1,114
Views
2
CrossRef citations to date
0
Altmetric
Influenza infections

A TLR9 agonist synergistically enhances protective immunity induced by an Alum-adjuvanted H7N9 inactivated whole-virion vaccine

, , , , &
Article: 2249130 | Received 01 Mar 2023, Accepted 13 Aug 2023, Published online: 28 Aug 2023

References

  • Mantel C, Cherian T. New immunization strategies: adapting to global challenges. Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz. 2020 Jan;63(1):25–31.
  • Ye Y, Zhang Q, Wei X, et al. Equitable access to COVID-19 vaccines makes a life-saving difference to all countries. Nat Hum Behav. 2022 Feb;6(2):207–216.
  • Tregoning JS, Flight KE, Higham SL, et al. Progress of the COVID-19 vaccine effort: viruses, vaccines and variants versus efficacy, effectiveness and escape. Nat Rev Immunol. 2021 Oct;21(10):626–636.
  • Nuwarda RF, Alharbi AA, Kayser V. An overview of influenza viruses and vaccines. Vaccines (Basel). 2021 Sep 17;9(9):1032.
  • Tregoning JS, Russell RF, Kinnear E. Adjuvanted influenza vaccines. Hum Vaccin Immunother. 2018 Mar 4;14(3):550–564.
  • Shi J, Zeng X, Cui P, et al. Alarming situation of emerging H5 and H7 avian influenza and effective control strategies. Emerg Microbes Infect. 2023 Dec;12(1):2155072.
  • Yu D, Xiang G, Zhu W, et al. The re-emergence of highly pathogenic avian influenza H7N9 viruses in humans in mainland China, 2019. Euro Surveill. 2019 May;24(21):1900273.
  • Wang J, Su N, Dong Z, et al. The fifth influenza A(H7N9) epidemic: a family cluster of infection in Suzhou city of China, 2016. Int J Infect Dis. 2018 Sep;74:128–135.
  • Zhu W, Zhou J, Li Z, et al. Biological characterisation of the emerged highly pathogenic avian influenza (HPAI) A(H7N9) viruses in humans, in mainland China, 2016 to 2017. Euro Surveill. 2017 May 11;22(19):30533.
  • Mulligan MJ, Bernstein DI, Winokur P, et al. Serological responses to an avian influenza A/H7N9 vaccine mixed at the point-of-Use With MF59 adjuvant. JAMA. 2014 Oct 8;312(14):1409–1419.
  • Wu UI, Hsieh SM, Lee WS, et al. Safety and immunogenicity of an inactivated cell culture-derived H7N9 influenza vaccine in healthy adults: a phase I/II, prospective, randomized, open-label trial. Vaccine. 2017 Jul 24;35(33):4099-4104.
  • Jackson LA, Campbell JD, Frey SE, et al. Effect of varying doses of a monovalent H7N9 influenza vaccine with and without AS03 and MF59 adjuvants on immune response. JAMA. 2015 Jul 21;314(3):237–246.
  • HogenEsch H, O'Hagan DT, Fox CB. Optimizing the utilization of aluminum adjuvants in vaccines: you might just get what you want. NPJ Vaccines. 2018;3:51.
  • Keitel WA, Campbell JD, Treanor JJ, et al. Safety and immunogenicity of an inactivated influenza A/H5N1 vaccine given with or without aluminum hydroxide to healthy adults: results of a phase I-II randomized clinical trial. J Infect Dis. 2008 Nov 1;198(9):1309–1316.
  • Keitel WA, Dekker CL, Mink C, et al. Safety and immunogenicity of inactivated, vero cell culture-derived whole virus influenza A/H5N1 vaccine given alone or with aluminum hydroxide adjuvant in healthy adults. Vaccine. 2009 Nov 5;27(47):6642–6648.
  • Young BE, Sadarangani SP, Leo YS. The avian influenza vaccine Emerflu. Why did it fail?. Why did it Fail? Expert Rev Vaccines. 2015;14(8):1125–1134.
  • Basavaraj VH, Sampath G, Hegde NR, et al. Evaluation of safety and immunogenicity of HNVAC, an MDCK-based H1N1 pandemic influenza vaccine, in Phase I single centre and Phase II/III multi-centre, double-blind, randomized, placebo-controlled, parallel assignment studies. Vaccine. 2014 Jul 31;32(35):4592–4597.
  • Liang XF, Wang HQ, Wang JZ, et al. Safety and immunogenicity of 2009 pandemic influenza A H1N1 vaccines in China: a multicentre, double-blind, randomised, placebo-controlled trial. Lancet. 2010 Jan 2;375(9708):56–66.
  • Bungener L, Geeraedts F, Ter Veer W, et al. Alum boosts TH2-type antibody responses to whole-inactivated virus influenza vaccine in mice but does not confer superior protection. Vaccine. 2008 May 2;26(19):2350–2359.
  • Bresson JL, Perronne C, Launay O, et al. Safety and immunogenicity of an inactivated split-virion influenza A/Vietnam/1194/2004 (H5N1) vaccine: phase I randomised trial. Lancet. 2006 May 20;367(9523):1657–1664.
  • Bernstein DI, Edwards KM, Dekker CL, et al. Effects of adjuvants on the safety and immunogenicity of an avian influenza H5N1 vaccine in adults. J Infect Dis. 2008 Mar 1;197(5):667–675.
  • Gong M, Zhou J, Yang C, et al. Insect cell-expressed hemagglutinin with CpG oligodeoxynucleotides plus alum as an adjuvant is a potential pandemic influenza vaccine candidate. Vaccine. 2012 Dec 14;30(52):7498–7505.
  • Miyaki C, Quintilio W, Miyaji EN, et al. Production of H5N1 (NIBRG-14) inactivated whole virus and split virion influenza vaccines and analysis of immunogenicity in mice using different adjuvant formulations. Vaccine. 2010 Mar 16;28(13):2505–2509.
  • Wack A, Baudner BC, Hilbert AK, et al. Combination adjuvants for the induction of potent, long-lasting antibody and T-cell responses to influenza vaccine in mice. Vaccine. 2008 Jan 24;26(4):552–561.
  • Bode C, Zhao G, Steinhagen F, et al. CpG DNA as a vaccine adjuvant. Expert Rev Vaccines. 2011 Apr;10(4):499-511.
  • Kayraklioglu N, Horuluoglu B, Klinman DM. CpG Oligonucleotides as vaccine adjuvants. Methods Mol Biol. 2021;2197:51–85.
  • Jackson S, Lentino J, Kopp J, et al. Immunogenicity of a two-dose investigational hepatitis B vaccine, HBsAg-1018, using a toll-like receptor 9 agonist adjuvant compared with a licensed hepatitis B vaccine in adults. Vaccine. 2018 Jan 29;36(5):668–674.
  • Moldoveanu Z, Love-Homan L, Huang WQ, et al. CpG DNA, a novel immune enhancer for systemic and mucosal immunization with influenza virus. Vaccine. 1998 Jul;16(11-12):1216–1224.
  • Cooper CL, Davis HL, Morris ML, et al. Safety and immunogenicity of CPG 7909 injection as an adjuvant to Fluarix influenza vaccine. Vaccine. 2004 Aug 13;22(23-24):3136–3143.
  • Aebig JA, Mullen GE, Dobrescu G, et al. Formulation of vaccines containing CpG oligonucleotides and alum. J Immunol Methods. 2007 Jun 30;323(2):139–146.
  • Miura K, Keister DB, Muratova OV, et al. Transmission-blocking activity induced by malaria vaccine candidates Pfs25/Pvs25 is a direct and predictable function of antibody titer. Malar J. 2007 Aug 8;6:107.
  • Davis HL. Novel vaccines and adjuvant systems: the utility of animal models for predicting immunogenicity in humans. Hum Vaccin. 2008 May-Jun;4(3):246–250.
  • Waldock J, Zheng L, Remarque EJ, et al. Assay harmonization and use of biological standards to improve the reproducibility of the Hemagglutination inhibition assay: a FLUCOP collaborative study. mSphere. 2021 Aug 25;6(4):e0056721.
  • Hoffmann E, Stech J, Guan Y, et al. Universal primer set for the full-length amplification of all influenza a viruses. Arch Virol. 2001 Dec;146(12):2275–2289.
  • Zhu Z, Fan H, Qi X, et al. Development and evaluation of a SYBR green-based real time RT-PCR assay for detection of the emerging avian influenza A (H7N9) virus. PLoS One. 2013;8(11):e80028.
  • Huber VC, McKeon RM, Brackin MN, et al. Distinct contributions of vaccine-induced immunoglobulin G1 (IgG1) and IgG2a antibodies to protective immunity against influenza. Clin Vaccine Immunol. 2006 Sep;13(9):981–990.
  • Rubtsova K, Rubtsov AV, van Dyk LF, et al. T-box transcription factor T-bet, a key player in a unique type of B-cell activation essential for effective viral clearance. Proc Natl Acad Sci U S A. 2013 Aug 20;110(34):E3216-24.
  • Bowen WS, Svrivastava AK, Batra L, et al. Current challenges for cancer vaccine adjuvant development. Expert Rev Vaccines. 2018 Mar;17(3):207–215.
  • Mutwiri G, Gerdts V, van Drunen Littel-van den Hurk S, et al. Combination adjuvants: the next generation of adjuvants? Expert Rev Vaccines. 2011 Jan;10(1):95–107.
  • Zhang T, He P, Guo D, et al. Research progress of aluminum phosphate adjuvants and their action mechanisms. Pharmaceutics. 2023 Jun 17;15(6):1756.
  • Hansen B, Sokolovska A, HogenEsch H, et al. Relationship between the strength of antigen adsorption to an aluminum-containing adjuvant and the immune response. Vaccine. 2007 Sep 4;25(36):6618–6624.
  • Capri S, Barbieri M, de Waure C, et al. Cost-effectiveness analysis of different seasonal influenza vaccines in the elderly Italian population. Hum Vaccin Immunother. 2018 Jun 3;14(6):1331–1341.
  • Kohli MA, Maschio M, Cartier S, et al. The cost-effectiveness of vaccination of older adults with an MF59-adjuvanted quadrivalent influenza vaccine compared to other available quadrivalent vaccines in Germany. Vaccines (Basel). 2022 Aug 25;10(9):1386.
  • Hehme N, Engelmann H, Kuenzel W, et al. Immunogenicity of a monovalent, aluminum-adjuvanted influenza whole virus vaccine for pandemic use. Virus Res. 2004 Jul;103(1-2):163–171.
  • Hsieh SM, Liu MC, Chen YH, et al. Safety and immunogenicity of CpG 1018 and aluminium hydroxide-adjuvanted SARS-CoV-2 S-2P protein vaccine MVC-COV1901: interim results of a large-scale, double-blind, randomised, placebo-controlled phase 2 trial in Taiwan. Lancet Respir Med. 2021 Dec;9(12):1396–1406.
  • Kang X, Li Y, Zhao Y, et al. Overcoming aging-associated poor influenza vaccine responses with CpG 1018 adjuvant. Vaccines (Basel). 2022 Nov 10;10(11):1894.
  • Strohmeier S, Amanat F, Campbell JD, et al. A CpG 1018 adjuvanted neuraminidase vaccine provides robust protection from influenza virus challenge in mice. NPJ Vaccines. 2022 Jul 22;7(1):81.
  • Coutelier JP, van der Logt JT, Heessen FW, et al. IgG2a restriction of murine antibodies elicited by viral infections. J Exp Med. 1987 Jan 1;165(1):64–69.
  • Hocart MJ, Mackenzie JS, Stewart GA. The IgG subclass responses induced by wild-type, cold-adapted and purified haemagglutinin from influenza virus A/Queensland/6/72 in CBA/CaH mice. J Gen Virol. 1988 Aug;69 (Pt 8):1873-1882.
  • Wagner A, Garner-Spitzer E, Jasinska J, et al. Age-related differences in humoral and cellular immune responses after primary immunisation: indications for stratified vaccination schedules. Sci Rep. 2018 Jun 29;8(1):9825.
  • Radvak P, Kosikova M, Kuo YC, et al. Highly pathogenic avian influenza A/Guangdong/17SF003/2016 is immunogenic and induces cross-protection against antigenically divergent H7N9 viruses. NPJ Vaccines. 2021 Feb 26;6(1):30.