Screening for neuraminidase inhibitor resistance markers among avian influenza viruses of the N4, N5, N6, and N8 neuraminidase subtypes

Journal of Virology

Volumn 92, Issue 1, 2018, Pages

  Choi, Won Suk ^a   Jeong, Ju Hwan ^a   Kwon, Jin Jung ^a   Ahn, Su Jeong ^a   Lloren, Khristine Kaith S ^a   Kwon, Hyeok Il ^a   Chae, Hee Bok ^a,b   Hwang, Jungwon ^c   Kim, Myung Hee ^c   Kim, Chul Joong ^d   Webby, Richard J ^e   Govorkova, Elena A ^e   Choi, Young Ki ^a   Baek, Yun Hee ^a   Song, Min Suk ^a  

^a Chungbuk National University College of Medicine   (South Korea)

^b Chungbuk National University Hospital   (South Korea)

^c Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

^d Chungnam National University   (South Korea)

^e ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

Avian influenza virus; N4; N5; N6; N8; Neuraminidase inhibitor; Random mutagenesis; Resistance

Indexed keywords

4 ACETAMIDO 5 AMINO 3 (1 ETHYLPROPOXY) 1 CYCLOHEXENE 1 CARBOXYLIC ACID; PERAMIVIR; UNCLASSIFIED DRUG; VIRUS SIALIDASE; VIRUS SIALIDASE 4; VIRUS SIALIDASE 5; VIRUS SIALIDASE 6; VIRUS SIALIDASE 8; ZANAMIVIR; ANTIVIRUS AGENT; CYCLOPENTANE DERIVATIVE; ENZYME INHIBITOR; GUANIDINE DERIVATIVE; OSELTAMIVIR; SIALIDASE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMAL CELL; ANTIVIRAL RESISTANCE; ANTIVIRAL SUSCEPTIBILITY; ARTICLE; AVIAN INFLUENZA VIRUS; CONTROLLED STUDY; DNA SEQUENCE; ENZYME ACTIVITY; ENZYME ANALYSIS; GENETIC STABILITY; HUMAN; HUMAN CELL; MDCK CELL LINE; MOLONEY MURINE LEUKEMIA VIRUS; NA GENE; NONHUMAN; PRIORITY JOURNAL; REVERSE GENETICS; SEQUENCE ANALYSIS; VIRUS INFECTIVITY; VIRUS REPLICATION; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; AVIAN INFLUENZA; BIRD; CHEMISTRY; CLASSIFICATION; DOG; DRUG EFFECTS; ENZYMOLOGY; GENETICS; INFLUENZA; MUTAGENESIS; ORTHOMYXOVIRIDAE; VIROLOGY;

AMINO ACID SUBSTITUTION; ANIMALS; ANTIVIRAL AGENTS; BIRDS; CYCLOPENTANES; DOGS; DRUG RESISTANCE, VIRAL; ENZYME INHIBITORS; GUANIDINES; HUMANS; INFLUENZA IN BIRDS; INFLUENZA, HUMAN; MADIN DARBY CANINE KIDNEY CELLS; MUTAGENESIS; NEURAMINIDASE; ORTHOMYXOVIRIDAE; OSELTAMIVIR; REVERSE GENETICS; ZANAMIVIR;

EID: 85038032957     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01580-17     Document Type: Article

References (54)

1. Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y. 1992. Evolution and ecology of influenza A viruses. Microbiol Rev 56:152-179
2. Webster RG, Govorkova EA. 2014. Continuing challenges in influenza. Ann N Y Acad Sci 1323:115-139. https://doi.org/10.1111/nyas.12462
3. Reperant LA, Kuiken T, Osterhaus AD. 2012. Influenza viruses: from birds to humans. Hum Vaccin Immunother 8:7-16. https://doi.org/10.4161/hv .8.1.18672
4. Kim CU, Lew W, Williams MA, Wu H, Zhang L, Chen X, Escarpe PA, Mendel DB, Laver WG, Stevens RC. 1998. Structure-activity relationship studies of novel carbocyclic influenza neuraminidase inhibitors. J Med Chem 41:2451-2460. https://doi.org/10.1021/jm980162u
5. Colman PM. 1994. Influenza virus neuraminidase: structure, antibodies, and inhibitors. Protein Sci 3:1687-1696. https://doi.org/10.1002/ pro.5560031007
6. Wolfe C, Greenwald I, Chen L. 2010. Pandemic (H1N1) 2009 and oseltamivir resistance in hematology/oncology patients. Emerg Infect Dis 16:1809. https://doi.org/10.3201/eid1611.101053
7. Moore C, Galiano M, Lackenby A, Abdelrahman T, Barnes R, Evans MR, Fegan C, Froude S, Hastings M, Knapper S. 2011. Evidence of person-toperson transmission of oseltamivir-resistant pandemic influenza A (H1N1) 2009 virus in a hematology unit. J Infect Dis 203:18-24. https:// doi.org/10.1093/infdis/jiq007
8. Hurt AC, Holien JK, Parker M, Kelso A, Barr IG. 2009. Zanamivir-resistant influenza viruses with a novel neuraminidase mutation. J Virol 83: 10366-10373. https://doi.org/10.1128/JVI.01200-09
9. Le QM, Kiso M, Someya K, Sakai YT, Nguyen TH, Nguyen KH, Pham ND, Nguyen HH, Yamada S, Muramoto Y. 2005. Avian flu: isolation of drug-resistant H5N1 virus. Nature 437:1108. https://doi.org/10.1038/ 4371108a
10. 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. https://doi .org/10.1086/508777
11. Mishin VP, Hayden FG, Gubareva LV. 2005. Susceptibilities of antiviralresistant influenza viruses to novel neuraminidase inhibitors. Antimicrob Agents Chemother 49:4515-4520. https://doi.org/10.1128/AAC.49.11 .4515-4520.2005
12. Hu Y, Lu S, Song Z, Wang W, Hao P, Li J, Zhang X, Yen HL, Shi B, Li T, Guan W, Xu L, Liu Y, Wang S, Tian D, Zhu Z, He J, Huang K, Chen H, Zheng L, Li X, Ping J, Kang B, Xi X, Zha L, Li Y, Zhang Z, Peiris M, Yuan Z. 2013. Association between adverse clinical outcome in human disease caused by novel influenza A H7N9 virus and sustained viral shedding and emergence of antiviral resistance. Lancet 381:2273-2279. https://doi .org/10.1016/S0140-6736(13)61125-3
13. Dapat C, Suzuki Y, Saito R, Kyaw Y, Myint YY, Lin N, Oo HN, Oo KY, Win N, Naito M. 2010. Rare influenza A (H3N2) variants with reduced sensitivity to antiviral drugs. Emerg Infect Dis 16:493. https://doi.org/10.3201/ eid1603.091321
14. Sheu TG, Deyde VM, Okomo-Adhiambo M, Garten RJ, Xu X, Bright RA, Butler EN, Wallis TR, Klimov AI, Gubareva LV. 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. https://doi.org/10.1128/AAC.00555-08
15. Song M-S, Marathe BM, Kumar G, Wong S-S, Rubrum A, Zanin M, Choi Y-K, Webster RG, Govorkova EA, Webby RJ. 2015. Unique determinants of neuraminidase inhibitor resistance among N3, N7, and N9 avian influenza viruses. J Virol 89:10891-10900. https://doi.org/10.1128/JVI .01514-15
16. Zhang Y, Chen M, Huang Y, Zhu W, Yang L, Gao L, Li X, Bi F, Huang C, Kang N. 2017. Human infections with novel reassortant H5N6 avian influenza viruses in China. Emerg Microbes Infect 6:e50. https://doi.org/ 10.1038/emi.2017.38
17. Jiang H, Wu P, Uyeki TM, He J, Deng Z, Xu W, Lv Q, Zhang J, Wu Y, Tsang TK. 2017. Preliminary epidemiologic assessment of human infections with highly pathogenic avian influenza A (H5N6) virus, China. Clin Infect Dis 65:383-388. https://doi.org/10.1093/cid/cix334
18. El-Shesheny R, Barman S, Feeroz M, Hasan M, Jones-Engel L, Franks J, Turner J, Seiler P, Walker D, Friedman K. 2017. Genesis of influenza A (H5N8) viruses. Emerg Infect Dis 23:1368-1371. https://doi.org/10.3201/ eid2308.170143
19. Kim Y-I, Pascua PNQ, Kwon H-I, Lim G-J, Kim E-H, Yoon S-W, Park S-J, Kim SM, Choi E-J, Si Y-J, Lee O-J, Shim W-S, Kim S-W, Mo I-P, Bae Y, Lim YT, Sung MH, Kim C-J, Webby RJ, Webster RG, Choi YK. 2014. Pathobiological features of a novel, highly pathogenic avian influenza A(H5N8) virus. Emerg Microbes Infect 3:e75. https://doi.org/10.1038/emi.2014.75
20. WHO. 2012. Meetings of the WHO working group on surveillance of influenza antiviral susceptibility-Geneva, November 2011 and June2012. Wkly Epidemiol Rec 87:369-374
21. van der Vries E, Jonges M, Herfst S, Maaskant J, Van der Linden A, Guldemeester J, Aron G, Bestebroer T, Koopmans M, Meijer A. 2010. Evaluation of a rapid molecular algorithm for detection of pandemic influenza A (H1N1) 2009 virus and screening for a key oseltamivir resistance (H275Y) substitution in neuraminidase. J Clin Virol 47:34-37. https://doi.org/10.1016/j.jcv.2009.09.030
22. Ives J, Carr J, Roberts N, Tai C, Mendel D, Kelly L, Lambkin R, Oxford J. 2000. An oseltamivir treatment-selected influenza A: N2 virus with a R292K mutation in the neuraminidase gene has reduced infectivity in vivo. J Clin Virol 18:251-269. https://doi.org/10.1016/S1386-6532(00)00111-6
23. Bi Y, Mei K, Shi W, Liu D, Yu X, Gao Z, Zhao L, Gao GF, Chen J, Chen Q.2015. Two novel reassortants of avian influenza A (H5N6) virus in China. J Gen Virol 96:975-981. https://doi.org/10.1099/vir.0.000056
24. Du Y, Chen M, Yang J, Jia Y, Han S, Holmes EC, Cui J. 2017. Molecular evolution and emergence of H5N6 avian influenza virus in central China. J Virol 91:e00143-17. https://doi.org/10.1128/JVI.00143-17
25. Liu M, Li X, Yuan H, Zhou J, Wu J, Bo H, Xia W, Xiong Y, Yang L, Gao R.2015. Genetic diversity of avian influenza A (H10N8) virus in live poultry markets and its association with human infections in China. Sci Rep 5:7632. https://doi.org/10.1038/srep07632
26. Wang M, Qi J, Liu Y, Vavricka CJ, Wu Y, Li Q, Gao GF. 2011. Influenza A virus N5 neuraminidase has an extended 150-cavity. J Virol 85: 8431-8435. https://doi.org/10.1128/JVI.00638-11
27. Wu Y, Qin G, Gao F, Liu Y, Vavricka CJ, Qi J, Jiang H, Yu K, Gao GF. 2013. Induced opening of influenza virus neuraminidase N2 150-loop suggests an important role in inhibitor binding. Sci Rep 3:1551. https://doi.org/ 10.1038/srep01551
28. Samson M, Pizzorno A, Abed Y, Boivin G. 2013. Influenza virus resistance to neuraminidase inhibitors. Antiviral Res 98:174-185. https://doi.org/ 10.1016/j.antiviral.2013.03.014
29. Orozovic G, Orozovic K, Lennerstrand J, Olsen B. 2011. Detection of resistance mutations to antivirals oseltamivir and zanamivir in avian influenza A viruses isolated from wild birds. PLoS One 6:e16028. https:// doi.org/10.1371/journal.pone.0016028
30. Stoll V, Stewart KD, Maring CJ, Muchmore S, Giranda V, Gu Y-Y, Wang G, Chen Y, Sun M, Zhao C. 2003. Influenza neuraminidase inhibitors: structure-based design of a novel inhibitor series. Biochemistry 42: 718-727. https://doi.org/10.1021/bi0205449
31. Eshaghi A, Shalhoub S, Rosenfeld P, Li A, Higgins RR, Stogios PJ, Savchenko A, Bastien N, Li Y, Rotstein C. 2014. Multiple influenza A (H3N2) mutations conferring resistance to neuraminidase inhibitors in a bone marrow transplant recipient. Antimicrob Agents Chemother 58: 7188-7197. https://doi.org/10.1128/AAC.03667-14
32. Hurt A, Lee R, Leang S, Cui L, Deng Y, Phuah S, Caldwell N, Freeman K, Komadina N, Smith D. 2011. Increased detection in Australia and Singapore of a novel influenza A (H1N1) 2009 variant with reduced oseltamivir and zanamivir sensitivity due to a S247N neuraminidase mutation. Euro Surveill 16:19884
33. Boltz DA, Douangngeun B, Phommachanh P, Sinthasak S, Mondry R, Obert C, Seiler P, Keating R, Suzuki Y, Hiramatsu H. 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. https://doi.org/10.1099/vir.0.017459-0
34. Abed Y, Baz M, Boivin G. 2009. A novel neuraminidase deletion mutation conferring resistance to oseltamivir in clinical influenza A/H3N2 virus. J Infect Dis 199:180-183. https://doi.org/10.1086/595736
35. Prachanronarong KL, Ozen A, Thayer KM, Yilmaz LS, Zeldovich KB, Bolon DN, Kowalik TF, Jensen JD, Finberg RW, Wang JP. 2016. Molecular basis for differential patterns of drug resistance in influenza N1 and N2 neuraminidase. J Chem Theory Comput 12:6098-6108. https://doi.org/ 10.1021/acs.jctc.6b00703
36. Hoffmann A, Schade D, Kirchmair J, Clement B, Sauerbrei A, Schmidtke M. 2016. Platform for determining the inhibition profile of neuraminidase inhibitors in an influenza virus N1 background. J Virol Methods 237:192-199. https://doi.org/10.1016/j.jviromet.2016.09.014
37. Hurt AC, Chotpitayasunondh T, Cox NJ, Daniels R, Fry AM, Gubareva LV, Hayden FG, Hui DS, Hungnes O, Lackenby A. 2012. Antiviral resistance during the 2009 influenza A H1N1 pandemic: public health, laboratory, and clinical perspectives. Lancet Infect Dis 12:240-248. https://doi.org/ 10.1016/S1473-3099(11)70318-8
38. Abed Y, Baz M, Boivin G. 2006. Impact of neuraminidase mutations conferring influenza resistance to neuraminidase inhibitors in the N1 and N2 genetic backgrounds. Antivir Ther 11:971
39. Zürcher T, Yates PJ, Daly J, Sahasrabudhe A, Walters M, Dash L, Tisdale M, McKimm-Breschkin JL. 2006. Mutations conferring zanamivir resistance in human influenza virus N2 neuraminidases compromise virus fitness and are not stably maintained in vitro. J Antimicrob Chemother 58:723-732. https://doi.org/10.1093/jac/dkl321
40. Abed Y, Goyette N, Boivin G. 2005. Generation and characterization of recombinant influenza A (H1N1) viruses harboring amantadine resistance mutations. Antimicrob Agents Chemother 49:556-559. https://doi .org/10.1128/AAC.49.2.556-559.2005
41. Neuraminidase Inhibitor Flu Treatment Investigator Group, Little K, Leang S-K, Butler J, Baas C, Harrower B, Mosse J, Barr IG, Hurt AC. 2015. Zanamivir-resistant influenza viruses with Q136K or Q136R neuraminidase residue mutations can arise during MDCK cell culture creating challenges for antiviral susceptibility monitoring. Euro Surveill 20. https://doi.org/10.2807/1560-7917.ES.2015.20.45.30060
42. Yen H-L, Hoffmann E, Taylor G, Scholtissek C, Monto AS, Webster RG, Govorkova EA. 2006. Importance of neuraminidase active-site residues to the neuraminidase inhibitor resistance of influenza viruses. J Virol 80:8787-8795. https://doi.org/10.1128/JVI.00477-06
43. Ho H-T, Hurt AC, Mosse J, Barr I. 2007. Neuraminidase inhibitor drug susceptibility differs between influenza N1 and N2 neuraminidase following mutagenesis of two conserved residues. Antivir Res 76:263-266. https://doi.org/10.1016/j.antiviral.2007.08.002
44. Burnham AJ, Baranovich T, Marathe BM, Armstrong J, Webster RG, Govorkova EA. 2014. Fitness costs for Influenza B viruses carrying neuraminidase inhibitor-resistant substitutions: underscoring the importance of E119A and H274Y. Antimicrob Agents Chemother 58:2718-2730. https://doi.org/10.1128/AAC.02628-13
45. Gaymard A, Charles-Dufant A, Sabatier M, Cortay J-C, Frobert E, Picard C, Casalegno J-S, Rosa-Calatrava M, Ferraris O, Valette M, Ottmann M, Lina B, Escuret V. 2016. Impact on antiviral resistance of E119V, I222L and R292K substitutions in influenza A viruses bearing a group 2 neuraminidase (N2, N3, N6, N7 and N9). J Antimicrob Chemother 71:3036-3045. https://doi.org/10.1093/jac/dkw275
46. Russell RJ, Haire LF, Stevens DJ, Collins PJ, Lin YP, Blackburn GM, Hay AJ, Gamblin SJ, Skehel JJ. 2006. The structure of H5N1 avian influenza neuraminidase suggests new opportunities for drug design. Nature 443:45-49. https://doi.org/10.1038/nature05114
47. Varghese JN, Smith PW, Sollis SL, Blick TJ, Sahasrabudhe A, McKimm-Breschkin JL, Colman PM. 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. https://doi.org/10.1016/ S0969-2126(98)00075-6
48. Ives JAL, Carr JA, Mendel DB, Tai CY, Lambkin R, Kelly L, Oxford JS, Hayden FG, Roberts NA. 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. Antivir Res 55:307-317. https://doi.org/10.1016/S0166-3542(02)00053-0
49. Hurt AC, Holien JK, Parker MW, Barr IG. 2009. Oseltamivir resistance and the H274Y neuraminidase mutation in seasonal, pandemic and highly pathogenic influenza viruses. Drugs 69:2523-2531. https://doi.org/10 .2165/11531450-000000000-00000
50. Wagner R, Matrosovich M, Klenk HD. 2002. Functional balance between haemagglutinin and neuraminidase in influenza virus infections. Rev Med Virol 12:159-166. https://doi.org/10.1002/rmv.352
51. Mitnaul LJ, Matrosovich MN, Castrucci MR, Tuzikov AB, Bovin NV, Kobasa D, Kawaoka Y. 2000. Balanced hemagglutinin and neuraminidase activities are critical for efficient replication of influenza A virus. J Virol 74:6015-6020. https://doi.org/10.1128/JVI.74.13.6015-6020.2000
52. 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 U S A 97:6108-6113. https://doi.org/10 .1073/pnas.100133697
53. Potier M, Mameli L, Belisle M, Dallaire L, Melancon S. 1979. Fluorometric assay of neuraminidase with a sodium (4-methylumbelliferyl-α-DNacetylneuraminate) substrate. Anal Biochem 94:287-296. https://doi.org/ 10.1016/0003-2697(79)90362-2
54. Okomo-Adhiambo M, Nguyen HT, Abd Elal A, Sleeman K, Fry AM, Gubareva LV. 2014. Drug susceptibility surveillance of influenza viruses circulating in the United States in 2011-2012: application of the WHO Antiviral Working Group criteria. Influenza Other Respir Viruses 8:258-265. https://doi.org/10.1111/irv.12215