Cone photoreceptors are the main targets for gene therapy of NPHP5 (IQCB1) or NPHP6 (CEP290) blindness: Generation of an all-cone Nphp6 hypomorph mouse that mimics the human retinal ciliopathy

Human Molecular Genetics

Volumn 20, Issue 7, 2011, Pages 1411-1423

  Cideciyan, Artur V ^a   Rachel, Rivka A ^b   Aleman, Tomas S ^a   Swider, Malgorzata ^a   Schwartz, Sharon B ^a   Sumaroka, Alexander ^a   Roman, Alejandro J ^a   Stone, Edwin M ^c,d   Jacobson, Samuel G ^a   Swaroop, Anand ^b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b NATIONAL EYE INSTITUTE   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^d UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENE PRODUCT; LIPOFUSCIN; NEPHROCYSTIN 5; NEPHROCYSTIN 6; UNCLASSIFIED DRUG;

ADOLESCENT; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLINDNESS; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; GENE MUTATION; GENE TARGETING; GENE THERAPY; HUMAN; LEBER CONGENITAL AMAUROSIS; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRESCHOOL CHILD; PRIORITY JOURNAL; RETINA CILIOPATHY; RETINA CONE; RETINA DISEASE; RETINA FOVEA; RETINA PIGMENT DEGENERATION; SCHOOL CHILD;

ADOLESCENT; ADULT; ALLELES; ANIMALS; ANTIGENS, NEOPLASM; CALMODULIN-BINDING PROTEINS; CHILD; CILIA; FEMALE; GENE THERAPY; HUMANS; LEBER CONGENITAL AMAUROSIS; MALE; MICE; MICE, MUTANT STRAINS; MIDDLE AGED; MUTATION; NEOPLASM PROTEINS; NUCLEAR PROTEINS; RETINAL CONE PHOTORECEPTOR CELLS; RETINAL PIGMENT EPITHELIUM; ROD CELL OUTER SEGMENT;

MUS;

EID: 79952578905     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddr022     Document Type: Article

References (61)

1. den Hollander, A.I., Roepman, R., Koenekoop, R.K. and Cremers, F.P. (2008) Leber congenital amaurosis: genes, proteins and disease mechanisms. Prog. Retin. Eye Res., 27, 391-419.
2. Wright, A.F., Chakarova, C.F., Abd El-Aziz, M.M. and Bhattacharya, S.S. (2010) Photoreceptor degeneration: genetic and mechanistic dissection of a complex trait. Nat. Rev. Genet., 11, 273-284.
3. Cideciyan, A.V. (2010) Leber congenital amaurosis due to RPE65 mutations and its treatment with gene therapy. Prog. Retin. Eye Res., 29, 398-427.
4. den Hollander, A.I., Koenekoop, R.K., Yzer, S., Lopez, I., Arends, M.L., Voesenek, K.E., Zonneveld, M.N., Strom, T.M., Meitinger, T., Brunner, H.G. et al. (2006) Mutations in the CEP290 (NPHP6) gene are a frequent cause of Leber congenital amaurosis. Am. J. Hum. Genet., 79, 556-561.
5. Perrault, I., Delphin, N., Hanein, S., Gerber, S., Dufier, J.L., Roche, O., Defoort-Dhellemmes, S., Dollfus, H., Fazzi, E., Munnich, A. et al. (2007) Spectrum of NPHP6/CEP290 mutations in Leber congenital amaurosis and delineation of the associated phenotype. Hum. Mutat., 28, 416.
6. Sayer, J.A., Otto, E.A., O'Toole, J.F., Nurnberg, G., Kennedy, M.A., Becker, C., Hennies, H.C., Helou, J., Attanasio, M., Fausett, B.V. et al. (2006) The centrosomal protein nephrocystin-6 is mutated in Joubert syndrome and activates transcription factor ATF4. Nat. Genet., 38, 674-681.
7. Chang, B., Khanna, H., Hawes, N., Jimeno, D., He, S., Lillo, C., Parapuram, S.K., Cheng, H., Scott, A., Hurd, R.E. et al. (2006) In-frame deletion in a novel centrosomal/ciliary protein CEP290/NPHP6 perturbs its interaction with RPGR and results in early-onset retinal degeneration in the rd16 mouse. Hum. Mol. Genet., 15, 1847-1857.
8. Craige, B., Tsao, C.C., Diener, D.R., Hou, Y., Lechtreck, K.F., Rosenbaum, J.L. and Witman, G.B. (2010) CEP290 tethers flagellar transition zone microtubules to the membrane and regulates flagellar protein content. J. Cell Biol., 190, 927-940.
9. Tsang, W.Y., Bossard, C., Khanna, H., Peränen, J., Swaroop, A., Malhotra, V. and Dynlacht, B.D. (2008) CP110 suppresses primary cilia formation through its interaction with CEP290, a protein deficient in human ciliary disease. Dev. Cell, 15, 187-197.
10. Kim, J., Krishnaswami, S.R. and Gleeson, J.G. (2008) CEP290 interacts with the centriolar satellite component PCM-1 and is required for Rab8 localization to the primary cilium. Hum. Mol. Genet., 17, 3796-3805.
11. Valente, E.M., Silhavy, J.L., Brancati, F., Barrano, G., Krishnaswami, S.R., Castori, M., Lancaster, M.A., Boltshauser, E., Boccone, L., Al-Gazali, L. et al. (2006) Mutations in CEP290, which encodes a centrosomal protein, cause pleiotropic forms of Joubert syndrome. Nat. Genet., 38, 623-625.
12. Brancati, F., Barrano, G., Silhavy, J.L., Marsh, S.E., Travaglini, L., Bielas, S.L., Amorini, M., Zablocka, D., Kayserili, H., Al-Gazali, L. et al. (2007) CEP290 mutations are frequently identified in the oculo-renal form of Joubert syndrome-related disorders. Am. J. Hum. Genet., 81, 104-113.
13. McEwen, D.P., Koenekoop, R.K., Khanna, H., Jenkins, P.M., Lopez, I., Swaroop, A. and Martens, J.R. (2007) Hypomorphic CEP290/NPHP6 mutations result in anosmia caused by the selective loss of G proteins in cilia of olfactory sensory neurons. Proc. Natl Acad. Sci. USA, 104, 15917-15922.
14. Otto, E.A., Loeys, B., Khanna, H., Hellemans, J., Sudbrak, R., Fan, S., Muerb, U., O'Toole, J.F., Helou, J., Attanasio, M. et al. (2005) Nephrocystin-5, a ciliary IQ domain protein, is mutated in Senior-Loken syndrome and interacts with RPGR and calmodulin. Nat. Genet., 37, 282-288.
15. Schäfer, T., Pütz, M., Lienkamp, S., Ganner, A., Bergbreiter, A., Ramachandran, H., Gieloff, V., Gerner, M., Mattonet, C., Czarnecki, P.G. et al. (2008) Genetic and physical interaction between the NPHP5 and NPHP6 gene products. Hum. Mol. Genet., 17, 3655-3662.
16. Murga-Zamalloa, C.A., Swaroop, A. and Khanna, H. (2009) RPGR-containing protein complexes in syndromic and non-syndromic retinal degeneration due to ciliary dysfunction. J. Genet., 88, 399-407.
17. Estrada-Cuzcano, A., Koenekoop, R.K., Coppieters, F., Kohl, S., Lopez, I., Collin, R.W., De Baere, E., Roeleveld, D., Marek, J., Bernd, A. et al. (2010) IQCB1 mutations in patients with Leber congenital amaurosis. Invest. Ophthalmol. Vis. Sci., Epub ahead of print.
18. Stone, E.M., Cideciyan, A.V., Aleman, T.S., Scheetz, T.E., Sumaroka, A., Ehlinger, M.A., Schwartz, S.B., Fishman, G.A., Traboulsi, E.I., Lam, B.L. et al. (2011) Variations in NPHP5 in patients with nonsyndromic Leber congenital amaurosis (LCA) and Senior-Loken syndrome. Arch. Ophthalmol., 129, 81-87.
19. Menotti-Raymond, M., David, V.A., Schäffer, A.A., Stephens, R., Wells, D., Kumar-Singh, R., O'Brien, S.J. and Narfström, K. (2007) Mutation in CEP290 discovered for cat model of human retinal degeneration. J. Hered., 98, 211-220.
20. Jacobson, S.G., Kemp, C.M., Narfstrom, K. and Nilsson, S.E. (1989) Rhodopsin levels and rod-mediated function in Abyssinian cats with hereditary retinal degeneration. Exp. Eye Res., 49, 843-852.
21. Kang Derwent, J.J., Padnick-Silver, L., McRipley, M., Giuliano, E., Linsenmeier, R.A. and Narfström, K. (2006) The electroretinogram components in Abyssinian cats with hereditary retinal degeneration. Invest. Ophthalmol. Vis. Sci., 47, 3673-3682.
22. Mears, A.J., Kondo, M., Swain, P.K., Takada, Y., Bush, R.A., Saunders, T.L., Sieving, P.A. and Swaroop, A. (2001) Nrl is required for rod photoreceptor development. Nat. Genet., 29, 447-452.
23. Curcio, C.A., Sloan, K.R., Kalina, R.E. and Hendrickson, A.E. (1990) Human photoreceptor topography. J. Comp. Neurol., 292, 497-523.
24. Aleman, T.S., Cideciyan, A.V., Sumaroka, A., Windsor, E.A., Herrera, W., White, D.A., Kaushal, S., Naidu, A., Roman, A.J., Schwartz, S.B. et al. (2008) Retinal laminar architecture in human retinitis pigmentosa caused by rhodopsin gene mutations. Invest. Ophthalmol. Vis. Sci., 49, 1580-1590.
25. Jacobson, S.G., Aleman, T.S., Sumaroka, A., Cideciyan, A.V., Roman, A.J., Windsor, E.A., Schwartz, S.B., Rehm, H.L. and Kimberling, W.J. (2009) Disease boundaries in the retina of patients with Usher syndrome caused by MYO7A gene mutations. Invest. Ophthalmol. Vis. Sci., 50, 1886-1894.
26. Beltran, W.A., Acland, G.M. and Aguirre, G.D. (2009) Age-dependent disease expression determines remodeling of the retinal mosaic in carriers of RPGR exon ORF15 mutations. Invest. Ophthalmol. Vis. Sci., 50, 3985-3995.
27. Jacobson, S.G. and Cideciyan, A.V. (2010) Treatment possibilities for retinitis pigmentosa. N. Engl. J. Med., 363, 1669-1671.
28. Feeney, L. (1978) Lipofuscin and melanin of human retinal pigment epithelium. Fluorescence, enzyme cytochemical, and ultrastructural studies. Invest. Ophthalmol. Vis. Sci., 17, 583-600.
29. Sparrow, J.R., Yoon, K.D., Wu, Y. and Yamamoto, K. (2010) Interpretations of fundus autofluorescence from studies of the bisretinoids of retina. Invest. Ophthalmol. Vis. Sci., 51, 4351-4357.
30. Insinna, C. and Besharse, J.C. (2008) Intraflagellar transport and the sensory outer segment of vertebrate photoreceptors. Dev. Dyn., 237, 1982-1992.
31. Cideciyan, A.V., Aleman, T.S., Jacobson, S.G., Khanna, H., Sumaroka, A., Aguirre, G.K., Schwartz, S.B., Windsor, E.A., He, S., Chang, B. et al. (2007) Centrosomal-ciliary gene CEP290/NPHP6 mutations result in blindness with unexpected sparing of photoreceptors and visual brain: implications for therapy of Leber congenital amaurosis. Hum. Mutat., 28, 1074-1083.
32. Bok, D. (1993) The retinal pigment epithelium: a versatile partner in vision. J. Cell Sci. Suppl., 17, 189-195.
33. 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 melanosome-specific autofluorescence. Invest. Ophthalmol. Vis. Sci., 50, 4386-4393.
34. Friedman, E. and Ts'o, M.O. (1968) The retinal pigment epithelium. II. Histologic changes associated with age. Arch. Ophthalmol., 79, 315-320.
35. Daniele, L.L., Lillo, C., Lyubarsky, A.L., Nikonov, S.S., Philp, N., Mears, A.J., Swaroop, A., Williams, D.S. and Pugh, E.N. Jr. (2005) Cone-like morphological, molecular, and electrophysiological features of the photoreceptors of the Nrl knockout mouse. Invest. Ophthalmol. Vis. Sci., 46, 2156-2167.
36. Farjo, R., Skaggs, J., Nagel, B., Quiambao, A., Nash, Z., Fliesler, S. and Naash, M. (2006) Retention of function without normal disc morphogenesis occurs in cone but not rod photoreceptors. J. Cell Biol., 173, 59-68.
37. Olsson, J.E., Gordon, J.W., Pawlyk, B.S., Roof, D., Hayes, A., Molday, R.S., Mukai, S., Cowley, G.S., Berson, E.L. and Dryja, T.P. (1992) Transgenic mice with a rhodopsin mutation (Pro23His): a mouse model of autosomal dominant retinitis pigmentosa. Neuron, 9, 815-830.
38. 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.
39. Lee, E.S. and Flannery, J.G. (2007) Transport of truncated rhodopsin and its effects on rod function and degeneration. Invest. Ophthalmol. Vis. Sci., 48, 2868-2876.
40. Louie, C.M., Caridi, G., Lopes, V.S., Brancati, F., Kispert, A., Lancaster, M.A., Schlossman, A.M., Otto, E.A., Leitges, M., Gröne, H.J. et al. (2010) AHI1 is required for photoreceptor outer segment development and is a modifier for retinal degeneration in nephronophthisis. Nat. Genet., 42, 175-180.
41. Lancaster, M.A. and Gleeson, J.G. (2009) The primary cilium as a cellular signaling center: lessons fromdisease.Curr.Opin.Genet. Dev., 19, 220-229.
42. Jones, B.W., Watt, C.B., Frederick, J.M., Baehr, W., Chen, C.K., Levine, E.M., Milam, A.H., Lavail, M.M. and Marc, R.E. (2003) Retinal remodeling triggered by photoreceptor degenerations. J. Comp. Neurol., 464, 1-16.
43. Marc, R.E. and Jones, B.W. (2003) Retinal remodeling in inherited photoreceptor degenerations. Mol. Neurobiol., 28, 139-147.
44. Rattner, A. and Nathans, J. (2005) The genomic response to retinal disease and injury: evidence for endothelin signaling from photoreceptors to glia. J. Neurosci., 25, 4540-4549.
45. Beltran, W.A., Wen, R., Acland, G.M. and Aguirre, G.D. (2007) Intravitreal injection of ciliary neurotrophic factor (CNTF) causes peripheral remodeling and does not prevent photoreceptor loss in canine RPGR mutant retina. Exp. Eye Res., 84, 753-771.
46. Avasthi, P., Watt, C.B., Williams, D.S., Le, Y.Z., Li, S., Chen, C.K., Marc, R.E., Frederick, J.M. and Baehr, W. (2009) Trafficking of membrane proteins to cone but not rod outer segments is dependent on heterotrimeric kinesin-II. J. Neurosci., 29, 14287-14298.
47. Fliegauf, M., Benzing, T. and Omran, H. (2007) When cilia go bad: cilia defects and ciliopathies. Nat. Rev. Mol. Cell Biol., 8, 880-893.
48. Roepman, R. and Wolfrum, U. (2007) Protein networks and complexes in photoreceptor cilia. Subcell. Biochem., 43, 209-235.
49. Khanna, H., Davis, E.E., Murga-Zamalloa, C.A., Estrada-Cuzcano, A., Lopez, I., den Hollander, A.I., Zonneveld, M.N., Othman, M.I., Waseem, N., Chakarova, C.F. et al. (2009) A common allele in RPGRIP1L is a modifier of retinal degeneration in ciliopathies. Nat. Genet., 41, 739-745.
50. Jeon, C.J., Strettoi, E. and Masland, R.H. (1998) The major cell populations of the mouse retina. J. Neurosci., 18, 8936-8946.
51. Delyfer, M.N., Léveillard, T., Mohand-Saïd, S., Hicks, D., Picaud, S. and Sahel, J.A. (2004) Inherited retinal degenerations: therapeutic prospects. Biol. Cell., 96, 261-269.
52. Chrysostomou, V., Valter, K. and Stone, J. (2009) Cone-rod dependence in the rat retina: variation with the rate of rod damage. Invest. Ophthalmol. Vis. Sci., 50, 3017-3023.
53. Zhu, X., Brown, B., Li, A., Mears, A.J., Swaroop, A. and Craft, C.M. (2003) GRK1-dependent phosphorylation of S and M opsins and their binding to cone arrestin during cone phototransduction in the mouse retina. J. Neurosci., 23, 6152-6160.
54. Farjo, R., Fliesler, S.J. and Naash, M.I. (2007) Effect of Rds abundance on cone outer segment morphogenesis, photoreceptor gene expression, and outer limiting membrane integrity. J. Comp. Neurol., 504, 619-630.
55. Feathers, K.L., Lyubarsky, A.L., Khan, N.W., Teofilo, K., Swaroop, A., Williams, D.S., Pugh, E.N. Jr and Thompson, D.A. (2008) Nrl-knockout mice deficient in Rpe65 fail to synthesize 11-cis retinal and cone outer segments. Invest. Ophthalmol. Vis. Sci., 49, 1126-1135.
56. Bramall, A.N., Wright, A.F., Jacobson, S.G. and McInnes, R.R. (2010) The genomic, biochemical, and cellular responses of the retina in inherited photoreceptor degenerations and prospects for the treatment of these disorders. Annu. Rev. Neurosci., 33, 441-472.
57. Huang, Y., Cideciyan, A.V., Papastergiou, G.I., Banin, E., Semple-Rowland, S.L., Milam, A.H. and Jacobson, S.G. (1998) Relation of optical coherence tomography to microanatomy in normal and rd chickens. Invest. Ophthalmol. Vis. Sci., 39, 2405-2416.
58. Cideciyan, A.V., Swider, M., Aleman, T.S., Roman, M.I., Sumaroka, A. and Schwartz, S.B. (2007) Reduced-illuminance autofluorescence imaging in ABCA4-associated retinal degenerations. J. Opt. Soc. Am. A, 24, 1457-1467.
59. 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. USA, 97, 8623-8628.
60. Aleman, T.S., LaVail, M.M., Montemayor, R., Ying, G., Maguire, M.M., Laties, A.M., Jacobson, S.G. and Cideciyan, A.V. (2001) Augmented rod bipolar cell function in partial receptor loss: an ERG study in P23H rhodopsin transgenic and aging normal rats. Vision Res., 41, 2779-2797.
61. Cheng, H., Aleman, T.S., Cideciyan, A.V., Khanna, R., Jacobson, S.G. and Swaroop, A. (2006) In vivo function of the orphan nuclear receptor NR2E3 in establishing photoreceptor identity during mammalian retinal development. Hum. Mol. Genet., 15, 2588-2602.