Evidence for purifying selection against synonymous mutations in mammalian exonic splicing enhancers

Molecular Biology and Evolution

Volumn 23, Issue 2, 2006, Pages 301-309

  Parmley, Joanna L ^a   Chamary, J V ^a   Hurst, Laurence D ^a  

^a University of Bath   (United Kingdom)

Author keywords

Codon usage bias; Mutation rate; Purifying selection; Splicing; Synonymous sites

Indexed keywords

AMINO ACID SUBSTITUTION; ARTICLE; EVOLUTION; EXON; GENETIC VARIABILITY; INTRON; MUTATION; RNA SPLICING; SINGLE NUCLEOTIDE POLYMORPHISM;

ALTERNATIVE SPLICING; ANIMALS; EVOLUTION, MOLECULAR; EXONS; HUMANS; INTRONS; MICE; MUTATION; POLYMORPHISM, SINGLE NUCLEOTIDE; SELECTION (GENETICS);

MAMMALIA;

EID: 30744469841     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msj035     Document Type: Article

References (62)

1. Akashi, H., and A. Eyre-Walker. 1998. Translational selection and molecular evolution. Curr. Opin. Genet. Dev. 8:688-693.
2. Bird, A. P. 1980. DNA methylation and the frequency of CpG in animal DNA. Nucleic Acids Res. 8:1499-1504.
3. Blencowe, B. J. 2000. Exonic splicing enhancers: mechanism of action, diversity and role in human genetic diseases. Trends Biochem. Sci. 25:106-110.
4. Bulmer, M., K. H. Wolfe, and P. M. Sharp. 1991. Synonymous nucleotide substitution rates in mammalian genes: implications for the molecular clock and the relationship of mammalian orders. Proc. Natl. Acad. Sci. USA 88:5974-5978.
5. Bustamante, C. D., R. Nielsen, and D. L. Hartl. 2002. A maximum likelihood method for analyzing pseudogene evolution: implications for silent site evolution in humans and rodents. Mol. Biol. Evol. 19:110-117.
6. Capon, F., M. H. Allen, M. Ameen, A. D. Burden, D. Tillman, J. N. Barker, and R. C. Trembath. 2004. A synonymous SNP of the corneodesmosin gene leads to increased mRNA stability and demonstrates association with psoriasis across diverse ethnic groups. Hum. Mol. Genet. 13:2361-2368.
7. Carlini, D. B., and J. E. Genut. 2005. Synonymous SNPs provide evidence for selective constraint on human exonic splicing enhancers. J. Mol. Evol. (in press).
8. Chamary, J. V., and L. D. Hurst. 2004. Similar rates but different modes of sequence evolution in introns and at exonic silent sites in rodents: evidence for selectively driven codon usage. Mol. Biol. Evol. 21:1014-1023.
9. _. 2005a. Biased codon usage near intron-exon junctions: selection on splicing enhancers, splice-site recognition or something else? Trends Genet. 21:256-259.
10. _. 2005b. Evidence for selection on synonymous mutations affecting stability of mRNA secondary structure in mammals. Genome Biol. 6:R75.
11. Clark, A. G., S. Glanowski, R. Nielsen et al. (17 co-authors). 2003. Inferring nonneutral evolution from human-chimp-mouse orthologous gene trios. Science 302:1960-1963.
12. Comeron, J. M. 2004. Selective and mutational patterns associated with gene expression in humans: influences on synonymous composition and intron presence. Genetics 167:1293-1304.
13. Cooper, D. N., and M. Krawczak. 1989. Cytosine methylation and the fate of CpG dinucleotides in vertebrate genomes. Hum. Genet. 83:181-188.
14. Coulter, L. R., M. A. Landree, and T. A. Cooper. 1997. Identification of a new class of exonic splicing enhancers by in vivo selection. Mol. Cell. Biol. 17:2143-2150.
15. dos Reis, M., R. Savva, and L. Wernisch. 2004. Solving the riddle of codon usage preferences: a test for translational selection. Nucleic Acids Res. 32:5036-5044.
16. Duan, J., and M. A. Antezana. 2003. Mammalian mutation pressure, synonymous codon choice, and mRNA degradation. J. Mol. Evol. 57:694-701.
17. Duan, J., M. S. Wainwright, J. M. Comeron, N. Saitou, A. R. Sanders, J. Gelernter, and P. V. Gejman. 2003. Synonymous mutations in the human dopamine receptor D2 (DRD2) affect mRNA stability and synthesis of the receptor. Hum. Mol. Genet. 12:205-216.
18. Duret, L. 2002. Evolution of synonymous codon usage in metazoans. Curr. Opin. Genet. Dev. 12:640-649.
19. Eskesen, S. T., F. N. Eskesen, and A. Ruvinsky. 2004. Natural selection affects frequencies of AG and GT dinucleotides at the 5′ and 3′ ends of exons. Genetics 167:543-550.
20. Eyre-Walker, A. 1991. An analysis of codon usage in mammals: selection or mutation bias? J. Mol. Evol. 33:442-449.
21. Eyre-Walker, A., and P. D. Keightley. 1999. High genomic deleterious mutation rates in hominids. Nature 397:344-347.
22. Fairbrother, W. G., and L. A. Chasin. 2000. Human genomic sequences that inhibit splicing. Mol. Cell. Biol. 20:6816-6825.
23. Fairbrother, W. G., D. Holste, C. B. Burge, and P. A. Sharp. 2004a. Single nucleotide polymorphism-based validation of exonic splicing enhancers. PLoS Biol. 2:e268.
24. Fairbrother, W. G., R. F. Yeh, P. A. Sharp, and C. B. Burge. 2002. Predictive identification of exonic splicing enhancers in human genes. Science 297:1007-1013.
25. Fairbrother, W. G., G. W. Yeo, R. Yeh, P. Goldstein, M. Mawson, P. A. Sharp, and C. B. Burge. 2004b. RESCUE-ESE identifies candidate exonic splicing enhancers in vertebrate exons. Nucleic Acids Res. 32:W187-W190.
26. Graveley, B. R., K. J. Hertel, and T. Maniatis. 1998. A systematic analysis of the factors that determine the strength of pre-mRNA splicing enhancers. EMBO J. 17:6747-6756.
27. Hellmann, I., S. Zollner, W. Enard, I. Ebersberger, B. Nickel, and S. Paabo. 2003. Selection on human genes as revealed by comparisons to chimpanzee cDNA. Genome Res. 13: 831-837.
28. Hurst, L. D., and C. Pal. 2001. Evidence for purifying selection acting on silent sites in BRCA1. Trends Genet. 17:62-65.
29. Iida, K., and H. Akashi. 2000. A test of translational selection at 'silent' sites in the human genome: base composition comparisons in alternatively spliced genes. Gene 261:93-105.
30. Ikemura, T. 1985. Codon usage and tRNA content in unicellular and multicellular organisms. Mol. Biol. Evol. 2:13-34.
31. Keightley, P. D., and A. Eyre-Walker. 2000. Deleterious mutations and the evolution of sex. Science 290:331-333.
32. Keightley, P. D., and D. J. Gaffney. 2003. Functional constraints and frequency of deleterious mutations in noncoding DNA of rodents. Proc. Natl. Acad. Sci. USA 100:13402-13406.
33. Kimura, M. 1977. Preponderance of synonymous changes as evidence for the neutral theory of molecular evolution. Nature 267:275-276.
34. King, J. L., and T. H. Jukes. 1969. Non-Darwinian evolution. Science 164:788-798.
35. Kogan, S., and E. N. Trifonov. 2005. Gene splice sites correlate with nucleosome positions. Gene 352:57-62.
36. Lavner, Y., and D. Kotlar. 2005. Codon bias as a factor in regulating expression via translation rate in the human genome. Gene 345:127-138.
37. Lercher, M. J., J. V. Chamary, and L. D. Hurst. 2004. Genomic regionality in rates of evolution is not explained by clustering of genes of comparable expression profile. Genome Res. 14:1002-1013.
38. Li, W. H. 1993. Unbiased estimation of the rates of synonymous and nonsynonymous substitution. J. Mol. Evol. 36:96-99.
39. Lim, L. P., and C. B. Burge. 2001. A computational analysis of sequence features involved in recognition of short introns. Proc. Natl. Acad. Sci. USA 98:11193-11198.
40. Liu, H. X., L. Cartegni, M. Q. Zhang, and A. R. Krainer. 2001. A mechanism for exon skipping caused by nonsense or missense mutations in BRCA1 and other genes. Nat. Genet. 27:55-58.
41. Liu, H. X., M. Zhang, and A. R. Krainer. 1998. Identification of functional exonic splicing enhancer motifs recognized by individual SR proteins. Genes Dev. 12:1998-2012.
42. Louie, E., J. Ott, and J. Majewski. 2003. Nucleotide frequency variation across human genes. Genome Res. 13:2594-2601.
43. Lu, J., and C. I. Wu. 2005. Weak selection revealed by the whole-genome comparison of the X chromosome and autosomes of human and chimpanzee. Proc. Natl. Acad. Sci. USA 102: 4063-4067.
44. Majewski, J., and J. Ott. 2002. Distribution and characterization of regulatory elements in the human genome. Genome Res. 12: 1827-1836.
45. O'Neill, R. J., F. E. Brennan, M. L. Delbridge, R. H. Crozier, and J. A. Graves. 1998. De novo insertion of an intron into the mammalian sex determining gene, SRY. Proc. Natl. Acad. Sci. USA 95:1653-1657.
46. Orban, T. I., and E. Olah. 2001. Purifying selection on silent sites - a constraint from splicing regulation? Trends Genet. 17:252-253.
47. Pagani, F., M. Raponi, and F. E. Baralle. 2005. Synonymous mutations in CFTR exon 12 affect splicing and are not neutral in evolution. Proc. Natl. Acad. Sci. USA 102:6368-6372.
48. Pond, S. K., and S. V. Muse. 2005. Site-to-site variation of synonymous substitution rates. Mol. Biol. Evol. (in press).
49. Robberson, B. L., G. J. Cote, and S. M. Berget. 1990. Exon definition may facilitate splice site selection in RNAs with multiple exons. Mol. Cell. Biol. 10:84-94.
50. Roy, S. W., A. Fedorov, and W. Gilbert. 2003. Large-scale comparison of intron positions in mammalian genes shows intron loss but no gain. Proc. Natl. Acad. Sci. USA 100:7158-7162.
51. Schaal, T. D., and T. Maniatis. 1999. Selection and characterization of pre-mRNA splicing enhancers: identification of novel SR protein-specific enhancer sequences. Mol. Cell. Biol. 19:1705-1719.
52. Sharp, P. M., M. Averof, A. T. Lloyd, G. Matassi, and J. F. Peden. 1995. DNA-sequence evolution: the sounds of silence. Phil. Trans. R. Soc. Lond. B 349:241-247.
53. Spellman, R., A. Rideau, A. Matlin, C. Gooding, F. Robinson, N. McGlincy, S. N. Grellscheid, J. Southby, M. Wollerton, and C. W. Smith. 2005. Regulation of alternative splicing by PTB and associated factors. Biochem. Soc. Trans. 33:457-460.
54. Sved, J., and A. Bird. 1990. The expected equilibrium of the CpG dinucleotide in vertebrate genomes under a mutation model. Proc. Natl. Acad. Sci. USA 87:4692-4696.
55. Tamura, K., and M. Nei. 1993. Estimation of the number of nucleotide substitutions in the control region of mitochondrial-DNA in humans and chimpanzees. Mol. Biol. Evol. 10:512-526.
56. Tian, H., and R. Kole. 1995. Selection of novel exon recognition elements from a pool of random sequences. Mol. Cell. Biol. 15:6291-6298.
57. Urrutia, A. O., and L. D. Hurst. 2003. The signature of selection mediated by expression on human genes. Genome Res. 13:2260-2264.
58. Wang, Z., M. E. Rolish, G. Yeo, V. Tung, M. Mawson, and C. B. Burge. 2004. Systematic identification and analysis of exonic splicing silencers. Cell 119:831-845.
59. Willie, E., and J. Majewski. 2004. Evidence for codon bias selection at the pre-mRNA level in eukaryotes. Trends Genet. 20:534-538.
60. Xing, Y., and C. Lee. 2005. Evidence of functional selection pressure for alternative splicing events that accelerate evolution of protein subsequences. Proc. Natl. Acad. Sci. USA. 102: 13526-13531.
61. Yeo, G., S. Hoon, B. Venkatesh, and C. B. Burge. 2004. Variation in sequence and organization of splicing regulatory elements in vertebrate genes. Proc. Natl. Acad. Sci. USA 101:15700-15705.
62. Yeo, G. W., E. Van Nostrand, D. Holste, T. Poggio, and C. B. Burge. 2005. Identification and analysis of alternative splicing events conserved in human and mouse. Proc. Natl. Acad. Sci. USA 102:2850-2855.