Retinitis pigmentosa genes implicated in the population of America: A systematic review

Olivia Margarita Narváez; Hugo Mendieta Zerón; Orlando Torres; Magally Escobar; Martha Liliana Trujillo Güiza

Olivia Margarita Narváez Facultad de Optometría, Universidad Santo Tomás, Bucaramanga, Colombia https://orcid.org/0000-0001-6203-4669
Hugo Mendieta Zerón Faculty of Medicine, Autonomous University of the State of Mexico
Orlando Torres Facultad de Medicina Veterinaria, Universidad Antonio Nariño, Bogotá, Colombia https://orcid.org/0000-0002-3218-6423
Magally Escobar Facultad de Medicina, Universidad Antonio Nariño, Bogotá, Colombia https://orcid.org/0000-0002-8082-3407
Martha Liliana Trujillo Güiza Facultad de Medicina, Universidad Antonio Nariño, Bogotá, Colombia https://orcid.org/0000-0001-8792-3681

Keywords: Autosomal dominant, Autosomal recessive, Inheritance pattern, Retinitis pigmentosa, X linked

Abstract

Introduction/Aim. To summarize the findings of studies related to genes implicated with retinitis pigmentosa, in autosomal dominant (adRP), autosomal recessive (arRP), and X-linked RP (xlRP) patients in America.

Material and Methods. In this comprehensive search of literature via the Medline / PubMed database, SciELO, Redalyc, ScienceDirect, and Google Scholar (English/Spanish); 75 articles between 2010-2020 were reviewed, the final analysis was done from 21 articles.

Results. The main genes mutations found in America for adRP were RHO (Rhodopsin) and PRPF31 (Pre-MRNA Processing Factor 31); for arRP, USH2A (Usherin 2A) and EYS, (eyes shut homolog; and for xlRP, RPGR (retinitis pigmentosa GTPase regulator) and RP2 (retinitis pigmentosa 2).

Conclusion Most of the genes currently found worldwide to cause RP were present in America, with similarities and differences with other populations in Asia and Europe.

References

1. Orphanet. 2021. The portal for rare diseases and orphan drugs. Retinitis pigmentosa. Retrieved from https://www.orpha.net/consor/cgi-bin/Disease_Search.php?lng=EN&data_id=659
2. Dias MF, Joo K, Kemp JA, et al. Molecular genetics and emerging therapies for retinitis pigmentosa: Basic research and clinical perspectives. Prog Retin Eye Res. 2018;63:107-131. https://doi.org/10.1016/j.preteyeres.2017.10.004.
3. Verbakel SK, van Huet RAC, Boon CJF, et al. Non-syndromic retinitis pigmentosa. Prog Retin Eye Res. 2018;66:157-186. https://doi.org/10.1016/j.preteyeres.2018.03.005.
4. Lunghi C, Galli-Resta L, Binda P, et al. Visual Cortical Plasticity in Retinitis Pigmentosa. Invest Ophthalmol Vis Sci. 2019;60(7):2753-2763. https://doi.org/10.1167/iovs.18-25750.
5. Daiger SP, Bowne SJ, Sullivan LS. Genes and Mutations Causing Autosomal Dominant Retinitis Pigmentosa. Cold Spring Harb Perspect Med. 2014;5(10):a017129. https://doi.org/10.1101/cshperspect.a017129.
6. Trapani I, Puppo A, Auricchio A. Vector platforms for gene therapy of inherited retinopathies. Prog Retin Eye Res. 2014;43:108-28. https://doi.org/10.1016/j.preteyeres.2014.08.001.
7. Delgado-Pelayo SA. Retinosis. Rev Med MD. 2012;3(3):163–166.
8. Motta FL, Martin RP, Filippelli-Silva R, et al. Relative frequency of inherited retinal dystrophies in Brazil. Sci Rep. 2018;8(1):15939. https://doi.org/10.1038/s41598-018-34380-0.
9. Zenteno JC, García-Montaño LA, Cruz-Aguilar M, et al. Extensive genic and allelic heterogeneity underlying inherited retinal dystrophies in Mexican patients molecularly analyzed by next-generation sequencing. Mol Genet Genomic Med. 2020;8(1):10.1002/mgg3.1044. https://doi.org/10.1002/mgg3.1044.
10. Zhang Q, Xu M, Verriotto JD, et al. Next-generation sequencing-based molecular diagnosis of 35 Hispanic retinitis pigmentosa probands. Sci Rep. 2016;6:32792. https://doi.org/10.1038/srep32792.
11. Coussa RG, Chakarova C, Ajlan R, et al. Genotype and Phenotype Studies in Autosomal Dominant Retinitis Pigmentosa (adRP) of the French Canadian Founder Population. Invest Ophthalmol Vis Sci. 2015;56(13):8297-305. https://doi.org/10.1167/iovs.15-17104. Erratum in: Invest Ophthalmol Vis Sci. 2017 Sep 1;58(11):4768.
12. Benaglio P, San Jose PF, Avila-Fernandez A, et al. Mutational screening of splicing factor genes in cases with autosomal dominant retinitis pigmentosa. Mol Vis. 2014;20:843-51.
13. Tamayo Fernández M, Urrego Duque LF. Genética de la Retinitis pigmentosa. 2003, nov. 20. https://www.javeriana.edu.co/documents/5782625/5901279/COLECCION+DERECHO+A+VIVIR+EN+DESVENTAJA+FOLLETO+%23%2014.pdf/7a970e9f-9813-4b0f-ad13-2518c656fd3c
14. Palma MMD, Martin D, Salles MV, et al. Retinal dystrophies and variants in PRPH2. Arq Bras Oftalmol. 2019;82(2):158-160. https://doi.org/10.5935/0004-2749.20190033.
15. Bryant L, Lozynska O, Marsh A, et al. Identification of a novel pathogenic missense mutation in PRPF31 using whole exome sequencing: a case report. Br J Ophthalmol. 2019;103(6):761-767. https://doi.org/10.1136/bjophthalmol-2017-311405.
16. McGuigan DB, Heon E, Cideciyan AV, et al. EYS Mutations Causing Autosomal Recessive Retinitis Pigmentosa: Changes of Retinal Structure and Function with Disease Progression. Genes (Basel). 2017;8(7):178. https://doi.org/10.3390/genes8070178.
17. 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):285-90. https://doi.org/10.1038/gim.2014.132.
18. Guzmán HO, Palacios AM, De Almada MI, Utrera RA. A novel homozygous MYO7A mutation involved in a Venezuelan population with high frequency of USHER1B. Ophthalmic Genet. 2016;37(3):328-30. https://doi.org/10.3109/13816810.2015.1071410.
19. Sullivan LS, Bowne SJ, Koboldt DC, et al. A Novel Dominant Mutation in SAG, the Arrestin-1 Gene, Is a Common Cause of Retinitis Pigmentosa in Hispanic Families in the Southwestern United States. Invest Ophthalmol Vis Sci. 2017;58(5):2774-2784. https://doi.org/10.1167/iovs.16-21341.
20. Santana EE, Fuster-García C, Aller E, et al. Genetic Screening of the Usher Syndrome in Cuba. Front Genet. 2019;10:501. https://doi.org/10.3389/fgene.2019.00501.
21. Mullins RF, Kuehn MH, Radu RA, et al. Autosomal recessive retinitis pigmentosa due to ABCA4 mutations: clinical, pathologic, and molecular characterization. Invest Ophthalmol Vis Sci. 2012;53(4):1883-94. https://doi.org/10.1167/iovs.12-9477.
22. Ladino LY, Galvis J, Yasnó D, Ramírez A, Beltrán OI. Variante patogénica homocigótica del gen BBS10 en un paciente con síndrome de Bardet-Biedl. Biomedica. 2018;38(3):308-20. https://doi.org/10.7705/biomedica.v38i4.4199.
23. López G, Gelvez N, Urrego LF, et al. Análisis Molecular de las Mutaciones 2299delG y C759F en Individuos Colombianos con Retinitis Pigmentosa e Hipoacusia Neurosensorial Molecular. NOVA 2014;12(22):131–141. https://doi.org/10.22490/24629448.1038
24. Seyedahmadi BJ, Rivolta C, Keene JA, et al. Comprehensive screening of the USH2A gene in Usher syndrome type II and non-syndromic recessive retinitis pigmentosa. Exp Eye Res. 2004;79(2):167-73. https://doi.org/10.1016/j.exer.2004.03.005.
25. Esperón-Álvarez A, Rosado-Ruíz-Apodaca I, Santana-Hernández E, et al. Análisis genético molecular de las mutaciones c . 2299delG y c . 2276C > G en el gen USH2A en pacientes Cubanos con síndrome Usher tipo 2. Rev Cubana Genet Comunit. 2017;11(1):14-19.
26. Breuer DK, Yashar BM, Filippova E, 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. https://doi.org/10.1086/340848.
27. Churchill JD, Bowne SJ, Sullivan LS, et al. Mutations in the X-linked retinitis pigmentosa genes RPGR and RP2 found in 8.5% of families with a provisional diagnosis of autosomal dominant retinitis pigmentosa. Invest Ophthalmol Vis Sci. 2013;54(2):1411-6. https://doi.org/10.1167/iovs.12-11541.
28. 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):3647-54. https://doi.org/10.1093/hmg/dds194.
29. Perez-Carro R, Corton M, Sánchez-Navarro I, et al. Panel-based NGS Reveals Novel Pathogenic Mutations in Autosomal Recessive Retinitis Pigmentosa. Sci Rep. 2016;6:19531. https://doi.org/10.1038/srep19531. Erratum in: Sci Rep. 2016 Apr 22;6:24843.
30. Ezquerra-Inchausti M, Barandika O, Anasagasti A, et al. High prevalence of mutations affecting the splicing process in a Spanish cohort with autosomal dominant retinitis pigmentosa. Sci Rep. 2017;7:39652. https://doi.org/10.1038/srep39652.
31. Huang L, Zhang Q, Huang X, et al. Mutation screening in genes known to be responsible for Retinitis Pigmentosa in 98 Small Han Chinese Families. Sci Rep. 2017;7(1):1948. https://doi.org/10.1038/s41598-017-00963-6.
32. Loukovitis Eleftherios D, Stoimeni Anastasia A, Tranos Paris G, Koukoula Stavrenia Ch, Anogeianakis George A, Recent Developments on the major genes involved in retinitis pigmentosa. IP Int J Ocul Oncol Oculoplasty 2020;6(3):157-166. https://doi.org/10.18231/j.ijooo.2020.036.
33. al-Maghtheh M, Inglehearn CF, Keen TJ, et al. Identification of a sixth locus for autosomal dominant retinitis pigmentosa on chromosome 19. Hum Mol Genet. 1994;3(2):351-4. https://doi.org/10.1093/hmg/3.2.351.
34. Gandra M, Anandula V, Authiappan V, et al. Retinitis pigmentosa: mutation analysis of RHO, PRPF31, RP1, and IMPDH1 genes in patients from India. Mol Vis. 2008;14:1105-13.
35. Van Cauwenbergh C, Coppieters F, Roels D, et al. Mutations in Splicing Factor Genes Are a Major Cause of Autosomal Dominant Retinitis Pigmentosa in Belgian Families. PLoS One. 2017;12(1):e0170038. https://doi.org/10.1371/journal.pone.0170038.
36. Beryozkin A, Levy G, Blumenfeld A, et al. Genetic Analysis of the Rhodopsin Gene Identifies a Mosaic Dominant Retinitis Pigmentosa Mutation in a Healthy Individual. Invest Ophthalmol Vis Sci. 2016;57(3):940-7. https://doi.org/10.1167/iovs.15-18702.
37. Martínez-Gimeno M, Gamundi MJ, Hernan I, et al. Mutations in the pre-mRNA splicing-factor genes PRPF3, PRPF8, and PRPF31 in Spanish families with autosomal dominant retinitis pigmentosa. Invest Ophthalmol Vis Sci. 2003;44(5):2171-7. https://doi.org/10.1167/iovs.02-0871.
38. Kim MS, Joo K, Seong MW, et al. Genetic Mutation Profiles in Korean Patients with Inherited Retinal Diseases. J Korean Med Sci. 2019;34(21):e161. doi: 10.3346/jkms.2019.34.e161. Erratum in: J Korean Med Sci. 2019 Sep 09;34(35):e245. https://doi.org/10.3346/jkms.2019.34.e161. Erratum in: J Korean Med Sci. 2019 Sep 09;34(35):e245.
39. Ziviello C, Simonelli F, Testa F, et al. Molecular genetics of autosomal dominant retinitis pigmentosa (ADRP): a comprehensive study of 43 Italian families. J Med Genet. 2005;42(7):e47. https://doi.org/10.1136/jmg.2005.031682.
40. Ali MU, Rahman MSU, Cao J, Yuan PX. Genetic characterization and disease mechanism of retinitis pigmentosa; current scenario. 3 Biotech. 2017;7(4):251. https://doi.org/10.1007/s13205-017-0878-3.
41. Ferrari S, Di Iorio E, Barbaro V, et al. Retinitis pigmentosa: genes and disease mechanisms. Curr Genomics. 2011;12(4):238-49. https://doi.org/10.2174/138920211795860107.
42. Toualbi L, Toms M, Moosajee M. USH2A-retinopathy: From genetics to therapeutics. Exp Eye Res. 2020;201:108330. https://doi.org/10.1016/j.exer.2020.108330.
43. Tracewska AM, Kocyła-Karczmarewicz B, Rafalska A, et al. Genetic Spectrum of ABCA4-Associated Retinal Degeneration in Poland. Genes (Basel). 2019;10(12):959. https://doi.org/10.3390/genes10120959.
44. Sharon D, Banin E. Nonsyndromic retinitis pigmentosa is highly prevalent in the Jerusalem region with a high frequency of founder mutations. Mol Vis. 2015;21:783-92.
45. Fahim AT, Bouzia Z, Branham KH, et al. Detailed clinical characterisation, unique features and natural history of autosomal recessive RDH12-associated retinal degeneration. Br J Ophthalmol. 2019;103(12):1789-1796. https://doi.org/10.1136/bjophthalmol-2018-313580.
46. Numa S, Oishi A, Higasa K, et al. EYS is a major gene involved in retinitis pigmentosa in Japan: genetic landscapes revealed by stepwise genetic screening. Sci Rep. 2020;10(1):20770. https://doi.org/10.1038/s41598-020-77558-1.
47. Bocquet B, Lacroux A, Surget MO, et al. Relative frequencies of inherited retinal dystrophies and optic neuropathies in Southern France: assessment of 21-year data management. Ophthalmic Epidemiol. 2013;20(1):13-25. https://doi.org/10.3109/09286586.2012.737890.
48. Kurata K, Hosono K, Hayashi 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. https://doi.org/10.3390/ijms20061518.
49. Bravo-Gil N, González-Del Pozo M, Martín-Sánchez M, et al. Unravelling the genetic basis of simplex Retinitis Pigmentosa cases. Sci Rep. 2017;7:41937. https://doi.org/10.1038/srep41937.
50. Smith SO. Structure and activation of the visual pigment rhodopsin. Annu Rev Biophys. 2010;39:309-28. https://doi.org/10.1146/annurev-biophys-101209-104901
51. Ali-Nasser T, Zayit-Soudry S, Banin E, et al. Autosomal dominant retinitis pigmentosa with incomplete penetrance due to an intronic mutation of the PRPF31 gene. Mol Vis. 2022;28:359-368.
52. Megaw RD, Soares DC, Wright AF. RPGR: Its role in photoreceptor physiology, human disease, and future therapies. Exp Eye Res. 2015;138:32-41. https://doi.org/10.1016/j.exer.2015.06.007.
53. Patil SB, Hurd TW, Ghosh AK, Murga-Zamalloa CA, Khanna H. Functional analysis of retinitis pigmentosa 2 (RP2) protein reveals variable pathogenic potential of disease-associated missense variants. PLoS One. 2011;6(6):e21379. https://doi.org/doi: 10.1371/journal.pone.0021379..
54. Cai X, Conley SM, Naash MI. RPE65: role in the visual cycle, human retinal disease, and gene therapy. Ophthalmic Genet. 2009;30(2):57-62. https://doi.org/10.1080/13816810802626399.
55. Aleman TS, Uyhazi KE, Serrano LW, et al. RDH12 Mutations Cause a Severe Retinal Degeneration With Relatively Spared Rod Function. Invest Ophthalmol Vis Sci. 2018;59(12):5225-5236. https://doi.org/10.1167/iovs.18-24708.
56. Daich Varela M, Moya R, Schlottmann PG, et al. Ophthalmic genetics in South America. Am J Med Genet C Semin Med Genet. 2020;184(3):753-761. https://doi.org/10.1002/ajmg.c.31832.