PRPF4 mutations cause autosomal dominant retinitis pigmentosa

Human Molecular Genetics

Volumn 23, Issue 11, 2014, Pages 2926-2939

  Chen, Xue ^a   Liu, Yuan ^a   Sheng, Xunlun ^b   Tam, Pancy O S ^c   Zhao, Kanxing ^d   Chen, Xuejuan ^a   Rong, Weining ^b   Liu, Yani ^b   Liu, Xiaoxing ^a   Pan, Xinyuan ^a   Chen, Li Jia ^c   Zhao, Qingshun ^e   Vollrath, Douglas ^f   Pang, Chi Pui ^c   Zhao, Chen ^a  

^a THE FIRST AFFILIATED HOSPITAL OF NANJING MEDICAL UNIVERSITY   (China)

^b Ningxia People's Hospital   (China)

^c CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^d TIANJIN MEDICAL UNIVERSITY   (China)

^e NANJING UNIVERSITY   (China)

^f STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; AGED; ARTICLE; AUTOSOMAL DOMINANT DISORDER; FEMALE; GENE; GENE MUTATION; HAPLOINSUFFICIENCY; HETEROZYGOTE; HUMAN; LUCIFERASE ASSAY; MAJOR CLINICAL STUDY; MALE; PEDIGREE; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PRPF4 GENE; RETINITIS PIGMENTOSA; ZEBRA FISH; ADOLESCENT; AMINO ACID SEQUENCE; CHEMISTRY; CHILD; DOMINANT GENE; DOWN REGULATION; GENETICS; METABOLISM; MIDDLE AGED; MISSENSE MUTATION; MOLECULAR GENETICS; SEQUENCE ALIGNMENT; YOUNG ADULT;

PRPF4 PROTEIN, HUMAN; SMALL NUCLEAR RIBONUCLEOPROTEIN;

ADOLESCENT; ADULT; AGED; AMINO ACID SEQUENCE; CHILD; DOWN-REGULATION; FEMALE; GENES, DOMINANT; HUMANS; MALE; MIDDLE AGED; MOLECULAR SEQUENCE DATA; MUTATION, MISSENSE; PEDIGREE; PROMOTER REGIONS, GENETIC; RETINITIS PIGMENTOSA; RIBONUCLEOPROTEIN, U4-U6 SMALL NUCLEAR; SEQUENCE ALIGNMENT; YOUNG ADULT;

EID: 84899915430     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddu005     Document Type: Article

References (54)

1. Carrillo, J., Martinez, P., Solera, J., Moratilla, C., Gonzalez, A., Manguan-Garcia, C., Aymerich, M., Canal, L., Del Campo, M., Dapena, J.L. et al. (2012) High resolution melting analysis for the identification of novel mutations inDKC1andTERTgenes in patients with dyskeratosis congenita. Blood Cells Mol. Dis., 49, 140-146.
2. Chizzolini, M., Galan, A., Milan, E., Sebastiani, A., Costagliola, C. and Parmeggiani, F. (2011)Goodepidemiologic practice in retinitis pigmentosa: from phenotyping to biobanking. Curr. Genomics, 12, 260-266.
3. Collin, R.W., Safieh, C., Littink, K.W., Shalev, S.A., Garzozi, H.J., Rizel, L., Abbasi, A.H., Cremers, F.P., den Hollander, A.I., Klevering, B.J. et al. (2010) Mutations in C2ORF71 cause autosomal-recessive retinitis pigmentosa. Am. J. Hum. Genet., 86, 783-788.
4. Hartong, D.T., Berson, E.L. and Dryja, T.P. (2006) Retinitis pigmentosa. Lancet, 368, 1795-1809.
5. McKie, A.B., McHale, J.C., Keen, T.J., Tarttelin, E.E., Goliath, R., van Lith-Verhoeven, J.J., Greenberg, J., Ramesar, R.S., Hoyng, C.B., Cremers, F.P. et al. (2001) Mutations in the pre-mRNA splicing factor gene PRPC8 in autosomal dominant retinitis pigmentosa (RP13). Hum. Mol. Genet., 10, 1555-1562.
6. Vithana, E.N., Abu-Safieh, L., Allen, M.J., Carey, A., Papaioannou, M., Chakarova, C., Al-Maghtheh, M., Ebenezer, N.D., Willis, C., Moore, A.T. et al. (2001) A human homolog of yeast pre-mRNA splicing gene, PRP31, underlies autosomal dominant retinitis pigmentosa on chromosome 19q13.4 (RP11). Mol. Cell, 8, 375-381.
7. Chakarova, C.F., Hims, M.M., Bolz, H., Abu-Safieh, L., Patel, R.J., Papaioannou, M.G., Inglehearn, C.F., Keen, T.J., Willis, C., Moore, A.T. et al. (2002) Mutations in HPRP3, a third member of pre-mRNA splicing factor genes, implicated in autosomal dominant retinitis pigmentosa. Hum. Mol. Genet., 11, 87-92.
8. Keen, T.J., Hims, M.M., McKie, A.B., Moore, A.T., Doran, R.M., Mackey, D.A., Mansfield, D.C., Mueller, R.F., Bhattacharya, S.S., Bird, A.C. et al. (2002) Mutations in a protein target of the Pim-1 kinase associated with the RP9 form of autosomal dominant retinitis pigmentosa. Eur. J. Hum. Genet., 10, 245-249.
9. Zhao, C., Bellur, D.L., Lu, S., Zhao, F., Grassi, M.A., Bowne, S.J., Sullivan, L.S., Daiger, S.P., Chen, L.J., Pang, C.P. et al. (2009) Autosomal-dominant retinitis pigmentosa caused by a mutation in SNRNP200, a gene required for unwinding of U4/U6 snRNAs. Am. J. Hum. Genet., 85, 617-627.
10. Li, N., Mei, H., MacDonald, I.M., Jiao, X. and Hejtmancik, J.F. (2010) Mutations in ASCC3L1 on 2q11.2 are associated with autosomal dominant retinitis pigmentosa in a Chinese family. Invest. Ophthalmol. Vis. Sci., 51, 1036-1043.
11. Tanackovic, G., Ransijn, A., Ayuso, C., Harper, S., Berson, E.L. and Rivolta, C. (2011) A missense mutation in PRPF6 causes impairment of pre-mRNA splicing and autosomal-dominant retinitis pigmentosa. Am. J. Hum. Genet., 88, 643-649.
12. Liu, S., Rauhut, R., Vornlocher, H.P. and Luhrmann, R. (2006) The network of protein-protein interactions within the human U4/U6.U5 tri-snRNP. RNA, 12, 1418-1430.
13. Wahl, M.C., Will, C.L. and Luhrmann, R. (2009) The spliceosome: design principles of a dynamic RNP machine. Cell, 136, 701-718.
14. Cheng, S.C. and Abelson, J. (1987) Spliceosome assembly in yeast. Genes Dev., 1, 1014-1027.
15. Lamond, A.I., Konarska, M.M., Grabowski, P.J. and Sharp, P.A. (1988) Spliceosome assembly involves the binding and release of U4 small nuclear ribonucleoprotein. Proc. Natl. Acad. Sci. U S A, 85, 411-415.
16. Pikielny, C.W., Rymond, B.C. and Rosbash, M. (1986) Electrophoresis of ribonucleoproteins reveals an ordered assembly pathway of yeast splicing complexes. Nature, 324, 341-345.
17. Chen, X., Zhao, K., Sheng, X., Li, Y., Gao, X., Zhang, X., Kang, X., Pan, X., Liu, Y., Jiang, C. et al. (2013) Targeted sequencing of 179 genes associated with hereditary retinal dystrophies and 10 candidate genes identifies novel and known mutations in patients with various retinal diseases. Invest. Ophthalmol. Vis. Sci., 54, 2186-2197.
18. Lauber, J., Plessel, G., Prehn, S., Will, C.L., Fabrizio, P., Groning, K., Lane, W.S. and Luhrmann, R. (1997) The human U4/U6 snRNP contains 60 and 90 kD proteins that are structurally homologous to the yeast splicing factors Prp4p and Prp3p. RNA, 3, 926-941.
19. Wang,A., Forman-Kay, J., Luo, Y., Luo, M.,Chow,Y.H., Plumb, J., Friesen, J.D., Tsui, L.C., Heng, H.H., Woolford, J.L. Jr. et al. (1997) Identification and characterization of human genes encoding Hprp3p and Hprp4p, interacting components of the spliceosome. Hum. Mol. Genet., 6, 2117-2126.
20. Horowitz, D.S., Kobayashi, R. and Krainer, A.R. (1997) A new cyclophilin and the human homologues of yeast Prp3 and Prp4 form a complex associated with U4/U6 snRNPs. RNA, 3, 1374-1387.
21. Gonzalez-Santos, J.M., Wang, A., Jones, J., Ushida, C., Liu, J. and Hu, J. (2002) Central region of the human splicing factor Hprp3p interacts with Hprp4p. J. Biol. Chem., 277, 23764-23772.
22. Kojima, T., Zama, T., Wada, K., Onogi, H. and Hagiwara,M.(2001) Cloning of human PRP4 reveals interaction with Clk1. J. Biol. Chem., 276, 32247-32256.
23. Trede, N.S., Medenbach, J., Damianov, A., Hung, L.H., Weber, G.J., Paw, B.H., Zhou, Y., Hersey, C., Zapata, A., Keefe, M. et al. (2007) Network of coregulated spliceosome components revealed by zebrafish mutant in recycling factor p110. Proc. Natl. Acad. Sci. USA, 104, 6608-6613.
24. Linder, B., Dill, H., Hirmer, A., Brocher, J., Lee, G.P., Mathavan, S., Bolz, H.J., Winkler, C., Laggerbauer, B. and Fischer, U. (2011) Systemic splicing factor deficiency causes tissue-specific defects: a zebrafish model for retinitis pigmentosa. Hum. Mol. Genet., 20, 368-377.
25. Krainer, A.R., Conway, G.C. and Kozak, D. (1990) The essential pre-mRNA splicing factor SF2 influences 5 ' splice site selection by activating proximal sites. Cell, 62, 35-42.
26. Zhang, Z., Lotti, F., Dittmar, K., Younis, I., Wan, L., Kasim, M. and Dreyfuss, G. (2008) SMN deficiency causes tissue-specific perturbations in the repertoire ofsnRNAsand widespread defects in splicing. Cell, 133, 585-600.
27. Cao, H., Wu, J., Lam, S., Duan, R., Newnham, C., Molday, R.S., Graziotto, J.J., Pierce, E.A. and Hu, J. (2011) Temporal and tissue specific regulation of RP-associated splicing factor genes PRPF3, PRPF31 and PRPC8-implications in the pathogenesis of RP. PLoS One, 6, e15860.
28. Abu-Safieh, L., Vithana, E.N., Mantel, I., Holder, G.E., Pelosini, L., Bird, A.C. and Bhattacharya, S.S. (2006) A large deletion in the adRP gene PRPF31: evidence that haploinsufficiency is the cause of disease. Mol. Vis., 12, 384-388.
29. Rio Frio, T., Civic, N., Ransijn, A., Beckmann, J.S. and Rivolta, C. (2008) Two trans-acting eQTLs modulate the penetrance of PRPF31 mutations. Hum. Mol. Genet., 17, 3154-3165.
30. Saini, S., Robinson, P.N., Singh, J.R. and Vanita, V. (2012) A novel 7 bp deletion in PRPF31 associated with autosomal dominant retinitis pigmentosa with incomplete penetrance in an Indian family. Exp. Eye Res., 104, 82-88.
31. Venturini, G., Rose, A.M., Shah, A.Z., Bhattacharya, S.S. and Rivolta, C. (2012) CNOT3 is a modifier of PRPF31 mutations in retinitis pigmentosa with incomplete penetrance. PLoS Genet., 8, e1003040.
32. Graziotto, J.J., Inglehearn, C.F., Pack, M.A. and Pierce, E.A. (2008) Decreased levels of the RNA splicing factor Prpf3 in mice and zebrafish do not cause photoreceptor degeneration. Invest. Ophthalmol. Vis. Sci., 49, 3830-3838.
33. Yin, J., Brocher, J., Fischer, U. and Winkler, C. (2011) Mutant Prpf31 causes pre-mRNA splicing defects and rod photoreceptor cell degeneration in a zebrafish model for retinitis pigmentosa. Mol. Neurodegener., 6, 56.
34. Ayadi, L., Callebaut, I., Saguez, C., Villa, T., Mornon, J.P. and Banroques, J. (1998) Functional and structural characterization of the prp3 binding domain of the yeast prp4 splicing factor. J. Mol. Biol., 284, 673-687.
35. Zhang, W.J. and Wu, J.Y. (1996) Functional properties of p54, a novel SR protein active in constitutive and alternative splicing. Mol. Cell. Biol., 16, 5400-5408.
36. Huranova, M., Ivani, I., Benda, A., Poser, I., Brody, Y., Hof, M., Shav-Tal, Y., Neugebauer, K.M. and Stanek, D. (2010) The differential interaction of snRNPs with pre-mRNA reveals splicing kinetics in living cells. J. Cell. Biol., 191, 75-86.
37. Tanackovic, G., Ransijn, A., Thibault, P.,Abou Elela, S., Klinck, R., Berson, E.L., Chabot, B. and Rivolta, C. (2011) PRPF mutations are associated with generalized defects in spliceosome formation and pre-mRNA splicing in patients with retinitis pigmentosa. Hum. Mol. Genet., 20, 2116-2130.
38. Raghunathan, P.L. and Guthrie, C. (1998) RNA unwinding in U4/U6 snRNPs requires ATP hydrolysis and the DEIH-box splicing factor Brr2. Curr. Biol., 8, 847-855.
39. van Nues, R.W. and Beggs, J.D. (2001) Functional contacts with a range of splicing proteins suggest a central role for Brr2p in the dynamic control of the order of events in spliceosomes of Saccharomyces cerevisiae. Genetics, 157, 1451-1467.
40. Nguyen, T.H., Li, J., Galej, W.P., Oshikane, H.,Newman, A.J. and Nagai, K. (2013) Structural basis of Brr2-Prp8 interactions and implications for U5 snRNP biogenesis and the spliceosome active site. Structure, 21, 910-919.
41. Yuan, L., Kawada, M., Havlioglu, N., Tang, H. and Wu, J.Y. (2005) Mutations in PRPF31 inhibit pre-mRNA splicing of rhodopsin gene and cause apoptosis of retinal cells. J. Neurosci., 25, 748-757.
42. Wilkie, S.E., Vaclavik, V., Wu, H., Bujakowska, K., Chakarova, C.F., Bhattacharya, S.S., Warren, M.J. and Hunt, D.M. (2008) Disease mechanism for retinitis pigmentosa (RP11) caused by missense mutations in the splicing factor gene PRPF31. Mol. Vis., 14, 683-690.
43. Zhao, C., Lu, S., Zhou, X., Zhang, X., Zhao, K. and Larsson, C. (2006) A novel locus (RP33) for autosomal dominant retinitis pigmentosa mapping to chromosomal region 2cen-q12.1. Hum. Genet., 119, 617-623.
44. Demirci, F.Y., Rigatti, B.W., Wen, G., Radak, A.L., Mah, T.S., Baic, C.L., Traboulsi, E.I., Alitalo, T., Ramser, J. and Gorin, M.B. (2002) X-linked cone-rod dystrophy (locus COD1): identification of mutations in RPGR exon ORF15. Am. J. Hum. Genet., 70, 1049-1053.
45. Meindl, A., Dry, K., Herrmann, K., Manson, F., Ciccodicola, A., Edgar, A., Carvalho, M.R., Achatz, H., Hellebrand, H., Lennon,A. et al. (1996)Agene (RPGR) with homology to the RCC1 guanine nucleotide exchange factor is mutated in X-linked retinitis pigmentosa (RP3). Nat. Genet., 13, 35-42.
46. Messeguer, X., Escudero, R., Farre, D., Nunez, O., Martinez, J. and Alba, M.M.(2002)PROMO:detection ofknowntranscription regulatory elements using species-tailored searches. Bioinformatics, 18, 333-334.
47. Farre, D., Roset, R., Huerta, M., Adsuara, J.E., Rosello, L., Alba, M.M. and Messeguer, X. (2003) Identification of patterns in biological sequences at the ALGGEN server: PROMO and MALGEN. Nucleic Acids. Res., 31, 3651-3653.
48. Arnold, K., Bordoli, L., Kopp, J. and Schwede, T. (2006) The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics, 22, 195-201.
49. Kiefer, F., Arnold, K., Kunzli, M., Bordoli, L. and Schwede, T. (2009) The SWISS-MODEL Repository and associated resources. Nucleic Acids. Res., 37, D387-D392.
50. Livak, K.J. and Schmittgen, T.D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods, 25, 402-408.
51. Rittie, L. and Fisher, G.J. (2005) Isolation and culture of skin fibroblasts. Methods Mol. Med., 117, 83-98.
52. Pinsonneault, J., Nielsen, C.U. and Sadee, W. (2004) Genetic variants of the humanH+/dipeptide transporter PEPT2: analysis of haplotype functions. J. Pharmacol. Exp. Ther., 311, 1088-1096.
53. Ho, S.N., Hunt, H.D., Horton, R.M., Pullen, J.K. and Pease, L.R. (1989) Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene, 77, 51-59.
54. Horton, R.M., Cai, Z.L., Ho, S.N. and Pease, L.R. (1990) Gene splicing by overlap extension: tailor-made genes using the polymerase chain reaction. Biotechniques, 8, 528-535.