ABCA4 and ROM1: Implications for modification of the PRPH2-associated macular dystrophy phenotype

Investigative Ophthalmology and Visual Science

Volumn 51, Issue 8, 2010, Pages 4253-4265

  Poloschek, Charlotte M ^a   Bach, Michael ^a   Lagrèze, Wolf A ^a   Glaus, Esther ^b   Lemke, Johannes R ^c   Berger, Wolfgang ^b   Neidhardt, John ^b  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF ZURICH   (Switzerland)

^c UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ABCA4 GENE; ADULT; AGED; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE COURSE; DISEASE SEVERITY; DNA MODIFICATION; DNA SEQUENCE; ELECTROPHYSIOLOGY; FEMALE; GENE; GENE FUNCTION; GENE IDENTIFICATION; GENETIC ASSOCIATION; GENETIC SCREENING; GENETIC VARIABILITY; HETEROZYGOSITY; HUMAN; MALE; MICROARRAY ANALYSIS; MUTATIONAL ANALYSIS; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PRPH2 GENE; RETINA MACULA DEGENERATION; ROM1 GENE; VISUAL IMPAIRMENT; ELECTROOCULOGRAPHY; ELECTRORETINOGRAPHY; FLUORESCENCE ANGIOGRAPHY; GENETICS; GENOTYPE; MIDDLE AGED; MUTATION; NUCLEOTIDE SEQUENCE; OPHTHALMOSCOPY; PATHOLOGY; PEDIGREE; PHOTORECEPTOR CELL;

ABC TRANSPORTER; ABCA4 PROTEIN, HUMAN; INTERMEDIATE FILAMENT PROTEIN; MEMBRANE PROTEIN; NERVE PROTEIN; PERIPHERIN; ROM1 PROTEIN, HUMAN;

ADULT; AGED; AGED, 80 AND OVER; ATP-BINDING CASSETTE TRANSPORTERS; DNA MUTATIONAL ANALYSIS; ELECTROOCULOGRAPHY; ELECTRORETINOGRAPHY; FEMALE; FLUORESCEIN ANGIOGRAPHY; GENOTYPE; HUMANS; INTERMEDIATE FILAMENT PROTEINS; MACULAR DEGENERATION; MALE; MEMBRANE GLYCOPROTEINS; MEMBRANE PROTEINS; MIDDLE AGED; MUTATION; NERVE TISSUE PROTEINS; OPHTHALMOSCOPY; PEDIGREE; PHENOTYPE; PHOTORECEPTOR CELLS, VERTEBRATE; YOUNG ADULT;

EID: 77954735797     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.09-4655     Document Type: Article

References (84)

1. Farrar GJ, Kenna P, Jordan SA, et al. A three-base-pair deletion in the peripherin-RDS gene in one form of retinitis pigmentosa. Nature. 1991;354:478-480.
2. Wells J, Wroblewski J, Keen J, et al. Mutations in the human retinal degeneration slow (RDS) gene can cause either retinitis pigmentosa or macular dystrophy. Nat Genet. 1993;3:213-218.
3. Kajiwara K, Hahn LB, Mukai S, Travis GH, Berson EL, Dryja TP. Mutations in the human retinal degeneration slow gene in autosomal dominant retinitis pigmentosa. Nature. 1991;354:480-483.
4. Gruning G, Millan JM, Meins M, et al. Mutations in the human peripherin/RDS gene associated with autosomal dominant retinitis pigmentosa. Hum Mutat. 1994;3:321-323.
5. Sullivan LS, Bowne SJ, Birch DG, et al. Prevalence of diseasecausing mutations in families with autosomal dominant retinitis pigmentosa: a screen of known genes in 200 families. Invest Ophthalmol Vis Sci. 2006;47:3052-3064.
6. Kajiwara K, Berson EL, Dryja TP. Digenic retinitis pigmentosa due to mutations at the unlinked peripherin/RDS and ROM1 loci. Science. 1994;264:1604-1608.
7. Dryja TP, Hahn LB, Kajiwara K, Berson EL. Dominant and digenic mutations in the peripherin/RDS and ROM1 genes in retinitis pigmentosa. Invest Ophthalmol Vis Sci. 1997;38:1972-1982.
8. Kajiwara K, Sandberg MA, Berson EL, Dryja TP. A null mutation in the human peripherin/RDS gene in a family with autosomal dominant retinitis punctata albescens. Nat Genet. 1993;3:208-212.
9. Michaelides M, Holder GE, Bradshaw K, Hunt DM, Moore AT. Cone-rod dystrophy, intrafamilial variability, and incomplete penetrance associated with the R172W mutation in the peripherin/RDS gene. Ophthalmology. 2005;112:1592-1598.
10. Nakazawa M, Kikawa E, Chida Y, Tamai M. Asn244His mutation of the peripherin/RDS gene causing autosomal dominant cone-rod degeneration. Hum Mol Genet. 1994;3:1195-1196.
11. Nakazawa M, Kikawa E, Chida Y, Wada Y, Shiono T, Tamai M. Autosomal dominant cone-rod dystrophy associated with mutations in codon 244 (Asn244His) and codon 184 (Tyr184Ser) of the peripherin/RDS gene. Arch Ophthalmol. 1996;114:72-78.
12. Fishman GA, Stone EM, Alexander KR, Gilbert LD, Derlacki DJ, Butler NS. Serine-27-phenylalanine mutation within the peripherin/ RDS gene in a family with cone dystrophy. Ophthalmology. 1997;104:299-306.
13. Wroblewski JJ, Wells JA 3rd, Eckstein A, et al. Macular dystrophy associated with mutations at codon 172 in the human retinal degeneration slow gene. Ophthalmology. 1994;101:12-22.
14. Renner AB, Tillack H, Kraus H, et al. Morphology and functional characteristics in adult vitelliform macular dystrophy. Retina. 2004;24:929-939.
15. Felbor U, Schilling H, Weber BH. Adult vitelliform macular dystrophy is frequently associated with mutations in the peripherin/RDS gene. Hum Mutat. 1997;10:301-309.
16. Zhuk SA, Edwards AO. Peripherin/RDS and VMD2 mutations in macular dystrophies with adult-onset vitelliform lesion. Mol Vis. 2006;12:811-815.
17. Apfelstedt-Sylla E, Theischen M, Ruther K, Wedemann H, Gal A, Zrenner E. Extensive intrafamilial and interfamilial phenotypic variation among patients with autosomal dominant retinal dystrophy and mutations in the human RDS/peripherin gene. Br J Ophthalmol. 1995;79:28-34.
18. Nichols BE, Drack AV, Vandenburgh K, Kimura AE, Sheffield VC, Stone EM. A 2 base pair deletion in the RDS gene associated with butterfly-shaped pigment dystrophy of the fovea. Hum Mol Genet. 1993;2:601-603.
19. Nichols BE, Sheffield VC, Vandenburgh K, Drack AV, Kimura AE, Stone EM. Butterfly-shaped pigment dystrophy of the fovea caused by a point mutation in codon 167 of the RDS gene. Nat Genet. 1993;3:202-207.
20. Travis GH, Hepler JE. A medley of retinal dystrophies. Nat Genet. 1993;3:191-192.
21. Haider NB, Ikeda A, Naggert JK, Nishina PM. Genetic modifiers of vision and hearing. Hum Mol Genet. 2002;11:1195-1206.
22. Nadeau JH. Modifier genes in mice and humans. Nat Rev Genet. 2001;2:165-174.
23. Danciger M, Ogando D, Yang H, et al. Genetic modifiers of retinal degeneration in the rd3 mouse. Invest Ophthalmol Vis Sci. 2008; 49:2863-2869.
24. Haider NB, Zhang W, Hurd R, et al. Mapping of genetic modifiers of Nr2e3 rd7/rd7 that suppress retinal degeneration and restore blue cone cells to normal quantity. Mamm Genome. 2008;19:145-154.
25. Johnson BA, Aoyama N, Friedell NH, Ikeda S, Ikeda A. Genetic modification of the schisis phenotype in a mouse model of Xlinked retinoschisis. Genetics. 2008;178:1785-1794.
26. Wong G, Conger SB, Burmeister M. Mapping of genetic modifiers affecting the eye phenotype of ocular retardation (Chx10or-J) mice. Mamm Genome. 2006;17:518-525.
27. Liu Q, Saveliev A, Pierce EA. The severity of retinal degeneration in Rp1h gene-targeted mice is dependent on genetic background. Invest Ophthalmol Vis Sci. 2009;50:1566-1574.
28. Humphries MM, Kiang S, McNally N, et al. Comparative structural and functional analysis of photoreceptor neurons of Rho-/- mice reveal increased survival on C57BL/6J in comparison to 129Sv genetic background. Vis Neurosci. 2001;18:437-443.
29. Samardzija M, Wenzel A, Naash M, Reme CE, Grimm C. Rpe65 as a modifier gene for inherited retinal degeneration. Eur J Neurosci. 2006;23:1028-1034.
30. Rio Frio T, Civic N, Ransijn A, Beckmann JS, Rivolta C. Two trans-acting eQTLs modulate the penetrance of PRPF31 mutations. Hum Mol Genet. 2008;17:3154-3165.
31. Travis GH, Christerson L, Danielson PE, et al. The human retinal degeneration slow (RDS) gene: chromosome assignment and structure of the mRNA. Genomics. 1991;10:733-739.
32. Travis GH, Sutcliffe JG, Bok D. The retinal degeneration slow (rds) gene product is a photoreceptor disc membrane-associated glycoprotein. Neuron. 1991;6:61-70.
33. Sanyal S, De Ruiter A, Hawkins RK. Development and degeneration of retina in rds mutant mice: light microscopy. J Comp Neurol. 1980;194:193-207.
34. Sanyal S, Jansen HG. Absence of receptor outer segments in the retina of rds mutant mice. Neurosci Lett. 1981;21:23-26.
35. Arikawa K, Molday LL, Molday RS, Williams DS. Localization of peripherin/rds in the disk membranes of cone and rod photoreceptors: relationship to disk membrane morphogenesis and retinal degeneration. J Cell Biol. 1992;116:659-667.
36. Moritz OL, Molday RS. Molecular cloning, membrane topology, and localization of bovine rom-1 in rod and cone photoreceptor cells. Invest Ophthalmol Vis Sci. 1996;37:352-362.
37. Bascom RA, Manara S, Collins L, Molday RS, Kalnins VI, McInnes RR. Cloning of the cDNA for a novel photoreceptor membrane protein (rom-1) identifies a disk rim protein family implicated in human retinopathies. Neuron. 1992;8:1171-1184.
38. Goldberg AF, Moritz OL, Molday RS. Heterologous expression of photoreceptor peripherin/rds and Rom-1 in COS-1 cells: assembly, interactions, and localization of multisubunit complexes. Biochemistry. 1995;34:14213-14219.
39. Clarke G, Goldberg AF, Vidgen D, et al. Rom-1 is required for rod photoreceptor viability and the regulation of disk morphogenesis. Nat Genet. 2000;25:67-73.
40. Maia-Lopes S, Silva ED, Silva MF, Reis A, Faria P, Castelo-Branco M. Evidence of widespread retinal dysfunction in patients with Stargardt disease and morphologically unaffected carrier relatives. Invest Ophthalmol Vis Sci. 2008;49:1191-1199.
41. Allikmets R, Singh N, Sun H, et al. A photoreceptor cell-specific ATP-binding transporter gene (ABCR) is mutated in recessive Stargardt macular dystrophy. Nat Genet. 1997;15:236-246.
42. Sun H, Nathans J. Stargardt's ABCR is localized to the disc membrane of retinal rod outer segments. Nat Genet. 1997;17:15-16.
43. Molday LL, Rabin AR, Molday RS. ABCR expression in foveal cone photoreceptors and its role in Stargardt macular dystrophy. Nat Genet. 2000;25:257-258.
44. 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.
45. Sullivan JM. Focus on molecules: ABCA4 (ABCR): an import-directed photoreceptor retinoid flipase. Exp Eye Res. 2009;89(5): 602-603.
46. Maugeri A, van Driel MA, van de Pol DJ, et al. The 2588G3C mutation in the ABCR gene is a mild frequent founder mutation in the Western European population and allows the classification of ABCR mutations in patients with Stargardt disease. Am J Hum Genet. 1999;64:1024-1035.
47. Rozet JM, Gerber S, Souied E, et al. Spectrum of ABCR gene mutations in autosomal recessive macular dystrophies. Eur J Hum Genet. 1998;6:291-295.
48. Gerth C, Andrassi-Darida M, Bock M, Preising MN, Weber BH, Lorenz B. Phenotypes of 16 Stargardt macular dystrophy/fundus flavimaculatus patients with known ABCA4 mutations and evaluation of genotype-phenotype correlation. Graefes Arch Clin Exp Ophthalmol. 2002;240:628-638.
49. Briggs CE, Rucinski D, Rosenfeld PJ, Hirose T, Berson EL, Dryja TP. Mutations in ABCR (ABCA4) in patients with Stargardt macular degeneration or cone-rod degeneration. Invest Ophthalmol Vis Sci. 2001;42:2229-2236.
50. Cremers FP, van de Pol DJ, van Driel M, et al. Autosomal recessive retinitis pigmentosa and cone-rod dystrophy caused by splice site mutations in the Stargardt's disease gene ABCR. Hum Mol Genet. 1998;7:355-362.
51. Fishman GA, Stone EM, Eliason DA, Taylor CM, Lindeman M, Derlacki DJ. ABCA4 gene sequence variations in patients with autosomal recessive cone-rod dystrophy. Arch Ophthalmol. 2003; 121:851-855.
52. Valverde D, Riveiro-Alvarez R, Aguirre-Lamban J, et al. Spectrum of the ABCA4 gene mutations implicated in severe retinopathies in Spanish patients. Invest Ophthalmol Vis Sci. 2007;48:985-990.
53. Klevering BJ, Blankenagel A, Maugeri A, Cremers FP, Hoyng CB, Rohrschneider K. Phenotypic spectrum of autosomal recessive cone-rod dystrophies caused by mutations in the ABCA4 (ABCR) gene. Invest Ophthalmol Vis Sci. 2002;43:1980-1985.
54. Maugeri A, Klevering BJ, Rohrschneider K, et al. Mutations in the ABCA4 (ABCR) gene are the major cause of autosomal recessive cone-rod dystrophy. Am J Hum Genet. 2000;67:960-966.
55. Martinez-Mir A, Paloma E, Allikmets R, et al. Retinitis pigmentosa caused by a homozygous mutation in the Stargardt disease gene ABCR. Nat Genet. 1998;18:11-12.
56. Shroyer NF, Lewis RA, Yatsenko AN, Lupski JR. Null missense ABCR (ABCA4) mutations in a family with stargardt disease and retinitis pigmentosa. Invest Ophthalmol Vis Sci. 2001;42:2757-2761.
57. Fukui T, Yamamoto S, Nakano K, et al. ABCA4 gene mutations in Japanese patients with Stargardt disease and retinitis pigmentosa. Invest Ophthalmol Vis Sci. 2002;43:2819-2824.
58. Rudolph G, Kalpadakis P, Haritoglou C, Rivera A, Weber BH. Mutations in the ABCA4 gene in a family with Stargardt's disease and retinitis pigmentosa (STGD1/RP19) (in German). Klin Monatsbl Augenheilkd. 2002;219:590-596.
59. Allikmets R, Shroyer NF, Singh N, et al. Mutation of the Stargardt disease gene (ABCR) in age-related macular degeneration. Science. 1997;277:1805-1807.
60. Souied EH, Ducroq D, Rozet JM, et al. ABCR gene analysis in familial exudative age-related macular degeneration. Invest Ophthalmol Vis Sci. 2000;41:244-247.
61. De La Paz MA, Guy VK, Abou-Donia S, et al. Analysis of the Stargardt disease gene (ABCR) in age-related macular degeneration. Ophthalmology. 1999;106:1531-1536.
62. Webster AR, Heon E, Lotery AJ, et al. An analysis of allelic variation in the ABCA4 gene. Invest Ophthalmol Vis Sci. 2001;42:1179-1189.
63. Downes SM, Fitzke FW, Holder GE, et al. Clinical features of codon 172 RDS macular dystrophy: similar phenotype in 12 families. Arch Ophthalmol. 1999;117:1373-1383.
64. Nakazawa M, Wada Y, Tamai M. Macular dystrophy associated with monogenic Arg172Trp mutation of the peripherin/RDS gene in a Japanese family. Retina. 1995;15:518-523.
65. Piguet B, Heon E, Munier FL, et al. Full characterization of the maculopathy associated with an Arg-172-Trp mutation in the RDS/ peripherin gene. Ophthalmic Genet. 1996;17:175-186.
66. Reig C, Serra A, Gean E, et al. A point mutation in the RDSperipherin gene in a Spanish family with central areolar choroidal dystrophy. Ophthalmic Genet. 1995;16:39-44.
67. Kohl S, Christ-Adler M, Apfelstedt-Sylla E, et al. RDS/peripherin gene mutations are frequent causes of central retinal dystrophies. J Med Genet. 1997;34:620-626.
68. World Medical Association Declaration of Helsinki: ethical principles for medical research involving human subjects. JAMA 2000;284:3043-3045.
69. von Ruckmann A, Fitzke FW, Bird AC. Distribution of fundus autofluorescence with a scanning laser ophthalmoscope. Br J Ophthalmol. 1995;79:407-412.
70. Marmor MF, Fulton AB, Holder GE, Miyaki Y, Brigell M, Bach M. Standard for clinical electroretinography (2008 update). Doc Ophthalmol. 2009;118:69-77.
71. Hood DC, Bach M, Brigell M, et al. ISCEV guidelines for clinical multifocal electroretinography (2007 edition). Doc Ophthalmol. 2008;116:1-11.
72. Marmor MF, Hood DC, Keating D, Kondo M, Seeliger MW, Miyake Y. Guidelines for basic multifocal electroretinography (mfERG). Doc Ophthalmol. 2003;106:105-115.
73. Bascom RA, Liu L, Humphries P, Fishman GA, Murray JC, McInnes RR. Polymorphisms and rare sequence variants at the ROM1 locus. Hum Mol Genet. 1993;2:1975-1977.
74. Bascom RA, Liu L, Heckenlively JR, Stone EM, McInnes RR. Mutation analysis of the ROM1 gene in retinitis pigmentosa. Hum Mol Genet. 1995;4:1895-1902.
75. Martinez-Mir A, Vilela C, Bayes M, et al. Putative association of a mutant ROM1 allele with retinitis pigmentosa. Hum Genet. 1997; 99:827-830.
76. Shroyer NF, Lewis RA, Allikmets R, et al. The rod photoreceptor ATP-binding cassette transporter gene, ABCR, and retinal disease: from monogenic to multifactorial. Vision Res. 1999;39:2537-2544.
77. Cideciyan AV, Swider M, Aleman TS, et al. ABCA4 disease progression and a proposed strategy for gene therapy. Hum Mol Genet. 2009;18:931-941.
78. Klevering BJ, Yzer S, Rohrschneider K, et al. Microarray-based mutation analysis of the ABCA4 (ABCR) gene in autosomal recessive cone-rod dystrophy and retinitis pigmentosa. Eur J Hum Genet. 2004;12:1024-1032.
79. Mata NL, Tzekov RT, Liu X, Weng J, Birch DG, Travis GH. Delayed dark-adaptation and lipofuscin accumulation in abcr-/- mice: implications for involvement of ABCR in age-related macular degeneration. Invest Ophthalmol Vis Sci. 2001;42:1685-1690.
80. Leroy BP, Kailasanathan A, De Laey JJ, Black GC, Manson FD. Intrafamilial phenotypic variability in families with RDS mutations: exclusion of ROM1 as a genetic modifier for those with retinitis pigmentosa. Br J Ophthalmol. 2007;91:89-93.
81. Goldberg AF, Molday RS. Defective subunit assembly underlies a digenic form of retinitis pigmentosa linked to mutations in peripherin/rds and rom-1. Proc Natl Acad Sci U S A. 1996;93:13726-13730.
82. Goldberg AF, Molday RS. Subunit composition of the peripherin/ rds-rom-1 disk rim complex from rod photoreceptors: hydrodynamic evidence for a tetrameric quaternary structure. Biochemistry. 1996;35:6144-6149.
83. Katsanis N, Ansley SJ, Badano JL, et al. Triallelic inheritance in Bardet-Biedl syndrome, a Mendelian recessive disorder. Science.2001;293:2256-2259.
84. Badano JL, Kim JC, Hoskins BE, et al. Heterozygous mutations in BBS1, BBS2 and BBS6 have a potential epistatic effect on Bardet- Biedl patients with two mutations at a second BBS locus. Hum Mol Genet. 2003;12:1651-1659.