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Immunological Investigations
A Journal of Molecular and Cellular Immunology
Volume 50, 2021 - Issue 7
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Better, Faster, Stronger: mRNA Vaccines Show Promise for Influenza Vaccination in Older Adults

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References

  • Anderson EJ, Rouphael NG, Widge AT, Jackson LA, Roberts PC, Makhene M, Chappell JD, Denison MR, Stevens LJ, Pruijssers AJ, et al. 2020. Safety and immunogenicity of SARS-CoV-2 mRNA-1273 vaccine in older adults. N Engl J Med. 383(25):2427–38.
  • Baden LR, El Sahly HM, Essink B, Kotloff K, Frey S, Novak R, Diemert D, Spector SA, Rouphael N, Creech CB, et al. 2021. Efficacy and safety of the mRNA-1273 SARS-CoV-2 vaccine. N Engl J Med. 384(5):403–16.
  • Bahl K, Senn JJ, Yuzhakov O, Bulychev A, Brito LA, Hassett KJ, Laska ME, Smith M, Almarsson O, Thompson J, et al. 2017. Preclinical and clinical demonstration of immunogenicity by mRNA vaccines against H10N8 and H7N9 influenza viruses. Mol Ther. 25(6):1316–27.
  • Barr IG, Donis RO, Katz JM, McCauley JW, Odagiri T, Trusheim H, Tsai TF, Wentworth DE. 2018. Cell culture-derived influenza vaccines in the severe 2017-2018 epidemic season: a step towards improved influenza vaccine effectiveness. NPJ Vaccines. 3:344.
  • Belongia EA, Simpson MD, King JP, Sundaram ME, Kelley NS, Osterholm MT, McLean HQ. 2016. Variable influenza vaccine effectiveness by subtype: a systematic review and meta-analysis of test-negative design studies. Lancet Infect Dis. 16(8):942–51.
  • Brazzoli M, Magini D, Bonci A, Buccato S, Giovani C, Kratzer R, Zurli V, Mangiavacchi S, Casini D, Brito LM, et al. 2016. Induction of broad-based immunity and protective efficacy by self-amplifying mRNA vaccines encoding influenza virus hemagglutinin. J Virol. 90(1):332–44.
  • Buschmann MD, Carrasco MJ, Alishetty S, Paige M, Alameh MG, Weissman D. 2021. Nanomaterial delivery systems for mRNA vaccines. Vaccines (Basel). 9(1):65.
  • CDC. 2021. Centers for disease control and prevention. COVID-19 Hospitalization and Death by Age.; [accessed 2021 March 3]. https://www.cdc.gov/coronavirus/2019-ncov/covid-data/investigations-discovery/hospitalization-death-by-age.html.
  • Chahal JS, Khan OF, Cooper CL, McPartlan JS, Tsosie JK, Tilley LD, Sidik SM, Lourido S, Langer R, Bavari S, et al. 2016. Dendrimer-RNA nanoparticles generate protective immunity against lethal Ebola, H1N1 influenza, and toxoplasma gondii challenges with a single dose. Proc Natl Acad Sci U S A. 113(29):E4133–42.
  • Chen JR, Liu YM, Tseng YC, Ma C. 2020. Better influenza vaccines: an industry perspective. J Biomed Sci. 27(1):33.
  • Corbett KS, Edwards DK, Leist SR, Abiona OM, Boyoglu-Barnum S, Gillespie RA, Himansu S, Schafer A, Ziwawo CT, DiPiazza AT, et al. 2020. SARS-CoV-2 mRNA vaccine design enabled by prototype pathogen preparedness. Nature. 586(7830):567–71.
  • Cunningham AL, McIntyre P, Subbarao K, Booy R, Levin MJ. 2021. Vaccines for older adults. BMJ (Clinical Research Ed). 372:372n188.
  • Della Cioppa G, Nicolay U, Lindert K, Leroux-Roels G, Clement F, Castellino F, Galli C, Groth N, Levin Y, Del Giudice G. 2014. A dose-ranging study in older adults to compare the safety and immunogenicity profiles of MF59(R)-adjuvanted and non-adjuvanted seasonal influenza vaccines following intradermal and intramuscular administration. Hum Vaccin Immunother. 10(6):1701–10.
  • DiazGranados CA, Dunning AJ, Kimmel M, Kirby D, Treanor J, Collins A, Pollak R, Christoff J, Earl J, Landolfi V, et al. 2014. Efficacy of high-dose versus standard-dose influenza vaccine in older adults. N Engl J Med. 371(7):635–45.
  • Feldman RA, Fuhr R, Smolenov I, Mick Ribeiro A, Panther L, Watson M, Senn JJ, Smith M, Almarsson PHS. 2019. mRNA vaccines against H10N8 and H7N9 influenza viruses of pandemic potential are immunogenic and well tolerated in healthy adults in phase 1 randomized clinical trials. Vaccine. 37(25):3326–34.
  • Fiore AE, Uyeki TM, Broder K, Finelli L, Euler GL, Singleton JA, Iskander JK, Wortley PM, Shay DK, Bresee JS, et al. 2010. Prevention and control of influenza with vaccines: recommendations of the Advisory Committee on Immunization Practices (ACIP), 2010. MMWR Recomm Rep. 59(RR–8):1–62.
  • Fleeton MN, Chen M, Berglund P, Rhodes G, Parker SE, Murphy M, Atkins GJ, Liljestrom P. 2001. Self-replicative RNA vaccines elicit protection against influenza A virus, respiratory syncytial virus, and a tickborne encephalitis virus. J Infect Dis. 183(9):1395–98.
  • Frey SE, Reyes MR, Reynales H, Bermal NN, Nicolay U, Narasimhan V, Forleo-Neto E, Arora AK. 2014. Comparison of the safety and immunogenicity of an MF59(R)-adjuvanted with a non-adjuvanted seasonal influenza vaccine in elderly subjects. Vaccine. 32(39):5027–34.
  • Geall AJ, Verma A, Otten GR, Shaw CA, Hekele A, Banerjee K, Cu Y, Beard CW, Brito LA, Krucker T, et al. 2012. Nonviral delivery of self-amplifying RNA vaccines. Proc Natl Acad Sci U S A. 109(36):14604–09.
  • Goronzy JJ, Weyand CM. 2013. Understanding immunosenescence to improve responses to vaccines. Nat Immunol. 14(5):428–36.
  • Gravenstein S, Davidson HE, Taljaard M, Ogarek J, Gozalo P, Han L, Mor V. 2017. Comparative effectiveness of high-dose versus standard-dose influenza vaccination on numbers of US nursing home residents admitted to hospital: a cluster-randomised trial. Lancet Respir Med. 5(9):738–46.
  • Grohskopf LA, Alyanak E, Broder KR, Blanton LH, Fry AM, Jernigan DB, Atmar RL. 2020. Prevention and control of seasonal influenza with vaccines: recommendations of the advisory committee on immunization practices - United States, 2020-21 influenza season. MMWR Recomm Rep. 69(8):1–24.
  • Haq K, McElhaney JE. 2014. Immunosenescence: influenza vaccination and the elderly. Curr Opin Immunol. 29:38–42.
  • Hekele A, Bertholet S, Archer J, Gibson DG, Palladino G, Brito LA, Otten GR, Brazzoli M, Buccato S, Bonci A, et al. 2013. Rapidly produced SAM((R)) vaccine against H7N9 influenza is immunogenic in mice. Emerg Microbes Infect. 2(8):e52.
  • Heron M. 2013. Deaths: leading causes for 2010. Natl Vital Stat Rep. 62(6):1–96.
  • Iuliano AD, Roguski KM, Chang HH, Muscatello DJ, Palekar R, Tempia S, Cohen C, Gran JM, Schanzer D, Cowling BJ, et al. 2018. Estimates of global seasonal influenza-associated respiratory mortality: a modelling study. Lancet. 391(10127):1285–300.
  • Jackson LA, Anderson EJ, Rouphael NG, Roberts PC, Makhene M, Coler RN, McCullough MP, Chappell JD, Denison MR, Stevens LJ, et al. 2020. An mRNA vaccine against SARS-CoV-2 - preliminary report. N Engl J Med. 383(20):1920–31.
  • Jirikowski GF, Sanna PP, Maciejewski-Lenoir D, Bloom FE. 1992. Reversal of diabetes insipidus in Brattleboro rats: intrahypothalamic injection of vasopressin mRNA. Science. 255(5047):996–98.
  • Kogut I, Scholz JL, Cancro MP, Cambier JC. 2012. B cell maintenance and function in aging. Semin Immunol. 24(5):342–49.
  • Krammer F, Smith GJD, Fouchier RAM, Peiris M, Kedzierska K, Doherty PC, Palese P, Shaw ML, Treanor J, Webster RG, et al. 2018. Influenza. Nat Rev Dis Primers. 4(1):3.
  • Lee JKH, Lam GKL, Shin T, Samson SI, Greenberg DP, Chit A. 2021. Efficacy and effectiveness of high-dose influenza vaccine in older adults by circulating strain and antigenic match: an updated systematic review and meta-analysis. Vaccine. 39:A24–A35.
  • Liang F, Lindgren G, Lin A, Thompson EA, Ols S, Rohss J, John S, Hassett K, Yuzhakov O, Bahl K, et al. 2017. Efficient targeting and activation of antigen-presenting cells in vivo after modified mRNA vaccine administration in rhesus macaques. Mol Ther. 25(12):2635–47.
  • Lindgren G, Ols S, Liang F, Thompson EA, Lin A, Hellgren F, Bahl K, John S, Yuzhakov O, Hassett KJ, et al. 2017. Induction of Robust B cell responses after influenza mRNA vaccination is accompanied by circulating hemagglutinin-specific ICOS+ PD-1+ CXCR3+ T follicular helper cells. Front Immunol. 8:81539.
  • Lutz J, Lazzaro S, Habbeddine M, Schmidt KE, Baumhof P, Mui BL, Tam YK, Madden TD, Hope MJ, Heidenreich R, et al. 2017. Unmodified mRNA in LNPs constitutes a competitive technology for prophylactic vaccines. NPJ Vaccines. 2:229.
  • Magini D, Giovani C, Mangiavacchi S, Maccari S, Cecchi R, Ulmer JB, De Gregorio E, Geall AJ, Brazzoli M, Bertholet S. 2016. Self-amplifying mRNA vaccines expressing multiple conserved influenza antigens confer protection against homologous and heterosubtypic viral challenge. PloS One. 11(8):e0161193.
  • McElhaney JE, Xie D, Hager WD, Barry MB, Wang Y, Kleppinger A, Ewen C, Kane KP, Bleackley RC. 2006. T cell responses are better correlates of vaccine protection in the elderly. J Immunol. 176(10):6333–39.
  • Meurens F. 2020. Flu RNA vaccine: a game changer? Vaccines (Basel). 8:4.
  • Murasko DM, Bernstein ED, Gardner EM, Gross P, Munk G, Dran S, Abrutyn E. 2002. Role of humoral and cell-mediated immunity in protection from influenza disease after immunization of healthy elderly. Exp Gerontol. 37(2–3):427–39.
  • Ng TWY, Cowling BJ, Gao HZ, Thompson MG. 2019. Comparative immunogenicity of enhanced seasonal influenza vaccines in older adults: a systematic review and meta-analysis. J Infect Dis. 219(10):1525–35.
  • Nicolay U, Heijnen E, Nacci P, Patriarca PA, Leav B. 2019. Immunogenicity of aIIV3, MF59-adjuvanted seasonal trivalent influenza vaccine, in older adults >/=65 years of age: meta-analysis of cumulative clinical experience. Int J Infect Dis. 85:SS1–S9.
  • Nikolich-Zugich J. 2018. The twilight of immunity: emerging concepts in aging of the immune system. Nat Immunol. 19(1):10–19.
  • Osterholm MT, Kelley NS, Sommer A, Belongia EA. 2012. Efficacy and effectiveness of influenza vaccines: a systematic review and meta-analysis. Lancet Infect Dis. 12(1):36–44.
  • Pardi N, Hogan MJ, Naradikian MS, Parkhouse K, Cain DW, Jones L, Moody MA, Verkerke HP, Myles A, Willis E, et al. 2018a. Nucleoside-modified mRNA vaccines induce potent T follicular helper and germinal center B cell responses. J Exp Med. 215(6):1571–88.
  • Pardi N, Hogan MJ, Pelc RS, Muramatsu H, Andersen H, DeMaso CR, Dowd KA, Sutherland LL, Scearce RM, Parks R, et al. 2017. Zika virus protection by a single low-dose nucleoside-modified mRNA vaccination. Nature. 543(7644):248–51.
  • Pardi N, Hogan MJ, Porter FW, Weissman D. 2018b. mRNA vaccines - a new era in vaccinology. Nat Rev Drug Discov. 17(4):261–79.
  • Petsch B, Schnee M, Vogel AB, Lange E, Hoffmann B, Voss D, Schlake T, Thess A, Kallen KJ, Stitz L, et al. 2012. Protective efficacy of in vitro synthesized, specific mRNA vaccines against influenza A virus infection. Nat Biotechnol. 30(12):1210–16.
  • Polack FP, Thomas SJ, Kitchin N, Absalon J, Gurtman A, Lockhart S, Perez JL, Perez Marc G, Moreira ED, Zerbini C, et al. 2020. Safety and efficacy of the BNT162b2 mRNA Covid-19 vaccine. N Engl J Med. 383(27):2603–15.
  • Rockman S, Laurie KL, Parkes S, Wheatley A, Barr IG. 2020. New technologies for influenza vaccines. Microorganisms. 8(11):11.
  • Rolfes MA, Flannery B, Chung JR, O’Halloran A, Garg S, Belongia EA, Gaglani M, Zimmerman RK, Jackson ML, Monto AS, et al. 2019. Effects of influenza vaccination in the United States during the 2017-2018 influenza season. Clin Infect Dis. 69(11):1845–53.
  • Sahin U, Muik A, Derhovanessian E, Vogler I, Kranz LM, Vormehr M, Baum A, Pascal K, Quandt J, Maurus D, et al. 2020. COVID-19 vaccine BNT162b1 elicits human antibody and TH1 T cell responses. Nature. 586(7830):594–99.
  • Scorza FB, Pardi N. 2018. New kids on the block: RNA-based influenza virus vaccines. Vaccines (Basel). 6(2):20.
  • Shaw AC, Goldstein DR, Montgomery RR. 2013. Age-dependent dysregulation of innate immunity. Nat Rev Immunol. 13(12):875–87.
  • Solana R, Tarazona R, Gayoso I, Lesur O, Dupuis G, Fulop T. 2012. Innate immunosenescence: effect of aging on cells and receptors of the innate immune system in humans. Semin Immunol. 24(5):331–41.
  • Thompson WW, Shay DK, Weintraub E, Brammer L, Cox N, Anderson LJ, Fukuda K. 2003. Mortality associated with influenza and respiratory syncytial virus in the United States. JAMA. 289(2):179–86.
  • Van Buynder PG, Konrad S, Van Buynder JL, Brodkin E, Krajden M, Ramler G, Bigham M. 2013. The comparative effectiveness of adjuvanted and unadjuvanted trivalent inactivated influenza vaccine (TIV) in the elderly. Vaccine. 31(51):6122–28.
  • Vogel AB, Lambert L, Kinnear E, Busse D, Erbar S, Reuter KC, Wicke L, Perkovic M, Beissert T, Haas H, et al. 2018. Self-amplifying RNA vaccines give equivalent protection against influenza to mRNA vaccines but at much lower doses. Mol Ther. 26(2):446–55.
  • Walsh EE, Frenck RW Jr., Falsey AR, Kitchin N, Absalon J, Gurtman A, Lockhart S, Neuzil K, Mulligan MJ, Bailey R, et al. 2020. Safety and immunogenicity of two RNA-based Covid-19 vaccine candidates. N Engl J Med. 383(25):2439–50.
  • Widge AT, Rouphael NG, Jackson LA, Anderson EJ, Roberts PC, Makhene M, Chappell JD, Denison MR, Stevens LJ, Pruijssers AJ, et al. 2021. Durability of responses after SARS-CoV-2 mRNA-1273 vaccination. N Engl J Med. 384(1):80–82.
  • Wolff JA, Malone RW, Williams P, Chong W, Acsadi G, Jani A, Felgner PL. 1990. Direct gene transfer into mouse muscle in vivo. Science. 247(4949 Pt 1):1465–68.

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