Mutations in MFSD8, encoding a lysosomal membrane protein, are associated with nonsyndromic autosomal recessive macular dystrophy

Ophthalmology

Volumn 122, Issue 1, 2015, Pages 170-179

  Roosing, Susanne ^a,b,i   Van Den Born, L Ingeborgh ^c   Sangermano, Riccardo ^a,b   Banfi, Sandro ^d,e   Koenekoop, Robert K ^f   Zonneveld Vrieling, Marijke N ^a   Klaver, Caroline C W ^g   Van Lith Verhoeven, Janneke J C ^h   Cremers, Frans P M ^a,b   Den Hollander, Anneke I ^a,b   Hoyng, Carel B ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^c ROTTERDAM EYE HOSPITAL   (Netherlands)

^d TELETHON INSTITUTE OF GENETICS AND MEDICINE TIGEM   (Italy)

^e SECOND UNIVERSITY OF NAPLES   (Italy)

^f MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^g ERASMUS MEDICAL CENTER   (Netherlands)

^h CPRLab   (Netherlands)

ⁱ ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LYSOSOME ASSOCIATED MEMBRANE PROTEIN; CARRIER PROTEIN; MFSD8 PROTEIN, HUMAN;

ADULT; AGED; ARTICLE; AUTOFLUORESCENCE IMAGING; AUTOSOMAL RECESSIVE DISORDER; CASE STUDY; CLINICAL FEATURE; COHORT ANALYSIS; COLOR VISION DEFECT; COLOR VISION TEST; CONTROLLED STUDY; ELECTRORETINOGRAPHY; EXOME; EXON SKIPPING; EYE PHOTOGRAPHY; GENE; GENE IDENTIFICATION; GENE SEQUENCE; GENETIC ASSOCIATION; GENETIC VARIABILITY; HETEROZYGOTE; HUMAN; LINKAGE ANALYSIS; MACULAR DEGENERATION; MAJOR CLINICAL STUDY; MFSD8 GENE; MIDDLE AGED; MISSENSE MUTATION; NEXT GENERATION SEQUENCING; NONSYNDROMIC AUTOSOMAL RECESSIVE MACULAR DYSTROPHY; OPHTHALMOSCOPY; OPTICAL COHERENCE TOMOGRAPHY; OUTCOME ASSESSMENT; PERIMETRY; PRIORITY JOURNAL; RESTRICTION MAPPING; SEGREGATION ANALYSIS; SEQUENCE ANALYSIS; SLIT LAMP; SPLICING DEFECT; VISUAL ACUITY; FEMALE; GENETICS; MALE; MUTATION; NUCLEOTIDE SEQUENCE; PEDIGREE;

ADULT; AGED; DNA MUTATIONAL ANALYSIS; ELECTRORETINOGRAPHY; EXOME; FEMALE; GENOME-WIDE ASSOCIATION STUDY; HUMANS; LYSOSOME-ASSOCIATED MEMBRANE GLYCOPROTEINS; MACULAR DEGENERATION; MALE; MEMBRANE TRANSPORT PROTEINS; MIDDLE AGED; MUTATION; PEDIGREE; TOMOGRAPHY, OPTICAL COHERENCE; VISUAL FIELD TESTS;

EID: 84920736369     PISSN: 01616420     EISSN: 15494713     Source Type: Journal    
DOI: 10.1016/j.ophtha.2014.07.040     Document Type: Article

References (59)

1. Michaelides M, Hunt DM, Moore AT. The cone dysfunction syndromes. Br J Ophthalmol 2004;88:291-7.
2. Hamel CP. Cone rod dystrophies. Orphanet J Rare Dis [serial online] 2007;2:7. Available at: www.ojrd.com/content/2/1/7. Accessed July 23, 2014.
3. 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;85:240-7.
4. Kohl S, Baumann B, Broghammer M, et al. Mutations in the CNGB3 gene encoding the beta-subunit of the cone photoreceptor cGMP-gated channel are responsible for achromatopsia (ACHM3) linked to chromosome 8q21. Hum Mol Genet 2000;9:2107-16.
5. Thiadens AA, Slingerland NW, Roosing S, et al. Genetic etiology and clinical consequences of complete and incomplete achromatopsia. Ophthalmology 2009;116:1984-9.
6. Thiadens AA, Somervuo V, van den Born LI, et al. Progressive loss of cones in achromatopsia: an imaging study using spectral-domain optical coherence tomography. Invest Ophthalmol Vis Sci 2010;51:5952-7.
7. Michaelides M, Hardcastle AJ, Hunt DM, Moore AT. Progressive cone and cone-rod dystrophies: phenotypes and underlying molecular genetic basis. Surv Ophthalmol 2006;51:232-58.
8. Thiadens AA, Phan TM, Zekveld-Vroon RC, et al; Writing Committee for the Cone Disorders Study Group Consortium. Clinical course, genetic etiology, and visual outcome in cone and cone-rod dystrophy. Ophthalmology 2012;119:819-26.
9. Michaelides M, Chen LL, Brantley MA Jr, et al. ABCA4 mutations and discordant ABCA4 alleles in patients and siblings with bull's-eye maculopathy. Br J Ophthalmol 2007;91:1650-5.
10. Wycisk KA, Zeitz C, Feil S, et al. Mutation in the auxiliary calcium-channel subunit CACNA2D4 causes autosomal recessive cone dystrophy. Am J Hum Genet 2006;79:973-7.
11. Wissinger B, Gamer D, Jagle H, et al. CNGA3 mutations in hereditary cone photoreceptor disorders. Am J Hum Genet 2001;69:722-37.
12. Kellner U, Wissinger B, Kohl S, et al. Molecular genetic findings in patients with congenital cone dysfunction. Mutations in the CNGA3, CNGB3, or GNAT2 genes [in German]. Ophthalmologe 2004;101:830-5.
13. Michaelides M, Aligianis IA, Ainsworth JR, et al. Progressive cone dystrophy associated with mutation in CNGB3. Invest Ophthalmol Vis Sci 2004;45:1975-82.
14. Littink KW, Koenekoop RK, van den Born LI, et al. Homozygosity mapping in patients with cone-rod dystrophy: novel mutations and clinical characterizations. Invest Ophthalmol Vis Sci 2010;51:5943-51.
15. Kohl S, Coppieters F, Meire F, et al; European Retinal Disease Consortium. A nonsense mutation in PDE6H causes autosomal-recessive incomplete achromatopsia. Am J Hum Genet 2012;91:527-32.
16. Roosing S, van den Born LI, Hoyng CB, et al. Maternal uniparental isodisomy of chromosome 6 reveals a TULP1 mutation as a novel cause of cone dysfunction. Ophthalmology 2013;120:1239-46.
17. Cremers FP, van de Pol DJ, van Driel M, et al. Autosomal recessive retinitis pigmentosa and cone-rod dystrophy caused by splice site mutations in the Stargardt's disease gene ABCR. Hum Mol Genet 1998;7:355-62.
18. Parry DA, Toomes C, Bida L, et al. Loss of the metalloprotease ADAM9 leads to cone-rod dystrophy in humans and retinal degeneration in mice. Am J Hum Genet 2009;84:683-91.
19. Estrada-Cuzcano AI, Neveling K, Kohl S, et al; European Retinal Disease Consortium. Mutations in C8orf37, encoding a ciliary protein, are associated with autosomal-recessive retinal dystrophies with early macular involvement. Am J Hum Genet 2012;90:102-9.
20. Ostergaard E, Batbayli M, Duno M, et al. Mutations in PCDH21 cause autosomal recessive cone-rod dystrophy. J Med Genet 2010;47:665-9.
21. Henderson RH, Li Z, Abd El Aziz MM, et al. Biallelic mutation of protocadherin-21 (PCDH21) causes retinal degeneration in humans. Mol Vis [serial online] 2010;16:46-52. Available at: http://www.molvis.org/molvis/v16/a6/. Accessed July 23, 2014.
22. 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;48:5431-8.
23. Huang L, Zhang Q, Li S, et al. Exome sequencing of 47 Chinese families with cone-rod dystrophy: mutations in 25 known causative genes. PLoS One [serial online] 2013;8:e65546. Available at: http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0065546. Accessed July 23, 2014.
24. Henderson RH, Waseem N, Searle R, et al. An assessment of the Apex microarray technology in genotyping patients with Leber congenital amaurosis and early-onset severe retinal dystrophy. Invest Ophthalmol Vis Sci 2007;48:5684-9.
25. Littink KW, van den Born LI, Koenekoop RK, et al. Mutations in the EYS gene account for approximately 5% of autosomal recessive retinitis pigmentosa and cause a fairly homogeneous phenotype. Ophthalmology 2010;117:2026-33.
26. Zhang Q, Li S, Xiao X, et al. The 208delG mutation in FSCN2 does not associate with retinal degeneration in Chinese individuals. Invest Ophthalmol Vis Sci 2007;48:530-3.
27. Ugur Iseri SA, Durlu YK, Tolun A. A novel recessive GUCY2D mutation causing cone-rod dystrophy and not Leber's congenital amaurosis. Eur J Hum Genet 2010;18:1121-6.
28. Durlu YK, Koroglu C, Tolun A. Novel recessive cone-rod dystrophy caused by POC1B mutation. JAMA Ophthalmol 2014;95:131-42.
29. Roosing S, Lamers IJ, de Vrieze E, et al. Disruption of the basal body protein POC1B results in autosomal-recessive cone-rod dystrophy. Am J Hum Genet 2014;95:131-42.
30. Pras E, Abu A, Rotenstreich Y, et al. Cone-rod dystrophy and a frameshift mutation in the PROM1 gene. Mol Vis [serial online] 2009;15:1709-16. Available at: http://www.molvis.org/molvis/v15/a183/. Accessed July 23, 2014.
31. 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;93:110-7.
32. den Hollander AI, Black A, Bennett J, Cremers FP. Lighting a candle in the dark: advances in genetics and gene therapy of recessive retinal dystrophies. J Clin Invest 2010;120:3042-53.
33. Roosing S, Thiadens AA, Hoyng CB, et al. Causes and consequences of inherited cone disorders. Prog Retin Eye Res 2014;42C:1-26.
34. Zeitz C, Jacobson SG, Hamel CP, et al; Congenital Stationary Night Blindness Consortium. Whole-exome sequencing identifies LRIT3 mutations as a cause of autosomal-recessive complete congenital stationary night blindness. Am J Hum Genet 2013;92:67-75.
35. Audo I, Bujakowska K, Orhan E, et al. Whole-exome sequencing identifies mutations in GPR179 leading to auto-somal- recessive complete congenital stationary night blindness. Am J Hum Genet 2012;90:321-30.
36. Thiadens AA, Klaver CC. Genetic testing and clinical characterization of patients with cone-rod dystrophy [letter]. Invest Ophthalmol Vis Sci 2010;51:6904-5. author reply 6905.
37. Marmor MF, Fulton AB, Holder GE, et al; International Society for Clinical Electrophysiology of Vision. ISCEV standard for full-field clinical electroretinography (2008 update). Doc Ophthalmol 2009;118:69-77.
38. Nagy E, Maquat LE. A rule for termination-codon position within intron-containing genes: when nonsense affects RNA abundance. Trends Biochem Sci 1998;23:198-9.
39. Siintola E, Topcu M, Aula N, et al. The novel neuronal ceroid lipofuscinosis gene MFSD8 encodes a putative lysosomal transporter. Am J Hum Genet 2007;81:136-46.
40. Aiello C, Terracciano A, Simonati A, et al. Mutations in MFSD8/CLN7 are a frequent cause of variant-late infantile neuronal ceroid lipofuscinosis [report online]. Hum Mutat 2009;30:E530-40.
41. Kousi M, Siintola E, Dvorakova L, et al. Mutations in CLN7/MFSD8 are a common cause of variant late-infantile neuronal ceroid lipofuscinosis. Brain 2009;132:810-9.
42. Topcu M, Tan H, Yalnizoglu D, et al. Evaluation of 36 patients from Turkey with neuronal ceroid lipofuscinosis: clinical, neurophysiological, neuroradiological and histopathologic studies. Turk J Pediatr 2004;46:1-10.
43. Aldahmesh MA, Al-Hassnan ZN, Aldosari M, Alkuraya FS. Neuronal ceroid lipofuscinosis caused by MFSD8 mutations: a common theme emerging. Neurogenetics 2009;10:307-11.
44. Stogmann E, El Tawil S, Wagenstaller J, et al. A novel mutation in the MFSD8 gene in late infantile neuronal ceroid lipofuscinosis. Neurogenetics 2009;10:73-7.
45. Damme M, Brandenstein L, Fehr S, et al. Gene disruption of Mfsd8 in mice provides the first animal model for CLN7 disease. Neurobiol Dis 2014;65:12-24.
46. Steenhuis P, Herder S, Gelis S, et al. Lysosomal targeting of the CLN7 membrane glycoprotein and transport via the plasma membrane require a dileucine motif. Traffic 2010;11:987-1000.
47. Sharifi A, Kousi M, Sagne C, et al. Expression and lysosomal targeting of CLN7, a major facilitator superfamily transporter associated with variant late-infantile neuronal ceroid lipofuscinosis. Hum Mol Genet 2010;19:4497-514.
48. Steenhuis P, Froemming J, Reinheckel T, Storch S. Proteolytic cleavage of the disease-related lysosomal membrane glycoprotein CLN7. Biochim Biophys Acta 2012;1822:1617-28.
49. Pinckers A. Clinical color vision examination. Doc Ophthalmol Proc Ser 1984;39:171-9.
50. Sarpong A, Schottmann G, Ruther K, et al. Protracted course of juvenile ceroid lipofuscinosis associated with a novel CLN3 mutation (p.Y199X). Clin Genet 2009;76:38-45.
51. Chan CH, Mitchison HM, Pearce DA. Transcript and in silico analysis of CLN3 in juvenile neuronal ceroid lipofuscinosis and associated mouse models. Hum Mol Genet 2008;17:3332-9.
52. Wang X, Wang H, Sun V, et al. Comprehensive molecular diagnosis of 179 Leber congenital amaurosis and juvenile retinitis pigmentosa patients by targeted next generation sequencing. J Med Genet 2013;50:674-88.
53. Wang F, Wang H, Tuan HF, et al. Next generation sequencing-based molecular diagnosis of retinitis pigmentosa: identification of a novel genotype-phenotype correlation and clinical refinements. Hum Genet 2014;133:331-45.
54. den Hollander AI, Roepman R, Koenekoop RK, Cremers FP. Leber congenital amaurosis: genes, proteins and disease mechanisms. Prog Retin Eye Res 2008;27:391-419.
55. Anderson GW, Goebel HH, Simonati A. Human pathology in NCL. Biochim Biophys Acta 2013;1832:1807-26.
56. Kim JY, Zhao H, Martinez J, et al. Noncanonical autophagy promotes the visual cycle. Cell 2013;154:365-76.
57. Liu J, Lu W, Reigada D, et al. Restoration of lysosomal pH in RPE cells from cultured human and ABCA4(-/-) mice: pharmacologic approaches and functional recovery. Invest Ophthalmol Vis Sci 2008;49:772-80.
58. Settembre C, Fraldi A, Medina DL, Ballabio A. Signals from the lysosome: a control centre for cellular clearance and energy metabolism. Nat Rev Mol Cell Biol 2013;14:283-96.
59. Mirza M, Volz C, Karlstetter M, et al. Progressive retinal degeneration and glial activation in the CLN6 (nclf) mouse model of neuronal ceroid lipofuscinosis: a beneficial effect of DHA and curcumin supplementation. PLoS One [serial online] 2013;8:e75963. Available at: http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0075963. Accessed July 23, 2014.