I222 Neuraminidase Mutations Further Reduce Oseltamivir Susceptibility of Indonesian Clade 2.1 Highly Pathogenic Avian Influenza A(H5N1) Viruses

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  McKimm Breschkin, Jennifer L ^a   Barrett, Susan ^a   Pudjiatmoko, ^b   Azhar, Muhammad ^b   Wong, Frank Y K ^a   Selleck, Paul ^a   Mohr, Peter G ^a   McGrane, James ^c   Kim, Mia ^c,d,e,f  

^a CSIRO   (Australia)

^b INDONESIAN AGENCY FOR AGRICULTURAL RESEARCH AND DEVELOPMENT   (Indonesia)

^c FOOD AND AGRICULTURE ORGANIZATION OF THE UNITED NATIONS   (Indonesia)

^d Centre collaborateur de l'Organisation mondiale de la santé animale   (France)

^e National Veterinary Services Laboratories   (United States)

^f National Veterinary Services Laboratories ^*

Author keywords

[No Author keywords available]

Indexed keywords

OSELTAMIVIR; PERAMIVIR; VIRUS SIALIDASE; ZANAMIVIR;

ANTIVIRAL SUSCEPTIBILITY; ARTICLE; AVIAN INFLUENZA VIRUS; CAMBODIA; CLADISTICS; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG BINDING; GENE MUTATION; GENE SEQUENCE; GENETIC CORRELATION; GENETIC VARIABILITY; GEOGRAPHIC DISTRIBUTION; IC 50; INDONESIA; INFLUENZA VIRUS A H5N1; NONHUMAN; NUCLEOTIDE SEQUENCE; PANDEMIC INFLUENZA; THAILAND; VIET NAM; VIRUS ATTACHMENT; VIRUS GENE; VIRUS ISOLATION; VIRUS STRAIN;

ANTIVIRAL AGENTS; DRUG RESISTANCE, VIRAL; HUMANS; INFLUENZA A VIRUS, H5N1 SUBTYPE; MUTATION; NEURAMINIDASE; OSELTAMIVIR;

AVES; INFLUENZA A VIRUS;

EID: 84878919371     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0066105     Document Type: Article

References (57)

1. FAO (2012) FAOAIDE news-Animal Influenza Disease Emergency Situation Update 83. Available: http://www.fao.org/docrep/015/an333e/an333e00.pdf. Accessed 27 Jun 2012.
2. WHO (2013) Cumulative number of confirmed human cases for avian influenza A(H5N1) reported to WHO, 2003-2013. Available: http://www.who.int/influenza/human_animal_interface/EN_GIP_20130201CumulativeNumberH5N1cases.pdf. Accessed 11 Feb 2013.
3. von Itzstein M, Wu WY, Kok GB, Pegg MS, Dyason JC, et al. (1993) Rational design of potent sialidase-based inhibitors of influenza virus replication. Nature 363: 418-423.
4. Kim CU, Lew W, Williams MA, Liu H, Zhang L, et al. (1997) Influenza neuraminidase inhibitors possessing a novel hydrophobic interaction in the enzyme active site: design, synthesis, and structural analysis of carbocyclic sialic acid analogues with potent anti-influenza activity. J Am Chem Soc 119: 681-690.
5. Babu YS, Chand P, Bantia S, Kotian P, Dehghani A, et al. (2000) BCX-1812 (RWJ-270201): discovery of a novel, highly potent, orally active, and selective influenza neuraminidase inhibitor through structure-based drug design. J Med Chem 43: 3482-3486.
6. Varghese JN, Smith PW, Sollis SL, Blick TJ, Sahasrabudhe A, 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.
7. Meijer A, Lackenby A, Hungnes O, Lina B, van-der-Werf S, et al. (2009) Oseltamivir-resistant influenza virus A (H1N1), Europe, 2007-08 season. Emerg Infect Dis 15: 552-560.
8. Hurt AC, Ernest J, Deng YM, Iannello P, Besselaar TG, 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.
9. Dharan NJ, Gubareva LV, Meyer JJ, Okomo-Adhiambo M, McClinton RC, et al. (2009) Infections with oseltamivir-resistant influenza A(H1N1) virus in the United States. JAMA 301: 1034-1041.
10. Matsuzaki Y, Mizuta K, Aoki Y, Suto A, Abiko C, et al. (2010) A two-year survey of the oseltamivir-resistant influenza A(H1N1) virus in Yamagata, Japan and the clinical effectiveness of oseltamivir and zanamivir. Virol J 7: 53.
11. Boltz DA, Douangngeun B, Phommachanh P, Sinthasak S, Mondry R, et al. (2010) Emergence of H5N1 avian influenza viruses with reduced sensitivity to neuraminidase inhibitors and novel reassortants in Lao People's Democratic Republic. J Gen Virol 91: 949-959.
12. Hurt AC, Selleck P, Komadina N, Shaw R, Brown L, et al. (2007) Susceptibility of highly pathogenic A(H5N1) avian influenza viruses to the neuraminidase inhibitors and adamantanes. Antiviral Res 73: 228-231.
13. McKimm-Breschkin JL, Selleck PW, Usman TB, Johnson MA, (2007) Reduced sensitivity of influenza A (H5N1) to oseltamivir. Emerg Infect Dis 13: 1354-1357.
14. Naughtin M, Dyason JC, Mardy S, Sorn S, von Itzstein M, et al. (2011) Neuraminidase inhibitor sensitivity and receptor-binding specificity of Cambodian clade 1 highly pathogenic H5N1 influenza virus. Antimicrob Agents Chemother 55: 2004-2010.
15. Rameix-Welti MA, Agou F, Buchy P, Mardy S, Aubin JT, et al. (2006) Natural variation can significantly alter sensitivity to oseltamivir of Influenza A(H5N1) viruses. Antimicrob Agents Chemother 50: 3809-3815.
16. Rayner JM, Cheung CL, Smith GJD, Wang P, Tai H, et al. (2007) Naturally Occurring Antiviral Drug Resistance in Avian H5N1 Virus. Options for the Control of Influenza VI. Toronto, Ontario. 68, p48.
17. Hill AW, Guralnick RP, Wilson MJ, Habib F, Janies D, (2009) Evolution of drug resistance in multiple distinct lineages of H5N1 avian influenza. Infect Genet Evol 9: 169-178.
18. Deyde VM, Nguyen T, Bright RA, Balish A, Shu B, et al. (2009) Detection of molecular markers of antiviral resistance in influenza A (H5N1) viruses using a pyrosequencing method. Antimicrob Agents Chemother 53: 1039-1047.
19. Wetherall NT, Trivedi T, Zeller J, Hodges-Savola C, McKimm-Breschkin JL, et al. (2003) Evaluation of neuraminidase enzyme assays using different substrates to measure susceptibility of influenza virus clinical isolates to neuraminidase inhibitors: report of the Neuraminidase Inhibitor Susceptibility Network. J Clin Microbiol 41: 742-750.
20. Ilyushina NA, Seiler JP, Rehg JE, Webster RG, Govorkova EA, (2010) Effect of neuraminidase inhibitor-resistant mutations on pathogenicity of clade 2.2 A/Turkey/15/06 (H5N1) influenza virus in ferrets. PLoS Pathog 6: e1000933.
21. Collins PJ, Haire LF, Lin YP, Liu J, Russell RJ, et al. (2008) Crystal structures of oseltamivir-resistant influenza virus neuraminidase mutants. Nature 453: 1258-1261.
22. Ilyushina NA, Hay A, Yilmaz N, Boon AC, Webster RG, et al. (2008) Oseltamivir-ribavirin combination therapy for highly pathogenic H5N1 influenza virus infection in mice. Antimicrob Agents Chemother 52: 3889-3897.
23. Varghese JN, McKimm-Breschkin JL, Caldwell JB, Kortt AA, Colman PM, (1992) The structure of the complex between influenza virus neuraminidase and sialic acid, the viral receptor. Proteins 14: 327-332.
24. Varghese JN, Colman PM, (1991) Three-dimensional structure of the neuraminidase of influenza virus A/Tokyo/3/67 at 2.2 A resolution. J Mol Biol 221: 473-486.
25. Nguyen HT, Fry AM, Gubareva LV, (2012) Neuraminidase inhibitor resistance in influenza viruses and laboratory testing methods. Antivir Ther 17: 159-173.
26. McKimm-Breschkin J, Trivedi T, Hampson A, Hay A, Klimov A, et al. (2003) Neuraminidase sequence analysis and susceptibilities of influenza virus clinical isolates to zanamivir and oseltamivir. Antimicrob Agents Chemother 47: 2264-2272.
27. Monto AS, McKimm-Breschkin JL, Macken C, Hampson AW, Hay A, 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.
28. Le MT, Wertheim HF, Nguyen HD, Taylor W, Hoang PV, et al. (2008) Influenza A H5N1 clade 2.3.4 virus with a different antiviral susceptibility profile replaced clade 1 virus in humans in northern Vietnam. PLoS One 3: e3339.
29. Takano R, Kiso M, Igarashi M, Le QM, Sekijima M, et al. (2013) Molecular mechanisms underlying oseltamivir resistance mediated by an I117V substitution in the neuraminidase of subtype H5N1 avian influenza A viruses. J Infect Dis 207: 89-97.
30. Barrett S, Mohr PG, Schmidt PM, McKimm-Breschkin JL, (2011) Real time enzyme inhibition assays provide insights into differences in binding of neuraminidase inhibitors to wild type and mutant influenza viruses. PLoS One 6: e23627.
31. McKimm-Breschkin JL, Rootes C, Mohr PG, Barrett S, Streltsov VA, (2012) 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. J Antimicrob Chemother 67: 1874-1883.
32. Oakley AJ, Barrett S, Peat TS, Newman J, Streltsov VA, et al. (2010) Structural and functional basis of resistance to neuraminidase inhibitors of influenza B viruses. J Med Chem 53: 6421-6431.
33. CDC (2009) Oseltamivir-resistant 2009 pandemic influenza A (H1N1) virus infection in two summer campers receiving prophylaxis-North Carolina, 2009. MMWR Morb Mortal Wkly Rep 58: 969-972.
34. Govorkova EA, Ilyushina NA, Marathe BM, McClaren JL, Webster RG, (2010) Competitive fitness of oseltamivir-sensitive and-resistant highly pathogenic H5N1 influenza viruses in a ferret model. J Virol 84: 8042-8050.
35. Hurt AC, Holien JK, Barr IG, (2009) In vitro generation of neuraminidase inhibitor resistance in A(H5N1) influenza viruses. Antimicrob Agents Chemother 53: 4433-4440.
36. Nguyen HT, Fry AM, Loveless PA, Klimov AI, Gubareva LV, (2010) Recovery of a multidrug-resistant 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 51: 983-984.
37. Pizzorno A, Bouhy X, Abed Y, Boivin G, (2011) Generation and Characterization of Recombinant Pandemic Influenza A(H1N1) Viruses Resistant to Neuraminidase Inhibitors. J Infect Dis 203: 25-31.
38. van der Vries E, Stelma FF, Boucher CA, (2010) Emergence of a multidrug-resistant pandemic influenza A (H1N1) virus. N Engl J Med 363: 1381-1382.
39. Wibawa H, Henning J, Wong F, Selleck P, Junaidi A, et al. (2011) A molecular and antigenic survey of H5N1 highly pathogenic avian influenza virus isolates from smallholder duck farms in Central Java, Indonesia during 2007-2008. Virol J 8: 425.
40. Eshaghi A, Patel SN, Sarabia A, Higgins RR, Savchenko A, et al. (2011) Multidrug-resistant pandemic (H1N1) 2009 infection in immunocompetent child. Emerg Infect Dis 17: 1472-1474.
41. Baz M, Abed Y, McDonald J, Boivin G, (2006) Characterization of multidrug-resistant influenza A/H3N2 viruses shed during 1 year by an immunocompromised child. Clin Infect Dis 43: 1555-1561.
42. Hatakeyama S, Ozawa M, Kawaoka Y, (2011) In vitro selection of influenza B viruses with reduced sensitivity to neuraminidase inhibitors. Clin Microbiol Infect 17: 1332-1335.
43. Hatakeyama S, Sugaya N, Ito M, Yamazaki M, Ichikawa M, et al. (2007) Emergence of influenza B viruses with reduced sensitivity to neuraminidase inhibitors. JAMA 297: 1435-1442.
44. Sleeman K, Sheu TG, Moore Z, Kilpatrick S, Garg S, et al. (2011) Influenza B viruses with mutation in the neuraminidase active site, north Carolina, USA, 2010-11. Emerg Infect Dis 17: 2043-2046.
45. Smith BJ, McKimm-Breshkin JL, McDonald M, Fernley RT, Varghese JN, et al. (2002) Structural studies of the resistance of influenza virus neuramindase to inhibitors. J Med Chem 45: 2207-2212.
46. Govorkova EA, Ilyushina NA, McClaren JL, Naipospos TS, Douangngeun B, et al. (2009) Susceptibility of highly pathogenic H5N1 influenza viruses to the neuraminidase inhibitor oseltamivir differs in vitro and in a mouse model. Antimicrob Agents Chemother 53: 3088-3096.
47. Takano R, Kiso M, Igarashi M, Le QM, Sekijima M, et al. (2012) Molecular Mechanisms Underlying Oseltamivir Resistance Mediated by an I117V Substitution in the Neuraminidase of Subtype H5N1 Avian Influenza A Viruses. J Infect Dis.
48. Hurt AC, Leang SK, Speers DJ, Barr IG, Maurer-Stroh S, (2012) Mutations I117V and I117M and oseltamivir sensitivity of pandemic (H1N1) 2009 viruses. Emerg Infect Dis 18: 109-112.
49. Landon MR, Amaro RE, Baron R, Ngan CH, Ozonoff D, et al. (2008) Novel druggable hot spots in avian influenza neuraminidase H5N1 revealed by computational solvent mapping of a reduced and representative receptor ensemble. Chem Biol Drug Des 71: 106-116.
50. Oo C, Barrett J, Hill G, Mann J, Dorr A, et al. (2001) Pharmacokinetics and dosage recommendations for an oseltamivir oral suspension for the treatment of influenza in children [erratum appears in Paediatric Drugs 2001;3(4):246]. Paediatr Drugs 3: 229-236.
51. Morrison D, Roy S, Rayner C, Amer A, Howard D, et al. (2007) A randomized, crossover study to evaluate the pharmacokinetics of amantadine and oseltamivir administered alone and in combination. PLoS ONE 2: e1305.
52. Wattanagoon Y, Stepniewska K, Lindegardh N, Pukrittayakamee S, Silachamroon U, et al. (2009) Pharmacokinetics of high-dose oseltamivir in healthy volunteers. Antimicrob Agents Chemother 53: 945-952.
53. Burmeister WP, Ruigrok RW, Cusack S, (1992) The 2.2 A resolution crystal structure of influenza B neuraminidase and its complex with sialic acid. EMBO J 11: 49-56.
54. Abed Y, Pizzorno A, Bouhy X, Boivin G, (2011) Role of Permissive Neuraminidase Mutations in Influenza A/Brisbane/59/2007-like (H1N1) Viruses. PLoS Pathog 7: e1002431.
55. Bloom JD, Gong LI, Baltimore D, (2010) Permissive secondary mutations enable the evolution of influenza oseltamivir resistance. Science 328: 1272-1275.
56. Potier M, Mameli L, Belisle M, Dallaire L, Melancon SB, (1979) Fluorometric assay of neuraminidase with a sodium (4-methylumbelliferyl- alpha-D-N-acetylneuraminate) substrate. Anal Biochem 94: 287-296.
57. Hall TA, (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic acids symposium series 41: 95-98.