January 2013
Volume 54, Issue 1
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Letters to the Editor  |   January 2013
Author Response: Retinal Phenotypes in Patients Homozygous for the G1961E Mutation in the ABCA4 Gene
Author Affiliations & Notes
  • Tomas R. Burke
    The Oxford Deanery, Stoke Mandeville Hospital, Aylesbury, United Kingdom; and the
  • Rando Allikmets
    Departments of Ophthalmology, Pathology and Cell Biology, Columbia University, New York, New York.
Investigative Ophthalmology & Visual Science January 2013, Vol.54, 521. doi:https://doi.org/10.1167/iovs.12-11528
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      Tomas R. Burke, Rando Allikmets; Author Response: Retinal Phenotypes in Patients Homozygous for the G1961E Mutation in the ABCA4 Gene. Invest. Ophthalmol. Vis. Sci. 2013;54(1):521. https://doi.org/10.1167/iovs.12-11528.

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      © ARVO (1962-2015); The Authors (2016-present)

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Introduction
We appreciate the interest and comments of Burton et al. 1 relating to our recent publication “Retinal phenotypes in patients homozygous for the G1961E mutation in the ABCA4 gene.” 2 In our report of 12 patients homozygous for the G1961E mutation, six patients had “milder” and six had more “severe” retinal disease phenotypes (as suggested by the extent of retinal changes present). Of the six patients in the latter group, five had additional mutations detected in cis with G1961E on either one or both chromosomes (i.e., complex alleles), clearly exacerbating protein dysfunction and, consequently, disease severity. We concluded that the G1961E mutation causes disease in homozygosity and that these patients exhibit a wide range of retinal phenotypes. 
Therefore, our findings were consistent with the authors' statement that “there may not be a meaningful difference in the phenotype” between patients homozygous and (compound) heterozygous for the G1961E mutation. The publications that they cited, together with other reports (both from our group as well as that from others), have shown that G1961E, in either compound heterozygous or homozygous state, tends to be associated with a localized retinal disease phenotype, including bull's eye maculopathy, the absence of a “silent” choroid on fluorescein angiogram, and a normal full-field electroretinogram. 35 The cumulative evidence suggests that even in cases of a “severe” second mutation (those resulting in a nonfunctional protein, such as nonsense mutations and frameshift-generating variants), G1961E tends to yield a “milder” phenotype, although variation in phenotype has also been reported in such patients. 6  
With regard to age of onset of visual symptoms in ABCA4 disease, the severity of phenotype may also be affected by environmental or genetic (other than ABCA4) modifying factors and their effects on ABCA4 protein function. This parameter is also affected by either the presence or the absence of foveal sparing. It is clear from reviewing the literature pertaining to ABCA4 disease that variations in age of onset are common, even for genetically homogeneous family members. Nonetheless, trends in age of onset emerge from the studies of patient cohorts that carry at least one mutation, which is the same for the entire cohort, and these have suggested that this is generally later for patients with the G1961E mutation. 
In summary, patients homozygous and heterozygous for the G1961E mutation in the ABCA4 gene tend to demonstrate a milder phenotype, including a later age of onset of visual symptoms. However, there are exceptions to this rule. 
References
Burton DSM Ali M McKibbin M. Retinal phenotypes in patients homozygous for the G1961E mutation in the ABCA4 gene. Invest Ophthalmol Vis Sci . 2013; 54: 520. [CrossRef] [PubMed]
Burke TR Fishman GA Zernant J Retinal phenotypes in patients homozygous for the G1961E mutation in the ABCA4 gene. Invest Ophthalmol Vis Sci . 2012; 53: 4458–4467. [CrossRef] [PubMed]
Fishman GA Stone EM Grover S Derlacki DJ Haines HL Hockey RR. Variation of clinical expression in patients with Stargardt dystrophy and sequence variations in the ABCR gene. Arch Ophthalmol . 1999; 117: 504–510. [CrossRef] [PubMed]
Simonelli F Testa F Zernant J Genotype-phenotype correlation in Italian families with Stargardt disease. Ophthalmic Res . 2005; 37: 159–167. [CrossRef] [PubMed]
Cella W Greenstein VC Zernant-Rajang J G1961E mutant allele in the Stargardt disease gene ABCA4 causes bull's eye maculopathy. Exp Eye Res . 2009; 89: 16–24. [CrossRef] [PubMed]
Burke TR Tsang SH Zernant J Smith RT Allikmets R. Familial discordance in Stargardt disease. Mol Vis . 2012; 18: 227–233. [PubMed]
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