Biochemical properties of purified human retinol dehydrogenase 12 (RDH 12): Catalytic efficiency toward retinoids and C9 aldehydes and effects of cellular retinol-binding protein type I (CRBPI) and cellular retinaldehyde-binding protein (CRALBP) on the oxidation and reduction of retinoids

Biochemistry

Volumn 44, Issue 18, 2005, Pages 7035-7047

  Belyaeva, Olga V ^a   Korkina, Olga V ^a   Stetsenko, Anton V ^a,e   Kim, Tom ^b,c   Nelson, Peter S ^b,c   Kedishvili, Natalia Y ^a,d  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c Fred Hutchinson Cancer Research Center   (United States)

^d UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^e UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALDEHYDES; BINDING ENERGY; CATALYSIS; OXIDATION; PEROXIDES; SUBSTRATES;

HUMAN RETINOL; LEBER CONGENITAL AMAUROSIS 3 (LCA); RETINOIDS; RETINOL DEHYDROGENASE;

PROTEINS;

ALDEHYDE; CELLULAR RETINOL BINDING PROTEIN; PROTEIN CELLULAR RETINALDEHYDE BINDING PROTEIN; PROTEIN RETINOL DEHYDROGENASE 12; RETINOID; RETINOL DEHYDROGENASE; UNCLASSIFIED DRUG; VITAMIN BINDING PROTEIN;

ARTICLE; BINDING AFFINITY; CATALYSIS; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME BINDING; ENZYME KINETICS; ENZYME SPECIFICITY; HUMAN; HUMAN TISSUE; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; TISSUE SPECIFICITY;

ALCOHOL OXIDOREDUCTASES; ALDEHYDES; CARRIER PROTEINS; CATALYSIS; HISTIDINE; HUMANS; KINETICS; MUTAGENESIS, INSERTIONAL; ORGAN SPECIFICITY; OXIDATION-REDUCTION; PHOTORECEPTORS, VERTEBRATE; PROTEIN BINDING; RETINA; RETINALDEHYDE; RETINOIDS; RETINOL-BINDING PROTEINS;

EID: 18244398944     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi050226k     Document Type: Article

References (67)

1. Haeseleer, F., Jang, G.-F., Imanishi, Y., Driessen, C. A. G. G., Matsumura, M., Nelson, P. S., and Palczewski, K. (2002) Dual-substrate specificity short chain retinol dehydrogenases from the vertebrate retina, J. Biol. Chem. 277, 45537-45546.
2. Janecke, A. R., Thompson, D. A., Utermann, G., Becker, C., Hubner, C. A., Schmid, E., McHenry, C. L., Nair, A. R., Ruschendorf, F., Heckenlively, J., Wissinger, B., Nurnberg, P., and Gal, A. (2004) Mutations in RDH12 encoding a photoreceptor cell retinol dehydrogenase cause childhood-onset severe retinal dystrophy, Nat. Genet. 36, 850-854.
3. Perrault, I., Hanein, S., Gerber, S., Barbet, F., Ducroq, D., Dollfus, H., Hamel, C., Dufier, J. L., Munnich, A., Kaplan, J., and Rozet, J. M. (2004) Retinal dehydrogenase 12 (RDH12) mutations in Leber congenital amaurosis, Am. J. Hum. Genet. 75, 639-646.
4. Noy, N. (2000) Retinoid-binding proteins: mediators of retinoid action, Biochem. J. 348, 481-495.
5. Folli, C., Calderone, V., Ottonello, S., Bolchi, A., Zanotti, G., Stoppini, M., and Berni, R. (2001) Identification, retinoid binding, and X-ray analysis of a human retinol-binding protein, Proc. Natl. Acad. Sci. U.S.A. 98, 3710-3715.
6. Vogel, S., Mendelsohn, C. L., Mertz, J. R., Piantedosi, R., Waldburger, C., Gottesman, M. E., and Blaner, W. S. (2001) Characterization of a new member of the fatty acid-binding protein family that binds all-trans-retinol, J. Biol. Chem. 276, 1353-1360.
7. Folli, C., Calderone, V., Ramazzina, I., Zanotti, G., and Berni, R. (2002) Ligand binding and structural analysis of a human putative cellular retinol-binding protein, J. Biol. Chem. 277, 41970-41977.
8. MacDonald, P. N., and Ong, D. E. (1987) Binding specificities of cellular retinol-binding protein and cellular retinol-binding protein, type II, J. Biol. Chem. 262, 10550-10556.
9. Levin, M. S., Locke, B., Yang, N. C., Li, E., and Gordon, J. I. (1988) Comparison of the ligand binding properties of two homologous rat apocellular retinol-binding proteins expressed in Escherichia coli, J. Biol. Chem. 263, 17715-17723.
10. Li, E., Qian, S. J., Winter, N. S., d'Avignon, A., Levin, M. S., and Gordon, J. I. (1991) Fluorine nuclear magnetic resonance analysis of the ligand binding properties of two homologous rat cellular retinol-binding proteins expressed in Escherichia coli, J. Biol. Chem. 266, 3622-3629.
11. Golovleva, I., Bhattacharya, S., Wu, Z., Shaw, N., Yang, Y., Andrabi, K., West, K. A., Burstedt, M. S., Forsman, K., Holmgren, G., Sandgren, O., Noy, N., Qin, J., and Crabb, J. W. (2003) Disease-causing mutations in the cellular retinaldehyde binding protein tighten and abolish ligand interactions, J. Biol. Chem. 278, 12397-12402.
12. Saari, J. C. (1990) Enzymes and proteins of the mammalian visual cycle, in Progress in Retinal Research (Osborn, N., Chader, G., Eds.) Vol. 9, pp 363-381, Pergamon Press, Oxford, U.K.
13. Intres, R., Goldflam, S., Cook, J. R., and Crabb, J. W. (1994) Molecular cloning and structural analysis of the human gene encoding cellular retinaldehyde-binding protein, J. Biol. Chem. 269, 25411-25418.
14. Napoli, J. L. (1999) Interactions of retinoid binding proteins and enzymes in retinoid metabolism, Biochim. Biophys. Acta 1440, 139-162.
15. Lin, B., White, J. T., Ferguson, C., Wang, S., Vessella, R., Bumgarner, R., True, L. D., Hood, L., and Nelson, P. S. (2001) Prostate short-chain dehydrogenase reductase 1 (PSDR1): a new member of the short-chain steroid dehydrogenase/reductase family highly expressed in normal and neoplastic prostate epithelium, Cancer Res. 61, 1611-1618.
16. Kedishvili, N. Y., Chumakova, O. V., Chetyrkin, S. V., Belyaeva, O. V., Lapshina, E. A., Lin, D. W., Matsumura, M., and Nelson, P. S. (2002) Evidence that the human gene for prostate short-chain dehydrogenase/reductase (PSDR1) encodes a novel retinal reductase (RalR1), J. Biol. Chem. 277, 28909-28915.
17. Belyaeva, O. V., Stetsenko, A. V., Nelson, P., and Kedishvili, N. Y. (2003) Properties of short-chain dehydrogenase/reductase RalR1: characterization of purified enzyme, its orientation in the microsomal membrane, and distribution in human tissues and cell lines, Biochemistry 42, 14838-14845.
18. Kasus-Jacobi, A., Ou, J., Bashmakov, Y. K., Shelton, J. M., Richardson, J. A., Goldstein, J. L., and Brown, M. S. (2003) Characterization of mouse short-chain aldehyde reductase (SCALD), an enzyme regulated by sterol regulatory element-binding proteins, J. Biol. Chem. 278, 32380-32389.
19. Esterbauer, H., Schaur, R. J., and Zollner, H. (1991) Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes, Free Radical Biol. Med. 11, 81-128.
20. Winkler, B. S., Boulton, M. E., Gottsch, J. D., and Sternberg, P. (1999) Oxidative damage and age-related macular degeneration, Mol. Vision 5, 32-42.
21. Bok, D. (2002) New insights and new approaches toward the study of age-related macular degeneration, Proc. Natl. Acad. Sci. U.S.A. 99, 14619-14621.
22. Beatty, S., Koh, H., Phil, M., Henson, D., and Boulton, M. (2000) The role of oxidative stress in the pathogenesis of age-related macular degeneration, Surv. Ophthalmol. 45, 115-134.
23. Nowak, M., Swietochowska, E., Wielkoszynski, T., Marek, B., Karpe, J., Gorski, J., Glogowska-Szelag, J., Kos-Kudla, B., and Ostrowska, Z. (2003) Changes in blood antioxidants and several lipid peroxidation products in women with age-related macular degeneration, Eur. J. Ophthalmol. 13, 281-286.
24. +-dependent dehydrogenase that oxidizes all-trans-retinol and 3α-hydroxysteroids, J. Biol. Chem. 273, 19778-19785.
25. Chetyrkin, S. V., Belyaeva, O. V., Gough, W. H., and Kedishvili, N. Y. (2001) Characterization of a novel type of human microsomal 3α- hydroxysteroid dehydrogenase: unique tissue distribution and catalytic properties, J. Biol. Chem. 276, 22278-22286.
26. Chetyrkin, S. V., Hu, J., Gough, W. H., Dumaual, N., and Kedishvili, N. Y. (2001) Further characterization of human microsomal 3α-hydroxysteroid dehydrogenase, Arch. Biochem. Biophys. 386, 1-10.
27. Lowry, O. H., Rosebrough, N. H., Farr, A. L., and Randall, R. J. (1951) Protein measurement with the Folin phenol reagent, J. Biol. Chem. 193, 265-275.
28. Lapshina, E. A., Belyaeva, O. V., Chumakova, O. V., and Kedishvili, N. Y. (2003) Differential recognition of the free versus bound retinol by human microsomal retinol/sterol dehydrogenases: characterization of the holo-CRBP dehydrogenase activity of RoDH-4, Biochemistry 42, 776-784.
29. Leatherbarrow, R. J. (1989-1992) GraFit user's guide, Erithacus Software Limited, London, UK.
30. Livak, K. J., and Schmittgen, T. D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method, Methods 25, 402-408.
31. McBee, J. K., Van Hooser, J. P., Jang, G. F., and Palczewski, K. (2001) Isomerization of 11-cis-retinoids to all-trans-retinoids in vitro and in vivo, J. Biol. Chem. 276, 48483-48493.
32. Urbach, J., and Rando, R. R. (1994) Isomerization of all-trans-retinoic acid to 9-cis-retinoic acid, Biochem. J. 299, 459-465.
33. Wang, X., Penzes, P., and Napoli, J. L. (1996) Cloning of a cDNA encoding an aldehyde dehydrogenase and its expression in Escherichia coli. Recognition of retinal as substrate, J. Biol. Chem. 271, 16288-16293.
34. Posch, K. C., Burns, R. D., and Napoli, J. L. (1992) Biosynthesis of all-trans-retinoic acid from retinal. Recognition of retinal bound to cellular retinol binding protein (type I) as substrate by a purified cytosolic dehydrogenase, J. Biol. Chem. 267, 19676-19682.
35. Wang, J., Chai, X., Eriksson, U., and Napoli, J. L. (1999) Activity of human 11-cis-retinol dehydrogenase (Rdh5) with steroids and retinoids and expression of its mRNA in extra-ocular human tissue, Biochem. J. 338, 23-27.
36. Saari, J. C. (1994) Retinoids in photosensitive system, in The Retinoids: Biology, Chemistry and Medicine (Sporn, M. B., Roberts, A. B., Goodman, D. S., Eds), pp 351-385, Raven Press, New York.
37. Belyaeva, O. V., and Kedishvili, N. Y. (2002) Human pancreas protein 2 (PAN2) has a retinal reductase activity and is ubiquitously expressed in human tissues, FEBS Lett. 531, 489-493.
38. Fex, G., and Johannesson, G. (1984) Radioimmunological determination of cellular retinol-binding protein in human tissue extracts, Cancer Res. 44, 3029-3032.
39. Ong, D. E., and Page, D. L. (1986) Quantitation of cellular retinol-binding protein in human organs, Am. J. Clin. Nutr. 44, 425-430.
40. Eskild, W., Troen, G., Blaner, W. S., Nilsson, A., and Hansson, V. (2000) Evidence for independent control at the mRNA and protein levels of cellular retinol binding protein 1 in rat Sertoli cells, J. Reprod. Fertil. 119, 101-109.
41. Kedishvili N. Y. (2002) Multifunctional nature of human retinol dehydrogenases, Curr. Org. Chem. 6, 1247-1257.
42. Julia, P., Farres, J., and Pares, X. (1983) Purification and partial characterization of a rat retina alcohol dehydrogenase active with ethanol and retinol, Biochem. J. 213, 547-550.
43. Yang, Z. N., Davis, G. J., Hurley, T. D., Stone, C. L., Li, T. K., and Bosron, W. F. (1994) Catalytic efficiency of human alcohol dehydrogenases for retinol oxidation and retinal reduction, Alcohol.: Clin. Exp. Res. 18, 587-591.
44. Molotkov, A., Deltour, L., Foglio, M. H., Cuenca, A. E., and Duester, G. (2002) Distinct retinoid metabolic functions for alcohol dehydrogenase genes Adh1 and Adh4 in protection against vitamin A toxicity or deficiency revealed in double null mutant mice, J. Biol. Chem. 277, 13804-13811.
45. Crosas, B., Hyndman, D. J., Gallego, O., Martras, S., Pares, X., Flynn, T. G., and Farres, J. (2003) Human aldose reductase and human small intestine aldose reductase are efficient retinal reductases: consequences for retinoid metabolism, Biochem. J. 373, 973-979.
46. Simon, A., Hellman, U., Wernstedt, C., and Eriksson, U. (1995) The retinal pigment epithelial-specific 11-cis retinol dehydrogenase belongs to the family of short chain alcohol dehydrogenases, J. Biol. Chem. 270, 1107-1112.
47. Chai, X., Boerman, M. H., Zhai, Y., and Napoli, J. L. (1995) Cloning of a cDNA for liver microsomal retinol dehydrogenase. A tissue-specific, short-chain alcohol dehydrogenase, J. Biol. Chem. 270, 3900-3904.
48. Haeseleer, F., Huang, J., Lebioda, L., Saari, J. C., and Palczewski, K. (1998) Molecular characterization of a novel short-chain dehydrogenase/reductase that reduces all-trans-retinal, J. Biol. Chem. 273, 21790-21799.
49. Rattner, A., Smallwood, P. M., and Nathans, J. (2000) Identification and characterization of all-trans-retinol dehydrogenase from photoreceptor outer segments, the visual cycle enzyme that reduces all-trans-retinal to all-trans-retinol, J. Biol. Chem. 275, 11034-11043.
50. Wu, B. X., Chen, Y., Chen, Y., Fan, J., Rohrer, B., Crouch, R. K., and Ma, J. X. (2002) Cloning and characterization of a novel all-trans retinol short-chain dehydrogenase/reductase from the RPE, Invest. Ophthalmol. Visual Sci. 43, 3365-3372.
51. Bok, D., Ong, D. E., and Chytil, F. (1984) Immunocytochemical localization of cellular retinol binding protein in the rat retina, Invest. Ophthalmol Visual Sci. 25, 877-883.
52. Bunt-Milam, A. H., and Saari, J. C. (1983) Immunocytochemical localization of two retinoid-binding proteins in vertebrate retina, J. Cell Biol. 97, 703-712.
53. Saari, J. C., Bunt-Milam, A. H., Bredberg, D. L., and Garwin, G. G. (1984) Properties and immunocytochemical localization of three retinoid-binding proteins from bovine retina, Vision Res. 24, 1595-603.
54. Gonzalez-Fernandez, F. (2002) Evolution of the visual cycle: the role of retinoid-binding proteins, J. Endocrinol. 175, 75-88.
55. Maeda, A., Maeda, T., Imanishi, Y., Kuksa, V., Alekseev, A., Bronson, D. J., Zhang, H., Zhu, L., Sun, W., Saperstein, D. A., Rieke, F., Baehr, W., and Palczewski, K. (2005) Role of photoreceptor-specific retinol dehyrogenase (PRRDH) in the retinoid cycle in vivo, J. Biol. Chem., published online Mar 8, http://www.jbc.org/cgi/reprint/M501757200v1.
56. Blomstrand, R., Ingemansson, S. O., Jensen, M., and Hedstrom, C. G. (1984) Normal electroretinogram and no toxicity signs after chronic and acute administration of the alcohol dehydrogenase inhibitor 4-methylpyrazole to the cynomolgus monkey (Macaca fascicularis)-a possible new treatment of methanol poisoning, Drug Alcohol Depend. 13, 9-20.
57. Akagi, Y., Yajima, Y., Kador, P. F., Kuwabara, T., and Kinoshita, J. H. (1984) Localization of aldose reductase in the human eye, Diabetes 33, 562-566.
58. Wyss, A. (2004) Carotene oxygenases: a new family of double bond cleavage enzymes, J. Nutr. 134, 246S-250S.
59. Matschinsky, F. M. (1968) Quantitative histochemistry of nicotinamide adenine nucleotides in retina of monkey and rabbit, J. Neurochem. 15, 643-657.
60. Veech, R. L., Eggleston, L. V., and Krebs, H. A. (1969) The redox state of free nicotinamide-adenine dinucleotide phosphate in the cytoplasm of rat liver, Biochem. J. 115, 609-619.
61. Esterbauer, H. (1993) Cytotoxicity and genotoxicity of lipid-oxidation products, Am. J. Clin. Nutr. 57, 779S-786S.
62. Bazan, N. G. (1990) Supply of n-3 polyunsaturated fatty acids and their significance in the central nervous system, in Nutrition and the Brain, (Wurtman, R. J., and Wurtman, J. J., Eds.) Vol. 8, pp 1-24 Raven, New York.
63. Anderson, R. E., Maude, M. B., McClellan, M., Matthes, M. T., Yasumura, D., and LaVail, M. M. (2002) Low docosahexaenoic acid levels in rod outer segments of rats with P23H and S334ter rhodopsin mutations, Mol. Vision 8, 351-358.
64. Luckey, S. W., and Petersen, D. R. (2001) Metabolism of 4-hydroxynonenal by rat Kupffer cells, Arch. Biochem. Biophys. 389, 77-83.
65. Srivastava, S., Chandra, A., Wang, L. F., Seifert, W. E., Jr., DaGue, B. B., Ansari, N. H., Srivastava, S. K., and Bhatnagar, A. (1998) Metabolism of the lipid peroxidation product, 4-hydroxy-trans-2-nonenal, in isolated perfused rat heart, J. Biol. Chem. 273, 10893-10900.
66. Srivastava, S., Dixit, B. L., Cai, J., Sharma, S., Hurst, H. E., Bhatnagar, A., and Srivastava, S. K. (2000) Metabolism of lipid peroxidation product, 4-hydroxynonenal (HNE) in rat erythrocytes: role of aldose reductase, Free Radical Biol. Med. 29, 642-651.
67. Pappa, A., Estey, T., Manzer, R., Brown, D., and Vasiliou, V. (2003) Human aldehyde dehydrogenase 3A1 (ALDH3A1): biochemical characterization and immunohistochemical localization in the cornea, Biochem. J. 376, 615-623.