The combined effect of oseltamivir and favipiravir on influenza a virus evolution

Genome Biology and Evolution

Volumn 9, Issue 7, 2017, Pages 1913-1924

  Ormond, Louise ^a,b   Liu, Ping ^c   Matuszewski, Sebastian ^a,b   Renzette, Nicholas ^b,c   Bank, Claudia ^a,b,d   Zeldovich, Konstantin ^c   Bolon, Daniel N ^c   Kowalik, Timothy F ^c   Finberg, Robert W ^c   Jensen, Jeffrey D ^a,b,e   Wang, Jennifer P ^c  

^a EPFL   (Switzerland)

^b SWISS INSTITUTE OF BIOINFORMATICS   (Switzerland)

^c UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^d INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

^e ARIZONA STATE UNIVERSITY   (United States)

Author keywords

Genetic hitchhiking; Influenza; Mutational meltdown; Population genetics

Indexed keywords

AMIDE; ANTIVIRUS AGENT; FAVIPIRAVIR; OSELTAMIVIR; PYRAZINE DERIVATIVE;

ANIMAL; CELL LINE; CLASSIFICATION; DOG; DRUG EFFECTS; EVOLUTION; INFLUENZA A VIRUS; MUTATION RATE; ORTHOMYXOVIRUS INFECTION; POPULATION GENETICS; VIROLOGY;

AMIDES; ANIMALS; ANTIVIRAL AGENTS; BIOLOGICAL EVOLUTION; CELL LINE; DOGS; GENETICS, POPULATION; INFLUENZA A VIRUS; MUTATION RATE; ORTHOMYXOVIRIDAE INFECTIONS; OSELTAMIVIR; PYRAZINES;

EID: 85028394569     PISSN: None     EISSN: 17596653     Source Type: Journal    
DOI: 10.1093/gbe/evx138     Document Type: Article

References (55)

1. Bank C, et al. 2016. An experimental evaluation of drug-induced mutational meltdown as an antiviral treatment strategy. Evolution 70:2470-2484.
2. Baranovich T, et al. 2013. T-705 (favipiravir) induces lethal mutagenesis in nfluenza A H1N1 viruses in vitro. J Virol. 87:3741-3751.
3. Barton NH. 2010. Genetic linkage and natural selection. Philos Trans R Soc Lond B Biol Sci. 365:2559-2569.
4. Bergstrom CT, Pritchard J. 1998. Germline bottlenecks and the evolutionary maintenance of mitochondrial genomes. Genetics 149:2135-2146.
5. Bloom JD, Gong LI, Baltimore D. 2010. Permissive secondary mutations enable the evolution of influenza oseltamivir resistance. Science 328:1272-1275.
6. Bouvier NM, Rahmat S, Pica N. 2012. Enhanced mammalian transmissibility of seasonal influenza A/H1N1 viruses encoding an oseltamivir-resistant neuraminidase. J Virol. 86:7268-7279.
7. Butler J, et al. 2014. Estimating the fitness advantage conferred by permissive neuraminidase mutations in recent oseltamivir-resistant A(H1N1)pdm09 influenza viruses. PLoS Pathog. 10:e1004065.
8. Charlesworth B. 2009. Fundamental concepts in genetics: effective population size and patterns of molecular evolution and variation. Nat Rev Genet. 10:195-205.
9. Charlesworth B, Charlesworth D. 1997. Rapid fixation of deleterious alleles can be caused by Muller's ratchet. Genet Res. 70:63-73.
10. Charlesworth B, Morgan MT, Charlesworth D. 1993. The effect of deleterious mutations on neutral molecular variation. Genetics 134:1289-1303.
11. Cheung PP, et al. 2014. Generation and characterization of influenza A viruses with altered polymerase fidelity. Nat Commun. 5:4794.
12. Collins PJ, et al. 2008. Crystal structures of oseltamivir-resistant influenza virus neuraminidase mutants. Nature 453:1258-1261.
13. Daniels RS, et al. 1985. Fusion mutants of the influenza virus hemagglutinin glycoprotein. Cell 40:431-439.
14. Ewens WJ. 1967. The probability of survival of a mutant. Heredity 22:307-310.
15. Felsenstein J. 1974. The evolutionary advantage of recombination. Genetics 78:737-756.
16. Fisher RA. 1930. The genetical theory of natural selection. Oxford: Oxford University Press.
17. Foll M, et al. 2014. Influenza virus drug resistance: a time-sampled population genetics perspective. PLoS Genet. 10:e1004185.
18. Furuta Y, et al. 2013. Favipiravir (T-705), a novel viral RNA polymerase inhibitor. Antiviral Res. 100:446-454.
19. Ghedin E, et al. 2012. Presence of oseltamivir-resistant pandemic A/H1N1 minor variants before drug therapy with subsequent selection and transmission. J Infect Dis. 206:1504-1511.
20. Ginting TE, et al. 2012. Amino acid changes in hemagglutinin contribute to the replication of oseltamivir-resistant H1N1 influenza viruses. J Virol. 86:121-127.
21. Gordo I, Charlesworth B. 2000a. On the speed of Muller's ratchet. Genetics 156:2137-2140.
22. Gordo I, Charlesworth B. 2000b. The degeneration of asexual haploid populations and the speed of Muller's ratchet. Genetics 154:1379-1387.
23. Gordo I, Charlesworth B. 2001. The speed of Muller's ratchet with background selection, and the degeneration of Y chromosomes. Genet Res. 78:149-161.
24. Grande-Pérez A, Sierra S, Castro MG, Domingo E, Lowenstein PR. 2002. Molecular indetermination in the transition to error catastrophe: systematic elimination of lymphocytic choriomeningitis virus through mutagenesis does not correlate linearly with large increases in mutant spectrum complexity. Proc Natl Acad Sci USA. 99:12938-12943.
25. Grenfell BT, et al. 2004. Unifying the epidemiological and evolutionary dynamics of pathogens. Science 303:327-332.
26. Gubareva LV, Kaiser L, Matrosovich MN, Soo-Hoo Y, Hayden FG 2001. Selection of influenza virus mutants in experimentally infected volunteers treated with oseltamivir. J Infect Dis. 183:523-531.
27. Haigh J. 1978. The accumulation of deleterious genes in a population-Muller's Ratchet. Theor Popul Biol. 14:251-267.
28. Hill WG, Robertson A. 1966. The effect of linkage on limits to artificial selection. Genet Res. 8:269-294.
29. Irwin KK, et al. 2016. On the importance of skewed offspring distributions and background selection in virus population genetics. Heredity 117:393-399.
30. Ives JA, et al. 2002. The H274Y mutation in the influenza A/H1N1 neur-aminidase active site following oseltamivir phosphate treatment leave virus severely compromised both in vitro and in vivo. Antiviral Res. 55:307-317.
31. Jin H, Leser GP, Zhang J, Lamb RA 1997. Influenza virus hemagglutinin and neuraminidase cytoplasmic tails control particle shape. EMBO J. 16:1236-1247.
32. Jorde PE, Ryman N. 2007. Unbiased estimator for genetic drift and effective population size. Genetics 177:927-935.
33. Loeb LA, et al. 1999. Lethal mutagenesis of HIV with mutagenic nucleoside analogs. Proc Natl Acad Sci USA. 96:1492-1497.
34. Loeb LA, Mullins JI 2000. Lethal mutagenesis of HIV by mutagenic ribo-nucleoside analogs. AIDS Res Hum Retroviruses 16:1-3.
35. Lynch M, Bürger R, Butcher D, Gabriel W. 1993. The mutational meltdown in asexual populations. J Hered. 84:339-344.
36. Maynard Smith J, Haigh J. 1974. The hitch-hiking effect of a favourable gene. Genet Res. 23:23-35.
37. McVean GA, Charlesworth B. 2000. The effects of Hill-Robertson interference between weakly selected mutations on patterns of molecular evolution and variation. Genetics 155:929-944.
38. Meijer A, et al. 2014. Global update on the susceptibility of human influenza viruses to neuraminidase inhibitors, 2012-2013. Antiviral Res. 110:31-41.
39. Mitchison DA. 2012. Prevention of drug resistance by combined drug treatment of tuberculosis. Handb Exp Pharmacol. 211:87-98.
40. Moscona A. 2005. Oseltamivir resistance-disabling our influenza defenses. N Engl J Med. 353:2633-2636.
41. Moscona A. 2009. Global transmission of oseltamivir-resistant influenza. N Engl J Med. 360:953-956.
42. Muller HJ. 1932. Some genetic aspects of sex. Am Nat. 66:118-138.
43. Muller HJ. 1964. The relation of recombination to mutational advance. Mutat Res. 106:2-9.
44. Noton SL, et al. 2007. Identification of the domains of the influenza A virus M1 matrix protein required for NP binding, oligomerization and incorporation into virions. J Gen Virol. 88:2280-2290.
45. Noton SL, et al. 2009. Studies of an influenza Avirus temperature-sensitive mutant identify a late role for NP in the formation of infectious virions. J Virol. 83:562-571.
46. Pariente N, Sierra S, Lowenstein PR, Domingo E. 2001. Efficient virus extinction by combinations of a mutagen and antiviral inhibitors. J Virol. 75:9723-9730.
47. Reed ML, et al. 2009. Amino acid residues in the fusion peptide pocket regulate the pH of activation of the H5N1 influenza virus hemagglutinin protein. J Virol. 83:3568-3580.
48. Rossman JS, Lamb RA 2011. Influenza virus assembly and budding. Virology 411:229-236.
49. Sierra S, Davila M, Lowenstein PR, Domingo E. 2000. Response of foot-and-mouth disease virus to increased mutagenesis: influence of vira load and fitness in loss of infectivity. J Virol. 74:8316-8323.
50. Smee DF, Tarbet EB, Furuta Y, Morrey JD, Barnard DL 2013. Synergistic combinations of favipiravir and oseltamivir against wild-type pandemic and oseltamivir-resistant influenza A virus infections in mice. Future Virol. 8:1085-1094.
51. Takashita E, et al. 2015. Global update on the susceptibility of human nfluenza viruses to neuraminidase inhibitors, 2013-2014. Antiviral Res. 117:27-38.
52. Thoennes S, et al. 2008. Analysis of residues near the fusion peptide in the nfluenza hemagglutinin structure for roles in triggering membrane fusion. Virology 370:403-414.
53. Varghese JN, et al. 1998. Drug design against a shifting target: a structural basis for resistance to inhibitors in a variant of influenza virus neuraminidase. Structure 6:735-746.
54. Ward J Jr. 1963. Hierarchical grouping to optimize an objective function. J Am Stat Assoc. 58:236-244.
55. Wright S. 1931. Evolution in Mendelian populations. Genetics 16:97-159.