Summary
Dissociated embryonic chicken retinal cells regenerate in rotary culture into cellular spheres that consist of subareas expressing all three nuclear layers in an inside-out sequence (rosetted vitroretinae). However, when pigmented cells from the eye margin (peripheral retinal pigment epithelium) are added to the system, the sequence of layers is identical with that of an in-situ retina (laminar vitroretinae). In order to elucidate further the lamina-stabilizing effect exerted by the retinal pigment epithelium, we have compared both systems, laying particular emphasis on the ultrastructure of the basal lamina and of Müller glia processes. Ultrastructurally, in both systems, an outer limiting membrane, inner segments of photoreceptors and the segregation of cell bodies into three cell layers develop properly. Synapses are detectable in a premature state, although only in the inner plexiform layer of laminar vitroretinae. Although present in both systems, radial processes of juvenile Müller glia cells are properly fixed at their endfeet only in laminar vitroretinae, since a basal lamina is only expressed here. Large amounts of laminin are detected immunohistochemically within the retinal pigment epithelium and along a basal stalk that reaches inside the laminar vitroretinae. We conclude that the peripheral retinal pigment epithelium is essential for the expression of a basal lamina in vitro. Moreover, the basal lamina may be responsible both for stabilizing the correct polarity of retinal layers and for the final differentiation of the Müller cells.
Similar content being viewed by others
References
Adler R, Teitelman G (1974) Aggregates formed by mixtures of embryonic neural cells: activity of enzymes of the cholinergic system. Dev Biol 39:317–321
Akagawa K, Hicks D, Barnstable CJ (1987) Histiotypic organization and cell differentiation in rat retinal reaggregate cultures. Brain Res 437:298–308
Aramant R, Seiler M, Ehinger B, Bergström A, Gustavii B, Brundin P, Adolph AR (1990) Transplantation of human embryonic retina to adult rat retina. Rest Neurol Neurosci 2:9–22
Bennett GS (1987) Changes in intermediate filament composition during neurogenesis. Curr Top Dev Biol 21:151–184
Berg-von der Emde K, Wolburg H (1989) Müller(glial) cells but not astrocytes in the retina of the goldfish possess orthogonal arrays of particles. Glia 2:458–469
Bryan JA, Campochiaro PA (1986) A retinal pigment epithelial cell-derived growth factor(s). Arch Ophthalmol 104:422–425
Coulombre JL, Coulombre AJ (1965) Regeneration of neural retina from pigmented epithelium in the chick embryo. Dev Biol 12:79–92
Coulombre JL, Coulombre AJ (1970) Influence of mouse neural retina on regeneration of chick neural retina from chick embryonic pigmented epithelium. Nature 228:559–560
Debus E, Weber K, Osborn M (1983) Monoclonal antibodies specific for glial fibrillary acidic (GFA) protein and for each of the neurofilament triplet polypeptides. Differentiation 25:193–203
Detwiler SR, VanDyke RH (1953) The induction of neural retina from the pigment epithelial layer of the eye. J Exp Zool 122:367–384
Doe CQ, Goodman CS (1985) Early events in insect neurogenesis. I. Development and segmental differences in the pattern of neuronal precursor cells. Dev Biol 111:193–205
dorris F (1938) Differentiation of the chick eye in vitro. J Exp Zool 78:386–407
Dragomirov N (1936) Über Induktion sekundärer Retina im transplantierten Augenbecher bei Triton und Pelobates. Wilhelm Roux Archiv 134:716–737
Dreher Z, Wegner M, Stone J (1988) Müller cell endfeet at the inner surface of the retina: light microscopy. Vis Neurosci 1:169–180
Ekblom P, Alitalo K, Vaheri A, Timpl R, Saxen L (1980) Induction of a basement membrane glycoprotein in embryonic kidney: possible role of laminin in morphogenesis. Proc Natl Acad Sci USA 77:485–489
Fujisawa H (1973) The process of reconstruction of histological architecture from dissociated retinal cells. Wilhelm roux Archiv 171:312–330
Glees P, Meller K (1968) Morphology of neuroglia, vol 1. Bourne GH (ed). Academic Press, London
Hamburger V, Hamilton HL (1951) A series of normal stages in the development of the chick embryo. J Morphol 88:49–92
Hawkes R, Niday E, Gordon J (1982) A dot-immunobinding assay for monoclonal and other antibodies. Anal Biochem 119:142–147
Keefe JR (1973a) An analysis of urodelian retinal regeration: I. Studies of the cellular source of retinal regeneration in Notophthalmus viridescens utilizing 3H-thymidine and colchicine. J Exp Zool 184:185–206
Keefe JR (1973b) An analysis of urodelian retinal regeneration: II. Ultrastructural features of retinal regeneration in Notophthalmus viridescens. J Exp Zool 184:207–232
Keefe JR (1973c) An analysis of urodelian retinal regenration: III. Degradation of extruded melanin granules in Notophthalmus viridescens. J Exp Zool 184:233–238
Keefe JR (1973d) An analysis of urodelian retinal regeneration: IV. Studies of the cellular source of retinal regeneration in Triturus cristatus carnifex using 3H-thymidine. J Exp Zool 184:239–258
Klein G, Langegger M, Timpl R, Ekblom P (1988) Role of laminin A chain in the development of epithelial cell polarity. Cell 5:331–341
Kondor-Koch C, Bravo R, Fuller S, Cutler P, Garoff H (1986) Exocytotic pathways exist to both the apical and the basolateral cell surface of the polarized epithelial cell MDCK. Cell 43:297–306
Layer PG (1983) Comparative localization of acetylcholinesterase and pseudocholinesterase during morphogenesis of the chick brain. Proc Natl Acad Sci USA 80:6413–6417
Layer PG, Kotz S (1983) Asymmetrical developmental pattern of uptake of Lucifer Yellow into amacrine cells in the embryonic chick retina. Neuroscience 9:931–941
Layer PG, Willbold E (1989) Embryonic chicken retinal cells can regenerate all cell layers in vitro, but ciliary pigmented cells induce their correct polarity. Cell Tissue Res 258:233–242
Layer PG, Vollmer G, Kotz S (1983) Selective uptake of Lucifer Yellow into different cell populations of the developing chicken retina. Neurosci Lett 35:239–245
Layer PG, Alber R, Mansky P, Vollmer G, Willbold E (1990) Regeneration of a chimeric retina from single cells in vitro: cell-lineage-dependent formation of radial cell columns by segregated chick and quail cells. Cell Tissue Res 259:187–198
Lemmon V (1985) Monoclonal antibodies specific for glia in the chick nervous system. Dev Brain Res 23:111–120
Liu L, Layer PG, Gierer A (1983) Binding of FITC-coupled peanut-agglutinin (FITC-PNA) to embryonic chicken retinae reveals developmental spatio-temporal patterns. Dev Brain Res 8:223–229
Liu L, Cheng SH, Jiang LZ, Hansmann G, Layer PG (1988) The pigmented epithelium sustains cell growth and tissue differentiation of chicken retinal explants in vitro. Exp Eye Res 46:801–812
Maier W, Wolburg H (1979) Regeneration of the goldfish retina after exposure to different doses of ouabain. Cell Tissue Res 202:99–118
Martin GR, Timpl R (1987) Laminin and other basement membrane components. Annu Rev Cell Biol 3:37–85
Moscona AA (1952) Cell suspensions from organ rudiments of chick embryos. Exp Cell Res 3:535
Okada TS (1983) Recent progress in studies of the transdifferentiation of eye tissue in vitro. Cell Differ 13:177–183
Orts-Llorca F, Genis-Galvez JM (1960) Experimental production of retinal septa in the chick embryo. Differentiation of pigment epithelium into neural retina. Acta Anat (Basel) 42:31–70
Prada FA, Magalhaes MM, Coimbra A, Genis-Galvez JM (1989) Morphological differentiation of the Müller cell: Golgi and electron microscopy study in the chick retina. J Morphol 201:11–22
Price J, Turner D, Cepko C (1987) Lineage analysis in the vertebrate nervous system by retrovirus-mediated gene transfer. Proc Natl Acad Sci USA 84:156–160
Rathjen FG, Wolff JM, Frank R, Bonhoeffer F, Rutishauser U (1987) Membrane glycoproteins involved in neurite fasciculation. J Cell Biol 104:343–353
Reh TA, Nagy T, Gretton H (1987) Retinal pigmented epithelial cells induced to transdifferentiate to neurons by laminin. Nature 330:68–71
Reichenbach A (1989) Attempt to classify glial cells by means of their process specialization using the rabbit retinal Müller cell as an example of cytotopographic specialization of glial cells. Glia 2:250–259
Reichenbach A, Schneider H, Leibnitz L, Reichelt W, Schaaf P, Schümann R (1989) The structure of rabbit retinal Müller (glial) cells is adapted to the surrounding retinal layers. Anat Embryol 180:71–79
Robinson SR, Dreher Z (1990) Müller cells in adult rabbit retinae: morphology, distribution and implications for function and development. J Comp Neurol 292:178–192
Rodriguez-Boulan E (1983) Membrane biogenesis, enveloped RNA viruses, and epithelial cell polarity. Mod Cell Biol 1:119–170
Sheffield JB, Moscona AA (1969) Early stages in the reaggregation of embryonic chick neural retina cells. Exp Cell Res 57:462–466
Simons K, Fuller S (1985) Cell surface polarity in epithelia. Annu Rev Cell Biol 1:243–288
Stroeva OG (1960) Experimental analysis of the eye morphogenesis in mammals. J Embryol Exp Morphol 8:349–368
Szaro BG, Gainer H (1988) Immunocytochemical identification of non-neuronal intermediate filament proteins in the developing Xenopus laevis nervous system. Dev Brain Res 43:207–224
Tsunematsu Y, Coulombre AJ (1981) Demonstration of transdifferentiation of neural retina from pigmented retina in culture. Dev Growth Differ 23:297–311
Vollmer G, Layer PG (1986a) Reaggregation of chick retinal and mixtures of retinal and pigment epithelial cells: the degree of laminar organization is dependent on age. Neurosci Lett 63:91–95
Vollmer G, Layer PG (1986b) An in vitro model of proliferation and differentiation of the chick retina: coaggregates of retinal and pigment epithelial cells. J Neurosci 6:1885–1896
Vollmer G, Layer PG (1987) Cholinesterases and cell proliferation in “nonstratified” and “stratified” cell aggregates from chicken retina and tectum. Cell Tissue Res 250:481–487
Vollmer G, Layer PG, Gierer A (1984) Reaggregation of embryonic chick retina cells: pigment epithelial cells induce a high order of stratification. Neurosci Lett 48:191–196
Wolburg H, Berg K (1988) Distribution of orthogonal arrays of particles in the Müller cell membrane of the mouse retina. Glia 1:246–252
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Wolburg, H., Willbold, E. & Layer, P.G. Müller glia endfeet, a basal lamina and the polarity of retinal layers form properly in vitro only in the presence of marginal pigmented epithelium. Cell Tissue Res 264, 437–451 (1991). https://doi.org/10.1007/BF00319034
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00319034