Influenza B virus neuraminidase: a potential target for next-generation vaccines?

References

• Kosik I, Yewdell JW. Influenza a virus hemagglutinin specific antibodies interfere with virion neuraminidase activity via two distinct mechanisms. Virology. 2017;500:178–183. doi: 10.1016/j.virol.2016.10.024
   PubMed Web of Science ®Google Scholar
• Hensen L, Kedzierska K, Koutsakos M. Innate and adaptive immunity toward influenza B viruses. Future Microbiol. 2020;15(11):1045–1058. doi: 10.2217/fmb-2019-0340
   PubMed Web of Science ®Google Scholar
• Koutsakos M, Nguyen TH, Barclay WS, et al. Knowns and unknowns of influenza B viruses. Future Microbiol. 2016;11(1):119–135. doi: 10.2217/fmb.15.120
   PubMed Web of Science ®Google Scholar
• Caini S, Kusznierz G, Garate VV, et al. The epidemiological signature of influenza B virus and its B/Victoria and B/Yamagata lineages in the 21st century. PLoS One. 2019;14(9):e0222381. doi: 10.1371/journal.pone.0222381
   PubMed Web of Science ®Google Scholar
• Barr IG, Vijaykrishna D, Sullivan SG Differential age susceptibility to influenza B/Victoria lineage viruses in the 2015 Australian influenza season. Eurosurveillance. 2016;21(4):30118. doi: 10.2807/1560-7917.ES.2016.21.4.30118
   Web of Science ®Google Scholar
• Paget J, Caini S, Del Riccio M, et al. Has influenza B/Yamagata become extinct and what implications might this have for quadrivalent influenza vaccines? Eurosurveillance. 2022;27(39):2200753. doi: 10.2807/1560-7917.ES.2022.27.39.2200753
   Web of Science ®Google Scholar
• Osterhaus A, Rimmelzwaan G, Martina B, et al. Influenza B virus in seals. Science. 2000;288(5468):1051–1053. doi: 10.1126/science.288.5468.1051
   PubMed Web of Science ®Google Scholar
• Ohishi K, Ninomiya A, Kida H, et al. Serological evidence of transmission of human influenza a and B viruses to Caspian seals (phoca caspica). Microbiol Immunol. 2002;46(9):639–644. doi: 10.1111/j.1348-0421.2002.tb02746.x
   PubMed Web of Science ®Google Scholar
• Ran Z, Shen H, Lang Y, et al. Domestic pigs are susceptible to infection with influenza B viruses. J Virol. 2015;89(9):4818–4826. doi: 10.1128/JVI.00059-15
   PubMed Web of Science ®Google Scholar
• Koutsakos M, Wheatley AK, Laurie K, et al. Influenza lineage extinction during the COVID-19 pandemic? Nature Rev Microbiol. 2021;19(12):741–742. doi: 10.1038/s41579-021-00642-4
   PubMed Web of Science ®Google Scholar
• Dhanasekaran V, Sullivan S, Edwards KM, et al. Human seasonal influenza under COVID-19 and the potential consequences of influenza lineage elimination. Nat Commun. 2022;13(1):1721. doi: 10.1038/s41467-022-29402-5
   PubMed Web of Science ®Google Scholar
• Bedford T, Suchard MA, Lemey P, et al. Integrating influenza antigenic dynamics with molecular evolution. Elife. 2014;3:e01914. doi:10.7554/eLife.01914
   PubMed Web of Science ®Google Scholar
• de Jong JC, Beyer Walter E.P., Palache WE, et al. Mismatch between the 1997/1998 influenza vaccine and the major epidemic a (H3N2) virus strain as the cause of an inadequate vaccine‐induced antibody response to this strain in the elderly. J Med Virol. 2000;61(1):94–99. doi: 10.1002/(SICI)1096-9071(200005)61:1<94:AID-JMV15>3.0.CO;2-C
   PubMed Web of Science ®Google Scholar
• Krammer F, Palese P Advances in the development of influenza virus vaccines. Nat Rev Drug Discov. 2015;14(3):167–182. doi: 10.1038/nrd4529
   PubMed Web of Science ®Google Scholar
• JE S, PC S. Importance of antigenic composition of influenza virus vaccine in protecting against the natural disease; observations during the winter of 1947-1948. Am J Public Health Nations Health. 1949;39(3):345–355. doi: 10.2105/AJPH.39.3.345
   PubMed Web of Science ®Google Scholar
• Payne A-M. The influenza programme of WHO. Bullet World Health Organ. 1953;8(5–6):755.
   PubMedGoogle Scholar
• Hutchinson EC, Charles PD, Hester SS, et al. Conserved and host-specific features of influenza virion architecture. Nat Commun. 2014;5(1):1–11. doi: 10.1038/ncomms5816
   Google Scholar
• Wang Q, Tian X, Chen X, et al. Structural basis for receptor specificity of influenza B virus hemagglutinin. Proceedings of the National Academy of Sciences. 2007;104 (43):p. 16874–16879.
   Google Scholar
• Burmeister W, Ruigrok R, Cusack S The 2.2 a resolution crystal structure of influenza B neuraminidase and its complex with sialic acid. EMBO J. 1992;11(1):49–56. doi: 10.1002/j.1460-2075.1992.tb05026.x
   PubMed Web of Science ®Google Scholar
• Du W, de Vries E, van Kuppeveld FJ, et al. Second sialic acid‐binding site of influenza A virus neuraminidase: binding receptors for efficient release. FEBS J. 2021;288(19):5598–5612. doi: 10.1111/febs.15668
   PubMed Web of Science ®Google Scholar
• Cohen M, Zhang X-Q, Senaati HP, et al. Influenza a penetrates host mucus by cleaving sialic acids with neuraminidase. Virol J. 2013;10(1):1–13. doi: 10.1186/1743-422X-10-321
   PubMedGoogle Scholar
• Rajendran M, Krammer F, McMahon M The human antibody response to the influenza virus neuraminidase following infection or vaccination. Vaccines. 2021;9(8):846. doi: 10.3390/vaccines9080846
   Web of Science ®Google Scholar
• Tao J, Wang H, Wang W, et al. Binding mechanism of oseltamivir and influenza neuraminidase suggests perspectives for the design of new anti-influenza drugs. PLoS Comput Biol. 2022;18(7):e1010343. doi: 10.1371/journal.pcbi.1010343
   PubMed Web of Science ®Google Scholar
• Andrews DM, Cherry PC, Humber DC, et al. Synthesis and influenza virus sialidase inhibitory activity of analogues of 4-guanidino-Neu5Ac2en (zanamivir) modified in the glycerol side-chain. Eur J Med Chem. 1999;34(7–8):563–574. doi: 10.1016/S0223-5234(00)80026-4
   PubMed Web of Science ®Google Scholar
• Sarukhanyan E, Shanmugam TA, Dandekar T. In silico studies reveal peramivir and zanamivir as an optimal drug treatment even if H7N9 avian type influenza virus acquires further resistance. Molecules. 2022;27(18):5920. doi: 10.3390/molecules27185920
   PubMed Web of Science ®Google Scholar
• Caceres CJ, Seibert B, Cargnin Faccin F, et al. Influenza antivirals and animal models. FEBS Open Bio. 2022;12(6):1142–1165. doi: 10.1002/2211-5463.13416
   PubMed Web of Science ®Google Scholar
• Trebbien R, Pedersen SS, Vorborg K, et al. Development of oseltamivir and zanamivir resistance in influenza A (H1N1) pdm09 virus, Denmark, 2014. Eurosurveillance. 2017;22(3):30445. doi: 10.2807/1560-7917.ES.2017.22.3.30445
   Web of Science ®Google Scholar
• Orozovic G, Orozovic K, Järhult JD, Tripp, R., et al. Study of oseltamivir and zanamivir resistance-related mutations in influenza viruses isolated from wild mallards in Sweden. PLoS One. 2014;9(2):e89306. doi: 10.1371/journal.pone.0089306
   PubMed Web of Science ®Google Scholar
• Moscona A Oseltamivir resistance—disabling our influenza defenses. N Engl J Med. 2005;353(25):2633–2636. doi: 10.1056/NEJMp058291
   PubMed Web of Science ®Google Scholar
• Couch RB, Kasel JA, Gerin JL, et al. Induction of partial immunity to influenza by a neuraminidase-specific vaccine. J Infect Dis. 1974;129(4):411–420. doi: 10.1093/infdis/129.4.411
   PubMed Web of Science ®Google Scholar
• Murphy BR, Kasel JA, Chanock RM Association of serum anti-neuraminidase antibody with resistance to influenza in man. N Engl J Med. 1972;286(25):1329–1332. doi: 10.1056/NEJM197206222862502
   PubMed Web of Science ®Google Scholar
• Memoli MJ, Shaw PA, Han A, Moscona, A., et al. Evaluation of antihemagglutinin and antineuraminidase antibodies as correlates of protection in an influenza A/H1N1 virus healthy human challenge model. MBio. 2016;7(2):10.1128/mBio.00417-16. doi: 10.1128/mBio.00417-16
   PubMed Web of Science ®Google Scholar
• Maier HE, Nachbagauer R, Kuan G, et al. Pre-existing antineuraminidase antibodies are associated with shortened duration of influenza a (H1N1) pdm virus shedding and illness in naturally infected adults. Clinl Infect Dis. 2020;70(11):2290–2297. doi: 10.1093/cid/ciz639
   PubMed Web of Science ®Google Scholar
• Couch RB, Atmar RL, Franco LM, et al. Antibody correlates and predictors of immunity to naturally occurring influenza in humans and the importance of antibody to the neuraminidase. J Infect Dis. 2013;207(6):974–981. doi: 10.1093/infdis/jis935
   PubMed Web of Science ®Google Scholar
• Hobson D, Curry R, Beare A, et al. The role of serum haemagglutination-inhibiting antibody in protection against challenge infection with influenza A2 and B viruses. Epidemiol Infect. 1972;70(4):767–777. doi: 10.1017/S0022172400022610
   Google Scholar
• Monto AS, Petrie JG, Cross RT, et al. Antibody to influenza virus neuraminidase: an independent correlate of protection. J Infect Dis. 2015;212(8):1191–1199. doi: 10.1093/infdis/jiv195
   PubMed Web of Science ®Google Scholar
• Johansson BE, Brett IC. Recombinant influenza B virus HA and NA antigens administered in equivalent amounts are immunogenically equivalent and induce equivalent homotypic and broader heterovariant protection in mice than conventional and live influenza vaccines. Hum Vaccines. 2008;4(6):420–424. doi: 10.4161/hv.4.6.6201
   PubMed Web of Science ®Google Scholar
• Wohlbold TJ, Nachbagauer R, Xu H, Griffin, D E., et al. Vaccination with adjuvanted recombinant neuraminidase induces broad heterologous, but not heterosubtypic, cross-protection against influenza virus infection in mice. MBio. 2015;6(2):e02556–14. doi: 10.1128/mBio.02556-14
   PubMed Web of Science ®Google Scholar
• McMahon M, Kirkpatrick E, Stadlbauer D, Schultz-Cherry, S., et al. Mucosal immunity against neuraminidase prevents influenza B virus transmission in Guinea Pigs. MBio. 2019;10(3):e00560–19. doi: 10.1128/mBio.00560-19
   PubMed Web of Science ®Google Scholar
• Kim K-H, Li Z, Bhatnagar N, et al. Universal protection against influenza viruses by multi-subtype neuraminidase and M2 ectodomain virus-like particle. PLOS Pathogens. 2022;18(8):e1010755. doi: 10.1371/journal.ppat.1010755
   PubMedGoogle Scholar
• Wohlbold TJ, Podolsky KA, Chromikova V, et al. Broadly protective murine monoclonal antibodies against influenza B virus target highly conserved neuraminidase epitopes. Nat Microbiol. 2017;2(10):1415–1424. doi: 10.1038/s41564-017-0011-8
   PubMed Web of Science ®Google Scholar
• Madsen A, Dai Y-N, McMahon M, et al. Human antibodies targeting influenza B virus neuraminidase active site are broadly protective. Immunity. 2020;53(4):852–863. e7. doi: 10.1016/j.immuni.2020.08.015
   PubMed Web of Science ®Google Scholar
• Piepenbrink MS, Nogales A, Basu M, Moscona, A., et al. Broad and protective influenza B virus neuraminidase antibodies in humans after vaccination and their clonal persistence as plasma cells. MBio. 2019;10(2):e00066–19. doi: 10.1128/mBio.00066-19
   PubMed Web of Science ®Google Scholar
• Stadlbauer D, Zhu X, McMahon M, et al. Broadly protective human antibodies that target the active site of influenza virus neuraminidase. Science. 2019;366(6464):499–504. doi: 10.1126/science.aay0678
   PubMed Web of Science ®Google Scholar
• Yasuhara A, Yamayoshi S, Kiso M, et al. A broadly protective human monoclonal antibody targeting the sialidase activity of influenza a and B virus neuraminidases. Nat Commun. 2022;13(1):6602. doi: 10.1038/s41467-022-34521-0
   PubMed Web of Science ®Google Scholar
• Momont C, Dang HV, Zatta F, et al. A pan-influenza antibody inhibiting neuraminidase via receptor mimicry. Nature. 2023;1–8.
   Web of Science ®Google Scholar
• Gravel C, Li C, Wang J, et al. Qualitative and quantitative analyses of virtually all subtypes of influenza a and B viral neuraminidases using antibodies targeting the universally conserved sequences. Vaccine. 2010;28(36):5774–5784. doi: 10.1016/j.vaccine.2010.06.075
   PubMed Web of Science ®Google Scholar
• Doyle TM, Li C, Bucher DJ, et al. A monoclonal antibody targeting a highly conserved epitope in influenza B neuraminidase provides protection against drug resistant strains. Biochem Biophys Res Commun. 2013;441(1):226–229. doi: 10.1016/j.bbrc.2013.10.041
   PubMed Web of Science ®Google Scholar
• Curry R, Brown J, Baker F, et al. Serological studies with purified neuraminidase antigens of influenza B viruses. Epidemiol Infect. 1974;72(2):197–204. doi: 10.1017/S0022172400023408
   Google Scholar
• Air GM, Laver WG, Luo M, et al. Antigenic, sequence, and crystal variation in influenza B neuraminidase. Virology. 1990;177(2):578–587. doi: 10.1016/0042-6822(90)90523-T
   PubMed Web of Science ®Google Scholar
• Virk RK, Jayakumar J, Mendenhall IH, et al. Divergent evolutionary trajectories of influenza B viruses underlie their contemporaneous epidemic activity. Proceedings of the National Academy of Sciences. 2020;117 (1):p. 619–628.
   Google Scholar
• Vijaykrishna D, Holmes EC, Joseph U, et al. The contrasting phylodynamics of human influenza B viruses. Elife. 2015;4:e05055. doi: 10.7554/eLife.05055
   PubMed Web of Science ®Google Scholar
• Kilbourne ED, Johansson BE, Grajower B. Independent and disparate evolution in nature of influenza A virus hemagglutinin and neuraminidase glycoproteins. Proceedings of the National Academy of Sciences. 1990;87 (2):p. 786–790.
   Google Scholar
• Sandbulte MR, Westgeest KB, Gao J, et al. Discordant antigenic drift of neuraminidase and hemagglutinin in H1N1 and H3N2 influenza viruses. Proceedings of the National Academy of Sciences. 2011;108 (51):p. 20748–20753.
   Google Scholar
• Laver W, Air G, Webster R, et al. Amino acid sequence changes in antigenic variants of type a influenza virus N2 neuraminidase. Virology. 1982;122(2):450–460. doi: 10.1016/0042-6822(82)90244-6
   PubMed Web of Science ®Google Scholar
• Westgeest KB, de Graaf M, Fourment M, et al. Genetic evolution of the neuraminidase of influenza a (H3N2) viruses from 1968 to 2009 and its correspondence to haemagglutinin evolution. J Gen Virol. 2012;93(Pt 9):1996. doi: 10.1099/vir.0.043059-0
   PubMedGoogle Scholar
• Sultana I, Yang K, Getie-Kebtie M, et al. Stability of neuraminidase in inactivated influenza vaccines. Vaccine. 2014;32(19):2225–2230. doi: 10.1016/j.vaccine.2014.01.078
   PubMed Web of Science ®Google Scholar
• Getie‐Kebtie M, Sultana I, Eichelberger M, et al. Label‐free mass spectrometry‐based quantification of hemagglutinin and neuraminidase in influenza virus preparations and vaccines. Influenza Other Respir Viruses. 2013;7(4):521–530. doi: 10.1111/irv.12001
   PubMed Web of Science ®Google Scholar
• Ito H, Nishimura H, Kisu T, Cao, Y., et al. Low response in eliciting neuraminidase inhibition activity of sera among recipients of a split, monovalent pandemic influenza vaccine during the 2009 pandemic. PLoS One. 2020;15(5):e0233001. doi: 10.1371/journal.pone.0233001
   PubMed Web of Science ®Google Scholar
• Couch RB, Atmar RL, Keitel WA, et al. Randomized comparative study of the serum antihemagglutinin and antineuraminidase antibody responses to six licensed trivalent influenza vaccines. Vaccine. 2012;31(1):190–195. doi: 10.1016/j.vaccine.2012.10.065
   PubMed Web of Science ®Google Scholar
• Johansson BE, Matthews JT, Kilbourne ED. Supplementation of conventional influenza a vaccine with purified viral neuraminidase results in a balanced and broadened immune response. Vaccine. 1998;16(9–10):1009–1015. doi: 10.1016/S0264-410X(97)00279-X
   PubMed Web of Science ®Google Scholar
• Johansson BE, Pokorny BA, Tiso VA Supplementation of conventional trivalent influenza vaccine with purified viral N1 and N2 neuraminidases induces a balanced immune response without antigenic competition. Vaccine. 2002;20(11–12):1670–1674. doi: 10.1016/S0264-410X(01)00490-X
   PubMed Web of Science ®Google Scholar
• Bosch BJ, Bodewes R, de Vries RP, et al. Recombinant soluble, multimeric HA and NA exhibit distinctive types of protection against pandemic swine-origin 2009 a (H1N1) influenza virus infection in ferrets. J Virol. 2010;84(19):10366–10374. doi: 10.1128/JVI.01035-10
   PubMed Web of Science ®Google Scholar
• Schotsaert M, Ysenbaert T, Smet A, et al. Long-lasting cross-protection against influenza A by neuraminidase and M2e-based immunization strategies. Sci Rep. 2016;6(1):24402. doi: 10.1038/srep24402
   PubMedGoogle Scholar
• Liu W-C, Lin C-Y, Tsou Y-T, et al. Cross-reactive neuraminidase-inhibiting antibodies elicited by immunization with recombinant neuraminidase proteins of H5N1 and pandemic H1N1 influenza a viruses. J Virol. 2015;89(14):7224–7234. doi: 10.1128/JVI.00585-15
   PubMed Web of Science ®Google Scholar
• Pardi N, Carreño JM, O’Dell G, et al. Development of a pentavalent broadly protective nucleoside-modified mRNA vaccine against influenza B viruses. Nat Commun. 2022;13(1):4677. doi: 10.1038/s41467-022-32149-8
   PubMed Web of Science ®Google Scholar