A maximum likelihood method for detecting directional evolution in protein sequences and its application to influenza a virus

Molecular Biology and Evolution

Volumn 25, Issue 9, 2008, Pages 1809-1824

  Kosakovsky Pond, Sergei L ^a   Poon, Art F Y ^a   Leigh Brown, Andrew J ^b   Frost, Simon D W ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Directional selection; Episodic selection; Evolution of influenza; Maximum likelihood

Indexed keywords

AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; GENETIC VARIABILITY; INFLUENZA VIRUS A; NONHUMAN; PHYLOGENY; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; SEROTYPE;

AVES; INFLUENZA A VIRUS;

EID: 49749094696     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msn123     Document Type: Article

References (66)

1. Anisimova M, Bielawski JP, Yang Z. 2002. Accuracy and power of Bayes prediction of amino acid sites under positive selection. Mol Biol Evol. 19(6):950-958.
2. Bao Y, Bolotov P, Dernovoy D, Kiryutin B, Zaslavsky L, Tatusova T, Ostell J, Lipman D. 2007. The influenza virus resource at the national center for biotechnology information. J Virol. 82(2):596-601.
3. Bush RM, Bender CA, Subbarao K, Cox NJ, Fitch WM. 1999. Predicting the evolution of human influenza A. Science. 286(5446):1921-1925.
4. Colman PM, Varghese JN, Laver WG. 1983. Structure of the catalytic and antigenic sites in influenza virus neuraminidase. Nature. 303(5921):41-44.
5. Conant GC, Wagner GP, Stadler PF. 2007. Modeling amino acid substitution patterns in orthologous and paralogous genes. Mol Phylogenet Evol. 42(2):298-307.
6. Dayhoff MO, Eck EV, Park CM. 1972. A model of evolutionary change in proteins. In: Dayhoff MO, editor. Atlas of protein sequence and structure. Vol. 5. Washington (DC): National Biomedical Research Foundation. p. 89-99.
7. Doron-Faigenboim A, Pupko T. 2007. A combined empirical and mechanistic codon model. Mol Biol Evol. 24(2):388-397.
8. Felsenstein J. 1981. Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol. 17:368-376.
9. Goldman N, Yang Z. 1994. A codon-based model of nucleotide substitution for protein-coding DNA sequences. Mol Biol Evol. 11(5):725-736.
10. Guindon SA, Rodrigo G, Dyer KA, Huelsenbeck JP. 2004. Modeling the site-specific variation of selection patterns along lineages. Proc Natl Acad Sci USA. 101(35):12957-12962.
11. Harter C, James P, Bachi T, Semenza G, Brunner J. 1989. Hydrophobic binding of the ectodomain of influenza hemagglutinin to membranes occurs through the "fusion peptide". J Biol Chem. 264(11):6459-6464.
12. Holm S. 1979. A simple sequentially rejective multiple test procedure. Scand J Stat. 6:65-70.
13. Jones D, Taylor W, Thornton J. 1992. The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci. 8(3):275-282.
14. Kass R, Raftery A. 1995. Bayes factors. J Am Stat Assoc. 90(430):773-795.
15. Kaverin NV, Rudneva IA, Govorkova EA, Timofeeva TA, Shilov AA, Kochergin-Nikitsky KS, Krylov PS, Webster RG. 2007. Epitope mapping of the hemagglutinin molecule of a highly pathogenic H5N1 influenza virus by using monoclonal antibodies. J Virol. 81(23):12911-12917.
16. Kosakovsky Pond SL, Frost SDW. 2005a. A simple hierarchical approach to modeling distributions of substitution rates. Mol Biol Evol. 22:223-234.
17. Kosakovsky Pond SL, Frost SDW. 2005b. A genetic algorithm approach to detecting lineage-specific variation in selection pressure. Mol Biol Evol. 22(3):478-485.
18. Kosakovsky Pond SL, Frost SDW. 2005c. Not so different after all: a comparison of methods for detecting amino acid sites under selection. Mol Biol Evol. 22(5):1208-1222.
19. Kosakovsky Pond SL, Frost SDW, Muse SV. 2005. HyPhy: hypothesis testing using phylogenies. Bioinformatics. 21(5):676-679.
20. Kosakovsky Pond SL, Posada D, Gravenor MB, Woelk CH, Frost SD. 2006. Automated phylogenetic detection of recombination using a genetic algorithm. Mol Biol Evol. 23(10):1891-1901.
21. Kosiol C, Holmes I, Goldman N. 2007. An empirical codon model for protein sequence evolution. Mol Biol Evol. 24(7):1464-1479.
22. Lindstrom S, Sugita S, Endo A, Ishida M, Huang P, Xi SH, Nerome K. 1996. Evolutionary characterization of recent human H3N2 influenza A isolates from Japan and China: novel changes in the receptor binding domain. Arch Virol. 141(7):1349-1355.
23. Maddison DR, Swofford DL, Maddison WP. 1997. NEXUS: an extensible file format for systematic information. Syst Biol. 46(4):590-621.
24. McClellan DA, McCracken KG. 2001. Estimating the influence of selection on the variable amino acid sites of the cytochrome b protein functional domains. Mol Biol Evol. 18(6):917-925.
25. McDonald JH, Kreitman M. 1991. Adaptive protein evolution at the Adh locus in Drosophila. Nature. 351(6328):652-654.
26. Miyata T, Yasunaga T. 1980. Molecular evolution of mRNA: a method for estimating evolutionary rates of synonymous and amino acid substitutions from homologous nucleotide sequences and its application. J Mol Evol. 16(1):23-36.
27. Moler C, Van Loan C. 1978. Nineteen dubious ways to compute the exponential of a matrix. Siam Rev. 20:801-836.
28. Munk K, Pritzer E, Kretzschmar E, Gutte B, Garten W, Klenk HD. 1992. Carbohydrate masking of an antigenic epitope of influenza virus haemagglutinin independent of oligosaccharide size. Glycobiology. 2(3):233-240.
29. Muse SV. 1995. Evolutionary analyses of DNA sequences subject to constraints on secondary structure. Genetics. 139:1429-1439.
30. Muse SV. 1996. Estimating synonymous and nonsynonymous substitution rates. Mol Biol Evol. 13(1):105-114.
31. Muse SV, Gaut BS. 1994. A likelihood approach for comparing synonymous and nonsynonymous nucleotide substitution rates, with application to the chloroplast genome. Mol Biol Evol. 11:715-724.
32. Nei M. 2005. Selectionism and neutralism in molecular evolution. Mol Biol Evol. 22(12):2318-2342.
33. Nei M, Gojobori T. 1986. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol. 3:418-426.
34. Nelson MI, Holmes EC. 2007. The evolution of epidemic influenza. Nat Rev Genet. 8(3):196-205.
35. Nelson MI, Simonsen L, Viboud C, Miller MA, Holmes EC. 2007. Phylogenetic analysis reveals the global migration of seasonal influenza A viruses. PLoS Pathog. 3(9):1220-1228.
36. Nelson MI, Viboud C, Simonsen L, et al. (12 co-authors). 2008. Multiple reassortment events in the evolutionary history of H1N1 influenza A virus since 1918. PLoS Pathog. 4(2):e1000012.
37. Nickle DC, Heath L, Jensen MA, Gilbert PB, Mullins JI, Kosakovsky Pond SL. 2007. HIV-specific probabilistic models of protein evolution. PLoS ONE. 2:e503.
38. Nielsen R, Yang ZH. 1998. Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene. Genetics. 148:929-936.
39. Pupko T, Pe'er I, Shamir R, Graur D. 2000. A fast algorithm for joint reconstruction of ancestral amino acid sequences. Mol Biol Evol. 17:890-896.
40. Quesenberry C, Hurst D. 1964. Large-sample simultaneous confidence intervals for multinomial proportions. Techonometrics. 6:191-195.
41. Ray SC, Fanning L, Wang X-H, Netski DM, Kenny-walsh E, Thomas DL. 2005. Divergent and convergent evolution after a common-source outbreak of hepatitis C virus. J Exp Med. 201(11):1753-1759.
42. Russell CA, Jones TC, Barr IG, et al. (28 co-authors). 2008. The global circulation of seasonal influenza A (H3N2) viruses. Science. 320(5874):340-346.
43. Sabeti PC, Schaffner SF, Fry B, Lohmueller J, Varilly P, Shamovsky O, Palma A, Mikkelsen TS, Altshuler D, Lander ES. 2006. Positive natural selection in the human lineage. Science. 312(5780):1614-1620.
44. Saitou N, Nei M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 4(4):406-425.
45. Self SG, Liang KY. 1987. Asymptotic properties of maximum likelihood estimators and likelihood ratio tests under nonstandard conditions. J Am Stat Assoc. 82(398):605-1310.
46. Seoighe C, Ketwaroo F, Pillay V, et al. (11 co-authors). 2007. A model of directional selection applied to the evolution of drug resistance in HIV-1. Mol Biol Evol. 24(4):1025-1031.
47. Shih AC-C, Hsiao T-C, Ho M-S, Li W-H. 2007. Simultaneous amino acid substitutions at antigenic sites drive influenza A hemagglutinin evolution. Proc Natl Acad Sci USA. 104(15):6283-6288.
48. Siepel A, Haussler D. 2004. Phylogenetic estimation of context-dependent substitution rates by maximum likelihood. Mol Biol Evol. 21:468-488.
49. Smith DJ, Lapedes AS, de Jong JC, Bestebroer TM, Rimmelzwaan GF, Osterhaus ADME, Fouchier RAM. 2004. Mapping the antigenic and genetic evolution of influenza virus. Science. 305(5682):371-376.
50. Stanfel L. 1996. A new approach to clustering the amino acids. J Theor Biol. 183(2):195-205.
51. Stevens J, Blixt O, Tumpey TM, Taubenberger JK, Paulson JC, Wilson IA. 2006. Structure and receptor specificity of the hemagglutinin from an H5N1 influenza virus. Science. 312(5772):404-410.
52. Suzuki Y. 2006. Natural selection on the influenza virus genome. Mol Biol Evol. 23(10):1902-1911.
53. Suzuki Y, Nei M. 2004. False-positive selection identified by ML-based methods: examples from the Sig1 gene of the diatom Thalassiosira weissflogii and the tax gene of a human T-cell lymphotropic virus. Mol Biol Evol. 21(5):914-921.
54. Swanson WJ, Nielsen R, Yang Q. 2003. Pervasive adaptive evolution in mammalian fertilization proteins. Mol Biol Evol. 20(1):18-20.
55. Tamura K, Nei M. 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. Wang M, Lamberth K, Harndahl M, et al. (15 co-authors). 2007. CTL epitopes for influenza A including the H5N1 bird flu; genome-, pathogen-, and hla-wide screening. Vaccine. 25(15):2823-2831.
57. Webster RG, Govorkova EA. 2006. H5N1 influenza-continuing evolution and spread. N Engl J Med. 355(21):2174-2177.
58. Whelan S, Goldman N. 2001. A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol. 18:691-699.
59. Wilson IA, Skehel JJ, Wiley DC. 1981. Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3 Å resolution. Nature. 289(5796):366-373.
60. Xia X, Li WH. 1998. What amino acid properties affect protein evolution? J Mol Evol. 47(5):557-564.
61. Yampolsky LY, Stoltzfus A. 2005. The exchangeability of amino acids in proteins. Genetics. 170(4):1459-1472.
62. Yang Z. 1998. Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution. Mol Biol Evol. 15:568-573.
63. Yang Z, Kumar S, Nei M. 1995. A new method of inference of ancestral nucleotide and amino acid sequences. Genetics. 141:1641-1650.
64. Yang Z, Nielsen R, Goldman N, Pedersen AM. 2000. Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics. 155(1):431-449.
65. Yang ZH. 2000. Maximum likelihood estimation on large phylogenies and analysis of adaptive evolution in human influenza virus A. J Mol Evol. 51:423-432.
66. Yang ZH, Nielsen R. 2002. Codon-substitution models for detecting molecular adaptation at individual sites along specific lineages. Mol Biol Evol. 19:908-917.