A missense mutation in GUCY2D acts as a genetic modifier in RPE65-related Leber congenital amaurosis

Ophthalmic Genetics

Volumn 25, Issue 3, 2004, Pages 205-217

  Silva, Eduardo ^a,b   Dharmaraj, Sharola ^a,b   Li, Ying Ying ^b   Pina, Ana Luisa ^c   Carter, Robert Colin ^b   Loyer, Magali ^c   Traboulsi, Elias ^d   Theodossiadis, George ^e   Koenekoop, Robert K ^c   Sundin, Olof H ^a   Maumenee, Irene H ^b  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c MONTREAL CHILDREN S HOSPITAL   (Canada)

^d LERNER RESEARCH INSTITUTE   (United States)

^e UNIVERSITY OF ATHENS   (Greece)

Author keywords

Genetic modifier; GUCY2D; Leber congenital amaurosis; RPE65

Indexed keywords

ISOLEUCINE; VALINE;

ADULT; AIPL1 GENE; ARTICLE; CASE REPORT; CRX GENE; DISEASE SEVERITY; FEMALE; GENE; GENE DISRUPTION; GENE FUNCTION; GENE SEGREGATION; GENETIC SCREENING; GENETIC VARIABILITY; GENOTYPE PHENOTYPE CORRELATION; GUCY2D GENE; HETEROZYGOSITY; HOMOZYGOSITY; HUMAN; LEBER CONGENITAL AMAUROSIS; MISSENSE MUTATION; PEDIGREE; PHENOTYPE; PHOTORECEPTOR; PRIORITY JOURNAL; RETINA DYSTROPHY; RPE65 GENE; RPGRIP1 GENE; SIBLING;

ADULT; BLINDNESS; CARRIER PROTEINS; CHROMOSOME SEGREGATION; EYE PROTEINS; FEMALE; GENOTYPE; GUANYLATE CYCLASE; HOMOZYGOTE; HUMANS; MUTATION, MISSENSE; PEDIGREE; PHENOTYPE; PROTEINS; RECEPTORS, CELL SURFACE; RETINAL DEGENERATION; SIBLINGS;

EID: 9144240146     PISSN: 13816810     EISSN: None     Source Type: Journal    
DOI: 10.1080/13816810490513451     Document Type: Article

References (53)

1. Kajiwara K, Berson EL, Dryja TP. Digenic retinitis pigmentosa due to mutations in the unlinked peripherin/RDS and ROM1 loci. Science 1994;264:1604-1608.
2. Balciuniene J, Dahl N, Borg E, Samuelsson E, Koisti MJ, Pettersson U, Jazin EE. Evidence of digenic inheritance of non-syndromic hereditary hearing loss in a Swedish family. Am J Hum Genet. 1998;63: 786-793.
3. Scriver CR, Waters PJ. Monogenic traits are not simple: lessons from phenylketonuria. Trends Genet. 1999;15:267-272.
4. Dipple KM, McCabe ER. Modifier genes convert "simple" Mendelian disorders to complex traits. Mol Genet Metab. 2000;71:43-50.
5. Goldberg AF, Moritz OL, Molday RS. Heterologous expression of photoreceptor peripherin/rds and Rom-1 in COS-1 cells: assembly, interactions, and localization of multisubunit complexes. Biochemistry. 1995;31;34(43):14213- 9.
6. Leber T. Uber retinitis pigmentosa und angebore amaurose. Graefes Arch Klin Ophthalmol 1869;15:1-25.
7. Perrault I, Hanein S, Gerber S, Barbet F, Dufier JL, Munnich A, Rozet JM, Kaplan J. Evidence of autosomal dominant Leber congenital amaurosis (LCA) underlain by a CRX heterozygous null allele. J Med Genet. 2003;40:e90.
8. Sohocki MM, Sullivan LS, Mintz-Hittner HA, Birch D, Heckenlively JR, Freund CL, McInnes RR, Daiger SP. A range of clinical phenotypes associated with mutations in CRX, a photoreceptor transcription-factor gene. Am J Hum Genet. 1998;63:1307-1315.
9. Foxman SG, Heckenlively JR, Bateman B, Wirttschafter JD. Classification of congenital and early-onset retinitis pigmentosa. Arch Ophthalmol. 1985;103:1502-1506.
10. Noble KG, Carr RE. Leber's congenital amaurosis. A retrospective study of 33 cases and a histopathological study of one case. Arch Ophthalmol. 1978;96:818-821.
11. Perrault I, Rozet JM, Calvas P, Gerber S, Camuzat A, Dollfus H, Chatelin S, Souied E, Ghazi I, Leowski C, Bonnemaison M, LePaslier D, Frezal J, Dufier JL, Pittler S, Munnich A, Kaplan J. Retinal-specific guanylate cyclase gene mutations in Leber's congenital amaurosis. Nat Genet. 1996;14:461-403.
12. Gu SM, Thompson D, Srisailapathy-Srikumari CR, Lorenz B, Finckh U, Nicoletti A, Murthy KR, Rathmann M, Kumaramanickavel G, Denton MJ, Gal A. Mutations in RPE65 cause autosomal recessive childhood-onset severe retinal dystrophy. Nat Genet. 1997;17:194-197.
13. Marlhens F, Bareil C, Griffoin JM, Zrenner E, Amalric P, Eliaou C, Liu SY, Harris E, Redmond TM, Arnaud B, Clausters M, Hamel CP. Mutations in RPE65 cause Leber's congenital amaurosis. Nat Genet. 1997;17:139-141.
14. Freund CL, Wang QL, Chen S, Muskat B, Wiles CD, Sheffield VC, Jacobson SG, McInnes RR, Zack DJ, Stone EM. De novo mutations in the CRX homeobox gene associated with Leber congenital amaurosis. Nat Genet. 1998;18:311-312.
15. Sohocki MM, Bowne SJ, Sullivan LS, Blackshaw S, Cepko CL, Payne AM, Bhattacharya SS, Khaliq S, Mehdi SQ, Birch DG, Harrison WR, Elder FFB, Heckenlively JR, Daiger SP. Mutations in a new photoreceptor-pineal gene on 17p cause Leber congenital amaurosis. Nat Genet. 2000;24:79-83.
16. Lotery AJ, Jacobson SG, Fishman GA, Weleber RG, Fulton AB, Namperumalsamy P, Heon E, Levin AV, Grover S, Rosenow JR, Kopp KK, Sheffield VC, Stone EM. Mutations in the CRB1 gene cause Leber congenital amaurosis. Arch Ophthalmol. 2001;119:415-420.
17. Dryja TP, Adams SM, Grimsby JL, McGee TL, Hong D, Li T, Andreasson S, Berson EL. Null RPGRIP1 alleles in patients with Leber Congenital Amaurosis. Am J Hum Genet. 2001;68:1295-1298.
18. Stockton DW, Lewis RA, Abboud EB, Al-Rajhi A, Jabak M, Anderson KL, Lupski JR. A novel locus for Leber congenital amaurosis on chromosome 14q24. Hum Genet. 1998;103:328-333.
19. Dharmaraj S, Li Y, Robitaille JM, Silva E, Zhu D, Mitchell TM, Maltby LP, Baffoe-Bonnie AB, Maumenee IH. A novel locus for Leber congenital amaurosis maps to chromosome 6q. Am J Hum Genet. 2000;66:319-326.
20. Keen TJ, Mohamed MD, McKibbin M, Rashid Y, Jafri H, Maumenee IH, Inglehearn CF. Identification of a locus (LCA9) for Leber's congenital amaurosis on chromosome 1p36. Eur J Hum Genet. 2003;11:420-423.
21. Thompson DA, Li Y, McHenry CL, Carlson TJ, Ding X, Sieving PA, Apfelstedt-Sylla E, Gal A. Mutations in the gene encoding lecithin retinol acyltransferase are associated with early-onset severe retinal dystrophy. Nat Genet. 2001; 28:123-124.
22. Paloma E, Hjelmqvist L, Bayes M, Garcia-Sandoval B, Ayuso C, Balcells S, Gonzalez-Duarte R. Novel mutations in the TULP1 gene causing autosomal recessive retinitis pigmentosa. Invest Ophthalmol Vis Sci. 2000;41;656-659.
23. Banerjee P, Kleyn PW, Knowles JA, Lewis CA, Ross BM, Parano E, Kovats SG, Lee JJ, Penchaszadeh GK, Ott J, Jacobson SG, Gilliam TC. TULP1 mutation in two extended Dominican kindreds with autosomal recessive retinitis pigmentosa. Nat Genet. 1998;18:177-179.
24. Hagstrom SA, North MA, Nishina PL, Berson EL, Dryja TP. Recessive mutations in the gene encoding the tubby-like protein TULP1 in patients with retinitis pigmentosa. Nat Genet. 1998;18:174-176.
25. Redmond TM, Yu S, Lee E, Bok D, Hamasaki D, Chen N, Goletz P, Ma JX, Crouch RK, Pfeifer K. Rpe65 is necessary for production of n-cis-vitamin A in the retinal visual cycle. Nat Genet. 1998;20:344-351.
26. Woodruff ML, Wang Z, Chung HY, Redmond TM, Fain GL, Lem J. Spontaneous activity of opsin apoprotein is a cause of Leber congenital amaurosis. Nat Genet. 2003;35:158-164.
27. Dizhoor AM, Lowe DG, Olshevskaya EV, Laura RP, Hurley JB. The human photoreceptor membrane guanylyl cyclase, RetGC, is present in outer segments and is regulated by calcium and a soluble activator. Neuron. 1994;12:1345-1352.
28. Tucker CL, Ramamurthy V, Pina AL, Loyer M, Dharmaraj S, Li Y, Maumenee IH, Hurley JB, Koenekoop RK. Functional analyses of mutant recessive GUCY2D alleles identified in Leber congenital amaurosis patients: protein domain comparisons and dominant negative effects. Mol Vis. 2004;10:297-303.
29. Dharmaraj S, Silva ER, Pina AL, Li YY, Yang JM, Carter CR, Loyer MK, El-Hilali HK,Traboulsi EK, Sundin OK, Zhu IDK, Koenekoop RK, Maumenee IH. Mutational analysis and clinical correlation in Leber congenital amaurosis. Ophthalmic Genet. 2000;21:135-150.
30. Morimura H, Fishman GA, Grover SA, Fulton AB, Berson EL, Dryja TP. Mutations in the RPE65 gene in patients with autosomal recessive retinitis pigmentosa or leber congenital amaurosis. Proc Natl Acad Sci U S A. 1998;95:3088-3093.
31. Tucker CL, Laura RP, Hurley JB. Domain-specific stabilization of photoreceptor membrane guanylyl cyclase by adenine nucleotides and guanylyl cyclase activating proteins (GCAPs). Biochemistry. 1997;36: 11995-2000.
32. Dizhoor AM, Hurley JB. Regulation of photoreceptor membrane guanylyl cyclases by guanylyl cyclase activator proteins. Methods. 1999;19: 521-531.
33. Laura RP, Hurley JB. The kinase homology domain of retinal guanylyl cyclase 1 and 2 specifies the affinity and cooperativity of interaction with uanylyl cyclase activating protein-2. Biochem. 1998; 37:11264-11271.
34. Perrault I, Rozet JM, Gerber S, Ghazi I, Ducroq D, Souied E, Leowski C, Bonnemaison M, Dufier JL, Munnich A, Kaplan J. Spectrum of retGC1 mutations in Leber's congenital amaurosis. Eur J Hum Genet. 2000;8:578-582.
35. Kelsell RE, Gregory-Evans K, Payne AM, Perrault I, Kaplan J, Yang RB, Garbers DL, Bird AC, Moore AT, Hunt DM. Mutations in the retinal guanylate cyclase (RETGC-1) gene in dominant cone-rod dystrophy. Hum Mol Genet. 1998;7:1179-1184.
36. Payne AM, Morris AG, Downes SM, Johnson S, Bird AC, Moore AT, Bhattacharya SS, Hunt DM. Clustering and frequency of mutations in the retinal guanylate cyclase (GUCY2D) gene in patients with dominant cone-rod dystrophies. J Med Genet. 2001;38:611-614.
37. Thompson DA, Gal A. Genetic defects in vitamin A metabolism of the retinal pigment epithelium. Review. Dev Ophthalmol. 2003;37: 141-154.
38. Mata NL, Moghrabi WN, Lee JS, Bui TV, Radu RA, Horwitz J, Travis GH. Rpe65 is a retinyl ester binding protein that presents insoluble substrate to the isomerase in retinal pigment epithelial cells. J Biol Chem. 2004;279:635-643.
39. Grimm C, Wenzel A, Hafezi F, Yu S, Redmond TM, Reme CE. Protection of Rpe65-deficient mice identifies rhodopsin as a mediator of light-induced retinal degeneration. Nat Genet. 2000;25:63-66.
40. Ekesten B, Gouras P, Salchow DJ. Ultraviolet and middle wavelength sensitive cone responses in the electroretinogram (ERG) of normal and Rpe65 -/- mice. Vision Res. 2001;41:2425-2433.
41. Seeliger MW, Grimm C, Stahlberg F, Friedburg C, Jaissle G, Zrenner E, Guo H, Reme CE, Humphries P, Hofmann F, Biel M, Fariss RN, Redmond TM, Wenzel A. New views on RPE65 deficiency: the rod system is the source of vision in a mouse model of Leber congenital amaurosis. Nat Genet. 2001;29:70-74.
42. Das SR, Bhardwaj N, Kjeldbye H, Gouras P. Muller cells of the chicken retina synthesize 11-cis-retinol. Biochem J. 1992;285:907-913.
43. Hicks D, Sahel J. The implications of rod-dependent cone survival for basic and clinical research. Invest Ophthalmol Vis Sci. 1999;40:3071-3074.
44. Liu X, Seno K, Nishizawa Y, Hayashi F, Yamazaki A, Matsumoto H, Wakabayashi T, Usukura J. Ultrastructural localization of retinal guanylate cyclase in human and monkey retinas. Exp Eye Res. 1994; 59:761-768.
45. Yzer S, van den Born LI, Schuil J, Kroes HY, van Genderen MM, Boonstra FN, van den Helm B, Brunner HG, Koenekoop RK, Cremers FP. A Tyr368His RPE65 founder mutation is associated with variable expression and progression of early onset retinal dystrophy in 10 families of a genetically isolated population. J Med Genet. 2003;40: 709-713.
46. Koenekoop RK, Fishman GA, Iannaccone A, Ezzeldin H, Ciccarelli ML, Baldi A, Sunness JS, Lotery AJ, Jablonski MM, Pittler SJ, Maumenee I. Electroretinographic abnormalities in parents of patients with Leber congenital amaurosis who have heterozygous GUCY2D mutations. Arch Ophthalmol. 2002;120:1325-1330.
47. Felius J, Thompson DA, Khan NW, Bingham EL, Jamison JA, Kemp JA, Sieving PA. Clinical course and visual function in a family with mutations in the RPE65 gene. Arch Ophthalmol. 2002;120:55-61.
48. Allikmets RL, Zernant J, Külm M, Perrault I, den Hollander A, Dharmaraj S, Koenekoop R, Kaplan J, Cremers F, Maumenee I. Genotyping microarray (disease chip) for Leber congenital amaurosis Invest Ophthalmol Vis Sci. 2003;44:A285.
49. Perrault I, Rozet JM, Ghazi I, Leowski C, Bonnemaison M, Gerber S, Ducroq D, Cabot A, Souied E, Dufier JL, Munnich A, Kaplan J. Different functional outcome of RetGC1 and RPE65 gene mutations in Leber congenital amaurosis. Am J Hum Genet. 1999;64:1225-1228.
50. Thompson DA, Gyurus P, Fleischer LL, Bingham EL, McHenry CL, Apfelstedt-Sylla E, Zrenner E, Lorenz B, Richards JE, Jacobson SG, Sieving PA, Gal A. Genetics and phenotypes of RPE65 mutations in inherited retinal degeneration. Invest Ophthalmol Vis Sci. 2000;41: 4293-4299.
51. Cazeneuve C, Ajrapetyan H, Papin S, Roudot-Thoraval F, Genevieve D, Mndjoyan E, Papazian M, Sarkisian A, Babloyan A, Boissier B, Duquesnoy P, Kouyoumdjian JC, Girodon-Boulandet E, Grateau G, Sarkisian T, Amselem S. Identification of MEFV-independent modifying genetic factors for familial Mediterranean fever. Am J Hum Genet. 2000;67:1136-1143.
52. Wenzel A, Grimm C, Samardzija M, Reme CE. The genetic modifier Rpe65Leu(450): effect on light damage susceptibility in c-Fos-deficient mice. Invest Ophthalmol Vis Sci. 2003;44:2798-2802.
53. Wenzel A, Reme CE, Williams TP, Hafezi F, Grimm C. The Rpe65 Leu450Met variation increases retinal resistance against light-induced degeneration by slowing rhodopsin regeneration. J Neurosci. 2001;21:53-58.