Challenges confronting precision medicine in the context of inherited retinal disorders

References

• Das SK, Menezes ME, Bhatia S, et al. Gene therapies for cancer: strategies, challenges and successes. J Cell Physiol. 2015;230(2):259–271.
   PubMed Web of Science ®Google Scholar
• Gerstung M, Beisel C, Rechsteiner M, et al. Reliable detection of subclonal single-nucleotide variants in tumour cell populations. Nat Commun. 2012;3:811.
   PubMed Web of Science ®Google Scholar
• Pearce JM. The ophthalmoscope: Helmholtz’s Augenspiegel. Eur Neurol. 2009;61:244–249.
   PubMed Web of Science ®Google Scholar
• Dryja TP, McGee TL, Reichel E, et al. A point mutation of the rhodopsin gene in one form of retinitis pigmentosa. Nature. 1990;343(6256):364–366.
   PubMed Web of Science ®Google Scholar
• Daiger SP, Sullivan LS, Bowne SJ. RETNET. Available from: https://sph.uth.edu/retnet/
   Google Scholar
• Chiang JP, Trzupek K. The current status of molecular diagnosis of inherited retinal dystrophies. Curr Opin Ophthalmol. 2015;26(5):346–351.
   PubMed Web of Science ®Google Scholar
• Chiang JP, Lamey T, McLaren T, et al. Progress and prospects of next-generation sequencing testing for inherited retinal dystrophy. Expert Rev Mol Diagn. 2015;15(10):1269–1275.
   PubMed Web of Science ®Google Scholar
• Karali M, Banfi S. Inherited retinal dystrophies: the role of gene expression regulators. Int J Biochem Cell Biol. 2015;61:115–119.
   PubMed Web of Science ®Google Scholar
• Pierce EA, Bennett J. The Status of RPE65 gene therapy trials: safety and efficacy. Cold Spring Harb Perspect Med. 2015;5(9):a017285.
   PubMed Web of Science ®Google Scholar
• Riazuddin SA, Zulfiqar F, Zhang Q, et al. Autosomal recessive retinitis pigmentosa is associated with mutations in RP1 in three consanguineous Pakistani families. Invest Ophthalmol Vis Sci. 2005;46(7):2264–2270.
   PubMed Web of Science ®Google Scholar
• Rivolta C, Sweklo EA, Berson EL, et al. Missense mutation in the USH2A gene: association with recessive retinitis pigmentosa without hearing loss. Am J Hum Genet. 2000;66:1975–1978.
   PubMed Web of Science ®Google Scholar
• Estrada-Cuzcano A, Koenekoop RK, Senechal A, et al. BBS1 mutations in a wide spectrum of phenotypes ranging from nonsyndromic retinitis pigmentosa to Bardet-Biedl syndrome. Arch Ophthalmol. 2012;130(11):1425–1432.
   PubMed Web of Science ®Google Scholar
• Xu M, Yang L, Wang F, et al. Mutations in human IFT140 cause non-syndromic retinal degeneration. Hum Genet. 2015;134(10):1069–1078.
   PubMed Web of Science ®Google Scholar
• Bujakowska KM, Zhang Q, Siemiatkowska AM, et al. Mutations in IFT172 cause isolated retinal degeneration and Bardet-Biedl syndrome. Hum Mol Genet. 2015;24:230–242.
   PubMed Web of Science ®Google Scholar
• Shankar SP, Birch DG, Ruiz RS, et al. Founder effect of a c.828+3A>T splice site mutation in peripherin 2 (PRPH2) causing autosomal dominant retinal dystrophies. JAMA Ophthalmol. 2015;133(5):511–517.
   PubMed Web of Science ®Google Scholar
• Gorin MB, Jackson KE, Ferrell RE, et al. A peripherin/retinal degeneration slow mutation (Pro-210-Arg) associated with macular and peripheral retinal degeneration. Ophthalmology. 1995;102(2):246–255.
   PubMed Web of Science ®Google Scholar
• 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(8):620–626.
   PubMed Web of Science ®Google Scholar
• Gal A, Xu S, Piczenik Y, et al. Gene for autosomal dominant congenital stationary night blindness maps to the same region as the gene for the beta-subunit of the rod photoreceptor cGMP phosphodiesterase (PDEB) in chromosome 4p16.3. Hum Mol Genet. 1994;3:323–325.
   PubMed Web of Science ®Google Scholar
• Sergouniotis PI, Sohn EH, Li Z, et al. Phenotypic variability in RDH5 retinopathy (fundus albipunctatus). Ophthalmology. 2011;118(8):1661–1670.
   PubMed Web of Science ®Google Scholar
• Nakazawa M, Wada Y, Tamai M. Arrestin gene mutations in autosomal recessive retinitis pigmentosa. Arch Ophthalmol. 1998;116(4):498–501.
   PubMedGoogle Scholar
• Eisenberger T, Slim R, Mansour A, et al. Targeted next-generation sequencing identifies a homozygous nonsense mutation in ABHD12, the gene underlying PHARC, in a family clinically diagnosed with Usher syndrome type 3. Orph J Rare Dis. 2012;7:59–71.
   PubMed Web of Science ®Google Scholar
• Nishiguchi KM, Avila-Fernandez A, Van Huet RA, et al. Exome sequencing extends the phenotypic spectrum for ABHD12 mutations: from syndromic to nonsyndromic retinal degeneration. Ophthalmology. 2014;121(8):1620–1627.
   PubMed Web of Science ®Google Scholar
• Tsang SH, Burke T, Oll M, et al. Whole exome sequencing identifies CRB1 defect in an unusual maculopathy phenotype. Ophthalmology. 2014;121(9):1773–1782.
   PubMed Web of Science ®Google Scholar
• Kruk J, Kubasik-Kładna K, Aboul-Einein HY. The role oxidative stress in the pathogenesis of eye diseases: current status and a dual role of physical activity. Mini Rev Med Chem. 2015 Nov 19; 16(3):241–257.
   PubMed Web of Science ®Google Scholar
• Perez VL, Saeed AM, Tan Y, et al. The eye: A window to the soul of the immune system. J Autoimmun. 2013;45:7–14.
   PubMed Web of Science ®Google Scholar
• Suspitsin EN, Sokolenko AP, Lyazina LV, et al. Exome sequencing of a family with Bardet-Biedl syndrome identifies the common Russian mutation c.1967_1968delTAinsC in BBS7. Mol Syndromol. 2015;6(2):96–98.
   PubMedGoogle Scholar
• Khan AO, Bergmann C, Eisenberger T, et al. A TULP1 founder mutation, p.Gln301*, underlies a recognizable congenital rod-cone dystrophy phenotype on the Arabian Peninsula. Br J Ophthalmol. 2015;99(4):488–492.
   PubMed Web of Science ®Google Scholar
• Venturini G, Koskiniemi-Kuendig H, Harper S, et al. Two specific mutations are prevalent causes of recessive retinitis pigmentosa in North American patients of Jewish ancestry. Genet Med. 2015;17(4):285–290.
   PubMed Web of Science ®Google Scholar
• Doucette L, Green J, Black C, et al. Molecular genetics of achromatopsia in Newfoundland reveal genetic heterogeneity, founder effects and the first cases of Jalili syndrome in North America. Ophthalmic Genet. 2013;34(3):119–129.
   PubMed Web of Science ®Google Scholar
• Ebermann I, Koenekoop RK, Lopez I, et al. An USH2A founder mutation is the major cause of Usher syndrome type 2 in Canadians of French origin and confirms common roots of Quebecois and Acadians. Eur J Hum Genet. 2009;17(1):80–84.
   PubMed Web of Science ®Google Scholar
• Auslender N, Bandah D, Rizel L, et al. Four USH2A founder mutations underlie the majority of Usher syndrome type 2 cases among non-Ashkenazi Jews. Genet Test. 2008;12(2):289–294.
   PubMedGoogle Scholar
• Ebermann I, Lopez I, Bitner-Glindzicz M, et al. Deafblindness in French Canadians from Quebec: a predominant founder mutation in the USH1C gene provides the first genetic link with the Acadian population. Genome Biol. 2007;8(4):R47.
   PubMed Web of Science ®Google Scholar
• Ouyang XM, Hejtmancik JF, Jacobson SG, et al. USH1C: a rare cause of USH1 in a non-Acadian population and a founder effect of the Acadian allele. Clin Genet. 2003;63(2):150–153.
   PubMed Web of Science ®Google Scholar
• Zito I, Morris A, Tyson P, et al. Sequence variation within the RPGR gene: evidence for a founder complex allele. Hum Mutat. 2000;16(3):273–274.
   PubMed Web of Science ®Google Scholar
• Gerber S, Rozet JM, Takezawa SI, et al. The photoreceptor cell-specific nuclear receptor gene (PNR) accounts for retinitis pigmentosa in the Crypto-Jews from Portugal (Marranos), survivors from the Spanish Inquisition. Hum Genet. 2000;107:276–284.
   PubMed Web of Science ®Google Scholar
• Tucker BA, Scheetz TE, Mullins RF, et al. Exome sequencing and analysis of induced pluripotent stem cells identify the cilia-related gene male germ cell-associated kinase (MAK) as a cause of retinitis pigmentosa. Proc Natl Acad Sci USA. 2011;108(34):E569–576.
   PubMed Web of Science ®Google Scholar
• Sundin OH, Yang JM, Li Y, et al. Genetic basis of total colourblindness among the Pingelapese islanders. Nat Genet. 2000;25(3):289–293.
   PubMed Web of Science ®Google Scholar
• Sullivan LS, Bowne SJ, Birch DG, et al. Prevalence of disease-causing mutations in families with autosomal dominant retinitis pigmentosa: a screen of known genes in 200 families. Invest Ophthalmol Vis Sci. 2006;47(7):3052–3064.
   PubMed Web of Science ®Google Scholar
• Fernandez-San Jose P, Blanco-Kelly F, Corton M, et al. Prevalence of Rhodopsin mutations in autosomal dominant retinitis pigmentosa in Spain: clinical and analytical review in 200 families. Acta Ophthalmol. 2015;93(1):e38–44.
   PubMed Web of Science ®Google Scholar
• Fahim AT, Daiger SP, Weleber RG. Retinitis pigmentosa overview. GeneReviews. Available from: http://www.ncbi.nlm.nih.gov/books/NBK1417/
   Google Scholar
• Prokisch H, Hartig M, Hellinger R, et al. A population-based epidemiological and genetic study of X-linked retinitis pigmentosa. Invest Ophthalmol Vis Sci. 2007;48(9):4012–4018.
   PubMed Web of Science ®Google Scholar
• Zhao Y, Hosono K, Suto K, et al. The first USH2A mutation analysis of Japanese autosomal recessive retinitis pigmentosa patients: a totally different mutation profile with the lack of frequent mutations found in Caucasian patients. J Hum Genet. 2014;59(9):521–528.
   PubMed Web of Science ®Google Scholar
• Sharon D, Banin E. Nonsyndromic retinitis pigmentosa is highly prevalent in the Jerusalem region with a high frequency of founder mutations. Mol Vis. 2015;21:783–792.
   PubMed Web of Science ®Google Scholar
• 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 USA. 1996;93(24):13726–13730.
   PubMed Web of Science ®Google Scholar
• Zheng QY, Yan D, Ouyang XM, et al. Digenic inheritance of deafness caused by mutations in genes encoding cadherin 23 and protocadherin 15 in mice and humans. Hum Mol Genet. 2005;14(1):103–111.
   PubMed Web of Science ®Google Scholar
• Wang F, Wang H, Tuan HF, et al. Next generation sequencing-based molecular diagnosis of retinitis pigmentosa: identification of a novel genotype-phenotype correlation and clinical refinements. Hum Genet. 2014;133(3):331–345.
   PubMed Web of Science ®Google Scholar
• DeLuca AP, Whitmore SS, Barnes J, et al. Hypomorphic mutations in TRNT1 cause retinitis pigmentosa with erythrocytic microcytosis. Hum Mol Genet. 2016;25(1):44–56.
   PubMedGoogle Scholar
• Glöckle N, Kohl S, Mohr J, et al. Panel-based next generation sequencing as a reliable and efficient technique to detect mutations in unselected patients with retinal dystrophies. Eur J Hum Genet. 2014;22(1):99–104.
   PubMed Web of Science ®Google Scholar
• Weisschuh N, Mayer AK, Strom TM, et al. Mutation detection in patients with retinal dystrophies using targeted next generation sequencing. PLoS One. 2016;11(1):e0145951.
   PubMed Web of Science ®Google Scholar
• Carneiro MO, Russ C, Ross MG, et al. Pacific biosciences sequencing technology for genotyping and variation discovery in human data. BMC Genomics. 2012;13:375.
   PubMed Web of Science ®Google Scholar
• Machini K, Douglas J, Braxton A, et al. Genetic counselors’ views and experiences with the clinical integration of genome sequencing. J Genet Couns. 2014;23(4):496–505.
   PubMed Web of Science ®Google Scholar
• Good BM, Ainscough BJ, McMichael JF, et al. Organizing knowledge to enable personalization of medicine in cancer. Genome Biol. 2014;15:438.
   PubMed Web of Science ®Google Scholar
• Lewis RA Oculocutaneous Albinism Type 1. GeneReviews. Available from: http://www.ncbi.nlm.nih.gov/books/NBK1166/
   Google Scholar
• Chiang PW, Spector E, Tsai ACH. Ocularcutaneous albinism spectrum. Am J Med Genet Part A. 2009;149A:1590–1591.
   PubMed Web of Science ®Google Scholar
• Gonzaga-Jauregui C, Harel T, Gambin T, et al. Exome sequence analysis suggests that genetic burden contributes to phenotypic variability and complex neuropathy. Cell Reports. 2015;12:1169–1183.
   PubMed Web of Science ®Google Scholar
• Henn BM, Botigue LR, Bustamante CD, et al. Estimating the mutation load in human genomes. Nat Rev Genet. 2015;16:333–343.
   PubMed Web of Science ®Google Scholar
• Braun TA, Mullins RF, Wagner AH, et al. Non-exomic and synonymous variants in ABCA4 are an important cause of Stargardt disease. Hum Mol Genet. 2013;22:5136–5145.
   PubMed Web of Science ®Google Scholar
• Zernant J, Xie YA, Ayuso C, et al. Analysis of the ABCA4 genomic locus in Stargardt disease. Hum Mol Genet. 2014;23:6797–6806.
   PubMed Web of Science ®Google Scholar
• Webb TR, Parfitt DA, Gardner JC, et al. Deep intronic mutation in OFD1, identified by targeted genomic next-generation sequencing, causes a severe form of X-linked retinitis pigmentosa (RP23). Hum Mol Genet. 2012;21(16):3647–3654.
   PubMed Web of Science ®Google Scholar
• Small KW, DeLuca AP, Whitmore SS, et al. North Carolina macular dystrophy is caused by dysregulation of the retinal transcription factor PRDM13. Ophthalmol 2015; pii: S0161-6420(15)01153-7. doi:10.1016/j.ophtha.2015.10.006. [Epub ahead of print].
   PubMed Web of Science ®Google Scholar
• Nadeau JH. Modifier genes in mice and humans. Nat Rev Genet. 2001;2(3):165–174.
   PubMed Web of Science ®Google Scholar
• McKay GJ, Clarke S, Davis JA, et al. Pigmented paravenous chorioretinal atrophy is associated with a mutation within the crumbs homolog 1 (CRB1) gene. Invest Ophthalmol Vis Sci. 2005;46:322–328.
   PubMed Web of Science ®Google Scholar
• Strom SP, Gorin MB. Evaluation of autosomal dominant retinal dystrophy genes in an unaffected cohort suggests rare or private missense variants may often be benign. Mol Vis. 2013;19:980–985.
   PubMedGoogle Scholar
• Venturini G, Rose AM, Shah AZ, et al. CNOT3 is a modifier of PRPF31 mutations in retinitis pigmentosa with incomplete penetrance. PLoS Genet. 2012;8(11):e1003040.
   PubMed Web of Science ®Google Scholar
• Bolk S, Pelet A, Hofstra RMW, et al. A human model for multigenic inheritance. Phenotypic expression in Hirschsprung disease requires both the RET gene and a new 9q31 locus. Pnas. 1997;1:268–273.
   Google Scholar
• Green RC, Berg JS, Grody WW, et al. ACMG recommendations for reporting of incidental findings in clinical exome and genome sequencing. Genet in Med. 2013;15:565–574.
   PubMed Web of Science ®Google Scholar