Characterization of disease-associated mutations affecting an exonic splicing enhancer and two cryptic splice sites in exon 13 of the cystic fibrosis transmembrane conductance regulator gene

Human Molecular Genetics

Volumn 12, Issue 16, 2003, Pages 2031-2040

  Aznarez, Isabel ^a,b   Chan, Elayne M ^a,b   Zielenski, Julian ^a   Blencowe, Benjamin J ^b   Tsui, Lap Chee ^a,b,c  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; PYRIMIDINE DERIVATIVE; TRANSMEMBRANE CONDUCTANCE REGULATOR;

ANIMAL CELL; CLINICAL ARTICLE; CONTROLLED STUDY; CYSTIC FIBROSIS; DISEASE ASSOCIATION; DISEASE SEVERITY; ENHANCER REGION; EXON; GENE CONSTRUCT; GENE DELETION; GENE FUNCTION; GENE MUTATION; GENETIC DISORDER; HUMAN; HUMAN CELL; MODULATION; NONHUMAN; PREDICTION; PRIORITY JOURNAL; REVIEW; RNA SPLICING; SEQUENCE ANALYSIS;

ANIMALS; BASE SEQUENCE; COS CELLS; CYSTIC FIBROSIS; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; ENHANCER ELEMENTS (GENETICS); EXONS; HUMANS; MUTATION; NUCLEAR PROTEINS; PLASMIDS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA PRECURSORS; RNA SPLICE SITES; RNA SPLICING; TRANS-ACTIVATORS; TRANSFECTION;

ANIMALIA;

EID: 0042420388     PISSN: 09646906     EISSN: None     Source Type: Journal    
DOI: 10.1093/hmg/ddg215     Document Type: Review

References (51)

1. Welsh, M., Tsui, L.-C., Boat, T.F. and Beaudet, A.L. (1995) Cystic fibrosis. In Scriver, R.S., Beaudet, A.L., Sly, W.S. and Valle, D. (eds), The Metabolic and Molecular Bases of Inherited Disease. McGraw-Hill, Inc. New York, pp. 3799-3876.
2. Holsclaw, D.S., Perlmutter, A.D., Jockin, H. and Shwachman, H. (1971) Genital abnormalities in male patients with cystic fibrosis. J. Urol., 106, 568-574.
3. Zielenski, J. and Tsui, L.-C. (1995) Cystic fibrosis: genotypic and phenotypic variations. Annu. Rev. Genet., 29, 777-807.
4. Zielenski, J. (2000) Genotype and phenotype in cystic fibrosis. Respiration, 67, 117-133.
5. Rommens, J.M., Iannuzzi, M.C., Kerem, B., Drumm, M.L., Melmer, G., Dean, M., Rozmahel, R., Cole, J.L., Kennedy, D. and Hidaka N. (1989) Identification of the cystic fibrosis gene: chromosome walking and jumping. Science, 245, 1059-1065.
6. Riordan, J.R., Rommens, J.M., Kerem, B., Alon, N., Rozmahel, R., Grzelczak, Z., Zielenski, J., Lok, S., Plavsic, N. and Chou, J.L. (1989) Identification of the cystic fibrosis gene: cloning and characterization of complementary DNA. Science, 245, 1066-1073.
7. Kerem, B., Rommens, J.M., Buchanan, J.A., Markiewicz, D., Cox, T.K., Chakravarti, A., Buchwald, M. and Tsui, L.-C. (1989) Identification of the cystic fibrosis gene: genetic analysis. Science, 245, 1073-1080.
8. Zielenski, J., Rozmahel, R., Bozon, D., Kerem, B., Grzelczak, Z., Riordan, J.R., Rommens, J. and Tsui, L.-C. (1991) Genomic DNA sequence of the cystic fibrosis transmembrane conductance regulator (CFTR) gene. Genomics, 10, 214-228.
9. Chiba-Falek, O., Kerem, E., Shoshani, T., Aviram, M., Augarten, A., Bentur, L., Tal, A., Tullis, E., Rahat, A. and Kerem, B. (1998) The molecular basis of disease variability among cystic fibrosis patients carrying the 3849 + 10 kb C→T mutation. Genomics, 53, 276-283.
10. Zielenski, J., Patrizio, P., Corey, M., Handelin, B., Markiewicz, D., Asch, R. and Tsui, L.-C. (1995) CFTR gene variant for patients with congenital absence of vas deferens. Am. J. Hum. Genet., 57, 958-960.
11. Chiba-Falek, O., Parad, R.B., Kerem, E. and Kerem, B. (1999) Variable levels of normal RNA in different fetal organs carrying a cystic fibrosis transmembrane conductance regulator splicing mutation. Am. J. Respir Crit. Care Med., 159, 1998-2002.
12. Nissim-Rafinia, M., Chiba-Falek, O., Sharon, G., Boss, A. and Kerem, B. (2000) Cellular and viral splicing factors can modify the splicing pattern of CFTR transcripts carrying splicing mutations. Hum. Mol. Genet., 9, 1771-1778.
13. Pagani, F., Buratti, E., Stuani, C., Romano, M., Zuccato, E., Niksic, M., Giglio, L., Faraguna, D. and Baralle, F.E. (2000) Splicing factors induce cystic fibrosis transmembrane regulator exon 9 skipping through a nonevolutionary conserved intronic element. J. Biol. Chem., 275, 21041-21047.
14. Newman, A. (1998) RNA splicing. Curr. Biol., 8, R903-R905.
15. Cartegni, L., Chew, S.L. and Krainer, A.R. (2002) Listening to silence and understanding nonsense: exonic mutations that affect splicing. Nat. Rev. Genet., 3, 285-298.
16. Graveley, B.R. (2000) Sorting out the complexity of SR protein functions. RNA, 6, 1197-1211.
17. Nissim-Rafinia, M. and Kerem, B. (2002) Splicing regulation as a potential genetic modifier. Trends Genet., 18, 123-127.
18. Zielenski, J., Aznarez, I., Onay, T., Tzounzouris, J., Markiewicz, D. and Tsui, L.-C. (2002) CFTR mutation detection by multiplex heteroduplex (mHET) analysis on MDE gel. In Skach, W. (ed.). Cystic Fibrosis Methods and Protocols, in Methods in Molecular Medicine Series. The Humana Press, Totowa NJ, 70, pp. 3-19.
19. Zielenski, J., Bozon, D., Markiewicz, D., Aubin, G., Simard, F., Rommens, J.M. and Tsui, L.-C. (1993) Analysis of CFTR transcripts in nasal epithelial cells and lymphoblasts of a cystic fibrosis patient with 621 + 1G→T and 711 + 1G→T mutations. Hum. Mol. Genet., 2, 683-687.
20. Shapiro, M.B. and Senapathy, P. (1987) RNA splice junctions of different classes of eukaryotes: sequence statistics and functional implications in gene expression. Nucl. Acids Res., 15, 7155-7174.
21. Hull, J., Shackleton, S. and Harris, A. (1994) Analysis of mutations and alternative splicing patterns in the CFTR gene using mRNA derived from nasal epithelial cells. Hum. Mol. Genet., 3, 1141-1146.
22. Yeakley, J.M., Morfin, J.P., Rosenfeld, M.G. and Fu, X.D. (1996) A complex of nuclear proteins mediates SR protein binding to a purine-rich splicing enhancer. Proc. Natl Acad. Sci. USA, 93, 7582-7587.
23. Liu, H.X., Zhang, M. and Krainer, A.R. (1998) Identification of functional exonic splicing enhancer motifs recognized by individual SR proteins. Genes Dev., 12, 1998-2012.
24. Tacke, R., Tohyama, M., Ogawa, S. and Manley, J.L. (1998) Human Tra2 proteins are sequence-specific activators of pre-mRNA splicing. Cell, 93, 139-148.
25. Staffa, A. and Cochrane, A. (1994) The tat/rev intron of human immunodeficiency virus type 1 is inefficiently spliced because of suboptimal signals in the 3′ splice site. J. Virol., 68, 3071-3079.
26. Cramer, P., Caceres, J.F., Cazalla, D., Kadener, S., Muro, A.F., Baralle, F.E. and Kornblihtt, A.R. (1999) Coupling of transcription with alternative splicing: RNA pol II promoters modulate SF2/ASF and 9G8 effects on an exonic splicing enhancer. Mol. Cell., 4, 251-258.
27. Wong, L.J., Wang, J., Zhang, Y.H., Hsu, E., Heim, R.A., Bowman, C.M. and Woo, M.S. (2001) Improved detection of CFTR mutations in Southern California Hispanic CF patients. Hum. Mutat., 18, 296-307.
28. Eldridge, A.G., Li, Y., Sharp, P.A. and Blencowe, B.J. (1999) The SRm160/300 splicing coactivator is required for exon-enhancer function. Proc. Natl Acad. Sci. USA, 96, 6125-6130.
29. Hofmann, Y., Lorson, C.L., Stamm, S., Androphy, E.J. and Wirth, B. (2000) Htra2-beta 1 stimulates an exonic splicing enhancer and can restore full-length SMN expression to survival motor neuron 2 (SMN2). Proc. Natl Acad. Sci. USA, 97, 9618-9623.
30. Dirksen, W.P., Li, X., Mayeda, A., Krainer, A.R. and Rottman, F.M. (2000) Mapping the SF2/ASF binding sites in the bovine growth hormone exonic splicing enhancer. J. Biol. Chem., 275, 29170-29177.
31. Mercier, B., Raguenes, O., Estivill, X., Morral, N., Kaplan, G.C., McClure, M., Grebe, T.A., Kessler, D., Pignatti, P.F., Marigo, C. et al. (1994) Complete detection of mutations in cystic fibrosis patients of Native American origin. Hum. Genet., 94, 629-632.
32. Bombieri, C., Benetazzo, M., Saccomani, A., Belpinati, F., Gile, L.S., Luisetti, M. and Pignatti, P.F. (1998) Complete mutational screening of the CFTR gene in 120 patients with pulmonary disease. Hum. Genet., 103, 718-722.
33. Clavel, C., Pennaforte, F., Pigeon, F., Verlingue, C., Birembaut, P. and Ferec, C. (1997) Identification of four novel mutations in the cystic fibrosis transmembrane conductance regulator gene: E664X, 2113delA, 306delTAGA, and delta M1140. Hum. Mutat., 9, 368-369.
34. Chen, J.M., Cutler, C., Jacques, C., Boeuf, G., Denamur, E., Lecointre, G., Mercier, B., Cramb, G. and Ferec, C. (2001) A combined analysis of the cystic fibrosis transmembrane conductance regulator: implications for structure and disease models. Mol. Biol. Evol., 18, 1771-1788.
35. Ge, H. and Manley, J.L. (1990) A protein factor, ASF, controls cell-specific alternative splicing of SV40 early pre-mRNA in vitro. Cell, 62, 25-34.
36. Krainer, A.R., Mayeda, A., Kozak, D. and Binns, G. (1991) Functional expression of cloned human splicing factor SF2: homology to RNA-binding proteins, U1 70K, and Drosophila splicing regulators. Cell, 66, 383-394.
37. Li, Y. and Blencowe, B.J. (1999) Distinct factor requirements for exonic splicing enhancer function and binding of U2AF to the polypyrimidine tract. J. Biol. Chem., 274, 35074-35079.
38. Sun, Q., Mayeda, A., Hampson, R.K., Krainer, A.R. and Rottman, F.M. (1993) General splicing factor SF2/ASF promotes alternative splicing by binding to an exonic splicing enhancer. Genes Dev., 7, 2598-2608.
39. Groman, J.D., Meyer, M.E., Wilmott, R.W., Zeitlin, P.L. and Cutting, G.R. (2002) Variant cystic fibrosis phenotypes in the absence of CFTR mutations. N. Engl. J. Med., 347, 401-407.
40. Vankeerberghen, A., Wei, L., Jaspers, M., Cassiman, J.J., Nilius, B. and Cuppens, H. (1998) Characterization of 19 disease-associated missense mutations in the regulatory domain of the cystic fibrosis transmembrane conductance regulator. Hum. Mol. Genet., 7, 1761-1769.
41. Keeling, K.M. and Bedwell, D.M. (2002) Clinically relevant aminoglycosides can suppress disease-associated premature stop mutations in the IDUA and P53 cDNAs in a mammalian translation system. J. Mol. Med., 80, 367-376.
42. Chang, J.G., Hsieh-Li, H.M., Jong, Y.J., Wang, N.M., Tsai, C.H. and Li, H. (2001) Treatment of spinal muscular atrophy by sodium butyrate. Proc. Natl Acad Sci. USA, 98, 9808-9813.
43. Cartegni, L. and Krainer, A.R. (2003) Correction of disease-associated exon skipping by synthetic exon-specific activators. Nat. Struct. Biol., 10, 120-125.
44. Skordis, L.A., Dunckley, M.G., Yue, B., Eperon, I.C. and Muntoni, F. (2003) Bifunctional antisense oligonucleotides provide a trans-acting splicing enhancer that stimulates SMN2 gene expression in patient fibroblasts. Proc. Natl Acad. Sci. USA, 100, 4114-4119.
45. Blencowe, B.J. (2000) Exonic splicing enhancers: mechanism of action, diversity and role in human genetic diseases. Trends Biochem. Sci., 25, 106-110.
46. Caceres, J.F. and Kornblihtt, A.R. (2002) Alternative splicing: multiple control mechanisms and involvement in human disease. Trends Genet., 18, 186-193.
47. Faustino, N.A. and Cooper, T.A. (2003) Pre-mRNA splicing and human disease. Genes Dev., 17, 419-437.
48. Rozmahel, R., Wilschanski, M., Matin, A., Plyte, S., Oliver, M., Auerbach, W., Moore, A., Forstner, J., Durie, P., Nadeau, J. et al. (1996) Modulation of disease severity in cystic fibrosis transmembrane conductance regulator deficient mice by a secondary genetic factor. Nat. Genet., 12, 280-287.
49. Zielenski, J., Corey, M., Rozmahel, R., Markiewicz, D., Aznarez, I., Casals, T., Larriba, S., Mercier, B., Cutting, G.R., Krebsova, A. et al. (1999) Detection of a cystic fibrosis modifier locus for meconium ileus on human chromosome 19q13. Nat. Genet., 22, 128-129.
50. 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.
51. Slomski, R., Schloesser, M., Berg, L.P., Wagner, M., Kakkar, V.V., Cooper, D.N. and Reiss, J. (1992) Omission of exon 12 in cystic fibrosis transmembrane conductance regulator (CFTR) gene transcripts. Hum. Genet., 89, 615-619.