Protein misinteraction avoidance causes highly expressed proteins to evolve slowly

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 14, 2012, Pages

  Yang, Jian Rong ^a,b   Liao, Ben Yang ^b,c   Zhuang, Shi Mei ^a   Zhang, Jianzhi ^b  

^a SUN YAT SEN UNIVERSITY   (China)

^b UNIVERSITY OF MICHIGAN   (United States)

^c NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL PROTEIN; MEMBRANE PROTEIN;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; GENE EXPRESSION; GENE MUTATION; GENETIC CORRELATION; GENETIC TRANSCRIPTION AND TRANSLATION; GENOMICS; MOLECULAR EVOLUTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN MISINTERACTION AVOIDANCE; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN UNFOLDING; SACCHAROMYCES CEREVISIAE; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; SIMULATION;

EVOLUTION, CHEMICAL; GENOME, FUNGAL; PROTEIN BINDING; PROTEIN FOLDING; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84859473329     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1117408109     Document Type: Article

References (61)

1. Hurst LD, Smith NG (1999) Do essential genes evolve slowly? Curr Biol 9:747-750. (Pubitemid 29350853)
2. Pál C, Papp B, Hurst LD (2001) Highly expressed genes in yeast evolve slowly. Genetics 158:927-931. (Pubitemid 32552328)
3. Zhang J, He X (2005) Significant impact of protein dispensability on the instantaneous rate of protein evolution. Mol Biol Evol 22:1147-1155. (Pubitemid 40471427)
4. Wall DP, et al. (2005) Functional genomic analysis of the rates of protein evolution. Proc Natl Acad Sci USA 102:5483-5488. (Pubitemid 40530284)
5. Liao BY, Scott NM, Zhang J (2006) Impacts of gene essentiality, expression pattern, and gene compactness on the evolutionary rate of mammalian proteins. Mol Biol Evol 23:2072-2080. (Pubitemid 44536815)
6. Zhang L, Li WH (2004) Mammalian housekeeping genes evolve more slowly than tissue-specific genes. Mol Biol Evol 21:236-239. (Pubitemid 38314611)
7. Drummond DA, Raval A, Wilke CO (2006) A single determinant dominates the rate of yeast protein evolution. Mol Biol Evol 23:327-337. (Pubitemid 43100047)
8. Hirsh AE, Fraser HB (2001) Protein dispensability and rate of evolution. Nature 411:1046-1049.
9. Fraser HB, Hirsh AE, Steinmetz LM, Scharfe C, Feldman MW (2002) Evolutionary rate in the protein interaction network. Science 296:750-752. (Pubitemid 34442006)
10. Jordan IK, Wolf YI, Koonin EV (2003) No simple dependence between protein evolution rate and the number of protein-protein interactions: Only the most prolific interactors tend to evolve slowly. BMC Evol Biol 3:1.
11. Wolf MY, Wolf YI, Koonin EV (2008) Comparable contributions of structural-functional constraints and expression level to the rate of protein sequence evolution. Biol Direct 3:40.
12. Wolf YI, Carmel L, Koonin EV (2006) Unifying measures of gene function and evolution. Proc Biol Sci 273:1507-1515. (Pubitemid 47308739)
13. Drummond DA, Wilke CO (2008) Mistranslation-induced protein misfolding as a dominant constraint on coding-sequence evolution. Cell 134:341-352. (Pubitemid 352010328)
14. Subramanian S, Kumar S (2004) Gene expression intensity shapes evolutionary rates of the proteins encoded by the vertebrate genome. Genetics 168:373-381. (Pubitemid 39346602)
15. Rocha EP, Danchin A (2004) An analysis of determinants of amino acids substitution rates in bacterial proteins. Mol Biol Evol 21:108-116. (Pubitemid 38233524)
16. Wang Z, Zhang J (2009) Why is the correlation between gene importance and gene evolutionary rate so weak? PLoS Genet 5:e1000329.
17. Liao BY, Weng MP, Zhang J (2010) Impact of extracellularity on the evolutionary rate of mammalian proteins. Genome Biol Evol 2:39-43.
18. Geiler-Samerotte KA, et al. (2011) Misfolded proteins impose a dosage-dependent fitness cost and trigger a cytosolic unfolded protein response in yeast. Proc Natl Acad Sci USA 108:680-685.
19. Drummond DA, Bloom JD, Adami C, Wilke CO, Arnold FH (2005) Why highly expressed proteins evolve slowly. Proc Natl Acad Sci USA 102:14338-14343. (Pubitemid 41429699)
20. Yang JR, Zhuang SM, Zhang J (2010) Impact of translational error-induced and error-free misfolding on the rate of protein evolution. Mol Syst Biol 6:421.
21. Wolfe KH, Shields DC (1997) Molecular evidence for an ancient duplication of the entire yeast genome. Nature 387:708-713. (Pubitemid 27270611)
22. Zhou T, Weems M, Wilke CO (2009) Translationally optimal codons associate with structurally sensitive sites in proteins. Mol Biol Evol 26:1571-1580.
23. Jaramillo A, Wernisch L, Héry S, Wodak SJ (2002) Folding free energy function selects native-like protein sequences in the core but not on the surface. Proc Natl Acad Sci USA 99:13554-13559. (Pubitemid 35215420)
24. Berezovsky IN, Zeldovich KB, Shakhnovich EI (2007) Positive and negative design in stability and thermal adaptation of natural proteins. PLoS Comput Biol 3:e52.
25. Capriotti E, Fariselli P, Casadio R (2005) I-Mutant2.0: Predicting stability changes upon mutation from the protein sequence or structure. Nucleic Acids Res 33:W306-W310. (Pubitemid 44529932)
26. Huh WK, et al. (2003) Global analysis of protein localization in budding yeast. Nature 425:686-691.
27. Ghaemmaghami S, et al. (2003) Global analysis of protein expression in yeast. Nature 425:737-741. (Pubitemid 37314318)
28. Qian W, He X, Chan E, Xu H, Zhang J (2011) Measuring the evolutionary rate of protein-protein interaction. Proc Natl Acad Sci USA 108:8725-8730.
29. Kuriyan J, Eisenberg D (2007) The origin of protein interactions and allostery in colocalization. Nature 450:983-990. (Pubitemid 350273628)
30. Zhang J, Maslov S, Shakhnovich EI (2008) Constraints imposed by non-functional protein-protein interactions on gene expression and proteome size. Mol Syst Biol 4:210.
31. Stambolsky P, et al. (2010) Modulation of the vitamin D3 response by cancer-associated mutant p53. Cancer Cell 17:273-285.
32. Vavouri T, Semple JI, Garcia-Verdugo R, Lehner B (2009) Intrinsic protein disorder and interaction promiscuity are widely associated with dosage sensitivity. Cell 138:198-208.
33. Johnson ME, Hummer G (2011) Nonspecific binding limits the number of proteins in a cell and shapes their interaction networks. Proc Natl Acad Sci USA 108:603-608.
34. Heo M, Maslov S, Shakhnovich E (2011) Topology of protein interaction network shapes protein abundances and strengths of their functional and nonspecific interactions. Proc Natl Acad Sci USA 108:4258-4263.
35. Deeds EJ, Ashenberg O, Gerardin J, Shakhnovich EI (2007) Robust protein protein interactions in crowded cellular environments. Proc Natl Acad Sci USA 104:14952-14957. (Pubitemid 47628407)
36. Ueda HR, et al. (2004) Universality and flexibility in gene expression from bacteria to human. Proc Natl Acad Sci USA 101:3765-3769. (Pubitemid 38381052)
37. Deeds EJ, Ashenberg O, Shakhnovich EI (2006) A simple physical model for scaling in protein-protein interaction networks. Proc Natl Acad Sci USA 103:311-316. (Pubitemid 43122397)
38. Miyazawa S, Jernigan R (1985) Estimation of effective interresidue contact energies from protein crystal structures: Quasi-chemical approximation. Macromolecules 18:534-552.
39. Kyte J, Doolittle RF (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157:105-132.
40. Akashi H, Gojobori T (2002) Metabolic efficiency and amino acid composition in the proteomes of Escherichia coli and Bacillus subtilis. Proc Natl Acad Sci USA 99:3695-3700. (Pubitemid 34252168)
41. Ashburner M, et al. (2000) Gene ontology: Tool for the unification of biology. Nat Genet 25:25-29. (Pubitemid 30257031)
42. Fields S, Song O (1989) A novel genetic system to detect protein-protein interactions. Nature 340:245-246. (Pubitemid 19171591)
43. Gavin AC, et al. (2002) Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature 415:141-147.
44. Tarassov K, et al. (2008) An in vivo map of the yeast protein interactome. Science 320:1465-1470. (Pubitemid 351929421)
45. Oren M, Rotter V (2010) Mutant p53 gain-of-function in cancer. Cold Spring Harb Perspect Biol 2:a001107.
46. Plata G, Gottesman ME, Vitkup D (2010) The rate of the molecular clock and the cost of gratuitous protein synthesis. Genome Biol 11:R98.
47. Eames M, Kortemme T (2007) Structural mapping of protein interactions reveals differences in evolutionary pressures correlated to mRNA level and protein abundance. Structure 15:1442-1451. (Pubitemid 350051922)
48. Gout JF, Kahn D, Duret L (2010) The relationship among gene expression, the evolution of gene dosage, and the rate of protein evolution. PLoS Genet 6:e1000944.
49. Cherry JL (2010) Expression level, evolutionary rate, and the cost of expression. Genome Biol Evol 2:757-769.
50. Liberles DA, Tisdell MD, Grahnen JA (2011) Binding constraints on the evolution of enzymes and signalling proteins: The important role of negative pleiotropy. Proc Biol Sci 278:1930-1935.
51. Fernández A, Lynch M (2011) Non-adaptive origins of interactome complexity. Nature 474:502-505.
52. Engel SR, et al. (2010) Saccharomyces Genome Database provides mutant phenotype data. Nucleic Acids Res 38:D433-D436.
53. Wapinski I, Pfeffer A, Friedman N, Regev A (2007) Natural history and evolutionary principles of gene duplication in fungi. Nature 449:54-61. (Pubitemid 47373776)
54. Larkin MA, et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948. (Pubitemid 350162903)
55. Gu X, Zhang J (1997) A simple method for estimating the parameter of substitution rate variation among sites. Mol Biol Evol 14:1106-1113. (Pubitemid 27463301)
56. Holstege FC, et al. (1998) Dissecting the regulatory circuitry of a eukaryotic genome. Cell 95:717-728. (Pubitemid 28544132)
57. Stark C, et al. (2011) The BioGRID Interaction Database: 2011 update. Nucleic Acids Res 39:D698-D704.
58. Berman HM, et al. (2000) The Protein Data Bank. Nucleic Acids Res 28:235-242. (Pubitemid 30047768)
59. Kabsch W, Sander C (1983) Dictionary of protein secondary structure: Pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22:2577-2637.
60. Yang ZR, Thomson R, McNeil P, Esnouf RM (2005) RONN: The bio-basis function neural network technique applied to the detection of natively disordered regions in proteins. Bioinformatics 21:3369-3376. (Pubitemid 41222441)
61. Mirny LA, Shakhnovich EI (1996) How to derive a protein folding potential? A new approach to an old problem. J Mol Biol 264:1164-1179. (Pubitemid 27019500)