The influence of selection for protein stability on dN/dS estimations

Genome Biology and Evolution

Volumn 6, Issue 10, 2014, Pages 2956-2967

  Dasmeh, Pouria ^a,b,c   Serohijos, Adrian W R ^a   Kepp, Kasper P ^b   Shakhnovich, Eugene I ^a  

^a HARVARD UNIVERSITY   (United States)

^b TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^c MAX PLANCK INSTITUTE OF IMMUNOBIOLOGY AND EPIGENETICS   (Germany)

Author keywords

dN dS; Folding stability; Maximum likelihood; Molecular evolution; Positive selection; Protein evolution

Indexed keywords

PROTEIN;

CHEMISTRY; CLASSIFICATION; GENETIC SELECTION; GENETICS; MOLECULAR EVOLUTION; PHYLOGENY; PROTEIN STABILITY;

EVOLUTION, MOLECULAR; PHYLOGENY; PROTEIN STABILITY; PROTEINS; SELECTION, GENETIC;

EID: 84965189652     PISSN: None     EISSN: 17596653     Source Type: Journal    
DOI: 10.1093/gbe/evu223     Document Type: Article

References (77)

1. Anisimova M, Bielawski JP, Yang Z. 2001. Accuracy and power of the likelihood ratio test in detecting adaptive molecular evolution. Mol Biol Evol. 18:1585-1592.
2. Bloom JD, et al. 2005. Thermodynamic prediction of protein neutrality. Proc Natl Acad Sci U S A. 102:606-611.
3. Charlesworth B. 2009. Fundamental concepts in genetics: effective population size and patterns of molecular evolution and variation. Nat Rev Genet. 10:195-205.
4. Chen Y, Dokholyan NV. 2008. Natural selection against protein aggregation on self-interacting and essential proteins in yeast, fly, and worm. Mol Biol Evol. 25:1530-1533.
5. Chen P, Shakhnovich EI. 2009. Lethal mutagenesis in viruses and bacteria. Genetics 183:639-650.
6. Cherry JL. 2010. Highly expressed and slowly evolving proteins share compositional properties with thermophilic proteins. Mol Biol Evol. 27: 735-741.
7. Chiti F, Dobson CM. 2006. Protein misfolding, functional amyloid, and human disease. Annu Rev Biochem. 75:333-366.
8. Dasmeh P, Kepp KP. 2012. Bridging the gap between chemistry, physiology, andevolution: quantifying the functionalityof spermwhalemyoglobinmutants. CompBiochem PhysiolAMol Integr Physiol. 161:9-17.
9. Dasmeh P, Serohijos AWR, Kepp KP, Shakhnovich EI. 2013. Positively selected sites in cetacean myoglobins contribute to protein stability. PLoS Comput Biol. 9(3):e1002929.
10. de Juan D, Pazos F, Valencia A. 2013. Emerging methods in protein coevolution. Nat Rev Genet. 14:249-261.
11. Ding F, Dokholyan NV. 2006. Emergence of protein fold families through rational design. PLoS Comput Biol. 2(7):e85.
12. Mirny LA, Shakhnovich EI. 1999. Universally conserved positions in protein folds: reading evolutionary signals about stability, folding kinetics and function. J Mol Biol. 291.1:177-196.
13. Dokholyan NV, Shakhnovich EI. 2001. Understanding hierarchical protein evolution from first principles. J Mol Biol. 312:289-307.
14. Drummond DA, Bloom JD, Adami C, Wilke CO, Arnold FH. 2005. Why highly expressed proteins evolve slowly. Proc Natl Acad Sci U S A. 102: 14338-14343.
15. Drummond DA, Wilke CO. 2008. Mistranslation-induced protein misfolding as a dominant constraint on coding-sequence evolution. Cell 134: 341-352.
16. Du X, Lipman DJ, Cherry JL. 2013. Why does a protein's evolutionary rate vary over time? Genet Biol Evol. 5:494-503.
17. Dyson HJ, Wright PE. 2005. Intrinsically unstructured proteins and their functions. Nat Rev Mol Cell Biol. 6:197-208.
18. Felsenstein J, Churchill GA. 1996. A hidden Markov model approach to variation among sites in rate of evolution. Mol Biol Evol. 13:93-104.
19. Fersht AR, Matouschek A, Serrano L. 1992. The folding of an enzyme. I. Theory of protein engineering analysis of stability and pathway of protein folding. J Mol Biol. 224:771-782.
20. Fisher RA. 1999. The genetical theory of natural selection: a complete variorum edition. New York: Oxford University Press.
21. Goldstein RA. 2008. The structure of protein evolution and the evolution of protein structure. Curr Opin Struct Biol. 18:170-177.
22. Goldstein RA. 2011. The evolution and evolutionary consequences of marginal thermostability in proteins. Proteins 79:1396-1407.
23. Goldstein RA. 2013. Population size dependence of fitness effect distribution and substitution rate probed by biophysical model of protein thermostability. Genome Biol Evol. 5:1584-1593.
24. 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 U S A. 108: 4258-4263.
25. Holder M, Lewis PO. 2003. Phylogeny estimation: traditional and Bayesian approaches. Nat Rev Genet. 4:275-284.
26. Kimura M. 1962. On the probability of fixation of mutant genes in a population. Genetics 47:713.
27. Kimura M. 1977. Preponderance of synonymous changes as evidence for the neutral theory of molecular evolution. Nature 267:275-276.
28. Kuhlman B, Baker D. 2000. Native protein sequences are close to optimal for their structures. Proc Natl Acad Sci U S A. 97:10383-10388.
29. Kullback S, Leibler RA. 1951. On information and sufficiency. Ann Math Stat 22:79-86.
30. Kumar S. 2005. Molecular clocks: four decades of evolution. Nat Rev Genet. 6:654-662.
31. Li L, Mirny LA, Shakhnovich EI. 2000. Kinetics, thermodynamics and evolution of non-native interactions in a protein folding nucleus. Nat Struct Biol. 7:336-342.
32. Lio' P, Goldman N. 1998. Models of molecular evolution and phylogeny. Genome Res. 8:1223-1244.
33. Lobkovsky AE, Wolf YI, Koonin EV. 2010. Universal distribution of protein evolution rates as a consequence of protein folding physics. Proc Natl Acad Sci U S A. 107:2983-2988.
34. Lynch M, Conery JS. 2003. The origins of genome complexity. Science 302:1401-1404.
35. Mailund T, Dutheil JY, Hobolth A, Lunter G, Schierup MH. 2011. Estimating divergence time and ancestral effective population size of Bornean and Sumatran orangutan subspecies using a coalescent hidden Markov model. PLoS Genet. 7(3):e1001319.
36. Margoliash E. 1963. Primary structure and evolution of cytochrome c. Proc Natl Acad Sci U S A. 50:672-679.
37. Mesnick SL, et al. 1999. Culture and genetic evolution in whales. Science 284:2055a.
38. Mirny LA, Abkevich VI, Shakhnovich EI. 1998. How evolution makes proteins fold quickly. Proc Natl Acad Sci U S A. 95(9):4976-4981.
39. Mustonen V, Lässig M. 2009. From fitness landscapes to seascapes: nonequilibrium dynamics of selection and adaptation. Trends Genet. 25: 111-119.
40. Nielsen R, et al. 2005. A scan for positively selected genes in the genomes of humans and chimpanzees. PLoS Biol. 3(6):e170.
41. Nielsen R, Yang Z. 1998. Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene. Genetics 148:929-936.
42. Phillips SEV. 1980. Structure and refinement of oxymyoglobin at 1.6 Å resolutions. J Mol Biol. 142:531-554.
43. Pollock DD, Thiltgen G, Goldstein RA. 2012. Amino acid coevolution induces an evolutionary Stokes shift. Proc Natl Acad Sci U S A. 109: E1352-E1359.
44. Privalov PL, Khechinashvili NN. 1974. A thermodynamic approach to the problem of stabilization of globular protein structure: a calorimetric study. J Mol Biol. 86:665-684.
45. Rannala B, Yang Z. 2003. Bayes estimation of species divergence times and ancestral population sizes using DNA sequences from multiple loci. Genetics 164:1645-1656.
46. Sarai A, et al. 2001. Thermodynamic databases for proteins and protein-nucleic acid interactions. Biopolymers 61(2):121-126.
47. Sawyer SA, Parsch J, Zhang Z, Hartl DL. 2007. Prevalence of positive selection among nearly neutral amino acid replacements in Drosophila. Proc Natl Acad Sci U S A. 104:6504-6510.
48. Sawyer SL, Malik HS. 2006. Positive selection of yeast nonhomologous endjoining genes and a retrotransposon conflict hypothesis. Proc Natl Acad Sci U S A. 103:17614-17619.
49. Scott EE, Paster EV, Olson JS. 2000. The stabilities of mammalian apomyoglobin vary over a 600-fold range and can be enhanced by comparative mutagenesis. J Biol Chem. 275:27129-27136.
50. Serohijos AWR, et al. 2008. Phenylalanine-508 mediates a cytoplasmicmembrane domain contact in the CFTR 3D structure crucial to assembly and channel function. Proc Natl Acad Sci U S A. 105:3256-3261.
51. Serohijos AWR, Lee SY, Shakhnovich EI. 2013. Highly abundant proteins favor more stable 3D structures in yeast. Biophys J. 104: L1-L3.
52. Serohijos AWR, Rimas Z, Shakhnovich EI. 2012. Protein biophysics explains why highly abundant proteins evolve slowly. Cell Rep. 2:249-256.
53. Serohijos AWR, Shakhnovich EI. 2014. Contribution of selection for protein folding stability in shaping the patterns of polymorphisms in coding regions. Mol Biol Evol. 31(1):156-176.
54. Shakhnovich EI, Finkelstein AV. 1989. Theory of cooperative transitions in protein molecules. I. Why denaturation of globular protein is a firstorder phase transition. Biopolymers 28:1667-1680.
55. Simonetti FL, et al. 2013. MISTIC: mutual information server to infer coevolution. Nucleic Acids Res. 41. W1:W8-W14.
56. Soskine M, Tawfik DS. 2010. Mutational effects and the evolution of new protein functions. Nat Rev Genet. 11:572-582.
57. Soto C. 2003. Unfolding the role of protein misfolding in neurodegenerative diseases. Nat Rev Neurosci. 4:49-60.
58. Suzuki T, Imai K. 1998. Evolution ofmyoglobin. CMLS Cell Mol Life Sci. 54: 979-1004.
59. Swanson WJ, Wong A, Wolfner MF, Aquadro CF. 2004. Evolutionary expressed sequence tag analysis of Drosophila female reproductive tracts identifies genes subjected to positive selection. Genetics 168: 1457-1465.
60. Taverna DM, Goldstein RA. 2002a. Why are proteins marginally stable? Proteins 46:105-109.
61. Taverna DM, Goldstein RA. 2002b. Why are proteins so robust to site mutations? J Mol Biol. 315:479-484.
62. Tokuriki N, Stricher F, Schymkowitz J, Serrano L, Tawfik DS. 2007. The stability effects of protein mutations appear to be universally distributed. J Mol Biol. 369:1318-1332.
63. UniProt Consortium. 2008. The universal protein resource (UniProt). Nucleic Acid Res. 35:D190-D195.
64. Whelan S, Goldman N. 1999. Distributions of statistics used for the comparison of models of sequence evolution in phylogenetics. Mol Biol Evol. 16:1292-1299.
65. Williams PD, Pollock DD, Blackburne BP, Goldstein RA. 2006. Assessing the accuracy of ancestral protein reconstruction methods. PLoS Comput Biol. 2(6):e69.
66. Wylie CS, Shakhnovich EI. 2011. A biophysical protein folding model accounts for most mutational fitness effects in viruses. Proc Natl Acad Sci U S A. 108:9916-9921.
67. Yang Z. 1998. Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution. Mol Biol Evol. 15:568-573.
68. Yang Z. 2006. Computational Molecular Evolution. Oxford: Oxford University Press.
69. Yang Z. 2007. PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol. 24:1586-1591.
70. Yang Z, Bielawski JP. 2000. Statistical methods for detecting molecular adaptation. Trends Ecol Evol. 15: 496-503.
71. Yang Z, Rannala B. 2012.Molecular phylogenetics: principles and practice. Nat Rev Genet. 13:303-314.
72. Yang Z, Wong WSW, Nielsen R. 2005. Bayes empirical Bayes inference of amino acid sites under positive selection. Mol Biol Evol. 22:1107-1118.
73. Yin S, Ding F, Dokholyan NV. 2007a. Eris: an automated estimator of protein stability. Nat Methods. 4:466-467.
74. Yin S, Ding F, Dokholyan NV. 2007b. Modeling backbone flexibility improves protein stability estimation. Structure 15:1567-1576.
75. Zeldovich KB, Chen P, Shakhnovich EI. 2007. Protein stability imposes limits on organism complexity and speed of molecular evolution. Proc Natl Acad Sci U S A. 104:16152-16157.
76. Zuckerkandl E, Pauling L. 1962. Molecular disease, evolution and genetic heterogeneity. In: Kasha M, Pullman B, editors. Horizons in biochemistry. New York: Academic Press. p. 189-225.
77. Zuckerkandl E, Pauling L. 1965. Evolutionary divergence and convergence in proteins. In: Bryson V, Vogel HJ, editors. Evolving genes and proteins. New York: Academic Press. p. 97-166.