261
Views
2
CrossRef citations to date
0
Altmetric
Case Report

Clinical characteristics of high myopia in female carriers of pathogenic RPGR mutations: a case series and review of the literature

ORCID Icon, , , , , , & show all
Pages 295-303 | Received 16 Feb 2022, Accepted 01 Aug 2022, Published online: 26 Aug 2022

References

  • Hartong DT, Berson EL, Dryja TP. Retinitis pigmentosa. Lancet. 2006;368(9549):1795–809. doi:10.1016/S0140-6736(06)69740-7.
  • Daiger SP, Sullivan LS, Bowne SJ. Genes and mutations causing retinitis pigmentosa. Clin Genet. 2013;84(2):132–41. doi:10.1111/cge.12203.
  • RetNet - Retinal Information Network. [Accessed 2022 February 14]. https://sph.uth.edu/retnet/
  • Nájera C, Millán JM, Beneyto M, Prieto F. Epidemiology of retinitis pigmentosa in the Valencian community (Spain). Genet Epidemiol. 1995;12(1):37–46. doi:10.1002/gepi.1370120105.
  • Greenberg J, Bartmann L, Ramesar R, Beighton P. Retinitis pigmentosa in Southern Africa. Clin Genet. 1993;44(5):232–35. doi:10.1111/j.1399-0004.1993.tb03888.x.
  • Berson EL, Rosner B, Simonoff E. Risk factors for genetic typing and detection in retinitis pigmentosa. Am J Ophthalmol. 1980;89(6):763–75. doi:10.1016/0002-9394(80)90163-4.
  • Sieving PA, Fishman GA. Refractive errors of retinitis pigmentosa patients. Br J Ophthalmol. 1978;62(3):163–67.
  • Sanchez Tocino H, Diez Montero C, Villanueva Gómez A, Lobo Valentin R, Montero-Moreno JA. Phenotypic high myopia in X-linked retinitis pigmentosa secondary to a novel mutation in the RPGR gene. Ophthalmic Genet. 2019;40(2):170–76. doi:10.1080/13816810.2019.1605385.
  • Talib M, van Schooneveld MJ, Van Cauwenbergh C, Wijnholds J, ten Brink JB, Florijn RJ, Schalij-Delfos NE, Dagnelie G, van Genderen MM, De Baere E, et al. The spectrum of structural and functional abnormalities in Female carriers of pathogenic variants in the RPGR gene. Investigative Ophthalmology & Visual Science. 2018;59(10):4123–33. doi:10.1167/iovs.17-23453.
  • Breuer DK, Yashar BM, Filippova E, Hiriyanna S, Lyons RH, Mears AJ, Asaye B, Acar C, Vervoort R, Wright AF, et al. A comprehensive mutation analysis of RP2 and RPGR in a North American cohort of families with X-linked retinitis pigmentosa. Am J Hum Genet. 2002;70(6):1545–54. doi:10.1086/340848.
  • Bader I, Brandau O, Achatz H, Apfelstedt-Sylla E, Hergersberg M, Lorenz B, Wissinger B, Wittwer B, Rudolph G, Meindl A, et al. X-Linked retinitis pigmentosa: RPGR mutations in most families with definite X linkage and clustering of mutations in a short sequence stretch of exon ORF15. Invest Ophthalmol Vis Sci. 2003;44(4):1458–63. doi:10.1167/iovs.02-0605.
  • Megaw RD, Soares DC, Wright AF. RPGR: Its role in photoreceptor physiology, human disease, and future therapies. Exp Eye Res. 2015;138:32–41. doi:10.1016/j.exer.2015.06.007.
  • Wright AF, Shu X. Focus on molecules: RPGR. Exp Eye Res. 2007;85(1):1–2. doi:10.1016/j.exer.2006.03.006.
  • Hong D-H, Pawlyk B, Sokolov M, Strissel KJ, Yang J, Tulloch B, Wright AF, Arshavsky VY, Li T. RPGR isoforms in photoreceptor connecting cilia and the transitional zone of motile cilia. Invest Ophthalmol Vis Sci. 2003;44(6):2413–21. doi:10.1167/iovs.02-1206.
  • Khanna H. More than meets the eye: current understanding of RPGR function. In: Ash J, Anderson R, LaVail M, Bowes Rickman C, Hollyfield J, Grimm C, editors. Retinal degenerative diseases. Advances in Experimental Medicine and Biology. Springer International Publishing; 2018. p. 521–38. doi:10.1007/978-3-319-75402-4_64.
  • Vervoort R, Wright AF. Mutations of RPGR in X-linked retinitis pigmentosa (RP3). Hum Mutat. 2002;19(5):486–500. doi:10.1002/humu.10057.
  • Migeon BR. X-Linked diseases: susceptible females. Genet Med. 2020;22(7):1156–74. doi:10.1038/s41436-020-0779-4.
  • Parmeggiani F, Barbaro V, De Nadai K, Lavezzo E, Toppo S, Chizzolini M, Palù G, Parolin C, Di Iorio E. Identification of novel X-linked gain-of-function RPGR-ORF15 mutation in Italian family with retinitis pigmentosa and pathologic myopia. Sci Rep. 2016;6(1):39179. doi:10.1038/srep39179.
  • Yokoyama A, Maruiwa F, Hayakawa M, Kanai A, Vervoort R, Wright AF, Yamada K, Niikawa N, Naōi N. Three novel mutations of the RPGR gene exon ORF15 in three Japanese families with X-linked retinitis pigmentosa. Am J Med Genet. 2001;104(3):232–38.
  • Cehajic-Kapetanovic J, Xue K, Martinez-Fernandez de la Camara C, Nanda A, Davies A, Wood LJ, Salvetti AP, Fischer MD, Aylward JW, Barnard AR, et al. Initial results from a first-in-human gene therapy trial on X-linked retinitis pigmentosa caused by mutations in RPGR. Nat Med. 2020;26(3):354–59. doi:10.1038/s41591-020-0763-1.
  • Prosseda PP, Tran M, Kowal T, Wang B, Sun Y. Advances in ophthalmic optogenetics: approaches and applications. Biomolecules. 2022;12(2):269. doi:10.3390/biom12020269.
  • Martinez-Fernandez De La Camara C, Nanda A, Salvetti AP, Fischer MD, MacLaren RE. Gene therapy for the treatment of X-linked retinitis pigmentosa. Expert Opin Orphan Drugs. 2018;6(3):167–77. doi:10.1080/21678707.2018.1444476.
  • Yang J, Yan R, Roy A, Xu D, Poisson J, Zhang Y. The I-TASSER suite: protein structure and function prediction. Nat Methods. 2015;12(1):7–8. doi:10.1038/nmeth.3213.
  • Stenson PD, Mort M, Ball EV, Shaw K, Phillips A, Cooper DN. The human gene mutation database: building a comprehensive mutation repository for clinical and molecular genetics, diagnostic testing and personalized genomic medicine. Hum Genet. 2014;133(1):1–9. doi:10.1007/s00439-013-1358-4.
  • Sandberg MA, Rosner B, Weigel-DiFranco C, Dryja TP, Berson EL. Disease course of patients with X-linked retinitis pigmentosa due to RPGR gene mutations. Invest Ophthalmol Vis Sci. 2007;48(3):1298–304. doi:10.1167/iovs.06-0971.
  • Comander J, Weigel-DiFranco C, Sandberg MA, Berson EL. Visual function in carriers of X-linked retinitis pigmentosa. Ophthalmology. 2015;122(9):1899–906. doi:10.1016/j.ophtha.2015.05.039.
  • Talib M, van Schooneveld MJ, Thiadens AA, Fiocco M, Wijnholds J, Florijn RJ, Schalij-Delfos NE, van Genderen MM, Putter H, Cremers Frans PM, et al. Clinical and genetic characteristics of male patients with RPGR-associated retinal dystrophies: a long-term follow-up study. Retina. 2019;39(6):1186–99. doi:10.1097/IAE.0000000000002125.
  • Vervoort R, Lennon A, Bird AC, Tulloch B, Axton R, Miano MG, Meindl A, Meitinger T, Ciccodicola A, Wright AF. Mutational hot spot within a new RPGR exon in X-linked retinitis pigmentosa. Nat Genet. 2000;25(4):462–66. doi:10.1038/78182.
  • Jin Z-B, Liu X-Q, Hayakawa M, Murakami A, Nao-I N Mutational analysis of RPGR and RP2 genes in Japanese patients with retinitis pigmentosa: identification of four mutations. Mol Vis. 2006;12:1167–74.
  • Fahim AT, Bowne SJ, Sullivan LS, Webb KD, Williams JT, Wheaton DK, Birch DG, Daiger SP, Janecke AR. Allelic heterogeneity and genetic modifier loci contribute to clinical variation in males with X-linked retinitis pigmentosa due to RPGR mutations. PLoS One. 2011;6(8):e23021. doi:10.1371/journal.pone.0023021.
  • Hong D-H, Pawlyk BS, Adamian M, Li T. Dominant, gain-of-function mutant produced by truncation of RPGR. Invest Ophthalmol Vis Sci. 2004;45(1):36–41. doi:10.1167/iovs.03-0787.
  • Sullivan LS, Bowne SJ, Birch DG, Hughbanks-Wheaton D, Heckenlively JR, Lewis RA, Garcia CA, Ruiz RS, Blanton SH, Northrup H, 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):3052–64. doi:10.1167/iovs.05-1443.
  • Rao KN, Anand M, Khanna H. The carboxyl terminal mutational hotspot of the ciliary disease protein RPGRORF15 (retinitis pigmentosa GTPase regulator) is glutamylated in vivo. Biol Open. 2016;5(4):424–28. doi:10.1242/bio.016816.
  • Sharon D, Bruns GA, McGee TL, Sandberg MA, Berson EL, Dryja TP. X-Linked retinitis pigmentosa: mutation spectrum of the RPGR and RP2 genes and correlation with visual function. Invest Ophthalmol Vis Sci. 2000;41(9):2712–21.
  • Zhao K, Wang L, Wang L, Wang L, Zhang Q, Wang Q. Novel deletion of the RPGR gene in a Chinese family with X-linked retinitis pigmentosa. Ophthalmic Genet. 2001;22(3):187–94. doi:10.1076/opge.22.3.187.2221.
  • Banin E, Mizrahi-Meissonnier L, Neis R, Silverstein S, Magyar I, Abeliovich D, Roepman R, Berger W, Rosenberg T, Sharon D. A non-ancestral RPGR missense mutation in families with either recessive or semi-dominant X-linked retinitis pigmentosa. Am J Med Genet a. 2007;143A(11):1150–58. doi:10.1002/ajmg.a.31642.
  • Roepman R, van Duijnhoven G, Rosenberg T, Pinckers AJ, Bleeker-Wagemakers LM, Bergen AA, Post J, Beck A, Reinhardt R, Ropers HH, et al. Positional cloning of the gene for X-linked retinitis pigmentosa 3: homology with the guanine-nucleotide-exchange factor RCC1. Hum Mol Genet. 1996;5(7):1035–41. doi:10.1093/hmg/5.7.1035.
  • Rao KN, Zhang W, Li L, Anand M, Khanna H. Prenylated retinal ciliopathy protein RPGR interacts with PDE6δ and regulates ciliary localization of Joubert syndrome-associated protein INPP5E. Hum Mol Genet. 2016;25(20):4533–45. doi:10.1093/hmg/ddw281.
  • Sangermano R, Deitch I, Peter VG, Ba-Abbad R, Place EM, Zampaglione E, Wagner NE, Fulton AB, Coutinho-Santos L, Rosin B, et al. Broadening INPP5E phenotypic spectrum: detection of rare variants in syndromic and non-syndromic IRD. Npj Genom Med. 2021;6(1):1–10. doi:10.1038/s41525-021-00214-8.
  • Walia S, Fishman GA, Swaroop A, Branham KEH, Lindeman M, Othman M, Weleber RG. Discordant phenotypes in fraternal twins having an identical mutation in exon ORF15 of the RPGR gene. Arch Ophthalmol. 2008;126(3):379–84. doi:10.1001/archophthalmol.2007.72.
  • Koenekoop RK, Loyer M, Hand CK, Al Mahdi H, Dembinska O, Beneish R, Racine J, Rouleau GA. Novel RPGR mutations with distinct retinitis pigmentosa phenotypes in French-Canadian families. Am J Ophthalmol. 2003;136(4):678–87. doi:10.1016/s0002-9394(03)00331-3.
  • Kurata K, Hosono K, Hayashi T, Mizobuchi K, Katagiri S, Miyamichi D, Nishina S, Sato M, Azuma N, Nakano T, et al. X-linked retinitis pigmentosa in Japan: clinical and genetic findings in male patients and female carriers. Int J Mol Sci. 2019;20(6):1518. doi:10.3390/ijms20061518.
  • Nishiguchi KM, Tearle RG, Liu YP, Oh EC, Miyake N, Benaglio P, Harper S, Koskiniemi-Kuendig H, Venturini G, Sharon D, et al. Whole genome sequencing in patients with retinitis pigmentosa reveals pathogenic DNA structural changes and NEK2 as a new disease gene. Proc Natl Acad Sci U S a. 2013;110(40):16139–44. doi:10.1073/pnas.1308243110.
  • Birtel J, Gliem M, Mangold E, Müller PL, Holz FG, Neuhaus C, Lenzner S, Zahnleiter D, Betz C, Eisenberger T, et al. Next-generation sequencing identifies unexpected genotype-phenotype correlations in patients with retinitis pigmentosa. PLoS One. 2018;13(12):e0207958. doi:10.1371/journal.pone.0207958.
  • Fahim AT, Sullivan LS, Bowne SJ, Jones KD, Wheaton DKH, Khan NW, Heckenlively JR, Jayasundera KT, Branham KH, Andrews CA, et al. X-Chromosome inactivation is a biomarker of clinical severity in female carriers of RPGR-associated X-linked retinitis pigmentosa. Ophthalmol Retina. 2020;4(5):510–20. doi:10.1016/j.oret.2019.11.010.
  • Moreno-Leon L, West EL, O’Hara-Wright M, Li L, Nair R, He J, Anand M, Sahu B, Chavali VRM, Smith AJ, et al. RPGR isoform imbalance causes ciliary defects due to exon ORF15 mutations in X-linked retinitis pigmentosa (XLRP). Hum Mol Genet. 2021;29(22):3706–16. doi:10.1093/hmg/ddaa269.
  • Hsia Y, Ho T-C. Posterior staphyloma of extreme pathologic myopia. JAMA Ophthalmol. 2020;138(5):e191663. doi:10.1001/jamaophthalmol.2019.1663.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.