#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Estimating the Fitness Advantage Conferred by Permissive Neuraminidase Mutations in Recent Oseltamivir-Resistant A(H1N1)pdm09 Influenza Viruses


Antimicrobial resistance is an increasing problem for the treatment of infectious diseases. In 2007–2008 human seasonal A(H1N1) influenza viruses rapidly acquired resistance to the most commonly used anti-influenza drug oseltamivir, via a H275Y amino acid mutation within the neuraminidase (NA) protein. In 2009 the oseltamivir sensitive A(H1N1)pdm09 virus (encoding NA 275H) emerged in the human population, rapidly replacing the oseltamivir resistant seasonal A(H1N1) virus. However, there is increasing concern that currently circulating A(H1N1)pdm09 viruses may similarly acquire oseltamivir resistance (via the NA H275Y mutation) and become widespread. Here we demonstrate that two novel amino acid changes present in virtually all recent A(H1N1)pdm09 viruses (NA V241I and N369K) enable the acquisition of the NA H275Y oseltamivir resistance mutation without compromising viral fitness. As such recent A(H1N1)pdm09 viruses are now one step closer to acquiring widespread oseltamivir resistance.


Vyšlo v časopise: Estimating the Fitness Advantage Conferred by Permissive Neuraminidase Mutations in Recent Oseltamivir-Resistant A(H1N1)pdm09 Influenza Viruses. PLoS Pathog 10(4): e32767. doi:10.1371/journal.ppat.1004065
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004065

Souhrn

Antimicrobial resistance is an increasing problem for the treatment of infectious diseases. In 2007–2008 human seasonal A(H1N1) influenza viruses rapidly acquired resistance to the most commonly used anti-influenza drug oseltamivir, via a H275Y amino acid mutation within the neuraminidase (NA) protein. In 2009 the oseltamivir sensitive A(H1N1)pdm09 virus (encoding NA 275H) emerged in the human population, rapidly replacing the oseltamivir resistant seasonal A(H1N1) virus. However, there is increasing concern that currently circulating A(H1N1)pdm09 viruses may similarly acquire oseltamivir resistance (via the NA H275Y mutation) and become widespread. Here we demonstrate that two novel amino acid changes present in virtually all recent A(H1N1)pdm09 viruses (NA V241I and N369K) enable the acquisition of the NA H275Y oseltamivir resistance mutation without compromising viral fitness. As such recent A(H1N1)pdm09 viruses are now one step closer to acquiring widespread oseltamivir resistance.


Zdroje

1. Hahne S, Donker T, Meijer A, Timen A, van Steenbergen J, et al.. (2009) Epidemiology and control of influenza A(H1N1)v in the Netherlands: the first 115 cases. Euro Surveill 14: : pii = 19267.

2. CaoB, LiXW, MaoY, WangJ, LuHZ, et al. (2009) Clinical features of the initial cases of 2009 pandemic influenza A (H1N1) virus infection in China. N Engl J Med 361: 2507–2517.

3. MontoAS, McKimm-BreschkinJL, MackenC, HampsonAW, HayA, et al. (2006) Detection of influenza viruses resistant to neuraminidase inhibitors in global surveillance during the first 3 years of their use. Antimicrob Agents Chemother 50: 2395–2402.

4. EscuretV, FrobertE, Bouscambert-DuchampM, SabatierM, GrogI, et al. (2008) Detection of human influenza A (H1N1) and B strains with reduced sensitivity to neuraminidase inhibitors. J Clin Virol 41: 25–28.

5. NISN (2005) Use of influenza antivirals during 2003-2004 and monitoring of neuraminidase inhibitor resistance. Wkly Epidemiol Rec 80: 156.

6. HurtAC, BarrIG (2008) Influenza viruses with reduced sensitivity to the neuraminidase inhibitor drugs in untreated young children. Commun Dis Intell Q Rep 32: 57–62.

7. SheuTG, DeydeVM, Okomo-AdhiamboM, GartenRJ, XuX, et al. (2008) Surveillance for neuraminidase inhibitor resistance among human influenza A and B viruses circulating worldwide from 2004 to 2008. Antimicrob Agents Chemother 52: 3284–3292.

8. IvesJA, CarrJA, MendelDB, TaiCY, LambkinR, et al. (2002) The H274Y mutation in the influenza A/H1N1 neuraminidase active site following oseltamivir phosphate treatment leave virus severely compromised both in vitro and in vivo. Antiviral Res 55: 307–317.

9. AbedY, GoyetteN, BoivinG (2004) A reverse genetics study of resistance to neuraminidase inhibitors in an influenza A/H1N1 virus. Antivir Ther 9: 577–581.

10. HerlocherML, TrusconR, EliasS, YenHL, RobertsNA, et al. (2004) Influenza viruses resistant to the antiviral drug oseltamivir: transmission studies in ferrets. J Infect Dis 190: 1627–1630.

11. HaugeSH, DudmanS, BorgenK, LackenbyA, HungnesO (2009) Oseltamivir-resistant influenza viruses A (H1N1), Norway, 2007-08. Emerg Infect Dis 15: 155–162.

12. MosconaA (2009) Global transmission of oseltamivir-resistant influenza. N Engl J Med 360: 953–956.

13. MeijerA, LackenbyA, HungnesO, LinaB, van-der-WerfS, et al. (2009) Oseltamivir-resistant influenza virus A (H1N1), Europe, 2007-08 season. Emerg Infect Dis 15: 552–560.

14. HurtAC, ErnestJ, DengYM, IannelloP, BesselaarTG, et al. (2009) Emergence and spread of oseltamivir-resistant A(H1N1) influenza viruses in Oceania, South East Asia and South Africa. Antiviral Res 83: 90–93.

15. BloomJD, GongLI, BaltimoreD (2010) Permissive secondary mutations enable the evolution of influenza oseltamivir resistance. Science 328: 1272–1275.

16. BouvierNM, RahmatS, PicaN (2012) Enhanced mammalian transmissibility of seasonal influenza A/H1N1 viruses encoding an oseltamivir-resistant neuraminidase. J Virol 86: 7268–7279.

17. AbedY, PizzornoA, BouhyX, BoivinG (2011) Role of permissive neuraminidase mutations in influenza A/Brisbane/59/2007-like (H1N1) viruses. PLoS Pathog 7: e1002431.

18. WolfeC, GreenwaldI, ChenL (2010) Pandemic (H1N1) 2009 and oseltamivir resistance in hematology/oncology patients. Emerg Infect Dis 16: 1809–1811.

19. MooreC, GalianoM, LackenbyA, AbdelrahmanT, BarnesR, et al. (2011) Evidence of person-to-person transmission of oseltamivir-resistant pandemic influenza A(H1N1) 2009 virus in a hematology unit. J Infect Dis 203: 18–24.

20. ChenLF, DaileyNJ, RaoAK, FleischauerAT, GreenwaldI, et al. (2011) Cluster of oseltamivir-resistant 2009 pandemic influenza A (H1N1) virus infections on a hospital ward among immunocompromised patients—North Carolina, 2009. J Infect Dis 203: 838–846.

21. CDC (2009) Oseltamivir-resistant 2009 pandemic influenza A (H1N1) virus infection. Morb Mortal Wkly Rep 58: 969–972.

22. LeQM, WertheimHF, TranND, van DoornHR, NguyenTH, et al. (2010) A community cluster of oseltamivir-resistant cases of 2009 H1N1 influenza. N Engl J Med 362: 86–87.

23. StormsAD, GubarevaLV, SuS, WheelingJT, Okomo-AdhiamboM, et al. (2012) Oseltamivir-resistant pandemic (H1N1) 2009 virus infections, United States, 2010-11. Emerg Infect Dis 18: 308–311.

24. Lackenby A, Moran Gilad J, Pebody R, Miah S, Calatayud L, et al.. (2011) Continued emergence and changing epidemiology of oseltamivir-resistant influenza A(H1N1)2009 virus, United Kingdom, winter 2010/11. Euro Surveill 16: : pii = 19784.

25. HurtAC, HardieK, WilsonNJ, DengYM, OsbournM, et al. (2011) Community transmission of oseltamivir-resistant A(H1N1)pdm09 influenza. N Engl J Med 365: 2541–2542.

26. HurtAC, HardieK, WilsonNJ, DengYM, OsbournM, et al. (2012) Characteristics of a widespread community cluster of H275Y oseltamivir-resistant A(H1N1)pdm09 influenza in Australia. J Infect Dis 206: 148–157.

27. HurtAC, Nor'eSS, McCawJM, FryerHR, MosseJ, et al. (2010) Assessing the viral fitness of oseltamivir-resistant influenza viruses in ferrets, using a competitive-mixtures model. J Virol 84: 9427–9438.

28. NHMRC (2004) Australian code of practice for the care and use of animals for scientific purposes. http://www.nhmrc.gov.au/_files_nhmrc/publications/attachments/ea16.pdf.

29. ReedLJ, MuenchH (1938) A simple method of estimating fifty per cent endpoints. AM J Epidemiol 27: 493–497.

30. BarrIG, KomadinaN, HurtA, ShawR, DurrantC, et al. (2003) Reassortants in recent human influenza A and B isolates from South East Asia and Oceania. Virus Res 98: 35–44.

31. HoffmannE, NeumannG, KawaokaY, HobomG, WebsterRG (2000) A DNA transfection system for generation of influenza A virus from eight plasmids. Proc Natl Acad Sci USA 97: 6108–6113.

32. BloomJD, NayakJS, BaltimoreD (2011) A computational-experimental approach identifies mutations that enhance surface expression of an oseltamivir-resistant influenza neuraminidase. PLoS One 6: e22201.

33. YenHL, McKimm-BreschkinJL, ChoyKT, WongDD, CheungPP, et al. (2013) Resistance to neuraminidase inhibitors conferred by an R292K mutation in a human influenza virus H7N9 isolate can be masked by a mixed R/K viral population. MBio 4: e00396–13.

34. YenHL, HerlocherLM, HoffmannE, MatrosovichMN, MontoAS, et al. (2005) Neuraminidase inhibitor-resistant influenza viruses may differ substantially in fitness and transmissibility. Antimicrob Agents Chemother 49: 4075–4084.

35. HurtAC, BarrIG, KomadinaN, HampsonAW (2004) A novel means of identifying the neuraminidase type of currently circulating human A(H1) influenza viruses. Virus Res 103: 79–83.

36. DengYM, CaldwellN, HurtA, ShawT, KelsoA, et al. (2011) A comparison of pyrosequencing and neuraminidase inhibition assays for the detection of oseltamivir-resistant pandemic influenza A(H1N1) 2009 viruses. Antiviral Res 90: 87–91.

37. McCawJM, ArinaminpathyN, HurtAC, McVernonJ, McLeanAR (2011) A mathematical framework for estimating pathogen transmission fitness and inoculum size using data from a competitive mixtures animal model. PLoS Comput Biol 7: e1002026.

38. PerelsonAS, RibeiroRM (2013) Modeling the within-host dynamics of HIV infection. BMC Biol 11: 96.

39. BeaucheminCA, HandelA (2011) A review of mathematical models of influenza A infections within a host or cell culture: lessons learned and challenges ahead. BMC Public Health 11 Suppl 1S7.

40. SmithAM, PerelsonAS (2011) Influenza A virus infection kinetics: quantitative data and models. Wiley Interdiscip Rev Syst Biol Med 3: 429–445.

41. PinillaLT, HolderBP, AbedY, BoivinG, BeaucheminCA (2012) The H275Y neuraminidase mutation of the pandemic A/H1N1 influenza virus lengthens the eclipse phase and reduces viral output of infected cells, potentially compromising fitness in ferrets. J Virol 86: 10651–10660.

42. PetrieSM, GuarnacciaT, LaurieKL, HurtAC, McVernonJ, et al. (2013) Reducing uncertainty in within-host parameter estimates of influenza infection by measuring both infectious and total viral load. PLoS One 8: e64098.

43. ColmanPM (1994) Influenza virus neuraminidase: structure, antibodies, and inhibitors. Protein Sci 3: 1687–1696.

44. NayakDP, HuiEK, BarmanS (2004) Assembly and budding of influenza virus. Virus Res 106: 147–165.

45. BaoY, BolotovP, DernovoyD, KiryutinB, ZaslavskyL, et al. (2008) The influenza virus resource at the National Center for Biotechnology Information. J Virol 82: 596–601.

46. SeibertCW, KaminskiM, PhilippJ, RubbenstrothD, AlbrechtRA, et al. (2010) Oseltamivir-resistant variants of the 2009 pandemic H1N1 influenza A virus are not attenuated in the guinea pig and ferret transmission models. J Virol 84: 11219–11226.

47. MemoliMJ, DavisAS, ProudfootK, ChertowDS, HrabalRJ, et al. (2011) Multidrug-resistant 2009 pandemic influenza A(H1N1) viruses maintain fitness and transmissibility in ferrets. J Infect Dis 203: 348–357.

48. KisoM, ShinyaK, ShimojimaM, TakanoR, TakahashiK, et al. (2010) Characterization of oseltamivir-resistant 2009 H1N1 pandemic influenza A viruses. PLoS Pathog 6: e1001079.

49. HamelinME, BazM, AbedY, CoutureC, JoubertP, et al. (2010) Oseltamivir-resistant pandemic A/H1N1 virus is as virulent as its wild-type counterpart in mice and ferrets. PLoS Pathog 6: e1001015.

50. AbedY, PizzornoA, BouhyX, RheaumeC, BoivinG (2014) Impact of Potential Permissive Neuraminidase Mutations on Viral Fitness of the H275Y Oseltamivir-Resistant Influenza A(H1N1)pdm09 Virus In Vitro, in Mice and in Ferrets. J Virol 88: 1652–1658.

51. DuanS, BoltzDA, SeilerP, LiJ, BragstadK, et al. (2010) Oseltamivir-resistant pandemic H1N1/2009 influenza virus possesses lower transmissibility and fitness in ferrets. PLoS Pathog 6: e1001022.

52. WHO (2013) Influenza. http://www.who.int/influenza/gisrs_laboratory/flunet/en/.

53. Takashita E, Ejima M, Itoh R, Miura M, Ohnishi A, et al.. (2014) A community cluster of influenza A(H1N1)pdm09 virus exhibiting cross-resistance to oseltamivir and peramivir in Japan, November to December 2013. Euro Surveill 19: : pii = 20666.

54. NIID (2014) Weekly reports of influenza virus isolation/detection, from week 18 of 2013 to week 6 of 2014, Japan. http://www.nih.go.jp/niid/images/iasr/rapid/inf/2014_6w/sinin1e_140206.gif.

55. NIID (2014) Detection of A(H1N1)pdm09 viruses with H275Y mutation in Japan. http://www.nih.go.jp/niid/images/flu/resistance/20140203/dr13-14e20140203-2.gif.

56. CNIC (2014) Chinese Influenza Weekly Report, Week 04 2014. www.cnic.org.cn/eng/show.php?contentid=691.

57. KelsoA, HurtAC (2012) The ongoing battle against influenza: Drug-resistant influenza viruses: why fitness matters. Nat Med 18: 1470–1471.

58. HurtAC, ButlerJ, KelsoA, BarrIG (2012) Influenza antivirals and resistance: the next 10 years? Expert Rev Anti Infect Ther 10: 1221–1223.

59. ThorlundK, AwadT, BoivinG, ThabaneL (2011) Systematic review of influenza resistance to the neuraminidase inhibitors. BMC Infect Dis 11: 134.

60. HaydenFG (2013) Newer influenza antivirals, biotherapeutics and combinations. Influenza Other Respir Viruses 7 Suppl 163–75.

Štítky
Hygiena a epidemiológia Infekčné lekárstvo Laboratórium

Článok vyšiel v časopise

PLOS Pathogens


2014 Číslo 4
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autori: MUDr. Tomáš Ürge, PhD.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#