The effect of single amino acid substitution at position 220 in the hemagglutinin glycoprotein on avian influenza H7N9 candidate vaccine virus.
Amino Acid Substitution
Animals
Dogs
Hemagglutinin Glycoproteins, Influenza Virus
/ chemistry
Influenza A Virus, H7N9 Subtype
/ genetics
Influenza Vaccines
/ chemistry
Madin Darby Canine Kidney Cells
Mutagenesis
N-Acetylneuraminic Acid
/ metabolism
Neuraminidase
/ metabolism
Reassortant Viruses
/ genetics
Reverse Genetics
Antigenicity
Avian influenza H7N9 virus
Growth characteristic
Hemagglutinin
Receptor affinity
Substitution
Journal
Virus genes
ISSN: 1572-994X
Titre abrégé: Virus Genes
Pays: United States
ID NLM: 8803967
Informations de publication
Date de publication:
Apr 2021
Apr 2021
Historique:
received:
14
07
2020
accepted:
18
01
2021
pubmed:
20
2
2021
medline:
17
8
2021
entrez:
19
2
2021
Statut:
ppublish
Résumé
Influenza vaccines represent the most effective preventive strategy to control influenza virus infections; however, adaptive mutations frequently occur in the hemagglutinin (HA) glycoprotein during the preparation of candidate vaccine virus and production of vaccine in embryonated eggs. In our previous study, we constructed candidate vaccine virus (HA-R) to match the highly pathogenic avian influenza H7N9 viruses A/Guangdong/17SF003/2016 as part of a pandemic preparedness program. However, mixed amino acids (R, G, and I) were presented at position 220 (H3 numbering) in HA during passage in embryonated eggs. The residue at position 220 is located close to the receptor-binding site and the biological characteristics of this site remain to be elucidated. Therefore, in this study, using reverse genetics, we constructed two viruses carrying the single substitution in position 220 of HA (HA-G and HA-I) and evaluated the biological effects of substitution (R with G/I) on receptor binding, neuraminidase (NA) activity, growth characteristics, genetic stability, and antigenicity. The results revealed both mutant viruses exhibited lower HA binding affinities to two receptor types (sialic acid in alpha2,3- and alpha2,6-linkage to galactose, P < 0.001) and significant better growth characteristics compared to HA-R in two cells. Moreover, under similar NA enzymatic activity, the two mutant viruses eluted more easily from agglutinated erythrocytes than HA-R. Collectively, these results implied the balance of HA and NA in mutant viruses was a stronger determinant of viral growth than the individual amino acid in the HA position 220 in HA-R without strong binding between HA and sialylated receptors. Importantly, both the substitutions conferred altered antigenicity to the mutant viruses. In conclusion, amino acid substitutions at position 220 can substantially influence viral biological properties.
Identifiants
pubmed: 33606171
doi: 10.1007/s11262-021-01827-y
pii: 10.1007/s11262-021-01827-y
doi:
Substances chimiques
Hemagglutinin Glycoproteins, Influenza Virus
0
Influenza Vaccines
0
Neuraminidase
EC 3.2.1.18
N-Acetylneuraminic Acid
GZP2782OP0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
164-171Subventions
Organisme : National Key Research and Development Program
ID : 2020ZX10101016
Organisme : National Mega-projects for Infectious Diseases
ID : 2017ZX10303401-004
Organisme : National Mega-projects for Infectious Diseases
ID : 2018ZX10305409-004-002
Organisme : Gansu Provincial Health Industry Scientific Research Project
ID : GSWSKY2017-28
Références
Smith GJD, Vijaykrishna D, Bahl J, Lycett SJ, Worobey M, Pybus OG, Ma SK, Cheung CL, Raghwani J, Samir Bhatt JS, Peiris M, Guan Yi, Rambaut A (2009) Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic. Nature 459(7250):1122–1125. https://doi.org/10.1038/nature08182
doi: 10.1038/nature08182
pubmed: 19516283
Bui C, Bethmont A, Chughtai AA, Gardner L, Sarkar S, Hassan S, Seale H, MacIntyre CR (2016) A systematic review of the comparative epidemiology of avian and human influenza a H5N1 and H7N9 - lessons and unanswered questions. Transbound Emerg Dis 63(6):602–620. https://doi.org/10.1111/tbed.12327
doi: 10.1111/tbed.12327
pubmed: 25644240
Li Li, Liu Y, Peng Wu, Peng Z, Wang X, Chen T, Wong JYT, Yang J, Bond HS, Wang L, Lau YC, Zheng J, Feng S, Qin Y, Fang VJ, Jiang H, Lau EHY, Liu S, Qi J, Zhang J, Yang J, He Y, Zhou M, Cowling BJ, Feng L, Hongjie Yu (2019) Influenza-associated excess respiratory mortality in China, 2010–15: a population-based study. Lancet Public Health 4(9):e473–e481. https://doi.org/10.1016/S2468-2667(19)30163-X
doi: 10.1016/S2468-2667(19)30163-X
pubmed: 31493844
Danielle Iuliano A, Roguski KM, Chang HH, Muscatello DJ, Palekar R, Tempia S, Cohen C, Gran JM, Schanzer D, Cowling BJ, Peng Wu, Kyncl J, Ang LW, Park M, Redlberger-Fritz M, Hongjie Yu, Espenhain L, Krishnan A, Emukule G, van Asten L, Pereira S, da Silva S, Aungkulanon UB, Widdowson M-A, Bresee JS, Network G-A (2018) Estimates of global seasonal influenza-associated respiratory mortality: a modelling study. Lancet 391(10127):1285–1300. https://doi.org/10.1016/S0140-6736(17)33293-2
doi: 10.1016/S0140-6736(17)33293-2
pubmed: 29248255
McLean KA, Goldin S, Nannei C, Sparrow E, Torelli G (2016) The 2015 global production capacity of seasonal and pandemic influenza vaccine. Vaccine 34(45):5410–5413
doi: 10.1016/j.vaccine.2016.08.019
Wang W, Janine Lu, Cotter CR, Wen K, Jin H, Chen Z (2013) Identification of critical residues in the hemagglutinin and neuraminidase of influenza virus H1N1pdm for vaccine virus replication in embryonated chicken eggs. J Virol 87(8):4642–4649
doi: 10.1128/JVI.03271-12
Barman S, Franks J, Turner JC, Yoon S-W, Webster RG, Webby RJ (2015) Egg-adaptive mutations in H3N2v vaccine virus enhance egg-based production without loss of antigenicity or immunogenicity. Vaccine 33(28):3186–3192
doi: 10.1016/j.vaccine.2015.05.011
Parker L, Wharton SA, Martin SR, Cross K, Lin Y, Liu Y, Feizi T, Daniels RS, McCauley JW (2016) Effects of egg-adaptation on receptor-binding and antigenic properties of recent influenza A (H3N2) vaccine viruses. J Gen Virol 97(6):1333–1344
doi: 10.1099/jgv.0.000457
Zost SJ, Parkhouse K, Gumina ME, Kim K, Perez SD, Wilson PC, Treanor JJ, Sant AJ, Cobey S, Hensley SE (2017) Contemporary H3N2 influenza viruses have a glycosylation site that alters binding of antibodies elicited by egg-adapted vaccine strains. Proc Natl Acad Sci USA 114(47):12578–12583
doi: 10.1073/pnas.1712377114
Garretson TA, Petrie JG, Martin ET, Monto AS, Hensley SE (2018) Identification of human vaccinees that possess antibodies targeting the egg-adapted hemagglutinin receptor binding site of an H1N1 influenza vaccine strain. Vaccine 36(28):4095–4101
doi: 10.1016/j.vaccine.2018.05.086
Doyle JD, Chung JR, Kim SS, Gaglani M, Raiyani C, Zimmerman RK, Nowalk MP, Jackson ML, Jackson LA, Monto AS, Martin ET, Belongia EA, McLean HQ, Foust A, Sessions W, Berman LaShondra, Garten RJ, Barnes JR, Wentworth DE, Fry AM, Patel MM, Flannery B (2018) Interim estimates of 2017–18 seasonal influenza vaccine effectiveness - united states, february 2018. MMWR Morb Mortal Wkly Rep 67(6):180–185
doi: 10.15585/mmwr.mm6706a2
Skowronski DM, Janjua NZ, De Serres G, Sabaiduc S, Eshaghi A, Dickinson JA, Fonseca K, Winter A-L, Gubbay JB, Krajden M, Petric M, Charest H, Bastien N, Kwindt TL, Mahmud SM, Van Caeseele P, Li Y (2014) Low 2012–13 influenza vaccine effectiveness associated with mutation in the egg-adapted H3N2 vaccine strain not antigenic drift in circulating viruses. PLoS ONE 9(3):e92153. https://doi.org/10.1371/journal.pone.0092153
doi: 10.1371/journal.pone.0092153
pubmed: 24667168
pmcid: 3965421
Wu NC, Zost SJ, Thompson AJ, Oyen D, Nycholat CM, McBride R, Paulson JC, Hensley SE, Wilson IA (2017) A structural explanation for the low effectiveness of the seasonal influenza H3N2 vaccine. PLoS Pathog 13(10):e1006682. https://doi.org/10.1371/journal.ppat.1006682
doi: 10.1371/journal.ppat.1006682
pubmed: 29059230
pmcid: 5667890
Li X, Gao Y, Ye Z (2019) A Single Amino Acid Substitution at Residue 218 of Hemagglutinin Improves the Growth. J Virol 93(19):e00570-e619. https://doi.org/10.1128/JVI.00570-1915
doi: 10.1128/JVI.00570-1915
pubmed: 31270231
pmcid: 6744242
Teng Q, Dawei Xu, Shen W, Liu Q, Rong G, Li X, Yan L, Yang J, Chen H, Hai Yu, Ma W, Lia Z (2016) Single mutation at position 190 in hemagglutinin enhances binding affinity for human type sialic acid receptor and replication of h9n2 avian influenza virus in mice. J Virol 90(21):9806–9825
doi: 10.1128/JVI.01141-16
Asaoka N, Tanaka Y, Sakai T, Fujii Y, Ohuchi R, Ohuchi M (2006) Low growth ability of recent influenza clinical isolates in MDCK cells is due to their low receptor binding affinities. Microbes Infect 8(2):511–51917
doi: 10.1016/j.micinf.2005.08.006
Ito T, Suzuki Y, Takada A, Kawamoto A, Otsuki K, Masuda H, Yamada M, Suzuki T, Kida H, Kawaoka Y (1997) Differences in sialic acid-galactose linkages in the chicken egg amnion and allantois influence human influenza virus receptor specificity and variant selection. J Virol 71(4):3357–3362
doi: 10.1128/JVI.71.4.3357-3362.1997
Shinya K, Ebina M, Yamada S, Ono M, Kasai N, Kawaoka Y (2006) Avian flu: influenza virus receptors in the human airway. Nature 440(7083):435–436
doi: 10.1038/440435a
Gaymard A, Le Briand N, Frobert E, Lina B, Escuret V (2016) Functional balance between neuraminidase and haemagglutinin in influenza viruses. Clin Microbiol Infect 22(12):975–983
doi: 10.1016/j.cmi.2016.07.007
Liu L, Jian Lu, Li Zi, Zhou J, Guo J, Li X, Liu J, Shu Y, Wang D (2018) 220 Mutation in the hemagglutinin of avian influenza A (H7N9) virus alters antigenicity during vaccine strain development. Hum Vaccin Immunother 14(3):532–539
doi: 10.1080/21645515.2017.1419109
de Graaf M, Fouchier RAM (2014) Role of receptor binding specificity in influenza A virus transmission and pathogenesis. EMBO J 33(8):823–841
doi: 10.1002/embj.201387442
Yang H, Chen L-M, Carney PJ, Donis RO, Stevens J (2010) Structures of receptor complexes of a North American H7N2 influenza hemagglutinin with a loop deletion in the receptor binding site. PLoS Pathog 6(9):e1001081. https://doi.org/10.1371/journal.ppat.1001081
doi: 10.1371/journal.ppat.1001081
pubmed: 20824086
pmcid: 2932715
Zhao Y, Zhijun Yu, Liu L, Wang T, Sun W, Wang C, Xia Z, Gao Y, Zhou Bo, Qian J, Xia X (2016) Adaptive amino acid substitutions enhance the virulence of a novel human H7N9 influenza virus in mice. Vet Microbiol 187:8–14
doi: 10.1016/j.vetmic.2016.02.027
Li D, Saito R, Suzuki Y, Sato I, Zaraket H, Dapat C, Caperig-Dapat IM, Suzuki H (2009) In vivo and in vitro alterations in influenza A/H3N2 Virus M2 and hemagglutinin genes: effect of passage in MDCK-SIAT cells and conventional MDCK cells. J Clin Microbiol 47(2):466–468
doi: 10.1128/JCM.00892-08
World Health Organization. (2019) Guidelines for the safe development and production of vaccines to human pandemic influenza viruses and influenza viruses with pandemic potential. https://www.who.int/biologicals/expert_committee/Annex_3_WHO_TRS_1016_web3.pdf?ua=1 . Accessed 10 Dec 2019
Liang L, Deng G, Shi J, Wang S, Zhang Q, Kong H, Chunyang Gu, Guan Y, Suzuki Y, Li Y, Jiang Y, Tian G, Liu L, Li C, Chen H (2015) Genetics, receptor binding, replication, and mammalian transmission of H4 avian influenza viruses isolated from live poultry markets in China. J Virol 90(3):1455–1469
doi: 10.1128/JVI.02692-15
Kallewaard NL, Corti D, Collins PJ, Neu U, McAuliffe JM, Benjamin E, Wachter-Rosati L, Palmer-Hill FJ, Yuan AQ, Walker PA, Vorlaender MK, Bianchi S, Guarino B, De Marco A, Vanzetta F, Agatic G, Foglierini M, Pinna D, Fernandez-Rodriguez B, Fruehwirth A, Silacci C, Ogrodowicz RW, Martin SR, Sallusto F, Suzich JA, Lanzavecchia A, Zhu Q, Gamblin SJ, Skehel JJ (2016) Structure and function analysis of an antibody recognizing all influenza A subtypes. Cell 166(3):596–608
doi: 10.1016/j.cell.2016.05.073
Feier R, Lingling C, Kun Q, Mingbin L, Haiying C, Jianfang Z (2019) Generation and preliminary characterization of chimeric antibodies against neuraminidase of H7N9 subtype influenza A virus. Chin J Exp Clin Virol 33(2):212–216
Castrucci MR, Kawaoka Y (1993) Biologic importance of neuraminidase stalk length in influenza A virus. J Virol 67:759–764
doi: 10.1128/JVI.67.2.759-764.1993
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(14):6316–6323
doi: 10.1128/JVI.74.14.6316-6323.2000
Diederich S, Berhane Y, Embury-Hyatt C, Hisanaga T, Handel K, Cottam-Birt C, Ranadheera C, Kobasa D, Pasick J (2015) Hemagglutinin-neuraminidase balance influences the virulence phenotype of a recombinant H5N3 influenza a virus possessing a polybasic HA0 cleavage site. J Virol 89(21):10724–10734
doi: 10.1128/JVI.01238-15
World Health Organization. (2011). Manual for the laboratory diagnosis and virological surveillance of influenza. World Health Organization. https://apps.who.int/iris/handle/10665/44518
Benton DJ, Wharton SA, Martin SR, McCauley JW (2017) Role of neuraminidase in influenza A(H7N9) virus receptor binding. J Virol 91(11):e02293-e2316. https://doi.org/10.1128/JVI.02293-16
doi: 10.1128/JVI.02293-16
pubmed: 28356530
pmcid: 5432883
Zhu W, Zhou J, Li Z, Yang L, Li X, Huang W, Zou S, Chen W, Wei H, Tang J, Liu L, Dong J, Wang D, Shu Y (2017) Biological characterisation of the emerged highly pathogenic avian influenza (HPAI) A(H7N9) viruses in humans, in mainland China, 2016 to 2017. Euro Surveill. https://doi.org/10.2807/1560-7917.ES.2017.22.19.30533
doi: 10.2807/1560-7917.ES.2017.22.19.30533
pubmed: 28537546
pmcid: 5476987
Matrosovich M, Matrosovich T, Carr J, Roberts NA, Klenk H-D (2003) Overexpression of the α-2,6-sialyltransferase in MDCK cells increases influenza virus sensitivity to neuraminidase inhibitors. J Virol 77(15):8418–8425
doi: 10.1128/JVI.77.15.8418-8425.2003
Zhu X, McBride R, Nycholat CM, Wenli Yu, Paulson JC, Wilson IA (2012) Influenza Virus Neuraminidases with Reduced Enzymatic Activity That Avidly Bind Sialic Acid Receptors. J Virol 86(24):13371–13383. https://doi.org/10.1128/JVI.01426-1237
doi: 10.1128/JVI.01426-1237
pubmed: 23015718
pmcid: 3503043
World Health Organization (2015) Production and testing of influenza high growth reassortants. World Health Organization. https://apps.who.int/iris/handle/10665/204453
World Health Organization (2018) Antigenic and genetic characteristics of zoonotic influenza viruses and development of candidate vaccine viruses for pandemic preparedness. https://www.who.int/influenza/vaccines/virus/201809_zoonotic_vaccinevirusupdate.pdf?ua=1 . Accessed 16 Sept 2020
Lamb YN (2019) Cell-based quadrivalent inactivated influenza virus vaccine (Flucelvax® Tetra/Flucelvax Quadrivalent®): a review in the prevention of influenza. Drugs 79(12):1337–1348
doi: 10.1007/s40265-019-01176-z
Manini I, Domnich A, Amicizia D, Rossi S, Pozzi T, Gasparini R, Panatto D, Montomoli E (2015) Flucelvax (Optaflu) for seasonal influenza. Expert Rev Vaccines 14(6):789–804
doi: 10.1586/14760584.2015.1039520
Chambers BS, Li Y, Hodinka RL, Hensley SE (2014) Recent H3N2 influenza virus clinical isolates rapidly acquire hemagglutinin or neuraminidase mutations when propagated for antigenic analyses. J Virol 88(18):10986–10989
doi: 10.1128/JVI.01077-14
Zhang H, Han Q, Ping X, Li L, Chang C, Chen Z, Shu Y, Ke X, Sun B (2015) A single NS2 mutation of K86R promotes PR8 vaccine donor virus growth in Vero cells. Virology 482:32–40
doi: 10.1016/j.virol.2015.03.004
Pratip S, Sameer SC, Sarah SC (2011) Antigenic variability in Neuraminidase protein of influenza A/H3N2 vaccine strains (1968–2009). Bioinformation 7(2):76–81
Nicholas CW, Huibin L, Andrew JT, Douglas CW, Wilson WSN, Rameshwar UK, Chih-Wei L, Corwin MN, Ryan M, Weiwen L, James CP, Chris KPM, Ian AW (2019) Preventing an antigenically disruptive mutation in egg-based H3N2 seasonal influenza vaccines by mutational incompatibility. Cell Host Microbe 25(6):836–844
doi: 10.1016/j.chom.2019.04.013
Jean-Sébastien C, Olivier F, Vanessa E, Maude B, Corinne B, Laetitia L, Thierry E, Martine V, Emilie F, Sylvie P, Bruno P, Bruno L, Michèle O (2014) Functional balance between the hemagglutinin and neuraminidase of influenza A(H1N1)pdm09 HA D222 variants. PLoS One. https://doi.org/10.1371/journal.pone.0104009
doi: 10.1371/journal.pone.0104009
Mathilde R, Alexandra E, Bertrand C, Aurélien T, Mendy B, Alan H, Yi P, Olivier F, Bruno L (2012) Rescue of a H3N2 influenza virus containing a deficient neuraminidase protein by a hemagglutinin with a low receptor-binding affinity. PLoS One. https://doi.org/10.1371/journal.pone.0033880
doi: 10.1371/journal.pone.0033880
Rui X, Xueyong Z, Ryan M, Corwin MN, Wenli Y, James CP, Ian AW (2012) Functional balance of the hemagglutinin and neuraminidase activities accompanies the emergence of the 2009 H1N1 influenza pandemic. J Virol 86(17):9221–9232
doi: 10.1128/JVI.00697-12
Moser C, Müller M, Kaeser MD, Weydemann U, Amacker M (2013) Influenza virosomes as vaccine adjuvant and carrier system. Expert Rev Vaccines 12(7):779–791
doi: 10.1586/14760584.2013.811195
Petsch B, Schnee M, Vogel AB, Lange E, Hoffmann B, Voss D, Schlake T, Thess A, Kallen KJ, Stitz L, Kramps T (2012) Protective efficacy of in vitro synthesized, specific mRNA vaccines against influenza A virus infection. Nat Biotechnol 30(12):1210–1216
doi: 10.1038/nbt.2436
Cox MM, Hashimoto Y (2011) A fast track influenza virus vaccine produced in insect cells. J Invertebr Pathol 107(Suppl):S31–S41
doi: 10.1016/j.jip.2011.05.003