Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

A molecular view of vertebrate retinal development

  • 98 Accesses

  • 65 Citations

Abstract

Immunological probes have begun to identify molecules that delineate cell layers and cell types during the formation of the retina and other parts of the optic cup. Within the developing retina, cell-type-specific monoclonal antibodies have been used to show that differentiation occurs before cells reach their final laminar position. Cell surface molecules have been found expressed in position-dependent gradients across the retina. These molecules may convey positional information to the retinal cells and their topographic connections. One such molecule is a modified carbohydrate group on a ganglioside, suggesting that such groups may play a role in neural development. A variety of molecules that are expressed by rod photoreceptors at defined stages of their differentiation have been characterized. These molecules have been used to show the development of subcellular compartments within rods. In vitro studies have suggested that photoreceptor molecules expressed at different times are under different forms of regulation. Some of these cell-specific molecules have been shown to be under transcriptional control and thus defined cell interactions seem to be linked to changes in gene expression during retinal development.

This is a preview of subscription content, log in to check access.

References

  1. Abney E. R., Williams B. P., and Raff M. C. (1983) Tracing the development of oligodendrocytes from precursor cells using monoclonal antibodies, fluorescence-activated cell sorting, and cell culture.Dev. Biol. 100, 166–171.

  2. Akagawa K. and Barnstable C. J. (1986) Identification and characterisation of cell types in monolayer cultures of rat retina using monoclonal antibodies.Brain Res. 383, 110–120.

  3. Akagawa K. and Barnstable C. J. (1987) Identification and characterisation of cell types accumulating GABA in rat retinal cultures using cell type specific monoclonal antibodies.Brain Res. 408, 156–162.

  4. Baird A., Esch F., Gospodarowicz D., and Guillemin R. (1985) Retina and eye derived endothelial cell growth factors: Partial molecular characterization and identity with acidic and basic fibroblast growth factors.Biochemistry 24, 7855–7860.

  5. Barbera A. J., Marchase R. B., and Roth S. (1973) Adhesive recognition and retinotectal specificity.Proc. Nat. Acad. Sci. USA 70, 2482–2486.

  6. Barde Y. A., Edgar D., and Thoenen H. (1982) Purification of new neurotrophic factor from mammalian brain.EMBO J. 1, 549–553.

  7. Barnstable C. J. (1980) Monoclonal antibodies which recognise different cell types in the rat retina.Nature 286, 231–235.

  8. Barnstable C. J. (1981) Developmental studies of rat retina cells using cell-type-specific monoclonal antibodies, inMonoclonal Antibodies to Neural Antigens. (McKay R., Raff M. C., and Reichardt L. F., eds.) pp. 219–230, Cold Spring Harbor, NY.

  9. Barnstable C. J. (1982) Immunological studies of the retina, inNeuroimmunology (Brockes J., ed.) pp. 183–214, Plenum, New York, NY.

  10. Barnstable C. J. (1985) Monoclonal antibodies as molecular probes of the nervous system, inHybridoma Technology in the Biosciences and Medicine (Springer T., ed.) pp. 269–289, Plenum, New York, NY.

  11. Barnstable C. J. and Constantine-Paton M. (1984) Initial events of lamination in the mammalian retina.Soc. Neurosci. Abstr. 10, 787.

  12. Barnstable C. J. and Dräger U. C. (1984) Thy-1: A ganglion cell specific marker of rodent retina.Neuroscience 11, 847–855.

  13. Barnstable C. J., Akagawa K., Hofstein R., and Horn J. P. (1983) Monoclonal antibodies that label discrete cell types in the mammalian nervous system.Cold Spring harbor Symp. Quant. Biol. 48, 863–876.

  14. Barnstable C. J., Hofstein R., and Akagawa K. (1985) A marker of early amacrine cell development in rat retina.Dev. Brain Res. 20, 286–290.

  15. Bastiani M. J., Du Lac S., and Goodman C. S. (1985) The first neuronal growth cones in insect embryos. Model system for studying the development of neuronal specificity, inModel Neural Networks and Behavior (Selverston A. I., ed.) pp. 149–174. Plenum, New York, NY.

  16. Ben-Shaul Y., Hausman R. E., and Moscona A. A. (1979) Visualization of a cell surface glycoprotein, the retina cognin on embryonic cells by immunolatex labeling and scanning electron microscopy.Dev. Biol. 72, 89–101.

  17. Ben-Shaul Y., Hausman R. E., and Moscona A. A. (1980) Age-dependent differences in cognin regeneration on embryonic retina cells: Immunolabeling and SEM studies.Dev. Neurosci. 3, 66–74.

  18. Bentley D. and Caudy M. (1983a) Pioneer axons lose directed growth after selective killing of guidepost cells.Nature 304, 62–65.

  19. Bentley D. and Caudy M. (1983b)_Navigational substrates for peripheral pioneer growth cones: Limb-axis polarity cues, limb-segment boundaries, and guidepost neurons.Cold Spring Harbor Symp. Quant. Biol. 48, 573–585.

  20. Besharse J. C., Forestner D. M., and Defoe D. M. (1985) Membrane assembley in retinal photoreceptors. III. Distinct membrane domains of the connecting cilium of developing rods.J. Neurosci. 5, 1035–1048.

  21. Blum A. S. and Barnstable C. J. (1986) Structure and regulation of a developmentally restricted neuronal surface antigen.J. Cell Biol. 103, 231a.

  22. Bonhoeffer F. Huf J. (1985) Position-dependent properties of retinal axons and their growth cones.Nature 315, 409–410.

  23. Brackenbury R., Thiery J.-P., Rutishauser U., and Edelman G. M. (1977) Adhesion among neural cells of the chick embryo. I. An immunological assay for molecules involved in cell-cell binding.J. Biol. Chem. 252, 6835–6840.

  24. Brady R. C. and Hilfer S. R. (1982) Optic cup formation: A calcium regulated process.Proc. Nat. Acad. Sci. USA 79, 5587–5591.

  25. Braekvelt C. R. and Hollenberg M. J. (1970) The development of the retina of the albino rat.Am. J. Anat. 127, 281–302.

  26. Brugge J. S., Cotton P. C., Queral A. E., Barrett J. N., Nonner D., and Keane R. W. (1985) Neurones express high levels of a structurally modified activated form of pp60c src.Nature 316, 554–557.

  27. Buskirk D. R., Thiery J.-P., Rutishauser U., and Edelman G. M. (1980) Antibodies to a neural cell adhesion molecule disrupt histogenesis in cultured chick retinae.Nature 285, 488–489.

  28. Cheresh D. A., Reisfeld R. A., and Varki, A. P. (1984) O-acetylation of disialoganglioside GD3 by human melanoma cells creates a unique antigenic determinant.Science 225, 844–846.

  29. Cheresh D. A., Pierschbacher M. D., Herzig M. A., and Mujoo K. (1986) Disialogangliosides GD2 and GD3 are involved in the attachment of human melanoma and neuroblastoma cells to extracellular matrix proteins.J. Cell Biol. 102, 688–696.

  30. Constantine-Paton M., Blum A. S., Mendez-Otero R., and Barnstable C. J. (1986) A cell surface molecule distributed in a dorsoventral gradient in the perinatal rat retina.Nature 324, 459–462.

  31. Cotton P. C. and Brugge J. S. (1983) Neural tissues express high levels of the cellular src gene product pp60c-src.Mol. Cell. Biol. 3, 1157–1162.

  32. Daniloff J. K., Chuong, C.-M., Levi G., and Edelman G. M. (1986) Differential distribution of cell adhesion molecules during histogenesis of the chick nervous system.J. Neurosci. 6, 739–758.

  33. David, S., Miller R. H., Patel, R. and Raff M. C. (1984) Effects of neonatal transection on glial cell development in the rat optic nerve: Evidence that the oligodendrocyte-type2 astrocyte lineage depends on axons for its survival.J. Neurocytol. 13, 961–974.

  34. De Camilli P., Ueda T. E., Bloom F. E., Battenberg E., and Greengard P. (1979) Widespread distribution of protein I in the central and peripheral nervous systems.Proc. Nat. Acad. Sci. USA 76, 5977–5981.

  35. Denham S. (1967) A cell proliferation study of the neural retina in the two day rat.J. Embryol. Exp. Morphol. 18, 53–66.

  36. Devoto S. and Barnstable C. J. (1987) SVP38: A synaptic vesicle protein whose appearance correlates closely with synaptogenesis in the rat nervous systemAnn. NY Acad. Sci. (in press).

  37. Dodd J., Solter D., and Jessell T. M. (1984) Monoclonal antibodies against carbohydrate differentiation antigens identify subsets of primary sensory neurons.Nature 311, 469–472.

  38. Dowling J. E. (1964) Nutritional and inherited blindness in the rat.Exp. Eye Res. 3, 348–356.

  39. Dräger U. C., Edwards D. L., and Barnstable C. J. (1984) Antibodies against filamentous components in discrete cell types of the mouse retina.J. Neurosci. 4, 2025–2042.

  40. Drenckhahn D. and Wagner H.-J. (1985) Relation of retinomotor responses and contractile proteins in vertebrate retinas.Eur. J. Cell. Biol. 37, 156–168.

  41. Edelman G. M., Hoffman S., Chuong C.-M., Thiery J.-P., Brackenbury R., Gallin W. J., Grumet M., Greenberg M. E., Hemperly J. J., Cohen C., and Cunningham B. A. (1983) Structure and modulation of neural cell adhesion molecules in early and late embryogenesis.Cold Spring Harbor Symp. Quant. Biol. 48, 515–526.

  42. Edwards J. G., Campbell J. A., Robson R. T., and Vicker M. G. (1975) Trypsinized BHK 21 cells aggregate in the presence of divalent cations.J. Cell Sci. 19, 653–667.

  43. Fekete D. M. and Barnstable C. J. (1983) The subcellular localisation of rat photoreceptor specific antigens.J. Neurocytol. 12, 785–803.

  44. Fujita S. (1962) Kinetica of cellular proliferation.Exp. Cell Res. 28, 52–60.

  45. Fulcrand J. and Privat A. (1977) Neuroglial reactions secondary to Wallerian degeneration in the optic nerve of the postnatal rat: Ultrastructural and quantitative study.J. Comp. Neurol. 176, 189–224.

  46. Gonzalez-Fernandez F., Landers R. A., Glazebrook P. A., Fong S.-L., Liou G. I., Lam D. M. K., and Bridges C. D. B. (1984a) An extracellular retinol-binding glycoprotein in the eyes of mutant rats with retinal dystrophy: Development, localization, and biosynthesis.J. Cell Biol. 99, 2092–2098.

  47. Gonzalez-Fernandez F., Landers, R. A., Fong S.-L., Liou F. I., and Bridges C. D. B. (1984b) Interstitial retinal retinol-binding protein in the interphotoreceptor matrix of normal and dystrophic rats, inThe Inter Photoreceptor in Matrix in Health bondeceptor in Matrix in Health and disease (Bridges C. D. and Adler, A. J., eds.) pp 213–229.Alan R. Liss, New York, NY.

  48. Goridis C., Hirn M., Santoni M.-J., Genarini G., Deagostini-Bazin H., Jordan B. R., Kiefer M., and Steinmetz M. (1985) Isolation of mouse N-CAM-related cDNA: Detection and cloning using monoclonal antibodies.EMBO J. 4, 631–635.

  49. Grumet M., Hoffman S. and Edelman G. M. (1984) Two antigenically related neuronal cell adhesion molecules of different specificities mediate neuron-neuron and neuron-glia adhesion.Proc. Nat. Acad. Sci. USA 81, 267–271.

  50. Grunewald G. B., Pratt R. S., and Lilien J. (1982) Enzymatic dissection of embryonic cell adhesive mechanisms. III. Immunological identification of a component of the calcium-dependent adhesive system of embryonic chick neural retina cells.J. Cell Sci. 55, 69–83.

  51. Halfter W., Deiss S., and Schwarz U. (1985) The formation of the axonal pattern in the embryonic avian retina.J. Comp. Neurol. 232, 466–480.

  52. Hatta K. and Takeichi M. (1986) Expression of N-adherin adhesion molecules associated with early morphogenetic events in chicken development.Nature 320, 447–449.

  53. Hatta K., Okada T. S., and Takeichi M. (1985) A monoclonal antibody disrupting calcium-dependent cell-cell adhesion of brain tissues: Possible role of its target antigen in animal pattern formation.Proc. Nat. Acad. Sci. USA 82, 2789–2793.

  54. He H. T., Barbet J., Chaix J. C., and Goridis C. (1986) Phosphatidylinositol is involved in the membrane attachment of N-CAM-120, the smallest component of the cell adhesion molecule.EMBO J. 5, 2489–2494.

  55. Hicks D. and Barnstable C. J. (1986) Lectin and antibody labelling of developing rat photoreceptor cells: An electron microscope immunocytochemical study.J. Neurocytol. 15, 219–230.

  56. Hicks D. and Barnstable C. T. (1987) Different monoclonal antibodies reveal different binding patterns on developing and adult retina.J. Histochem. Cytochem (In Press).

  57. Hilfer S. R., Brady R. C., and Wang J-J. W. (1981) Intracellular and extracellular changes during early ocular development in the chick embryo, inOcular Size and Shape: Regulation During Development (Hilfer S. R. and Sheffield J. B., eds.) pp. 47–78, Springer-Verlag, New York, NY.

  58. Hinds J. W. and Hinds P. L. (1978) Early development of amacrine cells in the mouse retina: An electron microscope, serial section analysis.J. Comp. Neurol. 179, 277–300.

  59. Hockfield S., McKay R. D., Hendry S. H. C., and Jones E. G. (1983) A surface antigen that identifies ocular dominance columns in the visual cortex and laminar features of the lateral geniculate nucleus.Cold Spring Harbor Symp. Quant. Biol. 48, 877–890.

  60. Hoffman S. and Edelman G. M. (1983) Kinetics of homophilic binding by E and A forms of the neural cell adhesion molecule.Proc. Nat. Acad. Sci. USA 80, 5762–5766.

  61. Hoffman S., Friedlander D. R., Chuong C.-M., Grumet M., and Edelman G. M. (1986) Differential contributions of Ng-CAM and N-CAM to cell adhesion in different neural regions.J. Cell Biol. 103, 145–158.

  62. Holt C. (1980) Cell Movements inXenopus development.Nature 287, 850–852.

  63. Horvitz H. R., Sternberg P. W., Greenwald I. S., Fixsen W., and Ellis H. M. (1983), Mutations that affect neural cell lineages and cell fates during the development of the nematodeCaenorhabditis elegans.Cold Spring Harbor Symp. Quant. Biol. 48, 453–463.

  64. Jessell T. M. and Dodd J. (1985) Structure and expression of differentiation antigens on functional subclasses of primary sensory neurons.Phil. Trans. R. Soc. (Lond) B308, 271–281.

  65. Johnson J. E., Barde Y.-A., Schwab M., and Thoenen H. (1986) Brain-derived neurotrophic factor supports the survival of cultured rat retinal ganglion cells.J. Neurosci. 6, 3031–3038.

  66. Johnston M. C., Nodoen M. D., Hazelton R. D., Coulombre J. L., and Coulombre A. J. (1979) Origins of avian ocular and periocular tissues.Exp. Eye Res. 29, 27–43.

  67. Juurlink B. H. J. and Federoff S. (1980) Differentiation capabilities of mouse optic stalk in isolation of its immediatein vivo environment.Dev. Biol. 78, 215–221.

  68. Kapfhammer J. P., Grunewald B. E., and Raper J. A. (1986) The selective inhibition of growth cone extension by specific neurites in culture.J. Neurosci. 6, 2527–2534.

  69. Keane R. W., Lipsich L. A., and Brugge J. S. (1984) Differentiation and transformation of neural plate cells.Dev. Biol. 103, 38–52.

  70. Krotoski D. M., Domingo C., and Bronner-Fraser M. (1986) Distribution of a putative cell surface receptor for fibronectin and laminin in the avian embryo.J. Cell Biol. 103, 1061–1071.

  71. Levitt P. (1984) A monoclonal antibody to limbic system neurons.Science 223, 299–301.

  72. Lindsay R. M., Thoenen H., and Barde Y. A. (1985) Placode and neural crest derived sensory neurons are responsive at early developmental stages to brain-derived neurotrophic factor.Dev. Biol. 112, 319–328.

  73. Magnani J. L., Thomas W. A., and Steinberg M. S. (1981) Two distinct adhesion mechanisms in embryonic neural retina cells. I. A kinetic analysis.Dev. Biol. 81, 96–105.

  74. Marchase R. B. (1977) Biochemical investigations of retinotectal adhesive specificity.J. Cell Biol. 75, 237–257.

  75. Marchase R. B., Harges P., and Jakoi E. R. (1981) Ligatin from embryonic chick neural retina inhibits retinal cell adhesion.Dev. Biol 86, 250–255.

  76. Marchase R. B., Koro L. A., Kelly C. M., and McClay D. R. (1982) Retinal ligatin recognizes glycoproteins bearing oligosaccharides terminating in phosphodiester linked glucose.Cell 28, 813–820.

  77. Molday R. S. and Mac Kenzie D. (1983) Monoclonal antibodies to rhodopsin: Characterization, crossreactivity and application as structural probes.Biochemistry 22, 653–660.

  78. Morrison R. S., Sharma A., De Vellis J., and Bradshaw R. A. (1986) Basic fibroblast growth factor supports the survival of cerebral cortical neurons in primary culture.Proc. Nat. Acad. Sci. USA 83, 7537–7541.

  79. Morse D. E. and McCann P. S. (1984) Neueoectoderm of the early embryonic rat eye. Scanning electron microscopy.Invest. Ophthalmol. Vis. Sci. 25, 899–907.

  80. Moscona A. A. and Housman R. E. (1977) Biological and biochemical studies on embryonic cell-cell recognition, inCell and Tissues Interactions. (Lash J. W. and Burger M. M., eds.) pp. 173–185. Raven, New York, NY.

  81. Murray B. A., Hemperly J. J., Gallin W. J., MacGregor J. S., Edelman G. M., and Cunningham B. A. (1984) Isolation of cDNA clones for the chick neural cell adhesion molecule (N-CAM).Proc. Nat. Acad. Sci: USA 81, 5584–5588.

  82. Murray B. A., Hemperly J. J., Prediger E. A., Edelman G. M., and Cunningham B. A. (1986) Alternatively spliced mRNAs code for different polypeptide chains of the chicken neural cell adhesion molecule (N-CAM).J. Cell Biol. 102, 189–193.

  83. Ophir I., Moscona A. A., and Ben-Shaul Y. (1983) Localization of retina cognin in embryonic neural retina tissue by immuno-scanning electron microscopy.Cell Differ. 13, 133–141.

  84. Papermaster D. S., Schneider B. G., and Besharse J. (1985) Vesicular transport of newly synthesized opsin from the golgi apparatus toward the rod outer segment.Invest. Ophthalmol. Vis. Sci. 26, 1386–1404.

  85. Pollerberg G. E., Schachner M., and Davoust J. (1986) Differentiation state-dependent surface mobilities of two forms of the neural cell adhesion molecule.Nature 324, 462–465.

  86. Raff M. C., Miller R. H., and Noble M. (1983) A glial progenitor cell that develops invitro into an astrocyte or an oligodendrocyte depending on culture medium.Nature 303, 390–396.

  87. Raff M. C., Williams B., and Miller R. H. (1984) Thein vitro differentiation of a bipotential glial progenitor cell.EMBO J. 3, 1857–1864.

  88. Rakic P. (1981) Developmental events leading to laminar and areal organization of the neocortex, inThe Organization of the Cerebral Cortex (Schmitt F. O., Worden F. G., Adelman G., and Dennis S. G. eds.) pp. 7–28. MIT, Cambridge, MA.

  89. Raper J. A. and Kapfhammer J. P. (1986) The tissue specificity of contact mediated avoidance between growth cones and axons.Soc. Neurosci. Abstr. 12, 1335.

  90. Regan L. J., Dodd J., Barondes S. H., and Jessell T. M. (1986) Selective expression of endogenous lactose-binding lectins and lactoseries glycoconjugates in subsets of rat sensory neurons.Proc. Nat. Acad. Sci. USA 83, 2248–2252.

  91. Rutishauser U. (1983) Molecular and Biological properties of a neural cell adhesion molecule.Cold Spring Harbor Symp. Quant. Biol. 48, 501–514.

  92. Salton S. R. J., Richter-Landsberg C., Greene L. A., and Shelanski M. L. (1983) Nerve growth factor inducible large external (NILE) glycoprotein: Studies of a central and peripheral neuronal marker.J. Neurosci. 3, 441–454.

  93. Schachner M., Faissner A., Kruse J., Lindner J., Meier D. H., Rathjen F. G., and Wernecke H. (1983) Cell-type specificity and developmental expression of neural cell-surface components involved in cell interactions and of structurally related molecules.Cold Spring Harbor Symp. Quant. Biol. 48, 557–568.

  94. Schauer R. (1971) Hydroxylation and O-acetylation ofN-acetylneuraminic acid bound to glycoproteins of isolated subcellular membranes from porcine and bovine submaxillary glands.Hoppe-Seyler's Z. Physiol. Chem. 352, 1282–1290.

  95. Schlosshauer B., Schwartz U., and Rutishauser U. (1984) Topological distribution of different forms of neural cell adhesion molecule in the developing chick visual system.Nature 310, 141–143.

  96. Sidman R. L. (1961) Histogenesis of mouse retina studied with thymidine-H3, inStructure of the Eye (Smelser G. K., ed.) pp. 487–506. Academic, London, UK.

  97. Skoff R. P., Price D. L., and Stocks A. (1976) Electron microscopic autoradiographic studies of gliogenesis in rat optic nerve. I. Cell proliferation.J. Comp. Neurol. 169, 291–312.

  98. Sorge L. K., Levy B. T., and Maness P. F. (1984) pp60c-src is developmentally regulated in the neural retina.Cell 36, 249–257.

  99. Sparrow J. R. and Barnstable C. J. (1986) Expression of cell and synapse specific antigens in rat retinal explant culture.Soc. Neurosci. Abstr. 12, 643.

  100. Steinberg M. S. (1964) The problem of adhesive selectivity in cellular interactions, inCellular Membranes in Development. (Locke M. ed.) pp. 321–366. Academic, New York, NY.

  101. Steinberg M. S. and Granger R. E. (1966) The re-acquisition of adhesiveness by trypsinized chick embryonic cellsin vitro.Am. Zool. 6, 337a.

  102. Steinberg R. H., Fisher S. K., and Anderson S. H. (1980) Disc morphogenesis in vertebrate photoreceptors.J. Comp. Neurol. 190, 501–518.

  103. Stroeva O. G. (1960) Experimental analysis of the eye morphogenesis in mammals.J. Embryol. Exp. Morphol. 8, 349–368.

  104. Stryer L. (1985) Molecular design of an amplification cascade in vision.Biopolymers 24, 29–47.

  105. Sulston J. E. (1983) Neuronal cell lineages in the nematodeCaenorhabditis elegans.Cold Spring Harbor symp. Quant. Biol. 48, 443–452.

  106. Takeichi M. (1977) Functional correlation between cell adhesive properties and some cell surface proteins.J. Cell Biol. 75, 464–474.

  107. Takeichi M., Ozaki H. S., Tokumaga K., and Okada T. S. (1979) Experimantal manipulation of cell surface to affect cellular recognition mechanisms.Dev. Biol. 70, 195–205.

  108. Tauchi M. and Masland R. H. (1984) The shape and arrangement of the cholinergic neurons in the rabbit retina.Proc. R. Soc. Lond. B 223, 101–119.

  109. Temple S. and Raff M. C. (1985) Differentiation of a bipotential glial progenitor cell in single cell microculture.Nature 313, 223–225.

  110. Thomas J. B., Bastiani M. J., Bate C. M., and Goodman C. S. (1984) From grasshopper toDrosophila: A common plan for neruonal development.Nature 310, 203–207.

  111. Thomson L. K., Horowitz P. M., Bentley K. L., Thomas D. D., Alderete J. F., and Klebe R. J. (1986) Localization of the ganglioside-binding site of fibronectin.J. Biol. Chem. 261, 5209–5214.

  112. Treisman J. E., Morabito M., and Barnstable C. J. (1987) Developmental expression of opsin, a photoreceptor-specific gene.Proc. Miami Winter Symp. (in press).

  113. Trisler D., Bekenstein J., and Daniels M. P. (1986) Antibody to a molecular marker of cell position inhibits synapse formation in retina.Proc. Nat. Acad. Sci. USA 83, 4194–4198.

  114. Trisler G. D., Schneider M. D., and Nirenberg M. (1981a) A topographic gradient of molecules in retina can be used to identify neuron position.Proc. Nat. Acad. Sci. USA 78, 2145–2149.

  115. Trisler G. D., Schneider M. D., Moskal J. R., and Nirenberg M. (1981b) A gradient of molecules in avian retina with dorsoventral polarity, inMonoclonal Antibodies to Neural Antigens (McKay R., Raff M. C., and Reichardt L. F., eds.) pp. 231–245.Cold-Spring Harbor, New York.

  116. Troccoli N. M. and Housman R. E. (1985) Vesicle interactions as a model for the retinal cell-cell recognition mediated by R-cognin.Cell Differ.16, 43–49.

  117. Van Veen T., Katial A., Shinohara T., Barrett D. J., Wiggert B., Chader G. J., and Nickerson J. M. (1986) Retinal photoreceptor neurons and pinealocyutes accumulate mRNA for interphotoreceptor retinoid binding protein (IRBP).FEBS Lett. 208, 133–137.

  118. Vardimon L., Fox L. E., and Moscona A. A. (1986) Accumulation of c-src mRNA is developmentally regulated in embryonic neural retina.Mol. Cell. Biol. 6, 4109–4111.

  119. Vaughan D. K. and Fisher S. K. (1985) Distribution of F-actin in retinal cells.Invest. Ophthalmol. Vis. Sci. 26 (suppl.), 248.

  120. Vollmer G. and Layer P. G. (1986) Anin vitro model of proliferation and differentiation of the chick retina: Coaggregtes of retinal and pigment epithelial cells. J. Neurosci.6, 1885–1896.

  121. Wagner J. A. and D'Amore P. A. (1986) Neurite out-growth induced by an endothelial cell mitogen isolated from retina.J. Cell biol. 103, 1363–1367.

  122. Walicke P., Cowan W. M., Ueno N., Baird A., and Guillemin R. (1986) Fibroblast growth factor promotes survival of dissociated hippocampal neurons and enhances neurite extention.Proc. Nat. acad. Sci. USA 83, 3012–3016.

  123. Wang J. W. and Hilfer S. R. (1982) The effect of inhibitors of glycoconjugate synthesis on optic cup formation in the chick embryo. Dev. Biol.,92, 41–53.

  124. Wässle H. and Riemann H. J. (1978) The mosaic of nerve cells in the mammalian retina.Proc. R. Soc. Lond. B 200, 441–461.

  125. Weidman T. A. and Kuwabara T. (1968) Postnatal development of the rat retina. An electron microscopic study.Arch. Ophthalmol. 79, 470–484.

  126. Yoshida M., Kawai S., and Toyoshima K. (1980) Uninfected avian cells contain structurally unrelated progenitors of viral sarcoma genes.Nature 287, 653–654.

  127. Young R. W. (1985) Cell differentiation in the retina of the mouse.Anat. Rec. 21, 199–205.

Download references

Author information

Correspondence to Colin J. Barnstable.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Barnstable, C.J. A molecular view of vertebrate retinal development. Mol Neurobiol 1, 9 (1987). https://doi.org/10.1007/BF02935263

Download citation

Index Entries

  • Vertebrate retinal development
  • retinal development, in vertebrates
  • development, of the vertebrate retina
  • embryonic retina
  • optic cup formation
  • optic stalk
  • retinal lamination
  • positional information within the retina
  • axon outgrowth cues, retinal
  • cell adhesion molecules, retinal
  • photoreceptor development
  • proto-oncogenes and growth factors, retinal