Supraependymal Cells Research Articles

The Spinal Ependymal Layer in Health and Disease.

Ependymal cells are epithelial support cells that line the central canal and ventricular cavities of the central nervous system, providing the interface between the cerebrospinal fluid and the parenchyma of the brain and spinal cord. The spinal ependymal layer (SEL) is composed of 3 main cell types: tanycytes, ependymocytes, and cerebrospinal fluid-contacting neurons. A fourth cell type, termed the supraependymal cell, is also occasionally described. Cells of the SEL show restricted proliferative capacity in health but display neural stem cell properties both in vitro and in vivo in various disease states. A growing body of literature is devoted to the regenerative roles of the SEL, particularly in the context of spinal cord injury, where mechanical damage to the spinal cord leads to a significant increase in SEL proliferation. SEL-derived cell progeny migrate to sites of injury within the injured spinal cord parenchyma and contribute primarily to glial scar formation. In additional to their role as endogenous neural stem cells, cells of the SEL may be an important source of cytokines and other cell signaling molecules, such as tumor necrosis factor, heat shock proteins, and various growth factors. The SEL has become of recent interest to neuroscience researchers because of its potential to participate in and respond to diseases affecting the spinal cord (eg, traumatic spinal cord injury) and neurodegenerative disease. The intimate association of the SEL with the cerebrospinal fluid makes intrathecal therapies a viable option, and recent studies highlight the potential promise of treatments that augment SEL responses to disease.

Morphological changes in the mink area postrema during growth and under different stages of sexual activity.

The histological features of the area postrema (AP) of mink brains of both sexes were investigated at different ages and physiological conditions with light and electron microscopy. The mink AP was a twin-winged structure located at the dorsal surface of the medulla oblongata and consisted of neurons, glial cells, and both continuous and fenestrated capillaries enmeshed in a rich neuropil. The ventricular surface of the mink AP was covered by a single layer of tanycytes except at its most caudal part that was covered by a basal membrane derived from the pia mater. Supraependymal cells and intraventricular axons were also a common finding over the apical poles of tanycytes. However, our study demonstrates that the mink AP acquires the above general features at an advanced postnatal time and that, once fully developed, it undergoes morphological changes that can be directly linked to the aging process and sexual activity of the animals.

Lectinhistochemistry and ultrastructure of microglial response to monosodium glutamate-mediated neurotoxicity in the arcuate nucleus.

In this study we describe the most relevant morphological features of the microglial reaction that takes place in the arcuate nucleus (AN) after neurotoxic injury induced by a single subcutaneous injection of monosodium glutamate (MSG) in neonatal rats. The time course of the reaction was evaluated by lectinhistochemistry. Microglial/macrophagic cells were labelled with the lectin obtained from Lycopersicon esculentum and with B4 isolectin from Griffonia simplicifolia. The microglial response was also studied by ultrastructural observations. The histochemical study revealed the presence of few reactive microglial cells at 6 h post-injection. These cells were intensely stained and had a globular morphology but contained no neuronal debris inside them when observed under the electron microscope. At 12 h post-injection, the number of microglial cells had increased and, at the same time, intense phagocytic activity was observed ultrastructurally. The microglial reaction peaked at 24 and 36 h post-injection, when the number of microglial/macrophagic cells was maximum, although the ultrastructural observations showed that at 36 h the amount of debris ingested by macrophages was decreased with respect to animals sacrificed at 24 h. Finally, at 4 days after neurotoxic injection the number and morphology of microglial cells were similar to those observed in the control rats. The ultrastructural study also revealed the existence of microglial cell mitosis in the territory of the AN together with a strong increase in the number of supraependymal cells resembling macrophages in the third ventricle during the lesion. Our data demonstrate that activated microglial cells initially extend throughout the damaged territory, but from 24-36 h onwards they are especially patent in the ventrolateral portions of the AN.

Supraependymal cells and fibers during the early stages of chick rhombencephalic development.

Supraependymal cellular elements are a constant feature in the adult cerebroventricular system. However, there has been no analysis of their distribution and morphology during the embryonic stages of the chick brain. The ultrastructural features of the rhombencephalic luminal surface of chick embryos ranging from stage 10 to 22 were studied with both scanning and transmission electron microscopy. In addition, immunocytochemistry and confocal laser microscopy were used to examine the presence of 68 kD neurofilaments in supraependymal elements. The ultrastructural observations revealed significant morphological differences in the apical cell surface between the cells at rhombomere boundaries and those in the rhombomere bodies. These differences support the idea that the boundary and the body of rhombomeres contain two morphologically distinct cell types. Supraependymal (SE) cells and SE fibers were present in the rhombencephalon of all embryos studied from stage 12 to 22. The cells were bipolar spindle-shaped. The SE fibers showed a characteristic spatial pattern within the rhombencephalon, following a straight course parallel to the rhombomere boundaries. The SE fibers showed varicosities and their endings contained small vesicles. Both SE cells and SE fibers were positive for 68 kD neurofilaments. Their morphology and reactivity for neurofilaments indicate a neuronal function. The constant presence of SE cells and SE fibers on the surface of the developing rhombencephalon, their special pattern and close relationship with the neural tube fluid (NTF) suggest that these supraependymal elements may be involved in a neuronal signalling pathway between different parts of the same rhombomere and also in chemical communication and integration within the ventricular system, linking distant parts of the developing central nervous system by means of NTF.

Fetal ependyma in sheep and goat. A scanning electron microscopy study.

Morphology of the surface of apical membranes of ependymal cells has been studied in the whole ventricular system of the brain in goat and sheep fetuses using a scanning electron microscope. The surface structure of the ependymal lining surface in fetuses of small ruminants is very similar to that in adult animals. Supraependymal cells were found only in the lower part of the third cerebral ventricle in goat fetuses, but not in sheep fetuses. In small ruminants the ependymal surface is already regionally differentiated within the end of the first half of prenatal development. Fetal ependyma of goats and sheep, unlike the adult ependyma, is characterized by a high secretory activity, which is independent of sex or age of fetuses.

Origin, nature, and some functional considerations of intraventricular macrophages, with special reference to the epiplexus cells.

Intraventricular macrophages encompass the supraependymal, free-floating, and epiplexus (Kolmer) cells; the supraependymal cells lie in close apposition to the ventricular ependyma, the epiplexus cells are closely associated with the choroid plexus epithelium, and the free-floating cells are at a variable distance from the epithelial surface. Although the three cell types are regarded as one cellular entity, the epiplexus cells preponderate. On scanning electron microscopy, the epiplexus cells display diverse morphological forms, ranging from round to bipolar to stellate, and bear a variable number of cytoplasmic processes. Transmission electron microscopy shows the presence of large numbers of lysosomes. The phagocytic nature of epiplexus cells is shown by their intense staining for nonspecific esterase and active uptake of tracers, e.g., horseradish peroxidase and rhodamine isothiocynate, administered intravenously or intraperitoneally. The mode of entry of these tracers in the cerebral ventricles is by way of transepithelial transport. In rats, the population of intraventricular macrophages increases steadily after birth until 17 days of age; thereafter, their cell population remains relatively unchanged. The early upsurge is attributed to proliferation of residential cells and/or influx of circulating monocytes/stromal macrophages through the process of "emperipolesis." The immunophenotypic features of intraventricular macrophages are consistent with other mononuclear phagocytes being immunoreactive for OX-42, OX-18, OX-6, and OX-1 and ED1 for the detection of CR3 receptors, MHC class I and II antigens, leucocyte common antigen, and macrophage antigen, respectively. The expression of these antigens is noticeably enhanced following the injection of lipopolysaccharide (LPS) into postnatal rats. Remarkably, the intraventricular macrophages are induced to express MHC class II (Ia) antigen after LPS or interferon-gamma injections. Furthermore, the expression of transferrin receptors as detected with OX-26 is also upregulated after these treatments. Epiplexus cells are also elicited to display a de novo expression of nitric oxide synthase-like immunoreactivity following intracerebral injection of LPS. They also respond vigorously to a single nonpenetrative blast. Results of our series of studies suggest that, besides their primary function as scavenger cells, the intraventricular macrophages partake in possible immunological responses and iron regulation in the ventricular system or the brain as a whole.

Origin, nature, and some functional considerations of intraventricular macrophages, with special reference to the epiplexus cells

Intraventricular macrophages encompass the supraependymal, free-floating, and epiplexus (Kolmer) cells; the supraependymal cells lie in close apposition to the ventricular ependyma, the epiplexus cells are closely associated with the choroid plexus epithelium, and the free-floating cells are at a variable distance from the epithelial surface. Although the three cell types are regarded as one cellular entity, the epiplexus cells preponderate. On scanning electron microscopy, the epiplexus cells display diverse morphological forms, ranging from round to bipolar to stellate, and bear a variable number of cytoplasmic processes. Transmission electron microscopy shows the presence of large numbers of lysosomes. The phagocytic nature of epiplexus cells is shown by their intense staining for nonspecific esterase and active uptake of tracers, e.g., horseradish peroxidase and rhodamine isothiocynate, administered intravenously or intraperitoneally. The mode of entry of these tracers in the cerebral ventricles is by way of transepithelial transport. In rats, the population of intraventricular macrophages increases steadily after birth until 17 days of age; thereafter, their cell population remains relatively unchanged. The early upsurge is attributed to proliferation of residential cells and/or influx of circulating monocytes/stromal macrophages through the process of “emperipolesis.” The immunophenotypic features of intraventricular macrophages are consistent with other mononuclear phagocytes being immunoreactive for OX-42, OX-18, OX-6, and OX-1 and ED1 for the detection of CR3 receptors, MHC class I and II antigens, leucocyte common antigen, and macrophage antigen, respectively. The expression of these antigens is noticeably enhanced following the injection of lipopolysaccharide (LPS) into postnatal rats. Remarkably, the intraventricular macrophages are induced to express MHC class II (Ia) antigen after LPS or interferon-γ injections. Furthermore, the expression of transferrin receptors as detected with OX-26 is also upregulated after these treatments. Epiplexus cells are also elicited to display a de novo expression of nitric oxide synthase-like immunoreactivity following intracerebral injection of LPS. They also respond vigorously to a single nonpenetrative blast. Results of our series of studies suggest that, besides their primary function as scavenger cells, the intraventricular macrophages partake in possible immunological responses and iron regulation in the ventricular system or the brain as a whole. Microsc. Res. Tech. 41:43–56, 1998. © 1998 Wiley-Liss, Inc.

Morphology of Supraependymal Cells and Their Occurence in the Cerebral Ventricles of Sheep and Goats. A Scanning Electron Microscopy Study

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Organum vasculosum laminae terminalis (OVLT) in rabbit and rat: topographic studies.

The microcirculation and fine structure of the rabbit and rat organum vasculosum laminae terminalis (OVLT) were examined by light microscopy and scanning and transmission electron microscopy. In both animals, the microcirculation is composed of a superficial and a deep vascular bed but the system is more complex and extensive in the rabbit. This was particularly true of the deep vascular bed. In the rabbit, the deep bed is composed of fenestrated capillaries, which are arranged in glomerular tufts surrounded by very wide perivascular spaces (PVS). In contrast, the deep vascular bed of the rat OVLT usually consists of only one or two small vessels. These are either fenestrated and surrounded by a PVS or lined by continuous endothelium with only a few fenestrae and without a dilated PVS. A corresponding difference was seen in the contours of the ventricular surface. It is much more irregular in the rabbit than in the rat and numerous bulges reflect the underlying vascular tufts and pockets of PVS in the rabbit. Supraependymal cells are present in both species and two sizes of them occur in the rabbit. The results demonstrate that the microcirculation of the OVLT is more elaborate and more highly developed in the rabbit than in the rat. We suggest that this might result in a different neurohemal microenvironment and, ultimately, in functional differences.

Early ependymal changes in experimental hydrocephalus after mumps virus inoculation in hamsters.

To elucidate the pathogenesis of early ventricular dilatation in hydrocephalus, we examined early morphological changes in ependymal layers at the lateral ventricles in suckling hamsters without aqueductal stenosis 5 days after the intracerebral inoculation of mumps virus. Mumps virus antigen was detectable in all ependymal cells. The ependymal cilia had almost disappeared and only the microvilli remained. A number of supraependymal cells were also observed on the surface of the lateral ventricles. Transmission electron microscopy revealed intracytoplasmic viral-like inclusions in the infected ependymal cells. These results suggest that functional and morphological disturbances in infected ependymal cells may cause early ventricular dilatation before aqueductal stenosis occurs.

Supra-neuroectodermal cells and fibers on the primary nasal cavity and in the fourth ventricle of mouse and human embryos: scanning and transmission electron microscopic studies.

Neuroectoderm-derived epithelia of the primary nasal cavity and the fourth ventricular floor and roof were observed by scanning (SEM) and transmission electron microscopy (TEM) and SEM-TEM correlative views in mouse embryos of 9th to 13th days of gestation, and in 38 externally normal human embryos ranging at Carnegie stages from 13 to 18 (about 5 to 7 weeks of gestation). Smooth-surfaced spindle-shaped cells with one or more cytoplasmic processes and cord-like cytoplasmic structures were observed by SEM on the wall of the primary nasal cavity of both species. They had morphological features similar to those of neuronal type 1 supraependymal (SE) cells and SE fibers on the floor and roof of the fourth ventricle in both species. Type 1 SE cells, SE fibers, and corresponding structures in the primary nasal cavity were localized in relation to the underlying developing nerve and vascular systems. Furthermore, their processes and fibers ran roughly parallel to these underlying structures and they penetrated the epithelial layer at the ends, suggesting a connection with underlying structures. From TEM and SEM-TEM correlative observations, SE fibers in the fourth ventricle and cord-like structures in the primary nasal cavity, both with a larger diameter, were deduced as single axon-like processes or bundles of processes. Those fibers and cord-like structures of smaller diameters were interpreted as elongated telophase bridges; both contained parallel packed microtubules and connected distant cells. Since these processes and fibers were generally longer and became fewer at later developmental stages, they appeared to be transient neuronal structures. They may play a development-related role in such morphogenetic cell movements as in the developing nerve and vascular systems in the epithelial and/or subepithelial layers, but not as direct rudiments of adult nerve tissues.

Glial fibrillary acidic protein-like immunoreactive ependymal elements in the third ventricle of the rat. A study at different stages of development.

Using the peroxidase-antiperoxidase method a study was made of the cells immunoreactive to glial fibrillary acidic protein (GFAP) anti-serum in the ependyma of the third ventricle of the rat at different stages of growth. Most of the ependymal cells of the third ventricle were seen to be unreactive to this protein; however, it was sometimes possible to observe some GFAP-immunoreactive ependymocytes and occasionally other immunoreactive cellular types, such as tanycytes and supraependymal cells. Despite this, the most frequent localization of the elements immunoreactive to the protein adopted the shape of an immunoreactive subependymal band situated parallel to the ventricular wall. As the weights of the animals increased an increase in the elements immunoreactive to this protein could be observed in all the zones considered, there being no differences between the male and female animals.

Scanning Electron Microscope of Supraependymal Neuronal Circuits in the Third Ventricle of Rhesus Monkey Brain

The supraependymal neurons have been generally demonstrated lying over the nonciliated areas, specially CVOs, on the walls of the third cerebral ventricle of a variety of mammals. However, such neurons have till date been reported on the ciliated ependyma only inguinea pigs (Mitchell and Card, 1978). In the present study, third ventricles of nine adult monkeys of both the sexes were studied by routine scanning electron microscopy after perfusion fixation in 10 per cent neutral buffered formalin, dehydration with graded series of ethanol and amylacetate, critical-point-drying with liquid carbondioxide and sputter-coating with gold.Systematic scanning of the lateral wall of the third ventricle revealed that the ependymal surface could be divided into oligo-, and profusely ciliated zones. Pleomorphic supraependymal cells were noticed over the ciliated regions of the ventricularwall particularly between the thalamus and the mammillary region dorsal and caudal to the infundibular recess (Fig. 1). These neuron-like cells typically consisted of cell somas of variable configurations together with extensive networks of interconnected neuritic processes. At higher magnifications, the neuronal bodies depicted diverse structural modifications(Fig.2). Processes of variable diameters coursed over the ciliary carpet of the lateral wall of the third ventricle(Fig.3). At times, the processes exhibiting varicosities over the supramammillaryzone(Fig.4)coursed for variabledistances over the ependymal lining. The majority of such neuritic processes appeared to penetrate the underlying ventricular wall.

Cells resembling intraventricular macrophages are present in the subretinal space of human foetal eyes

The subretinal spaces (SRS) in 17 human foetal eyes were investigated by light microscopy and scanning and transmission electron microscopy. A hitherto undocumented group of pleomorphic cells was detected on the apical surface of the retinal pigment epithelium (RPE) and on the undersurface of the neural retina. These cells formed a regularly spaced array in the peripheral SRS, particularly in the most anterior portion nearest the ciliary body anlage. The morphology of the SRS cells ranged from a small round or ovoid form with a few short basal pseudopodia to an extremely flattened dendritic form. Ultrastructural features, such as large melanophagolysosomes, consistent with a phagocytic function, were observed in some cells. These SRS cells bore remarkable resemblance to epiplexus and supraependymal cells, considered to be the resident population of macrophages on the ventricular surfaces of the brain. This morphological parallelism, together with the anatomically homologous location, is strong evidence that SRS cells represent a normal population of macrophages in the developing human eye. No features consistent with an RPE or neuronal origin were observed. The possible role of these cells as transient phagocytes in the SRS with a possible destiny as retinal microglia is discussed.

Development of the choroid plexus anlage and supraependymal structures in the fourth ventricular roof plate of human embryos: scanning electron microscopic observations.

The developing anlage of the choroid plexus and supraependymal structures in the fourth ventricular roof plates of nine normal human embryos ranging from Carnegie stages 14 to 19 were investigated with scanning electron microscopy. In the human embryos at stage 18, the first semimacroscopic choroidal anlage developed in the form of bilateral evaginations that ran dorsomedially and caudally from the bilateral corners of the rhombencephalon. The anlage became evident with even smaller and parallel ridges in the embryo at stage 19. Embryos at earlier stages exhibited surface membrane modifications such as convexity, microvilli, cilia, and spherical protrusions at the middle one-third of the rhombencephalon, which corresponded to the future choroidal anlage region. Two morphologically different groups of supraependymal cells (SE cells) were elucidated throughout the stages examined. Type 1 SE cells has spindle or tear-drop-like bodies, frequently with one or more long cytoplasmic processes. Type 2 SE cells were globular, with numerous fine pseudopodial processes. Type 1 SE cells were distributed mainly at the future choroidal anlage regions or on the anlage itself and were less frequently located at the rostral end of the roof. We found no general pattern in the distribution of type 2 SE cells. Supraependymal fibers (SE fibers) were seen as fine processes that were distributed similarly to type 1 SE cells and extended transversely for a long distance.

The dorso-lateral recess of the hypothalamic ventricle in neonatal rats.

Light and electron microscopy of the hypothalamic ventricle in neonatal rats demonstrate morphological specializations of the ventricular wall at the level of the premammillary region of the third ventricle. The morphological features are: (1) A ventricular recess that we have called the "hypothalamic dorso-lateral recess" (HDR). (2) The presence of intraventricular capillaries near the dorso-lateral recess. (3) The HDR possessing a specialized ependymal lining; this consists of non-ciliated cells with short microvilli and bleb-like processes. (4) The existence of cerebrospinal fluid-contacting neurons within the HDR. (5) The presence of numerous phagocytic supraependymal cells. The HDR is not found in adult rats. This indicates that the dorso-lateral recess may play a physiological role during development.

Fourth ventricular floor in human embryos: scanning electron microscopic observations.

The ultrastructural surface features of the normal fourth ventricular floor of seven human embryos ranging from Carnegie stage 14 to stage 19 (crown-rump length: 7.6-16.2 mm) were examined by using scanning electron microscopy (SEM). Low-power SEM views showed the median sulcus, sulcus limitans, and neuromeres, transient structures characteristic of the earlier embryonic period. High-power SEM observation revealed supraependymal cells (SE cells) and supraependymal fibers (SE fibers) which exhibited a characteristic localization, as well as generalized surface-membrane modifications such as microvilli and cilia. SE cells could be classified into two major groups. The type 1 SE cells seem to possess neuronal functions, as deduced from morphological similarities to their counterparts in adults and the specialized distribution closely related to neuromeres. The type 2 SE cell morphologically resembled the phagocytic SE cell described in related literature. SE fibers ran a course either rostrocaudally in the median sulcus or mediolaterally on the neuromeres, most frequently near the interneuromeric cleft; they made contact with type 1 SE cells and ependymal surface modifications and then penetrated the ependymal layer.

A scanning electron-microscopic study of "supramarginal cells" in the pituitary cleft of the rat.

Unusual cells lying above the marginal cellular layer of the rat pituitary cleft were studied by SEM and TEM. These cells - from their location termed supramarginal cells - have a characteristically irregular cell body from which arise a number of long and thin branched processes ending among the microvilli and cilia of the marginal cells delimiting the anterior and posterior walls of the cleft. Some supramarginal cells are star-shaped elements with thin extensions, others have a triangular or spindle-shaped body from which emerge long ameboid processes with fibril-like projections. Miniblebs, miniruffles, occasional veils and short microvilli extend over the surface of these elements. Supramarginal cells are very similar to the "Kolmer epiplexus cells" originally found on the choroid plexus or other areas of the third ventricular wall where they are known as "supraependymal cells". Present evidence suggests that supramarginal cells of pituitary cleft might have phagocytic properties and an hematogenous origin as monocytes and, as such, closely resemble Kolmer epiplexus cells of brain ventricles. Others might arise from "folliculo-stellate cells" or closely related marginal cells once they become free into the pituitary cleft. Supramarginal cells are recognized as motile phagocytes acting as scavengers and possibly regulating the extracellular environment of the cleft and associated adenohypophysial tissues.(ABSTRACT TRUNCATED AT 250 WORDS)

Supraependymal Cell Clusters Induced by ENU Treatment in Developing Rat Retina

ABSTRACT Supraependymal cell clusters in the retina induced by treatment with ethylnitrosourea in fetal and. neonatal rats are described. Following the early cytotoxic effects of this drug on the matrix layer, the supraependymal cell clusters began to form a protrusion from the matrix layer into the intraretinal space through the defective portion of the outer limiting membrane. The supraependymal cell clusters consisted of matrix cells and neurons, or matrix cells, neurons, photoreceptor‐like cells, and glial cells depending on the time of treatment. The clusters became smaller in size, but they remained at least for 7 days after treatment. Our findings indicate that defect of the outer limiting membrane induced by the cytotoxic effect of ethylnitrosourea may be an essential factor for the formation of supraependymal cell clusters, and that the clusters can be regarded as a type of tissue malformation or dysontogenetic anomaly.

Supramarginal cells in the rat pituitary cleft revealed by scanning electron microscopy.

An unusual cell type consisting of free elements widely scattered over the marginal epithelium of the rat pituitary cleft is revealed by SEM. Most of these supramarginal cells characteristically have irregularly shaped cell bodies from which thin branched processes extend. Supramarginal cells bear resemblances to Kolmer (epiplexus) cells and to supraependymal cells of the brain ventricles. Their ultrastructural features make it probable that supramarginal cells are phagocytes, and can be regarded as scavengers of the cleft. Considering the close topographical association between the hypophysial cleft and the floor or the 3rd ventricle, supramarginal cells may be members of the motile macrophagic Kolmer cells populating the ventricular surfaces of the brain.