The caudal neurosecretory system

Summary Recent information on the caudal neurosecretory system (urophysis) is collated, with special reference to cellular biology including neural relations, activity and chemistry of the biological principles associated with the urophysis, pharmacological analysis of the receptors for these principles, and their possible functions in a physiological sense. The existence of at least two principles, urotensins I and II, is well established. They differ pharmacologically and chemically and may arise from different cell types. At present, osmoregulation, cardiovascular regulation and reproduction are the most likely aspects of organismal physiology wherein these principles may be involved.Dedicated to Professor Doctor Berta Scharrer on the occasion of her seventieth birthday, with profound admiration and affection     

Brain stem innervation of the caudal neurosecretory system

Summary The innervation of the caudal neurosecretory system of Poecilia sphenops (black molly) was studied by use of the retrograde horseradish peroxidase (HRP) method. The structure of the caudal neurosecretory system in this species was well suited for application of HRP procedures. Acrylamide/HRP gel implants were placed in the nucleus of the caudal neurosecretory system. Two neuronal groups which contained HRP filled cells were found in the brain stem. Bilateral projections originate from the dorsal tegmentum of the midbrain and the reticular nucleus of the medulla.Supported by PHS 5429-19-4 and BNS 8206452The authors wish to thank Drs. R. Parsons, S. Freedman and J. Wells for reading this report and A. Angel for photographic assistance     

The caudal neurosecretory system of the teleostean Clupea melanostoma

Summary The caudal neurosecretory system of Clupea melanostoma is described. The urophyseal area in this species is merely a spinal cord enlargement divided into two distinct zones: a ventral and ventrolateral vascular zone where neurosecretory material is concentrated, and a dorsal cell-rich area where the perikarya of the neurosecretory cells are found.The hypothesis is advanced that the first-named vascular area has developed into the more differentiated urophysis of the less primitive teleosts while the dorsal cell-rich area has become part of the filum terminale. Two main types of neurosecretory cells are described.This work was supported by grant L 96 Z from the Consejo Nacional de Investigaciones Cientificas y Técnicas.     

The fine structure of the caudal neurosecretory system in Raia batis

Summary The fine structure of the caudal neurosecretory system in Raia batis was studied. Far-reaching similarities with ultrastructural details of other vertebrate neurosecretory systems were noted. The secretion is present in all parts of the system in the form of elementary neurosecretory granules which seem to be formed in the Golgi complex of the cell body. The morphology of the terminal region is discussed in relation to the possible mode of secretion release and in connection with the routes of secretion to the vascular lumen.The Dahlgren cell is not considered to be a secretory neuron, but a specialized glandular cell type, which has, to some extent, the same properties as nerve cells.Aided by grants from the Swedish Natural Science Research Council.     

Nitric oxide and neuromodulation in the caudal neurosecretory system of teleosts

Although evidence exists that nitric oxide (NO) mediates neuroendocrine secretion in mammals, the involvement of NO in the neuroendocrine regulation of non-mammalian vertebrates has yet to be investigated in detail. The present review conveys several recent data, suggesting that NO plays a modulatory role in the caudal neurosecretory system (CNSS) of teleosts. The presence and distribution of neuronal NO synthase (nNOS) was demonstrated in the CNSS of the Nile tilapia Oreochromis niloticus by means of NADPHd histochemistry, NOS immunohistochemistry, NOS immunogold electron microscopy, the citrulline assay for NOS activity and Western blot analysis. NO production by the caudal spinal cord homogenates was also evaluated by the oxyhemoglobin assay. On the whole, these findings indicate that caudal neurosecretory cells express NOS enzymes and presumably produce NO as a cotransmitter. Moreover, the comparison of the nNOS distribution with that of urotensins I and II (UI and UII) suggests that neurosecretory Dahlgren cells belong to two different functional subpopulations: a population of UI/UII secreting nitrergic neurons and a population of non-nitrergic neurons, which principally secrete UII. These results implicate NO as a putative modulator of the release of urotensins from the neurosecretory axon terminals. Therefore, like in mammals, NO appears to influence neuroendocrine secretion in teleosts.     

Immunoreactive methionine-enkephalin in the caudal neurosecretory system of the carp,Cyprinus carpio

Summary Methionine-enkephalin (Met-enk) was detected by immunocytochemistry and radioimmunoassay in the caudal neuro-secretory system of the carp Cyprinus carpio. Some cells showing urotensin I (UI)-immunoreactivity reacted to Met-enk antiserum, but others did not. Neurons with urotensin II (UII)-immunoreactivity did not react to Met-enk antiserum; neurons with both UI and UII immunoreactivities also displayed a negative Met-enk reaction. Met-enk was detected by radioimmunoassay in the urophysis, although the content was relatively small compared with that found in other parts of the central nervous system and in the pituitary.     

Urotensin II-immunoreactive neurons in the caudal neurosecretory system of freshwater and seawater fish

Summary Antiserum generated against synthetic urotensin II of the goby, Gillichthys mirabilis, was used to localize urotensin II in the caudal neurosecretory system in six species of freshwater teleosts; Cyprinus carpio, Carassius auratus, Oreochromis mossambicus, Oreochromis niloticus, Salmo gairdneri and Plecoglossus altivelis, and six species of seawater teleosts: Acanthogobius flavimanus, Pagrus major, Paapristipoma trilineatum, Trachurus japonicus, Seriola dumerili and Seriola quinqueradiata. In the carp, urotensin II-immunoreactive perikarya were classified into three groups according to their size and shape. Small cells were located in the spinal cord dorsal to the urophysis, medium-sized cells immediately anterior to the urophysis, and large cells anterior to the medium-sized cells. In each group, a small number of nonreactive cells was found. Urotensin II-immunoreactive nerve fibers extended toward the urophysis and terminated around the blood vessels. Other species of teleosts showed a similar immunoreaction to that observed in the carp. The immunoreaction of the urophysis was stronger in seawater fish than freshwater fish. Urotensin II-immunoreactive elements could not be detected in the brains of the carp, goldfish and goby.     

Cortisol and prolactin modulation of caudal neurosecretory system activity in the euryhaline flounder Platichthys flesus

Previous studies have shown roles for cortisol and prolactin in osmoregulatory adaptation to seawater and freshwater, respectively, in euryhaline fish. This study of the European flounder investigated the potential for these hormones to modulate activity of the caudal neurosecretory system (CNSS), which is thought to be involved in physiological adaptation to changing external salinity. Superfusion of isolated CNSS with either cortisol or prolactin (10 microM; 15 min) led to changes in firing activity in neuroendocrine Dahlgren cells, recorded extracellularly. Cortisol evoked a modest increase in overall firing activity, with the response delayed by 4 h after treatment. The response to prolactin was short latency, continued to build up over the subsequent 4-h wash period, and comprised increased firing activity together with recruitment of previously silent Dahlgren cells. Immunoreactivity for glucocorticoid and prolactin receptors was localised to Dahlgren cells. The CNSS expression level for glucocorticoid-2 receptor mRNA, measured by Q-PCR, was significantly lower in fish fully acclimated to freshwater, compared to seawater. No differences were seen between these two states for prolactin receptor mRNA expression. These results provide evidence for a modulatory action of both hormones on the neurosecretory function of the CNSS.     

The caudal neurosecretory system: control and function of a novel neuroendocrine system in fish.

The caudal neurosecretory system (CNSS) of fish was first defined over 70 years ago yet despite much investigation, a clear physiological role has yet to be elucidated. Although the CNSS structure is as yet thought to be confined to piscine species, the secreted peptides, urotensins I and II (UI and UII), have been detected in a number of vertebrate species, most recently illustrated by the isolation of UII in humans. The apparent importance of these peptides, suggested by their relative phylogenetic conservation, is further supported by the complex control mechanisms associated with their secretion. The CNSS in teleosts is known to receive extensive and diverse innervation from the higher central nervous system, with evidence for the presence of cholinergic, noradrenergic, serotonergic, and peptidergic descending inputs. Recent observations also suggest the presence of glucocorticoid receptors in the flounder CNSS, supporting previous evidence for a possible role as a pituitary-independent mechanism controlling cortisol secretion. The most convincing evidence as to a physiological role for the CNSS in fish has stemmed from the direct and indirect influence of the urotensins on osmoregulatory function. Recent advances allowing the measurement of circulating levels of UII in the flounder have supported this. In addition, there is evidence to suggest some seasonal variation in peptide levels supporting the notion that the CNSS may have an integrative role in the control of coordinated changes in the reproductive, osmoregulatory and nutritional systems of migratory euryhaline species.     

A histoenzymological investigation of the caudal neurosecretory system in six species of freshwater teleosts: a comparative study

Enzymecytochemical features of the caudal neurosecretory system of 6 species of freshwater teleosts, Gudusia chapra, Gonialosa manmina (Clupeidae, Clupeiformes), Oxygaster bacaila (Cyprinidae, Cypriniformes), Mystus bleekeri (Bagridae, Cypriniformes), Sciaena coiter (Scienidae, Perciformes), and Mastacembelus pancalus (Mastacembelidae, Mastacembeliformes) have been investigated with the help of several specific histochemical techniques. No sex-dependent variation have been observed in the enzymecytochemical characteristics of the caudal neurosecretory system of the present species. The Dahlgren cells show intense RNA activity. Caudal neurosecretion lacks carbohydrate but seems to possess small amount of lipid. Acid-phosphatase is located in the Dahlgren cells and axons. Alkaline-phosphatase has been observed in the Dahlgren cells, axons, and urophysial blood-capillaries. Acetylcholine esterase is present in the Dahlgren cells, axons, and urophysis of Mystus, Mastacembelus, and Gonialosa, but lacking in the other 3 species. It is concluded that the caudal neurosecretory system of Mystus, Mastacembelus, and Gopialosa is innervated by cholinergic neurons. Despite their different taxonomic positions, caudal neurosecretory system of all 6 species produce similar responses to various enzymecytochemical tests, except for acetylcholine esterase.     

Differential effects of low pH and aluminium on the caudal neurosecretory system of the brook trout, Salvelinus fontinalis

Brook trout were subjected to soft water at pH 6·5, 5·5 or 5·0 without aluminium added, or to water at pH 5·5 with 200,300 or 500 μg Al I^-1 added. The response of the caudal neurosecretory system to low pH or aluminium was evaluated after one week by measuring the urotensin I and urotensin II concentrations in the urophysis by radioimmunoassay, and by morphometric analysis of the caudal neurosecretory cells. A positive correlation was found between urotensin I concentrations and acidity, and a negative correlation was found between urotensin II concentrations and total aluminium in the water. Morphometric indices (cell size and proportion of lobed nuclei in the caudal neurosecretory cells) suggested increased synthetic activity in the caudal neurosecretory cells of fish at pH 5·5 compared to pH 6·5.     

Immunocytochemical localization of urotensin I neurons in the caudal neurosecretory system of the white sucker (Catostomus commersoni)

Summary The localization of urotensin I has been investigated in the caudal neurosecretory system of the white sucker (Catostomus commersoni). The peptide is present in all the cells of the system both large and small, in the large axons passing to the urophysis, and in fine beaded fibres not only within the urophysis but also in a fine plexus lateral to the large cells in the spinal cord proper. The possibility that the caudal neurosecretory system is not a functionally uniform system but rather a collection of dissimilar cells of different synaptic inputs with a common entity, urotensin I, is discussed. Moreover, the feasibility of a urotensin I feedback loop is described.Financial support for this investigation was provided in part by MRC (Canada). K.L. is MRC career investigator; K.L.W, was in receipt of an Alberta Heritage Foundation for Medical Research Fellowship. It is a pleasure to record the valuable technical assistance of Mrs. W. Ho and the dedicated assistance in the collection of the experimental animals by Mrs. Helen Wilson of Nanton, Alberta.     

Development of the caudal neurosecretory system of the nile tilapia Oreochromis niloticus: an immunohistochemical and electron microscopic study

The development of the caudal neurosecretory system (CNSS) of the Nile tilapia, Oreochromis niloticus, has been investigated by means of UI/oCRF (urotensin I/ovine corticotropin-releasing factor) immunohistochemistry and transmission electron microscopy. UI-like immunoreactive perikarya and fibers are first detected in the caudal spinal cord of larval fish about 4 days after hatching (stage 21). In the region of the future urophysis two bundles of strongly immunoreactive neurosecretory fibers are observed. At this stage, neurosecretory axons terminate on the meninx sheath of the spinal cord with immature neurosecretory terminals. The histogenesis of the urophysis begins at stage 24. The future neurohemal organ consists of a small ventral swelling of the spinal cord, which is associated with dilated vessels. At this stage, neurosecretory axons terminate on the basal lamina of the ingrowing blood vessels. Further development occurs by means of progressive branching of vessels and the concomitant increase in the number of neurosecretory terminals. In the caudal spinal cord, immunoreactive neurons also increase in number and progressively differentiate morphologically. Typical features of the mature CNSS are recognizable in 4-month-old juveniles. Data suggest that in tilapia both the synthesis and the release of urophysial hormones begin before morphogenesis of the neurohemal organ takes place.