1,012
Views
0
CrossRef citations to date
0
Altmetric
Review

Inactivated recombinant influenza vaccine: the promising direction for the next generation of influenza vaccine

&
Pages 409-418 | Received 19 Jan 2024, Accepted 18 Mar 2024, Published online: 25 Mar 2024

References

  • Iuliano AD, Roguski KM, Chang HH, et al. Estimates of global seasonal influenza-associated respiratory mortality: a modelling study. Lancet. 2018;391(10127):1285–1300. doi: 10.1016/S0140-6736(17)33293-2
  • Palese P. Orthomyxoviridae. Virology. 2007. 1647–1740.
  • Palese P, Tumpey TM, Garcia-Sastre A. What can we learn from reconstructing the extinct 1918 pandemic influenza virus? Immunity. 2006;24(2):121–124. doi: 10.1016/j.immuni.2006.01.007
  • Krammer F, Smith GJD, Fouchier RAM, et al. Influenza. Nat Rev Dis Primers. 2018 Jun 28;4(1):3. doi: 10.1038/s41572-018-0002-y
  • Ferdinands JM, Thompson MG, Blanton L, et al. Does influenza vaccination attenuate the severity of breakthrough infections? A narrative review and recommendations for further research. Vaccine. 2021;39(28):3678–3695. doi: 10.1016/j.vaccine.2021.05.011
  • Olson SM, Newhams MM, Halasa NB, et al. Vaccine effectiveness against life-threatening influenza illness in US children. Clin Infect Dis. 2022 Aug 25;75(2):230–238. doi: 10.1093/cid/ciab931
  • FDA. Common ingredients in U.S. Licensed vaccines. 2019. Available from: https://www.fda.gov/vaccines-blood-biologics/safety-availability-biologics/common-ingredients-us-licensed-vaccines.
  • Information for the 2023-2024 flu season 2024. 2024 Jan 16 [cited 2024 Feb 25]. Available from: https://www.cdc.gov/flu/season/faq-flu-season-2023-2024.htm
  • Li Y-T, Linster M, Mendenhall IH, et al. Avian influenza viruses in humans: lessons from past outbreaks. Br Med Bull. 2019;132(1):81–95. doi: 10.1093/bmb/ldz036
  • Bolton MJ, Ort JT, McBride R, et al. Antigenic and virological properties of an H3N2 variant that will likely dominate the 2021-2022 northern hemisphere influenza season. medRxiv. 2021:2021.12. 15.21267857.
  • Francis T, Salk JE, Pearson HE, et al. Protective effect of vaccination against induced influenza a 1. J Clin Investig. 1945;24(4):536–546. doi: 10.1172/JCI101633
  • Hannoun C. The evolving history of influenza viruses and influenza vaccines. Expert Rev Vaccines. 2013;12(9):1085–1094.
  • Burnet F. Growth of influenza virus in the allantoic cavity of the chick embryo. Aust J Exp Biol Med Sci. 1941;19(4):291–295. doi: 10.1038/icb.1941.44
  • Beyer W, Palache A, Osterhaus A. Comparison of serology and reactogenicity between influenza subunit vaccines and whole virus or split vaccines. Clin Drug Investig. 1998;15(1):1–12. doi: 10.2165/00044011-199815010-00001
  • Allen JD, Ray S, Ross TM. Split inactivated COBRA vaccine elicits protective antibodies against H1N1 and H3N2 influenza viruses. PLoS One. 2018;13(9):e0204284.
  • Kim YH, Hong KJ, Kim H, et al. Influenza vaccines: Past, present, and future. Rev Med Virol. 2022;32(1):e2243. doi: 10.1002/rmv.2243
  • Midthun KMS. CBER approval letter, influenza virus vaccine, live, intranasal (FluMist). 2003. Available from: https://web.archive.org/web/20070929154324/https://www.fda.gov/cber/approvltr/inflmed061703L.htm
  • Cox MM, Izikson R, Post P, et al. Safety, efficacy, and immunogenicity of flublok in the prevention of seasonal influenza in adults. Ther Adv Vaccines. 2015 Jul;3(4):97–108.
  • Zhao F, Liu L, Xu M, et al. Assessments of different inactivating reagents in formulating transmissible gastroenteritis virus vaccine. Virol J. 2020;17(1):1–9. doi: 10.1186/s12985-020-01433-8
  • Sanders B, Koldijk M, Schuitemaker H. Inactivated viral vaccines. Vaccine analysis: strategies. Principles Control. 2014;45–80.
  • Delrue I, Verzele D, Madder A, et al. Inactivated virus vaccines from chemistry to prophylaxis: merits, risks and challenges. Expert review of vaccines. Expert Rev Vaccines. 2012;11(6):695–719. doi: 10.1586/erv.12.38
  • Perrin P, Morgeaux S. Inactivation of DNA by β-propiolactone. Biologicals. 1995;23(3):207–211. doi: 10.1006/biol.1995.0034
  • Craig A. IARC monographs on the evaluation of carcinogenic risk of chemicals to man. Br J Cancer. 1973;27(2):190. doi: 10.1038/bjc.1973.23
  • Park J, Fong Legaspi SL, Schwartzman LM, et al. An inactivated multivalent influenza a virus vaccine is broadly protective in mice and ferrets. Sci Trans Med. 2022;14(653):eabo2167. doi: 10.1126/scitranslmed.abo2167
  • Španinger E, Bren U. Carcinogenesis of β-propiolactone: a computational study. Chem Res Toxicol. 2020 Mar 16;33(3):769–781.
  • Uittenbogaard JP, Zomer B, Hoogerhout P, et al. Reactions of β-propiolactone with nucleobase analogues, nucleosides, and peptides: implications for the inactivation of viruses. J Biol Chem. 2011;286(42):36198–36214. doi: 10.1074/jbc.M111.279232
  • Herrera-Rodriguez J, Signorazzi A, Holtrop M, et al. Inactivated or damaged? Comparing the effect of inactivation methods on influenza virions to optimize vaccine production. Vaccine. 2019 Mar 14;37(12):1630–1637. doi: 10.1016/j.vaccine.2019.01.086
  • Elveborg S, Monteil VM, Mirazimi A. Methods of inactivation of highly pathogenic viruses for molecular, serology or vaccine development purposes. Pathogens. 2022;11(2):271. doi: 10.3390/pathogens11020271
  • Budimir N, Huckriede A, Meijerhof T, et al. Induction of heterosubtypic cross-protection against influenza by a whole inactivated virus vaccine: the role of viral membrane fusion activity. PLoS One. 2012;7(1):e30898. doi: 10.1371/journal.pone.0030898
  • Gupta D, Parthasarathy H, Sah V, et al. Inactivation of SARS-CoV-2 by β-propiolactone causes aggregation of viral particles and loss of antigenic potential. Virus res. 2021 Nov 01;305:198555.
  • Budowsky E, Friedman E, Zheleznova N, et al. Principles of selective inactivation of viral genome. VI. Inactivation of the infectivity of the influenza virus by the action of β-propiolactone. Vaccine. 1991;9(6):398–402. doi: 10.1016/0264-410X(91)90125-P
  • Pawar SD, Murtadak VB, Kale SD, et al. Evaluation of different inactivation methods for high and low pathogenic avian influenza viruses in egg-fluids for antigen preparation. J Virol Methods. 2015;222:28–33. doi: 10.1016/j.jviromet.2015.05.004
  • Chen J-R, Liu Y-M, Tseng Y-C, et al. Better influenza vaccines: an industry perspective. J Biomed Sci. 2020;27(1):1–11. doi: 10.1186/s12929-020-0626-6
  • Parkman PD, Hopps HE, Rastogi SC, et al. Summary of clinical trials of influenza virus vaccines in adults. J Infect Dis. 1977;136(Supplement_3):S722–S730. doi: 10.1093/infdis/136.Supplement_3.S722
  • Huang X, Fan T, Li L, et al. Safety and immunogenicity of a quadrivalent, inactivated, split-virion influenza vaccine (IIV4-W) in healthy people aged 3-60 years: a phase III randomized clinical noninferiority trial. Human Vaccines Immunother. 2022;18(5):2079924. doi: 10.1080/21645515.2022.2079924
  • Soema PC, Kompier R, Amorij J-P, et al. Current and next generation influenza vaccines: formulation and production strategies. Eur J Pharm Biopharm. 2015;94:251–263. doi: 10.1016/j.ejpb.2015.05.023
  • Hampson AW. Vaccines for pandemic influenza. The history of our current vaccines, their limitations and the requirements to deal with a pandemic threat. Ann Acad Med Singapore. 2008;37(6):510. doi: 10.47102/annals-acadmedsg.V37N6p510
  • Lupulescu E, Ioniţă E, Botez D, et al. An immunogenicity and reactogenicity study of a purified, inactivated trivalent influenza vaccine for parenteral administration prepared for the 1996-1997 season. Bacteriol Virusol Parazitol Epidemiol (Bucharest, Romania: 1990). 1997;42(1–2):110–112.
  • Kon TC, Onu A, Berbecila L, et al. Influenza vaccine manufacturing: effect of inactivation, splitting and site of manufacturing. Comparison of influenza vaccine production processes. PLoS One. 2016;11(3):e0150700–e0150700. doi: 10.1371/journal.pone.0150700
  • Robertson CA, Mercer M, Selmani A, et al. Safety and immunogenicity of a full-dose, split-virion, inactivated, quadrivalent influenza vaccine in healthy children 6-35 months of age: a randomized controlled clinical trial. Pediatr Infect Dis J. 2019 Mar;38(3):323–328.
  • Sarsenbayeva G, Issagulov T, Kassenov M, et al. Safety and immunogenicity of trivalent inactivated influenza vaccine in adults 60 years of age and older: a phase II, a randomized, comparative trial in Kazakhstan. Human Vaccines Immunother. 2020;16(8):1791–1797. doi: 10.1080/21645515.2019.1705691
  • Shingai M, Nomura N, Sekiya T, et al. Potent priming by inactivated whole influenza virus particle vaccines is linked to viral RNA uptake into antigen presenting cells. Vaccine. 2021;39(29):3940–3951. doi: 10.1016/j.vaccine.2021.05.065
  • Geeraedts F, Bungener L, Pool J, et al. Whole inactivated virus influenza vaccine is superior to subunit vaccine in inducing immune responses and secretion of proinflammatory cytokines by DCs. Influenza and other respiratory viruses. Influenza Other Respir Viruses. 2008;2(2):41–51. doi: 10.1111/j.1750-2659.2008.00038.x
  • O’Gorman WE, Huang H, Wei Y-L, et al. The split virus influenza vaccine rapidly activates immune cells through Fcγ receptors. Vaccine. 2014 Oct 14;32(45):5989–5997. doi: 10.1016/j.vaccine.2014.07.115
  • Handabile C, Sekiya T, Nomura N, et al. Inactivated whole virus particle influenza vaccine induces anti-neuraminidase antibodies that May contribute to cross-protection against heterologous virus infection. Vaccines. 2022;10(5):804. doi: 10.3390/vaccines10050804
  • Ni Y, Guo J, Turner D, et al. An improved inactivated influenza vaccine with enhanced cross protection. Front Immunol. 2018;9:1815. doi: 10.3389/fimmu.2018.01815
  • Rajaram S, Boikos C, Gelone DK, et al. Influenza vaccines: the potential benefits of cell-culture isolation and manufacturing. Therapeutic advances in vaccines and immunotherapy. Ther Adv Vaccines Immunother. 2020;8:2515135520908121. doi: 10.1177/2515135520908121
  • Merten O-W, Hannoun C, Manuguerra J-C, et al. Production of influenza virus in cell cultures for vaccine preparation. Novel Strat The Design Prod Vac. 1996;141–151.
  • Lamb YN. Cell-based quadrivalent inactivated influenza virus vaccine (Flucelvax® Tetra/Flucelvax Quadrivalent®): a review in the prevention of influenza. Drugs. 2019;79(12):1337–1348. doi: 10.1007/s40265-019-01176-z
  • Yu ED, Grifoni A, Sutherland A, et al. Balanced cellular and humoral immune responses targeting multiple antigens in adults receiving a quadrivalent inactivated influenza vaccine. Vaccines. 2021;9(5):426. doi: 10.3390/vaccines9050426
  • Garcia-Sastre A, Palese P. Genetic manipulation of negative-strand RNA virus genomes. Annu Rev Microbiol. 1993;47(1):765–790. doi: 10.1146/annurev.mi.47.100193.004001
  • Neumann G, Watanabe T, Ito H, et al. Generation of influenza a viruses entirely from cloned cDnas. Proc Nat Acad Sci. 1999;96(16):9345–9350. doi: 10.1073/pnas.96.16.9345
  • Hoffmann E, Neumann G, Kawaoka Y, et al. A DNA transfection system for generation of influenza a virus from eight plasmids. Proc Nat Acad Sci. 2000;97(11):6108–6113. doi: 10.1073/pnas.100133697
  • Krammer F. The human antibody response to influenza a virus infection and vaccination. Nat Rev Immunol. 2019;19(6):383–397. doi: 10.1038/s41577-019-0143-6
  • Kirkpatrick E, Qiu X, Wilson PC, et al. The influenza virus hemagglutinin head evolves faster than the stalk domain. Sci Rep. 2018;8(1):1–14. doi: 10.1038/s41598-018-28706-1
  • Krammer F, Palese P. Influenza virus hemagglutinin stalk-based antibodies and vaccines. Curr Opin Virol. 2013;3(5):521–530. doi: 10.1016/j.coviro.2013.07.007
  • Gomez Lorenzo MM, Fenton MJ. Immunobiology of Influenza Vaccines. Chest. 2013 Feb 01;143(2):502–510.
  • Thornlow DN, Macintyre AN, Oguin TH 3rd, et al. Altering the immunogenicity of hemagglutinin immunogens by hyperglycosylation and disulfide stabilization. Front Immunol. 2021;12:737973. doi: 10.3389/fimmu.2021.737973
  • Lin S-C, Liu W-C, Jan J-T, et al. Glycan masking of hemagglutinin for adenovirus vector and recombinant protein immunizations elicits broadly neutralizing antibodies against H5N1 avian influenza viruses. PLoS One. 2014;9(3):e92822. doi: 10.1371/journal.pone.0092822
  • Impagliazzo A, Milder F, Kuipers H, et al. A stable trimeric influenza hemagglutinin stem as a broadly protective immunogen. Science. 2015;349(6254):1301–1306. doi: 10.1126/science.aac7263
  • Darricarrère N, Qiu Y, Kanekiyo M, et al. Broad neutralization of H1 and H3 viruses by adjuvanted influenza HA stem vaccines in nonhuman primates. Sci, trans med. 2021;13(583):eabe5449. doi: 10.1126/scitranslmed.abe5449
  • Krammer F, Pica N, Hai R, et al. Chimeric hemagglutinin influenza virus vaccine constructs elicit broadly protective stalk-specific antibodies. J Virol. 2013;87(12):6542–6550. doi: 10.1128/JVI.00641-13
  • Sun W, Kirkpatrick E, Ermler M, et al. Development of influenza B universal vaccine candidates using the “mosaic” hemagglutinin approach. J Virol. 2019;93(12): doi: 10.1128/JVI.00333-19
  • Schneemann A, Speir JA, Tan GS, et al. A virus-like particle that elicits cross-reactive antibodies to the conserved stem of influenza virus hemagglutinin. J Virol. 2012;86(21):11686–11697. doi: 10.1128/JVI.01694-12
  • Liu X, Zhao T, Wang L, et al. A mosaic influenza virus-like particles vaccine provides broad humoral and cellular immune responses against influenza A viruses. NPJ Vaccin. 2023;8(1):132. doi: 10.1038/s41541-023-00728-5
  • Liao H-Y, Wang S-C, Ko Y-A, et al. Chimeric hemagglutinin vaccine elicits broadly protective CD4 and CD8 T cell responses against multiple influenza strains and subtypes. Proc Nat Acad Sci. 2020;117(30):17757–17763. doi: 10.1073/pnas.2004783117
  • Liu Y, Strohmeier S, González-Domínguez I, et al. Mosaic hemagglutinin-based whole inactivated virus vaccines induce broad protection against influenza B virus challenge in mice [original research]. Front Immunol. 2021 Sep 16;12:12.
  • Choi A, Bouzya B, Cortés Franco K-D, et al. Chimeric hemagglutinin-based influenza virus vaccines induce protective stalk-specific humoral immunity and cellular responses in mice. Immunohorizons. 2019;3(4):133–148. doi: 10.4049/immunohorizons.1900022
  • Nachbagauer R, Feser J, Naficy A, et al. A chimeric hemagglutinin-based universal influenza virus vaccine approach induces broad and long-lasting immunity in a randomized, placebo-controlled phase I trial. Nature Med. 2021 Jan 01;27(1):106–114. doi: 10.1038/s41591-020-1118-7
  • Andrews SF, Huang Y, Kaur K, et al. Immune history profoundly affects broadly protective B cell responses to influenza. Sci Transl Med. 2015 Dec 2;7(316):316ra192. doi: 10.1126/scitranslmed.aad0522
  • Chen M-W, Cheng T-J, Huang Y, et al. A consensus–hemagglutinin-based DNA vaccine that protects mice against divergent H5N1 influenza viruses. Proc Natl Acad Sci USA. 2008;105(36):13538–13543. doi: 10.1073/pnas.0806901105
  • Webby RJ, Weaver EA, Miyaji EN. Centralized consensus hemagglutinin genes induce protective immunity against H1, H3 and H5 influenza viruses. PLoS One. 2015;10(10):e0140702.
  • Petro-Turnquist EM, Bullard BL, Pekarek MJ, et al. Adenoviral-vectored centralized consensus hemagglutinin vaccine provides broad protection against H2 influenza a virus. Vaccines. 2022;10(6):926. doi: 10.3390/vaccines10060926
  • Huang Y, França MS, Allen JD, et al. Next generation of computationally optimized broadly reactive HA vaccines elicited cross-reactive immune responses and provided protection against H1N1 virus infection. Vaccines. 2021;9(7):793. doi: 10.3390/vaccines9070793
  • Allen JD. Design and characterization of computationally optimized broadly reactive antigen (cobra) vaccines against human seasonal influenza a (H3N2). Viruses: University of Georgia; 2021.
  • Yu J, Sreenivasan C, Sheng Z, et al. A recombinant chimeric influenza virus vaccine expressing the consensus H3 hemagglutinin elicits broad hemagglutination inhibition antibodies against divergent swine H3N2 influenza viruses. Vaccine. 2023;41(42):6318–6326. doi: 10.1016/j.vaccine.2023.09.007
  • Krammer F, Fouchier RA, Eichelberger MC, et al. Naction! How can neuraminidase-based immunity contribute to better influenza virus vaccines? MBio. 2018;9(2):10–1128. doi: 10.1128/mBio.02332-17
  • Essink B, Fierro C, Rosen J, et al. Immunogenicity and safety of MF59-adjuvanted quadrivalent influenza vaccine versus standard and alternate B strain MF59-adjuvanted trivalent influenza vaccines in older adults. Vaccine. 2020;38(2):242–250. doi: 10.1016/j.vaccine.2019.10.021
  • Coleman BL, Sanderson R, Haag MD, et al. Effectiveness of the MF59‐adjuvanted trivalent or quadrivalent seasonal influenza vaccine among adults 65 years of age or older, a systematic review and meta‐analysis. Influenza Resp Viruses. 2021;15(6):813–823. doi: 10.1111/irv.12871
  • Zhu W, Dong C, Wei L, et al. Promising adjuvants and platforms for influenza vaccine development. Pharmaceutics. 2021;13(1):68. doi: 10.3390/pharmaceutics13010068
  • Cole SL, Cybulski VA, Whitacre M, et al. Influenza vaccines using liposomal formulations of toll-like receptor (TLR) 7/8 and 4 agonists as adjuvants. J Immunol. 2020;204(1_Supplement):.245.12–.245.12. doi: 10.4049/jimmunol.204.Supp.245.12
  • Kaushik D, Dhingra S, Patil MT, et al. BBIQ, a pure TLR7 agonist, is an effective influenza vaccine adjuvant. Human Vaccines Immunother. 2020;16(8):1989–1996. doi: 10.1080/21645515.2019.1710409
  • Goff PH, Hayashi T, Martínez-Gil L, et al. Synthetic toll-like receptor 4 (TLR4) and TLR7 ligands as influenza virus vaccine adjuvants induce rapid, sustained, and broadly protective responses. J Virol. 2015;89(6):3221–3235. doi: 10.1128/JVI.03337-14
  • Moriyama M, Koshiba T, Ichinohe T. Influenza A virus M2 protein triggers mitochondrial DNA-mediated antiviral immune responses. Nat Commun. 2019;10(1):4624. doi: 10.1038/s41467-019-12632-5
  • Ritchie C, Li L. cGAMP as an adjuvant in antiviral vaccines and cancer immunotherapy. Biochemistry. 2020;59(18):1713–1715. doi: 10.1021/acs.biochem.0c00226
  • Vassilieva EV, Taylor DW, Compans RW. Combination of STING pathway agonist with saponin is an effective adjuvant in immunosenescent mice. Front Immunol. 2019;10:3006. doi: 10.3389/fimmu.2019.03006
  • Isakova-Sivak I, Stepanova E, Mezhenskaya D, et al. Influenza vaccine: Progress in a vaccine that elicits a broad immune response. Expert Rev Vaccines. 2021;20(9):1097–1112. doi: 10.1080/14760584.2021.1964961
  • Nguyen AT, Lau HMP, Sloane H, et al. Homologous peptides derived from influenza A, B and C viruses induce variable CD8 + T cell responses with cross-reactive potential. Clin Trans Imm. 2022;11(10):e1422. doi: 10.1002/cti2.1422
  • Wood LV, Gandhapudi SK, Sundarapandiyan K, et al. R-DOTAP (versamune): a novel enantiospecific cationic lipid nanoparticle that induces CD4 and CD8 cellular immune responses to whole protein and tumor-specific peptide antigens. Am Soc Clin Oncol. 2020;38(15_suppl):e15211–e15211. doi: 10.1200/JCO.2020.38.15_suppl.e15211
  • Gandhapudi SK, Shi H, Ward MR, et al. Recombinant protein vaccines formulated with enantio-specific cationic lipid R-DOTAP induce protective cellular and antibody-mediated immune responses in mice. Viruses. 2023;15(2):432. doi: 10.3390/v15020432
  • Flu. The history of influenza 2023. Available from: https://www.flu.com/Articles/2022/The-History-of-Influenza