Human cone visual pigment deletions spare sufficient photoreceptors to warrant gene therapy

Human Gene Therapy

Volumn 24, Issue 12, 2013, Pages 993-1006

  Cideciyan, Artur V ^a   Hufnagel, Robert B ^b   Carroll, Joseph ^c   Sumaroka, Alexander ^a   Luo, Xunda ^a   Schwartz, Sharon B ^a   Dubra, Alfredo ^c   Land, Megan ^c   Michaelides, Michel ^d   Gardner, Jessica C ^d   Hardcastle, Alison J ^d   Moore, Anthony T ^d   Sisk, Robert A ^b,e   Ahmed, Zubair M ^b   Kohl, Susanne ^f   Wissinger, Bernd ^f   Jacobson, Samuel G ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^c MEDICAL COLLEGE OF WISCONSIN   (United States)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

^e CINCINNATI EYE INSTITUTE   (United States)

^f Centre for Ophthalmology   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CONE OPSIN;

ADOLESCENT; ADULT; ARTICLE; BLUE CONE MONOCHROMACY; CHILD; CLINICAL ARTICLE; FEMALE; GENE DELETION; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VIVO STUDY; MALE; OPTICS; PHOTORECEPTOR; PRESCHOOL CHILD; RETINA CONE; SCHOOL CHILD; VISUAL DISORDER; X CHROMOSOME LINKED DISORDER;

ADOLESCENT; ADULT; ANIMALS; CHILD; CHILD, PRESCHOOL; COLOR VISION DEFECTS; FEMALE; GENE DELETION; GENETIC THERAPY; HUMANS; MICE; MIDDLE AGED; MUTATION; RETINAL CONE PHOTORECEPTOR CELLS; ROD OPSINS;

EID: 84890444228     PISSN: 10430342     EISSN: 15577422     Source Type: Journal    
DOI: 10.1089/hum.2013.153     Document Type: Article

References (66)

1. Applebury, M.L., Antoch, M.P., Baxter, L.C., et al. (2000). The murine cone photoreceptor: a single cone type expresses both S and M opsins with retinal spatial patterning. Neuron 27, 513-523.
2. Ayyagari, R., Kakuk, L.E., Coats, C.L., et al. (1999). Bilateral macular atrophy in blue cone monochromacy (BCM) with loss of the locus control region (LCR) and part of the red pigment gene. Mol. Vis. 5, 13.
3. Baseler, H.A., Brewer, A.A., Sharpe, L.T., et al. (2002). Reorganization of human cortical maps caused by inherited photoreceptor abnormalities. Nat. Neurosci. 5, 364-370. (Pubitemid 34279817)
4. Blackwell H.R., and Blackwell, O.M. (1957). Blue mono-cone monochromacy: a new color vision defect. J.Opt.Soc.Am.47, 338.
5. Blackwell, H.R., and Blackwell, O.M. (1961). Rod and cone receptor mechanisms in typical and atypical congenital achromatopsia. Vis. Res. 1, 62-107.
6. Borwein, B., Borwein, D., Medeiros, J., and McGowan, J.W. (1980). The ultrastructure of monkey foveal photoreceptors, with special reference to the structure, shape, size, and spacing of the foveal cones. Am. J. Anat. 159, 125-146. (Pubitemid 11200216)
7. Carroll, J., Neitz, M., Hofer, H., et al. (2004). Functional photoreceptor loss revealed with adaptive optics: an alternate cause of color blindness. Proc. Natl. Acad. Sci. USA 101, 8461-8466. (Pubitemid 38736597)
8. Carroll, J., Rossi, E.A., Porter, J., et al. (2010). Deletion of the X-linked opsin gene array locus control region (LCR) results in disruption of the cone mosaic. Vis. Res. 50, 1989-1999.
9. Carroll, J., Dubra, A., Gardner, J.C., et al. (2012). The effect of cone opsinmutations on retinal structure and the integrity of the photoreceptor mosaic. Invest. Ophthalmol. Vis. Sci. 53, 8006-8015.
10. Cho, K.I., Haque, M., Wang, J., et al. (2013). Distinct and atypical intrinsic and extrinsic cell death pathways between photoreceptor cell types upon specific ablation of Ranbp2 in cone photoreceptors. PLoS Genet. 9, e1003555.
11. Cideciyan, A.V., Zhao, X., Nielsen, L., et al. (1998). Mutation in the rhodopsin kinase gene slows recovery kinetics of rod and cone phototransductioninman.Proc.Natl.Acad.Sci.USA95, 328-333. (Pubitemid 28103953)
12. Cideciyan, A.V., Swider, M., Aleman, T.S., et al. (2007). Reducedilluminance autofluorescence imaging in ABCA4-associated retinal degenerations. J. Opt. Soc. Am. A. Opt. Image Sci. Vis. 24, 1457-1467. (Pubitemid 46951573)
13. Cooper, R.F., Dubis, A.M., Pavaskar, A., et al. (2011). Spatial and temporal variation of rod photoreceptor reflectance in the human retina. Biomed. Opt. Express 2, 2577-2589.
14. Crognale, M.A., Fry, M., Highsmith, J., et al. (2004). Characterization of a novel form of X-linked incomplete achromatopsia. Vis. Neurosci. 21, 197-203. (Pubitemid 39481956)
15. Curcio, C.A., Sloan, K.R., Kalina, R.E., and Hendrickson, A.E. (1990). Human photoreceptor topography. J. Comp. Neurol. 292, 497-523. (Pubitemid 20076633)
16. Curcio, C.A., Allen, K.A., Sloan, K.R., et al. (1991). Distribution and morphology of human cone photoreceptors stained with anti-blue opsin. J. Comp. Neurol. 312, 610-624.
17. Dalkara, D., Byrne, L.C., Klimczak, R.R., et al. (2013). In vivodirected evolution of a new adeno-associated virus for therapeutic outer retinal gene delivery from the vitreous. Sci. Transl. Med. 5, 189ra76.
18. Daniele, L.L., Insinna, C., Chance, R., et al. (2011). A mouse Mopsin monochromat: retinal cone photoreceptors have increased M-opsin expression when S-opsin is knocked out. Vis. Res. 51, 447-458.
19. Dubra, A., Sulai, Y., Norris, J.L., et al. (2011). Noninvasive imaging of the human rod photoreceptor mosaic using a confocal adaptive optics scanning ophthalmoscope. Biomed. Opt. Express 2, 1864-1876.
20. Gawande, A.A., Donovan, W.J., Ginsburg, A.P., and Marmor, M.F. (1989). Photoaversion in retinitis pigmentosa. Br. J. Ophthalmol. 73, 115-120. (Pubitemid 19056443)
21. Gibbs, D., Cideciyan, A.V., Jacobson, S.G., and Williams, D.S. (2009). Retinal pigment epithelium defects in humans and mice with mutations in MYO7A: imaging melanosomespecific autofluorescence. Invest. Ophthalmol. Vis. Sci. 50, 4386-4393.
22. Hauswirth, W.W., Aleman, T.S., Kaushal, S., et al. (2008). Treatment of leber congenital amaurosis due to RPE65 mutations by ocular subretinal injection of adeno-associated virus gene vector: short-term results of a phase I trial. Hum. Gene Ther. 19, 979-990.
23. Hendrickson, A., and Drucker, D. (1992). The development of parafoveal and mid-peripheral human retina. Behav. Brain Res. 49, 21-31.
24. Hendrickson, A., Possin, D., Vajzovic, L., and Toth, C.A. (2012). Histologic development of the human fovea from midgestation to maturity. Am. J. Ophthalmol. 154, 767-778.
25. Hofer, H., Carroll, J., Neitz, J., et al. (2005). Organization of the human trichromatic cone mosaic. J. Neurosci. 25, 9669-9679. (Pubitemid 41510907)
26. Humphries, M.M., Rancourt, D., Farrar, G.J., et al. (1997). Retinopathy induced in mice by targeted disruption of the rhodopsin gene. Nat. Genet. 15, 216-219. (Pubitemid 27061648)
27. Humphries, M.M., Kenna, P.F., Campbell, M. et al. (2012). C1q enhances cone photoreceptor survival in a mouse model of autosomal recessive retinitis pigmentosa. Eur. J. Hum. Genet. 20, 64-68.
28. Jacobson, S.G., Cideciyan, A.V., Ratnakaram, R., et al. (2012). Gene therapy for Leber congenital amaurosis caused by RPE65 mutations: safety and efficacy in 15 children and adults followed up to 3 years. Arch. Ophthalmol. 130, 9-24.
29. Jonnal, R.S., Besecker, J.R., Derby, J.C., et al. (2010). Imaging outer segment renewal in living human cone photoreceptors. Opt. Express 18, 5257-5270.
30. Kay, C.N., Ryals, R.C., Aslanidi, G.V., et al. (2013). Targeting photoreceptors via intravitreal delivery using novel, capsidmutated AAV vectors. PLoS One 8, e62097.
31. Kellner, U., Wissinger, B., Tippmann, S., et al. (2004). Blue cone monochromatism: clinical findings in patients with mutations in the red/green opsin gene cluster. Graefes Arch. Clin. Exp. Ophthalmol. 242, 729-735. (Pubitemid 39386371)
32. Kocaoglu, O.P., Lee, S., Jonnal, R.S., et al. (2011). Imaging cone photoreceptors in three dimensions and in time using ultrahigh resolution optical coherence tomography with adaptive optics. Biomed. Opt. Express 2, 748-763.
33. Lem, J., Krasnoperova, N.V., Calvert, P.D., et al. (1999). Morphological, physiological, and biochemical changes in rhodopsin knockout mice. Proc. Natl. Acad. Sci. USA 96, 736-741. (Pubitemid 29061278)
34. Leng, T., Marmor, M.F., Kellner, U., et al. (2012). Foveal cavitation as an optical coherence tomography finding in central cone dysfunction. Retina 32, 1411-1419.
35. Leveillard, T., and Sahel, J.-A. (2010). Rod-derived cone viability factor for treating blinding diseases: from clinic to redox signaling. Sci. Transl. Med. 2, 1-5.
36. Liang, Y., Fotiadis, D., Maeda, T., et al. (2004). Rhodopsin signaling and organization in heterozygote rhodopsin knockout mice. J. Biol. Chem. 279, 48189-48196. (Pubitemid 39540974)
37. Lujan, B.J., Roorda, A., Knighton, R.W., and Carroll, J. (2011). Revealing Henle's fiber layer using spectral domain optical coherence tomography. Invest. Ophthalmol. Vis. Sci. 52, 1486-1492.
38. Maguire, A.M., Simonelli, F., Pierce, E.A., et al. (2008). Safety and efficacy of gene transfer for Leber's congenital amaurosis. N. Engl. J. Med. 358, 2240-2248. (Pubitemid 351724453)
39. Makino, C.L., Wen, X.H., Michaud, N.A., et al. (2012). Rhodopsin expression level affects rod outer segment morphology and photoresponse kinetics. PLoS One 7, e37832.
40. Milam, A.H., Li, Z.Y., and Fariss, R.N. (1998). Histopathology of the human retina in retinitis pigmentosa. Prog. Retin. Eye Res. 17, 175-205. (Pubitemid 28339912)
41. Mizrahi-Meissonnier, L., Merin, S., Banin, E., and Sharon, D. (2010). Variable retinal phenotypes caused by mutations in the X-linked photopigment gene array. Invest. Ophthalmol. Vis. Sci. 51, 3884-3892.
42. Mustafi, D., Engel, A.H., and Palczewski, K. (2009). Structure of cone photoreceptors. Prog. Retin. Eye Res. 28, 289-302.
43. Mustafi, D., Kevany, B.M., Genoud, C., et al. (2011). Defective photoreceptor phagocytosis in a mouse model of enhanced S-cone syndrome causes progressive retinal degeneration. FASEB J. 25, 3157-3176.
44. Nathans, J., Piantanida, T.P., Eddy, R.L., et al. (1986a). Molecular genetics of inherited variation in human color vision. Science 232, 203-210. (Pubitemid 16046601)
45. Nathans, J., Thomas, D., and Hogness, D.S. (1986b). Molecular genetics of human color vision: the genes encoding blue, green, and red pigments. Science 232, 193-202. (Pubitemid 16046600)
46. Nathans, J., Davenport, C.M., Maumenee, I.H., et al. (1989). Molecular genetics of human blue cone monochromacy. Science 245, 831-838. (Pubitemid 19223659)
47. Neitz, J., and Neitz, M. (2011). The genetics of normal and defective color vision. Vis. Res. 51, 633-651.
48. Osterberg, G. (1935). Topography of the layer of rods and cones in the human retina. Acta Ophthal. Suppl. 6, 1-103.
49. Palczewski, K. (2010). Retinoids for treatment of retinal diseases. Trends Pharmacol. Sci. 31, 284-295.
50. Rossi, E.A., Achtman, R.L., Guidon, A., et al. (2013). Visual function and cortical organization in carriers of blue cone monochromacy. PLoS One 8, e57956.
51. Saari, J.C. (2000). Biochemistry of visual pigment regeneration: the Friedenwald lecture. Invest. Ophthalmol. Vis. Sci. 41, 337-348. (Pubitemid 30080432)
52. Sakami, S., Maeda, T., Bereta, G., et al. (2011). Probing mechanisms of photoreceptor degeneration in a new mouse model of the common form of autosomal dominant retinitis pigmentosa due to P23H opsin mutations. J. Biol. Chem. 286, 10551-10567.
53. Smith, V.C., Pokorny, J., Delleman, J.W., et al. (1983). X-linked incomplete achromatopsia with more than one class of functional cones. Invest. Ophthalmol. Vis. Sci. 24, 451-457. (Pubitemid 13098559)
54. Spaide, R.F., and Curcio, C.A. (2011). Anatomical correlates to the bands seen in the outer retina by optical coherence tomography: literature review and model. Retina 31, 1609-1619.
55. Srinivasan, V.J., Monson, B.K., Wojtkowski, M., et al. (2008). Characterization of outer retinal morphology with high-speed, ultrahigh-resolution optical coherence tomography. Invest. Ophthalmol. Vis. Sci. 49, 1571-1579.
56. Stockman, A., Sharpe, L.T., and Fach, C. (1999). The spectral sensitivity of the human short-wavelength sensitive cones derived from thresholds and color matches. Vis. Res. 39, 2901-2927. (Pubitemid 29240651)
57. Syed, R., Sundquist, S.M., Ratnam, K., et al. (2013). Highresolution images of retinal structure in patients with choroideremia. Invest. Ophthalmol. Vis. Sci. 54, 950-961.
58. Tachibanaki, S., Tsushima, S., and Kawamura, S. (2001). Low amplification and fast visual pigment phosphorylation as mechanisms characterizing cone photoresponses. Proc. Natl. Acad. Sci. USA 98, 14044-14049. (Pubitemid 33116021)
59. Ueyama, H., Muraki-Oda, S., Yamade, S., et al. (2012). Unique haplotype in exon 3 of cone opsin mRNA affects splicing of its precursor, leading to congenital color vision defect. Biochem. Biophys. Res. Commun. 424, 152-157.
60. Von Helmholtz, H. (1866). Concerning the perceptions in general. In Treatise on Physiological Optics, III. J.P.C. Southall, ed. (Dover, New York, NY) pp. 1-18.
61. Wang, J.S., and Kefalov, V.J. (2011). The cone-specific visual cycle. Prog. Retin. Eye Res. 30, 115-128.
62. Wang, Y., Macke, J.P., Merbs, S.L., et al. (1992). A locus control region adjacent to the human red and green visual pigment genes. Neuron 9, 429-440.
63. Weleber, R.G. (2002). Infantile and childhood retinal blindness: a molecular perspective (The Franceschetti Lecture). Ophthalmic Genet. 23, 71-97. (Pubitemid 34765366)
64. Xie, B., Nakanishi, S., Guo, Q., et al. (2010). A novel middlewavelength opsin (M-opsin) null-mutation in the retinal cone dysfunction rat. Exp. Eye Res. 91, 26-33.
65. Youdelis, C., and Hendrickson, A.H. (1986). A qualitative and quantitative analysis of the human fovea during development. Vis. Res. 26, 847-855.
66. Young, T. (1802). The Bakerian Lecture: on the theory of light and colours. Phil. Trans. R. Soc. 92, 12-48.