Mistranslation-Induced Protein Misfolding as a Dominant Constraint on Coding-Sequence Evolution

Cell

Volumn 134, Issue 2, 2008, Pages 341-352

  Drummond, D Allan ^a   Wilke, Claus O ^b  

^a HARVARD UNIVERSITY   (United States)

^b UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

CHEMBIO; EVO_ECOL; PROTEINS

Indexed keywords

MESSENGER RNA;

ARTICLE; CELL STRUCTURE; CODING; CODON USAGE; ESCHERICHIA COLI; FLY; GENE EXPRESSION; GENE SEQUENCE; HUMAN; METAZOON; MOLECULAR EVOLUTION; MOUSE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; RNA TRANSLATION; WORM; YEAST;

METAZOA;

EID: 47549097539     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2008.05.042     Document Type: Article

References (68)

1. Akashi H. Synonymous codon usage in Drosophila melanogaster: Natural selection and translational accuracy. Genetics 136 (1994) 927-935
2. Anfinsen C. The Molecular Basis of Evolution (1959), John Wiley & Sons, New York
3. Bacher J.M., and Schimmel P. An editing-defective aminoacyl-tRNA synthetase is mutagenic in aging bacteria via the SOS response. Proc. Natl. Acad. Sci. USA 104 (2007) 1907-1912
4. Bierne N., and Eyre-Walker A. The problem of counting sites in the estimation of the synonymous and nonsynonymous substitution rates: Implications for the correlation between the synonymous substitution rate and codon usage bias. Genetics 165 (2003) 1587-1597
5. Bloom J.D., Labthavikul S., Otey C.R., and Arnold F.H. Protein stability promotes evolvability. Proc. Natl. Acad. Sci. USA 103 (2006) 5869-5874
6. Boles E., Schulte F., Miosga T., Freidel K., Schluter E., Zimmermann F.K., Hollenberg C.P., and Heinisch J.J. Characterization of a glucose-repressed pyruvate kinase (Pyk2p) in Saccharomyces cerevisiae that is catalytically insensitive to fructose-1,6-bisphosphate. J. Bacteriol. 179 (1997) 2987-2993
7. Bridgham J.T., Carroll S.M., and Thornton J.W. Evolution of hormone-receptor complexity by molecular exploitation. Science 312 (2006) 97-101
8. Bucciantini M., Giannoni E., Chiti F., Baroni F., Formigli L., Zurdo J., Taddei N., Ramponi G., Dobson C.M., and Stefani M. Inherent toxicity of aggregates implies a common mechanism for protein misfolding diseases. Nature 416 (2002) 507-511
9. Chamary J.V., Parmley J.L., and Hurst L.D. Hearing silence: Non-neutral evolution at synonymous sites in mammals. Nat. Rev. Genet. 7 (2006) 98-108
10. Choi J.K., Kim S.C., Seo J., Kim S., and Bhak J. Impact of transcriptional properties on essentiality and evolutionary rate. Genetics 175 (2007) 199-206
11. Dean A.M., and Thornton J.W. Mechanistic approaches to the study of evolution: The functional synthesis. Nat. Rev. Genet. 8 (2007) 675-688
12. Dittmar K.A., Goodenbour J.M., and Pan T. Tissue-specific differences in human transfer RNA expression. PLoS Genet. 2 (2006) e221
13. Dorus S., Vallender E.J., Evans P.D., Anderson J.R., Gilbert S.L., Mahowald M., Wyckoff G.J., Malcom C.M., and Lahn B.T. Accelerated evolution of nervous system genes in the origin of Homo sapiens. Cell 119 (2004) 1027-1040
14. dos Reis M., Savva R., and Wernisch L. Solving the riddle of codon usage preferences: A test for translational selection. Nucleic Acids Res. 32 (2004) 5036-5044
15. Drummond D.A., Bloom J.D., Adami C., Wilke C.O., and Arnold F.H. Why highly expressed proteins evolve slowly. Proc. Natl. Acad. Sci. USA 102 (2005) 14338-14343
16. Drummond D.A., Raval A., and Wilke C.O. A single determinant dominates the rate of yeast protein evolution. Mol. Biol. Evol. 23 (2006) 327-337
17. Duret L., and Mouchiroud D. Expression pattern and, surprisingly, gene length shape codon usage in Caenorhabditis, Drosophila, and Arabidopsis. Proc. Natl. Acad. Sci. USA 96 (1999) 4482-4487
18. Duret L., and Mouchiroud D. Determinants of substitution rates in mammalian genes: Expression pattern affects selection intensity but not mutation rate. Mol. Biol. Evol. 17 (2000) 68-74
19. Edgar R.C. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32 (2004) 1792-1797
20. Freeland S.J., and Hurst L.D. The genetic code is one in a million. J. Mol. Evol. 47 (1998) 238-248
21. Gruzman A., Wood W.L., Alpert E., Prasad M.D., Miller R.G., Rothstein J.D., Bowser R., Hamilton R., Wood T.D., Cleveland D.W., et al. Common molecular signature in SOD1 for both sporadic and familial amyotrophic lateral sclerosis. Proc. Natl. Acad. Sci. USA 104 (2007) 12524-12529
22. Guo H.H., Choe J., and Loeb L.A. Protein tolerance to random amino acid change. Proc. Natl. Acad. Sci. USA 101 (2004) 9205-9210
23. Ikemura T. Codon usage and tRNA content in unicellular and multicellular organisms. Mol. Biol. Evol. 2 (1985) 13-34
24. Ingvarsson P.K. Gene expression and protein length influence codon usage and rates of sequence evolution in Populus tremula. Mol. Biol. Evol. 24 (2007) 836-844
25. Koonin E.V., and Wolf Y.I. Evolutionary systems biology: Links between gene evolution and function. Curr. Opin. Biotechnol. 17 (2006) 481-487
26. Kourie J.I., and Henry C.L. Ion channel formation and membrane-linked pathologies of misfolded hydrophobic proteins: The role of dangerous unchaperoned molecules. Clin. Exp. Pharmacol. Physiol. 29 (2002) 741-753
27. Kramer E.B., and Farabaugh P.J. The frequency of translational misreading errors in E. coli is largely determined by tRNA competition. RNA 13 (2007) 87-96
28. Krylov D.M., Wolf Y.I., Rogozin I.B., and Koonin E.V. Gene loss, protein sequence divergence, gene dispensability, expression level, and interactivity are correlated in eukaryotic evolution. Genome Res. 13 (2003) 2229-2235
29. Lee J.W., Beebe K., Nangle L.A., Jang J., Longo-Guess C.M., Cook S.A., Davisson M.T., Sundberg J.P., Schimmel P., and Ackerman S.L. Editing-defective tRNA synthetase causes protein misfolding and neurodegeneration. Nature 443 (2006) 50-55
30. Lemos B., Bettencourt B.R., Meiklejohn C.D., and Hartl D.L. Evolution of proteins and gene expression levels are coupled in Drosophila and are independently associated with mRNA abundance, protein length, and number of protein-protein interactions. Mol. Biol. Evol. 22 (2005) 1345-1354
31. Li W.H., Wu C.I., and Luo C.C. A new method for estimating synonymous and nonsynonymous rates of nucleotide substitution considering the relative likelihood of nucleotide and codon changes. Mol. Biol. Evol. 2 (1985) 150-174
32. Liao B.Y., Scott N.M., and Zhang J. Impacts of gene essentiality, expression pattern, and gene compactness on the evolutionary rate of mammalian proteins. Mol. Biol. Evol. 23 (2006) 2072-2080
33. Marais G., Domazet-Loso T., Tautz D., and Charlesworth B. Correlated evolution of synonymous and nonsynonymous sites in Drosophila. J. Mol. Evol. 59 (2004) 771-779
34. Markiewicz P., Kleina L.G., Cruz C., Ehret S., and Miller J.H. Genetic studies of the lac repressor. XIV. Analysis of 4000 altered Escherichia coli lac repressors reveals essential and non-essential residues, as well as "spacers" which do not require a specific sequence. J. Mol. Biol. 240 (1994) 421-433
35. Ogle J.M., and Ramakrishnan V. Structural insights into translational fidelity. Annu. Rev. Biochem. 74 (2005) 129-177
36. Pakula A.A., and Sauer R.T. Genetic analysis of protein stability and function. Annu. Rev. Genet. 23 (1989) 289-310
37. Pál C., Papp B., and Hurst L.D. Highly expressed genes in yeast evolve slowly. Genetics 158 (2001) 927-931
38. Pál C., Papp B., and Lercher M.J. An integrated view of protein evolution. Nat. Rev. Genet. 7 (2006) 337-348
39. Parker J. Errors and alternatives in reading the universal genetic code. Microbiol. Rev. 53 (1989) 273-298
40. Parmley J.L., Urrutia A.O., Potrzebowski L., Kaessmann H., and Hurst L.D. Splicing and the evolution of proteins in mammals. PLoS Biol. 5 (2007) e14
41. Popescu C.E., Borza T., Bielawski J.P., and Lee R.W. Evolutionary rates and expression level in Chlamydomonas. Genetics 172 (2006) 1567-1576
42. Rocha E.P. Codon usage bias from tRNA's point of view: Redundancy, specialization, and efficient decoding for translation optimization. Genome Res. 14 (2004) 2279-2286
43. Rocha E.P., and Danchin A. An analysis of determinants of amino acids substitution rates in bacterial proteins. Mol. Biol. Evol. 21 (2004) 108-116
44. Sekijima Y., Wiseman R.L., Matteson J., Hammarstrom P., Miller S.R., Sawkar A.R., Balch W.E., and Kelly J.W. The biological and chemical basis for tissue-selective amyloid disease. Cell 121 (2005) 73-85
45. Sharp P.M., and Li W.H. The rate of synonymous substitution in enterobacterial genes is inversely related to codon usage bias. Mol. Biol. Evol. 4 (1987) 222-230
46. Sharp P.M., and Cowe E. Synonymous codon usage in Saccharomyces cerevisiae. Yeast 7 (1991) 657-678
47. Soto C. Unfolding the role of protein misfolding in neurodegenerative diseases. Nat. Rev. Neurosci. 4 (2003) 49-60
48. Stefani M. Generic cell dysfunction in neurodegenerative disorders: Role of surfaces in early protein misfolding, aggregation, and aggregate cytotoxicity. Neuroscientist 13 (2007) 519-531
49. Stefani M., and Dobson C.M. Protein aggregation and aggregate toxicity: New insights into protein folding, misfolding diseases and biological evolution. J. Mol. Med. 81 (2003) 678-699
50. Stoebel D.M., Dean A.M., and Dykhuizen D.E. The cost of expression of Escherichia coli lac operon proteins is in the process, not in the products. Genetics 178 (2008) 1653-1660
51. Stoletzki N., and Eyre-Walker A. Synonymous codon usage in Escherichia coli: Selection for translational accuracy. Mol. Biol. Evol. 24 (2007) 374-381
52. Subramanian S., and Kumar S. Gene expression intensity shapes evolutionary rates of the proteins encoded by the vertebrate genome. Genetics 168 (2004) 373-381
53. Wakeley J. The excess of transitions among nucleotide substitutions: new methods of estimating transition bias underscore its significance. Trends Ecol. Evol. 11 (1996) 158-162
54. Wall D.P., Hirsh A.E., Fraser H.B., Kumm J., Giaever G., Eisen M.B., and Feldman M.W. Functional genomic analysis of the rates of protein evolution. Proc. Natl. Acad. Sci. USA 102 (2005) 5483-5488
55. Wang H.Y., Chien H.C., Osada N., Hashimoto K., Sugano S., Gojobori T., Chou C.K., Tsai S.F., Wu C.I., and Shen C.K. Rate of evolution in brain-expressed genes in humans and other primates. PLoS Biol. 5 (2007) e13
56. Warringer J., Ericson E., Fernandez L., Nerman O., and Blomberg A. High-resolution yeast phenomics resolves different physiological features in the saline response. Proc. Natl. Acad. Sci. USA 100 (2003) 15724-15729
57. Wilke C.O. Molecular clock in neutral protein evolution. BMC Genet. 5 (2004) 25
58. Wilke C.O., and Drummond D.A. Population genetics of translational robustness. Genetics 173 (2006) 473-481
59. Wilson A.C., Carlson S.S., and White T.J. Biochemical evolution. Annu. Rev. Biochem. 46 (1977) 573-639
60. Wright S.I., Yau C.B., Looseley M., and Meyers B.C. Effects of gene expression on molecular evolution in Arabidopsis thaliana and Arabidopsis lyrata. Mol. Biol. Evol. 21 (2004) 1719-1726
61. Wyckoff G.J., Malcom C.M., Vallender E.J., and Lahn B.T. A highly unexpected strong correlation between fixation probability of nonsynonymous mutations and mutation rate. Trends Genet. 21 (2005) 381-385
62. Yang Z. PAML: A program package for phylogenetic analysis by maximum likelihood. Comput. Appl. Biosci. 13 (1997) 555-556
63. Yang Z. Computational Molecular Evolution (2006), Oxford University Press, Oxford
64. Yang Z., and Nielsen R. Mutation-selection models of codon substitution and their use to estimate selective strengths on codon usage. Mol. Biol. Evol. 25 (2008) 568-579
65. Zhang L., and Li W.H. Mammalian housekeeping genes evolve more slowly than tissue-specific genes. Mol. Biol. Evol. 21 (2004) 236-239
66. Zhao L., Longo-Guess C., Harris B.S., Lee J.W., and Ackerman S.L. Protein accumulation and neurodegeneration in the woozy mutant mouse is caused by disruption of SIL1, a cochaperone of BiP. Nat. Genet. 37 (2005) 974-979
67. Zhu G., Golding G.B., and Dean A.M. The selective cause of an ancient adaptation. Science 307 (2005) 1279-1282
68. Zuckerkandl E. Evolutionary processes and evolutionary noise at the molecular level I. Functional density in proteins. J. Mol. Evol. 7 (1976) 167-183