Aberrant metabolites in mouse models of congenital blinding diseases: Formation and storage of retinyl esters

Biochemistry

Volumn 45, Issue 13, 2006, Pages 4210-4219

  Maeda, Akiko ^a   Maeda, Tadao ^a   Imanishi, Yoshikazu ^a   Golczak, Marcin ^a   Moise, Alexander R ^a   Palczewski, Krzysztof ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL ORGANS; CHROMOPHORES; DISEASE CONTROL; DRUG THERAPY; ESTERS; GENES; TRANSPLANTATION (SURGICAL);

ABERRANT METABOLITES; CONGENITAL BLINDING DISEASES; DARK-ADAPTED CONDITIONS; RETINAL PIGMENT EPITHELIUM (RPE);

METABOLITES;

11 CIS RETINAL; OPSIN; PROTEIN RPE65; RETINOID; RETINOL ESTER; RETINYLAMINE; UNCLASSIFIED DRUG; VISUAL PIGMENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL ORGANELLE; CHROMATOPHORE; CONGENITAL BLINDNESS; CONTROLLED STUDY; DARK ADAPTATION; GENE DISRUPTION; GENE MUTATION; ISOMERIZATION; KNOCKOUT MOUSE; MOUSE; NONHUMAN; PHOTORECEPTOR; PIGMENT EPITHELIUM; PRIORITY JOURNAL; RETINOSOME; VISUAL DISORDER;

ALCOHOL OXIDOREDUCTASES; ANIMALS; BLINDNESS; CARRIER PROTEINS; CIS-TRANS-ISOMERASES; DISEASE MODELS, ANIMAL; ESTERS; EYE PROTEINS; MICE; MICE, KNOCKOUT; MICROSCOPY, CONFOCAL; RETINA; RETINOIDS;

ANIMALIA;

EID: 33645552900     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi052382x     Document Type: Article

References (49)

1. Filipek, S., Stenkamp, R. E., Teller, D. C., and Palczewski, K. (2003) G protein-coupled receptor rhodopsin: A prospectus, Annu. Rev. Physiol. 65, 851-879.
2. Ridge, K. D., Abdulaev, N. G., Sousa, M., and Palczewski, K. (2003) Phototransduction: crystal clear, Trends Biochem. Sci. 28, 479-487.
3. Okada, T., Ernst, O. P., Palczewski, K., and Hofmann, K. P. (2001) Activation of rhodopsin: new insights from structural and biochemical studies, Trends Biochem. Sci. 26, 318-324.
4. Palczewski, K. (2006) G Protein-coupled receptor rhodopsin, Annu. Rev. Biochem. (in press).
5. Rando, R. R. (1991) Membrane phospholipids as an energy source in the operation of the visual cycle, Biochemistry 30, 595-602.
6. McBee, J. K., Palczewski, K., Baehr, W., and Pepperberg, D. R. (2001) Confronting complexity: the interlink of phototransduction and- retinoid metabolism in the vertebrate retina, Prog. Retinal Eye Res. 20, 469-529.
7. Thompson, D. A., and Gal, A. (2003) Vitamin A metabolism in the retinal pigment epithelium: genes, mutations, and diseases, Prog. Retinal Eye Res. 22, 683-703.
8. Gottesman, M. E., Quadro, L., and Blaner, W. S. (2001) Studies of vitamin A metabolism in mouse model systems, BioEssays 23, 409-419.
9. Simon, A., Lagercrantz, J., Bajalica-Lagererantz, S., and Eriksson, U. (1996) Primary structure of human 11-cis retinol dehydrogenase and organization and chromosomal localization of the corresponding gene, Genomics 36, 424-430.
10. 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.
11. Kim, T. S., Maeda, A., Maeda, T., Heinlein, C., Kedishvili, N., Palczewski, K., and Nelson, P. S. (2005) Delayed dark adaptation in 11-cis-retinol dehydrogenase deficient mice: A role of RDH11 in visual processes in vivo, J. Biol. Chem. 280, 8694-8704.
12. Yamamoto, H., Simon, A., Eriksson, U., Harris, E., Berson, E. L., and Dryja, T. P. (1999) Mutations in the gene encoding 11-cis retinol dehydrogenase cause delayed dark adaptation and fundus albipunctatus, Nat. Genet. 22, 188-191.
13. Nakamura, M., Hotta, Y., Tanikawa, A., Terasaki, H., and Miyake, Y. (2000) A high association with cone dystrophy in fundus albipunctatus caused by mutations of the RDH5 gene, Invest. Ophthalmol. Visual Sci. 41, 3925-3932.
14. Marmor, M. F., Haeseleer, F., and Palczewski, K. (2003) Albipunctate retinopathy with cone dysfunction and no abnormality in the RDH5 or RLBP1 genes, Retina 23, 543-546.
15. Driessen, C. A., Winkens, H. J., Hoffmann, K., Kuhlmann, L. D., Janssen, B. P., Van Vugt, A. H., Van Hooser, J. P., Wieringa, B. E., Deutman, A. F., Palczewski, K., Ruether, K., and Janssen, J. J. (2000) Disruption of the 11-cis-retinol dehydrogenase gene leads to accumulation of cis-retinols and cis-retinyl esters, Mol. Cell. Biol. 20, 4275-4287.
16. Jang, G. F., McBee, J. K., Alekseev, A. M., Haeseleer, F., and Palczewski, K. (2000) Stereoisomeric specificity of the retinoid cycle in the vertebrate retina, J. Biol. Chem. 275, 28128-28138.
17. Jang, G. F., Van Hooser, J. P., Kuksa, V., McBee, J. K., He, Y. G., Janssen, J. J., Driessen, C. A., and Palczewski, K. (2001) Characterization of a dehydrogenase activity responsible for oxidation of 11-cis-retinol in the retinal pigment epithelium of mice with a disrupted RDH5 gene. A model for the human hereditary disease fundus albipunctatus, J. Biol. Chem. 276, 32456-32465.
18. Shang, E., Lai, K., Packer, A. I., Paik, J., Blaner, W. S., de Morais Vieira, M., Gouras, P., and Wolgemuth, D. J. (2002) Targeted disruption of the mouse cis-retinol dehydrogenase gene: visual and nonvisual functions, J. Lipid Res. 43, 590-597.
19. Imanishi, Y., Batten, M. L., Piston, D. W., Baehr, W., and Palczewski, K. (2004) Noninvasive two-photon imaging reveals retinyl ester storage structures in the eye, J. Cell Biol. 164, 373-383.
20. Imanishi, Y., Gerke, V., and Palczewski, K. (2004) Retinosomes: new insights into intracellular managing of hydrophobic substances in lipid bodies, J. Cell Biol. 166, 447-453.
21. Saari, J. C., Garwin, G. G., Van Hooser, J. P., and Palczewski, K. (1998) Reduction of all-trans-retinal limits regeneration of visual pigment in mice, Vision Res. 38, 1325-1333.
22. Redmond, T. M., Yu, S., Lee, E., Bok, D., Hamasaki, D., Chen, N., Goletz, P., Ma, J. X., Crouch, R. K., and Pfeifer, K. (1998) Rpe65 is necessary for production of 11-cis-vitamin A in the retinal visual cycle, Nat. Genet. 20, 344-351.
23. Redmond, T. M., Poliakov, E., Yu, S., Tsai, J. Y., Lu, Z., and Gentleman, S. (2005) Mutation of key residues of RPE65 abolishes its enzymatic role as isomerohydrolase in the visual cycle, Proc. Natl. Acad. Sci. U.S.A. 102, 13658-13663.
24. Moiseyev, G., Chen, Y., Takahashi, Y., Wu, B. X., and Ma, J. X. (2005) RPE65 is the isomerohydrolase in the retinoid visual cycle, Proc. Natl. Acad. Sci. U.S.A. 102, 12413-12418.
25. Takahashi, Y., Moiseyev, G., Chen, Y., and Ma, J. X. (2005) Identification of conserved histidines and glutamic ,acid as key residues for isomerohydrolase activity of RPE65, an enzyme of the visual cycle in the retinal pigment epithelium, FEBS Lett. 579, 5414-5418.
26. Jin, M., Li, S., Moghrabi, W. N., Sun, H., and Travis, G. H. (2005) Rpe65 is the retinoid isomerase in bovine retinal pigment epithelium, Cell 122, 449-459.
27. Mata, N. L., Moghrabi, W. N., Lee, J. S., Bui, T. V., Radu, R. A., Horwitz, J., and Travis, G. H. (2004) Rpe65 is a retinyl ester binding protein that presents insoluble substrate to the isomerase in retinal pigment epithelial cells, J. Biol. Chem. 279, 635-643.
28. Lem, J., Krasnoperova, N. V., Calvert, P. D., Kosaras, B., Cameron, D. A., Nicolo, M., Makino, C. L., and Sidman,. R. L. (1999) Morphological, physiological, and biochemical changes in rhodopsin knockout mice, Proc. Natl. Acad. Sci. U.S.A. 96, 736-741.
29. Batten, M. L., Imanishi, Y., Maeda, T., Tu, D. C., Moise, A. R., Bronson, D., Possin, D., Van Gelder, R. N., Baehr, W., and Palczewski, K. (2004) Lecithin-retinol acyltransferase is essential for accumulation of all-trans-retinyl esters in the eye and in the liver, J. Biol. Chem. 279, 10422-10432.
30. Maeda, A., Maeda, T., Imanishi, Y., Kuksa, V., Alekseev, A., Bronson, J. D., Zhang, H., Zhu, L., Sun, W., Saperstein, D. A., Rieke, F., Baehr, W., and Palczewski, K. (2005) Role of photoreceptor-specific retinol dehydrogenase in the retinoid cycle in vivo, J. Biol. Chem. 280, 18822-18832.
31. Van Hooser, J. P., Aleman, T. S., He, Y. G., Cideciyan, A. V., Kuksa, V., Pittler, S. J., Stone, E. M., Jacobson, S. G., and Palczewski, K. (2000) Rapid restoration of visual pigment and function with oral retinoid in a mouse model of childhood blindness, Proc. Natl. Acad. Sci. U.S.A. 97, 8623-8628.
32. Moise, A. R., Kuksa, V., Blaner, W. S., Baehr, W., and Palczewski, K. (2005) Metabolism and transactivation activity of 13,14-dihydroretinoic acid, J. Biol. Chem. 280, 27815-27825.
33. Yang, T., Snider, B. B., and Oprian, D. D. (1997) Synthesis and characterization of a novel retinylamine analog inhibitor of constitutively active rhodopsin mutants found in patients with autosomal dominant retinitis pigmentosa, Proc. Natl. Acad. Sci. U.S.A. 94, 13559-13564.
34. Van Hooser, J. P., Liang, Y., Maeda, T., Kuksa, V., Jang, G. F., He, Y. G., Rieke, F., Fong, H. K., Detwiler, P. B., and Palczewski, K. (2002) Recovery of visual functions in a mouse model of Leber congenital amaurosis, J. Biol. Chem. 277, 19173-19182.
35. Stecher, H., Gelb, M. H., Saari, J. C., and Palczewski, K. (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.
36. McBee, J. K., Kuksa, V., Alvarez, R., de Lera, A. R., Prezhdo, O., Haeseleer, F., Sokal, I., and Palczewski, K. (2000) Isomerization of all-trans-retinol to cis-retinols in bovine retinal pigment epithelial cells: dependence on the specificity of retinoid-binding proteins, Biochemistry 39, 11370-11380.
37. Jeon, C. J., Strettoi, E., and Masland, R. H. (1998) The major cell populations of the mouse retina, J. Neurosci. 18, 8936-8946.
38. Golczak, M., Kuksa, V., Maeda, T., Moise, A. R., and Palczewski, K. (2005) Positively charged retinoids are potent and selective inhibitors of the trans-cis isomerization in the retinoid (visual) cycle, Proc. Natl. Acad. Sci. U.S.A. 102, 8162-8167.
39. Cideciyan, A. V., Haeseleer, F., Fariss, R. N., Aleman, T. S., Jang, G. F., Verlinde, C. L., Marmor, M. F., Jacobson, S. G., and Palczewski, K. (2000) Rod and cone visual cycle consequences of a null mutation in the 11-cis-retinol dehydrogenase gene in man, Vision Neurosci. 17, 667-678.
40. Kuksa, V., Imanishi, Y., Batten, M., Palczewski, K., and Moise, A. R. (2003) Retinoid cycle in the vertebrate retina: experimental approaches and mechanisms of isomerization, Vision Res. 43, 2959-2981.
41. Golczak, M., Imanishi, Y., Kuksa, V., Maeda, T., Kubota, R., and Palczewski, K. (2005) Lecithin:retinol acyltransferase is responsible for amidation of retinylamine, a potent inhibitor of the retinoid cycle, J. Biol. Chem. 280, 42263-42273.
42. Liang, Y., Fotiadis, D., Maeda, T., Maeda, A., Modzelewska, A., Filipek, S., Saperstein, D. A., Engel, A., and Palczewski, K. (2004) Rhodopsin signaling and organization in heterozygote rhodopsin knockout mice, J. Biol. Chem. 279, 48189-48196.
43. Qtaishat, N. M., Redmond, T. M., and Pepperberg, D. R. (2003) Acute radiolabeling of retinoids in eye tissues of normal and rpe65-deficient mice, Invest. Ophthalmol. Visual Sci. 44, 1435-1446.
44. Jahng, W. J., David, C., Nesnas, N., Nakanishi, K., and Rando, R. R. (2003) A cleavable affinity biotinylating agent reveals a retinoid binding role for RPE65, Biochemistry 42, 6159-6168.
45. Gollapalli, D. R., Maiti, P., and Rando, R. R. (2004) RPE65 operates in the vertebrate visual cycle by stereospecifically binding all-trans-retinyl esters, Biochemistry 43, 7226.
46. Maeda, T., Van Hooser, J. P., Driessen, C. A., Filipek, S., Janssen, J. J., and Palczewski, K. (2003) Evaluation of the role of the retinal G protein-coupled receptor (RGR) in the vertebrate retina in vivo, J. Neurochem. 85, 944-956.
47. Saari, J. C., Nawrot, M., Kennedy, B. N., Garwin, G. G., Hurley, J. B., Huang, J., Possin, D. E., and Crabb, J. W. (2001) Visual cycle impairment in cellular retinaldehyde binding protein (CRALBP) knockout mice results in delayed dark adaptation, Neuron 29, 739-748.
48. Saari, J. C., Nawrot, M., Garwin, G. G., Kennedy, M. J., Hurley, J. B., Ghyselinck, N. B., and Chambon, P. (2002) Analysis of the visual cycle in cellular retinol-binding protein type I (CRBPI) knockout mice, Invest. Ophthalmol. Visual Sci. 43, 1730-1735.
49. Humphries, M. M., Rancourt, D., Farrar, G. J., Kenna, P., Hazel, M., Bush, R. A., Sieving, P. A., Sheils, D. M., McNally, N., Creighton, P., Erven, A., Boros, A., Gulya, K., Capecchi, M. R., and Humphries, P. (1997) Retinopathy induced in mice by targeted disruption of the rhodopsin gene, Nat. Genet. 15, 216-219.