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Characterization and localization of an aldehyde dehydrogenase to amacrine cells of bovine retina

Published online by Cambridge University Press:  02 June 2009

John C. Saari ,
Robert J. Champer ,
Mary Ann Asson-Batres ,
Gregory G. Garwin ,
Jing Huang ,
John W. Crabb  and
Ann H. Milam
John C. Saari
Affiliation:
Department of Ophthalmology, University of Washington, Seattle Department of Biochemistry, University of Washington, Seattle
Robert J. Champer
Affiliation:
Department of Ophthalmology, University of Washington, Seattle
Mary Ann Asson-Batres
Affiliation:
Department of Ophthalmology, University of Washington, Seattle
Gregory G. Garwin
Affiliation:
Department of Ophthalmology, University of Washington, Seattle
Jing Huang
Affiliation:
Department of Ophthalmology, University of Washington, Seattle
John W. Crabb
Affiliation:
The W. Alton Jones Cell Science Center, Lake Placid
Ann H. Milam
Affiliation:
Department of Ophthalmology, University of Washington, Seattle
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Abstract

An enzyme of bovine retina that catalyzes oxidation of retinaldehyde to retinoic acid was purified to homogeneity and a monoclonal antibody (mAb H-4) was generated. MAb H-4 recognized a single component (Mr = 55,000) in extracts of bovine retina and other bovine tissues. The antibody showed no cross-reactivity with extracts of rat, monkey, or human retinas. A 2067 bp cDNA was selected from a retina cDNA expression library using mAb H-4. The cDNA hybridized with a similarly sized, moderately abundant mRNA prepared from bovine retina. Nucleotide sequence analysis indicated that the cDNA contained a single open reading frame encoding 501 amino acids that have 88% sequence identity with the amino-acid sequence of human hepatic Class 1 aldehyde dehydrogenase. Amino-acid sequence analysis of purified enzyme demonstrated that the cDNA encodes the isolated enzyme. MAb H-4 specifically labeled the somata and processes of a subset of amacrine cells in bovine retinal sections. Labeled amacrine somata were located on both sides of the inner plexiform layer, and their processes ramified into two laminae within the inner plexiform layer. The inner radial processes of Müller (glial) cells were weakly reactive with mAb H-4. Weak immunostaining of amacrine cells was found in monkey retina with mAb H-4, but no signal was detected in rat or human retina. The results provide further evidence for metabolism and function of retinoids within cells of the inner retina and define a novel class of retinal amacrine cells.

Keywords

Aldehyde dehydrogenaseAmacrine cellsRetinaRetinoic acidRetinoids
Type
Research Articles
Information
Visual Neuroscience , Volume 12 , Issue 2 , March 1995 , pp. 263 - 272
Copyright
Copyright © Cambridge University Press 1995

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References

Crabb, J.W., Johnson, C.M., Carr, S.A., Armes, L.G. & Saari, J.C. (1988). The complete primary structure of the cellular retinaldehyde-binding protein from bovine retina. Journal of Biological Chemistry 263, 18678–18687.CrossRefGoogle ScholarPubMed
Duester, G., Shean, M.L., McBride, M.S. & Stewart, M.J. (1991). Retinole acid response element in the human alcohol dehydrogenase gene ADH3: Implications for regulation of retinole acid synthesis. Molecular and Cellular Biology 11, 1638–1646.Google Scholar
Dunn, T.J., Koleske, A.J., Lindahl, R. & Pitot, H.C. (1989). Phenobarbital-inducible aldehyde dehydrogenase in the rat. cDNA sequence and regulation of the mRNA by phénobarbital in responsive rats. Journal of Biological Chemistry 264, 13057–13065.CrossRefGoogle ScholarPubMed
Edwards, R.B. (1994). Biosynthesis of retinoic acid by Muller 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. 231–242. Oxford, U.K.: Pergamon Press, Ltd.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, 481–490.CrossRefGoogle ScholarPubMed
Gaur, V.P., DeLeeuw, A.M., Milam, A.H. & Saari, J.C. (1990). Localization of cellular retinoic acid-binding protein to amacrine cells. Experimental Eye Research 50, 505–511.CrossRefGoogle ScholarPubMed
Godbout, R. (1992). High levels of aldehyde dehydrogenase transcripts in the undifferentiated chick retina. Experimental Eye Research 54, 297–305.CrossRefGoogle ScholarPubMed
Godbout, R. (1993). Identification and characterization of transcripts present at elevated levels in the undifferentiated chick retina. Experimental Eye Research 56, 97–106.CrossRefGoogle ScholarPubMed
Helander, A. & Tottmar, O. (1986). Cellular distribution and properties of human blood aldehyde dehydrogenase. Alcoholism: Clinical and Experimental Research 10, 71–76.CrossRefGoogle ScholarPubMed
Hempel, J., Nicholas, H. & Lindahl, R. (1993). Aldehyde dehydrog-enases: Widespread structural and functional diversity within a shared framework. Protein Science 2, 1890–1900.CrossRefGoogle ScholarPubMed
Hempel, J., Von Bahr-Lindström, H. & Jörnvall, H. (1984). Aldehyde dehydrogenase from human liver. Primary structure of the cytoplasmic enzyme. European Journal of Biochemistry 141, 21–35.CrossRefGoogle Scholar
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, 8293–8297.CrossRefGoogle ScholarPubMed
Kelley, M.W., Turner, J.K. & Reh, T.A. (1994). Retinoic acid promotes differentiation of photoreceptors in vitro. Development 120, 2091–2102.CrossRefGoogle ScholarPubMed
Kochhar, D.M., Penner, J.D. & Tellone, C.I. (1984). Comparative teratogenic activities of two retinoids: Effects on palate and limb development. Teratogenesis, Carcinogenesis, and Mutagenesis 4, 377–387.CrossRefGoogle ScholarPubMed
Labrecque, J., Bhat, P.V. & Lacroix, A. (1993). Purification and partial characterization of a rat kidney aldehyde dehydrogenase that oxidizes retinal to retinic acid. Biochemistry and Cell Biology 71, 85–89.CrossRefGoogle Scholar
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, 1279–1285.CrossRefGoogle ScholarPubMed
Leo, M.A., Kim, C.-L., Lowe, N. & Lieber, C.S. (1989). Increased hepatic retinal dehydrogenase activity after phenobarbital and ethanol administration. Biochemical Pharmacology 38, 97–103.CrossRefGoogle ScholarPubMed
Masland, R.H. (1988). Amacrine cells. Trends in Neuroscience 11, 405–410.CrossRefGoogle ScholarPubMed
Matsudaira, P. (1987). Sequence from picomole quantities of proteins electroblotted onto polyvinylidene membranes. Journal of Biological Chemistry 262, 10035–10038.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, 390–399.CrossRefGoogle Scholar
McCaffery, P., Lee, M.-O., Wagner, M.A., Sladek, N.E. & Dräger, U.C. (1992). Asymmetrical retinoic acid synthesis in the dorsoventral axis of the retina. Development 115, 371–382.CrossRefGoogle ScholarPubMed
McCaffery, P., Tempst, P., Lara, G. & Dräger, U.C. (1991). Aldehyde dehydrogenase is a positional marker in the retina. Development 112, 693–702.CrossRefGoogle ScholarPubMed
Milam, A.H., Deleeuw, A.M., Gaur, V.P. & Saari, J.C. (1990). Localization 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, 123–129.CrossRefGoogle ScholarPubMed
Napoli, J.L. & Race, K.R. (1987). The biosynthesis of retinoic acid from retinol by rat tissues in vitro. Archives of Biochemistry and Biophysics 255, 95–101.CrossRefGoogle ScholarPubMed
Napoli, J.L., Posch, K.P., Fiorella, P.D. & Boerman, M.H.E.M. (1991). Physiological occurrence, biosynthesis and metabolism of retinoic acid: Evidence for roles of cellular retinol-binding protein (CRBP) and cellular retinoic acid-binding protein (CRALBP) in the pathway of retinoic acid homeosynthesis. Biomedicine and Pharmacotherapy 45, 131–143.CrossRefGoogle Scholar
Peterson, D.R. & Lindahl, R. (1993). Mammalian hepatic aldehyde dehydrogenases; An overview. Drug Metabolism Newsletter 23, 2–3.Google Scholar
Pettersson, H. & Tottmar, O. (1982). Aldehyde dehydrogenases in rat brain. Subcellular distribution and properties. Journal of Neurochemistry 38, 477–487.CrossRefGoogle ScholarPubMed
Posch, K.C., Burns, R.D. & Napoli, J.L. (1992). Biosynthesis of all-trans-retinoic acid from retinal. Recognition of retinal bound to eel lular retinol-binding protein (type I) as a substrate by a purified cytosolic dehydrogenase. Journal of Biological Chemistry 267, 19676–19682.CrossRefGoogle Scholar
Posch, K.C., Enrioht, J.W.J. & Napoli, J.L. (1989). Retinoic acid synthesis by cytosol from the alcohol dehydrogenase negative deer-mouse. Archives of Biochemistry and Biophysics 274, 171–178.CrossRefGoogle Scholar
Saari, J.C., Futterman, S. & Bredberg, L. (1978). Cellular retinol-and retinoic acid-binding proteins of bovine retina: Purification and properties. Journal of Biological Chemistry 253, 6432–6436.CrossRefGoogle 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, 13329–13333.CrossRefGoogle ScholarPubMed
Saari, J.C. & Garwin, G.G. (1992). Enzymatic synthesis of retinoic acid in retina. In Retinoids, Progress in Research and Clinical Applications, ed. Livrea, M. & Packer, L., pp. 147–158. New York: Marcel Dekker, Inc.Google Scholar
Saari, J.C., Bredberg, D.L., Garwin, G.G., Buczylko, J., Wheeler, T. & Palczewski, K. (1993). Assays of retinoid dehydrogenases by phase partition. Analytical Biochemistry 213, 128–132.CrossRefGoogle ScholarPubMed
Stone, K.K., McNulty, D.E., Lopresti, M.L., Crawford, J.M., Deangelis, R. & Williams, K.R. (1992). Elution and internal amino acid sequencing of PVDF-blotted proteins. In Techniques in Protein Chemistry III, ed. Angeletti, R.H., pp. 23–34. San Diego, California: Academic Press, Inc.CrossRefGoogle Scholar
Stumpf, W.E., Bidmon, H.-J. & Murakami, R. (1991). Retinoic acid binding sites in adult brain, pituitary, and retina. Naturwissenschaften 78, 561–562.CrossRefGoogle ScholarPubMed
Tsang, S.S., Yin, X., Guzzo-Arkuran, C., Jones, V.S. & Davison, A.J. (1993). Loss of resolution in gel electrophoresis of RNA: A problem associated with the presence of formaldehyde gradient. Biotechniques 14, 380–381.Google Scholar
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. 49–100. Oxford, U.K.: Pergamon Press.Google Scholar
Virca, G.D., Northemann, W., Shiels, R.R., Widera, G. & Broome, S. (1990). Simplified northern blot hybridization using 5% sodium dodecyl sulfate. Biotechniques 8, 370–371.Google ScholarPubMed
Wilkinson, M. (1991). Purification of RNA. In Essential Molecular Biology: A Practical Approach, ed. Brown, T.A., pp. 69–87. Oxford, U.K.: IRL Press.Google Scholar
Yoshida, A., Hsu, L.C. & Davé, V. (1992). Retinal oxidation activity and biological role of human cytosolic aldehyde dehydrogenase. Enzyme 46, 239–244.CrossRefGoogle ScholarPubMed