Identification of mutations causing inherited retinal degenerations in the Israeli and Palestinian populations using homozygosity mapping

Investigative Ophthalmology and Visual Science

Volumn 55, Issue 2, 2014, Pages 1149-1160

  Beryozkin, Avigail ^a   Zelinger, Lina ^a   Bandah Rozenfeld, Dikla ^a   Shevach, Elia ^a   Harel, Anat ^a   Storm, Tim ^b   Sagi, Michal ^a   Eli, Dalia ^a   Merin, Saul ^c   Banin, Eyal ^a   Sharon, Dror ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b INSTITUTE OF EPIDEMIOLOGY   (Germany)

^c St John Eye Hospital   (Israel)

Author keywords

Homozygosity mapping; Retinal degeneration; Retinitis pigmentosa

Indexed keywords

AMINO ACID; CELL NUCLEUS RECEPTOR; HETASTARCH; RETINAL DEHYDROGENASE;

ADOLESCENT; ADULT; ARAB; ARTICLE; AUTOFLUORESCENCE IMAGING; AUTOSOMAL RECESSIVE DISORDER; CEP 290 GENE; CHILD; CLINICAL ARTICLE; ELECTROOCULOGRAPHY; ELECTRORETINOGRAPHY; EYS GENE; GENE; GENE MAPPING; GENE MUTATION; HOMOZYGOSITY; HUMAN; INFANT; ISRAEL; LCA 5 GENE; LEBER CONGENITAL AMAUROSIS; MFRP GENE; MIDDLE AGED; MISSENSE MUTATION; MUTATIONAL ANALYSIS; NR 2 E3 GENE; OPHTHALMOSCOPY; OPTICAL COHERENCE TOMOGRAPHY; PATHOGENICITY; PEDIGREE ANALYSIS; PHENOTYPE; POLYMERASE CHAIN REACTION; PRESCHOOL CHILD; PRIORITY JOURNAL; PROM 1 GENE; RDH 12 GENE; RETINA DEGENERATION; RETINA FLUORESCEIN ANGIOGRAPHY; RETINITIS PIGMENTOSA; SCHOOL CHILD; SINGLE NUCLEOTIDE POLYMORPHISM; TULP 1 GENE; VISUAL ACUITY; YOUNG ADULT;

HOMOZYGOSITY MAPPING; RETINAL DEGENERATION; RETINITIS PIGMENTOSA;

ARABS; CHROMOSOME MAPPING; CONSANGUINITY; DNA MUTATIONAL ANALYSIS; ELECTRORETINOGRAPHY; EYE PROTEINS; FEMALE; GENETIC LINKAGE; GENETIC PREDISPOSITION TO DISEASE; HOMOZYGOTE; HUMANS; ISRAEL; JEWS; MALE; MUTATION; PEDIGREE; POLYMORPHISM, SINGLE NUCLEOTIDE; RETINAL DEGENERATION; RETINITIS PIGMENTOSA;

EID: 84894465581     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.13-13625     Document Type: Article

References (68)

1. Lander ES, Botstein D. Homozygosity mapping: a way to map human recessive traits with the DNA of inbred children. Science. 1987;236:1567-1570.
2. Woods CG, Valente EM, Bond J, Roberts E. A new method for autozygosity mapping using single nucleotide polymorphisms (SNPs) and EXCLUDEAR. J Med Genet. 2004;41:e101.
3. Littink KW, den Hollander AI, Cremers FP, Collin RW. The power of homozygosity mapping: discovery of new genetic defects in patients with retinal dystrophy. Adv Exp Med Biol. 2012;723:345-351.
4. den Hollander AI, Lopez I, Yzer S, et al. Identification of novel mutations in patients with Leber congenital amaurosis and juvenile RP by genome-wide homozygosity mapping with SNP microarrays. Invest Ophthalmol Vis Sci. 2007;48:5690-5698.
5. Bittles AH. Commentary: the background and outcomes of the first-cousin marriage controversy in Great Britain. Int J Epidemiol. 2009;38:1453-1458.
6. Chacon-Camacho OF, Jitskii S, Buentello-Volante B, et al. Exome sequencing identifies RDH12 compound heterozygous mutations in a family with severe retinitis pigmentosa. Gene. 2013;528:178-182.
7. Miano MG, Jacobson SG, Carothers A, et al. Pitfalls in homozygosity mapping. Am J Hum Genet. 2000;67:1348-1351.
8. Benayoun L, Spiegel R, Auslender N, et al. Genetic heterogeneity in two consanguineous families segregating early onset retinal degeneration: the pitfalls of homozygosity mapping. Am J Med Genet A. 2009;149A:650-656.
9. Zlotogora J. The molecular basis of autosomal recessive diseases among the Arabs and Druze in Israel. Hum Genet. 2010;128:473-479.
10. Vardi-Saliternik R, Friedlander Y, Cohen T. Consanguinity in a population sample of Israeli Muslim Arabs, Christian Arabs and Druze. Ann Hum Biol. 2002;29:422-431.
11. Cohen T, Vardi-Saliternik R, Friedlander Y. Consanguinity, intracommunity and intercommunity marriages in a population sample of Israeli Jews. Ann Hum Biol. 2004;31:38-48.
12. Zelinger L, Banin E, Obolensky A, et al. A missense mutation in DHDDS, encoding dehydrodolichyl diphosphate synthase, is associated with autosomal-recessive retinitis pigmentosa in Ashkenazi Jews. Am J Hum Genet. 2011;88:207-215.
13. Cohen B, Chervinsky E, Jabaly-Habib H, et al. A novel splice site mutation of CDHR1 in a consanguineous Israeli Christian Arab family segregating autosomal recessive cone-rod dystrophy. Mol Vis. 2012;18:2915-2921.
14. Dvir L, Srour G, Abu-Ras R, et al. Autosomal-recessive earlyonset retinitis pigmentosa caused by a mutation in PDE6G, the gene encoding the gamma subunit of rod cGMP phosphodiesterase. Am J Hum Genet. 2010;87:258-264.
15. Auslender N, Sharon D, Abbasi AH, et al. A common founder mutation of CERKL underlies autosomal recessive retinal degeneration with early macular involvement among Yemenite Jews. Invest Ophthalmol Vis Sci. 2007;48:5431-5438.
16. Bandah-Rozenfeld D, Mizrahi-Meissonnier L, Farhy C, et al. Homozygosity mapping reveals null mutations in FAM161A as a cause of autosomal-recessive retinitis pigmentosa. Am J Hum Genet. 2010;87:382-391.
17. Berson EL. Retinitis pigmentosa. The Friedenwald Lecture. Invest Ophthalmol Vis Sci. 1993;34:1659-1676.
18. Jacobson SG, Knighton RW, Levene RM. Dark-and lightadapted visual evoked cortical potentials in retinitis pigmentosa. Doc Ophthalmol. 1985;60:189-196.
19. Hartong DT, Berson EL, Dryja TP. Retinitis pigmentosa. Lancet. 2006;368:1795-1809.
20. Fazzi E, Signorini SG, Uggetti C, et al. Towards improved clinical characterization of Leber congenital amaurosis: neurological and systemic findings. Am J Med Genet A. 2005; 132A:13-19.
21. Szlyk JP, Fishman GA, Alexander KR, et al. Clinical subtypes of cone-rod dystrophy. Arch Ophthalmol. 1993;111:781-788.
22. Collin RW, van den Born LI, Klevering BJ, et al. High-resolution homozygosity mapping is a powerful tool to detect novel mutations causative of autosomal recessive RP in the Dutch population. Invest Ophthalmol Vis Sci. 2011;52:2227-2239.
23. Siemiatkowska AM, Arimadyo K, Moruz LM, et al. Molecular genetic analysis of retinitis pigmentosa in Indonesia using genome-wide homozygosity mapping. Mol Vis. 2011;17:3013-3024.
24. Beit-Ya'acov A, Mizrahi-Meissonnier L, Obolensky A, et al. Homozygosity for a novel ABCA4 founder splicing mutation is associated with progressive and severe Stargardt-like disease. Invest Ophthalmol Vis Sci. 2007;48:4308-4314.
25. Mackay DS. Dev Borman A, Moradi P, et al. RDH12 retinopathy: novel mutations and phenotypic description. Mol Vis. 2011;17:2706-2716.
26. Parker RO, Crouch RK. Retinol dehydrogenases (RDHs) in the visual cycle. Exp Eye Res. 2010;91:788-792.
27. Schuster A, Janecke AR, Wilke R, et al. The phenotype of earlyonset retinal degeneration in persons with RDH12 mutations. Invest Ophthalmol Vis Sci. 2007;48:1824-1831.
28. Janecke AR, Thompson DA, Utermann G, et al. Mutations in RDH12 encoding a photoreceptor cell retinol dehydrogenase cause childhood-onset severe retinal dystrophy. Nat Genet. 2004;36:850-854.
29. Perrault I, Hanein S, Gerber S, et al. Retinal dehydrogenase 12 (RDH12) mutations in leber congenital amaurosis. Am J Hum Genet. 2004;75:639-646.
30. Sun W, Gerth C, Maeda A, et al. Novel RDH12 mutations associated with Leber congenital amaurosis and cone-rod dystrophy: biochemical and clinical evaluations. Vision Res. 2007;47:2055-2066.
31. Xi Q, Pauer GJ, Ball SL, et al. Interaction between the photoreceptor-specific tubby-like protein 1 and the neuronalspecific GTPase dynamin-1. Invest Ophthalmol Vis Sci. 2007; 48:2837-2844.
32. Xi Q, Pauer GJ, Marmorstein AD, et al. Tubby-like protein 1 (TULP1) interacts with F-actin in photoreceptor cells. Invest Ophthalmol Vis Sci. 2005;46:4754-4761.
33. Hagstrom SA, North MA, Nishina PL, et al. Recessive mutations in the gene encoding the tubby-like protein TULP1 in patients with retinitis pigmentosa. Nat Genet. 1998;18:174-176.
34. Mataftsi A, Schorderet DF, Chachoua L, et al. Novel TULP1 mutation causing leber congenital amaurosis or early onset retinal degeneration. Invest Ophthalmol Vis Sci. 2007;48: 5160-5167.
35. Permanyer J, Navarro R, Friedman J, et al. Autosomal recessive retinitis pigmentosa with early macular affectation caused by premature truncation in PROM1. Invest Ophthalmol Vis Sci. 2010;51:2656-2663.
36. Zhang Q, Zulfiqar F, Xiao X, et al. Severe retinitis pigmentosa mapped to 4p15 and associated with a novel mutation in the PROM1 gene. Hum Genet. 2007;122:293-299.
37. Pras E, Abu A, Rotenstreich Y, et al. Cone-rod dystrophy and a frameshift mutation in the PROM1 gene. Mol Vis. 2009;15: 1709-1716.
38. Mandal MN, Vasireddy V, Jablonski MM, et al. Spatial and temporal expression of MFRP and its interaction with CTRP5. Invest Ophthalmol Vis Sci. 2006;47:5514-5521.
39. Won J, Smith RS, Peachey NS, et al. Membrane frizzled-related protein is necessary for the normal development and maintenance of photoreceptor outer segments. Vis Neurosci. 2008;25:563-574.
40. Ayala-Ramirez R, Graue-Wiechers F, Robredo V, et al. A new autosomal recessive syndrome consisting of posterior microphthalmos, retinitis pigmentosa, foveoschisis, and optic disc drusen is caused by a MFRP gene mutation. Mol Vis. 2006; 12:1483-1489.
41. Crespi J, Buil JA, Bassaganyas F, et al. A novel mutation confirms MFRP as the gene causing the syndrome of nanophthalmos-renititis pigmentosa-foveoschisis-optic disk drusen. Am J Ophthalmol. 2008;146:323-328.
42. van Wijk E, Kersten FF, Kartono A, et al. Usher syndrome and Leber congenital amaurosis are molecularly linked via a novel isoform of the centrosomal ninein-like protein. Hum Mol Genet. 2009;18:51-64.
43. Gerber S, Hanein S, Perrault I, et al. Mutations in LCA5 are an uncommon cause of Leber congenital amaurosis (LCA) type II. Hum Mutat. 2007;28:1245.
44. Abd El-Aziz MM, Barragan I, O'Driscoll CA, et al. EYS, encoding an ortholog of Drosophila spacemaker, is mutated in autosomal recessive retinitis pigmentosa. Nat Genet. 2008; 40:1285-1287.
45. Zelhof AC, Hardy RW, Becker A, Zuker CS. Transforming the architecture of compound eyes. Nature. 2006;443:696-699.
46. Husain N, Pellikka M, Hong H, et al. The agrin/perlecan-related protein eyes shut is essential for epithelial lumen formation in the Drosophila retina. Dev Cell. 2006;11:483-493.
47. Bandah-Rozenfeld D, Littink KW, Ben-Yosef T, et al. Novel null mutations in the EYS gene are a frequent cause of autosomal recessive retinitis pigmentosa in the Israeli population. Invest Ophthalmol Vis Sci. 2010;51:4387-4394.
48. Collin RW, Littink KW, Klevering BJ, et al. Identification of a 2 Mb human ortholog of Drosophila eyes shut/spacemaker that is mutated in patients with retinitis pigmentosa. Am J Hum Genet. 2008;83:594-603.
49. Valente EM, Silhavy JL, Brancati F, et al. Mutations in CEP290, which encodes a centrosomal protein, cause pleiotropic forms of Joubert syndrome. Nat Genet. 2006;38:623-625.
50. Kim J, Krishnaswami SR, Gleeson JG. CEP290 interacts with the centriolar satellite component PCM-1 and is required for Rab8 localization to the primary cilium. Hum Mol Genet. 2008;17:3796-3805.
51. Stowe TR, Wilkinson CJ, Iqbal A, Stearns T. The centriolar satellite proteins Cep72 and Cep290 interact and are required for recruitment of BBS proteins to the cilium. Mol Biol Cell. 2012;23:3322-3335.
52. Travaglini L, Brancati F, Attie-Bitach T, et al. Expanding CEP290 mutational spectrum in ciliopathies. Am J Med Genet A. 2009; 149A:2173-2180.
53. Coppieters F, Lefever S, Leroy BP, De Baere E. CEP290, a gene with many faces: mutation overview and presentation of CEP290base. Hum Mutat. 2010;31:1097-1108.
54. Papon JF, Perrault I, Coste A, et al. Abnormal respiratory cilia in non-syndromic Leber congenital amaurosis with CEP290 mutations. J Med Genet. 2010;47:829-834.
55. Kobayashi M, Hara K, Yu RT, Yasuda K. Expression and functional analysis of Nr2e3, a photoreceptor-specific nuclear receptor, suggest common mechanisms in retinal development between avians and mammals. Dev Genes Evol. 2008; 218:439-444.
56. Park SP, Hong IH, Tsang SH, et al. Disruption of the human cone photoreceptor mosaic from a defect in NR2E3 transcription factor function in young adults. Graefes Arch Clin Exp Ophthalmol. 2013;251:2299-2309.
57. Schorderet DF, Escher P. NR2E3 mutations in enhanced S-cone sensitivity syndrome (ESCS), Goldmann-Favre syndrome (GFS), clumped pigmentary retinal degeneration (CPRD), and retinitis pigmentosa (RP). Hum Mutat. 2009;30:1475-1485.
58. Sharon D, Sandberg MA, Caruso RC, et al. Shared mutations in NR2E3 in enhanced S-cone syndrome, Goldmann-Favre syndrome, and many cases of clumped pigmentary retinal degeneration. Arch Ophthalmol. 2003;121:1316-1323.
59. Milam AH, Rose L, Cideciyan AV, et al. The nuclear receptor NR2E3 plays a role in human retinal photoreceptor differentiation and degeneration. Proc Natl Acad Sci U S A. 2002;99: 473-478.
60. Woods CG, Cox J, Springell K, et al. Quantification of homozygosity in consanguineous individuals with autosomal recessive disease. Am J Hum Genet. 2006;78:889-896.
61. Gibson J, Morton NE, Collins A. Extended tracts of homozygosity in outbred human populations. Hum Mol Genet. 2006; 15(5);789-95.
62. McQuillan R, Leutenegger AL, Abdel-Rahman R, et al. Runs of homozygosity in European populations. Am J Hum Genet. 2008;83:359-372.
63. Thiadens AA, den Hollander AI, Roosing S, et al. Homozygosity mapping reveals PDE6C mutations in patients with early-onset cone photoreceptor disorders. Am J Hum Genet. 2009;85: 240-247.
64. den Hollander AI, Davis J, van der Velde-Visser SD, et al. CRB1 mutation spectrum in inherited retinal dystrophies. Hum Mutat. 2004;24:355-369.
65. Davidson AE, Schwarz N, Zelinger L, et al. Mutations in ARL2BP, encoding ADP-ribosylation-factor-like 2 binding protein, cause autosomal-recessive retinitis pigmentosa. Am J Hum Genet. 2013;93:321-329.
66. Roosing S, Rohrschneider K, Beryozkin A, et al. Mutations in RAB28, encoding a farnesylated small GTPase, are associated with autosomal-recessive cone-rod dystrophy. Am J Hum Genet. 2013;93:110-117.
67. Sergouniotis PI, Davidson AE, Mackay DS, et al. Biallelic mutations in PLA2G5, encoding group V phospholipase A2, cause benign fleck retina. Am J Hum Genet. 2011;89:782-791.
68. Sergouniotis PI, Davidson AE, Mackay DS, et al. Recessive mutations in KCNJ13, encoding an inwardly rectifying potassium channel subunit, cause leber congenital amaurosis. Am J Hum Genet. 2011;89:183-190.