Hostname: page-component-586b7cd67f-l7hp2 Total loading time: 0 Render date: 2024-11-27T20:21:23.497Z Has data issue: false hasContentIssue false

Characterization of aldehyde dehydrogenase-positive amacrine cells restricted in distribution to the dorsal retina

Published online by Cambridge University Press:  02 June 2009

Ann H. Milam
Affiliation:
Department of Ophthalmology, University of Washington, Seattle
Daniel E. Possin
Affiliation:
Department of Ophthalmology, University of Washington, Seattle
Jing Huang
Affiliation:
Department of Ophthalmology, University of Washington, Seattle
Robert N. Fariss
Affiliation:
Department of Ophthalmology, University of Washington, Seattle
John G. Flannery
Affiliation:
School of Optometry, University of California, Berkeley
John C. Saari
Affiliation:
Department of Ophthalmology, University of Washington, Seattle Department of Biochemistry, University of Washington, Seattle

Abstract

A class 1 aldehyde dehydrogenase (ALDH) catalyzes oxidation of retinaldehyde to retinoic acid in bovine retina. We used immunocytochemistry and in situ hybridization to localize this enzyme in adult and fetal bovine retinas. Specific ALDH immunoreactivity was present in the cytoplasm of wide-field amacrine cells restricted in distribution to the dorsal part of the adult retina. The somata diameters ranged from ∼8 μ to ∼15 μ, and the cells increased in density from ∼125 cells/mm2 near the horizontal meridian to ∼425 cells/mm2 in the superior far periphery. The ALDH-positive cells had somata on both sides of the inner plexiform layer (IPL) and processes in two IPL strata. The majority of ALDH-positive cells were unreactive with antibodies against known amacrine cell enzymes and neurotransmitters, including GABA and glycine. The ALDH-positive amacrine cells also did not react with anti-cellular retinoic acid-binding protein, which was present in a subset of GABA-positive amacrine cells. In flat-mounted retinas processed by in situ hybridization, the larger ALDH-positive amacrine cells tended to be more heavily labeled. In addition to amacrine cells, Müller cell processes in the inner retina were weakly immunoreactive for ALDH; however, these glial cells did not contain ALDH mRNA. The pattern of ALDH expression in fetal bovine retinas was documented by immunocytochemistry. No ALDH reactivity was found before 5.5 months; for the remainder of the fetal period, ALDH immunoreactivity was present in amacrine cells similar to those in adult retina. The ALDH-positive amacrine cells in bovine retina are novel, being limited in distribution to the dorsal retina and unlabeled with other amacrine cell-specific markers. Identification of ALDH in amacrine cells provides additional evidence that cells of the inner retina are involved in retinoid metabolism.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1997

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Ambroziak, W. & Pietruszko, R. (1993). Metabolic role of aldehyde dehydrogenase. Advances in Experimental Medicine and Biology 328, 515.CrossRefGoogle ScholarPubMed
Bistner, S.I., Rubin, L. & Aguirre, G. (1973). Development of the bovine eye. American Journal of Veterinary Research 34, 112.Google ScholarPubMed
Chun, M.H., Brecha, N. & Wässle, H. (1992). Light- and electron-microscopic studies of the somatostatin-immunoreactive plexus in the cat retina. Cell and Tissue Research 267, 5766.CrossRefGoogle ScholarPubMed
Desjardin, L.E., Timmers, A.M.M. & Hauswirth, W.W. (1993). Transcription of photoreceptor genes during fetal retinal development. Evidence for positive and negative regulation. Journal of Biological Chemistry 268, 69536960.CrossRefGoogle ScholarPubMed
Dockham, P.A., Lee, M.O. & Sladek, N.E. (1992). Identification of human liver aldehyde dehydrogenases that catalyze the oxidation of aldophosphamide and retinaldehyde. Biochemical Pharmacology 43, 24532469.CrossRefGoogle ScholarPubMed
Dowling, J.E. & Wald, G. (1960). The biological action of vitamin A acid. Proceedings of the National Academy of Sciences of the U.S.A. 46, 587608.CrossRefGoogle Scholar
Edwards, R.B. (1994). Biosynthesis of retinoic acid by Müller glial cells: A model for the central nervous system. In Progress in Retinal and Eye Research, Vol. 13, ed. Osborne, N.N. & Chader, G.J., pp. 231242. Oxford: Pergamon Press.Google Scholar
Edwards, R.B., Adler, A.J., Dev, S. & Claycomb, R.C. (1992). Synthesis of retinoic acid from retinol by cultured rabbit Müller cells. Experimental Eye Research 54, 481490.CrossRefGoogle ScholarPubMed
Gaur, V., De Leeuw, A., Milam, A. & Saari, J. (1990). Localization of cellular retinoic acid-binding protein to amacrine cells of rat retina. Experimental Eye Research 50, 505511.CrossRefGoogle ScholarPubMed
Godbout, R., Packer, M., Poppema, S. & Dabbagh, L. (1996). Localization of cytosolic aldehyde dehydrogenase in the developing chick retina: In situ hybridization and immunohistochemical analyses. Developmental Dynamics 205, 319331.3.0.CO;2-#>CrossRefGoogle ScholarPubMed
Harland, R.M. (1991). In situ hybridization: An improved whole mount method for Xenopus embryos. Methods in Cell Biology 36, 685695.CrossRefGoogle ScholarPubMed
Hyatt, G.A., Schmitt, E.A., Marsh-Armstrong, N., Mccaffery, P., Dräger, U.C. & Dowling, J.E. (1996). Retinoic acid establishes ventral retinal characteristics. Development 122, 195204.CrossRefGoogle ScholarPubMed
Hyatt, G.A., Schmitt, E.A., Marsh-Armstrong, N.R. & Dowling, J.E. (1992). Retinoic acid-induced duplication of the zebrafish retina. Proceedings of the National Academy of Sciences of the U.S.A. 89, 82938297.CrossRefGoogle ScholarPubMed
Kastner, P., Grondona, J.M., Mark, M., Gansmuller, A., Lemeur, M., Decimo, D., Vonesch, J.-L., Dolle, P. & Chambon, P. (1994). Genetic analysis of RXR-alpha developmental function: Convergence of RXR and RAR signaling pathways in heart and eye morphogenesis. Cell 78, 9871003.CrossRefGoogle ScholarPubMed
Kelley, M.W., Turner, J.K. & Reh, T.A. (1994). Retinoic acid promotes differentiation of photoreceptors in vitro. Development 120, 20912102.CrossRefGoogle ScholarPubMed
Lee, M.O., Manthey, C.L. & Sladek, N.E. (1991). Identification of mouse liver aldehyde dehydrogenases that catalyze the oxidation of retinaldehyde to retinoic acid. Biochemical Pharmacology 42, 12791285.CrossRefGoogle ScholarPubMed
Marc, R.E. (1986). Neurochemical stratification in the inner plexiform layer of the vertebrate retina. Vision Research 26, 223238.CrossRefGoogle ScholarPubMed
Marsh-Armstrong, N., Mccaffery, P., Gilbert, W., Dowling, J.E. & Dräger, U.C. (1994). Retinoic acid is necessary for development of the ventral retina in zebrafish. Proceedings of the National Academy of Sciences of the U.S.A. 91, 72867290.CrossRefGoogle ScholarPubMed
Masland, R.H., IIIRizzo, J.F. & Sandell, J.H. (1993). Developmental variation in the structure of the retina. Journal of Neuroscience 13, 51945202.CrossRefGoogle ScholarPubMed
Mccaffery, P., Posch, K.C., Napoli, J.L., Gudas, L. & Dräger, U.C. (1993). Changing patterns of the retinoic acid system in the developing retina. Developmental Biology 158, 390399.CrossRefGoogle Scholar
Mccaffery, P., Tempst, P., Lara, G. & Dräger, U.C. (1991). Aldehyde dehydrogenase is a positional marker in the retina. Development 112, 693702.CrossRefGoogle ScholarPubMed
Milam, A.H., Dacey, D.M. & Dizhoor, A.M. (1993). Recoverin immuno-reactivity in mammalian cone bipolar cells. Visual Neuroscience 10, 112.CrossRefGoogle Scholar
Milam, A.H., De Leeuw, A.M., Gaur, V.P. & Saari, J.C. (1990). Immunolocalization of cellular retinoic acid binding protein to Müller cells and/or a subpopulation of GABA-positive amacrine cells in retinas of different species. Journal of Comparative Neurology 296, 123129.CrossRefGoogle ScholarPubMed
Osborne, N.N. & Beaton, D.W. (1986). Direct histochemical localization of 5,7-dihydroxytryptamine and the uptake of serotonin by a subpopulation of GABA neurons in the rabbit retina. Brain Research 382, 158162.CrossRefGoogle Scholar
Redburn, D.A. & Thomas, T.N. (1981). Evidence for a serotonin neuro-transmitter system in bovine retina. Vision Research 21, 16731676.CrossRefGoogle Scholar
Rickman, D.W., Blanks, J.C. & Brecha, N.C. (1996). Somatostatin-immunoreactive neurons in the adult rabbit retina. Journal of Comparative Neurology 365, 491503.3.0.CO;2-U>CrossRefGoogle ScholarPubMed
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, 1332913333.CrossRefGoogle ScholarPubMed
Saari, J.C., Champer, R.J., Asson-Batres, M.A., Garwin, G.G., Huang, J., Crabb, J.W. & Milam, A.H. (1995 a). Characterization and localization of an aldehyde dehydrogenase to amacrine cells of bovine retina. Visual Neuroscience 12, 263272.CrossRefGoogle ScholarPubMed
Saari, J.C., Huang, J., Asson-Batres, M.A., Champer, R.J., Garwin, G., Crabb, J.W., Possin, D.E. & Milam, A.H. (1995 b). Evidence of retinoid metabolism within cells of inner retina. Experimental Eye Research 60, 209212.CrossRefGoogle ScholarPubMed
Sager, S.M. (1987). Somatostatin-like immunoreactive material in the rabbit retina: Immunohistochemical staining using monoclonal antibodies. Journal of Comparative Neurology 266, 291299.CrossRefGoogle Scholar
Stumpf, W., Bidmon, H.-J. & Murakami, R. (1991). Retinoic acid binding sites in adult brain, pituitary, and retina. Naturwissenschaften 78, 561562.CrossRefGoogle ScholarPubMed
Timmers, A.M., Newton, B.R. & Hauswirth, W.W. (1993). Synthesis and stability of retinal photoreceptor mRNAs are coordinately regulated during bovine fetal development. Experimental Eye Research 56, 257265.CrossRefGoogle ScholarPubMed
Vaney, D.I. (1990). The mosaic of amacrine cells in the mammalian retina. In Progress in Retinal Research, Vol. 9, ed. Osborne, N.N. & Chader, G.J., pp. 49100. Oxford: Pergamon Press.Google Scholar
Warkany, M. & Schraffenberger, A.B. (1946). Congenital malformations induced in rats by maternal vitamin A deficiency. Archives of Ophthalmology 35, 150169.CrossRefGoogle ScholarPubMed
WÄssle, H. & Chun, M.H. (1988). Dopaminergic and indoleamine-accumulating amacrine cells express GABA-like immunoreactivity in the cat retina. Journal of Neuroscience 8, 33833394.CrossRefGoogle ScholarPubMed
White, C.A. & Chalupa, L.M. (1992). Ontogeny of somatostatin immunoreactivity in the cat retina. Journal of Comparative Neurology 317, 129144.CrossRefGoogle ScholarPubMed