Efficacy, Mechanism and Antiviral Resistance of Neuraminidase Inhibitors and Adamantane against Avian Influenza

Dyah Ayu Hewajuli, NLPI Dharmayanti

Abstract

Vaccination and antiviral drug are often used to control influenza. However, the effectiveness of vaccine was impaired due to the emergence of new variant of virus strain. Antiviral drug consists of prophylactic and curative substances, namely M2 ion channel inhibitors (adamantane; amantadine and rimantadine) and neuraminidase (NA) inhibitors (NAIs; oseltamivir, zanamivir, peramivir, laninamivir). The synthesis and modification of antiviral neuraminidase (NA) inhibitors (NAIs) and adamantanes increased the antiviral effectiveness. The mechanism of the neuraminidase inhibitor is to prevent influenza infection by inhibiting the release of the virus from internal cells. Adamantane is antiviral drug that selectively inhibits the flow of H+ ions through M2 protein to prevent the uncoating virus particles getting into the endosome. The substitution of (H275Y, S247N, I223L, K150N, R292K, I222T, R152K, R118K, E119V) on NA protein caused resistance of avian influenza virus against the neuraminidase inhibitor. The combination of mutations (S247N, I223L, K150N) increased the resistance of influenza A (H5N1) virus. The diffusion of adamantane resistance varies among HA subtypes, the species of host, the period of isolation, and region. Mutations at residues of 26, 27, 30, 31 or 34 transmembrane M2 protein caused adamantane resistance. The unique substitution (V27I) of M2 protein of clade 2.3.2 H5N1 subtype isolated in Indonesia in 2016 has been contributed to the amantadine resistance. Antiviral combination of M2 ion channel inhibitors and neuraminidase (NA) inhibitors is effective treatments for the resistance.

Keywords

Adamantane; neuraminidase inhibitor; resistance; avian influenza

Full Text:

PDF

References

Abed Y, Pizzorno A, Boivin G. 2012. Therapeutic activity of intramuscular peramivir in mice infected with are combinant influenza A/WSN/33(H1N1) virus containing the H275Y neuraminidase mutation. Antimicrob Agents Chemother. 56:4375-4380.

Achenbach JE, Bowen RA. 2013. Effect of oseltamivir carboxylate consumption on emergence of drug-resistant H5N2 avian influenza virus in Mallard ducks. Antimicrob Agents Chemother. 57:2171-2181.

Alves Galvão MG, Rocha Crispino Santos MA, Alves da Cunha AJL. 2014. Amantadine and rimantadine for influenza A in children and the elderly. Cochrane Database Syst Rev. 11:CD002745. doi: 10.1002/14651858.CD002745.pub4.

Astrahan P, Kass I, Cooper MA, Arkin IT. 2004. A novel method of resistance for influenza against a channelâ€blocking antiviral drug. Proteins. 55:251-257.

Azuma T, Ishiuchi H, Inoyama T, Teranishi Y, Yamaoka M, Sato T, Yamashita N, Tanaka H, Mino Y. 2015. Detection of peramivir and laninamivir, new anti-influenza drugs, in sewage effluent and river waters in Japan. PLoS One. 10:e0131412. doi: 10.1371/journal.pone.0131412.

Babu YS, Chand P, Bantia S, Kotian P, Dehghani A, El-Kattan Y, Lin TH, Hutchison TL, Elliott AJ, Parker CD, Ananth LS, Horn LL, Laver GW, Montgomery JA. 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.

Baumann J, Kouassi NM, Foni E, Klenk H, Matrosovicha M. 2016. H1N1 swine influenza viruses differ from avian precursors by a higher ph optimum of membrane fusion. J Virol. 9:1569-1577.

Belser JA, Brock N, Sun X, Jones J, Zanders N, Hodges E, A. Pulit-Penaloza J, Wentworth D, Tumpey TM, Davis T, Maines TR. 2018. Mammalian pathogenesis and transmission of avian influenza A (H7N9) viruses, Tennessee, USA, 2017. Emerg Infect Dis. 24:149-152.

Benton DJ, Wharton SA, Martin SR, McCauley JW. 2017. Role of neuraminidase in influenza a (H7N9) virus receptor binding. J Virol. 91:e02293-16. doi: 10.1128/JVI.02293-16

Boulo S, Akarsu H, Ruigrok RW, Baudin F. 2007. Nuclear traffic of influenza virus proteins and ribonucleoprotein complexes. Virus Res. 124:12-21.

[CDC] Centre for Disease Prevention and Control. Influenza Antiviral Medications: Summary for Clinicians | Health Professionals | Seasonal Influenza (Flu), 2018. Available from: http://www.cdc.gov/flu/profes

Chen W, Sun S, Li Z. 2012. Two glycosylation sites in H5N1 influenza virus hemagglutinin that affect binding preference by computer-based analysis. PLoS One. 7:e38794. doi: 10.1371/journal.pone.0038794.

Cheung CL, Rayner RM, Smith GJD, Wang P, Naipospos TSP, Zhang J, Yuen KY, Webster RG, Peiris JSM, Guan Y, Chen H. 2006. Distribution of amantadine-resistant H5N1 avian influenza variants in Asia. J Infect Dis. 193:1626-1629.

Cohen M, Zhang XQ, Senaati HP, Chen HW, Varki NM, Schooley RT, Gagneux P. 2013. Influenza A penetrates host mucus by cleaving sialic acids with neuraminidase. Virol J. 10:321.

De Conto F, Covan S, Arcangeletti MC, Orlandini G, Gatti R, Dettori G, Chezzi C. 2011. Differential infectious entry of human influenza A/NWS/33 virus (H1N1) in mammalian kidney cells. Virus Res. 155:221-230.

Dharmayanti NLPI, Ibrahim F, Soebandrio A. 2010. Amantadine resistant of Indonesian influenza H5N1 subtipe virus during 2003-2008. Microbiol Indones. 5:11-16.

Dharmayanti NLPI, Hartawan R, Hewajuli DA, Hardiman, Wibawa H, Pudjiatmoko. 2013. Karakteristik molekuler dan patogenesitas virus H5N1 Clade 2.3.2. asal Indonesia. JITV. 18:99-113.

Dharmayanti NLPI, Hartawan R, Pudjiatmoko, Wibawa H, Hardiman, Balish A, Donis R, Davis CT, Samaan G. 2014. Genetic characterization of Clade 2.3.2.1 Avian Influenza A (H5N1) Viruses, Indonesia, 2012. Emerg Infect Dis. 20:671-674.

Dong H, Fiorin G, DeGrado WF, Klein ML. 2014. Proton release from the histidine-tetrad in the M2 channel of the influenza A virus. J Phys Chem B. 118:12644-12651.

Dong G, Peng C, Luo J, Wang C, Han L, Wu B, Ji G, He H. 2015. Adamantane-resistant influenza a viruses in the world (1902-2013): Frequency and distribution of M2 gene mutations. PLoS One. 10:e0119115.

Douglas Jr RG. 1990. Antimicrobial agents. In: Goodman Gilman A, Rall TW, Nies AS, Taylor P, editors. Goodman and Gilman’s the pharmacological basis of therapeutics. New York (USA): Pergamon Press.

Drakopoulos A, Tzitzoglaki C, Ma C, Freudenberger K, Hoffmann A, Hu Y, Gauglitz G, Schmidtke M, Wang J, Kolocouris A. 2017. Affinity of rimantadine enantiomers against influenza A/M2 protein revisited. ACS Med Chem Lett. 8:145-150.

Durrant MG, Egget DL, Busath DD. 2015. Investigation of a recent rise of dual amantadine-resistance mutations in the influenza A M2 sequence. BMC Genet. 16:S3.

Franca M, Stallknecht DE, Howerth EW. 2013. Expression and distribution of sialic acid influenza virus receptors in wild birds. Avian Pathol. 42:60-71.

Gillespie L, Roosendahl P, Ng WC, Brooks AG, Reading PC, Londrigan SL. 2016. Endocytic function is critical for influenza A virus infection via DCSIGN and L-SIGN. Sci Rep. 6:19428. doi: 10.1038/srep19428

Gillman A, Muradrasoli S, Mardnas A, So¨derstro¨m H, Fedorova G, Lowenthal M, Wille M, Daggfeltd A. 2015a. Oseltamivir resistance in influenza A (H6N2) caused by an R292K substitution in neuraminidase is not maintained in mallards without drug pressure. PLoS One. 10:e0139415.

Gillman A, Nykvist M, Muradrasoli S, So¨ derstro¨m H, Wille M, Daggfeldt A, Brojer C, Waldenström J, Olsen B, Järhult JD. 2015b. Influenza A (H7N9) virus acquires resistance-related neuraminidase I222T substitution when infected mallards are exposed to low levels of oseltamivir in water. Antimicrob Agents Chemother. 59:5196-5202.

Gu RX, Liu LA, Wei DQ, Du JG, Liu L, Liu H. 2011. Free energy calculations on the two drug binding sites in the M2 proton channel. J Am Chem Soc. 133:10817-10825.

He G, Qiao J, Dong C, He C, Zhao L, Tian Y. 2008. Amantadine-resistance among H5N1 avian influenza viruses isolated in Northern China. Antiviral Res. 77:72-76.

Hewajuli DA. 2017. Sensitivitas virus avian influenza subtipe H5N1 clade 2.3.2 asal Indonesia terhadap obat antiviral amantadin [Tesis]. [Bogor (Indonesia)]: Institut Pertanian Bogor.

Hoopes JD, Driebe EM, Kelley E, Engelthaler DM, Keim PS, Perelson AS, Rong L, Went GT, Nguyen JT. 2011. Triple combination antiviral drug (TCAD) composed of amantadine, oseltamivir, and ribavirin impedes the selection of drug-resistant influenza A virus. PLoS One. 6:e29778. doi: 10.1371/journal.pone.0029778.

Hu F, Schmidt-Rohr K, Hong M. 2012. NMR detection of pH-dependent histidinewater proton exchange reveals the conduction mechanism of a transmembrane proton channel. J Am Chem Soc. 134:3703-3713.

Hu Y, Lu S, Song Z, Wang W, Hao P, Li J, Zhang X, Yen H, Shi B, Li T, Guan W, Xu L, Liu Y, Wang S, Zhang X, 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.

Huang L, Cao Y, Zhou J, Qin K, Zhu W, Zhu Y, Yan L, Wang D, Wei H, Shu Y. 2014. A conformational restriction in the influenza A virus neuraminidase binding site by R152 results in a combinational effect of I222T and H274Y on oseltamivir resistance. Antimicrob Agents Chemother. 58:1639-1645.

Hurt AC, Lee RT, Leang SK, Cui L, Deng YM, Phuah SP, Caldwell N, Freeman K, Komadina N, Smith D, Speers D, Kelso A, Lin RT, Maurer-Stroh S, Barr IG. 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. Eurosurveillance [Internet]. 16:19884. Available from: http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=19884

Hurt AC, Hardie K, Wilson NJ, Deng YM, Osbourn M, Leang SK, Lee RT, Iannello P, Gehrig N, Shaw R, Wark P, Caldwell N, Givney RC, Xue L, Maurer-Stroh S, Dwyer DE, Wang B, Smith DW, Levy A, Booy R, Dixit R, Merritt T, Kelso A, Dalton C, Durrheim D, Barr IG. 2012. Characteristics of a widespread community cluster of H275Y oseltamivir-resistant A (H1N1) pdm09 influenza in Australia. J Infect Dis. 206:148-157.

Ishizuka H, Yoshiba S, Okabe H, Yoshihara K. 2010. Clinical pharmacokinetics of laninamivir, a novel long-acting neuraminidase inhibitor, after single and multiple inhaled doses of its prodrug, CS-8958, in healthy male volunteers. J Clin Pharmacol. 50:1319-1329. doi: 10.1177/0091270009356297.

Ikematsu H, Kawai N, Iwaki N, Kashiwagi S. 2015. In vitro neuraminidase inhibitory activity of four neuraminidase inhibitors against clinical isolates of influenza virus in the Japanese 2012-2013 season. J Infect Chemother Off J Jpn Soc Chemother. 21:39-42.

Kalashnikov AI, Sysolyatin SV, Sakovich GV, Sonina EG, Shchurova IA. 2013. Facile method for the synthesis of oseltamivir phosphate. Russ Chem Bull. 62:163-170.

Kim CU, Lew W, Williams MA, Liu H, Zhang L, Swaminathan S, Bischofberger N, Chen MS, Mendel DB, Tai CY, Laver WG, Stevens RC. 1997. Influenza neuraminidase inhibitors possessing a novel hydrophobic interaction in the enzyme active site:? design, synthesis, and structural analysis of carbo cyclic sialic acid analogues with potent anti-influenza activity. J Am Chem Soc. 119:681-690. doi: 10.1021/ja963036t.

Kiso M, Kubo S, Ozawa M, Le QM, Nidom CA, Yamashita M, Kawaoka Y. 2010. Efficacy of the new neuraminidase inhibitor CS-8958 against H5N1 influenza viruses. PLoS Pathog. 6:e1000786.

Le TH, Nguyen NT. 2014. Evolutionary dynamics of highly pathogenic avian influenza A/H5N1 HA Clades and vaccine implementation in Vietnam. Clin Exp Vaccine Res. 3:117-127.

Lee N, Leo YS, Cao B, Chan PK, Kyaw WM, Uyeki TM, Tam WWS, Cheung CSK, Yung IMH, Li H, Gu L, Liu Y, Liu Z, Qu J, Hui DS. 2015. Neuraminidase inhibitors, superinfection and corticosteroids affect survival of influenza patients. Eur Respir J. 45:1642-1652.

Li JH, Dohna Z, Anchell NL, Adams SC, Dao NT, Xing Z, Cardona CJ. 2010. Adaptation and transmission of a duck-origin avian influenza virus in poultry species. Virus Res. 147:40-46.

Liang R, Li H, Swanson JM, Voth GA. 2014. Multiscale simulation reveals a multifaceted mechanism of proton permeation through the influenza A M2 proton channel. Proc Natl Acad Sci USA. 111:9396-9401. doi: 10.1073/pnas.1401997111.

Liang L, Deng G, Shi J, Wang S, Zhang Q, Kong H, Gu C, Guan Y, Suzuki Y, Li Y, Jiang Y, Tian G, Liu L, Li C, Chen H. 2016a. Genetics, receptor binding, replication, and mammalian transmission of H4 avian influenza viruses isolated from live poultry markets in China. J Virol. 90:1455-1469.

Liang R, Swanson JMJ, Madsen JJ, Hong M, DeGradoe WF, Votha GA. 2016b. Acid activation mechanism of the influenza A M2 proton channel. Proc Natl Acad Sci USA. 113:E6955-E6964. doi: 10.1073/pnas. 1615471113.

Lin PH, Chao TL, Kuo SW, Wang JT, Hung CC, Lin HC, Yang ZY, Ho SY, Chang CK, Huang MS, Chen HH, Chen YC, Lai HS, Chang SY, Chang SC, Yang PC. 2014. Virological, serological, and antiviral studies in an imported human case of Avian Influenza A (H7N9) Virus in Taiwan. Clin Infect Dis. 58:242-246.

Liu B, Ma P, Wang X, Kong Y, Zhang L, Liu B. 2014. Synthesis of three rimantadine schiff bases and their biological effects on serum albumin. Iran J Pharmaceu Res. 13:1183-1190.

Matrosovich MN, Gambaryan AS, Teneberg S, Piskarev VE, Yamnikova SS, Lvov DK, Robertson JS, Karlsson KA. 1997. Avian influenza A viruses differ from human viruses by recognition of sialyloligosaccharides and gangliosides and by a higher conservation of the HA receptor-binding site. Virology. 233:224-234.

Naguib MM, Kinne J, Chen H, Chan K, Joseph S, Wong P, Woo PCY, Wernery R, Beer M, Wernery U, Harder TC. 2015. Outbreaks of highly pathogenic avian influenza H5N1 Clade 2.3.2.1c in hunting falcons and kept wild birds in Dubai implicate intercontinental virus spread. J Gen Virol. 96:3212-3222.

Nguyen JT, Smee DF, Barnard DL, Julander JG, Gross M, Jong MD, Went GT. 2012. Efficacy of combined therapy with amantadine, oseltamivir, and ribavirin in vivo against susceptible and amantadine-resistant influenza A viruses. PLoS One. 7:e31006. doi: 10.1371/journal.pone.0031006.

Nguyen TH, Than VT, Thanh HD, Hung VK, Nguyen DT, Kim W. 2016. Intersubtipe reassortments of H5N1 Highly Pathogenic Avian Influenza viruses isolated from quail. PLoS One. 1-15. doi: 10.1371/journal. pone.0149608

Palese P, Tobita K, Ueda M, Compans RW. 1974. Characterization of temperature sensitive influenza virus mutants defective in neuraminidase. Virology. 61:397-410.

Petkova AM, Georgiev G, Seiler P, Darnell D, Franks J, Krauss S, Webby RJ, Webster RG. 2012. Spread of influenza virus A (H5N1) Clade 2.3.2.1 to Bulgaria in common buzzards. Emerg Infect Dis. 18:1596-1602.

Prichard WW. 1971. Pharmaceutical compositions and methods of controlling influenza a virus infection utilizing substituted adamantanes and tricyclo (4.3. 1.13. 8) undecanes. United States patent US 3,592,934.

Rudrawar S, Dyason JC, Rameix-Welti MA, Rose FJ, Kerry PS, Russell RJ, van der Werf S, Thomson RJ, Naffakh N, von Itzstein M. 2010. Novel sialic acid derivatives lock open the 150-loop of an influenza A virus group-1 sialidase. Nat Commun. 1:113. doi: 10.1038/ncomms1114.

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.

Seladi-Schulman J, Steel J, Lowen AC. 2013. Spherical influenza viruses have a fitness advantage in embryonated eggs, while filament-producing strains are selected in vivo. J Virol. 87:13343-13353.

Seladi-Schulman J, Campbell PJ, Suppiah S, Steel J, Lowen AC. 2014. Filament-producing mutants of influenza A/Puerto Rico/8/1934 (H1N1) virus have higher neuraminidase activities than the spherical wild-type. PLoS One. 9:e112462. doi: 10.1371/journal.pone. 0112462.

Seo S, Englund JA, Nguyen JT, Pukrittayakamee S, Lindegardh N, Tarning J, Tambyah PA, Renaud C, Went GT, deJong MD, Boeckh MJ. 2013. Combination therapy with amantadine, oseltamivir, and ribavirin for influenza A infection:safety and pharmacokinetics. Antiviral Therapy. 18:377-386.

Smith GJD, Naipospos TSP, Nguyen TD, De Jong MD, Vijaykrishna D, Usman TB, Hassa SS, Nguyen TV, Dao TV, Bui NA, Leung YHC, Cheung CL, Rayner JM, Zhang JX, Zhang LJ, Poon LLM, Li KS, Nguyen VC, Hien TT, Farrar J, Webster RG, Chen H, Peiris JSM, Guan Y. 2006. Evolution and adaptation of H5N1 influenza virus in avian and human hosts in Indonesia and Vietnam. Virology. 350:258-268.

Smith GJ, Vijaykrishna D, Ellis TM, Dyrting KC, Leung YH, Bahl J, Wong CW, Kai H, Chow MKW, Duan L, Chan ASL, Zhang LJ, Chen H, Luk GSM, Peiris JSM, Guan Y. 2009. Characterization of avian influenza viruses A (H5N1) from wild birds, Hong Kong, 2004–2008. Emerg Infect Dis. 15:402-407.

Stauffer SY, Feng, Nebioglu F, Heilig R, Picotti P, Helenius A. 2014. Stepwise priming by acidic pH and ahigh K+ concentration is required for efficient uncoating of influenza A virus cores after penetration. J Virol. 88:13029-13046.

Short KR, Brooks AG, Reading PC, Londrigan SL. The fate of influenza A virus after infection of human macrophages and dendritic cells. J Gen Virol. 93:2315-2325.

Thaa B, Levental I, Herrmann A, Veit M. 2011. Intrinsic membrane association of the cytoplasmic tail of influenza virus M2 protein and lateral membrane sorting regulated by cholesterol binding and palmitoylation. Biochem J. 437:389-397.

Thomaston JL, Alfonso-Prieto M, Woldeyes RA, Fraser JS, Klein ML, Fiorin G, DeGrado WF. 2015. High-resolution structures of the M2 channel from influenza A virus reveal dynamic pathways for proton stabilization and transduction. Proc Natl Acad Sci USA. 112:14260-14265. doi: 10.1073/pnas. 1518493112.

Thomaston JL, Grado WFD. 2016. Crystal structure of the drug-resistant S31N influenza M2 proton channel. Prot Sci. 25:1551-1554.

Vachieri SG, Xiong X, Collins PJ, Walker PA, Martin SR, Haire LF, Zhang Y, McCauley JW, Gamblin SJ, Skehel JJ. 2014. Receptor binding by H10 influenza viruses. Nature. 511:475-477.

Von Itzstein M, Wu WY, Kok GB, Pegg MS, Dyason JC, Jin B, Phan TV, Smythe ML, White HF, Oliver SW, Colman PM, Varghese JN, Ryan DM, Woods JM, Bethell RC, Hotham VJ, Cameron JM, Penn CR. 1993. Rational design of potent sialidase-based inhibitors of influenza virus replication. Nature. 363:418-423. doi: 10.1038/363418a0.

Von Itzstein M. 2007. The war against influenza: Discovery and development of sialidase inhibitors. Nat Rev. 6:967-974.

Vu DB, Nguyen TV, Le ST, Phan CH. 2017. An improved synthesis of amantadine hydrochloride. Org Process Res Dev. 21:1758-1760.

Wagner R, Wolff T, Herwig A, Pleschka S, Klenk HD. 2000. Interdependence of hemagglutinin glycosylation and neuraminidase as regulators of influenza virus growth: A study by reverse genetics. J Virol. 74:6316-6323.

Wan X, Dong L, Lan Y, Long L, Xu C, Zou S, Li Z, Wen L, Cai Z, Wang W, Li X, Yuan F, Sui H, Zhang Y, Dong J, Sun S, Gao Y, Wang M, Bai T, Yang L, Li D, Yang W, Yu H, Wang S, Feng Z, Wang Y, Guo Y, Webby RJ, Shu Y. 2011. Indications that live poultry markets are a major source of human H5N1 influenza virus infection in China. J Virol. 85:13432-13438.

Wang D, Harmon A, Jin J, Francis DH, Christopher-Hennings J, Nelson E, Montelaro RC, Li F. 2010. The lack of an inherent membrane targeting signal is responsible for the failure of the matrix (M1) protein of influenza A virus to bud into virus-like particles. J Virol. 84:4673-4681.

Watanabe A, Chang SC, Kim MJ, Chu DW, Ohashi Y, MARVEL Study Group. 2010. Long-acting neuraminidase inhibitor laninamivir octanoate versus oseltamivir for treatment of influenza: a double-blind, randomized, noninferiority clinical trial. Clin Infect Dis. 51:1167-1175.

Woods JM, Bethell RC, Coates JAV, Healy N, Hiscox SA, Pearson BA, Ryan DM, Ticehurst J, Tilling J, Walcotr SM, Penn CR. 1993. 4-Guanidino-2,4-Dideoxy-2,3-Dehydro-N-Acetylneuraminic Acid is a highly effective inhibitor both of the sialidase (neuraminidase) and of growth of a wide range of influenza a and b viruses in vitro. Antimicrob Agents Chemoth. 37:1473-1479.

Wright AK, Batsomboon P, Dai J, Hung I, Zhou H, Dudley GB, Cross TA. 2016. Differential binding of rimantadine enantiomers to influenza a M2 proton channel. Cross J Am Chem Soc. 138:1506-1509. doi: 10.1021/jacs.5b13129.

Wu WL, Siu-Ying L, Yixin C, Genyan W, Bobo WM, Wen X, Pui W, Wenjun S, Tianwei L, Kwok-Hung C, Kwok-Yung Y, Chen H. 2012. The 2008–2009 H1N1 influenza virus exhibits reduced susceptibility to antibody inhibition: Implications for the prevalence of oseltamivir resistant variant viruses. Antiviral Res. 93:144-153.

Yamashita M, Tomozawa T, Kakuta M, Tokumitsu A, Nasu H, Kubo S. 2009. CS-8958, a prodrug of the new neuraminidase inhibitor R-125489, shows long-acting anti-influenza virus activity. Antimicrob Agents Chemother. 53:186-192. doi: 10.1128/AAC.00333-08.

Yang ZF, Mok CK, Peiris JS, Zhong NS. 2015. Human infection with a novel avian influenza A (H5N6) virus. N Engl J Med. 373:487-489. doi: 10.1056/NEJMc1502983.

Zaraket H, Dapat C, Ghanem S, Ali Z, Lteif M, Kondo H, Dapat IC, Saito K, Kayali G, Suzuki H, Dbaibo G, Saito R. 2014. Characterization of human influenza viruses in Lebanon during 2010- 2011 and 2011-2012 post-pandemic seasons. Intervirology. 57:344-352. doi: 10.1159/000365758

Zhang Y, Whittaker GR. 2014. Influenza entry pathways in polarized MDCK cells. Biochem Biophys Res Commun. 450:234-239. doi: 10.1016/j.bbrc.2014. 05.095.

Zhang X, Song Z, He J, Yen H, Li J, Zhu Z, Tian D, Wang W, Xu L, Guan W, Liu Y, Wang S, Shi B, Zhang W, Qin B, Cai J, Wan Y, Xu C, Ren X, Chen H, Liu L, Yang Y, Zhou X, Zhou W, Xu J, Zhang X, Peiris M, Hu Y, Yuan Z. 2014. Drug susceptibility profile and pathogenicity of H7N9 influenza virus (Anhui1 lineage) with R292K substitution. Emerg Microbes Infect. 3:e78. doi:10.1038/emi.2014.80.

Zhu XB, Wang M, Wang SZ, Yao ZJ. 2012. Concise synthesis of zanamivir and its C4-thiocarbamido derivatives utilizing a 3 + 2-cycloadduct derived from D-glucono-delta-lactone. Tetrahedron. 68:2041-2044.

Refbacks

  • There are currently no refbacks.

Copyright (c)  2019 WARTAZOA. Indonesian Bulletin of Animal and Veterinary Sciences

Creative Commons License
This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.

View My Stats