Pathogenic mechanisms and the prospect of gene therapy for choroideremia

Expert Opinion on Orphan Drugs

Volumn 3, Issue 7, 2015, Pages 787-798

  Dimopoulos, Ioannis S ^a   Chan, Stephanie ^a   MacLaren, Robert E ^b,c   MacDonald, Ian M ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b OXFORD EYE HOSPITAL   (United Kingdom)

^c MOORFIELDS EYE HOSPITAL   (United Kingdom)

Author keywords

Choroideremia; Gene therapy; REP1; Retina

Indexed keywords

ATALUREN; GENE THERAPY AGENT; PARVOVIRUS VECTOR; VASCULOTROPIN INHIBITOR;

ANTIANGIOGENIC GENE THERAPY; CATARACT EXTRACTION; CELL MIGRATION; CHOROIDEREMIA; CLINICAL TRIAL (TOPIC); DIFFERENTIAL DIAGNOSIS; GENE THERAPY; GENETIC ASSOCIATION; GENETIC SCREENING; HUMAN; MOLECULAR DIAGNOSIS; MOLECULAR PATHOLOGY; NONHUMAN; PRIORITY JOURNAL; RETINA GYRATE ATROPHY; RETINA MACULA CYSTOID EDEMA; RETINITIS PIGMENTOSA; REVIEW; SUBRETINAL NEOVASCULARIZATION; TREATMENT OUTCOME; VIRAL GENE DELIVERY SYSTEM; X CHROMOSOME INACTIVATION;

EID: 84932178203     PISSN: None     EISSN: 21678707     Source Type: Journal    
DOI: 10.1517/21678707.2015.1046434     Document Type: Review

References (92)

1. MacDonald IM, Hume S, Chan S, et al. Choroideremia. 2003 Feb 21 [Updated 2015 Feb 26]. In: pagon RA, Adam MP, Ardinger HH, et al. editors. GeneReviews[Internet]. University ofWashington, Seattle; Seattle (WA): 1993-2015
2. van den Hurk JA, Schwartz M, van Bokhoven H, et al. Molecular basis of choroideremia (CHM): mutations involving the Rab escort protein-1 (REP-1) gene. Hum Mutat 1997;9(2):110-17
3. Jacobson SG, Cideciyan AV, Sumaroka A, et al. Remodeling of the human retina in choroideremia: rab escort protein 1 (REP-1) mutations. Invest Ophthalmol Vis Sci 2006;47(9):4113-20
4. Morgan JI, Han G, Klinman E, et al. High-resolution adaptive optics retinal imaging of cellular structure in choroideremia. Invest Ophthalmol Vis Sci 2014;55(10):6381-97.
5. Holz FG, Bindewald-Wittich A, Fleckenstein M, et al. Progression of geographic atrophy and impact of fundus autofluorescence patterns in age-related macular degeneration. Am J Ophthalmol 2007;143(3):463-72
6. Spaide RF. Fundus autofluorescence and age-related macular degeneration. Ophthalmology 2003;110(2):392-9
7. Preising MN, Wegscheider E, Friedburg C, et al. Fundus autofluorescence in carriers of choroideremia and correlation with electrophysiologic and psychophysical data. Ophthalmology 2009;116(6):1201-9; e1-2
8. Kärnä J. Choroideremia. A clinical and genetic study of 84 Finnish patients and 126 female carriers. Acta Ophthalmol Suppl 1986;176:1-68
9. Potter MJ, Wong E, Szabo SM, et al. Clinical findings in a carrier of a new mutation in the choroideremia gene. Ophthalmology 2004;111(10):1905-9
10. Rudolph G, Preising M, Kalpadakis P, et al. Phenotypic variability in three carriers from a family with choroideremia and a frameshift mutation 1388delCCinsG in the REP-1 gene. Ophthalmic Genet 2003;24(4):203-14
11. Nussbaum RL, Lewis RA, Lesko JG, et al. Choroideremia is linked to the restriction fragment length polymorphism DXYS1 at XQ13-21. Am J Hum Genet 1985;37(3):473-81
12. Schwartz M, Rosenberg T, Niebuhr E, et al. Choroideremia: further evidence for assignment of the locus to Xq13-Xq21. Hum Genet 1986;74(4):449-52
13. Merry DE, Lesko JG, Sosnoski DM, et al. Choroideremia and deafness with stapes fixation: a contiguous gene deletion syndrome in Xq21. Am J Hum Genet 1989;45(4):530-40
14. Sankila EM, Lehner T, Eriksson AW, et al. Haplotype and multipoint linkage analysis in Finnish choroideremia families. Hum Genet 1989;84(1):66-70
15. van de Pol TJ, Cremers FP, Brohet RM, et al. Derivation of clones from the choroideremia locus by preparative field inversion gel electrophoresis. Nucleic Acids Res 1990;18(4):725-31
16. Cremers FP, van de Pol DJ, van Kerkhoff LP, et al. Cloning of a gene that is rearranged in patients with choroideraemia. Nature 1990;347(6294):674-7
17. Seabra MC, Brown MS, Slaughter CA, et al. Purification of component A of Rab geranylgeranyl transferase: possible identity with the choroideremia gene product. Cell 1992;70(6):1049-57
18. Seabra MC, Brown MS, Goldstein JL. Retinal degeneration in choroideremia: deficiency of rab geranylgeranyl transferase. Science 1993;259(5093):377-81
19. Andres DA, Seabra MC, Brown MS, et al. cDNA cloning of component A of Rab geranylgeranyl transferase and demonstration of its role as a Rab escort protein. Cell 1993;73(6):1091-9
20. McTaggart KE, Tran M, Mah DY, et al. Mutational analysis of patients with the diagnosis of choroideremia. Hum Mutat 2002;20(3):189-96
21. Sergeev YV, Smaoui N, Sui R, et al. The functional effect of pathogenic mutations in Rab escort protein 1. Mutat Res 2009;665(1-2):44-50
22. Esposito G, De Falco F, Tinto N, et al. Comprehensive mutation analysis (20 families) of the choroideremia gene reveals a missense variant that prevents the binding of REP1 with Rab geranylgeranyl transferase. Hum Mutat 2011;32(12):1460-9
23. Rosenberg T, Schwartz M, Niebuhr E, et al. Choroideremia in interstitial deletion of the X chromosome. Ophthalmic Paediatr Genet 1986;7(3):205-10
24. Rosenberg T, Niebuhr E, Yang HM, et al. Choroideremia, congenital deafness and mental retardation in a family with an X chromosomal deletion. Ophthalmic Paediatr Genet 1987;8(3):139-43
25. Poloschek CM, Kloeckener-Gruissem B, Hansen LL, et al. Syndromic choroideremia: sublocalization of phenotypes associated with Martin-Probst deafness mental retardation syndrome. Invest Ophthalmol Vis Sci 2008;49(9):4096-104
26. Rush ET, Schaefer GB. Identification of an X-linked deletion syndrome through comparative genomic hybridization microarray. Semin Pediatr Neurol 2010;17(1):51-3
27. Cremers FP, Sankila EM, Brunsmann F, et al. Deletions in patients with classical choroideremia vary in size from 45 kb to several megabases. Am J Hum Genet 1990;47(4):622-8
28. Wang Q, Zhao FF, Shi YB. Four systems involved with congenital abnormalities: a new type of syndromic hearing loss-ADOC Wang's syndrome Acta Otolaryngol 2011;131(10):1117-22
29. Mukkamala K, Gentile RC, Willner J, et al. Choroideremia in a woman with ectodermal dysplasia and complex translocations involving chromosomes X, 1, and 3. Ophthalmic Genet 2010;31(4):178-82
30. Lorda-Sanchez IJ, Ibañez AJ, Sanz RJ, et al. Choroideremia, sensorineural deafness, and primary ovarian failure in a woman with a balanced X-4 translocation. Ophthalmic Genet 2000;21(3):185-9
31. Lee TK, McTaggart KE, Sieving PA, et al. Clinical diagnoses that overlap with choroideremia. Can J Ophthalmol 2003;38(5):364-72; quiz 372
32. Fujiki K, Hotta Y, Hayakawa M, et al. REP-1 gene mutations in Japanese patients with choroideremia. Graefes Arch Clin Exp Ophthalmol 1999;237(9):735-40
33. MacDonald IM, Mah DY, Ho YK, et al. A practical diagnostic test for choroideremia. Ophthalmology 1998;105(9):1637-40
34. Pereira-Leal JB, Seabra MC. The mammalian Rab family of small GTPases: definition of family and subfamily sequence motifs suggests a mechanism for functional specificity in the Ras superfamily. J Mol Biol 2000;301(4):1077-87
35. Barnard AR, Groppe M, MacLaren RE. Gene therapy for choroideremia using an adeno-associated viral (AAV) vector. Cold Spring Harb Perspect Med 2014;5(3):a017293
36. Corbeel L, Freson K. Rab proteins and Rabassociated proteins: major actors in the mechanism of protein-trafficking disorders. Eur J Pediatr 2008;167(7):723-9
37. Seabra MC, Ho YK, Anant JS. Deficient geranylgeranylation of Ram/Rab27 in choroideremia. J Biol Chem 1995;270(41):24420-7
38. Larijani B, Hume AN, Tarafder AK, et al. Multiple factors contribute to inefficient prenylation of Rab27a in Rab prenylation diseases. J Biol Chem 2003;278(47):46798-804
39. Tolmachova T, Ramalho JS, Anant JS, et al. Cloning, mapping and characterization of the human RAB27A gene. Gene 1999;239(1):109-16
40. Kohnke M, Delon C, Hastie ML, et al. Rab GTPase prenylation hierarchy and its potential role in choroideremia disease. PLoS One 2013;8(12):e81758.
41. Rak A, Pylypenko O, Niculae A, et al. Structure of the Rab7:REP-1 complex: insights into the mechanism of Rab prenylation and choroideremia disease. Cell 2004;117(6):749-60
42. Pylypenko O, Rak A, Reents R, et al. Structure of Rab escort protein-1 in complex with Rab geranylgeranyltransferase. Mol Cell 2003;11(2):483-94
43. Strunnikova N, Zein WM, Silvin C, et al. Serum biomarkers and trafficking defects in peripheral tissues reflect the severity of retinopathy in three brothers affected by choroideremia. Adv Exp Med Biol 2012;723:381-7
44. Sakamoto K, Honda T, Yokoya S, et al. Rab-small GTPases are involved in fluvastatin and pravastatin-induced vacuolation in rat skeletal myofibers. FASEB J 2007;21(14):4087-94
45. Zhou Q, Weis E, Ye M, et al. An internet-based health survey on the comorbidities of choroideremia patients. Ophthalmic Physiol Opt 2013;33(2):157-63
46. Wuthisiri W, Lingao MD, Capasso JE, et al. Lyonization in ophthalmology. Curr Opin Ophthalmol 2013;24(5):389-97
47. Perez-Cano HJ, Garnica-Hayashi RE, Zenteno JC. CHM gene molecular analysis and X-chromosome inactivation pattern determination in two families with choroideremia. Am J Med Genet A 2009;149A(10):2134-40
48. Carrel L, Willard HF. Heterogeneous gene expression from the inactive X chromosome: an X-linked gene that escapes X inactivation in some human cell lines but is inactivated in others. Proc Natl Acad Sci USA 1999;96(13):7364-9
49. Vajaranant TS, Fishman GA, Szlyk JP, et al. Detection of mosaic retinal dysfunction in choroideremia carriers electroretinographic and psychophysical testing. Ophthalmology 2008;115(4):723-9
50. Hayasaka S, Shoji K, Kanno C, et al. Differential diagnosis of diffuse choroidal atrophies. Diffuse choriocapillaris atrophy, choroideremia, and gyrate atrophy of the choroid and retina. Retina 1985;5(1):30-7
51. Heckenlively J. The frequency of posterior subcapsular cataract in the hereditary retinal degenerations. Am J Ophthalmol 1982;93(6):733-8
52. Edwards TL, Groppe M, MacLaren RE. Outcomes following cataract surgery in choroideremia. Eye (Lond) 2015;29(4):460-4
53. Robinson D, Tiedeman J. Choroideremia associated with a subretinal neovascular membrane. Case report. Retina 1987;7(2):70-4
54. Palejwala NV, Lauer AK, Weleber RG. Choroideremia associated with choroidal neovascularization treated with intravitreal bevacizumab. Clin Ophthalmol 2014;8:1675-9
55. Campos-Pavón J, Torres-Penã JL. Choroidal neovascularization secondary to choroideremia. Arch Soc Esp Oftalmol 2014:pii: S0365-6691(14)00104-X.
56. Endo K, Yuzawa M, Ohba N. Choroideremia associated with subretinal neovascular membrane. Acta Ophthalmol Scand 2000;78(4):483-6
57. Genead MA, Fishman GA. Cystic macular oedema on spectral-domain optical coherence tomography in choroideremia patients without cystic changes on fundus examination. Eye (Lond) 2011;25(1):84-90
58. Genead MA, McAnany JJ, Fishman GA. Topical dorzolamide for treatment of cystoid macular edema in patients with choroideremia. Retina 2012;32(4):826-33
59. Salvatore S, Fishman GA, Genead MA. Treatment of cystic macular lesions in hereditary retinal dystrophies. Surv Ophthalmol 2013;58(6):560-84
60. Grover AK, Samson SE. Antioxidants and vision health: facts and fiction. Mol Cell Biochem 2014;388(1-2):173-83
61. Hoffman DR, Hughbanks-Wheaton DK, Pearson NS, et al. Four-year placebocontrolled trial of docosahexaenoic acid in X-linked retinitis pigmentosa (DHAX trial): a randomized clinical trial. JAMA Ophthalmol 2014;132(7):866-73
62. Duncan JL, Aleman TS, Gardner LM, et al. Macular pigment and lutein supplementation in choroideremia. Exp Eye Res 2002;74(3):371-81
63. Zhao DY, Wintch SW, Ermakov IV, et al. Resonance Raman measurement of macular carotenoids in retinal, choroidal, and macular dystrophies. Arch Ophthalmol 2003;121(7):967-72
64. Freund P, Furgoch M, MacDonald IM. Genotype-phenotype analysis of male subjects affected by Choroideremia. Invest Ophthalmol Vis Sci 2013;54:ARVO abstract 1567
65. Coussa RG, Kim J, Traboulsi EI. Choroideremia: effect of age on visual acuity in patients and female carriers. Ophthalmic Genet 2012;33(2):66-73.
66. Moosajee M, Tulloch M, Baron RA, et al. Single choroideremia gene in nonmammalian vertebrates explains early embryonic lethality of the zebrafish model of choroideremia. Invest Ophthalmol Vis Sci 2009;50(6):3009-16
67. Tolmachova T, Anders R, Abrink M, et al. Independent degeneration of photoreceptors and retinal pigment epithelium in conditional knockout mouse models of choroideremia. J Clin Invest 2006;116(2):386-94
68. Tolmachova T, Wavre-Shapton ST, Barnard AR, et al. Retinal pigment epithelium defects accelerate photoreceptor degeneration in cell typespecific knockout mouse models of choroideremia. Invest Ophthalmol Vis Sci 2010;51(10):4913-20.
69. Krock BL, Bilotta J, Perkins BD. Noncell-autonomous photoreceptor degeneration in a zebrafish model of choroideremia. Proc Natl Acad Sci USA 2007;104(11):4600-5.
70. Gordiyenko NV, Fariss RN, Zhi C, et al. Silencing of the CHM gene alters phagocytic and secretory pathways in the retinal pigment epithelium. Invest Ophthalmol Vis Sci 2010;51(2):1143-50
71. Syed N, Smith JE, John SK, et al. Evaluation of retinal photoreceptors and pigment epithelium in a female carrier of choroideremia. Ophthalmology 2001;108(4):711-20
72. MacDonald IM, Chan CC, Hiriyanna KT, et al. REP-1 localization in the eye. Invest Ophthalmol Vis Sci 2005;46:ARVO abstract 540.
73. Syed R, Sundquist SM, Ratnam K, et al. High-resolution images of retinal structure in patients with choroideremia. Invest Ophthalmol Vis Sci 2013;54(2):950-61
74. MacDonald IM, Russell L, Chan CC. Choroideremia: new findings from ocular pathology and review of recent literature. Surv Ophthalmol 2009;54(3):401-7
75. Birch DG, Locke KG, Wen Y, et al. Spectral-domain optical coherence tomography measures of outer segment layer progression in patients with X-linked retinitis pigmentosa. JAMA Ophthalmol 2013;131(9):1143-50
76. Kaiser PK. Prospective evaluation of visual acuity assessment: a comparison of snellen versus ETDRS charts in clinical practice (An AOS Thesis). Trans Am Ophthalmol Soc 2009;107:311-24
77. Acton JH, Greenstein VC. Fundus-driven perimetry (microperimetry) compared to conventional static automated perimetry: similarities, differences, and clinical applications. Can J Ophthalmol 2013;48(5):358-63
78. MacLaren RE, Groppe M, Barnard AR, et al. Retinal gene therapy in patients with choroideremia: initial findings from a phase 1/2 clinical trial. Lancet 2014;383(9923):1129-37.
79. Moosajee M, Gregory-Evans K, Ellis CD, et al. Translational bypass of nonsense mutations in zebrafish rep1, pax2.1 and lamb1 highlights a viable therapeutic option for untreatable genetic eye disease. Hum Mol Genet 2008;17(24):3987-4000
80. Schwarz N, Carr AJ, Lane A, et al. Translational read-through of the RP2 Arg120stop mutation in patient iPSC-derived retinal pigment epithelium cells. Hum Mol Genet 2014;24(4):972-86
81. Goldmann T, Overlack N, Wolfrum U, et al. PTC124-mediated translational readthrough of a nonsense mutation causing Usher syndrome type 1C. Hum Gene Ther 2011;22(5):537-47
82. Nathwani AC, Reiss UM, Tuddenham EG, et al. Long-term safety and efficacy of factor IX gene therapy in hemophilia B. N Engl J Med 2014;371(21):1994-2004
83. Testa F, Maguire AM, Rossi S, et al. Three-year follow-up after unilateral subretinal delivery of adeno-associated virus in patients with Leber congenital Amaurosis type 2. Ophthalmology 2013;120(6):1283-91
84. Anand V, Barral DC, Zeng Y, et al. Gene therapy for choroideremia: in vitro rescue mediated by recombinant adenovirus. Vision Res 2003;43(8):919-26
85. Tolmachova T, Tolmachov OE, Barnard AR, et al. Functional expression of Rab escort protein 1 following AAV2-mediated gene delivery in the retina of choroideremia mice and human cells ex vivo. J Mol Med (Berl) 2013;91(7):825-37.
86. Vasireddy V, Mills JA, Gaddameedi R, et al. AAV-mediated gene therapy for choroideremia: preclinical studies in personalized models. PLoS One 2013;8(5):e61396
87. Cereso N, Pequiognot M, Robert L, et al. Proof of concept for AAV2/5-mediated gene therapy in iPSC-derived retinal pigment epithelium of a choroideremia patient. Mol Ther Methods Clin Develop 1, 2014:14011, doi:10.1038/mtm.2014.11.
88. Black A, Vasireddy V, Chung DC, et al. Adeno-associated virus 8-mediated gene therapy for choroideremia: preclinical studies in in vitro and in vivo models. J Gene Med 2014;16(5-6):122-30
89. Bainbridge JW, Smith AJ, Barker SS, et al. Effect of gene therapy on visual function in Leber's congenital amaurosis. N Engl J Med 2008;358(21):2231-9
90. Hauswirth WW, Aleman TS, Kaushal S, et al. Treatment of leber congenital amaurosis due to RPE65 mutations by ocular subretinal injection of adenoassociated virus gene vector: short-term results of a phase I trial. Hum Gene Ther 2008;19(10):979-90
91. Maguire AM, Simonelli F, Pierce EA, et al. Safety and efficacy of gene transfer for Leber's congenital amaurosis. N Engl J Med 2008;358(21):2240-8
92. Bennett J, Maguire AM, Cideciyan AV, et al. Stable transgene expression in rod photoreceptors after recombinant adenoassociated virus-mediated gene transfer to monkey retina. Proc Natl Acad Sci USA 1999;96(17):9920-5