Bivalent vaccines effectively protect mice against influenza A and respiratory syncytial viruses

References

• Obando-Pacheco P, Justicia-Grande AJ, Rivero-Calle I, et al. Respiratory syncytial virus seasonality: a global overview. J Infect Dis. 2018 Apr 11;217(9):1356–1364.
   PubMed Web of Science ®Google Scholar
• Lafond KE, Porter RM, Whaley MJ, et al. Global burden of influenza-associated lower respiratory tract infections and hospitalizations among adults: A systematic review and meta-analysis. PLoS Med. 2021 Mar 1;18(3):e1003550.
   PubMed Web of Science ®Google Scholar
• Bloom-Feshbach K, Alonso WJ, Charu V, et al. Latitudinal variations in seasonal activity of influenza and respiratory syncytial virus (RSV): A global comparative review. PLoS One. 2013;8(2):e54445.
   PubMed Web of Science ®Google Scholar
• Chadha M, Hirve S, Bancej C, et al. Human respiratory syncytial virus and influenza seasonality patterns-early findings from the WHO global respiratory syncytial virus surveillance. Influenza Other Respir Viruses. 2020 Nov;14(6):638–646.
   PubMed Web of Science ®Google Scholar
• Haney J, Vijayakrishnan S, Streetley J, et al. Coinfection by influenza A virus and respiratory syncytial virus produces hybrid virus particles. Nat Microbiol. 2022 Oct 24;7:1879–1890.
   PubMed Web of Science ®Google Scholar
• Zhirnov OP, Ikizler MR, Wright PF. Cleavage of influenza a virus hemagglutinin in human respiratory epithelium is cell associated and sensitive to exogenous antiproteases. J Virol. 2002 Sep;76(17):8682–8689.
   PubMed Web of Science ®Google Scholar
• Bullard BL, Weaver EA. Strategies targeting hemagglutinin as a universal influenza vaccine. Vaccines (Basel). 2021 Mar 13;9(3):257. doi:10.3390/vaccines9030257
   PubMed Web of Science ®Google Scholar
• Lu Y, Welsh JP, Swartz JR. Production and stabilization of the trimeric influenza hemagglutinin stem domain for potentially broadly protective influenza vaccines. Proc Natl Acad Sci U S A. 2014 Jan 7;111(1):125–130.
   PubMed Web of Science ®Google Scholar
• Wohlbold TJ, Nachbagauer R, Margine I, et al. Vaccination with soluble headless hemagglutinin protects mice from challenge with divergent influenza viruses. Vaccine. 2015 Jun 26;33(29):3314–3321.
   PubMed Web of Science ®Google Scholar
• Bommakanti G, Lu X, Citron MP, et al. Design of Escherichia coli-expressed stalk domain immunogens of H1N1 hemagglutinin that protect mice from lethal challenge. J Virol. 2012 Dec;86(24):13434–13444.
   PubMed Web of Science ®Google Scholar
• Bommakanti G, Citron MP, Hepler RW, et al. Design of an HA2-based Escherichia coli expressed influenza immunogen that protects mice from pathogenic challenge. Proc Natl Acad Sci U S A. 2010 Aug 3;107(31):13701–6.
   PubMed Web of Science ®Google Scholar
• Impagliazzo A, Milder F, Kuipers H, et al. A stable trimeric influenza hemagglutinin stem as a broadly protective immunogen. Science. 2015 Sep 18;349(6254):1301–1306.
   PubMed Web of Science ®Google Scholar
• van der Lubbe JEM, Verspuij JWA, Huizingh J, et al. Mini-HA is superior to full length hemagglutinin immunization in inducing stem-specific antibodies and protection against group 1 influenza virus challenges in mice. Front Immunol. 2018 Oct 12;9:2350.
   PubMed Web of Science ®Google Scholar
• Steel J, Lowen AC, Wang TT, et al. Influenza virus vaccine based on the conserved hemagglutinin stalk domain. mBio. 2010 May 18;1(1). doi:10.1128/mBio.00018-10.
   PubMed Web of Science ®Google Scholar
• Mathew NR, Angeletti D. Recombinant influenza vaccines: saviors to overcome immunodominance. Front Immunol. 2020 Jan 10;10:2997.
   PubMed Web of Science ®Google Scholar
• Fan X, Hashem AM, Chen Z, et al. Targeting the HA2 subunit of influenza A virus hemagglutinin via CD40L provides universal protection against diverse subtypes. Mucosal Immunol. 2015 Jan;8(1):211–220.
   PubMed Web of Science ®Google Scholar
• Gravel C, Muralidharan A, Duran A, et al. Synthetic vaccine affords full protection to mice against lethal challenge of influenza B virus of both genetic lineages. iScience. 2021 Oct 21;24(11):103328.
   PubMed Web of Science ®Google Scholar
• Mazur NI, Higgins D, Nunes MC, et al. The respiratory syncytial virus vaccine landscape: lessons from the graveyard and promising candidates. Lancet Infect Dis. 2018 Oct;18(10):e295–e311.
   PubMed Web of Science ®Google Scholar
• Feltes TF, Cabalka AK, Meissner HC, et al. Palivizumab prophylaxis reduces hospitalization due to respiratory syncytial virus in young children with hemodynamically significant congenital heart disease. J Pediatr. 2003 Oct;143(4):532–540.
   PubMed Web of Science ®Google Scholar
• McLellan JS, Ray WC, Peeples ME. Structure and function of respiratory syncytial virus surface glycoproteins. Curr Top Microbiol Immunol. 2013;372:83–104.
   PubMed Web of Science ®Google Scholar
• Krarup A, Truan D, Furmanova-Hollenstein P, et al. A highly stable prefusion RSV F vaccine derived from structural analysis of the fusion mechanism. Nat Commun. 2015 Sep 3;6:8143.
   PubMed Web of Science ®Google Scholar
• Mukhamedova M, Wrapp D, Shen CH, et al. Vaccination with prefusion-stabilized respiratory syncytial virus fusion protein induces genetically and antigenically diverse antibody responses. Immunity. 2021 Apr 13;54(4):769,780.e6.
   PubMed Web of Science ®Google Scholar
• Riffault S, Hagglund S, Guzman E, et al. A single shot pre-fusion-stabilized bovine RSV F vaccine is safe and effective in newborn calves with maternally derived antibodies. Vaccines (Basel). 2020 May 18;8(2):231. doi:10.3390/vaccines8020231
   PubMed Web of Science ®Google Scholar
• van der Fits L, Bolder R, Heemskerk-van der Meer M, et al. Adenovector 26 encoded prefusion conformation stabilized RSV-F protein induces long-lasting Th1-biased immunity in neonatal mice. NPJ Vaccines. 2020 Jun 12;5(1):49,y. eCollection 2020.
   PubMed Web of Science ®Google Scholar
• Eichinger KM, Kosanovich JL, Gidwani SV, et al. Prefusion RSV F immunization elicits Th2-mediated lung pathology in mice when formulated with a Th2 (but not a Th1/Th2-balanced) adjuvant despite complete viral protection. Front Immunol. 2020 Jul 29;11:1673.
   PubMed Web of Science ®Google Scholar
• Chu K, Lee S, Kim M, et al. Virus-like particles coexpressing the PreF and gt antigens of respiratory syncytial virus confer protection in mice. Nanomedicine (Lond). 2022 July 01;17(17):1159–1171.
   PubMed Web of Science ®Google Scholar
• Cherukuri A, Patton K, Gasser RA, et al. Adults 65 years old and older have reduced numbers of functional memory T cells to respiratory syncytial virus fusion protein. Clin Vaccine Immunol. 2013 Feb;20(2):239–247.
   PubMed Web of Science ®Google Scholar
• Shao HY, Lin YW, Yu SL, et al. Immunoprotectivity of HLA-A2 CTL peptides derived from respiratory syncytial virus fusion protein in HLA-A2 transgenic mouse. PLoS One. 2011;6(9):e25500.
   PubMed Web of Science ®Google Scholar
• McDermott DS, Knudson CJ, Varga SM. Determining the breadth of the respiratory syncytial virus-specific T cell response. J Virol. 2014 Mar;88(6):3135–3143.
   PubMed Web of Science ®Google Scholar
• De Baets S, Schepens B, Sedeyn K, et al. Recombinant influenza virus carrying the respiratory syncytial virus (RSV) F85-93 CTL epitope reduces RSV replication in mice. J Virol. 2013 Mar;87(6):3314–3323.
   PubMed Web of Science ®Google Scholar
• Chun S, Li C, Van Domselaar G, et al. Universal antibodies and their applications to the quantitative determination of virtually all subtypes of the influenza A viral hemagglutinins. Vaccine. 2008 Nov 11;26(48):6068–6076.
   PubMed Web of Science ®Google Scholar
• Osborn MJ, Panoskaltsis-Mortari A, McElmurry RT, et al. A picornaviral 2A-like sequence-based tricistronic vector allowing for high-level therapeutic gene expression coupled to a dual-reporter system. Mol Ther. 2005 Sep;12(3):569–574.
   PubMed Web of Science ®Google Scholar
• Muralidharan A, Russell M, Larocque L, et al. Targeting CD40 enhances antibody- and CD8-mediated protection against respiratory syncytial virus infection. Sci Rep. 2018 Nov 9;8(1):16648-z.
   Google Scholar
• World Health Organization. WHO global influenza surveillance network. manual for the laboratory diagnosis and virological surveillance of influenza. World Health Organization. 2011: 252.
   Google Scholar
• Russell MS, Thulasi Raman SN, Gravel C, et al. Single immunization of a vaccine vectored by a novel recombinant vaccinia virus affords effective protection against respiratory syncytial virus infection in cotton rats. Front Immunol. 2021 Sep 17;12:747866.
   PubMed Web of Science ®Google Scholar
• Hashem A, Jaentschke B, Gravel C, et al. Subcutaneous immunization with recombinant adenovirus expressing influenza A nucleoprotein protects mice against lethal viral challenge. Hum Vaccin Immunother. 2012 Apr;8(4):425–430.
   PubMed Web of Science ®Google Scholar
• Renne R, Brix A, Harkema J, et al. Proliferative and nonproliferative lesions of the rat and mouse respiratory tract. Toxicol Pathol. 2009 Dec;37(7 Suppl):5S–73S.
   PubMed Web of Science ®Google Scholar
• Berridge BR, Mowat V, Nagai H, et al. Non-proliferative and proliferative lesions of the cardiovascular system of the rat and mouse. J Toxicol Pathol. 2016;29(3 Suppl):1S–47S.
   PubMed Web of Science ®Google Scholar
• Lu LL, Suscovich TJ, Fortune SM, et al. Beyond binding: antibody effector functions in infectious diseases. Nat Rev Immunol. 2018 Jan;18(1):46–61.
   PubMed Web of Science ®Google Scholar
• van Erp EA, Luytjes W, Ferwerda G, et al. Fc-mediated antibody effector functions during respiratory syncytial virus infection and disease. Front Immunol. 2019 Mar 22;10(548).
   PubMed Web of Science ®Google Scholar
• Collins AM. Igg subclass co-expression brings harmony to the quartet model of murine IgG function. Immunol Cell Biol. 2016 Nov;94(10):949–954.
   PubMed Web of Science ®Google Scholar
• Taylor G. Animal models of respiratory syncytial virus infection. Vaccine. 2017 Jan 11;35(3):469–480.
   PubMed Web of Science ®Google Scholar
• Liu Z, Chen O, Wall JBJ, et al. Systematic comparison of 2A peptides for cloning multi-genes in a polycistronic vector. Sci Rep. 2017 May 19;7(1):2193–2192.
   PubMedGoogle Scholar
• Graves PN, Schulman JL, Young JF, et al. Preparation of influenza virus subviral particles lacking the HA1 subunit of hemagglutinin: unmasking of cross-reactive HA2 determinants. Virology. 1983 Apr 15;126(1):106–116.
   PubMed Web of Science ®Google Scholar
• Swalley SE, Baker BM, Calder LJ, et al. Full-length influenza hemagglutinin HA2 refolds into the trimeric low-pH-induced conformation. Biochemistry. 2004 May 18;43(19):5902–5911.
   PubMed Web of Science ®Google Scholar
• Krammer F, Palese P. Influenza virus hemagglutinin stalk-based antibodies and vaccines. Curr Opin Virol. 2013 Oct;3(5):521–530.
   PubMed Web of Science ®Google Scholar
• DiLillo DJ, Palese P, Wilson PC, et al. Broadly neutralizing anti-influenza antibodies require fc receptor engagement for in vivo protection. J Clin Invest. 2016 Feb;126(2):605–610.
   PubMed Web of Science ®Google Scholar
• DiLillo DJ, Tan GS, Palese P, et al. Broadly neutralizing hemagglutinin stalk-specific antibodies require FcgammaR interactions for protection against influenza virus in vivo. Nat Med. 2014 Feb;20(2):143–151.
   PubMed Web of Science ®Google Scholar
• Kotomina T, Korenkov D, Matyushenko V, et al. Live attenuated influenza vaccine viral vector induces functional cytotoxic T-cell immune response against foreign CD8+ T-cell epitopes inserted into NA and NS1 genes using the 2A self-cleavage site. Hum Vaccin Immunother. 2018;14(12):2964–2970.
   PubMed Web of Science ®Google Scholar
• Widjojoatmodjo MN, Bogaert L, Meek B, et al. Recombinant low-seroprevalent adenoviral vectors Ad26 and Ad35 expressing the respiratory syncytial virus (RSV) fusion protein induce protective immunity against RSV infection in cotton rats. Vaccine. 2015 Oct 5;33(41):5406–5414.
   PubMed Web of Science ®Google Scholar
• Salisch NC, Izquierdo Gil A, Czapska-Casey DN, et al. Adenovectors encoding RSV-F protein induce durable and mucosal immunity in macaques after two intramuscular administrations. NPJ Vaccines. 2019 Dec 20;4:54,4. eCollection 2019.
   PubMed Web of Science ®Google Scholar
• Tang A, Chen Z, Cox KS, et al. A potent broadly neutralizing human RSV antibody targets conserved site IV of the fusion glycoprotein. Nat Commun. 2019 Sep 12;10(1):4153–4151.
   PubMedGoogle Scholar
• Rossey I, McLellan JS, Saelens X, et al. Clinical potential of prefusion RSV F-specific antibodies. Trends Microbiol. 2018 Mar;26(3):209–219.
   PubMed Web of Science ®Google Scholar
• Erman M. Maddipatla M. Moderna working on combination COVID-19 vaccine booster and flu shot. Reuters; 2021. Available from: https://www.reuters.com/business/healthcare-pharmaceuticals/moderna-developing-single-dose-combination-vaccine-covid-19-flu-2021-09-09/.
   Google Scholar
• Fries L, Shinde V, Stoddard JJ, et al. Immunogenicity and safety of a respiratory syncytial virus fusion protein (RSV F) nanoparticle vaccine in older adults. Immun Ageing. 2017 Apr 12;14:8,7. eCollection 2017.
   PubMed Web of Science ®Google Scholar