In vitro passaging of a pandemic H1N1/09 virus selects for viruses with neuraminidase mutations conferring high-level resistance to oseltamivir and peramivir, but not to zanamivir

Journal of Antimicrobial Chemotherapy

Volumn 67, Issue 8, 2012, Pages 1874-1883

  Mckimm Breschkin, Jennifer L ^a   Rootes, Christina ^a   Mohr, Peter G ^a   Barrett, Susan ^a   Streltsov, Victor A ^a  

^a CSIRO   (Australia)

Author keywords

Combination therapy; H274Y; Haemagglutinin mutation; Influenza; Neuraminidase inhibitors

Indexed keywords

4 ACETAMIDO 5 AMINO 3 (1 ETHYLPROPOXY) 1 CYCLOHEXENE 1 CARBOXYLIC ACID; HEMAGGLUTININ; PERAMIVIR; SIALIDASE; ZANAMIVIR;

ANTIVIRAL RESISTANCE; ANTIVIRAL SUSCEPTIBILITY; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; ENZYME ASSAY; ERYTHROCYTE; GENE MUTATION; IN VITRO STUDY; INFLUENZA VIRUS A H1N1; NONHUMAN; NUCLEOTIDE SEQUENCE; VIRUS CULTURE;

ANIMALS; CELLS, CULTURED; CYCLOPENTANES; DOGS; DRUG RESISTANCE, VIRAL; GUANIDINES; HUMANS; INFLUENZA A VIRUS, H1N1 SUBTYPE; MOLECULAR SEQUENCE DATA; MUTATION, MISSENSE; NEURAMINIDASE; OSELTAMIVIR; RNA, VIRAL; SELECTION, GENETIC; SEQUENCE ANALYSIS, DNA; SERIAL PASSAGE; ZANAMIVIR;

EID: 84864521358     PISSN: 03057453     EISSN: 14602091     Source Type: Journal    
DOI: 10.1093/jac/dks150     Document Type: Article

References (53)

1. Varghese JN, Smith PW, Sollis SL et al. Drug design against a shifting target: a structural basis for resistance to inhibitors in a variant of influenza virus neuraminidase. Structure 1998; 6: 735-46.
2. Collins PJ, Haire LF, Lin YP et al. Crystal structures of oseltamivirresistant influenza virus neuraminidase mutants. Nature 2008; 453: 1258-61.
3. Smith BJ, McKimm-Breschkin JL, McDonald M et al. Structural studies of the resistance of influenza virus neuramindase to inhibitors. J Med Chem 2002; 45: 2207-12.
4. Hurt AC, Ernest J, Deng YM et al. Emergence and spread of oseltamivir-resistant A(H1N1) influenza viruses in Oceania, South East Asia and South Africa. Antiviral Res 2009; 83: 90-3.
5. Meijer A, Lackenby A, Hungnes O et al. Oseltamivir-resistant influenza virus A (H1N1), Europe, 2007-08 season. Emerg Infect Dis 2009; 15: 552-60.
6. Chen LF, Dailey NJ, Rao AK et al. Cluster of oseltamivir-resistant 2009 pandemic influenza A (H1N1) virus infections on a hospital ward among immunocompromised patients-North Carolina, 2009. J Infect Dis 2011; 203: 838-46.
7. Harvala H, Gunson R, Simmonds P et al. The emergence of oseltamivir-resistant pandemic influenza A(H1N1) 2009 virus amongst hospitalised immunocompromised patients in Scotland, November- December, 2009. Euro Surveill 2010; 15: pii=19536.
8. Tramontana AR, George B, Hurt AC et al. Oseltamivir resistance in adult oncology and hematology patients infected with pandemic (H1N1) 2009 virus, Australia. Emerg Infect Dis 2010; 16: 1068-75.
9. Campanini G, Piralla A, Rovida F et al. First case in Italy of acquired resistance to oseltamivir in an immunocompromised patient with influenza A/H1N1v infection. J Clin Virol 2010; 48: 220-2.
10. Memoli MJ, Hrabal RJ, Hassantoufighi A et al. Rapid selection of oseltamivir- and peramivir-resistant pandemic H1N1 virus during therapy in 2 immunocompromised hosts. Clin Infect Dis 2010; 50: 1252-5.
11. Chan PA, Connell NT, Gabonay AM et al. Oseltamivir-resistant 2009- 2010 pandemic influenza A (H1N1) in an immunocompromised patient. Clin Microbiol Infect 2010; 16: 1576-8.
12. Le QM, Wertheim HF, Tran ND et al. A community cluster of oseltamivir-resistant cases of 2009 H1N1 influenza. N Engl J Med 2010; 362: 86-7.
13. CDC. Oseltamivir-resistant 2009 pandemic influenza A (H1N1) virus infection in two summer campers receiving prophylaxis-North Carolina, 2009. MMWR Morb Mortal Wkly Rep 2009; 58: 969-72.
14. van der Vries E, Stelma FF, Boucher CA. Emergence of a multidrugresistant pandemic influenza A (H1N1) virus. N Engl J Med 2010; 363: 1381-2.
15. Nguyen HT, Fry AM, Loveless PA et al. Recovery of a multidrugresistant strain of pandemic influenza A 2009 (H1N1) virus carrying a dual H275Y/I223R mutation from a child after prolonged treatment with oseltamivir. Clin Infect Dis 2010; 51: 983-4.
16. Smee DF, Hurst BL, Wong MH et al. Combinations of oseltamivir and peramivir for the treatment of influenza A (H1N1) virus infections in cell culture and in mice. Antiviral Res 2010; 88: 38-44.
17. Duval X, van der Werf S, Blanchon T et al. Efficacy of oseltamivirzanamivir combination compared to each monotherapy for seasonal influenza: a randomized placebo-controlled trial. PLoS Med 2010; 7: e1000362.
18. Deng YM, Iannello P, Smith I et al. Transmission of influenza A(H1N1) 2009 pandemic viruses in Australian swine. Influenza Other Respi Viruses 2012; 6: e42-7.
19. Barrett S, Mohr PG, Schmidt PM et al. Real time enzyme inhibition assays provide insights into differences in binding of neuraminidase inhibitors to wild type and mutant influenza viruses. PLoS One 2011; 6: e23627.
20. McKimm-Breschkin JL, Blick TJ, Sahasrabudhe A et al. Generation and characterization of variants of NWS/G70C influenza virus after in vitro passage in 4-amino-Neu5Ac2en and 4-guanidino-Neu5Ac2en. Antimicrob Agents Chemother 1996; 40: 40-6.
21. Potier M, Mameli L, Belisle M et al. Fluorometric assay of neuraminidase with a sodium (4-methylumbelliferyl-a-D-N-acetylneuraminate) substrate. Anal Biochem 1979; 94: 287-96.
22. Oakley AJ, Barrett S, Peat TS et al. Structural and functional basis of resistance to neuraminidase inhibitors of influenza B viruses. J Med Chem 2010; 53: 6421-31.
23. Baum EZ, Wagaman PC, Ly L et al. A point mutation in influenza B neuraminidase confers resistance to peramivir and loss of slow binding. Antiviral Res 2003; 59: 13-22.
24. Kati WM, Saldivar AS, Mohamadi F et al. GS4071 is a slow-binding inhibitor of influenza neuraminidase from both A and B strains. Biochem Biophys Res Commun 1998; 244: 408-13.
25. Pegg MS, von Itzstein M. Slow-binding inhibition of sialidase from influenza virus. Biochem Mol Biol Int 1994; 32: 851-8.
26. von Itzstein M, WuWY, Kok GB et al. Rational design of potent sialidasebased inhibitors of influenza virus replication. Nature 1993; 363: 418-23.
27. Wang MZ, Tai CY, Mendel DB. Mechanism by which mutations at His274 alter sensitivity of influenza a virus N1 neuraminidase to oseltamivir carboxylate and zanamivir. Antimicrob Agents Chemother 2002; 46: 3809-16.
28. Blick TJ, Tiong T, Sahasrabudhe A et al. Generation and characterization of an influenza virus neuraminidase variant with decreased sensitivity to the neuraminidase-specific inhibitor 4-guanidino-Neu5Ac2en. Virology 1995; 214: 475-84.
29. McKimm-Breschkin JL, Sahasrabudhe A, Blick TJ et al. Mutations in a conserved residue in the influenza virus neuraminidase active site decreases sensitivity to Neu5Ac2en-derived inhibitors. J Virol 1998; 72: 2456-62.
30. McKimm-Breschkin JL. Resistance of influenza viruses to neuraminidase inhibitors-a review. Antiviral Res 2000; 47: 1-17.
31. Blick TJ, Sahasrabudhe A, McDonald M et al. The interaction of neuraminidase and hemagglutinin mutations in influenza virus in resistance to 4-guanidino-Neu5Ac2en. Virology 1998; 246: 95-103.
32. Rameix-Welti MA, Enouf V, Cuvelier F et al. Enzymatic properties of the neuraminidase of seasonal H1N1 influenza viruses provide insights for the emergence of natural resistance to oseltamivir. PLoS Pathog 2008; 4: e1000103.
33. Brookes DW, Miah S, Lackenby A et al. Pandemic H1N1 2009 influenza virus with the H275Y oseltamivir resistance neuraminidase mutation shows a small compromise in enzyme activity and viral fitness. J Antimicrob Chemother 2011; 66: 466-70.
34. Gubareva LV, Bethell R, Hart GJ et al. Characterization of mutants of influenza A virus selected with the neuraminidase inhibitor 4-guanidino-Neu5Ac2en. J Virol 1996; 70: 1818-27.
35. Liu Y, Childs RA, Matrosovich T et al. Altered receptor specificity and cell tropism of D222G haemagglutinin mutants from fatal cases of pandemic A(H1N1) 2009 influenza virus. J Virol 2010; 84: 12069-74.
36. Puzelli S, Facchini M, De Marco MA et al. Molecular surveillance of pandemic influenza A(H1N1) viruses circulating in Italy from May 2009 to February 2010: association between haemagglutinin mutations and clinical outcome. Euro Surveill 2010; 15: pii=19696.
37. Chen Z, Wang W, Zhou H et al. Generation of live attenuated novel influenza virus A/California/7/09 (H1N1) vaccines with high yield in embryonated chicken eggs. J Virol 2010; 84: 44-51.
38. Colman PM, Hoyne PA, Lawrence MC. Sequence and structure alignment of paramyxovirus hemagglutinin-neuraminidase with influenza virus neuraminidase. J Virol 1993; 67: 2972-80.
39. Vavricka CJ, Li Q, Wu Y et al. Structural and functional analysis of laninamivir and its octanoate prodrug reveals group specific mechanisms for influenza NA inhibition. PLoS Pathog 2011; 7: e1002249.
40. Lentz MR, Webster RG, Air GM. Site-directed mutation of the active site of influenza neuraminidase and implications for the catalytic mechanism. Biochemistry 1987; 26: 5351-8.
41. Abed Y, Baz M, Boivin G. A novel neuraminidase deletion mutation conferring resistance to oseltamivir in clinical influenza A/H3N2 virus. J Infect Dis 2009; 199: 180-3.
42. Nagaveni V, Prabhakar S, Vairamani M. Electrospray ionisation tandem mass spectrometric study of hydrogen-bonding interactions of some disaccharides with lysine. Rapid Commun Mass Spectrom 2001; 15: 1017-21.
43. Goto H, Kawaoka Y. A novel mechanism for the acquisition of virulence by a human influenza A virus. Proc Natl Acad Sci USA 1998; 95: 10224-8.
44. Li S, Schulman J, Itamura S et al. Glycosylation of neuraminidase determines the neurovirulence of influenza A/WSN/33 virus. J Virol 1993; 67: 6667-73.
45. Tashiro M, McKimm-Breschkin JL, Saito T et al. Surveillance for neuraminidase-inhibitor-resistant influenza viruses in Japan, 1996- 2007. Antivir Ther 2009; 14: 751-61.
46. Ison MG, Gubareva LV, Atmar RL et al. Recovery of drug-resistant influenza virus from immunocompromised patients: a case series. J Infect Dis 2006; 193: 760-4.
47. Hurt AC, Iannello P, Jachno K et al. Neuraminidase inhibitor-resistant and -sensitive influenza B viruses isolated from an untreated human patient. Antimicrob Agents Chemother 2006; 50: 1872-4.
48. Sheu TG, Deyde VM, Garten RJ et al. Detection of antiviral resistance and genetic lineage markers in influenza B virus neuraminidase using pyrosequencing. Antiviral Res 2010; 85: 354-60.
49. Hatakeyama S, Sugaya N, Ito M et al. Emergence of influenza B viruses with reduced sensitivity to neuraminidase inhibitors. JAMA 2007; 297: 1435-42.
50. Hatakeyama S, Ozawa M, Kawaoka Y. In vitro selection of influenza B viruses with reduced sensitivity to neuraminidase inhibitors. Clin Microbiol Infect 2011; 17: 1332-5.
51. Hurt AC, Holien JK, Barr IG. In vitro generation of neuraminidase inhibitor resistance in A(H5N1) influenza viruses. Antimicrob Agents Chemother 2009; 53: 4433-40.
52. Pizzorno A, Bouhy X, Abed Y et al. Generation and characterization of recombinant pandemic influenza A(H1N1) viruses resistant to neuraminidase inhibitors. J Infect Dis 2011; 203: 25-31.
53. Bloom JD, Gong LI, Baltimore D. Permissive secondary mutations enable the evolution of influenza oseltamivir resistance. Science 2010; 328: 1272-5.