Stability-mediated epistasis constrains the evolution of an influenza protein

eLife

Volumn 2013, Issue 2, 2013, Pages

  Gong, Lizhi Ian ^a   Suchard, Marc A ^b   Bloom, Jesse D ^a  

^a Fred Hutchinson Cancer Research Center   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; INFLUENZA PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ARTICLE; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; EPISTASIS; GENE MUTATION; HUMAN; HUMAN CELL; MOLECULAR EVOLUTION; NONHUMAN; PROTEIN STABILITY; RNA TRANSCRIPTION; TRANSCRIPTION INITIATION; VIROGENESIS; GENETICS; METABOLISM; MUTATION; ORTHOMYXOVIRUS;

EPISTASIS, GENETIC; EVOLUTION, MOLECULAR; HUMANS; MUTATION; ORTHOMYXOVIRIDAE; VIRAL PROTEINS;

EID: 84879064073     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.00631     Document Type: Article

References (55)

1. Alexander J, Bilsel P, del Guercio MF, Marinkovic-Petrovic A, Southwood S, Stewart S, et al. 2010. Identification of broad binding class I HLA supertype epitopes to provide universal coverage of influenza A virus. Hum Immunol 71:468-74. doi: 10.1016/j.humimm.2010.02.014.
2. Assarsson E, Bui HH, Sidney J, Zhang Q, Glenn J, Oseroff C, et al. 2008. Immunomic analysis of the repertoire of T-cell specificities for influenza A virus in humans. J Virol 82:12241-51. doi: 10.1128/JVI.01563-08.
3. Baresic A, Hopcroft LE, Rogers HH, Hurst JM, Martin AC. 2010. Compensated pathogenic deviations: analysis of structural effects. J Mol Biol 396:19-30. doi: 10.1016/j.jmb.2009.11.002.
4. Berkhoff EG, Boon AC, Nieuwkoop NJ, Fouchier RA, Sintnicolaas K, Osterhaus AD, et al. 2004. A mutation in the HLA-B*2705-restricted NP383-391 epitope affects the human influenza A virus-specific cytotoxic T-lymphocyte response in vitro. J Virol 78:5216-22. doi: 10.1128/JVI.78.10.5216-5222.2004.
5. Berkhoff EG, de Wit E, Geelhoed-Mieras MM, Boon AC, Symons J, Fouchier RA, et al. 2005. Functional constraints of influenza A virus epitopes limit escape from cytotoxic T lymphocytes. J Virol 79:11239-46. doi: 10.1128/JVI.79.17.11239-11246.2005.
6. Berkhoff EG, de Wit E, Geelhoed-Mieras MM, Boon AC, Symons J, Fouchier RA, et al. 2006. Fitness costs limit escape from cytotoxic T lymphocytes by influenza A viruses. Vaccine 24:6594-6. doi: 10.1016/j.vaccine.2006.05.051.
7. Berkhoff EG, Geelhoed-Mieras MM, Fouchier RA, Osterhaus AD, Rimmelzwaan GF. 2007. Assessment of the extent of variation in influenza A virus cytotoxic T-lymphocyte epitopes by using virus-specific CD8+ T-cell clones. J Gen Virol 88:530-5. doi: 10.1099/vir.0.82120-0.
8. Bershtein S, Segal M, Bekerman R, Tokuriki N, Tawfik DS. 2006. Robustness-epistasis link shapes the fitness landscape of a randomly drifting protein. Nature 444:929-32. doi: 10.1038/nature05385.
9. Bhatt S, Holmes EC, Pybus OG. 2011. The genomic rate of molecular adaptation of the human influenza A virus. Mol Biol Evol 28:2443-51. doi: 10.1093/molbev/msr044.
10. Bloom JD, Gong LI, Baltimore D. 2010. Permissive secondary mutations enable the evolution of influenza oseltamivir resistance. Science 328:1272-5. doi: 10.1126/science.1187816.
11. Bloom JD, Labthavikul ST, Otey CR, Arnold FH. 2006. Protein stability promotes evolvability. Proc Natl Acad Sci USA 103:5869-74. doi: 10.1073/pnas.0510098103.
12. Bloom JD, Raval A, Wilke CO. 2007. Thermodynamics of neutral protein evolution. Genetics 175:255-66. doi: 10.1534/genetics.106.061754.
13. Blount ZD, Borland CZ, Lenski RE. 2008. Historical contingency and the evolution of a key innovation in an experimental population of Escherichia coli. Proc Natl Acad Sci USA 105:7899-906. doi: 10.1073/pnas.0803151105.
14. Bridgham JT, Ortlund EA, Thornton JW. 2009. An epistatic ratchet constrains the direction of glucocorticoid receptor evolution. Nature 461:515-9. doi: 10.1038/nature08249.
15. Chang MW, Torbett BE. 2011. Accessory mutations maintain stability in drug-resistant HIV-1 protease. J Mol Biol 410:756-60. doi: 10.1016/j.jmb.2011.03.038.
16. Chen W, Calvo PA, Malide D, Gibbs J, Schubert U, Bacik I, et al. 2001. A novel influenza A virus mitochondrial protein that induces cell death. Nat Med 7:1306-12. doi: 10.1038/nm1201-1306.
17. Cheung YK, Cheng SC, Ke Y, Xie Y. 2012. Human immunogenic T cell epitopes in nucleoprotein of human influenza A (H5N1) virus. Hong Kong Med J 18(suppl 2):17-21.
18. DePristo MA, Weinreich DM, Hartl DL. 2005. Missense meanderings in sequence space: a biophysical view of protein evolution. Nat Rev Genet 6:678-87. doi: 10.1038/nrg1672.
19. DiBrino M, Parker KC, Margulies DH, Shiloach J, Turner RV, Biddison WE, et al. 1995. Identification of the peptide binding motif for HLA-B44, one of the most common HLA-B alleles in the Caucasian population. Biochemistry 34:10130-8. doi: 10.1021/bi00032a005.
20. Drummond AJ, Suchard MA, Xie D, Rambaut A. 2012. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29:1969-73. doi: 10.1093/molbev/mss075.
21. Gog JR, Rimmelzwaan GF, Osterhaus AD, Grenfell BT. 2003. Population dynamics of rapid fixation in cytotoxic T lymphocyte escape mutants of influenza A. Proc Natl Acad Sci USA 100:11143-7. doi: 10.1073/pnas.1830296100.
22. Hoffmann E, Neumann G, Kawaoka Y, Hobom G, Webster RG. 2000. A DNA transfection system for generation of influenza A virus from eight plasmids. Proc Natl Acad Sci USA 97:6108-13. doi: 10.1073/pnas.100133697.
23. Imai M, Watanabe T, Hatta M, Das SC, Ozawa M, Shinya K, et al. 2012. Experimental adaptation of an influenza H5 HA confers respiratory droplet transmission to a reassortant H5 HA/H1N1 virus in ferrets. Nature 486:420-8. doi: 10.1038/nature10831.
24. Jones DT, Taylor WR, Thornton JM. 1992. The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8:275-82. doi: 10.1093/bioinformatics/8.3.275.
25. Kimura M. 1985. The role of compensatory neutral mutations in molecular evolution. J Genet 64:7-19. doi: 10.1007/BF02923549.
26. Koelle K, Cobey S, Grenfell B, Pascual M. 2006. Epochal evolution shapes the phylodynamics of interpandemic influenza A (H3N2) in humans. Science 314:1898-903. doi: 10.1126/science.1132745.
27. Kondrashov AS, Sunyaev S, Kondrashov FA. 2002. Dobzhansky-Muller incompatibilities in protein evolution. Proc Natl Acad Sci USA 99:14878-83. doi: 10.1073/pnas.232565499.
28. Kryazhimskiy S, Dushoff J, Bazykin GA, Plotkin JB. 2011. Prevalence of epistasis in the evolution of influenza a surface proteins. PLoS Genet 7:e1001301. doi: 10.1371/journal.pgen.1001301.
29. Lunzer M, Golding GB, Dean AM. 2010. Pervasive cryptic epistasis in molecular evolution. PLoS Genet 6:e1001162. doi: 10.1371/journal.pgen.1001162.
30. Maynard Smith J. 1970. Natural selection and the concept of a protein space. Nature 225:563-4. doi: 10.1038/225563a0.
31. Meer MV, Kondrashov AS, Artzy-Randrup Y, Kondrashov FA. 2010. Compensatory evolution in mitochondrial tRNAs navigates valleys of low fitness. Nature 464:279-82. doi: 10.1038/nature08691.
32. Minin VN, Suchard MA. 2008. Counting labeled transitions in continuous-time Markov models of evolution. J Math Biol 56:391-412. doi: 10.1007/s00285-007-0120-8.
33. Murrell B, Moola S, Mabona A, Weighill T, Sheward D, Kosakovsky Pond SL, et al. 2013. FUBAR: a fast, unconstrained bayesian appRoximation for inferring selection. Mol Biol Evol 30:1196-1205. doi: 10.1093/molbev/mst030.
34. Ng AK, Zhang H, Tan K, Li Z, Liu JH, Chan PK, et al. 2008. Structure of the influenza virus A H5N1 nucleoprotein: implications for RNA binding, oligomerization, and vaccine design. FASEB J 22:3638-47. doi: 10.1096/fj.08-112110.
35. O'Brien JD, Minin VN, Suchard MA. 2009. Learning to count: robust estimates for labeled distances between molecular sequences. Mol Biol Evol 26:801-14. doi: 10.1093/molbev/msp003.
36. Ortlund EA, Bridgham JT, Redinbo MR, Thornton JW. 2007. Crystal structure of an ancient protein: evolution by conformational epistasis. Science 317:1544-8. doi: 10.1126/science.1142819.
37. Portela A, Digard P. 2002. The influenza virus nucleoprotein: a multifunctional RNA-binding protein pivotal to virus replication. J Gen Virol 83:723-34. doi: 10.1099/vir.0.18133-0.
38. Rambaut A, Pybus OG, Nelson MI, Viboud C, Taubenberger JK, Holmes EC. 2008. The genomic and epidemiological dynamics of human influenza A virus. Nature 453:615-9. doi: 10.1038/nature06945.
39. Rimmelzwaan GF, Berkhoff EG, Nieuwkoop NJ, Fouchier RA, Osterhaus AD. 2004a. Functional compensation of a detrimental amino acid substitution in a cytotoxic-T-lymphocyte epitope of influenza a viruses by comutations. J Virol 78:8946-9. doi: 10.1128/JVI.78.16.8946-8949.2004.
40. Rimmelzwaan GF, Boon AC, Voeten JT, Berkhoff EG, Fouchier RA, Osterhaus AD. 2004b. Sequence variation in the influenza A virus nucleoprotein associated with escape from cytotoxic T lymphocytes. Virus Res 103:97-100. doi: 10.1016/j.virusres.2004.02.020.
41. Salverda ML, Dellus E, Gorter FA, Debets AJ, van der Oost J, Hoekstra RF, et al. 2011. Initial mutations direct alternative pathways of protein evolution. PLoS Genet 7:e1001321. doi: 10.1371/journal.pgen.1001321.
42. Smith DJ, Lapedes AS, de Jong JC, Bestebroer TM, Rimmelzwaan GF, Osterhaus AD, et al. 2004. Mapping the antigenic and genetic evolution of influenza virus. Science 305:371-6. doi: 10.1126/science.1097211.
43. Stranzl T, Larsen MV, Lundegaard C, Nielsen M. 2010. NetCTLpan: pan-specific MHC class I pathway epitope predictions. Immunogenetics 62:357-68. doi: 10.1007/s00251-010-0441-4.
44. Taverna DM, Goldstein RA. 2002. Why are proteins marginally stable? Proteins 46:105-9. doi: 10.1002/prot.10016.
45. Tokuriki N, Tawfik DS. 2009. Stability effects of mutations and protein evolvability. Curr Opin Struct Biol 19:596-604. doi: 10.1016/j.sbi.2009.08.003.
46. Valkenburg SA, Rutigliano JA, Ellebedy AH, Doherty PC, Thomas PG, Kedzierska K. 2011. Immunity to seasonal and pandemic influenza A viruses. Microbes Infect 13:489-501. doi: 10.1016/j.micinf.2011.01.007.
47. van Nimwegen E. 2006. Epidemiology. Influenza escapes immunity along neutral networks. Science 314:1884-6. doi: 10.1126/science.1137300.
48. Vita R, Zarebski L, Greenbaum JA, Emami H, Hoof I, Salimi N, et al. 2010. The immune epitope database 2.0. Nucleic Acids Res 38:D854-62. doi: 10.1093/nar/gkp1004.
49. Voeten JT, Bestebroer TM, Nieuwkoop NJ, Fouchier RA, Osterhaus AD, Rimmelzwaan GF. 2000. Antigenic drift in the influenza A virus (H3N2) nucleoprotein and escape from recognition by cytotoxic T lymphocytes. J Virol 74:6800-7. doi: 10.1128/JVI.74.15.6800-6807.2000.
50. Wang X, Minasov G, Shoichet BK. 2002. Evolution of an antibiotic resistance enzyme constrained by stability and activity trade-offs. J Mol Biol 320:85-95. doi: 10.1016/S0022-2836(02)00400-X.
51. Weinreich DM, Delaney NF, Depristo MA, Hartl DL. 2006. Darwinian evolution can follow only very few mutational paths to fitter proteins. Science 312:111-4. doi: 10.1126/science.1123539.
52. Weinreich DM, Watson RA, Chao L. 2005. Perspective: sign epistasis and genetic constraint on evolutionary trajectories. Evolution 59:1165-74. doi: 10.1554/04-272.
53. Ye Q, Guu TS, Mata DA, Kuo RL, Smith B, Krug RM, et al. 2012. Biochemical and structural evidence in support of a coherent model for the formation of the double-helical influenza A virus ribonucleoprotein. MBio 4:e00467-12. doi: 10.1128/mBio.00467-12.
54. Ye Q, Krug RM, Tao YJ. 2006. The mechanism by which influenza A virus nucleoprotein forms oligomers and binds RNA. Nature 444:1078-82. doi: 10.1038/nature05379.
55. Zuckerkandl E, Pauling L. 1965. Evolutionary divergence and convergence in proteins. In: Bryson B, Vogel H, editors. Evolving Genes and Proteins. New York: Academic Press. p. 97-166.