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Localization of S-100 Protein in Mulier Cells of the Retina— 1

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Localization of S-100 Protein in Mulier Cells of the Retina— 1 Reports Localization of S-100 Protein in Mulier Cells of the Retina— 1. Light Microscopical Immunocytochemistry G. Terenghi,* D. Cocchia,f F. Micherti,f A. R. T. Pererson4 D. F. Cole,§ S. R. Bloom,11 ond J. M. Polok* S-100 is an acidic brain protein previously found to be pres- constituent and could be involved in the functions ent in glial cells of the brain and the nervous system of gut of normal and diseased retina10"; their identification and respiratory tract. Immunocytochemistry at the light by the use of a suitable marker is thus of primary microscopical level localized immunoreactivity for S-100 in relevance. In this study, we report on the immuno- the Mulier cells in the retina of rat, guinea pig, and Chinese cytochemical visualization at light microscopic level hamster. The Mulier cells represent the main glial com- ponent of the retina, with a structural role in the support of Mulier cells in the mammalian retina by using the and insulation of neurons and sensory elements. The use presence of S-100 protein as a marker for glial cells. of S-100 protein as an immunocytochemical marker of Materials and Methods. Albino rats (n = 5), guinea Miiller cells may be useful in the study of pathologic con- pigs (n = 5), and Chinese hamsters (n = 4) were used. ditions of the retina where glial cell proliferation could re- The animals were killed by exsanguination under flect the index of neuronal injury. Invest Ophthalmol Vis ether anaesthesia; the eyeballs were removed and im- Sci 24:976-980, 1983 mediately processed. The whole eye was fixed by im- mersion in a solution of 0.4% benzoquinone in 0.01 S-100 is an acidic protein that was isolated origi- M phosphate-buffered saline (pH 7.1-7.4) at 4°C for nally from bovine brain by Moore1 and subsequently 30 to 45 min and then rinsed several times in phos- was found to be widely distributed in the nervous phate-buffered saline. After fixation, an incision was system of many mammals.2 It is generally thought made at the level of the ora serrata and the posterior that in both central and peripheral nervous systems, half of the eye was separated from the anterior ocular the main localization of this protein is in glial ele- structures. ments, as recently demonstrated in the nervous sys- Cryostat blocks were prepared from the eyecup tem of the gut3 and the respiratory tract.4 with the retina in situ and sections were cut at 10 The morphologic identification of the glial cells is nm and 20 ^m thickness. Immunocytochemistry was of great importance for the study of their functional carried out according to the indirect immunofluo- relationship with neurons in normal and diseased rescence method,12 using rabbit S-100 antiserum13 at conditions. The retina, because of its relatively simple a dilution of 1/400 in phosphate-buffered saline. The organization and the particularly abundant glial com- sections were incubated with primary antibody for ponent, represents an unique model for the study of 16 to 20 hours at 4°C. Control sections were incu- neuronal and non-neuronal elements of the nervous bated with non-immune rabbit serum or first layer system. Although various retinal neuronal elements antiserum preabsorbed with purified S-100 protein have been recognized by immunocytochemistry,5 the (20 Mg/ml diluted antiserum). identification of glial cells of the retina is still based Results. In all the animals, the immunoreactive S- on silver impregnation methods as originally used by 100 appeared to be localized in those retinal cells Cajal,6 who supplied the classic anatomic description. corresponding to the classical description of Mulier The retina contains various forms of glial cells, cells (Fig. 1). Since these cells appeared evenly dis- such as astroglia, microglia, perivascular glia, and tributed in all retinal regions and presented a similar Mulier cells. In most species, it is this last type that morphologic appearance in all three species, a single constitutes the main structural framework.7 Although description of the results will be given. However, the Mulier cells have mainly a structural role, it is thought frequency of the cells varied between species, being that they could also provide nutrients to the sur- most numerous in the retina of Chinese hamster and rounding cells and modulate neuronal sensitivity.7"9 least numerous in the guinea pig retina. It is evident that Mulier cells are an important retinal The perikarya of the Mulier cells appeared to be 0146-0404/83/0700/976/$ 1.25 © Association for Research in Vision and Ophthalmology 976 Downloaded from iovs.arvojournals.org on 09/24/2021 No. 7 REPORTS 977 -ILM GCL IPL INL Fig. 1. S-100 immuno- reactivity localized to Milller cells of: A, rat ret- ina (X54O; scale bar = 20 urn); B, guinea pig retina ONL (X540; scale bar = 20 *im); C, Chinese hamster retina (X460; scale bar = 30/xm). Twenty-micrometer sec- tions. The cell bodies are clearly visible in the inner nuclear layer (INL) (ar- rows), with long processes radiating in opposite di- rections, forming a net- work of fibers in the outer nuclear layer (ONL) and terminating on the inner limiting membrane (ILM) with a pedicule-shaped ending. ILM = inner lim- iting membrane; GCL = ganglion cell layers; IPL = inner plexiform layer; INL = inner nuclear layer; ONL = outer nu- clear layer. OPL Downloaded from iovs.arvojournals.org on 09/24/2021 978 INVESTIGATIVE OPHTHALMOLOGY & VISUAL SCIENCE / July 1983 Vol. 24 INL Fig. 1. (Continued) OPL localized in approximately the middle of the inner Discussion. We report here on the immunocyto- nuclear layer; the cell bodies were irregular in shape, chemical localization at light microscopic level of S- very often showing a concave outline (Fig. 2). This 100 in the retina of three types of small mammals. feature is characteristic of the Muller cells and is con- The immunoreactivity for S-100 is localized mainly sistent with their supportive role and their ability to to cells corresponding to Muller cells, as described by fill the gaps between the rounded neuronal cell bodies. Cajal.6 No immunoreactivity was observed in gan- The main long processes radiated from the cell body glion cells, as reported recently by Linser14 in avian in opposite directions, occupying the full thickness retina. of the retina. In the centrifugal direction, the pro- The possibility that S-100 immunoreactivity could cesses presented numerous ramifications at the level be localized to either bipolar or interplexiform cells, of the outer nuclear layer, giving rise to a meshwork both retinal elements with centrifugal and centripetal of fibres which completely surrounded the photore- neuronal ramifications, was ruled out on the basis of ceptor cell bodies. In the opposite direction, the pro- the characteristic morphological appearance of the cesses reached the more inner layers of the retina, immunoreactive cells. These immunoreactive cells generally terminating in a pedicle that appeared to resembled Muller cells but not bipolar or interplex- be in contact with the inner limiting membrane (Fig. iform cells, as they showed indented nuclei, processes 3). At the level of the ganglion cell layer, the processes occupying the full thickness of the retina with pedicle- showed ramifications that surrounded most of the shaped terminations on the inner limiting membrane ganglion cells. In this layer, a few small cells im- and extensive networks of fibers surrounding the sen- munoreactive for S-100 were also observed, probably sory cell bodies. corresponding to astroglial elements (Fig. 3); they Our results are consistent with the findings of S- appeared sporadically distributed throughout the ret- 100 protein in glial cells of other areas of the cen1 ina and showed irregular cell bodies with compara- tral215 and peripheral nervous system3413 and em- tively short ramifications mainly confined to the same phasize the similarities of Muller cells and glial ele- layer. ments. Downloaded from iovs.arvojournals.org on 09/24/2021 No. 7 REPORTS 979 IPL Fig. 2. Rat retina, 10-ftm section, S-100 immunoreactivity in Miiller cell bodies, showing details of the irregular and in- INL dented outline (X88O; scale bar = 10 fim). IPL = inner plexiform layer; INL = inner nuclear layer; OPL = outer plexiform layer. OPL Although the Miiller cells form a supportive and shown to be involved in the accumulation of in- insulating framework for the neuronal elements, it creased glycogen deposits in the retina of Chinese is thought that they participate actively in the com- hamsters affected by severe diabetes.10 The potential plex functional mechanism of the retina. The high use of S-100 protein as a diagnostic marker of retinal content of glycogen and of enzymes related to glyco- diseases is also shown by the finding of glial elements lytic metabolism indicate clearly their probable role in retinoblastoma, which is thought to originate from in providing energy to the surrounding neurons.8 It retinal glial cells." has also been suggested that by occupying all the In conclusion, the Muller cells, like glial elements spaces between neurons, they contribute in reducing of other systems, contain S-100 protein, which could the extent of optical damage to the incident retinal represent a useful immunocytochemical marker for image.9 In more general terms, if injury in neuronal the investigation of pathologic conditions of the parenchyma can be visualized as a proliferation of retina. glial elements, immunostaining for S-100 protein might provide a useful means of assessing the extent Key words: glia, immunocytochemistry, Muller cells, retina, of the damage. As an example, Miiller cells have been S-100 protein Fig. 3. Rat retina, 10-^m section. S-100 immunoreac- tivity in the pedicule-shaped processes of the Muller cell GCL terminating on the inner limiting membrane (arrow).
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