Skip to main content
SpringerLink
Log in

Immunolocalization of cellular retinol-, retinaldehyde- and retinoic acid-binding proteins in rat retina during pre- and postnatal development

  • Published:
Journal of Neurocytology

Summary

Cellular retinol-, retinaldehyde- and retinoic acid-binding proteins were localized in rat retina during pre- and postnatal development by indirect immunofluorescence. Cryostat tissue sections were prepared daily from embryonic day 11 until the day of birth (E11–22) and from postnatal days 1–32 (P1–32). Cellular retinaldehyde- and retinol-binding proteins were first detected in retinal pigment epithelium on E13 and E18, respectively, and in Müller cells at P1 and P15. Parallel studies showed that in adult retina cellular retinoic acid-binding protein is present in a subpopulation of GABAergic amacrine cells. During retinal differentiation, cellular retinoic acid-binding protein was first detected at E18 in cells sclerad to the developing inner plexiform layer, suggesting that this binding protein is expressed in amacrine cells very early during differentiation. During early ocular morphogenesis, cellular retinoic acid-binding protein was present in mesenchymal cells enveloping the eye (E12–15), in the neuroblastic layer of the retina (E13–15), in the nerve fibre layer (E14–15), and the developing optic nerve (E15). Our results suggest that retinoic acid, the natural ligand of cellular retinoic acid-binding protein, may be involved in neuronal differentiation in the inner retina. The studies further support a role for cellular retinoic acid-binding protein in mediating the effects of retinoic acid on developing neural crest cells and raise new questions about the role of cellular retinaldehyde-binding protein in the visual cycle and during development.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Blaner, W. S., Das, K., Mertz, J. R., Das, S. R. &Goodman, D. S. (1986) Effects of dietary retinoic acid on cellular retinol- and retinoic acid-binding protein levels in various rat tissues.Journal of Lipid Research 27, 1084–8.

    PubMed  Google Scholar 

  • Bok, D., Ong, D. E. &Chytil, F. (1984) Immunocytochemical localization of cellular retinol-binding proteins in the rat retina.Investigative Ophthalmology and Visual Science 25, 877–83.

    PubMed  Google Scholar 

  • Bunt-Milam, A. H. &Saari, J. C. (1983) Immunocytochemical localization of two retinoid-binding proteins in vertebrate retina,Journal of Cell Biology 97, 703–12.

    PubMed  Google Scholar 

  • Carter-Dawson, L., Alvarez, R. A., Fong, S.-L., Liou, G. I., Sperling, H. G. &Bridges, C. D. B. (1986) Rhodopsin, 11-cis vitamin A, and interstitial retinolbinding protein (IRBP) during retinal development in normal andrd mutant mice.Developmental Biology 116, 431–8.

    PubMed  Google Scholar 

  • Chytil, F. &Ong, D. E. (1984) Cellular retinoid-binding proteins. InThe Retinoids (edited bySporn, M. B., Roberts, A. B. &Goodman, D. S.), Vol. 2, pp. 90–123. San Diego: Academic Press.

    Google Scholar 

  • Chytil, F. &Ong, D. E. (1987) Intracellular vitamin Abinding. proteins.Annual Review of Nutrition 7, 321–35.

    PubMed  Google Scholar 

  • Cullum, M. E., Johnson, B. C. &Zile, M. H. (1984) Comparison of fetal and adult retinol and retinoic acid binding proteins in bovine serum and pigment epithelium.International Journal of Vitamin and Nutrition Research 54, 297–305.

    Google Scholar 

  • Dencker, L., D'Argy, R., Danielsson, B. R. G., Ghantous, H. &Sperber, G. O. (1987) Saturable accumulation of retinoic acid in neural and neural crest derived cells in early embryonic development.Developmental Pharmacology and Therapeutics 10, 212–23.

    PubMed  Google Scholar 

  • Dowling, J. E. &Wald, G. (1960) The biological action of vitamin A acid.Proceedings of the National Academy of Science (USA) 46, 587–608.

    Google Scholar 

  • Eisenfeld, A. J., Bunt-Milam, A. H. &Saari, J. C. (1985) Localization of retinoid-binding proteins in developing rat retina.Experimental Eye Research 41, 299–304.

    PubMed  Google Scholar 

  • Floyd, E. E. &Jetten, A. M. (1988) Editorial. Retinoids, growth factors, and the tracheobronchial epithelium.Laboratory Investigation 59, 1–4.

    PubMed  Google Scholar 

  • Fuchs, E. (1988) Keratins as biochemical markers of epithelial differentiation.Trends in Genetics 4, 277–81.

    PubMed  Google Scholar 

  • Gaur, V. P., De Leeuw, A. M., Milam, A. H. &Saari, J. C. (1990) Localization of cellular retinoic acid-binding protein to amacrine cells of rat retina.Experimental Eye Research (in press).

  • Gaur, V. P., Saari, J. C., Bunt-Milam, A. H. &Garwin, G. G. (1986) Monoclonal antibodies against bovine cellular retinaldehyde-binding protein. Characterization and use in immunocytochemistry.Investigative Ophthalmology and Visual Science (Supplement) 27, 191.

    Google Scholar 

  • Giguere, V., Ong, E. S., Segui, P. &Evans, R. M. (1987) Identification of a receptor for the morphogen retinoic acid.Nature 330, 624–9.

    PubMed  Google Scholar 

  • Giguere, V., Ong, E. S., Evans, R. M. &Tabin, C. J. (1989) Spatial and temporal expression of the retinoic acid receptor in the regenerating amphibian limb.Nature 337, 566–9.

    PubMed  Google Scholar 

  • Goodman, D. S. (1984) Vitamin A and retinoids in health and disease.New England Journal of Medicine 310, 1023–31.

    PubMed  Google Scholar 

  • Grün, G. (1982) The development of the vertebrate retina: a comparative survey.Advances in Anatomy, Embryology and Cell Biology 78, 1–83.

    Google Scholar 

  • Lund, R. D. &Bunt, A. H. (1976) Prenatal development of central optic pathways in albino rats.Journal of Comparative Neurology 165, 247–64.

    PubMed  Google Scholar 

  • Maden, M., Ong, D. E., Summerbell, D. &Chytil, F. (1988) Spatial distribution of cellular protein binding to retinoic acid in the chick limb bud.Nature 335, 733–5.

    PubMed  Google Scholar 

  • Milam, A. H., de Leeuw, A. M., Gaur, V. P. &Saari, J. C. (1990) Immunolocalization of cellular retinoic acidbinding protein to Müller cells and/or a subpopulation of GABA positive amacrine cells in retinas of different species.Journal of Comparative Neurology (in press).

  • Momoi, T., Kitamoto, T., Kasuya-Sato, J., Seno, H. &Momoi, M. (1989) Developmental changes in the expression of cellular retinoic acid binding protein (CRABP) in the central nervous system of the chick embryo.Biomedical Research 10, 43–8.

    Google Scholar 

  • Ong, D. E., Crow, J. A. &Chytil, F. (1982) Radioimmunochemical determination of cellular retinol- and retinoic acid-binding proteins in cytosols of rat tissues.Journal of Biological Chemistry 257, 13385–9.

    PubMed  Google Scholar 

  • Petkovich, M., Brand, N. J., Krust, A. &Chambon, P. (1987) A human retinoic acid receptor which belongs to the family of nuclear receptors.Nature 330, 444–50.

    PubMed  Google Scholar 

  • Pratt, R. M., Goulding, E. H. &Abbott, B. D. (1987) Retinoic acid inhibits migration of cranial neural crest cells in the cultured mouse embryo.Journal of Craniofacial Genetics and Developmental Biology 7, 205–17.

    PubMed  Google Scholar 

  • Roberts, A. B. &Sporn, M. B. (1984) Cellular biology and biochemistry of the retinoids. InThe Retinoids (edited bySporn, M. B., Roberts, A. B. &Goodman, D. S.), Vol. 2, pp. 210–86. San Diego: Academic Press.

    Google Scholar 

  • Saari, J. C. (1989) Enzymes and proteins of the visual cycle. InProgress in Retinal Research (edited byOsborne, N. N. &Chader, G. J.), Vol. 8 (in press). Oxford: Pergamon Press.

    Google Scholar 

  • Saari, J. C. &Bredberg, D. L. (1982) Enzymatic reduction of 11-cis-retinal bound to cellular retinal-binding protein.Biochimica et Biophysica Acta 716, 266–72.

    PubMed  Google Scholar 

  • Saari, J. C., Bredberg, L. &Garwin, G. G. (1982) Identification of the endogenous retinoids associated with three cellular retinoid-binding proteins from bovine retina and retinal pigment epithelium.Journal of Biological Chemistry 257, 13329–33.

    PubMed  Google Scholar 

  • Saari, J. C., Bunt-Milam, A. H., Bredberg, L. &Garwin, G. G. (1984) Properties and immunocytochemical localization of three retinoid-binding proteins from bovine retina.Vision Research 24, 1595–1603.

    PubMed  Google Scholar 

  • Saari, J. C. &Futterman, S. (1976) Separable binding proteins for retinoic acid and retinol in bovine retina.Biochimica et Biophysica Acta 444, 789–93.

    PubMed  Google Scholar 

  • Saari, J. C., Futterman, S. &Bredberg, L. (1978) Cellular retinol- and retinoic acid-binding proteins of bovine retina.Journal of Biological Chemistry 253, 6432–6.

    PubMed  Google Scholar 

  • Thaller, C. &Eichele, G. (1987) Identification and spatial distribution of retinoids in the developing chick limb bud.Nature 327, 625–8.

    PubMed  Google Scholar 

  • Wald, G. (1968) The molecular basis of visual excitation.Nature 219, 800–7.

    PubMed  Google Scholar 

  • Wiggert, B., Bergsma, D. R., Helmsen, R. &Chader, G. J. (1978) Vitamin A receptors. Retinoic acid binding in ocular tissues.Biochemical Journal 169, 87–94.

    PubMed  Google Scholar 

  • Wiley, M. J., Cauwenbergs, P. &Taylor, I. M. (1983) Effects of retinoic acid on the development of the facial skeleton in hamsters: early changes involving cranial neural crest cells.Acta Anatomica 116, 180–92.

    PubMed  Google Scholar 

  • Wolbach, S. B. &Howe, P. R. (1925) Tissue changes following deprivation of fat soluble A vitamin.Journal of Experimental Medicine 42, 753–77.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Ophthalmology, University of Washington, 98195, Seattle, WA, USA

    A. M. De Leeuw, V. P. Gaur, J. C. Saari & A. H. Milam

  2. Department of Biochemistry, University of Washington, 98195, Seattle, WA, USA

    J. C. Saari

  3. Anatomy Department, Bowman Gray School of Medicine, Winston-Salem, USA

    V. P. Gaur

Authors
  1. A. M. De Leeuw
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. V. P. Gaur
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. C. Saari
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. A. H. Milam
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

De Leeuw, A.M., Gaur, V.P., Saari, J.C. et al. Immunolocalization of cellular retinol-, retinaldehyde- and retinoic acid-binding proteins in rat retina during pre- and postnatal development. J Neurocytol 19, 253–264 (1990). https://doi.org/10.1007/BF01217303

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01217303

Keywords

Search

Navigation