Next‐generation genetic testing for retinitis pigmentosa
dc.contributor.author | Sikkema‐raddatz, Birgit | en_US |
dc.contributor.author | Sijmons, Rolf H. | en_US |
dc.date.accessioned | 2012-07-12T17:23:09Z | |
dc.date.available | 2013-08-01T14:04:39Z | en_US |
dc.date.issued | 2012-06 | en_US |
dc.identifier.citation | Sikkema‐raddatz, Birgit ; Sijmons, Rolf H. (2012). "Nextâ generation genetic testing for retinitis pigmentosa ." Human Mutation 33(6): 963-972. <http://hdl.handle.net/2027.42/92029> | en_US |
dc.identifier.issn | 1059-7794 | en_US |
dc.identifier.issn | 1098-1004 | en_US |
dc.identifier.uri | https://hdl.handle.net/2027.42/92029 | |
dc.description.abstract | Molecular diagnostics for patients with retinitis pigmentosa (RP) has been hampered by extreme genetic and clinical heterogeneity, with 52 causative genes known to date. Here, we developed a comprehensive next‐generation sequencing (NGS) approach for the clinical molecular diagnostics of RP. All known inherited retinal disease genes ( n = 111) were captured and simultaneously analyzed using NGS in 100 RP patients without a molecular diagnosis. A systematic data analysis pipeline was developed and validated to prioritize and predict the pathogenicity of all genetic variants identified in each patient, which enabled us to reduce the number of potential pathogenic variants from approximately 1,200 to zero to nine per patient. Subsequent segregation analysis and in silico predictions of pathogenicity resulted in a molecular diagnosis in 36 RP patients, comprising 27 recessive, six dominant, and three X‐linked cases. Intriguingly, De novo mutations were present in at least three out of 28 isolated cases with causative mutations. This study demonstrates the enormous potential and clinical utility of NGS in molecular diagnosis of genetically heterogeneous diseases such as RP. De novo dominant mutations appear to play a significant role in patients with isolated RP, having major implications for genetic counselling. Hum Mutat 33:963–972, 2012. © 2012 Wiley Periodicals, Inc. | en_US |
dc.publisher | Wiley Subscription Services, Inc., A Wiley Company | en_US |
dc.subject.other | Clinical Molecular Diagnostics | en_US |
dc.subject.other | Blindness | en_US |
dc.subject.other | Retinitis Pigmentosa | en_US |
dc.subject.other | DNA Diagnostics | en_US |
dc.subject.other | NGS | en_US |
dc.title | Next‐generation genetic testing for retinitis pigmentosa | en_US |
dc.type | Article | en_US |
dc.rights.robots | IndexNoFollow | en_US |
dc.subject.hlbsecondlevel | Genetics | en_US |
dc.subject.hlbtoplevel | Health Sciences | en_US |
dc.subject.hlbtoplevel | Science | en_US |
dc.description.peerreviewed | Peer Reviewed | en_US |
dc.contributor.affiliationum | Department of Ophthalmology and Visual Sciences, University of Michigan, Ann Arbor, Michigan | en_US |
dc.contributor.affiliationother | Department of Human Genetics, Radboud University Nijmegen Medical Centre, P.O. Box 9101, 6500 HB Nijmegen, The Netherlands. | en_US |
dc.contributor.affiliationother | Augen Zentrum Siegburg, Siegburg, Germany | en_US |
dc.contributor.affiliationother | Rotterdam Eye Hospital, Rotterdam, The Netherlands | en_US |
dc.contributor.affiliationother | Institute for Genetic and Metabolic Disease, Nijmegen, The Netherlands | en_US |
dc.contributor.affiliationother | Nijmegen Centre for Molecular Life Sciences, Nijmegen, The Netherlands | en_US |
dc.contributor.affiliationother | Department of Ophthalmology, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands | en_US |
dc.contributor.affiliationother | Department of Human Genetics, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands | en_US |
dc.description.bitstreamurl | http://deepblue.lib.umich.edu/bitstream/2027.42/92029/1/22045_ftp.pdf | |
dc.description.bitstreamurl | http://deepblue.lib.umich.edu/bitstream/2027.42/92029/2/humu_22045_sm_SuppInfo.pdf | |
dc.identifier.doi | 10.1002/humu.22045 | en_US |
dc.identifier.source | Human Mutation | en_US |
dc.identifier.citedreference | Ng PC, Henikoff S. 2003. SIFT: predicting amino acid changes that affect protein function. Nucleic Acids Res 31: 3812 – 3814. | en_US |
dc.identifier.citedreference | Klevering BJ, Yzer S, Rohrschneider K, Zonneveld M, Allikmets R, van den Born LI, Maugeri A, Hoyng CB, Cremers FPM. 2004. Microarray‐based mutation analysis of the ABCA4 ( ABCR ) gene in autosomal recessive cone–rod dystrophy and retinitis pigmentosa. Eur J Hum Genet 12: 1024 – 1032. | en_US |
dc.identifier.citedreference | Li B, Krishnan VG, Mort ME, Xin F, Kamati KK, Cooper DN, Mooney SD, Radivojac P. 2009. Automated inference of molecular mechanisms of disease from amino acid substitutions. Bioinformatics 25: 2744 – 2750. | en_US |
dc.identifier.citedreference | Littink KW, Pott JWR, Collin RWJ, Kroes HY, Verheij JBGM, Blokland EAW, de Castro Miró M, Hoyng CB, Klaver CCW, Koenekoop RK, Rohrschneider K, Cremers FPM, van den Born LI, den Hollander AI. 2010. A novel nonsense mutation in CEP290 induces exon skipping and leads to a relatively mild retinal phenotype. Invest Ophthalmol Vis Sci 51: 3646 – 3652. | en_US |
dc.identifier.citedreference | Lorenz B, Poliakov E, Schambeck M, Friedburg C, Preising MN, Redmond TM. 2008. A comprehensive clinical and biochemical functional study of a novel RPE65 hypomorphic mutation. Invest Ophthalmol Vis Sci 49: 5235 – 5242. | en_US |
dc.identifier.citedreference | Lupski JR, Reid JG, Gonzaga‐Jauregui C, Rio Deiros D, Chen DCY, Nazareth L, Bainbridge M, Dinh H, Jing C, Wheeler DA, McGuire AL, Zhang F, Stankiewicz P, Halperin JJ, Yang C, Gehman C, Guo D, Irikat RK, Tom W, Fantin NJ, Muzny DM, Gibbs RA. 2010. Whole‐genome sequencing in a patient with Charcot–Marie–Tooth neuropathy. N Engl J Med 362: 1181 – 1191. | en_US |
dc.identifier.citedreference | Maguire AM, Simonelli F, Pierce EA, Pugh EN Jr, Mingozzi F, Bennicelli J, Banfi S, Marshall KA, Testa F, Surace EM, Rossi S, Lyubarsky A, Arruda VR, Konkle B, Stone E, Sun J, Jacobs J, Dell'Osso L, Hertle R, Ma JX, Redmond TM, Zhu X, Hauck B, Zelenaia O, Shindler KS, Maguire MG, Wright JF, Volpe NJ, McDonnell JW, Auricchio A, High KA, Bennett J. 2008. Safety and efficacy of gene transfer for Leber's congenital amaurosis. N Engl J Med 358: 2240 – 2248. | en_US |
dc.identifier.citedreference | Marmor MF, Fulton AB, Holder GE, Miyake Y, Brigell M, Bach M. 2009. ISCEV Standard for full‐field clinical electroretinography (2008 update). Doc Ophthalmol 118: 69 – 77. | en_US |
dc.identifier.citedreference | Maugeri A, Klevering BJ, Rohrschneider K, Blankenagel A, Brunner HG, Deutman AF, Hoyng CB, Cremers FPM. 2000. Mutations in the ABCA4 (ABCR) gene are the major cause of autosomal recessive cone–rod dystrophy. Am J Hum Genet 67: 960 – 966. | en_US |
dc.identifier.citedreference | McHenry CL, Liu Y, Feng W, Nair AR, Feathers KL, Ding X, Gal A, Vollrath D, Sieving PA, Thompson DA. 2004. MERTK arginine‐844‐cysteine in a patient with severe rod–cone dystrophy: loss of mutant protein function in transfected cells. Invest Ophthalmol Vis Sci 45: 1456 – 1463. | en_US |
dc.identifier.citedreference | Miller SA, Dykes DD, Polesky HF. 1988. A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res 16: 1215. | en_US |
dc.identifier.citedreference | Mokry M, Feitsma H, Nijman IJ, de Bruijn E, van der Zaag PJ, Guryev V, Cuppen E. 2010. Accurate SNP and mutation detection by targeted custom microarray‐based genomic enrichment of short‐fragment sequencing libraries. Nucleic Acids Res 38: e116. | en_US |
dc.identifier.citedreference | Muradov KG, Artemyev NO. 2000. Loss of the effector function in a transducin‐alpha mutant associated with Nougaret night blindness. J Biol Chem 275: 6969 – 6974. | en_US |
dc.identifier.citedreference | Najera C, Millan JM, Beneyto M, Prieto F. 1995. Epidemiology of retinitis pigmentosa in the Valencian community (Spain). Genet Epidemiol 12: 37 – 46. | en_US |
dc.identifier.citedreference | Ng SB, Buckingham KJ, Lee C, Bigham AW, Tabor HK, Dent KM, Huff CD, Shannon PT, Jabs EW, Nickerson DA, Shendure J, Bamshad MJ. 2010. Exome sequencing identifies the cause of a mendelian disorder. Nat Genet 42: 30 – 35. | en_US |
dc.identifier.citedreference | Nishiguchi KM, Friedman JS, Sandberg MA, Swaroop A, Berson EL, Dryja TP. 2004. Recessive NRL mutations in patients with clumped pigmentary retinal degeneration and relative preservation of blue cone function. Proc Natl Acad Sci USA 101: 17819 – 17824. | en_US |
dc.identifier.citedreference | Otto EA, Ramaswami G, Janssen S, Chaki M, Allen SJ, Zhou W, Airik R, Hurd TW, Ghosh AK, Wolf MT, Hoppe B, Neuhaus TJ, Bockenhauer D, Milford DV, Soliman NA, Antignac C, Saunier S, Johnson CA, Hildebrandt F; GPN Study Group. 2011. Mutation analysis of 18 nephronophthisis associated ciliopathy disease genes using a DNA pooling and next generation sequencing strategy. J Med Genet 48: 105 – 116. | en_US |
dc.identifier.citedreference | Pollard KS, Hubisz MJ, Rosenbloom KR, Siepel A. 2010. Detection of nonneutral substitution rates on mammalian phylogenies. Genome Res 20: 110 – 121. | en_US |
dc.identifier.citedreference | Roepman R, Letteboer SJF, Arts HH, van Beersum SEC, Lu X, Krieger E, Ferreira PA, Cremers FPM. 2005. Interaction of nephrocystin‐4 and RPGRIP1 is disrupted by nephronophthisis or Leber congenital amaurosis‐associated mutations. Proc Natl Acad Sci USA 102: 18520 – 18525. | en_US |
dc.identifier.citedreference | Shearer AE, DeLuca AP, Hildebrand MS, Taylor KR, Gurrola J II, Scherer S, Scheetz TE, Smith RJH. 2010. Comprehensive genetic testing for hereditary hearing loss using massively parallel sequencing. Proc Natl Acad Sci USA 107: 21104 – 21109. | en_US |
dc.identifier.citedreference | Simpson DA, Clark GR, Alexander S, Silvestri G, Willoughby CE. 2011. Molecular diagnosis for heterogeneous genetic diseases with targeted high‐throughput DNA sequencing applied to retinitis pigmentosa. J Med Genet 48: 145 – 151. | en_US |
dc.identifier.citedreference | Sun H, Smallwood PM, Nathans J. 2000. Biochemical defects in ABCR protein variants associated with human retinopathies. Nat Genet 26: 242 – 246. | en_US |
dc.identifier.citedreference | Thompson DA, Janecke AR, Lange J, Feathers KL, Hübner CA, McHenry CL, Stockton DW, Rammesmayer G, Lupski JR, Antinolo G, Ayuso C, Baiget M, Gouras P, Heckenlively JR, den Hollander A, Jacobson SG, Lewis RA, Sieving PA, Wissinger B, Yzer S, Zrenner E, Utermann G, Gal A. 2005. Retinal degeneration associated with RDH12 mutations results from decreased 11‐cis retinal synthesis due to disruption of the visual cycle. Hum Mol Genet 14: 3865 – 3875. | en_US |
dc.identifier.citedreference | Vadlamudi L, Dibbens LM, Lawrence KM, Iona X, McMahon JM, Murrell W, Mackay‐Sim A, Scheffer IE, Berkovic SF. 2010. Timing of de novo mutagenesis—a twin study of sodium‐channel mutations. N Engl J Med 363: 1335 – 1340. | en_US |
dc.identifier.citedreference | van den Born LI, Bergen AA, Bleeker‐Wagemakers EM. 1992. A retrospective study of registered retinitis pigmentosa patients in The Netherlands. Ophthalmic Paediatr Genet 13: 227 – 236. | en_US |
dc.identifier.citedreference | Vissers LELM, de Ligt J, Gilissen C, Janssen I, Steehouwer M, de Vries P, van Lier B, Arts P, Wieskamp N, del Rosario M, van Bon BWM, Hoischen A, de Vries BBA, Brunner HG, Veltman JA. 2010. A de novo paradigm for mental retardation. Nat Genet 42: 1109 – 1112. | en_US |
dc.identifier.citedreference | Wilkie SE, Newbold RJ, Deery E, Walker CE, Stinton I, Ramamurthy V, Hurley JB, Bhattacharya SS, Warren MJ, Hunt DM. 2000. Functional characterization of missense mutations at codon 838 in retinal guanylate cyclase correlates with disease severity in patients with autosomal dominant cone–rod dystrophy. Hum Mol Genet 9: 3065 – 3073. | en_US |
dc.identifier.citedreference | Worthey EA, Mayer AN, Syverson GD, Helbling D, Bonacci BB, Decker B, Serpe JM, Dasu T, Tschannen MR, Veith RL, Basehore MJ, Broeckel U, Tomita‐Mitchell A, Arca MJ, Casper JT, Margolis DA, Bick DP, Hessner MJ, Routes JM, Verbsky JW, Jacob HJ, Dimmock DP. 2011. Making a definitive diagnosis: successful clinical application of whole exome sequencing in a child with intractable inflammatory bowel disease. Genet Med 13: 255 – 262. | en_US |
dc.identifier.citedreference | Yzer S, van den Born LI, Schuil J, Kroes HY, van Genderen MM, Boonstra FN, van den Helm B, Brunner HG, Koenekoop RK, Cremers FPM. 2003. A Tyr368His RPE65 founder mutation is associated with variable expression and progression of early onset retinal dystrophy in 10 families of a genetically isolated population. J Med Genet 40: 709 – 713. | en_US |
dc.identifier.citedreference | Adzhubei IA, Schmidt S, Peshkin L, Ramensky VE, Gerasimova A, Bork P, Kondrashov AS, Sunyaev SR. 2010. A method and server for predicting damaging missense mutations. Nat Methods 7: 248 – 249. | en_US |
dc.identifier.citedreference | Ávila‐Fernández A, Cantalapiedra D, Aller E, Vallespín E, Aguirre‐Lambán J, Blanco‐Kelly F, Corton M, Riveiro‐Álvarez R, Allikmets R, Trujillo‐Tiebas MJ, Millán JM, Cremers FPM, Ayuso C. 2010. Mutation analysis of 272 Spanish families affected by autosomal recessive retinitis pigmentosa using a genotyping microarray. Mol Vis 16: 2550 – 2558. | en_US |
dc.identifier.citedreference | Bainbridge JWB, Smith AJ, Barker SS, Robbie S, Henderson R, Balaggan K, Viswanathan A, Holder GE, Stockman A, Tyler N, Petersen‐Jones S, Bhattacharya SS, Thrasher AJ, Fitzke FW, Carter BJ, Rubin GS, Moore AT, Ali RR. 2008. Effect of gene therapy on visual function in Leber's congenital amaurosis. N Engl J Med 358: 2231 – 2239. | en_US |
dc.identifier.citedreference | Bandah‐Rozenfeld D, Collin RWJ, Banin E, van den Born LI, Coene KLM, Siemiatkowska AM, Zelinger L, Khan MI, Lefeber DJ, Erdinest I, Testa F, Simonelli F, Voesenek K, Blokland EAW, Strom TM, Klaver CCW, Qamar R, Banfi S, Cremers FPM, Sharon D, den Hollander AI. 2010. Mutations in IMPG2, encoding interphotoreceptor matrix proteoglycan 2, cause autosomal‐recessive retinitis pigmentosa. Am J Hum Genet 87: 199 – 208. | en_US |
dc.identifier.citedreference | Bell J, Bodmer D, Sistermans E, Ramsden SC. 2007. Practice guidelines for the interpretation and reporting of unclassified variants (UVs) in clinical molecular genetics. Clin Mol Genet Soc. | en_US |
dc.identifier.citedreference | Berger W, Kloeckener‐Gruissem B, Neidhardt J. 2010. The molecular basis of human retinal and vitreoretinal diseases. Prog Retin Eye Res 29: 335 – 375. | en_US |
dc.identifier.citedreference | Boon CJF, van Schooneveld MJ, den Hollander AI, van Lith‐Verhoeven JJC, Zonneveld‐Vrieling MN, Theelen T, Cremers FPM, Hoyng CB, Klevering BJ. 2007. Mutations in the peripherin/RDS gene are an important cause of multifocal pattern dystrophy simulating STGD1/fundus flavimaculatus. Br J Ophthalmol 91: 1504 – 1511. | en_US |
dc.identifier.citedreference | Bowne SJ, Sullivan LS, Koboldt DC, Ding L, Fulton R, Abbott RM, Sodergren EJ, Birch DG, Wheaton DH, Heckenlively JR, Liu Q, Pierce EA, Weinstock GM, Daiger SP. 2011. Identification of disease‐causing mutations in autosomal dominant retinitis pigmentosa (adRP) using next‐generation DNA sequencing. Invest Ophthalmol Vis Sci 52: 494 – 503. | en_US |
dc.identifier.citedreference | Chen S, Wang QL, Xu S, Liu I, Li LY, Wang Y, Zack DJ. 2002. Functional analysis of cone‐rod homeobox (CRX) mutations associated with retinal dystrophy. Hum Mol Genet 11: 873 – 884. | en_US |
dc.identifier.citedreference | Choi M, Scholl UI, Ji W, Liu T, Tikhonova IR, Zumbo P, Nayir A, Bakkaloğlu A, Ozen S, Sanjad S, Nelson‐Williams C, Farhi A, Mane S, Lifton RP. 2009. Genetic diagnosis by whole exome capture and massively parallel DNA sequencing. Proc Natl Acad Sci USA 106: 19096 – 19101. | en_US |
dc.identifier.citedreference | Collin RWJ, Littink KW, Klevering BJ, van den Born LI, Koenekoop RK, Zonneveld MN, Blokland EAW, Strom TM, Hoyng CB, den Hollander AI, Cremers FPM. 2008. Identification of a 2 Mb human ortholog of Drosophila eyes shut/spacemaker that is mutated in patients with retinitis pigmentosa. Am J Hum Genet 83: 594 – 603. | en_US |
dc.identifier.citedreference | Collin RWJ, Safieh C, Littink KW, Shalev SA, Garzozi HJ, Rizel L, Abbasi AH, Cremers FPM, den Hollander AI, Klevering BJ, Ben‐Yosef T. 2010. Mutations in C2ORF71 cause autosomal‐recessive retinitis pigmentosa. Am J Hum Genet 86: 783 – 788. | en_US |
dc.identifier.citedreference | Collin RWJ, van den Born LI, Klevering BJ, de Castro‐Miró M, Littink KW, Arimadyo K, Azam M, Yazar V, Zonneveld MN, Paun CC, Siemiatkowska AM, Strom TM, Hehir‐Kwa JY, Kroes HY, de Faber JTHN, van Schooneveld MJ, Heckenlively JR, Hoyng CB, den Hollander AI, Cremers FPM. 2011. High‐resolution homozygosity mapping is a powerful tool to detect novel mutations causative for autosomal recessive RP in the Dutch population. Invest Ophthalmol Vis Sci 52: 2227 – 2239. | en_US |
dc.identifier.citedreference | Cremers FPM, van de Pol DJR, van Driel M, den Hollander AI, van Haren FJJ, Knoers NVAM, Tijmes N, Bergen AAB, Rohrschneider K, Blankenagel A, Pinckers AJLG, Deutman AF, Hoyng CB. 1998. Autosomal recessive retinitis pigmentosa and cone–rod dystrophy caused by splice site mutations in the Stargardt's disease gene ABCR. Hum Mol Genet 7: 355 – 362. | en_US |
dc.identifier.citedreference | Daiger SP, Sullivan LS, Gire AI, Birch DG, Heckenlively JR, Bowne SJ. 2008. Mutations in known genes account for 58% of autosomal dominant retinitis pigmentosa (adRP). Adv Exp Med Biol 613: 203 – 209. | en_US |
dc.identifier.citedreference | den Hollander AI, Black A, Bennett J, Cremers FPM. 2010. Lighting a candle in the dark: advances in genetics and gene therapy of recessive retinal dystrophies. J Clin Invest 120: 3042 – 3053. | en_US |
dc.identifier.citedreference | den Hollander AI, Heckenlively JR, van den Born LI, de Kok YJM, van der Velde‐Visser SD, Kellner U, Jurklies B, van Schooneveld MJ, Blankenagel A, Rohrschneider K, Wissinger B, Cruysberg JRM, Deutman AF, Brunner HG, Apfelstedt‐Sylla E, Hoyng CB, Cremers FPM. 2001. 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 69: 198 – 203. | en_US |
dc.identifier.citedreference | den Hollander AI, ten Brink JB, de Kok YJM, van Soest S, van den Born LI, van Driel MA, van de Pol DJR, Payne AM, Bhattacharya SS, Kellner U, Hoyng CB, Westerveld A, Brunner HG, Bleeker‐Wagemakers EM, Deutman AF, Heckenlively JR, Cremers FPM, Bergen AAB. 1999. Mutations in a human homologue of Drosophila crumbs cause retinitis pigmentosa (RP12). Nat Genet 23: 217 – 221. | en_US |
dc.identifier.citedreference | Dryja TP, Finn JT, Peng YW, McGee TL, Berson EL, Yau KW. 1995. Mutations in the gene encoding the alpha subunit of the rod cGMP‐gated channel in autosomal recessive retinitis pigmentosa. Proc Natl Acad Sci USA 92: 10177 – 10181. | en_US |
dc.identifier.citedreference | Hamdan FF, Gauthier J, Spiegelman D, Noreau A, Yang Y, Pellerin S, Dobrzeniecka S, Côté M, Perreau‐Linck E, Carmant L, D'Anjou G, Fombonne E, Addington AM, Rapoport JL, Delisi LE, Krebs MO, Mouaffak F, Joober R, Mottron L, Drapeau P, Marineau C, Lafrenière RG, Lacaille JC, Rouleau GA, Michaud JL; Synapse to Disease Group. 2009. Mutations in SYNGAP1 in autosomal nonsyndromic mental retardation. N Engl J Med 360: 599 – 605. | en_US |
dc.identifier.citedreference | Hartong DT, Berson EL, Dryja TP. 2006. Retinitis pigmentosa. Lancet 368: 1795 – 1809. | en_US |
dc.identifier.citedreference | Hayakawa M, Fujiki K, Kanai A, Matsumura M, Honda Y, Sakaue H, Tamai M, Sakuma T, Tokoro T, Yura T, Kubota N, Kawano S, Matsui M, Yuzawa M, Oguchi Y, Akeo K, Adachi E, Kimura T, Miyake Y, Horiguchi M, Wakabayashi K, Ishizaka N, Koizumi K, Uyama M, Ohba N. 1997. Multicenter genetic study of retinitis pigmentosa in Japan: I. Genetic heterogeneity in typical retinitis pigmentosa. Jpn J Ophthalmol 41: 1 – 6. | en_US |
dc.identifier.citedreference | Hauswirth WW, Aleman TS, Kaushal S, Cideciyan AV, Schwartz SB, Wang L, Conlon TJ, Boye SL, Flotte TR, Byrne BJ, Jacobson SG. 2008. 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 19: 979 – 990. | en_US |
dc.identifier.citedreference | He X, Lobsiger J, Stocker A. 2009. Bothnia dystrophy is caused by domino‐like rearrangements in cellular retinaldehyde‐binding protein mutant R234W. Proc Natl Acad Sci USA 106: 18545 – 18550. | en_US |
dc.identifier.citedreference | Hoischen A, van Bon BWM, Gilissen C, Arts P, van Lier B, Steehouwer M, de Vries P, de Reuver R, Wieskamp N, Mortier G, Devriendt K, Amorim MZ, Revencu N, Kidd A, Barbosa M, Turner A, Smith J, Oley C, Henderson A, Hayes IM, Thompson EM, Brunner HG, de Vries BBA, Veltman JA. 2010. De novo mutations of SETBP1 cause Schinzel–Giedion syndrome. Nat Genet 42: 483 – 485. | en_US |
dc.identifier.citedreference | Illing ME, Rajan RS, Bence NF, Kopito RR. 2002. A rhodopsin mutant linked to autosomal dominant retinitis pigmentosa is prone to aggregate and interacts with the ubiquitin proteasome system. J Biol Chem 277: 34150 – 34160. | en_US |
dc.identifier.citedreference | Jones MA, Bhide S, Chin E, Ng BG, Rhodenizer D, Zhang VW, Sun JJ, Tanner A, Freeze HH, Hegde MR. 2011. Targeted polymerase chain reaction‐based enrichment and next generation sequencing for diagnostic testing of congenital disorders of glycosylation. Genet Med 13: 921 – 932. | en_US |
dc.owningcollname | Interdisciplinary and Peer-Reviewed |
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