Why there is more to protein evolution than protein function: Splicing, nucleosomes and dual-coding sequence

Biochemical Society Transactions

Volumn 37, Issue 4, 2009, Pages 756-761

  Warnecke, Tobias ^a   Weber, Claudia C ^a   Hurst, Laurence D ^a  

^a University of Bath   (United Kingdom)

Author keywords

Dual coding sequence; Exonic splicing enhancer (ESE); Nucleosome; Protein evolution; Protein function; Splicing

Indexed keywords

AMINO ACID SEQUENCE; CHROMATIN IMMUNOPRECIPITATION; CODON; CONFERENCE PAPER; ESCHERICHIA COLI; EXON; GENE EXPRESSION; GENETIC VARIABILITY; HUMAN; INTRON; MOLECULAR DYNAMICS; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CONTENT; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN STRUCTURE; RNA SPLICING; SEQUENCE ANALYSIS; SINGLE NUCLEOTIDE POLYMORPHISM; ANIMAL; GENETICS; METABOLISM; PHYSIOLOGY; REVIEW;

MAMMALIA;

PROTEIN;

ANIMALS; EVOLUTION, MOLECULAR; HUMANS; NUCLEOSOMES; PROTEINS; RNA SPLICING;

EID: 70349333474     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST0370756     Document Type: Conference Paper

References (48)

1. Nishikawa, K. and Ooi, T. (1982) Correlation of the amino acid composition of a protein to its structural and biological characters. J. Biochem. 91, 1821-1824
2. Zuckerkandl, E. (1976) Evolutionary processes and evolutionary noise at the molecular level. II. A selectionist model for random fixations in proteins. J. Mol. Evol. 7, 269-311
3. Pal, C., Papp, B. and Lercher, M.J. (2006) An integrated view of protein evolution. Nat. Rev. Genet. 7, 337-348
4. Williams, E.J. and Hurst, L.D. (2002) Is the synonymous substitution rate in mammals gene-specific? Mol. Biol. Evol. 19, 1395-1398
5. Lobry, J.R. and Gautier, C. (1994) Hydrophobicity, expressivity and aromaticity are the major trends of amino-acid usage in 999 Escherichia coli chromosome-encoded genes. Nucleic Acids Res. 22, 3174-3180
6. Pascal, G., Medigue, C. and Danchin, A. (2005) Universal biases in protein composition of model prokaryotes. Proteins 60, 27-35
7. Foerstner, K.U., von Mering, C., Hooper, S.D. and Bork, P. (2005) Environments shape the nucleotide composition of genomes. EMBO Rep. 6, 1208-1213
8. Naya, H., Romero, H., Zavala, A., Alvarez, B. and Musto, H. (2002) Aerobiosis increases the genomic guanine plus cytosine content (GC%) in prokaryotes. J. Mol. Evol. 55, 260-264
9. Sabbia, V., Piovani, R., Naya, H., Rodriguez-Maseda, H., Romero, H. and Musto, H. (2007) Trends of amino acid usage in the proteins from the human genome. J. Biomol. Struct. Dyn. 25, 55-59
10. Akashi, H. and Gojobori, T. (2002) Metabolic efficiency and amino acid composition in the proteomes of Escherichia coli and Bacillus subtilis. Proc. Natl. Acad. Sci. U.S.A. 99, 3695-3700
11. Swire, J. (2007) Selection on synthesis cost affects interprotein amino acid usage in all three domains of life. J. Mol. Evol. 64, 558-571
12. Drummond, D.A., Raval, A. and Wilke, C.O. (2006) A single determinant dominates the rate of yeast protein evolution. Mol. Biol. Evol. 23, 327-337
13. Kim, P.M., Lu, L.J., Xia, Y. and Gerstein, M.B. (2006) Relating three-dimensional structures to protein networks provides evolutionary insights. Science 314, 1938-1941
14. Batada, N.N., Reguly, T., Breitkreutz, A., Boucher, L., Breitkreutz, B.J., Hurst, L.D. and Tyers, M. (2007) Still stratus not altocumulus: further evidence against the date/party hub distinction. PLoS Biol. 5, e154
15. Drummond, D.A. and Wilke, C.O. (2008) Mistranslation-induced protein misfolding as a dominant constraint on coding-sequence evolution. Cell 134, 341-352
16. Wolf, M.Y., Wolf, Y.I. and Koonin, E.V. (2008) Comparable contributions of structural-functional constraints and expression level to the rate of protein sequence evolution. Biol. Direct 3, 40
17. Chamary, J.V. and Hurst, L.D. (2005) Evidence for selection on synonymous mutations affecting stability of mRNA secondary structure in mammals. Genome Biol. 6, R75
18. Carlini, D.B. (2005) Context-dependent codon bias and messenger RNA longevity in the yeast transcriptome. Mol. Biol. Evol. 22, 1403-1411
19. Shabalina, S.A., Ogurtsov, A.Y. and Spiridonov, N.A. (2006) A periodic pattern of mRNA secondary structure created by the genetic code. Nucleic Acids Res. 34, 2428-2437
20. Berget, S.M. (1995) Exon recognition in vertebrate splicing. J. Biol. Chem. 270, 2411-2414
21. Fox-Walsh, K.L., Dou, Y., Lam, B.J., Hung, S.P., Baldi, P.F. and Hertel, K.J. (2005) The architecture of pre-mRNAs affects mechanisms of splice-site pairing. Proc. Natl. Acad. Sci. U.S.A. 102, 16176-16181
22. Blencowe, B.J. (2000) Exonic splicing enhancers: mechanism of action, diversity and role in human genetic diseases. Trends Biochem. Sci. 25, 106-110
23. Graveley, B.R., Hertel, K.J. and Maniatis, T. (1998) A systematic analysis of the factors that determine the strength of pre-mRNA splicing enhancers. EMBO J. 17, 6747-6756
24. Parmley, J.L. and Hurst, L.D. (2007) Exonic splicing regulatory elements skew synonymous codon usage near intron-exon boundaries in mammals. Mol. Biol. Evol. 24, 1600-1603
25. Parmley, J.L., Urrutia, A.O., Potrzebowski, L., Kaessmann, H. and Hurst, L.D. (2007) Splicing and the evolution of proteins in mammals. PLoS Biol. 5, e14
26. Warnecke, T., Parmley, J.L. and Hurst, L.D. (2008) Finding exonic islands in a sea of non-coding sequence: splicing related constraints on protein composition and evolution are common in intron-rich genomes. Genome Biol. 9, R29
27. 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
28. Carlini, D.B. and Genut, J.E. (2006) Synonymous SNPs provide evidence for selective constraint on human exonic splicing enhancers. J. Mol. Evol. 62, 89-98
29. Duret, L. and Mouchiroud, D. (2000) Determinants of substitution rates in mammalian genes: expression pattern affects selection intensity but not mutation rate. Mol. Biol. Evol. 17, 68-74
30. Liu, J., Zhang, Y., Lei, X. and Zhang, Z. (2008) Natural selection of protein structural and functional properties: a single nucleotide polymorphism perspective. Genome Biol. 9, R69
31. Henikoff, S. (2008) Nucleosome destabilization in the epigenetic regulation of gene expression. Nat. Rev. Genet. 9, 15-26
32. Lee, W., Tillo, D., Bray, N., Morse, R.H., Davis, R.W., Hughes, T.R. and Nislow, C. (2007) A high-resolution atlas of nucleosome occupancy in yeast. Nat. Genet. 39, 1235-1244
33. Shivaswamy, S., Bhinge, A., Zhao, Y., Jones, S., Hirst, M. and Iyer, V.R. (2008) Dynamic remodeling of individual nucleosomes across a eukaryotic genome in response to transcriptional perturbation. PLoS Biol. 6, e65
34. Mavrich, T.N., Jiang, C., Ioshikhes, I.P., Li, X., Venters, B.J., Zanton, S.J., Tomsho, L.P., Qi, J., Glaser, R.L., Schuster, S.C. et al. (2008) Nucleosome organization in the Drosophila genome. Nature 453, 358-362
35. Valouev, A., Ichikawa, J., Tonthat, T., Stuart, J., Ranade, S., Peckham, H., Zeng, K., Malek, J.A., Costa, G., McKernan, K. et al. (2008) A high-resolution, nucleosome position map of C. elegans reveals a lack of universal sequence-dictated positioning. Genome Res. 18, 1051-1063
36. Schones, D.E., Cui, K., Cuddapah, S., Roh, T.Y., Barski, A., Wang, Z., Wei, G. and Zhao, K. (2008) Dynamic regulation of nucleosome positioning in the human genome. Cell 132, 887-898
37. Widom, J. (2001) Role of DNA sequence in nucleosome stability and dynamics. Q. Rev. Biophys. 34, 269-324
38. Davey, C., Pennings, S., Meersseman, G., Wess, T.J. and Allan, J. (1995) Periodicity of strong nucleosome positioning sites around the chicken adult β-globin gene may encode regularly spaced chromatin. Proc. Natl. Acad. Sci. U.S.A. 92, 11210-11214
39. Warnecke, T., Batada, N.N. and Hurst, L.D. (2008) The impact of the nucleosome code on protein-coding sequence evolution in yeast. PLoS Genet. 4, e1000250
40. Washietl, S., Machne, R. and Goldman, N. (2008) Evolutionary footprints of nucleosome positions in yeast. Trends Genet. 24, 583-587
41. Chen, K., Meng, Q., Ma, L., Liu, Q., Tang, P., Chiu, C., Hu, S. and Yu, J. (2008) A novel DNA sequence periodicity decodes nucleosome positioning. Nucleic Acids Res. 36, 6228-6236
42. Murzin, A.G., Brenner, S.E., Hubbard, T. and Chothia, C. (1995) SCOP: a structural classification of proteins database for the investigation of sequences and structures. J. Mol. Biol. 247, 536-540
43. Bauer, F., Schweimer, K., Kluver, E., Conejo-Garcia, J.R., Forssmann, W.G., Rosch, P., Adermann, K. and Sticht, H. (2001) Structure determination of human and murine β-defensins reveals structural conservation in the absence of significant sequence similarity. Protein Sci. 10, 2470-2479
44. Hill, E.E., Morea, V. and Chothia, C. (2002) Sequence conservation in families whose members have little or no sequence similarity: the four-helical cytokines and cytochromes. J. Mol. Biol. 322, 205-233
45. Eyre-Walker, A. and Keightley, P.D. (2007) The distribution of fitness effects of new mutations. Nat. Rev. Genet. 8, 610-618
46. Akashi, H. (1994) Synonymous codon usage in Drosophila melanogaster: natural selection and translational accuracy. Genetics 136, 927-935
47. Vicario, S., Moriyama, E.N. and Powell, J.R. (2007) Codon usage in twelve species of Drosophila. BMC Evol. Biol. 7, 226
48. Warnecke, T. and Hurst, L.D. (2007) Evidence for a trade-off between translational efficiency and splicing regulation in determining synonymous codon usage in Drosophila melanogaster. Mol. Biol. Evol. 24, 2755-2762