Early onset retinal dystrophy due to mutations in LRAT: Molecular analysis and detailed phenotypic study

Investigative Ophthalmology and Visual Science

Volumn 53, Issue 7, 2012, Pages 3927-3938

  Dev Borman, Arundhati ^a,b   Ocaka, Louise A ^a   Mackay, Donna S ^a   Ripamonti, Caterina ^a   Henderson, Robert H ^a,b   Moradi, Phillip ^a,b   Hal, Georgina ^c   Black, Graeme C ^c   Robson, Anthony G ^a,b   Holder, Graham E ^a,b   Webster, Andrew R ^a,b   Fitzke, Fred ^a   Stockman, Andrew ^a   Moore, Anthony T ^a,b  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b MOORFIELDS EYE HOSPITAL   (United Kingdom)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; AUTOFLUORESCENCE IMAGING; CLINICAL EXAMINATION; CRITICAL FLICKER FUSION; DISEASE COURSE; ELECTRORETINOGRAPHY; EPIRETINAL MEMBRANE; FEMALE; GENE; GENETIC ANALYSIS; HUMAN; LECITHIN RETINOL ACYLTRANSFERASE GENE; MAJOR CLINICAL STUDY; MALE; MICROARRAY ANALYSIS; NIGHT BLINDNESS; OPHTHALMOSCOPY; OPTICAL COHERENCE TOMOGRAPHY; PERIMETRY; PHOTORECEPTOR; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RETINA MALFORMATION; SPECTRAL SENSITIVITY; VISUAL ACUITY; VISUAL FIELD; CONSANGUINITY; DARK ADAPTATION; DNA MICROARRAY; ENZYMOLOGY; GENETICS; INFANT; LEBER CONGENITAL AMAUROSIS; MOLECULAR BIOLOGY; MUTATION; NUCLEOTIDE SEQUENCE; PATHOLOGY; PHENOTYPE; PHOTORECEPTOR CELL; PHYSIOLOGY; PRESCHOOL CHILD; RETINA DYSTROPHY;

ACYLTRANSFERASE; LECITHIN RETINOL ACYLTRANSFERASE; LECITHIN-RETINOL ACYLTRANSFERASE; PRIMER DNA;

ACYLTRANSFERASES; CHILD, PRESCHOOL; CONSANGUINITY; DARK ADAPTATION; DNA MUTATIONAL ANALYSIS; DNA PRIMERS; ELECTRORETINOGRAPHY; FEMALE; HUMANS; INFANT; LEBER CONGENITAL AMAUROSIS; MALE; MOLECULAR BIOLOGY; MUTATION; NIGHT BLINDNESS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHENOTYPE; PHOTORECEPTOR CELLS, VERTEBRATE; RETINAL DYSTROPHIES; TOMOGRAPHY, OPTICAL COHERENCE; VISUAL ACUITY; VISUAL FIELD TESTS; VISUAL FIELDS;

EID: 84866766350     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.12-9548     Document Type: Article

References (73)

1. 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;358:2231-2239.
2. Maguire AM, Simonelli F, Pierce EA, et al. Safety and efficacy of gene transfer for Leber's congenital amaurosis. N Engl J Med. 2008;358:2240-2248.
3. Hauswirth WW, Aleman TS, Kaushal S, et al. 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. 2008;19: 979-990.
4. Gearhart PM, Gearhart C, Thompson DA, Petersen-Jones SM. Improvement of visual performance with intravitreal administration of 9-cis-retinal in Rpe65-mutant dogs. Arch Ophthalmol. 2010;128:1442-1448.
5. Batten ML, Imanishi Y, Tu DC, et al. Pharmacological and rAAV gene therapy rescue of visual functions in a blind mouse model of Leber congenital amaurosis. PLoS Med. 2005;2:e333.
6. Koenekoop RK, Racine J, Al Humaid S, et al. Oral synthetic cisretinoid therapy in subjects with leber congenital amaurosis (LCA) due to lecithin: retinol acyltransferase (LRAT) or retinal pigment epithelial 65 protein (RPE65) mutations: preliminary results of a phase Ib open label trial. ARVO Meeting Abstracts. 2011;52:3323.
7. Palczewski K. Retinoids for treatment of retinal diseases. Trends Pharmacol Sci. 2010;31:284-295.
8. von Leber T. Ueber Refinitis pigmentosa und angeborene Amaurose. Graefes Arch Clin Exp Ophthalmol. 1869;15:1-25.
9. Perrault I, Rozet JM, Calvas P, et al. Retinal-specific guanylate cyclase gene mutations in Leber's congenital amaurosis. Nat Genet. 1996;14:461-464.
10. Marlhens F, Bareil C, Griffoin JM, et al. Mutations in RPE65 cause Leber's congenital amaurosis. Nat Genet. 1997;17:139-141.
11. North MA, Naggert JK, Yan Y, Noben-Trauth K, Nishina PM. Molecular characterization of TUB, TULP1, and TULP2, members of the novel tubby gene family and their possible relation to ocular diseases. Proc Natl Acad Sci U S A. 1997;94: 3128-3133.
12. Freund CL, Wang QL, Chen S, et al. De novo mutations in the CRX homeobox gene associated with Leber congenital amaurosis. Nat Genet. 1998;18:311-312.
13. Sohocki MM, Bowne SJ, Sullivan LS, et al. Mutations in a new photoreceptor-pineal gene on 17p cause Leber congenital amaurosis. Nat Genet. 2000;24:79-83.
14. Gal A, Li Y, Thompson DA, et al. Mutations in MERTK, the human orthologue of the RCS rat retinal dystrophy gene, cause retinitis pigmentosa. Nat Genet. 2000;26:270-271.
15. Dryja TP, Adams SM, Grimsby JL, et al. Null RPGRIP1 alleles in patients with Leber congenital amaurosis. Am J Hum Genet. 2001;68:1295-1298.
16. den Hollander AI, Heckenlively JR, van den Born LI, et al. Leber congenital amaurosis and retinitis pigmentosa with Coats-like exudative vasculopathy are associated with mutations in the crumbs homologue 1 (CRB1) gene. Am J Hum Genet. 2001;69:198-203.
17. Thompson DA, Li Y, McHenry CL, et al. Mutations in the gene encoding lecithin retinol acyltransferase are associated with early-onset severe retinal dystrophy. Nat Genet. 2001;28:123-124.
18. Janecke AR, Thompson DA, Utermann G, et al. Mutations in RDH12 encoding a photoreceptor cell retinol dehydrogenase cause childhood-onset severe retinal dystrophy. Nat Genet. 2004;36:850-854.
19. den Hollander AI, Koenekoop RK, Yzer S, et al. Mutations in the CEP290 (NPHP6) gene are a frequent cause of Leber congenital amaurosis. Am J Hum Genet. 2006;79:556-561.
20. den Hollander AI, Koenekoop RK, Mohamed MD, et al. Mutations in LCA5, encoding the ciliary protein lebercilin, cause Leber congenital amaurosis. Nat Genet. 2007;39:889-895.
21. Wang H, den Hollander AI, Moayedi Y, et al. Mutations in SPATA7 cause Leber congenital amaurosis and juvenile retinitis pigmentosa. Am J Hum Genet. 2009;84:380-387.
22. Estrada-Cuzcano A, Koenekoop RK, Coppieters F, et al. IQCB1 mutations in patients with leber congenital amaurosis. Invest Ophthalmol Vis Sci. 2011;52:834-839.
23. Keen TJ, Mohamed MD, McKibbin M, et al. Identification of a locus (LCA9) for Leber's congenital amaurosis on chromosome 1p36. Eur J Hum Genet. 2003;11:420-423.
24. Foxman SG, Heckenlively JR, Bateman JB, Wirtschafter JD. Classification of congenital and early onset retinitis pigmentosa. Arch Ophthalmol. 1985;103:1502-1506.
25. MacDonald PN, Ong DE. Evidence for a lecithin-retinol acyltransferase activity in the rat small intestine. J Biol Chem. 1988;263:12478-12482.
26. Ruiz A, Kuehn MH, Andorf JL, Stone E, Hageman GS, Bok D. Genomic organization and mutation analysis of the gene encoding lecithin retinol acyltransferase in human retinal pigment epithelium. Invest Ophthalmol Vis Sci. 2001;42:31-37.
27. Ruiz A, Winston A, Lim YH, Gilbert BA, Rando RR, Bok D. Molecular and biochemical characterization of lecithin retinol acyltransferase. J Biol Chem. 1999;274:3834-3841.
28. Senechal A, Humbert G, Surget MO, et al. Screening genes of the retinoid metabolism: novel LRAT mutation in leber congenital amaurosis. Am J Ophthalmol. 2006;142:702-704.
29. Batten ML, Imanishi Y, Maeda T, et al. Lecithin-retinol acyltransferase is essential for accumulation of all-trans-retinyl esters in the eye and in the liver. J Biol Chem. 2004;279: 10422-10432.
30. -/- mice: comparable models of leber congenital amaurosis. Invest Ophthalmol Vis Sci. 2008;49:2384-2389.
31. Preising MN, Paunescu K, Friedburg C, Lorenz B. Genetic and clinical heterogeneity in LCA patients. The end of uniformity. Ophthalmologe. 2007;104:490-498.
32. den Hollander AI, Lopez I, Yzer S, et al. Identification of novel mutations in patients with Leber congenital amaurosis and juvenile RP by genome-wide homozygosity mapping with SNP microarrays. Invest Ophthalmol Vis Sci. 2007;48:5690-5698.
33. Pastinen T, Kurg A, Metspalu A, Peltonen L, Syvanen AC. Minisequencing: a specific tool for DNA analysis and diagnostics on oligonucleotide arrays. Genome Res. 1997;7:606-614.
34. Shumaker JM, Metspalu A, Caskey CT. Mutation detection by solid phase primer extension. Hum Mutat. 1996;7:346-354.
35. Mackay DS, Henderson RH, Sergouniotis PI, et al. Novel mutations in MERTK associated with childhood onset rodcone dystrophy. Mol Vis. 2010;16:369-377.
36. Kumar P, Henikoff S, Ng PC. Predicting the effects of coding non-synonymous variants on protein function using the SIFT algorithm. Nat Protoc. 2009;4:1073-1081.
37. Adzhubei IA, Schmidt S, Peshkin L, et al. A method and server for predicting damaging missense mutations. Nat Methods. 2010;7:248-249.
38. Ferrer-Costa C, Orozco M, de la Cruz X. Sequence-based prediction of pathological mutations. Proteins. 2004;57:811-819.
39. NHLBI Exome Sequencing Project (ESP) S, WA. Exome Variant Server
40. Holder GE, Brigell MG, Hawlina M, Meigen T, Vaegan, Bach M. ISCEV standard for clinical pattern electroretinography-2007 update. Doc Ophthalmol. 2007;114:111-116.
41. Marmor MF, Fulton AB, Holder GE, Miyake Y, Brigell M, Bach M. ISCEV Standard for full-field clinical electroretinography (2008 update). Doc Ophthalmol. 2009;118:69-77.
42. Jacobson SG, Voigt WJ, Parel JM, et al. Automated light- and dark-adapted perimetry for evaluating retinitis pigmentosa. Ophthalmology. 1986;93:1604-1611.
43. Steinmetz RL, Haimovici R, Jubb C, Fitzke FW, Bird AC. Symptomatic abnormalities of dark adaptation in patients with age-related Bruch's membrane change. Br J Ophthalmol. 1993;77:549-554.
44. Chen JC, Fitzke FW, Pauleikhoff D, Bird AC. Functional loss in age-related Bruch's membrane change with choroidal perfusion defect. Invest Ophthalmol Vis Sci. 1992;33:334-340.
45. Stockman A, Plummer DJ, Montag ED. Spectrally opponent inputs to the human luminance pathway: slow{thorn}M and -L cone inputs revealed by intense long-wavelength adaptation. J Physiol. 2005;566:61-76.
46. Hecht S, Verrijp CD. The influence of intensity, color and retinal location on the fusion frequency of intermittent illumination. Proc Natl Acad Sci U S A. 1933;19:522-535.
47. Stockman A, MacLeod DI, DePriest DD. The temporal properties of the human short-wave photoreceptors and their associated pathways. Vision Res. 1991;31:189-208.
48. den Hollander AI, Roepman R, Koenekoop RK, Cremers FP. Leber congenital amaurosis: genes, proteins and disease mechanisms. Prog Retin Eye Res. 2008;27:391-419.
49. Sweeney MO, McGee TL, Berson EL, Dryja TP. Low prevalence of lecithin retinol acyltransferase mutations in patients with Leber congenital amaurosis and autosomal recessive retinitis pigmentosa. Mol Vis. 2007;13:588-593.
50. Anantharaman V, Aravind L. Evolutionary history, structural features and biochemical diversity of the NlpC/P60 superfamily of enzymes. Genome Biol. 2003;4:R11.
51. Kiser PD, Golczak M, Maeda A, Palczewski K. Key enzymes of the retinoid (visual) cycle in vertebrate retina. Biochim Biophys Acta. 2012;1821:137-151.
52. Mondal MS, Ruiz A, Hu J, Bok D, Rando RR. Two histidine residues are essential for catalysis by lecithin retinol acyl transferase. FEBS Lett. 2001;489:14-18.
53. Bok D, Ruiz A, Yaron O, et al. Purification and characterization of a transmembrane domain-deleted form of lecithin retinol acyltransferase. Biochemistry. 2003;42:6090-6098.
54. Mateja A, Szlachcic A, Downing ME, et al. The structural basis of tail-anchored membrane protein recognition by Get3. Nature. 2009;461:361-366.
55. Jaissle GB, May CA, van de Pavert SA, et al. Bone spicule pigment formation in retinitis pigmentosa: insights from a mouse model. Graefes Arch Clin Exp Ophthalmol. 2010;248: 1063-1070.
56. Hagiwara A, Yamamoto S, Ogata K, et al. Macular abnormalities in patients with retinitis pigmentosa: prevalence on OCT examination and outcomes of vitreoretinal surgery. Acta Ophthalmol. 2011;89:e122-e125.
57. Ikeda Y, Hisatomi T, Murakami Y, et al. Retinitis pigmentosa associated with asteroid hyalosis. Retina. 2010;30:1278-1281.
58. Lorenz B, Wabbels B, Wegscheider E, Hamel CP, Drexler W, Preising MN. Lack of fundus autofluorescence to 488 nanometers from childhood on in patients with early-onset severe retinal dystrophy associated with mutations in RPE65. Ophthalmology. 2004;111:1585-1594.
59. Sergouniotis PI, Sohn EH, Li Z, et al. Phenotypic variability in RDH5 retinopathy (fundus albipunctatus). Ophthalmology. 2011;118:1661-1670.
60. Schatz P, Preising M, Lorenz B, et al. Lack of autofluorescence in fundus albipunctatus associated with mutations in RDH5. Retina. 2010;30:1704-1713.
61. Palczewska G, Maeda T, Imanishi Y, et al. Noninvasive multiphoton fluorescence microscopy resolves retinol and retinal condensation products in mouse eyes. Nat Med. 2010; 16:1444-1449.
62. Katz ML, Redmond TM. Effect of Rpe65 knockout on accumulation of lipofuscin fluorophores in the retinal pigment epithelium. Invest Ophthalmol Vis Sci. 2001;42: 3023-3030.
63. Jacobson SG, Cideciyan AV, Aleman TS, et al. Photoreceptor layer topography in children with leber congenital amaurosis caused by RPE65 mutations. Invest Ophthalmol Vis Sci. 2008; 49:4573-4577.
64. Jacobson SG, Aleman TS, Cideciyan AV, et al. Defining the residual vision in leber congenital amaurosis caused by RPE65 mutations. Invest Ophthalmol Vis Sci. 2009;50:2368-2375.
65. Pasadhika S, Fishman GA, Stone EM, et al. Differential macular morphology in patients with RPE65-, CEP290-, GUCY2D-, and AIPL1-related Leber congenital amaurosis. Invest Ophthalmol Vis Sci. 2010;51:2608-2614.
66. Huber G, Beck SC, Grimm C, et al. Spectral domain optical coherence tomography in mouse models of retinal degeneration. Invest Ophthalmol Vis Sci. 2009;50:5888-5895.
67. Zhang T, Zhang N, Baehr W, Fu Y. Cone opsin determines the time course of cone photoreceptor degeneration in Leber congenital amaurosis. Proc Natl Acad Sci U S A. 2011;108: 8879-8884.
68. Samardzija M, von Lintig J, Tanimoto N, et al. R91W mutation in Rpe65 leads to milder early-onset retinal dystrophy due to the generation of low levels of 11-cis-retinal. Hum Mol Genet. 2008;17:281-292.
69. Lorenz B, Poliakov E, Schambeck M, Friedburg C, Preising MN, Redmond TM. A comprehensive clinical and biochemical functional study of a novel RPE65 hypomorphic mutation. Invest Ophthalmol Vis Sci. 2008;49:5235-5242.
70. Parker R, Wang JS, Kefalov VJ, Crouch RK. Interphotoreceptor retinoid-binding protein as the physiologically relevant carrier of 11-cis-retinol in the cone visual cycle. J Neurosci. 2011;31: 4714-4719.
71. Takahashi Y, Moiseyev G, Chen Y, Nikolaeva O, Ma JX. An alternative isomerohydrolase in the retinal M̈uller cells of a cone-dominant species. Febs J. 2011;278:2913-2926.
72. Judd DB. Report of U.S. Secretariat Committee on Colorimetry and Artificial Daylight, Proceedings of the Twelfth Session of the CIE, Stockholm (pp. 11). Paris: Bureau Central de la CI; 1951:11.
73. Central Bureau of the Commission Internationale de l' ́Eclairage (CIE). Fundamental Chromaticity Diagram With Physiological Axes-Parts 1 and 2. Report No. 170-1. Vienna, Austria: CIE; 2006.