Distribution of SR protein exonic splicing enhancer motifs in human protein-coding genes

Nucleic Acids Research

Volumn 33, Issue 16, 2005, Pages 5053-5062

  Wang, Jinhua ^a   Smith, Philip J ^a   Krainer, Adrian R ^a   Zhang, Michael Q ^a  

^a Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; GENE PRODUCT; MESSENGER RNA; PROTEIN SR; UNCLASSIFIED DRUG; PROTEIN; RNA BINDING PROTEIN; RNA PRECURSOR;

ALTERNATIVE RNA SPLICING; AMINO ACID SEQUENCE; ARTICLE; COMPUTER PROGRAM; DNA FLANKING REGION; ENHANCER REGION; EXON; FREQUENCY ANALYSIS; GENETIC ANALYSIS; GENETIC CODE; GENETIC DATABASE; HUMAN; INTERNET; INTRON; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; RNA ANALYSIS; RNA SPLICING; SCORING SYSTEM; STATISTICAL ANALYSIS; STATISTICAL SIGNIFICANCE; BIOLOGY; CHEMISTRY; GENETICS; METABOLISM; REGULATORY RNA SEQUENCE; SEQUENCE ANALYSIS;

ALTERNATIVE SPLICING; COMPUTATIONAL BIOLOGY; EXONS; HUMANS; PROTEINS; REGULATORY SEQUENCES, RIBONUCLEIC ACID; RNA PRECURSORS; RNA SPLICE SITES; RNA SPLICING; RNA, MESSENGER; RNA-BINDING PROTEINS; SEQUENCE ANALYSIS, RNA; SOFTWARE;

EID: 24944433166     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gki810     Document Type: Article

References (58)

1. Hastings,M.L. and Krainer,A.R. (2001) Pre-mRNA splicing in the new millennium. Curr. Opin. Cell. Biol., 13, 302-309.
2. Sun,H. and Chasin,L.A. (2000) Multiple splicing defects in an intronic false exon. Mol. Cell. Biol., 20, 6414-6425.
3. Cartegni,L., Chew,S.L. and Krainer,A.R. (2002) Listening to silence and understanding nonsense: Exonic mutations that affect splicing. Nature Rev. Genet., 3, 285-298.
4. Blencowe,B.J. (2000) Exonic splicing enhancers: Mechanism of action, diversity and role in human genetic diseases. Trends Biochem. Sci., 25, 106-110.
5. Graveley,B.R. (2000) Sorting out the complexity of SR protein functions. RNA, 6, 1197-1211.
6. Birney,E., Kumar,S. and Krainer,A.R. (1993) Analysis of the RNA-recognition motif and RS and RGG domains: Conservation in metazoan pre-mRNA splicing factors. Nucleic Acids Res., 21, 5803-5816.
7. Shen,H., Kan,J.L. and Green,M.R. (2004) Arginine-serine-rich domains bound at splicing enhancers contact the branchpoint to promote prespliceosome assembly. Mol. Cell, 13, 367-376.
8. Shen,H. and Green,M.R. (2004) A pathway of sequential arginine-serine-rich domain-splicing signal interactions during mammalian spliceosome assembly. Mol. Cell, 16, 363-373.
9. Zuo,P. and Maniatis,T. (1996) The splicing factor U2AF35 mediates critical protein-protein interactions in constitutive and enhancer-dependent splicing. Genes Dev., 10, 1356-1368.
10. Graveley,B.R., Hertel,K.J. and Maniatis,T. (2001) The role of U2AF35 and U2AF65 in enhancer-dependent splicing. RNA, 7, 806-818.
11. Kan,J.L. and Green,M.R. (1999) Pre-mRNA splicing of IgM exons M1 and M2 is directed by a juxtaposed splicing enhancer and inhibitor. Genes Dev., 13, 462-471.
12. Krawczak,M., Reiss,J. and Cooper,D.N. (1992) The mutational spectrum of single base-pair substitutions in mRNA splice junctions of human genes: causes and consequences. Hum. Genet., 90, 41-54.
13. Liu,H.X., Cartegni,L., Zhang,M.Q. and Krainer,A.R. (2001) A mechanism for exon skipping caused by nonsense or missense mutations in BRCA1 and other genes. Nature Genet., 27, 55-58.
14. Cartegni,L. and Krainer,A.R. (2002) Disruption of an SF2/ASF-dependent exonic splicing enhancer in SMN2 causes spinal muscular atrophy in the absence of SMN1. Nature Genet., 30, 377-384.
15. Caputi,M., Kendzior,R.J.,Jr and Beemon,K.L. (2002) A nonsense mutation in the fibrillin-1 gene of a Marfan syndrome patient induces NMD and disrupts an exonic splicing enhancer. Genes Dev., 16, 1754-1759.
16. Aznarez,I., Chan,E.M., Zielenski,J., Blencowe,B.J. and Tsui,L.C. (2003) 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. Hum. Mol. Genet., 12, 2031-2040.
17. Colapietro,P., Gervasini,C., Natacci,F., Rossi,L., Riva,P. and Larizza,L. (2003) NF1 exon 7 skipping and sequence alterations in exonic splice enhancers (ESEs) in a neurofibromatosis 1 patient. Hum. Genet., 113, 551-554.
18. Pagani,F., Buratti,E., Stuani,C. and Baralle,F.E. (2003) Missense, nonsense, and neutral mutations define juxtaposed regulatory elements of splicing in cystic fibrosis transmembrane regulator exon 9. J. Biol. Chem., 278, 26580-26588.
19. Pagani,F., Stuani,C., Tzetis,M., Kanavakis,E., Efthymiadou,A., Doudounakis,S., Casals,T. and Baralle,F.E. (2003) New type of disease causing mutations: The example of the composite exonic regulatory elements of splicing in CFTR exon 12. Hum. Mol. Genet., 12, 1111-1120.
20. Ferrari,S., Giliani,S., Insalaco,A., Al-Ghonaium,A., Soresina,A.R., Loubser,M., Avanzini,M.A., Marconi,M., Badolato,R., Ugazio,A.G. et al. (2001) Mutations of CD40 gene cause an autosomal recessive form of immunodeficiency with hyper IgM. Proc. Natl Acad. Sci. USA, 98, 12614-12619.
21. Moseley,C., Mullis,P., Prince,M. and Phillips,J.,III (2002) An exon splice enhancer mutation causes autosomal dominant GH deficiency. J. Clin. Endocrinol. Metab., 87, 847-852.
22. Fackenthal,J.D., Cartegni,L., Krainer,A.R. and Olopade,O.I. (2002) BRCA2 T2722R is a deleterious allele that causes exon skipping. Am. J. Hum. Genet., 71, 625-631.
23. James,P.D., O'Brien,L.A., Hegadorn,C.A., Notley,C.R.P., Sinclair,G.D., Hough,C., Poon,M.-C. and Lillicrap,D. (2004) A novel type 2A von Willebrand factor mutation located at the last nucleotide of exon 26 (3538G>A) causes skipping of 2 nonadjacent exons. Blood, 104, 2739-2745.
24. Mas,C., Taske,N., Deutsch,S., Guipponi,M., Thomas,P., Covanis,A., Friis,M., Kjeldsen,M.J., Pizzolato,G.P., Villemure et al. (2004) Association of the connexin 36 gene with juvenile myocolonic epilepsy. J. Med. Genet., 41, e93.
25. Aretz,S., Uhlhaas,S., Sun,Y., Pagenstecher,C., Mangold,E., Caspari,R., Moslein,G., Schulmann,K., Propping,P. and Friedl,W. (2004) Familial adenomatous polyposis: Aberrant splicing due to missense or silent mutations in the APC gene. Hum. Mutat., 24, 370-380.
26. Zatkova,A., Messiaen,L., Vandenbroucke,I., Wieser,R., Fonatsch,C., Krainer,A.R. and Wimmer,K. (2004) Disruption of exonic splicing enhancer elements is the principal cause of exon skipping associated with seven nonsense or missense alleles of NF1. Hum. Mutat., 24, 491-501.
27. Coulter,L.R., Landree,M.A. and Cooper,T.A. (1997) Identification of a new class of exonic splicing enhancers by in vivo selection. Mol. Cell. Biol., 17, 2143-2150.
28. Tian,H. and Kole,R. (1995) Selection of novel exon recognition elements from a pool of random sequences. Mol. Cell. Biol., 15, 6291-6298.
29. Boukis,L.A. and Bruzik,J.P. (2001) Functional selection of splicing enhancers that stimulate trans-splicing in vitro. RNA, 7, 793-805.
30. Schaal,T.D. and Maniatis,T. (1999) Selection and characterization of pre-mRNA splicing enhancers: Identification of novel SR protein-specific enhancer sequences. Mol. Cell. Biol., 19, 1705-1719.
31. 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.
32. Liu,H.X., Chew,S.L., Cartegni,L., Zhang,M.Q. and Krainer,A.R. (2000) Exonic splicing enhancer motif recognized by human SC35 under splicing conditions. Mol. Cell. Biol., 20, 1063-1071.
33. Cartegni,L., Wang,J., Zhu,Z., Zhang,M.Q. and Krainer,A.R. (2003) ESEfinder: A web resource to identify exonic splicing enhancers. Nucleic Acids Res., 31, 3568-3571.
34. Gabut,M., Mine,M., Marsac,C., Brivet,M., Tazi,J. and Soret,J. (2005) The SR protein SC35 is responsible for aberrant splicing of the E1 alpha pyruvate dehydrogenase mRNA in a case of mental retardation with lactic acidosis. Mol. Cell. Biol., 25, 3286-3294.
35. Fairbrother,W.G., Yeh,R.F., Sharp,P.A. and Burge,C.B. (2002) Predictive identification of exonic splicing enhancers in human genes. Science, 297, 1007-1013.
36. Fairbrother,W.G., Yeo,G.W., Yeh,R., Goldstein,P., Mawson,M., Sharp,P.A. and Burge,C.B. (2004) Nucleic Acids Res., 32, W187-W190.
37. Zhang,X.H. and Chasin,L.A. (2004) Computational definition of sequence motifs governing constitutive exon splicing. Genes Dev., 18, 1241-1250.
38. Kasprzyk,A., Keefe,D., Smedley,D., London,D., Spooner,W., Melsopp,C., Hammond,M., Rocca-Serra,P., Cox,T. and Birney,E. (2004) EnsMart: A generic system for fast and flexible access to biological data. Genome Res., 14, 160-169.
39. Hubbard,T., Andrews,D., Caccamo,M., Cameron,G., Chen,Y., Clamp,M., Clarke,L., Coates,G., Cox,T., Cunningham,F. et al. (2004) Ensembl 2005. Nucleic Acids Res., 33, D447-D453.
40. Zhang,M.Q. (1997) Identification of protein coding regions in the human genome by quadratic discriminant analysis. Proc. Natl Acad. Sci. USA, 94, 565-568.
41. Schaal,T.D. and Maniatis,T. (1999) Multiple distinct splicing enhancers in the protein-coding sequences of a constitutively spliced pre-mRNA. Mol. Cell. Biol., 19, 261-273.
42. Mayeda,A., Screaton,G.R., Chandler,S.D., Fu,X.D. and Krainer,A.R. (1999) Substrate specificities of SR proteins in constitutive splicing are determined by their RNA recognition motifs and composite pre-mRNA exonic elements. Mol. Cell. Biol., 19, 1853-1863.
43. Lam,B.J. and Hertel,K.J. (2002) A general role for splicing enhancers in exon definition. RNA, 8, 1233-1241.
44. Ladd,A.N. and Cooper,T.A. (2002) Finding signals that regulate alternative splicing in the post-genomic era. Genome Biol., 3, reviews 0008.
45. Itoh,H., Washio,T. and Tomita,M. (2004) Computational comparative analyses of alternative splicing regulation using full-length cDNA of various eukaryotes. RNA, 10, 1005-1018.
46. Black,D.L. (2003) Mechanisms of alternative pre-messenger RNA splicing. Annu. Rev. Biochem., 72, 291-336.
47. Sironi,M., Menozzi,G., Riva,L., Cagliani,R., Comi,G.P., Bresolin,N., Giorda,R. and Pozzoli,U. (2004) Silencer elements as possible inhibitors of pseudoexon splicing. Nucleic Acids Res., 32, 1783-1791.
48. Selvakumar,M. and Helfman,D.M. (1999) Exonic splicing enhancers contribute to the use of both 3′ and 5′ splice site usage of rat beta-tropomyosin pre-mRNA. RNA, 5, 378-394.
49. Bourgeois,C.F., Popielarz,M., Hildwein,G. and Stévenin,J. (1999) Identification of a bidirectional splicing enhancer: Differential involvement of SR proteins in 5′ or 3′ splice site activation. Mol. Cell. Biol., 19, 7347-7356.
50. Tian,M. and Maniatis,T. (1994) A splicing enhancer exhibits both constitutive and regulated activities. Genes Dev., 8, 1703-1712.
51. Lorson,C.L. and Androphy,E.J. (2000) An exonic enhancer is required for inclusion of an essential exon in the SMA-determining gene SMN. Hum. Mol. Genet., 9, 259-265.
52. Hertel K.J. and Maniatis T. (1998), The function of multisite splicing enhancers. Mol. Cell, 1, 449-455.
53. Fairbrother,W.G., Holste,D., Burge,C.B. and Sharp,P.A. (2004) Single nucleotide polymorphism-based validation of exonic splicing enhancers. PLoS Biol., 2, E268.
54. Johnson,J.M., Castle,J., Garrett-Engele,P., Kan,Z., Loerch,P.M., Armour,C.D., Santos,R., Schadt,E.E., Stoughton,R. and Shoemaker,D.D. (2003) Genome-wide survey of human alternative pre-mRNA splicing with exon junction microarrays. Science, 302, 2141-2144.
55. Smith,C.W. and Valcárcel,J. (2000) Alternative pre-mRNA splicing: The logic of combinatorial control. Trends Biochem. Sci., 25, 381-388.
56. Stamm,S., Zhu,J., Nakai,K., Stoilov,P., Stoss,O. and Zhang,M.Q. (2000) An alternative-exon database and its statistical analysis. DNA Cell Biol., 19, 739-756.
57. Sorek,R. and Ast,G. (2003) Intronic sequences flanking alternatively spliced exons are conserved between human and mouse. Genome Res., 13, 1631-1637.
58. Philipps,D.L., Park,J.W. and Graveley,B.R. (2004) A computational and experimental approach toward a priori identification of alternatively spliced exons. RNA, 10, 1838-1844.