Insights into the function of rim protein in photoreceptors and etiology of Stargardt's disease from the phenotype in abcr knockout mice

Cell

Volumn 98, Issue 1, 1999, Pages 13-23

  Weng, Jian ^a   Mata, Nathan L ^a   Azarian, Sassan M ^a   Tzekov, Radouil T ^b   Birch, David G ^b   Travis, Gabriel H ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b RETINA FOUNDATION OF THE SOUTHWEST   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; LIPOFUSCIN; OPSIN; PHOSPHATIDYLETHANOLAMINE; RETINAL; RETINOID; RHODOPSIN; RIM PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DARK ADAPTATION; ELECTRORETINOGRAPHY; GENE MUTATION; KNOCKOUT MOUSE; MOUSE; NONHUMAN; PHENOTYPE; PHOTORECEPTOR; PIGMENT EPITHELIUM; PRIORITY JOURNAL; RECESSIVE INHERITANCE; RETINA DEGENERATION; RETINA ROD; STARGARDT DISEASE;

EID: 0033538438     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(00)80602-9     Document Type: Article

References (71)

1. Alexander, K.R., andFishman, G.A. (1984). Prolonged rod darkadaptation in retinitis pigmentosa. Br. J. Ophthalmol. 68, 561-569.
2. Allikmets, R., Singh, N., Sun, H., Shroyer, N.F., Hutchinson, A., Chidambaram, A., Gerrard, B., Baird, L., Stauffer, D., Peiffer, A., et al. (1997a). A photoreceptor cell-specific ATP-binding transporter gene (ABCR) is mutated in recessive Stargardt macular dystrophy. Nat. Genet. 15, 236-246.
3. Allikmets, R., Shroyer, N.F., Singh, N., Seddon, J.M., Lewis, R.A., Bernstein, P.S., Peiffer, A., Zabriskie, N.A., Li, Y., Hutchinson, A., et al. (1997b). Mutation of the Stargardt disease gene (ABCR) in age-related macular degeneration. Science 277, 1805-1807.
4. Anderson, R.E., andMaude, M.B. (1970). Phospholipids of bovine outer segments. Biochemistry 9, 3624-3628.
5. Azarian, S.M., andTravis, G.H. (1997). The photoreceptor rim protein is an ABC transporter encoded by the gene for recessive Stargardts-disease (ABCR). FEBS Lett. 409, 247-252.
6. Azarian, S.M., Megarity, C.F., Weng, J., Horvath, D.H., andTravis, G.H. (1998). The human photoreceptor rim protein gene (ABCR) -genomic structure and primer set information for mutation analysis. Hum. Genet. 702, 699-705.
7. Bergsma, D.R., Wiggert, B.N., Funahashi, M., Kuwabara, T., andChader, C.J. (1977). Vitamin A receptors in normal and dystrophic human retina. Nature 265, 66-67.
8. Birch, D.G., andHood, D.C. (1995). Abnormal rod photoreceptor function in retinitis pigmentosa. In Degenerative Diseases of the Retina, R. Anderson, J. Hollyfield, and M. LaVail, eds. (New York: Plenum), pp. 359-369.
9. Birnbach, C.D., Jarvelainen, M., Possin, D.E., andMilam, A.H. (1994). Histopathology and immunocytochemistry of the neurosensory retina in fundus flavimaculatus. Ophthalmology 101, 1211-1219.
10. Bligh, D.G., andDyer, W.J. (1959). A rapid method for total lipid extraction and purification. Can. J. Biochem. Physiol. 37, 911-917.
11. Carter-Dawson, L.D., and LaVail, M.M. (1979). Rods and cones in the mouse retina. I. Structural analysis using light and electron microscopy. J. Comp. Neurol. 188, 245-262.
12. Chen, H., andAnderson, R.E. (1992). Quantitation of phenacyl esters of retinal fatty acids by high-performance liquid chromatography. J. Chromatogr. 578, 124-129.
13. Cremers, F.P., van de Pol, D.J., van Driel, M., den Hollander, A.I., van Haren, F.J., Knoers, N.V., Tijmes, N., Bergen, A.A., Rohrschneider, K., Blankenagel, A., et al. (1998). Autosomal recessive retinitis pigmentosa and cone-rod dystrophy caused by splice site mutations in the Stargardt's disease gene ABCR. Hum. Mol. Genet. 7, 355-362.
14. Daemen, F.J., andBonting, S.L. (1969). Internal protonation in retinylidene phosphatidylethanolamine and the red-shift in rhodopsin. Nature 222, 879-881.
15. De Laey, J.J., andVerougstraete, C. (1995). Hyperlipofuscinosis and subretinal fibrosis in Stargardt's disease. Retina 15, 399-406.
16. Decottignies, A., Grant, A.M., Nichols, J.W., de Wet, H., McIntosh, D.B., andGoffeau, A. (1998). ATPase and multidrug transport activities of the overexpressed yeast ABC protein Yor1p. J. Biol. Chem. 273, 12612-12622.
17. Dogra, S., Krishnamurthy, S., Gupta, V., Dixit, B.L., Gupta, C.M., Sanglard, D., andPrasad, R. (1999). Asymmetric distribution of phosphatidylethanolamine in C-albicans: possible mediation by CDR1, a multidrug transporter belonging to ATP binding cassette (ABC) superfamily. Yeast 15, 111-121.
18. Eagle, R.C., Jr., Lucier, A.C., Bernardino, V.B., Jr., andYanoff, M. (1980). Retinal pigment epithelial abnormalities in fundusflavimaculatus: a light and electron microscopic study. Ophthalmology 87, 1189-1200.
19. Eldred, G.E. (1995). Lipofuscin fluorophore inhibits lysosomal protein degradation and may cause early stages of macular degeneration. Gerontology 41, 15-28.
20. Eldred, G.E., andKatz, M.L. (1988). Fluorophores of the human retinal pigment epithelium: separation and spectral characterization. Exp. Eye Res. 47, 71-86.
21. Eldred, G.E., andLasky, M.R. (1993). Retinal age pigments generated by self-assembling lysosomotropic detergents. Nature 361, 724-726.
22. Fain, G.L., Matthews, H.R., andCornwall, M.C. (1996). Dark adaptation in vertebrate photoreceptors. Trends Neurosci. 19, 502-507.
23. Feeney-Burns, L., andEldred, G.E. (1983). The fate of the phagosome: conversion to "age pigment" and impact in human retinal pigment epithelium. Trans. Ophthalmol. Soc. U. K. 103, 416-421.
24. Fishman, G.A., Farbman, J.S., andAlexander, K.R. (1991). Delayed rod dark adaptation in patients with Stargardt's disease. Ophthalmology 98, 957-962.
25. Fishman, G.A., Pulluru, P., Alexander, K.R., Derlacki, D.J., andGilbert, L.D. (1994). Prolonged rod dark adaptation in patients with cone-rod dystrophy. Am. J. Ophthalmol. 118, 362-367.
26. Fliesler, S.J., andAnderson, R.E. (1983). Chemistry and metabolism of lipids in the vertebrate retina. Prog. Lipid Res. 22, 79-131.
27. Granit, R. (1947). Sensory Mechanism of the Retina (London: Oxford University Press).
28. Groenendijk, G.W., De Grip, W.J., andDaemen, F.J. (1984). Rod outer segment membranes: good acceptors for retinoids? Vision Res. 24, 1623-1627.
29. Holz, F.G., Schutt, F., Kopitz, J., Eldred, G.E., Kruse, F.E., Volcker, H.E., andCantz, M. (1999). Inhibition of lysosomal degradative functions in RPE cells by a retinoid component of lipofuscin. Invest. Ophthalmol. Vis. Sci. 40, 737-743.
30. Hood, D.C., andBirch, D.G. (1993). Human cone receptor activity: the leading edge of the a-wave and models of receptor activity. Vis. Neurosci. 70, 857-871.
31. Hubbard, R., Brown, P.K., andBownds, D. (1971). Methodology of vitamin A and visual pigments. Methods Enzymol. 18C, 615-653.
32. Illing, M., Molday, L.L., andMolday, R.S. (1997). The 220-kDa rim protein of retinal rod outer segments is a member of the ABC transporter superfamily. J. Biol. Chem. 272, 10303-10310.
33. Jager, S., Palczewski, K., andHofmann, K.P. (1996). Opsin all-transretinal complex activates transducin by different mechanisms than photolyzed rhodopsin. Biochemistry 35, 2901-2908.
34. Jin, J., Jones, G.J., and Cornwall, M.C. (1994). Movement of retinal along cone and rod photoreceptors. Vis. Neurosci. 11, 389-399. Erratum: Vis. Neurosci. 11(5), 1994.
35. Jonas, J.B., Schneider, U., andNaumann, G.O. (1992). Count and density of human retinal photoreceptors. Graefes Arch. Clin. Exp. Ophthalmol. 230, 505-510.
36. Kedzierski, W., Bok, D., andTravis, G.H. (1999). Transgenic analysis of rds/peripherin N-glycosylation: effect on dimerization, interaction with rom1, and rescue of the rds null-phenotype. J. Neurochem. 72, 430-438.
37. Kliffen, M., van der Schaft, T.L., Mooy, C.M., andde Jong, P.T. (1997). Morphologic changes in age-related maculopathy. Microsc. Res. Tech. 36, 106-122.
38. Kolb, H., andGouras, P. (1974). Electron microscopic observations of human retinitis pigmentosa, dominantly inherited. Invest. Ophthalmol. 13, 487-498.
39. Lee, B.L., andHeckenlively, U.R. (1999). Stargardt's disease and fundus flavimaculatus. In Retina-Vitreous-Macula, D.R. Guyer, L.A. Yannuzzi, S. Chang, U.A. Shields, and W.R. Green, eds. (Philadelphia: W.B. Saunders), pp. 978-988.
40. Leibrock, C.S., Reuter, T., andLamb, T.D. (1998). Molecular basis of dark adaptation in rod photoreceptors. Eye 12, 511-520.
41. Lewis, R.A., Shroyer, N.F., Singh, N., Allikmets, R., Hutchinson, A., Li, Y., Lupski, J.R., Leppert, M., andDean, M. (1999). Genotype/phenotype analysis of a photoreceptor-specific ATP-binding cassette transporter gene, ABCR, in Stargardt disease. Am. J. Hum. Genet. 64, 422-434.
42. Lyubarsky, A.L., andPugh, E.N., Jr. (1996). Recovery phase of the murine rod photoresponse reconstructed from electroretinographic recordings. J. Neurosci. 16, 563-571.
43. Martinez-Mir, A., Paloma, E., Allikmets, R., Ayuso, C., Delrio, T., Dean, M., Vilageliu, L., Gonzalezduarte, R., andBalcells, S. (1998). Retinitis pigmentosa caused by a homozygous mutation in the Stargardt-disease gene ABCR. Nat. Genet. 18, 11-12.
44. Melia, T.J., Jr., Cowan, C.W., Angleson, J.K., andWensel, T.G. (1997). A comparison of the efficiency of G protein activation by ligand-free and light-activated forms of rhodopsin. Biophys. J. 73, 3182-3191.
45. Miljanich, G.P., Nemes, P.P., White, D.L., andDratz, E.A. (1981). The asymmetric transmembrane distribution of phosphatidylethanolamine, phosphatidylserine, and fatty acids of the bovine retinal rod outer segment disk membrane. J. Membr. Biol. 60, 249-255.
46. Nakatani, K., Tamura, T., andYau, K.W. (1991). Light adaptation in retinal rods of the rabbit and two other nonprimate mammals. J. Gen. Physiol. 97, 413-435.
47. Papermaster, D.S., Schneider, B.G., Zorn, M.A., andKraehenbuhl, J.P. (1978). Immunocytochemical localization of a large intrinsic membrane protein to the incisures and margins of frog rod outer segment disks. J. Cell Biol. 78, 415-425.
48. Parish, C.A., Hashimoto, M., Nakanishi, K., Dillon, J., andSparrow, J. (1998). Isolation and one-step preparation of A2E and iso-A2E, fluorophores from human retinal pigment epithelium. Proc. Natl. Acad. Sci. USA 95, 14609-14613.
49. Pepperberg, D.R., Birch, D.G., andHood, D.C. (1997). Photoresponses of human rods in vivo derived from paired-flash electroretinograms. Vis. Neurosci. 14, 73-82.
50. Poincelot, R.P., Millar, P.G., Kimbel, R.L, Jr., andAbrahamson, E.W. (1969). Lipid to protein chromophore transfer in the photolysis of visual pigments. Nature 221, 256-257.
51. Reinboth, J.J., Gautschi, K., Munz, K., Eldred, G.E., andReme, C.E. (1997). Lipofuscin in the retina: quantitative assay for an unprecedented autofluorescent compound (pyridinium bis-retinoid, A2-E) of ocular age pigment. Exp. Eye Res. 65, 639-643.
52. Rozet, J.M., Gerber, S., Souied, E., Perrault, I., Chatelin, S., Ghazi, I., Leowski, C., Dufier, J.L., Munnich, A., andKaplan, J. (1998). Spectrum of aber gene mutations in autosomal recessive macular dystrophies. Eur. J. Hum. Genet. 6, 291-295.
53. Saari, J.C., Garwin, G.G., Van Hooser, J.P., andPalczewski, K. (1998). Reduction of all-trans-retinal limits regeneration of visual pigment in mice. Vision Res. 38, 1325-1333.
54. Smit, J.J., Schinkel, A.H., Oude Elferink, R.P., Groen, A.K., Wagenaar, E., van Deemter, L., Mol, C.A., Ottenhoff, R., van der Lugt, N.M., andvan Roon, M.A. (1993). Homozygous disruption of the murine mdr2 P-glycoprotein gene leads to a complete absence of phospholipid from bile and to liver disease. Cell 75, 451-462.
55. Stargardt, K. (1909). Uber familiare, progressive degeneration in der maculagegend des auges. Graefes Arch. Ophthalmol. 71, 534-550.
56. Steinberg, R.H. (1985). Interactions between the retinal pigment epithelium and the neural retina. Doc. Ophthalmol. 60, 327-346.
57. Steinmetz, R.L, Garner, A., Maguire, J.I., andBird, A.C. (1991). Histopathology of incipient fundus flavimaculatus. Ophthalmology 98, 953-956.
58. Steinmetz, R.L., Haimovici, R., Jubb, C., Fitzke, F.W., andBird, A.C. (1993). Symptomatic abnormalities of dark adaptation in patients
59. with age-related Bruch's membrane change. Br. J. Ophthalmol. 77, 549-554.
60. Stone, E.M., Webster, A.R., Vandenburgh, K., Streb, L.M., Hockey, R.R., Lotery, A.J., andSheffield, V.C. (1998). Allelic variation in abcr associated with Stargardt-disease but not age-related macular degeneration. Nat. Genet. 20, 328-329.
61. Sun, H., andNathans, J. (1997). Stargardt's ABCR is localized to the disc membrane of retinal rod outer segments. Nat. Genet. 17, 15-16.
62. Sun, H., Molday, R.S., andNathans, J. (1999). Retinal stimulates ATP hydrolysis by purified reconstituted ABCR, the photoreceptor-specific ATP-binding cassette transporter responsible for Stargardt disease. J. Biol. Chem. 274, 8269-8281.
63. Surya, A., Foster, K.W., andKnox, B.E. (1995). Transducin activation by the bovine opsin apoprotein. J. Biol. Chem. 270, 5024-5031.
64. Suzuki, T., Fujita, Y., Noda, Y., andMiyata, S. (1986). A simple procedure for the extraction of the native chromophore of visual pigments: the formaldehyde method. Vision Res. 26, 425-429.
65. Tamura, T., Nakatani, K., andYau, K.W. (1989). Light adaptation in cat retinal rods. Science 245, 755-758.
66. Travis, G. (1998). Mechanisms of cell death in the inherited retinal degenerations. Am. J. Hum. Genet. 62, 503-508.
67. Tsang, S.H., Burns, M.E., Calvert, P.D., Gouras, P., Baylor, D.A., Goff, S.P., andArshavsky, V.Y. (1998). Role for the target enzyme in deactivation of photoreceptor G protein in vivo. Science 282, 117-121.
68. Wing, G.L., Blanchard, G.C., andWeiter, J.J. (1978). The topography and age relationship of lipofuscin concentration in the retinal pigment epithelium. Invest. Ophthalmol. Vis. Sci. 17, 601-607.
69. Wood, R., andLee, T. (1983). High performance liquid chromatography of fatty acids: quantitative analysis of saturated monoenoic, polyenoic, and geometrical isomers. J. Chromatogr. 254, 237-246.
70. Wu, G., andHubbell, W.L. (1993). Phospholipid asymmetry and transmembrane diffusion in photoreceptor disc membranes. Biochemistry 32, 879-888.
71. Zhou, Z., White, K.A., Polissi, A., Georgopoulos, C., andRaetz, C.R. (1998). Function of Escherichia coli MsbA, an essential ABC family transporter, in lipid A and phospholipid biosynthesis. J. Biol. Chem. 273, 12466-12475.