Increased cone sensitivity to ABCA4 deficiency provides insight into macular vision loss in Stargardt's dystrophy

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1822, Issue 7, 2012, Pages 1169-1179

  Conley, Shannon M ^a   Cai, Xue ^a   Makkia, Rasha ^a   Wu, Yalin ^b   Sparrow, Janet R ^b   Naash, Muna I ^a  

^a UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^b Howard Hughes Medical Institute   (United States)

Author keywords

A2E; ABCA4; Cone; Retinal degeneration; Stargardt's

Indexed keywords

ABC TRANSPORTER; ABCA4 PROTEIN; LIPOFUSCIN; RETINOID; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ELECTRON MICROSCOPY; ELECTRORETINOGRAPHY; EYE EXAMINATION; MACULAR VISION LOSS; MICROSCOPY; MORPHOMETRICS; MOUSE; NONHUMAN; OPHTHALMOSCOPY; PIGMENT EPITHELIUM; PRIORITY JOURNAL; PROTEIN DEFICIENCY; RETINA CONE; RETINA DEGENERATION; STARGARDT DISEASE; VISUAL DISORDER;

ANALYSIS OF VARIANCE; ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; BLINDNESS; DARK ADAPTATION; EYE PROTEINS; HUMANS; LIPOFUSCIN; MACULAR DEGENERATION; MICE; MICE, KNOCKOUT; MICROSCOPY, ELECTRON; PYRIDINIUM COMPOUNDS; RETINA; RETINAL CONE PHOTORECEPTOR CELLS; RETINAL PIGMENT EPITHELIUM; RETINAL ROD PHOTORECEPTOR CELLS; RETINALDEHYDE; RETINOIDS; VISION, OCULAR;

MUS;

EID: 84860888442     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2011.10.007     Document Type: Article

References (39)

1. Sun H., Nathans J. Stargardt's ABCR is localized to the disc membrane of retinal rod outer segments. Nat. Genet. 1997, 17:15-16.
2. Weng J., Mata N.L., Azarian S.M., Tzekov R.T., Birch D.G., Travis G.H. Insights into the function of Rim protein in photoreceptors and etiology of Stargardt's disease from the phenotype in abcr knockout mice. Cell 1999, 98:13-23.
3. Illing M., Molday L.L., Molday R.S. The 220-kDa rim protein of retinal rod outer segments is a member of the ABC transporter superfamily. J. Biol. Chem. 1997, 272:10303-10310.
4. Molday R.S. ATP-binding cassette transporter ABCA4: molecular properties and role in vision and macular degeneration. J. Bioenerg. Biomembr. 2007, 39:507-517.
5. Molday L.L., Rabin A.R., Molday R.S. ABCR expression in foveal cone photoreceptors and its role in Stargardt macular dystrophy. Nat. Genet. 2000, 25:257-258.
6. Sullivan J.M. Focus on molecules: ABCA4 (ABCR)-an import-directed photoreceptor retinoid flipase. Exp. Eye Res. 2009, 89:602-603.
7. Sun H., Nathans J. Mechanistic studies of ABCR, the ABC transporter in photoreceptor outer segments responsible for autosomal recessive Stargardt disease. J. Bioenerg. Biomembr. 2001, 33:523-530.
8. Hoffman C.J., Miller R.H., Hultin M.B. Correlation of factor VII activity and antigen with cholesterol and triglycerides in healthy young adults. Arterioscler. Thromb. 1992, 12:267-270.
9. Wu Y., Yanase E., Feng X., Siegel M.M., Sparrow J.R. Structural characterization of bisretinoid A2E photocleavage products and implications for age-related macular degeneration. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:7275-7280.
10. Parish C.A., Hashimoto M., Nakanishi K., Dillon J., Sparrow J. Isolation and one-step preparation of A2E and iso-A2E, fluorophores from human retinal pigment epithelium. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:14609-14613.
11. Sparrow J.R., Parish C.A., Hashimoto M., Nakanishi K. A2E, a lipofuscin fluorophore, in human retinal pigmented epithelial cells in culture. Investig. Ophthalmol. Vis. Sci. 1999, 40:2988-2995.
12. De S., Sakmar T.P. Interaction of A2E with model membranes. Implications to the pathogenesis of age-related macular degeneration. J. Gen. Physiol. 2002, 120:147-157.
13. Ben-Shabat S., Itagaki Y., Jockusch S., Sparrow J.R., Turro N.J., Nakanishi K. Formation of a nonaoxirane from A2E, a lipofuscin fluorophore related to macular degeneration, and evidence of singlet oxygen involvement. Angew. Chem. Int. Ed. Engl. 2002, 41:814-817.
14. Rozanowska M., Jarvis-Evans J., Korytowski W., Boulton M.E., Burke J.M., Sarna T. Blue light-induced reactivity of retinal age pigment. In vitro generation of oxygen-reactive species. J. Biol. Chem. 1995, 270:18825-18830.
15. Zhou J., Kim S.R., Westlund B.S., Sparrow J.R. Complement activation by bisretinoid constituents of RPE lipofuscin. Investig. Ophthalmol. Vis. Sci. 2009, 50:1392-1399.
16. Pawar A.S., Qtaishat N.M., Little D.M., Pepperberg D.R. Recovery of rod photoresponses in ABCR-deficient mice. Investig. Ophthalmol. Vis. Sci. 2008, 49:2743-2755.
17. Daniele L.L., Lillo C., Lyubarsky A.L., Nikonov S.S., Philp N., Mears A.J., Swaroop A., Williams D.S., Pugh E.N. Cone-like morphological, molecular, and electrophysiological features of the photoreceptors of the Nrl knockout mouse. Invest. Ophthalmol. Vis. Sci. 2005, 46:2156-2167.
18. Mears A.J., Kondo M., Swain P.K., Takada Y., Bush R.A., Saunders T.L., Sieving P.A., Swaroop A. Nrl is required for rod photoreceptor development. Nat. Genet. 2001, 29:447-452.
19. Tan E., Wang Q., Quiambao A.B., Xu X., Qtaishat N.M., Peachey N.S., Lem J., Fliesler S.J., Pepperberg D.R., Naash M.I., Al-Ubaidi M.R. The relationship between opsin overexpression and photoreceptor degeneration. Investig. Ophthalmol. Vis. Sci. 2001, 42:589-600.
20. Ding X.Q., Nour M., Ritter L.M., Goldberg A.F., Fliesler S.J., Naash M.I. The R172W mutation in peripherin/rds causes a cone-rod dystrophy in transgenic mice. Hum. Mol. Genet. 2004, 13:2075-2087.
21. Chakraborty D., Conley S.M., Stuck M.W., Naash M.I. Differences in RDS trafficking, assembly and function in cones versus rods: insights from studies of C150S-RDS. Hum. Mol. Genet. 2010, 19:4799-4812.
22. Kim S.R., Jang Y.P., Sparrow J.R. Photooxidation of RPE lipofuscin bisretinoids enhances fluorescence intensity. Vision Res. 2010, 50:729-736.
23. Wu L., Nagasaki T., Sparrow J.R. Photoreceptor cell degeneration in abcr (-/-) mice. Adv. Exp. Med. Biol. 2010, 664:533-539.
24. Farjo R., Fliesler S.J., Naash M.I. Effect of Rds abundance on cone outer segment morphogenesis, photoreceptor gene expression, and outer limiting membrane integrity. J. Comp. Neurol. 2007, 504:619-630.
25. Farjo R., Skaggs J.S., Nagel B.A., Quiambao A.B., Nash Z.A., Fliesler S.J., Naash M.I. Retention of function without normal disc morphogenesis occurs in cone but not rod photoreceptors. J. Cell Biol. 2006, 173:59-68.
26. Feathers K.L., Lyubarsky A.L., Khan N.W., Teofilo K., Swaroop A., Williams D.S., Pugh E.N., Thompson D.A. Nrl-knockout mice deficient in Rpe65 fail to synthesize 11-cis retinal and cone outer segments. Investig. Ophthalmol. Vis. Sci. 2008, 49:1126-1135.
27. Mata N.L., Weng J., Travis G.H. Biosynthesis of a major lipofuscin fluorophore in mice and humans with ABCR-mediated retinal and macular degeneration. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:7154-7159.
28. Radu R.A., Mata N.L., Bagla A., Travis G.H. Light exposure stimulates formation of A2E oxiranes in a mouse model of Stargardt's macular degeneration. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:5928-5933.
29. Umino Y., Solessio E., Barlow R.B. Speed, spatial, and temporal tuning of rod and cone vision in mouse. J. Neurosci. 2008, 28:189-198.
30. Baylor D.A., Lamb T.D., Yau K.W. The membrane current of single rod outer segments. J. Physiol. 1979, 288:589-611.
31. Perry R.J., McNaughton P.A. Response properties of cones from the retina of the tiger salamander. J. Physiol. 1991, 433:561-587.
32. Baylor D.A., Nunn B.J., Schnapf J.L. The photocurrent, noise and spectral sensitivity of rods of the monkey Macaca fascicularis. J. Physiol. 1984, 357:575-607.
33. Schnapf J.L., Nunn B.J., Meister M., Baylor D.A. Visual transduction in cones of the monkey Macaca-fascicularis. J. Physiol. (Lond.) 1990, 427:681-713.
34. Sparrow J.R., Yoon K.D., Wu Y., Yamamoto K. Interpretations of fundus autofluorescence from studies of the bisretinoids of the retina. Investig. Ophthalmol. Vis. Sci. 2010, 51:4351-4357.
35. Birnbach C.D., Jarvelainen M., Possin D.E., Milam A.H. Histopathology and immunocytochemistry of the neurosensory retina in fundus flavimaculatus. Ophthalmology 1994, 101:1211-1219.
36. Long K.O., Fisher S.K., Fariss R.N., Anderson D.H. Disc shedding and autophagy in the cone-dominant ground squirrel retina. Exp. Eye Res. 1986, 43:193-205.
37. -/- mouse retina are amenable to retinoid replacement. Invest Ophthalmol Vis Sci 2009, 50:4858-4864.
38. Rogers B.S., Symons R.C., Komeima K., Shen J., Xiao W., Swaim M.E., Gong Y.Y., Kachi S., Campochiaro P.A. Differential sensitivity of cones to iron-mediated oxidative damage. Investig. Ophthalmol. Vis. Sci. 2007, 48:438-445.
39. Schaeferhoff K., Michalakis S., Tanimoto N., Fischer M.D., Becirovic E., Beck S.C., Huber G., Rieger N., Riess O., Wissinger B., Biel M., Seeliger M.W., Bonin M. Induction of STAT3-related genes in fast degenerating cone photoreceptors of cpfl1 mice. Cell. Mol. Life Sci. 2010, 67:3173-3186.