Disruption of the 11-cis-retinol dehydrogenase gene leads to accumulation of cis-retinols and cis-retinyl esters

Molecular and Cellular Biology

Volumn 20, Issue 12, 2000, Pages 4275-4287

  Driessen, Carola A G G ^a   Winkens, Huub J ^a   Hoffmann, Kirstin ^b   Kuhlmann, Leonoor D ^a   Janssen, Bert P M ^a   Van Vugt, Anke H M ^a   Van Hooser, J Preston ^c   Wieringa, B E ^a   Deutman, August F ^a   Palczewski, Krzysztof ^c,d   Ruether, Klaus ^b   Janssen, Jacques J M ^a  

^a RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^b HUMBOLDT UNIVERSITY   (Germany)

^c UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALITRETINOIN; RETINOL; RETINOL DEHYDROGENASE; RETINOL ESTER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; DARK ADAPTATION; ENZYME ACTIVITY; EYE DISEASE; GENE DISRUPTION; MOUSE; NONHUMAN; PHOTORECEPTOR; PIGMENT EPITHELIUM; PRIORITY JOURNAL; PROTEIN SYNTHESIS;

ALCOHOL OXIDOREDUCTASES; ANIMALS; GENE DELETION; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; MICE; MICE, KNOCKOUT; RETINOIDS; VISION;

ANIMALIA; MURINAE;

EID: 19244379101     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.20.12.4275-4287.2000     Document Type: Article

References (48)

1. Bernstein, P. S., W. C. Law, and R. R. Rando. 1987. Isomerization of all-trans-retinoids to 11-cis-retinoids. Proc. Natl. Acad. Sci. USA 84:1849-1853.
2. Chai, X., Y. Zhai, and J. L. Napoli. 1997. cDNA cloning and characterization of a cis-retinol/3α-hydroxysterol short-chain alcohol dehydrogenase. J. Biol. Chem. 272:33125-33131.
3. Dolle, P., V. Fraulob, P. Kastner, and P. Chambon. 1994. Developmental expression of murine retinoid X receptor (RXR) genes. Mech. Dev. 45:91-104.
4. Driessen, C. A. G. G., A. P. M. Janssen, H. J. Winkens, A. H. M. Van Vugt, A. L. M. De Leeuw, and J. J. M. Janssen. 1995. Cloning and expression of a cDNA encoding bovine retinal pigment epithelial 11-cis-retinol dehydrogenase. Invest. Ophthalmol. Vis. Sci. 36:1988-1996.
5. Driessen, C. A. G. G., H. J. Winkens, E. D. Kuhlmann, A. P. M. Janssen, A. H. M. Van Vugt, A. F. Deutman, and J. J. M. Janssen. 1997. Cloning and structural analysis of the murine GCN5L1 gene. Gene 208:27-31.
6. Driessen, C. A. G. G., H. J. Winkens, E. D. Kuhlmann, A. P. M. Janssen, A. H. M. Van Vugt, A. F. Deutman, and J. J. M. Janssen. 1998. The visual cycle retinol dehydrogenase: possible involvement in the 9-cis-retinoic acid pathway, FEBS Lett. 428:135-140.
7. Goto, Y., N. S. Peachey, H. Ripps, and M. I. Naash. 1995. Functional abnormalities in transgenic mice expressing a mutant rhodopsin gene. Invest. Ophthalmol. Vis. Sci. 36:62-71.
8. Gu, S., D. A. Thompson, S. Srikumari, B. Lorenz, U. Finckh, A. Nicoletti, K. R. Murthy, M. Rathmann, G. Kumaramanickavel, M. J. Denton, and A. Gal. 1997. Mutations in RPE65 cause autusomal recessive childhood-onset severe retinal dystropy. Nat. Genet. 17:194-197.
9. Humphries, M. M., D. Rancourt, G. J. Farrar, P. Kenna, M. Hazel, R. A. Bush, P. A. Sieving, D. M. Sheils, N. McNally, P. Creighton, A. Erven, A. Boros, K. Gulya, M. R. Capecchi, and P. Humphries. 1997. Retinopathy induced in mice by targeted disruption of the rhodopsin gene. Nat. Genet. 15:216-219.
10. Janssen, J. J. M., A. P. M. Janssen, and A. H. M. Van Vugt. 1994. Characterization of monoclonal antibodies recognizing retinal pigment epithelial antigens. Invest. Ophthalmol. Vis. Sci. 35:189-198.
11. Janssen, J. J. M., E. D. Kuhlmann, A. H. M. Van Vugt, H. J. Winkens, A. P. M. Janssen, A. F. Deutman, and C. A. G. G. Driessen. 1999. Retinoic acid receptors and retinoid X receptors in the mature retina: subtype determination and cellular distribution. Curr. Eye Res. 19:338-347.
12. Kelley, M. W., J. K. Turner, and T. A. Reh. 1994. Retinoic acid promotes differentiation of photoreceptors in vitro. Development 120:2091-2102.
13. Kelley, M. W., R. C. Williams, J. K. Turner, J. M. Creech-Kraft, and T. A. Reh. 1999. Retinoic acid promotes rod photoreceptor differentiation in rat retina in vivo. Neuroreport 10:2389-2394.
14. Kirsch, M., M. Y. Lee, V. Meyer, A. Wiese, and H. D. Hofmann. 1997. Evidence for multiple, local functions of ciliary neurotrophic factor (CNTF) in retinal development: expression of CNTF and its receptors and in vitro effects on target cells. J. Neurochem. 68:979-990.
15. Kirsch, M., S. Schulz-Key, A. Wiese, S. Fuhrmann, and H. Hofmann. 1998. Ciliary neurotrophic factor blocks rod photoreceptor differentiation from postmitotic precursor cells in vitro. Cell Tissue Res. 291:207-216.
16. Lem, J., N. V. Krasnoperova, P. D. Calvert, B. Kosaras, D. A. Cameron, M. Nicolo, C. L. Makino, and R. L. Sidman. 1999. Morphological, physiological, and biochemical changes in rhodopsin knock-out mice. Proc. Natl. Acad. Sci. USA 96:736-741.
17. Liou, G. I., Y. Fei, N. S. Peachey, S. Matragoon, S. Wei, W. S. Blaner, Y. Wang, C. Liu, M. E. Gottesman, and H. Ripps. 1998. Early onset photoreceptor abnormalities induced by targeted disruption of the interphotoreceptor retinoid-binding protein gene. J. Neurosci. 18:4511-4520.
18. Marlhens, F., C. Bareil, J. Griffoin, E. Zrenner, P. Amalric, C. Eliaou, S. Liu, E. Harris, T. M. Redmond, B. Arnaud, M. Claustress, and C. P. Hamel. 1997. Mutations in RPE65 cause Leber's congenital amaurosis. Nat. Genet. 17:139-141.
19. Mata, N. L., and A. T. Tsin. 1998. Distribution of 11-cis LRAT, 11-cis RD and 11-cis REH in bovine retinal pigment epithelium membranes. Biochim. Biophys. Acta 1394:16-22.
20. Mata, N. L., E. T. Villazana, and A. T. Tsin. 1998. Colocalization of 11-cis retinyl esters and retinyl ester hydrolase activity in retinal pigment epithelium plasma membrane. Invest. Ophthalmol. Vis. Sci. 39:1312-1319.
21. Maw, M. A., B. Kennedy, A. Knight, R. Bridges, K. E. Roth, E. J. Mani, J. K. Mukkadan, D. Nancarrow, J. W. Crabb, and M. J. Denton. 1997. Mutation of the gene encoding cellular retinaldehyde binding protein in autosomal recessive retinitis pigmentosa. Nat. Genet. 17:198-200.
22. Mertz, J. R., E. Shang, R. Piantedosi, S. Wei, D. J. Wolgemuth, and W. S. Blaner. 1997. Identification and characterization of a stereospecific human enzyme that catalyzes 9-cis-retinol oxidation: a possible role in 9-cis-retinoic acid formation. J. Biol. Chem. 272:11744-11749.
23. Milam, A. H., A. M. De Leeuw, V. P. Gaur, and J. C. Saari. 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. J. Comp. Neurol. 296:123-129.
24. Morimura, H., G. A. Fishmann, S. A. Grover, A. B. Fulton, E. L. Berson, and T. P. Dryja. 1998. Mutations in the RPE65 gene in patients with autosomal recessive retinitis pigmentosa or Leber congenital amaurosis. Proc. Natl. Acad. Sci. USA 95:3088-3093.
25. Nakanishi, T., K. Ishii, N. Fukushima, M. Asanuma, E. Iwata, and N. Ogawa. 1996. Expression of mRNA encoding neurotrophic factors and its regulation in a hybrid neuronal cell line. Biochem. Mol. Biol. Int. 38:763-772.
26. Neophytou, C., A. B. Vernallis, A. Smith, and M. C. Raff. 1997. Müller-cell-derived leukaemia inhibitory factor arrests rod photoreceptor differentiation at a postmitotic pre-rod stage of development. Development 124:2345-2354.
27. Niederreither, K., V. Subbarayan, P. Dolle, and P. Chambon. 1999. Embryonic retinoic acid synthesis is essential for early mouse post-implantation development. Nat. Genet. 21:444-448.
28. Palczewski, K., and J. C. Saari. 1997. Activation and inactivation steps in the visual transduction pathway. Curr. Opin. Neurobiol. 7:500-504.
29. Palczewski, K., J. P. VanHooser, G. G. Garwin, J. Chen, G. I. Liou, and J. C. Saari. 1999. Kinetics of visual pigment regeneration in excised mouse eyes and in mice with a targeted disruption of the gene encoding interphotoreceptor retinoid-binding protein or arrestin. Biochemistry 38:12012-12019.
30. Quadro, L., W. S. Blaner, D. Salchow, S. Vogel, R. Piantedosi, P. Gouras, S. Freeman, M. P. Cosma, V. Colantuoni, and M. E. Gottesman. 1999. Impaired retinal function and vitamin A availability in mice lacking retinol-binding protein. EMBO J. 18:4633-4644.
31. Redmond, T. M., S. Yu, E. Lee, D. Bok, D. Hamasaki, N. Chen, P. Goletz, J. X. Ma, R. K. Crouch, and K. Pfeifer. 1998. RPE65 is necessary for production of 11-cis-vitamin A in the retinal visual cycle. Nat. Genet. 20:344-351.
32. Romert, A., P. Tuvendal, A. Simon, L. Dencker, and U. Eriksson. 1998. The identification of a 9-cis-retinol dehydrogenase in the mouse embryo reveals a pathway for synthesis of 9-cis-retinoic acid. Proc. Natl. Acad. Sci. USA 95: 4404-4409.
33. Saari, J. C., and D. L. Bredberg. 1987. Photochemistry and stereoselectivity of cellular retinaldehyde-binding protein from bovine retina. J. Biol. Chem. 262:7618-7622.
34. Saari, J. C., G. G. Garwin, J. P. Van Hooser, and K. Palczewski. 1998. Reduction of all-trans-retinal limits regeneration of visual pigment in mice. Vision Res. 38:1325-1333.
35. Saari, J. C., G. G. Garwin, F. Haeseleer, G.-F. Jang, and K. Palczewski. 2000. Phase partition and high-performance liquid chromatography assays of retinoid dehydrogenases. Methods Enzymol. 316:359-371.
36. Seeliger, M. W., I. Frank, S. Beck, and E. Zrenner. 1999. Phenotype in retinol deficiency due to a hereditary defect in retinol binding protein biosynthesis. Invest. Ophthalmol. Vis. Sec. 40:3-11.
37. Simon, A., U. Hellman, C. Wernstedt, and U. Eriksson. 1995. The retinal pigment epithelial-specific 11-cis-retinol dehydrogenase belongs to the family of short chain alcohol dehydrogenase. J. Biol. Chem. 270:1107-1112.
38. Simon, A., J. Lagercrantz, S. Bajalica-Lagercrantz, and U. Eriksson. 1996. Primary structure of human 11-cis-retinol dehydrogenase and organization and chromosomal localization of the corresponding gene. Genomics 36:424-430.
39. Simon, A., A. Romert, A. L. Gustafson, J. M. McCaffery, and U. Eriksson. 1999. Intracellular localization and membrane topology of 11-cis retinol dehydrogenase in the retinal pigment epithelium suggest a compartmentalized synthesis of 11-cis retinaldehyde. J. Cell Sci. 112:549-558.
40. Stecher, H., M. H. Gelb, J. C. Saari, and K. Palczewski. 1999. Preferential release of 11-cis-retinol from retinal pigment epithelial cells in the presence of cellular retinaldehyde-binding protein. J. Biol. Chem. 274:8577-8585.
41. Su, J., X. Chai, B. Kahn, and J. L. Napoli. 1998. cDNA cloning, tissue distribution, and substrate characteristics of a cis-retinol/3α-hydroxysterol short-chain dehydrogenase isozyme. J. Biol. Chem. 273:17910-17916.
42. Wang, J., X. Chai, U. Eriksson, and J. L. Napoli. 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.
43. Wendling, O., P. Chambon, and M. Mark. 1999. Retinoid X receptors are essential for early mouse development and placentogenesis. Proc. Natl. Acad. Sci. USA 96:547-551.
44. Weng, J., N. L. Mata, S. M. Azarian, R. T. Tzekov, D. G. Birch, and G. H. Travis. 1999. Insights into the function of rim protein in photoreceptors and etiology of Stargardt's disease from the phenotype in abcr knockout mice. Cell 98:13-23.
45. Winston, A., and R. R. Rando. 1998. Regulation of isomerohydrolase activity in the visual cycle. Biochemistry 37:2044-2050.
46. Yamamoto, H., A. Simon, U. Eriksson, E. Harris, E. L. Berson, and T. P. Dryja. 1999. Mutations in the gene encoding 11-cis-retinol dehydrogenase cause delayed dark adaptation and fundus albipunctatus. Nat. Genet. 22: 188-191.
47. Yang, R. B., S. W. Robinson, W. H. Xiong, K. W. Yau, D. G. Birch, and D. L. Garbers. 1999. Disruption of a retinal guanylyl cyclase gene leads to cone-specific dystrophy and paradoxical rod behavior. J. Neurosci. 19:5889-5897.
48. Zimmerman, W. F., F. Lion, F. J. M. Daemen, and S. L. Bonting. 1975. Biochemical aspects of the visual process. XXX. Distribution of stereospecific dehydrogenase activities in subcellular fractions of the bovine retina and pigment epithelium. Exp. Eye Res. 21:325-332.