid gland and the ultimobranchial body could explain the presence of calcitonin found in these glands in some adults.     

The fine structure of the vesicular component of the ultimobranchial gland of the domestic fowl

Summary The ultrastructure of the polymorphic vesicular component of the ultimobranchial gland of the domestic fowl (Gallus gallus domesticus) has been described in detail, together with the structure of the cell strands interconnecting the vesicles and the parathyroid nodules lying within the ultimobranchial stroma. The vesicles frequently appear to arise from the nodules by way of the cell strands. The strands show a structure of their component cells intermediate between that of the parathyroid and the vesicular cells, although the position at which the strand changes from an essentially parathyroid structure to an essentially vesicular structure is very variable. The degree and kind of secretory activity within different cell types has been described. A review of the structure of ultimobranchial glands throughout the vertebrates shows that similar tissue with a similar secretory potential has been observed in all vertebrate classes, suggesting a functional significance for this part of the gland.     

Morphological and histochemical changes of ultimobranchial follicles of the rat thyroid in the course of postnatal life.

Morphological and histochemical changes of ultimobranchial follicles of thyroid have been investigated in rats from newborn to 18 months of age. The first well-delimited ultimobranchial follicles, though with no lumen, were detected in the thyroid gland of 10-day-old rats. At 30 days of age, follicles possessing regular lumina were present in the thyroid. With age, the follicles gradually increased in volume assuming extreme dimensions in adult age. The follicles displayed varying shapes from simple cysts to bizarre forms. From the age of 50 days the cells of the follicular wall are separated from the cell debris contained in the lumen. The latter gave a PAS positive reaction. The cells of the ultimobranchial follicles did not exhibit argyrophilia and metachromasia showing that they differ considerably from the C-cells likewise of ultimobranchial origin, which are known to give marked argyrophilic and metachromatic reactions.     

Origin of cholinesterase-containing follicle cells and parafollicular cells of the developing thyroid gland in the rat

Summary The location of cholinesterase-containing cells in the thyroid gland and its precursors (median thyroid primordium and ultimobranchial bodies) has been investigated light-microscopically in rat embryos from the 13 to the 20th day of gestation.From the 13th to the 16th day of gestation the median thyroid primordium and the ultimobranchial bodies are distinct from each other. Cholinesterase-containing cells are found in both. On the 17th–18th day of gestation the reacting ultimobranchial cells spread into the median thyroid primordium where they take up a parafollicular position. At the 19th–20th day of gestation the distribution of cholinesterase-containing cells is as in the adult rat. The results seem to show that cholinesterase-containing follicular cells derive from the median thyroid primordium and cholinesterase-containing parafollicular cells from the ultimobranchial body.     

Circannual rhythms in the activity of the parathyroid gland and ultimobranchial body cells of the frog Rana temporaria (Anura, Amphibia)

The annual activity of the parathyroid gland cells and those of the ultimobranchial body cells of the frog Rana temporaria is quantitatively investigated by a morphometric study. A cosinor analysis shows a periodic succession of different parameters. The secretory activity of the parathyroid cells starts after a maximal value of external temperature in July. This activity is followed by an increase of plasma calcium which seems to induce the activity of the ultimobranchial cells.     

Embryonic induction and development of the ultimobranchial body in the embryogenesis of amphibia

At early embryonal and larval stages of development 7 species of amphibia have been studied. The ultimobranchial anlage and processes resulted in formation of the secretory follicle are investigated. Dynamics on changes of amount of the gland cells and the first appearance of capillaries are analyzed. In Anura and Urodela the anlage of the ultimobranchial gland develops from the epithelial lining of the pharynx behind the last branchial pocket rudiment. The gland is asymmetric and can be laid either in the right or in the left side of the body. Death of calcitonin-secreting cells is compensated at the expense of repeated anlage of follicles from the pharyngeal epithelium. The newly formed follicles can either incorporate into the existing gland, or form independent follicles. For amphibia formation of the capillary network around the gland after beginning of the follicular secretion is specific. Owing to these data, it is possible to conclude that the stimulus for the gland to become overgrown with capillaries is the beginning of calcitonin secretion.     

Effect of induced hypercalcemia on ultimobranchial gland of the lizard, Calotes versicolor.

The ultimobranchial of the lizard Calotes consists of parenchymal patches and several follicles. After induced hypercalcemia, the gland became more active suggesting the hypocalcemic secretion from the gland.     

Effect of a calcium rich environment on the ultimobranchial gland of Rana tigrina.

Thirty two specimens of Rana tigrina were divided into four equal groups : group I = controls; group II = injected with Vitamin D2 and placed in a 0.8% aqueous solution of CaCl2; group III = injected with Vitamin D2 and kept in tap water; group IV = placed only in a 0.8% CaCl2 solution. The experimental specimens exhibited varying degrees of hyperactivity of their ultimobranchial gland. Specimens from all the groups were X-rayed. The experimental ones showed different intensity of calcium deposit in their paravertebral lime sacs. The results indicate that prolonged challenge of high calcium induces hyperactivity of the ultimobranchial gland to produce larger quantity of calcitonin, to counteract the experimental hypercalcemia.     

Structure and behaviour of ultimobranchial gland in response to vitamin D3--induced hypercalcemia in male Clarias batrachus

Hypercalcemia was induced in Clarias batrachus by treating them with vitamin D3 (5,000 I.U./100 g body wt.) and/or 0.5% solution of CaCl2. The animals were killed on 1st, 3rd, 5th, 9th, 13th and 17th days after the initiation of the experiment. Histological preparations of the ultimobranchial gland (UBG) were made. The gland exhibits nuclear hypertrophy, hyperplasia and loss of staining response corresponding to the rise in serum calcium levels. At later intervals, the UBG shows exhaustion and degeneration which is evident from vacuolization and nuclear shrinkage of the ultimobranchial cells after day 13 in groups B and C and day 9 in group D.     

Observations on the fine structure,enzyme histochemistry,and innervation of parathyroid gland and ultimobranchial body of Chthonerpeton indistinctum (Gymnophiona,Amphibia)

Summary Fine structural and enzyme histochemical observations on ultimobranchial body and parathyroid gland of the caecilian Chthonerpeton are presented. The cell clusters and follicles of the ultimobranchial body consist mainly of granulated cells which are termed C-cells and obviously belong to the APUD cell series. In the larger follicles additional possibly exhausted degranulated cells and replacement cells occur. A rich supply of nerve fibres has been found in this gland. Frequently nerve terminals were observed to come into synaptic contact with the C-cells. Two categories of nerve fibres occur: a) fibres containing large polymorphic electron dense granules (probably purinergic fibres), b) fibres containing small electron transparent vesicles and a few electron dense granules (probably cholinergic fibres). The parathyroid gland consists of elongated cells (one cell type) poor in organelles and often containing fields of glycogen and lipid droplets. The cells are further characterized by fair amounts of lysosomal enzymes; they are interconnected by maculae adhaerentes and occludentes. No nerves and blood vessels have been found in the parathyroid gland of Chthonerpeton. This study has been supported by the Deutsche Forschungsgemeinschaft We 380/5.     

Cilia-forming potentials of endocrine organs originating from the foregut.

Cilia were found in intracellular localizations or on the surface of certain cells of frog thymus and chicken parathyroid gland and ultimobranchial body. The experimental observations suggest that ciliogenesis is probably a general property of branchiogenic epithelium, which either persists, or can be activated by certain influences after the functional differentiation of endocrine organs arising from the foregut.     

Pulmonary immunoreactive calcitonin in the African green monkey (Cercopithecus aethiops): Anatomic distribution

The hormone calcitonin, which occurs predominantly within the C cells of the mammalian thyroid gland, is also found within the pulmonary endocrine cells of the epithelium of the tracheobronchial tree. A study was made of the distribution of immunoreactive calcitonin (iCT) in the African green monkey. Using two different region-specific antisera, the total respiratory iCT comprised 2.5% and 5.8% of the total thyroid iCT. The mean concentration of iCT in the right lung exceeded that in the left, and the mean concentration of the right middle or right upper lobe exceeded that of all other lobes. Embryologically, the ultimobranchial bodies contribute their iCT-producing C cell primordia to the thyroid gland near the level of the primitive laryngotracheal cleft and shortly after the early arborization of the bronchial tree. In monkeys and most other mammals, the right main stem bronchus is larger and develops earlier than the left. The data suggest an early migration of cells from the ultimobranchial bodies to the bronchi, eventually giving rise to the iCT-containing pulmonary endocrine cells.     

Ultimobranchial gland of the domestic fowl

Summary The ultimobranchial gland (UBG) of birds is particularly rich in calcitonin, the hypocalcaemic hypophosphataemic hormone, that is secreted by the C-cells of the mammalian thyroid. The principal cells of the UBG have a striking resemblance with the mammalian C-cells, i.e., they possess small intracytoplasmic dense-core secretory granules, 150–300 nm in diameter. The gland also contains a second, morphologically distinct, endocrine cell type with larger granules, 500–800 nm in diameter. A sensitive immunocytochemical reaction was developed with the use of antibodies against salmon calcitonin. By means of this technique the presence of calcitonin-immunoreactive molecules was demonstrated in both secretory cell types of the UB gland of the chicken. This gland can thus be considered as a homogeneous calcitonin-producing tissue. Whether the secretory products are identical is discussed and differences in the secretory pathways are suggested.     

The ultimobranchial gland of the dogfishScyliorhinus canicula L. immunofluorescence cross-reactivities with anti-sera to different calcitonins

Summary Calcitonin in the ultimobranchial gland of the dogfishScyliorhinus canicula cross-reacts with anti-dogfish, anti-salmon and anti-porcine calcitonin, but not with anti-human calcitonin, using indirect immunofluorescence procedures. These results do not reflect completely expectations derived from the primary structures of the hormones, where known, and from their physiological interrelationships.     

Direct raises in blood Ca levels by infusing a high-Ca solution into the blood stream accelerate the secretion of calcitonin from the ultimobranchial gland in eels

In eels, a CaCl(2) solution was infused into the pneumatic duct vein. Plasma Ca levels were significantly increased during 3 hr and were followed by significant raises in plasma calcitonin levels. These results strongly suggest that, in eels, direct raises in blood Ca levels by infusion of a high-Ca solution via blood vessels can accelerate the secretion of calcitonin from the ultimobranchial gland.