Unexpected CEP290 mRNA splicing in a humanized knock-in mouse model for Leber congenital amaurosis

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Garanto, Alejandro ^a   Van Beersum, Sylvia E C ^a,b   Peters, Theo A ^a,b,c   Roepman, Ronald ^a,b   Cremers, Frans P M ^a,b   Collin, Rob W J ^a,b  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^c RADBOUD UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CEP290 GENE; CONTROLLED STUDY; DISEASE MODEL; EXON; FEMALE; GENE; GENE EXPRESSION; GENE MUTATION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; LEBER CONGENITAL AMAUROSIS; MOUSE; NONHUMAN; RETINA; RNA SPLICING; SPECIES DIFFERENCE; WESTERN BLOTTING;

ANIMALS; ANTIGENS, NEOPLASM; CELL LINE; DISEASE MODELS, ANIMAL; EXONS; FEMALE; GENE KNOCK-IN TECHNIQUES; HUMANS; LEBER CONGENITAL AMAUROSIS; MICE; NEOPLASM PROTEINS; PREGNANCY; RETINA; RNA SPLICING; SPECIES SPECIFICITY; TRANSCRIPTION, GENETIC;

EID: 84892377709     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0079369     Document Type: Article

References (40)

1. Koenekoop RK (2004) An overview of Leber congenital amaurosis: a model to understand human retinal development. Surv Ophthalmol 49: 379-398. doi:10.1016/j.survophthal.2004.04.003. PubMed: 15231395.
2. Stone EM (2007) Leber congenital amaurosis - a model for efficient genetic testing of heterogeneous disorders: LXIV Edward Jackson Memorial Lecture. Am J Ophthalmol 144: 791-811. doi:10.1016/j.ajo.2007.08.022. PubMed: 17964524.
3. den Hollander AI, Roepman R, Koenekoop RK, Cremers FPM (2008) Leber congenital amaurosis: genes, proteins and disease mechanisms. Prog Retin Eye Res 27: 391-419. doi:10.1016/j.preteyeres.2008.05.003. PubMed: 18632300.
4. Coppieters F, Lefever S, Leroy BP, De Baere E (2010) CEP290, a gene with many faces: mutation overview and presentation of CEP290base. Hum Mutat 31: 1097-1108. doi:10.1002/humu.21337.PubMed: 20690115.
5. den Hollander AI, Koenekoop RK, Yzer S, Lopez I, Arends ML et al. (2006) Mutations in the CEP290 (NPHP6) gene are a frequent cause of Leber congenital amaurosis. Am J Hum Genet 79: 556-561. doi:10.1086/507318. PubMed: 16909394.
6. Perrault I, Delphin N, Hanein S, Gerber S, Dufier JL et al. (2007) Spectrum of NPHP6/CEP290 mutations in Leber congenital amaurosis and delineation of the associated phenotype. Hum Mutat 28: 416. doi:10.1002/humu.9485. PubMed: 17345604.
7. Littink KW, Pott JW, Collin RWJ, Kroes HY, Verheij JB et al. (2010) A novel nonsense mutation in CEP290 induces exon skipping and leads to a relatively mild retinal phenotype. Invest Ophthalmol Vis Sci 51: 3646-3652. doi:10.1167/iovs.09-5074. PubMed: 20130272.
8. Hildebrandt F, Zhou W (2007) Nephronophthisis-associated ciliopathies. J Am Soc Nephrol 18: 1855-1871. doi:10.1681/ASN.2006121344. PubMed: 17513324.
9. Sayer JA, Otto EA, O'Toole JF, Nurnberg G, Kennedy MA et al. (2006) The centrosomal protein nephrocystin-6 is mutated in Joubert syndrome and activates transcription factor ATF4. Nat Genet 38: 674-681. doi:10.1038/ng1786. PubMed: 16682973.
10. Leitch CC, Zaghloul NA, Davis EE, Stoetzel C, Diaz-Font A et al. (2008) Hypomorphic mutations in syndromic encephalocele genes are associated with Bardet-Biedl syndrome. Nat Genet 40: 443-448. doi:10.1038/ng.97. PubMed: 18327255.
11. Frank V, den Hollander AI, Brüchle NO, Zonneveld MN, Nürnberg G et al. (2008) Mutations of the CEP290 gene encoding a centrosomal protein cause Meckel-Gruber syndrome. Hum Mutat 29: 45-52. doi:10.1002/humu.20614. PubMed: 17705300.
12. Nagase T, Ishikawa K, Nakajima D, Ohira M, Seki N et al. (1997) Prediction of the coding sequences of unidentified human genes. VII. The complete sequences of 100 new cDNA clones from brain which can code for large proteins in vitro. DNA Res 4: 141-150. doi:10.1093/dnares/4.2.141. PubMed: 9205841.
13. Craige B, Tsao CC, Diener DR, Hou Y, Lechtreck KF et al. (2010) CEP290 tethers flagellar transition zone microtubules to the membrane and regulates flagellar protein content. J Cell Biol 190: 927-940. doi:10.1083/jcb.201006105. PubMed: 20819941.
14. Garcia-Gonzalo FR, Corbit KC, Sirerol-Piquer MS, Ramaswami G, Otto EA et al. (2011) A transition zone complex regulates mammalian ciliogenesis and ciliary membrane composition. Nat Genet 43: 776-784. doi:10.1038/ng.891. PubMed: 21725307.
15. Barbelanne M, Song J, Ahmadzai M, Tsang WY (2013) Pathogenic NPHP5 mutations impair protein interaction with Cep290, a prerequisite for ciliogenesis. Hum: Mol Genet.
16. Chang B, Khanna H, Hawes N, Jimeno D, He S et al. (2006) In-frame deletion in a novel centrosomal/ciliary protein CEP290/NPHP6 perturbs its interaction with RPGR and results in early-onset retinal degeneration in the rd16 mouse. Hum Mol Genet 15: 1847-1857. doi:10.1093/hmg/ddl107. PubMed: 16632484.
17. Estrada-Cuzcano A, Roepman R, Cremers FPM, den Hollander AI, Mans DA (2012) Non-syndromic retinal ciliopathies: translating gene discovery into therapy. Hum Mol Genet 21: R111-R124. doi:10.1093/hmg/dds298. PubMed: 22843501.
18. Kolb H (2003) How the Retina Works. Am Sci 91: 28-35. doi:10.1511/2003.1.28.
19. Menotti-Raymond M, David VA, Schäffer AA, Stephens R, Wells D et al. (2007) Mutation in CEP290 discovered for cat model of human retinal degeneration. J Hered 98: 211-220. doi:10.1093/jhered/esm019.PubMed: 17507457.
20. Narfström K (1985) Progressive retinal atrophy in the Abyssinian cat. Clinical characteristics. Invest Ophthalmol Vis Sci 26: 193-200. PubMed: 3972501.
21. Rasband WS (1997-2012) Image J. In: USA Maryland, U. S. National Institutes of Health B. Available: http://imagej.nih.gov/ij/. Accessed 2013 September 22.
22. Collin RWJ, den Hollander AI, van der Velde-Visser SD, Bennicelli J, Bennett J et al. (2012) Antisense Oligonucleotide (AON)-based Therapy for Leber Congenital Amaurosis Caused by a Frequent Mutation in CEP290. Mol Ther Nucleic Acids 1: e14. doi:10.1038/mtna.2012.3. PubMed: 23343883.
23. Chang B, Hawes NL, Hurd RE, Wang J, Howell D et al. (2005) Mouse models of ocular diseases. Vis Neurosci 22: 587-593. PubMed: 16332269.
24. Won J, Shi LY, Hicks W, Wang J, Hurd R et al. (2011) Mouse model resources for vision research. J Ophthalmol, 2011: 2011: 391384. PubMed: 21052544
25. Song BJ, Tsang SH, Lin C-S (2007) Genetic models of retinal degeneration and targets for gene therapy. Gene Therapy Molecular Biol 11: 229-262.
26. Gerard X, Perrault I, Hanein S, Silva E, Bigot K et al. (2012) AON-mediated Exon Skipping Restores Ciliation in Fibroblasts Harboring the Common Leber Congenital Amaurosis CEP290 Mutation. Mol Ther Nucleic Acids 1: e29. doi:10.1038/mtna.2012.21. PubMed: 23344081.
27. Gladman JT, Bebee TW, Edwards C, Wang X, Sahenk Z et al. (2010) A humanized Smn gene containing the SMN2 nucleotide alteration in exon 7 mimics SMN2 splicing and the SMA disease phenotype. Hum Mol Genet 19: 4239-4252. doi:10.1093/hmg/ddq343. PubMed: 20705738.
28. Hims MM, Shetty RS, Pickel J, Mull J, Leyne M et al. (2007) A humanized IKBKAP transgenic mouse models a tissue-specific human splicing defect. Genomics 90: 389-396. doi:10.1016/j.ygeno.2007.05.012. PubMed: 17644305.
29. Vadolas J, Nefedov M, Wardan H, Mansooriderakshan S, Voullaire L et al. (2006) Humanized beta-thalassemia mouse model containing the common IVSI-110 splicing mutation. J Biol Chem 281: 7399-7405. doi:10.1074/jbc.M512931200. PubMed: 16421096.
30. Yang Y, Swaminathan S, Martin BK, Sharan SK (2003) Aberrant splicing induced by missense mutations in BRCA1: clues from a humanized mouse model. Hum Mol Genet 12: 2121-2131. doi:10.1093/hmg/ddg222. PubMed: 12915465.
31. Garanto A, Riera M, Pomares E, Permanyer J, de Castro-Miró M et al. (2011) High transcriptional complexity of the retinitis pigmentosa CERKL gene in human and mouse. Invest Ophthalmol Vis Sci 52: 5202-5214. doi:10.1167/iovs.10-7101. PubMed: 21508105.
32. Roca X, Krainer AR, Eperon IC (2013) Pick one, but be quick: 5′ splice sites and the problems of too many choices. Genes Dev 27: 129-144. doi:10.1101/gad.209759.112. PubMed: 23348838.
33. Collin RWJ, Littink KW, Klevering BJ, van den Born LI, Koenekoop RK et al. (2008) Identification of a 2 Mb human ortholog of Drosophila eyes shut/spacemaker that is mutated in patients with retinitis pigmentosa. Am J Hum Genet 83: 594-603. doi:10.1016/j.ajhg.2008.10.014. PubMed: 18976725.
34. Abd El-Aziz MM, Barragan I, O'Driscoll CA, Goodstadt L, Prigmore E et al. (2008) EYS, encoding an ortholog of Drosophila spacemaker, is mutated in autosomal recessive retinitis pigmentosa. Nat Genet 40: 1285-1287. doi:10.1038/ng.241. PubMed: 18836446.
35. Howes KA, Pennesi ME, Sokal I, Church-Kopish J, Schmidt B et al. (2002) GCAP1 rescues rod photoreceptor response in GCAP1/GCAP2 knockout mice. EMBO J 21: 1545-1554. doi:10.1093/emboj/21.7.1545. PubMed: 11927539.
36. Makino CL, Peshenko IV, Wen XH, Olshevskaya EV, Barrett R et al. (2008) A role for GCAP2 in regulating the photoresponse. Guanylyl cyclase activation and rod electrophysiology in GUCA1B knock-out mice. J Biol Chem 283: 29135-29143. doi:10.1074/jbc.M804445200. PubMed: 18723510.
37. Garanto A, Vicente-Tejedor J, Riera M, de la Villa P, Gonzàlez-Duarte R et al. (2012) Targeted knockdown of Cerkl, a retinal dystrophy gene, causes mild affectation of the retinal ganglion cell layer. Biochim Biophys Acta 1822: 1258-1269. doi:10.1016/j.bbadis.2012.04.004. PubMed: 22549043.
38. Liu X, Bulgakov OV, Darrow KN, Pawlyk B, Adamian M et al. (2007) Usherin is required for maintenance of retinal photoreceptors and normal development of cochlear hair cells. Proc Natl Acad Sci U S A 104: 4413-4418. doi:10.1073/pnas.0610950104. PubMed: 17360538.
39. Kurth I, Thompson DA, Rüther K, Feathers KL, Chrispell JD et al. (2007) Targeted disruption of the murine retinal dehydrogenase gene Rdh12 does not limit visual cycle function. Mol Cell Biol 27: 1370-1379. doi:10.1128/MCB.01486-06. PubMed: 17130236.
40. Acland GM, Aguirre GD, Ray J, Zhang Q, Aleman TS et al. (2001) Gene therapy restores vision in a canine model of childhood blindness. Nat Genet 28: 92-95. doi:10.1038/ng0501-92. PubMed: 11326284.