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Case Report

Is RPGR-related retinal dystrophy associated with systemic disease? A case series

ORCID Icon, ORCID Icon, , , , & show all
Pages 577-584 | Received 09 Sep 2022, Accepted 23 Dec 2022, Published online: 05 Jan 2023

References

  • Shu X, Fry AM, Tulloch B, Manson FDC, Crabb JW, Khanna H, Faragher AJ, Lennon A, He S, Trojan P, et al. RPGR ORF15 isoform co-localizes with RPGRIP1 at centrioles and basal bodies and interacts with nucleophosmin. Hum Mol Genet [Internet]. 2005 May 1;14(9):1183–97. doi:10.1093/hmg/ddi129.
  • Patnaik SR, Raghupathy RK, Zhang X, Mansfield D, Shu X. The role of RPGR and its interacting proteins in ciliopathies. Yu HG, editor. J Ophthalmol [Internet]. 2015;2015:414781. doi:10.1155/2015/414781.
  • Hong DH, Pawlyk BS, Shang J, Sandberg MA, Berson EL, Li T. A retinitis pigmentosa GTPase regulator (RPGR)-deficient mouse model for X-linked retinitis pigmentosa (RP3). Proc Natl Acad Sci USA. 2000 Mar;97(7):3649–54. doi:10.1073/pnas.97.7.3649.
  • 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 Aug;25(4):462–66. doi:10.1038/78182.
  • Murga-Zamalloa CA, Atkins SJ, Peranen J, Swaroop A, Khanna H. Interaction of retinitis pigmentosa GTPase regulator (RPGR) with RAB8A GTPase: implications for cilia dysfunction and photoreceptor degeneration. Hum Mol Genet. 2010 Sep;19(18):3591–98. doi:10.1093/hmg/ddq275.
  • Vössing C, Atigbire P, Eilers J, Markus F, Stieger K, Song F, Neidhardt J. The major ciliary isoforms of rpgr build different interaction complexes with inpp5e and rpgrip1l. Int J Mol Sci. 2021;22(7):1–17. doi:10.3390/ijms22073583.
  • Gerner M, Haribaskar R, Pütz M, Czerwitzki J, Walz G, Schäfer T. The retinitis pigmentosa GTPase regulator interacting protein 1 (RPGRIP1) links RPGR to the nephronophthisis protein network. Kidney Int [Internet]. 2010;77(10):891–96. https://www.sciencedirect.com/science/article/pii/S0085253815541434.
  • Mavlyutov TA, Zhao H, Ferreira PA. Species-specific subcellular localization of RPGR and RPGRIP isoforms: implications for the phenotypic variability of congenital retinopathies among species. Hum Mol Genet [Internet]. 2002 Aug 1;11(16):1899–907. doi:10.1093/hmg/11.16.1899.
  • Hong DH, 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 [Internet]. 2003 Jun 1;44(6):2413–21. doi:10.1167/iovs.02-1206.
  • Patil SB, Verma R, Venkatareddy M, Khanna H. Expression and localization of the ciliary disease protein retinitis pigmentosa GTPase regulator in mammalian kidney. Kidney Int [Internet]. 2010;78(6):622–23. https://www.sciencedirect.com/science/article/pii/S0085253815545985.
  • Meindl A, Dry K, Herrmann K, Manson F, Ciccodicola A, Edgar A, Carvalho MRS, Achatz H, Hellebrand H, Lennon A, et al. A gene (RPGR) with homology to the RCC1 guanine nucleotide exchange factor is mutated in X–linked retinitis pigmentosa (RP3). Nat Genet. 1996 May;13(1):35–42. doi:10.1038/ng0596-35.
  • Talib M, van Schooneveld MJ, Thiadens AA, Fiocco M, Wijnholds J, Florijn RJ, Schalij-Delfos NE, van Genderen MM, Putter H, Cremers FPM, et al. Clinical and genetic characteristics of male patients with RPGR-associated retinal dystrophies: a long-term follow-up study. Retina [Internet]. 2019;39(6):1186–99. https://journals.lww.com/retinajournal/Fulltext/2019/06000/CLINICAL_AND_GENETIC_CHARACTERISTICS_OF_MALE.21.aspx.
  • Cehajic Kapetanovic J, Barnard AR, MacLaren RE. Molecular therapies for choroideremia. Genes (Basel). 2019;10(10):738. doi:10.3390/genes10100738.
  • Ardura-Garcia C, Goutaki M, Carr SB, Crowley S, Halbeisen FS, Nielsen KG, Pennekamp P, Raidt J, Thouvenin G, Yiallouros PK, et al. Registries and collaborative studies for primary ciliary dyskinesia in Europe. ERJ Open Res. 2020 Apr;6(2):00005–2020. doi:10.1183/23120541.00005-2020.
  • Legendre M, Zaragosi LE, Mitchison HM. Motile cilia and airway disease. Semin Cell Dev Biol. 2021 Feb;110:19–33. doi:10.1016/j.semcdb.2020.11.007.
  • Brennan SK, Ferkol TW, Davis SD. Emerging genotype-phenotype relationships in primary ciliary dyskinesia. Int J Mol Sci. 2021;22(15):8272. doi:10.3390/ijms22158272.
  • Shoemark A, Boon M, Brochhausen C, Bukowy-Bieryllo Z, de Santi MM, Goggin P, Griffin P, Hegele RG, Hirst RA, Leigh MW, et al. International consensus guideline for reporting transmission electron microscopy results in the diagnosis of primary ciliary dyskinesia (BEAT PCD TEM Criteria). Eur Respir J [Internet]. 2020 Apr 1;55(4):1900725. http://erj.ersjournals.com/content/55/4/1900725.abstract.
  • van Dorp DB, Wright AF, Carothers AD, Bleeker-Wagemakers EM. A family with RP3 type of X-linked retinitis pigmentosa: an association with ciliary abnormalities. Hum Genet. 1992 Jan;88(3):331–34. doi:10.1007/BF00197269.
  • Zito I, Downes SM, Patel RJ, Cheetham ME, Ebenezer ND, Jenkins SA, Bhattacharya SS, Webster AR, Holder GE, Bird AC, et al. RPGR mutation associated with retinitis pigmentosa, impaired hearing, and sinorespiratory infections. J Med Genet. 2003;40:609–15.
  • Moore A, Escudier E, Roger G, Tamalet A, Pelosse B, Marlin S, Clément A, Geremek M, Delaisi B, Bridoux AM, et al. RPGR is mutated in patients with a complex X linked phenotype combining primary ciliary dyskinesia and retinitis pigmentosa. J Med Genet. 2006;43(4):326–33. doi:10.1136/jmg.2005.034868.
  • Bukowy-Bieryłło Z, Ziętkiewicz E, Loges NT, Wittmer M, Geremek M, Olbrich H, Fliegauf M, Voelkel K, Rutkiewicz E, Rutland J, et al. RPGR mutations might cause reduced orientation of respiratory cilia. Pediatr Pulmonol [Internet]. 2013 Apr 1;48(4):352–63. doi:10.1002/ppul.22632.
  • Sengillo JD, Fridman G, Cho YG, Buchovecky C, Tsang SH. Novel mutation in retinitis pigmentosa GTPase regulator gene causes primary ciliary dyskinesia and retinitis pigmentosa. Ophthalmic Surg Lasers Imaging Retina [Internet]. 2018 Jul 1;49(7):548–52. doi:10.3928/23258160-20180628-14.
  • Iannaccone A, Breuer DK, Wang XF, Kuo SF, Normando EM, Filippova E, Baldi A, Hiriyanna S, MacDonald CB, Baldi F, et al. Clinical and immunohistochemical evidence for an X linked retinitis pigmentosa syndrome with recurrent infections and hearing loss in association with an RPGR mutation. J Med Genet. 2003;40:e118.
  • 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 Oct;136(4):678–87. doi:10.1016/S0002-9394(03)00331-3.
  • Marmoy OR, Moinuddin M, Thompson DA. An alternative electroretinography protocol for children: a study of diagnostic agreement and accuracy relative to ISCEV standard electroretinograms. Acta Ophthalmol [Internet]. 2022;100(3):322–30. https://onlinelibrary.wiley.com/doi/abs/10.1111/aos.14938
  • Robson AG, Frishman LJ, Grigg J, Hamilton R, Jeffrey BG, Kondo M, Li S, McCulloch DL. ISCEV standard for full-field clinical electroretinography (2022 update). Doc Ophthalmol. 2022 Jun;144(3):165–77. doi:10.1007/s10633-022-09872-0.
  • Odom JV, Bach M, Brigell M, Holder GE, McCulloch DL, Mizota A, Tormene AP. ISCEV standard for clinical visual evoked potentials: (2016 update). Doc Ophthalmol. 2016 Aug;133(1):1–9. doi:10.1007/s10633-016-9553-y.
  • Sharon D, Ben-Yosef T, Goldenberg-Cohen N, Pras E, Gradstein L, Soudry S, Mezer E, Zur D, Abbasi AH, Zeitz C, et al. A nationwide genetic analysis of inherited retinal diseases in Israel as assessed by the Israeli inherited retinal disease consortium (IIRDC). Hum Mutat. 2020;41(1):140–49. doi:10.1002/humu.23903.
  • Turro E, Astle WJ, Megy K, Gräf S, Greene D, Shamardina O, Allen HL, Sanchis-Juan A, Frontini M, Thys C, et al. Whole-genome sequencing of patients with rare diseases in a national health system. Nature. 2020;583(7814):96–102. doi:10.1038/s41586-020-2434-2.
  • Carss K, Arno G, Erwood M, Stephens J, Sanchis-Juan A, Hull S, Megy K, Grozeva D, Dewhurst E, Malka S, et al. Comprehensive rare variant analysis via whole-genome sequencing to determine the molecular pathology of inherited retinal disease. Am J Hum Genet. 2017;100(1):75–90. doi:10.1016/j.ajhg.2016.12.003.
  • Van’s Gravesande KS, Omran H. Primary ciliary dyskinesia: clinical presentation, diagnosis and genetics. Ann Med. 2005;37(6):439–49. doi:10.1080/07853890510011985.
  • Zhang Q, Giacalone JC, Searby C, Stone EM, Tucker BA, Sheffield VC. Disruption of RPGR protein interaction network is the common feature of RPGR missense variations that cause XLRP. Proc Natl Acad Sci USA. 2019;116(4):1353–60. doi:10.1073/pnas.1817639116.
  • Hong DH, Pawlyk BS, Adamian M, Sandberg MA, Li T. A single, abbreviated RPGR-ORF15 variant reconstitutes RPGR function in vivo. Invest Ophthalmol Vis Sci. 2005;46(2):435–41. doi:10.1167/iovs.04-1065.
  • Wright RN, Hong DH, Perkins B. Misexpression of the constitutive Rpgr(ex1-19) variant leads to severe photoreceptor degeneration. Invest Ophthalmol Vis Sci. 2011 Jul;52(8):5189–201. doi:10.1167/iovs.11-7470.
  • Brunner S, Colman D, Travis AJ, Luhmann UFO, Shi W, Feil S, Imsand C, Nelson J, Grimm C, Rülicke T, et al. Overexpression of RPGR leads to male infertility in mice due to defects in flagellar assembly. Biol Reprod. 2008;79(4):608–17. doi:10.1095/biolreprod.107.067454.
  • Shu X, Black GC, Rice JM, Hart-Holden N, Jones A, O’Grady A, Ramsden S, Wright AF. RPGR mutation analysis and disease: an update. Hum Mutat. 2007;28(4):322–28. doi:10.1002/humu.20461.
  • Kuehni CE, Lucas JS. Diagnosis of primary ciliary dyskinesia: summary of the ERS task force report. Breathe (Sheff). 2017 Sep;13(3):166–78. doi:10.1183/20734735.008517.
  • 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. 2020;29(22):3706–16. doi:10.1093/hmg/ddaa269.
  • Horani A, Ferkol TW. Primary ciliary dyskinesia and associated sensory ciliopathies. Expert Rev Respir Med [Internet]. 2016 Mar 28;10(5):569–76. https://pubmed.ncbi.nlm.nih.gov/26967669.
  • Driscoll JA, Bhalla S, Liapis H, Ibricevic A, Brody SL. Autosomal dominant polycystic kidney disease is associated with an increased prevalence of radiographic bronchiectasis. Chest. 2008 May;133(5):1181–88. doi:10.1378/chest.07-2147.
  • Budny B, Chen W, Omran H, Fliegauf M, Tzschach A, Wisniewska M, Jensen LR, Raynaud M, Shoichet SA, Badura M, et al. A novel X-linked recessive mental retardation syndrome comprising macrocephaly and ciliary dysfunction is allelic to oral–facial–digital type I syndrome. Hum Genet. 2006 Sep;120(2):171–78. doi:10.1007/s00439-006-0210-5.
  • Khan AO. A stargardt disease-like phenotype in GAS8-related primary ciliary dyskinesia. Ophthalmic Genet [Internet]. 2022;43(5):713–15. doi:10.1080/13816810.2022.2090012.
  • Waters AM, Beales PL. Ciliopathies: an expanding disease spectrum. Pediatr Nephrol [Internet]. 2011 Jul 01;26(7):1039–56. https://pubmed.ncbi.nlm.nih.gov/21210154.
  • Hunter DG, Fishman GA, Kretzer FL. Abnormal axonemes in X-linked retinitis pigmentosa. Arch Ophthalmol [Internet]. 1988 Mar 1;106(3):362–68. doi:10.1001/archopht.1988.01060130388028.
  • Arden GB, Fox B. Increased incidence of abnormal nasal cilia in patients with retinitis pigmentosa [17]. Nature. 1979;279(5713):534–36. doi:10.1038/279534a0.
  • Murga-Zamalloa CA, Swaroop A, Khanna H. RPGR-containing protein complexes in syndromic and non-syndromic retinal degeneration due to ciliary dysfunction. J Genet [Internet]. 2009 Dec;88(4):399–407. https://pubmed.ncbi.nlm.nih.gov/20090203.
  • Shapiro AJ, Leigh MW. Value of transmission electron microscopy for primary ciliary dyskinesia diagnosis in the era of molecular medicine: genetic defects with normal and non-diagnostic ciliary ultrastructure. Ultrastruct Pathol. 2017;41(6):373–85. doi:10.1080/01913123.2017.1362088.
  • Mysore N, Koenekoop J, Li S, Ren H, Keser V, Lopez-Solache I, Koenekoop RK. A review of secondary photoreceptor degenerations in systemic disease. Cold Spring Harb Perspect Med. 2014 Dec;5(11):a025825. doi:10.1101/cshperspect.a025825.
  • Adams NA, Awadein A, Toma HS. The Retinal Ciliopathies. Ophthalmic Genet [Internet]. 2007 Jan 1;28(3):113–25. doi:10.1080/13816810701537424.
  • Escudier E, Duquesnoy P, Papon JF, Amselem S. Ciliary defects and genetics of primary ciliary dyskinesia. Paediatr Respir Rev. 2009 Jun;10(2):51–54. doi:10.1016/j.prrv.2009.02.001.
  • 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 Mar;126(3):379–84. doi:10.1001/archophthalmol.2007.72.
  • 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 Mar;26(3):354–59. doi:10.1038/s41591-020-0763-1.
  • NCT03116113 [Internet]. NCT Clinical Trials; [accessed 2022 Apr 26]. https://clinicaltrials.gov/ct2/show/NCT03116113.
  • NCT03316560 [Internet]. NCT Clinical Trials; [accessed 2022 Apr 26]. https://clinicaltrials.gov/ct2/show/NCT03316560.
  • NCT03252847 [Internet]. NCT Clinical Trials; [accessed 2022 Apr 26]. https://clinicaltrials.gov/ct2/show/NCT03252847.
  • Fischer MD, McClements ME, Martinez-Fernandez de la Camara C, Bellingrath JS, Dauletbekov D, Ramsden SC, Hickey DG, Barnard AR, MacLaren RE. Codon-optimized RPGR improves stability and efficacy of AAV8 gene therapy in two mouse models of X-linked retinitis pigmentosa. Mol Ther [Internet]. 2017;25(8):1854–65. https://www.sciencedirect.com/science/article/pii/S152500161730223X.

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