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A Novel Recombinant Influenza Virus Neuraminidase Vaccine Candidate Stabilized by a Measles Virus Phosphoprotein Tetramerization Domain Provides Robust Protection from Virus Challenge in the Mouse Model.

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Strohmeier S, Amanat F, Zhu X, McMahon M, Deming ME, Pasetti MF, Neuzil KM, Wilson IA, Krammer F
OpenAccess logo mBio 12 e0224121 (2021)
Cited: 24 times
EuropePMC logo PMID: 34809451

Abstract

Current seasonal influenza virus vaccines do not induce robust immune responses to neuraminidase. Several factors, including immunodominance of hemagglutinin over neuraminidase, instability of neuraminidase in vaccine formulations, and variable, nonstandardized amounts of neuraminidase in the vaccines, may contribute to this effect. However, vaccines that induce strong antineuraminidase immune responses would be beneficial, as they are highly protective. Furthermore, antigenic drift is slower for neuraminidase than for hemagglutinin, potentially providing broader coverage. Here, we designed stabilized recombinant versions of neuraminidase by replacing the N-terminal cytoplasmic domain, transmembrane, and extracellular stalk with tetramerization domains from the measles or Sendai virus phosphoprotein or from an Arabidopsis thaliana transcription factor. The measles virus tetramerization domain-based construct, termed N1-MPP, was chosen for further evaluation, as it retained antigenicity, neuraminidase activity, and structural integrity and provided robust protection in vivo against lethal virus challenge in the mouse model. We tested N1-MPP as a standalone vaccine, admixed with seasonal influenza virus vaccines, or given with seasonal influenza virus vaccines but in the other leg of the mouse. Admixture with different formulations of seasonal vaccines led to a weak neuraminidase response, suggesting a dominant effect of hemagglutinin over neuraminidase when administered in the same formulation. However, administration of neuraminidase alone or with seasonal vaccine administered in the alternate leg of the mouse induced robust antibody responses. Thus, this recombinant neuraminidase construct is a promising vaccine antigen that may enhance and broaden protection against seasonal influenza viruses.

Articles - 7s0i mentioned but not cited (2)

  1. A Novel Recombinant Influenza Virus Neuraminidase Vaccine Candidate Stabilized by a Measles Virus Phosphoprotein Tetramerization Domain Provides Robust Protection from Virus Challenge in the Mouse Model. Strohmeier S, Amanat F, Zhu X, McMahon M, Deming ME, Pasetti MF, Neuzil KM, Wilson IA, Krammer F. mBio 12 e0224121 (2021)
  2. Surface-Controlled Sialoside-Based Biosensing of Viral and Bacterial Neuraminidases. Alshanski I, Toraskar S, Gordon-Levitan D, Massetti M, Jain P, Vaccaro L, Kikkeri R, Hurevich M, Yitzchaik S. Langmuir 40 7471-7478 (2024)


Reviews citing this publication (4)

  1. Influenza and Universal Vaccine Research in China. Li J, Zhang Y, Zhang X, Liu L. Viruses 15 116 (2022)
  2. Broadly Protective Neuraminidase-Based Influenza Vaccines and Monoclonal Antibodies: Target Epitopes and Mechanisms of Action. Abbadi N, Mousa JJ. Viruses 15 200 (2023)
  3. Anti-neuraminidase immunity in the combat against influenza. Zhang X, Ross TM. Expert Rev Vaccines 23 474-484 (2024)
  4. Immune response in influenza virus infection and modulation of immune injury by viral neuraminidase. Jiang H, Zhang Z. Virol J 20 193 (2023)

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  1. A pan-influenza antibody inhibiting neuraminidase via receptor mimicry. Momont C, Dang HV, Zatta F, Hauser K, Wang C, di Iulio J, Minola A, Czudnochowski N, De Marco A, Branch K, Donermeyer D, Vyas S, Chen A, Ferri E, Guarino B, Powell AE, Spreafico R, Yim SS, Balce DR, Bartha I, Meury M, Croll TI, Belnap DM, Schmid MA, Schaiff WT, Miller JL, Cameroni E, Telenti A, Virgin HW, Rosen LE, Purcell LA, Lanzavecchia A, Snell G, Corti D, Pizzuto MS. Nature 618 590-597 (2023)
  2. Immunization with matrix-, nucleoprotein and neuraminidase protects against H3N2 influenza challenge in pH1N1 pre-exposed pigs. Vatzia E, Feest K, McNee A, Manjegowda T, Carr BV, Paudyal B, Chrun T, Maze EA, Mccarron A, Morris S, Everett HE, MacLoughlin R, Salguero FJ, Lambe T, Gilbert SC, Tchilian E. NPJ Vaccines 8 19 (2023)
  3. A CpG 1018 adjuvanted neuraminidase vaccine provides robust protection from influenza virus challenge in mice. Strohmeier S, Amanat F, Campbell JD, Traquina P, Coffman RL, Krammer F. NPJ Vaccines 7 81 (2022)
  4. An In Vitro Microneutralization Assay for Influenza Virus Serology. Cuevas F, Kawabata H, Krammer F, Carreño JM. Curr Protoc 2 e465 (2022)
  5. Novel Epitopes of the Influenza Virus N1 Neuraminidase Targeted by Human Monoclonal Antibodies. Kirkpatrick Roubidoux E, Sano K, McMahon M, Carreño JM, Capuano C, Jiang K, Simon V, van Bakel H, Wilson P, Krammer F. J Virol 96 e0033222 (2022)
  6. Prevalence and mechanisms of evolutionary contingency in human influenza H3N2 neuraminidase. Lei R, Tan TJC, Hernandez Garcia A, Wang Y, Diefenbacher M, Teo C, Gopan G, Tavakoli Dargani Z, Teo QW, Graham CS, Brooke CB, Nair SK, Wu NC. Nat Commun 13 6443 (2022)
  7. Immunity induced by vaccination with recombinant influenza B virus neuraminidase protein breaks viral transmission chains in guinea pigs in an exposure intensity-dependent manner. McMahon M, Tan J, O'Dell G, Kirkpatrick Roubidoux E, Strohmeier S, Krammer F. J Virol 97 e0105723 (2023)
  8. Nanoparticle display of neuraminidase elicits enhanced antibody responses and protection against influenza A virus challenge. Pascha MN, Ballegeer M, Roelofs MC, Meuris L, Albulescu IC, van Kuppeveld FJM, Hurdiss DL, Bosch BJ, Zeev-Ben-Mordehai T, Saelens X, de Haan CAM. NPJ Vaccines 9 97 (2024)
  9. A Recombinant Mosaic HAs Influenza Vaccine Elicits Broad-Spectrum Immune Response and Protection of Influenza a Viruses. Liu X, Luo C, Yang Z, Zhao T, Yuan L, Xie Q, Liao Q, Liao X, Wang L, Yuan J, Wu N, Sun C, Yan H, Luo H, Shu Y. Vaccines (Basel) 12 1008 (2024)
  10. Aerosol immunization with influenza matrix, nucleoprotein, or both prevents lung disease in pig. Vatzia E, Paudyal B, Dema B, Carr BV, Sedaghat-Rostami E, Gubbins S, Sharma B, Moorhouse E, Morris S, Ulaszewska M, MacLoughlin R, Salguero FJ, Gilbert SC, Tchilian E. NPJ Vaccines 9 188 (2024)
  11. Capsid virus-like particle display improves recombinant influenza neuraminidase antigen stability and immunogenicity in mice. Kang H, Martinez MR, Aves KL, Okholm AK, Wan H, Chabot S, Malik T, Sander AF, Daniels R. iScience 27 110038 (2024)
  12. CircRNA based multivalent neuraminidase vaccine induces broad protection against influenza viruses in mice. Yue X, Zhong C, Cao R, Liu S, Qin Z, Liu L, Zhai Y, Luo W, Lian Y, Zhang M, Lu H, Wang Y, Xu M, Liu S, Lv K, Sun Y, Zhu X, Mai H, Liao J, Yang J, Deng L, Liu Y, Sun C, Zheng KW, Shu Y, Chen YQ. NPJ Vaccines 9 170 (2024)
  13. Drift and shape-new insights into human immunity against influenza virus neuraminidase. Fox A. mBio 14 e0165423 (2023)
  14. Headless hemagglutinin-containing influenza viral particles direct immune responses toward more conserved epitopes. Hamele CE, Luo Z, Leonard RA, Spurrier MA, Burke KN, Webb SR, Rountree W, Li Z, Heaton BE, Heaton NS. J Virol 98 e0116624 (2024)
  15. Increased efficacy of influenza virus vaccine candidate through display of recombinant neuraminidase on virus like particles. Guzman Ruiz L, Zollner AM, Hoxie I, Arcalis E, Krammer F, Klausberger M, Jungbauer A, Grabherr R. Front Immunol 15 1425842 (2024)
  16. Production of Influenza Virus Glycoproteins Using Insect Cells. Loganathan M, Francis B, Krammer F. Methods Mol Biol 2762 43-70 (2024)
  17. Supplementation of seasonal vaccine with multi-subtype neuraminidase and M2 ectodomain virus-like particle improves protection against homologous and heterologous influenza viruses in aged mice. Raha JR, Kim KH, Bhatnagar N, Liu R, Le CTT, Park BR, Grovenstein P, Pal SS, Ko EJ, Shin CH, Wang BZ, Kang SM. Antiviral Res 225 105877 (2024)
  18. Within-host influenza viral diversity in the pediatric population as a function of age, vaccine, and health status. Sobel Leonard A, Mendoza L, McFarland AG, Marques AD, Everett JK, Moncla L, Bushman FD, Odom John AR, Hensley SE. Virus Evol 10 veae034 (2024)


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