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Characterization of two distinct neuraminidases from avian-origin human-infecting H7N9 influenza viruses.

OpenAccess logo Cell Res 23 1347-55 (2013)
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Cited: 66 times
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Abstract

An epidemic of an avian-origin H7N9 influenza virus has recently emerged in China, infecting 134 patients of which 45 have died. This is the first time that an influenza virus harboring an N9 serotype neuraminidase (NA) has been known to infect humans. H7N9 viruses are divergent and at least two distinct NAs and hemagglutinins (HAs) have been found, respectively, from clinical isolates. The prototypes of these viruses are A/Anhui/1/2013 and A/Shanghai/1/2013. NAs from these two viruses are distinct as the A/Shanghai/1/2013 NA has an R294K substitution that can confer NA inhibitor oseltamivir resistance. Oseltamivir is by far the most commonly used anti-influenza drug due to its potency and high bioavailability. In this study, we show that an R294K substitution results in multidrug resistance with extreme oseltamivir resistance (over 100 000-fold) using protein- and virus-based assays. To determine the molecular basis for the inhibitor resistance, we solved high-resolution crystal structures of NAs from A/Anhui/1/2013 N9 (R294-containing) and A/Shanghai/1/2013 N9 (K294-containing). R294K substitution results in an unfavorable E276 conformation for oseltamivir binding, and consequently loss of inhibitor carboxylate interactions, which compromises the binding of all classical NA ligands/inhibitors. Moreover, we found that R294K substitution results in reduced NA catalytic efficiency along with lower viral fitness. This helps to explain why K294 has predominantly been found in clinical cases of H7N9 infection under the selective pressure of oseltamivir treatment and not in the dominant human-infecting viruses. This implies that oseltamivir can still be efficiently used in the treatment of H7N9 infections.

Reviews - 4mwr mentioned but not cited (1)

  1. The current state of research on influenza antiviral drug development: drugs in clinical trial and licensed drugs. Li Y, Huo S, Yin Z, Tian Z, Huang F, Liu P, Liu Y, Yu F. mBio 14 e0127323 (2023)

Articles - 4mwr mentioned but not cited (3)

  1. Characterization of two distinct neuraminidases from avian-origin human-infecting H7N9 influenza viruses. Wu Y, Bi Y, Vavricka CJ, Sun X, Zhang Y, Gao F, Zhao M, Xiao H, Qin C, He J, Liu W, Yan J, Qi J, Gao GF. Cell Res. 23 1347-1355 (2013)
  2. Unique Determinants of Neuraminidase Inhibitor Resistance among N3, N7, and N9 Avian Influenza Viruses. Song MS, Marathe BM, Kumar G, Wong SS, Rubrum A, Zanin M, Choi YK, Webster RG, Govorkova EA, Webby RJ. J. Virol. 89 10891-10900 (2015)
  3. Virtual screening approach to identifying influenza virus neuraminidase inhibitors using molecular docking combined with machine-learning-based scoring function. Zhang L, Ai HX, Li SM, Qi MY, Zhao J, Zhao Q, Liu HS. Oncotarget 8 83142-83154 (2017)


Reviews citing this publication (11)

  1. Pandemic potential of avian influenza A (H7N9) viruses. Watanabe T, Watanabe S, Maher EA, Neumann G, Kawaoka Y. Trends Microbiol. 22 623-631 (2014)
  2. Epidemiology, Evolution, and Pathogenesis of H7N9 Influenza Viruses in Five Epidemic Waves since 2013 in China. Su S, Gu M, Liu D, Cui J, Gao GF, Zhou J, Liu X. Trends Microbiol. 25 713-728 (2017)
  3. H7N9: a low pathogenic avian influenza A virus infecting humans. Liu J, Xiao H, Wu Y, Liu D, Qi X, Shi Y, Gao GF. Curr Opin Virol 5 91-97 (2014)
  4. Avian influenza A (H7N9) virus infection in humans: epidemiology, evolution, and pathogenesis. Husain M. Infect. Genet. Evol. 28 304-312 (2014)
  5. Viral lung infections: epidemiology, virology, clinical features, and management of avian influenza A(H7N9). To KK, Chan JF, Yuen KY. Curr Opin Pulm Med 20 225-232 (2014)
  6. Adaptation of influenza viruses to human airway receptors. Thompson AJ, Paulson JC. J Biol Chem 296 100017 (2021)
  7. Pains and Gains from China's Experiences with Emerging Epidemics: From SARS to H7N9. Wei P, Cai Z, Hua J, Yu W, Chen J, Kang K, Qiu C, Ye L, Hu J, Ji K. Biomed Res Int 2016 5717108 (2016)
  8. A Review of Clinical Influenza A and B Infections With Reduced Susceptibility to Both Oseltamivir and Zanamivir. Abed Y, Boivin G. Open Forum Infect Dis 4 ofx105 (2017)
  9. H7N9: A killer in the making or a false alarm? Nailwal H, Kamra K, Lal SK. Can. J. Microbiol. 60 425-429 (2014)
  10. Considerations for the rapid deployment of vaccines against H7N9 influenza. Chua BY, Brown LE, Jackson DC. Expert Rev Vaccines 13 1327-1337 (2014)
  11. A systemic review on medicinal plants and their bioactive constituents against avian influenza and further confirmation through in-silico analysis. Dutta AK, Gazi MS, Uddin SJ. Heliyon 9 e14386 (2023)

Articles citing this publication (51)

  1. Genesis, Evolution and Prevalence of H5N6 Avian Influenza Viruses in China. Bi Y, Chen Q, Wang Q, Chen J, Jin T, Wong G, Quan C, Liu J, Wu J, Yin R, Zhao L, Li M, Ding Z, Zou R, Xu W, Li H, Wang H, Tian K, Fu G, Huang Y, Shestopalov A, Li S, Xu B, Yu H, Luo T, Lu L, Xu X, Luo Y, Liu Y, Shi W, Liu D, Gao GF. Cell Host Microbe 20 810-821 (2016)
  2. Letter Human infections with recently-emerging highly pathogenic H7N9 avian influenza virus in China. Zhang F, Bi Y, Wang J, Wong G, Shi W, Hu F, Yang Y, Yang L, Deng X, Jiang S, He X, Liu Y, Yin C, Zhong N, Gao GF. J. Infect. 75 71-75 (2017)
  3. Characterization of drug-resistant influenza A(H7N9) variants isolated from an oseltamivir-treated patient in Taiwan. Marjuki H, Mishin VP, Chesnokov AP, Jones J, De La Cruz JA, Sleeman K, Tamura D, Nguyen HT, Wu HS, Chang FY, Liu MT, Fry AM, Cox NJ, Villanueva JM, Davis CT, Gubareva LV. J. Infect. Dis. 211 249-257 (2015)
  4. Assessment of the internal genes of influenza A (H7N9) virus contributing to high pathogenicity in mice. Bi Y, Xie Q, Zhang S, Li Y, Xiao H, Jin T, Zheng W, Li J, Jia X, Sun L, Liu J, Qin C, Gao GF, Liu W. J. Virol. 89 2-13 (2015)
  5. Letter Phylogenetics of varied subtypes of avian influenza viruses in China: potential threat to humans. Shi W, Li W, Li X, Haywood J, Ma J, Gao GF, Liu D. Protein Cell 5 253-257 (2014)
  6. Emergence of H7N9 Influenza A Virus Resistant to Neuraminidase Inhibitors in Nonhuman Primates. Itoh Y, Shichinohe S, Nakayama M, Igarashi M, Ishii A, Ishigaki H, Ishida H, Kitagawa N, Sasamura T, Shiohara M, Doi M, Tsuchiya H, Nakamura S, Okamatsu M, Sakoda Y, Kida H, Ogasawara K. Antimicrob. Agents Chemother. 59 4962-4973 (2015)
  7. An influenza A virus (H7N9) anti-neuraminidase monoclonal antibody with prophylactic and therapeutic activity in vivo. Wilson JR, Guo Z, Reber A, Kamal RP, Music N, Gansebom S, Bai Y, Levine M, Carney P, Tzeng WP, Stevens J, York IA. Antiviral Res. 135 48-55 (2016)
  8. Changes in the Length of the Neuraminidase Stalk Region Impact H7N9 Virulence in Mice. Bi Y, Xiao H, Chen Q, Wu Y, Fu L, Quan C, Wong G, Liu J, Haywood J, Liu Y, Zhou B, Yan J, Liu W, Gao GF. J. Virol. 90 2142-2149 (2016)
  9. Emergence and Adaptation of a Novel Highly Pathogenic H7N9 Influenza Virus in Birds and Humans from a 2013 Human-Infecting Low-Pathogenic Ancestor. Qi W, Jia W, Liu D, Li J, Bi Y, Xie S, Li B, Hu T, Du Y, Xing L, Zhang J, Zhang F, Wei X, Eden JS, Li H, Tian H, Li W, Su G, Lao G, Xu C, Xu B, Liu W, Zhang G, Ren T, Holmes EC, Cui J, Shi W, Gao GF, Liao M. J. Virol. 92 (2018)
  10. Editorial Seeing is believing: anti-PD-1/PD-L1 monoclonal antibodies in action for checkpoint blockade tumor immunotherapy. Tan S, Zhang CW, Gao GF. Signal Transduct Target Ther 1 16029 (2016)
  11. New Threats from H7N9 Influenza Virus: Spread and Evolution of High- and Low-Pathogenicity Variants with High Genomic Diversity in Wave Five. Quan C, Shi W, Yang Y, Yang Y, Liu X, Xu W, Li H, Li J, Wang Q, Tong Z, Wong G, Zhang C, Ma S, Ma Z, Fu G, Zhang Z, Huang Y, Song H, Yang L, Liu WJ, Liu Y, Liu W, Gao GF, Bi Y. J. Virol. 92 (2018)
  12. An overview of the characteristics of the novel avian influenza A H7N9 virus in humans. Tan KX, Jacob SA, Chan KG, Lee LH. Front Microbiol 6 140 (2015)
  13. Structure of influenza virus N7: the last piece of the neuraminidase "jigsaw" puzzle. Sun X, Li Q, Wu Y, Wang M, Liu Y, Qi J, Vavricka CJ, Gao GF. J. Virol. 88 9197-9207 (2014)
  14. Letter Continuous reassortments with local chicken H9N2 virus underlie the human-infecting influenza A (H7N9) virus in the new influenza season, Guangdong, China. Qi W, Shi W, Li W, Huang L, Li H, Wu Y, Yan J, Jiao P, Zhu B, Ma J, Gao GF, Liao M, Liu D. Protein Cell 5 878-882 (2014)
  15. Discovery of potential drugs for human-infecting H7N9 virus containing R294K mutation. He JY, Li C, Wu G. Drug Des Devel Ther 8 2377-2390 (2014)
  16. Identification of novel compounds against an R294K substitution of influenza A (H7N9) virus using ensemble based drug virtual screening. Tran N, Van T, Nguyen H, Le L. Int J Med Sci 12 163-176 (2015)
  17. Role of R292K mutation in influenza H7N9 neuraminidase toward oseltamivir susceptibility: MD and MM/PB(GB)SA study. Phanich J, Rungrotmongkol T, Kungwan N, Hannongbua S. J. Comput. Aided Mol. Des. 30 917-926 (2016)
  18. Viral genome and antiviral drug sensitivity analysis of two patients from a family cluster caused by the influenza A(H7N9) virus in Zhejiang, China, 2013. Gao HN, Yao HP, Liang WF, Wu XX, Wu HB, Wu NP, Yang SG, Zhang Q, Su KK, Guo J, Zheng SF, Zhu YX, Chen HL, Yuen KY, Li LJ. Int. J. Infect. Dis. 29 254-258 (2014)
  19. Drug Susceptibility Evaluation of an Influenza A(H7N9) Virus by Analyzing Recombinant Neuraminidase Proteins. Gubareva LV, Sleeman K, Guo Z, Yang H, Hodges E, Davis CT, Baranovich T, Stevens J. J. Infect. Dis. 216 S566-S574 (2017)
  20. 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). Gaymard A, Charles-Dufant A, Sabatier M, Cortay JC, Frobert E, Picard C, Casalegno JS, Rosa-Calatrava M, Ferraris O, Valette M, Ottmann M, Lina B, Escuret V. J. Antimicrob. Chemother. 71 3036-3045 (2016)
  21. Molecular docking of potential inhibitors for influenza H7N9. Liu Z, Zhao J, Li W, Wang X, Xu J, Xie J, Tao K, Shen L, Zhang R. Comput Math Methods Med 2015 480764 (2015)
  22. Resistance to Mutant Group 2 Influenza Virus Neuraminidases of an Oseltamivir-Zanamivir Hybrid Inhibitor. Wu Y, Gao F, Qi J, Bi Y, Fu L, Mohan S, Chen Y, Li X, Pinto BM, Vavricka CJ, Tien P, Gao GF. J. Virol. 90 10693-10700 (2016)
  23. News CASCIRE surveillance network and work on avian influenza viruses. Bi Y, Shi W, Chen J, Chen Q, Ma Z, Wong G, Tian W, Yin R, Fu G, Yang Y, Liu WJ, Quan C, Wang Q, He S, Li X, Xia Q, Wang L, Pan Z, Li L, Li H, Xu W, Luo Y, Zeng H, Dai L, Xiao H, Sharshov K, Shestopalov A, Shi Y, Yan J, Li X, Liu Y, Lei F, Liu W, Gao GF. Sci China Life Sci 60 1386-1391 (2017)
  24. Convergent Evolution of Human-Isolated H7N9 Avian Influenza A Viruses. Xiang D, Shen X, Pu Z, Irwin DM, Liao M, Shen Y. J. Infect. Dis. 217 1699-1707 (2018)
  25. H7N9 influenza A virus in turkeys in Minnesota. Lebarbenchon C, Pedersen JC, Sreevatsan S, Ramey AM, Dugan VG, Halpin RA, Ferro PJ, Lupiani B, Enomoto S, Poulson RL, Smeltzer M, Cardona CJ, Tompkins SM, Wentworth DE, Stallknecht DE, Brown JD. J. Gen. Virol. 96 269-276 (2015)
  26. Letter Ribavirin is effective against drug-resistant H7N9 influenza virus infections. Bi Y, Wong G, Liu Y, Liu L, Gao GF, Shi Y. Protein Cell 7 611-614 (2016)
  27. Source of oseltamivir resistance due to single E119D and double E119D/H274Y mutations in pdm09H1N1 influenza neuraminidase. Hanpaibool C, Leelawiwat M, Takahashi K, Rungrotmongkol T. J Comput Aided Mol Des 34 27-37 (2020)
  28. 220 mutation in the hemagglutinin of avian influenza A (H7N9) virus alters antigenicity during vaccine strain development. Liu L, Lu J, Li Z, Zhou J, Guo J, Li X, Liu J, Shu Y, Wang D. Hum Vaccin Immunother 14 532-539 (2018)
  29. Letter Avian Influenza A (H7N9) Virus in a Wild Land Bird in Central China, Late 2015. Yao Y, Zhang T, Yang W, Shao Z, He B, Chen X, Wu L, Jin E, Liu H, Chen J, Chen J. Virol Sin 33 96-99 (2018)
  30. Computational assay of Zanamivir binding affinity with original and mutant influenza neuraminidase 9 using molecular docking. Thai KM, Le DP, Tran NV, Nguyen TT, Tran TD, Le MT. J. Theor. Biol. 385 31-39 (2015)
  31. Risk Assessment of Fifth-Wave H7N9 Influenza A Viruses in Mammalian Models. Sun X, Belser JA, Pappas C, Pulit-Penaloza JA, Brock N, Zeng H, Creager HM, Le S, Wilson M, Lewis A, Stark TJ, Shieh WJ, Barnes J, Tumpey TM, Maines TR. J. Virol. 93 (2019)
  32. Solving the mystery of H7N9 by crystal balls. Yuen KY. Cell Res. 23 1335-1336 (2013)
  33. Synthesis of Sulfo-Sialic Acid Analogues: Potent Neuraminidase Inhibitors in Regards to Anomeric Functionality. Vavricka CJ, Muto C, Hasunuma T, Kimura Y, Araki M, Wu Y, Gao GF, Ohrui H, Izumi M, Kiyota H. Sci Rep 7 8239 (2017)
  34. Letter Atypical group 1 neuraminidase pH1N1-N1 bound to a group 1 inhibitor. Wu Y, Vavricka CJ, Wu Y, Li Q, Rudrawar S, Thomson RJ, von Itzstein M, Gao GF, Qi J. Protein Cell 6 771-773 (2015)
  35. Development of a quadruple qRT-PCR assay for simultaneous identification of highly and low pathogenic H7N9 avian influenza viruses and characterization against oseltamivir resistance. Yang Y, Li S, Wong G, Ma S, Xu Z, Zhao X, Li H, Xu W, Zheng H, Lin J, Zhao Q, Liu W, Liu Y, Gao GF, Bi Y. BMC Infect. Dis. 18 406 (2018)
  36. Risk assessment of human infection with avian influenza A (H7N9) virus in Taiwan. Jian SW, Liu DP, Chang FY. J. Formos. Med. Assoc. 113 397-399 (2014)
  37. Chances and challenges in China. Tefsen B. Protein Cell 7 233-235 (2016)
  38. Cross-reactivity between avian influenza A (H7N9) virus and divergent H7 subtypic- and heterosubtypic influenza A viruses. Guo L, Wang D, Zhou H, Wu C, Gao X, Xiao Y, Ren L, Paranhos-BaccalĂ  G, Shu Y, Jin Q, Wang J. Sci Rep 6 22045 (2016)
  39. Detecting the Neuraminidase R294K Mutation in Avian Influenza A (H7N9) Virus Using Reverse Transcription Droplet Digital PCR Method. Lou X, Yan H, Su L, Sun Y, Wang X, Gong L, Chen Y, Li Z, Fang Z, Mao H, Chen K, Zhang Y. Viruses 15 983 (2023)
  40. Diverse biological characteristics and varied virulence of H7N9 from Wave 5. Bao L, Bi Y, Wong G, Qi W, Li F, Lv Q, Wang L, Liu F, Yang Y, Zhang C, Liu WJ, Quan C, Jia W, Liu Y, Liu W, Liao M, Gao GF, Qin C. Emerg Microbes Infect 8 94-102 (2019)
  41. Evolutionary dynamics of the H7N9 avian influenza virus based on large-scale sequence analysis. Xiong J, Zhao P, Yang P, Yan Q, Jiang L. PLoS ONE 14 e0220249 (2019)
  42. Genomic characterization of influenza A (H7N9) viruses isolated in Shenzhen, Southern China, during the second epidemic wave. Fang S, Wang X, Dong F, Jin T, Liu G, Lu X, Peng B, Wu W, Liu H, Kong D, Tang X, Qin Y, Mei S, Xie X, He J, Ma H, Zhang R, Cheng J. Arch. Virol. 161 2117-2132 (2016)
  43. Highly pathogenic avian influenza H7N9 viruses with reduced susceptibility to neuraminidase inhibitors showed comparable replication capacity to their sensitive counterparts. Tang J, Zhang J, Zhou J, Zhu W, Yang L, Zou S, Wei H, Xin L, Huang W, Li X, Cheng Y, Wang D. Virol. J. 16 87 (2019)
  44. Impact of the R292K Mutation on Influenza A (H7N9) Virus Resistance towards Peramivir: A Molecular Dynamics Perspective. Mtambo SE, Ugbaja SC, Kumalo HM. Molecules 27 1645 (2022)
  45. In Silico Studies Reveal Peramivir and Zanamivir as an Optimal Drug Treatment Even If H7N9 Avian Type Influenza Virus Acquires Further Resistance. Sarukhanyan E, Shanmugam TA, Dandekar T. Molecules 27 5920 (2022)
  46. Plasticity of the 340-Loop in Influenza Neuraminidase Offers New Insight for Antiviral Drug Development. Han N, Ng JTY, Li Y, Mu Y, Huang Z. Int J Mol Sci 21 (2020)
  47. Risk of Environmental Exposure to H7N9 Influenza Virus via Airborne and Surface Routes in a Live Poultry Market in Hebei, China. Zhang C, Guo K, Cui H, Chen L, Zhang C, Wang X, Li J, Fu Y, Wang Z, Guo Z, Liu J, Dong S. Front Cell Infect Microbiol 11 688007 (2021)
  48. Structural and inhibitor sensitivity analysis of influenza B-like viral neuraminidases derived from Asiatic toad and spiny eel. Li L, Chai Y, Peng W, Li D, Sun L, Gao GF, Qi J, Xiao H, Liu WJ, von Itzstein M, Gao F. Proc Natl Acad Sci U S A 119 e2210724119 (2022)
  49. Substitution of I222L-E119V in neuraminidase from highly pathogenic avian influenza H7N9 virus exhibited synergistic resistance effect to oseltamivir in mice. Tang J, Gao R, Liu L, Zhang S, Liu J, Li X, Fang Q, Feng Z, Xu C, Huang W, Wang D. Sci Rep 11 16293 (2021)
  50. Targeting the Human Influenza a Virus: The Methods, Limitations, and Pitfalls of Virtual Screening for Drug-like Candidates Including Scaffold Hopping and Compound Profiling. Scior T, Cuanalo-Contreras K, Islas AA, Martinez-Laguna Y. Viruses 15 1056 (2023)
  51. The inhibitory effect of sodium baicalin on oseltamivir-resistant influenza A virus via reduction of neuraminidase activity. Jin J, Chen Y, Wang D, Ma L, Guo M, Zhou C, Dou J. Arch. Pharm. Res. 41 664-676 (2018)