Immunology and efficacy of MF59-adjuvanted vaccines

References

• O’Hagan DT, Ott GS, De Gregorio E, Seubert A. 2012. The mechanism of action of MF59 - an innately attractive adjuvant formulation. Vaccine. 30:4341–4348. doi:10.1016/j.vaccine.2011.09.061.
   PubMed Web of Science ®Google Scholar
• O’Hagan DT, Ott GS, Nest GV, Rappuoli R, Giudice GD. 2013. The history of MF59((R)) adjuvant: a phoenix that arose from the ashes. Expert Rev Vaccines. 12:13–30. doi:10.1586/erv.12.140.
   PubMed Web of Science ®Google Scholar
• O’Hagan DT, Friedland LR, Hanon E, Didierlaurent AM. 2017. Towards an evidence based approach for the development of adjuvanted vaccines. Curr Opin Immunol. 47:93–102. doi:10.1016/j.coi.2017.07.010.
   PubMed Web of Science ®Google Scholar
• Galli G, Hancock K, Hoschler K, DeVos J, Praus M, Bardelli M, Malzone C, Castellino F, Gentile C, McNally T, et al. Fast rise of broadly cross-reactive antibodies after boosting long-lived human memory B cells primed by an MF59 adjuvanted prepandemic vaccine. Proc Natl Acad Sci U S A. 2009;106:7962–7967. doi:10.1073/pnas.0903181106.
   PubMed Web of Science ®Google Scholar
• O’Hagan DT, Rappuoli R, De Gregorio E, Tsai T, Del Giudice G. 2011. MF59 adjuvant: the best insurance against influenza strain diversity. Expert Rev Vaccines. 10:447–462. doi:10.1586/erv.11.23.
   PubMed Web of Science ®Google Scholar
• Dupuis M, McDonald DM, Ott G. Distribution of adjuvant MF59 and antigen gD2 after intramuscular injection in mice. Vaccine. 18;1999:434–439.
   PubMed Web of Science ®Google Scholar
• Dupuis M, Denis-Mize K, LaBarbara A, Peters W, Charo IF, McDonald DM, Ott G. Immunization with the adjuvant MF59 induces macrophage trafficking and apoptosis. Eur J Immunol. 2001;31:2910–2918. doi:10.1002/1521-4141(2001010)31:10<2910::AID-IMMU2910>3.0.CO;2-3.
   PubMed Web of Science ®Google Scholar
• Hui G, Hashimoto C. 2007. The requirement of CD80, CD86, and ICAM-1 on the ability of adjuvant formulations to potentiate antibody responses to a Plasmodium falciparum blood-stage vaccine. Vaccine. 25:8549–8556. doi:10.1016/j.vaccine.2007.10.010.
   PubMed Web of Science ®Google Scholar
• Seubert A, Monaci E, Pizza M, O’Hagan DT, Wack A. The adjuvants aluminum hydroxide and MF59 induce monocyte and granulocyte chemoattractants and enhance monocyte differentiation toward dendritic cells. J Immunol. 180;2008:5402–5412.
   PubMed Web of Science ®Google Scholar
• Calabro S, Tortoli M, Baudner BC, Pacitto A, Cortese M, O’Hagan DT, De Gregorio E, Seubert A, Wack A. Vaccine adjuvants alum and MF59 induce rapid recruitment of neutrophils and monocytes that participate in antigen transport to draining lymph nodes. Vaccine. 2011;29:1812–1823. doi:10.1016/j.vaccine.2010.12.090.
   PubMed Web of Science ®Google Scholar
• Cioncada R, Maddaluno M, Vo HTM, Woodruff M, Tavarini S, Sammicheli C, Tortoli M, Pezzicoli A, De Gregorio E, Carroll MC, et al. Vaccine adjuvant MF59 promotes the intranodal differentiation of antigen-loaded and activated monocyte-derived dendritic cells. PLoS One. 2017;12:e0185843. doi:10.1371/journal.pone.0185843.
   PubMed Web of Science ®Google Scholar
• Mastelic Gavillet B, Eberhardt CS, Auderset F, Castellino F, Seubert A, Tregoning JS, Lambert PH, de Gregorio E, Del Giudice G, Siegrist CA. MF59 Mediates Its B Cell Adjuvanticity by Promoting T Follicular Helper Cells and Thus Germinal Center Responses in Adult and Early Life. J Immunol. 2015;194:4836–4845. doi:10.4049/jimmunol.1402071.
   PubMed Web of Science ®Google Scholar
• Ko EJ, Lee YT, Kim KH, Jung YJ, Lee Y, Denning TL, Kang SM. Effects of MF59 Adjuvant on Induction of Isotype-Switched IgG Antibodies and Protection after Immunization with T-Dependent Influenza Virus Vaccine in the Absence of CD4+ T Cells. J Virol. 2016;90:6976–6988. doi:10.1128/JVI.00339-16.
   PubMed Web of Science ®Google Scholar
• Kamath AT, Mastelic B, Christensen D, Rochat AF, Agger EM, Pinschewer DD, Andersen P, Lambert PH, Siegrist CA. Synchronization of dendritic cell activation and antigen exposure is required for the induction of Th1/Th17 responses. J Immunology. 2012;188:4828–4837. doi:10.4049/jimmunol.1103183.
   PubMed Web of Science ®Google Scholar
• McKee AS, MacLeod MK, Kappler JW, Marrack P. 2010. Immune mechanisms of protection: can adjuvants rise to the challenge?. BMC Biol. 8:37. doi:10.1186/1741-7007-8-37.
   PubMed Web of Science ®Google Scholar
• Dubois Cauwelaert N, Desbien AL, Hudson TE, Pine SO, Reed SG, Coler RN, Orr MT. The TLR4 Agonist Vaccine Adjuvant, GLA-SE, Requires Canonical and Atypical Mechanisms of Action for TH1 Induction. PLoS One. 2016;11:e0146372. doi:10.1371/journal.pone.0146372.
   PubMed Web of Science ®Google Scholar
• Pulendran B. Immune activation: death, danger and dendritic cells. Curr Biol. 14;2004:R30–2.
   PubMed Web of Science ®Google Scholar
• Seubert A, Calabro S, Santini L, Galli B, Genovese A, Valentini S, Aprea S, Colaprico A, D'Oro U, Giuliani MM, et al. Adjuvanticity of the oil-in-water emulsion MF59 is independent of Nlrp3 inflammasome but requires the adaptor protein MyD88. Proc Natl Acad Sci U S A. 2011;108:11169–11174. doi:10.1073/pnas.1107941108.
   PubMed Web of Science ®Google Scholar
• Hui GS, Hashimoto CN. 2008. Adjuvant formulations possess differing efficacy in the potentiation of antibody and cell mediated responses to a human malaria vaccine under selective immune genes knockout environment. Int Immunopharmacol. 8:1012–1022. doi:10.1016/j.intimp.2008.03.005.
   PubMed Web of Science ®Google Scholar
• Ellebedy AH, Lupfer C, Ghoneim HE, DeBeauchamp J, Kanneganti TD, Webby RJ. 2011. Inflammasome-independent role of the apoptosis-associated speck-like protein containing CARD (ASC) in the adjuvant effect of MF59. Proc Natl Acad Sci U S A. 108:2927–2932. doi:10.1073/pnas.1012455108.
   PubMed Web of Science ®Google Scholar
• Wilkinson TM, Li CK, Chui CS, Huang AK, Perkins M, Liebner JC, Lambkin-Williams R, Gilbert A, Oxford J, Nicholas B et al. Preexisting influenza-specific CD4+ T cells correlate with disease protection against influenza challenge in humans. Nat Med. 2012;18:274–280. doi:10.1038/nm.2612.
   PubMed Web of Science ®Google Scholar
• Caproni E, Tritto E, Cortese M, Muzzi A, Mosca F, Monaci E, Baudner B, Seubert A, De Gregorio E. MF59 and Pam3CSK4 boost adaptive responses to influenza subunit vaccine through an IFN type I-independent mechanism of action. J Immunol. 2012;188:3088–3098. doi:10.4049/jimmunol.1101764.
   PubMed Web of Science ®Google Scholar
• Knudsen NP, Olsen A, Buonsanti C, Follmann F, Zhang Y, Coler RN, Fox CB, Meinke A, D'Oro U, Casini D, et al. Different human vaccine adjuvants promote distinct antigen-independent immunological signatures tailored to different pathogens. Sci Rep. 2016;6:19570. doi:10.1038/srep19570.
   PubMed Web of Science ®Google Scholar
• Singh M, Ugozzoli M, Kazzaz J, Chesko J, Soenawan E, Mannucci D, Titta F, Contorni M, Volpini G, Del Guidice GA et al. A preliminary evaluation of alternative adjuvants to alum using a range of established and new generation vaccine antigens. Vaccine. 2006;24:1680–1686. doi:10.1016/j.vaccine.2005.09.046.
   PubMed Web of Science ®Google Scholar
• Bernstein DI, Edwards KM, Dekker CL, Belshe R, Talbot HK, Graham IL, Noah DL, He F, Hill H. Effects of adjuvants on the safety and immunogenicity of an avian influenza H5N1 vaccine in adults. J Infect Dis. 2008;197:667–675. doi:10.1086/527489.
   PubMed Web of Science ®Google Scholar
• Didierlaurent AM, Morel S, Lockman L, Giannini SL, Bisteau M, Carlsen H, Kielland A, Vosters O, Vanderheyde N, Schiavetti F, et al. AS04, an aluminum salt- and TLR4 agonist-based adjuvant system, induces a transient localized innate immune response leading to enhanced adaptive immunity. J Immunol. 2009;183:6186–6197. doi:10.4049/jimmunol.0901474.
   PubMed Web of Science ®Google Scholar
• Ko EJ, Lee YT, Kim KH, Lee Y, Jung YJ, Kim MC, Lee YN, Kang T, Kang SM. Roles of Aluminum Hydroxide and Monophosphoryl Lipid A Adjuvants in Overcoming CD4+ T Cell Deficiency To Induce Isotype-Switched IgG Antibody Responses and Protection by T-Dependent Influenza Vaccine. J Immunol. 2017;198:279–291. doi:10.4049/jimmunol.1600173.
   PubMed Web of Science ®Google Scholar
• Belshe RB, Frey SE, Graham IL, Anderson EL, Jackson LA, Spearman P, Edupuganti S, Mulligan MJ, Rouphael N, Winokur P, et al. Immunogenicity of avian influenza A/Anhui/01/2005(H5N1) vaccine with MF59 adjuvant: a randomized clinical trial. JAMA. 2014;312:1420–1428. doi:10.1001/jama.2014.12609.
   PubMed Web of Science ®Google Scholar
• Reisinger KS, Holmes SJ, Pedotti P, Arora AK, Lattanzi M. 2014. A dose-ranging study of MF59((R))-adjuvanted and non-adjuvanted A/H1N1 pandemic influenza vaccine in young to middle-aged and older adult populations to assess safety, immunogenicity, and antibody persistence one year after vaccination. Hum Vaccin Immunother. 10:2395–2407. doi:10.4161/hv.29393.
   PubMed Web of Science ®Google Scholar
• Knuf M, Leroux-Roels G, Rumke H, Rivera L, Pedotti P, Arora AK, Lattanzi M, Kieninger D, Cioppa GD. Immunogenicity and safety of cell-derived MF59(R)-adjuvanted A/H1N1 influenza vaccine for children. Hum Vaccin Immunother. 2015;11:358–376. doi:10.4161/21645515.2014.987014.
   PubMed Web of Science ®Google Scholar
• Vesikari T, Forsten A, Arora A, Tsai T, Clemens R. 2015. Influenza vaccination in children primed with MF59-adjuvanted or non-adjuvanted seasonal influenza vaccine. Hum Vaccin Immunother. 11:2102–2112. doi:10.1080/21645515.2015.1044167.
   PubMed Web of Science ®Google Scholar
• Nakaya HI, Clutterbuck E, Kazmin D, Wang L, Cortese M, Bosinger SE, Patel NB, Zak DE, Aderem A, Dong T, et al. Systems biology of immunity to MF59-adjuvanted versus nonadjuvanted trivalent seasonal influenza vaccines in early childhood. Proc Natl Acad Sci U S A. 2016;113:1853–1858. doi:10.1073/pnas.1519690113.
   PubMed Web of Science ®Google Scholar
• Vesikari T, Kirstein J, Devota Go G, Leav B, Ruzycky ME, Isakov L, de Bruijn M, Oberye J, Heijnen E. Efficacy, immunogenicity, and safety evaluation of an MF59-adjuvanted quadrivalent influenza virus vaccine compared with non-adjuvanted influenza vaccine in children: a multicentre, randomised controlled, observer-blinded, phase 3 trial. Lancet Respir Med. 2018;6:345–356. doi:10.1016/S2213-2600(18)30108-5.
   PubMed Web of Science ®Google Scholar
• Van Der Maas N, Dijs-Elsinga J, Kemmeren J, Van Lier A, Knol M, De Melker H. 2016. Safety of vaccination against influenza A (H1N1) during pregnancy in the Netherlands: results on pregnancy outcomes and infant’s health: cross-sectional linkage study. BJOG. 123:709–717. doi:10.1111/1471-0528.13329.
   PubMed Web of Science ®Google Scholar
• Fabiani M, Bella A, Rota MC, Clagnan E, Gallo T, D’Amato M, Pezzotti P, Ferrara L, Demicheli V, Martinelli D. A/H1N1 pandemic influenza vaccination: A retrospective evaluation of adverse maternal, fetal and neonatal outcomes in a cohort of pregnant women in Italy. Vaccine. 2015;33:2240–2247. doi:10.1016/j.vaccine.2015.03.041.
   PubMed Web of Science ®Google Scholar
• Palma P, Romiti ML, Bernardi S, Pontrelli G, Mora N, Santilli V, Tchidjou HK, Aquilani A, Cotugno N, Alghisi F, et al. Safety and immunogenicity of a monovalent MF59(R)-adjuvanted A/H1N1 vaccine in HIV-infected children and young adults. Biologicals. 2012;40:134–139. doi:10.1016/j.biologicals.2011.12.001.
   PubMed Web of Science ®Google Scholar
• Fabbiani M, Di Giambenedetto S, Sali M, Farina S, Sansonetti P, Tamburrini E, Dal Verme LZ, Delogu G, De Luca A, Kelvin D, et al. Immune response to influenza A (H1N1)v monovalent MF59-adjuvanted vaccine in HIV-infected patients. Vaccine. 2011;29:2836–2839. doi:10.1016/j.vaccine.2011.02.020.
   PubMed Web of Science ®Google Scholar
• Noh JY, Song JY, Choi WS, Lee J, Seo YB, Kwon YJ, Ko GJ, Cha DR, Kang YS, Lee YK, et al. Immunogenicity of trivalent influenza vaccines in patients with chronic kidney disease undergoing hemodialysis: MF59-adjuvanted versus non-adjuvanted vaccines. Hum Vaccin Immunother. 2016;12(290):2–8. doi:10.1080/21645515.2016.1191717.
   Google Scholar
• Bernstein DI, Munoz FM, Callahan ST, Rupp R, Wootton SH, Edwards KM, Turley CB, Stanberry LR, Patel SM, Mcneal MM, et al. Safety and efficacy of a cytomegalovirus glycoprotein B (gB) vaccine in adolescent girls: A randomized clinical trial. Vaccine. 2016;34:313–319. doi:10.1016/j.vaccine.2015.11.056.
   PubMed Web of Science ®Google Scholar
• Nelson CS, Huffman T, Jenks JA, Cisneros De La Rosa E, Xie G, Vandergrift N, Pass RF, Pollara J, Permar SR. HCMV glycoprotein B subunit vaccine efficacy mediated by nonneutralizing antibody effector functions. Proc Natl Acad Sci U S A; 2018
   Google Scholar
• Monaci E, Mancini F, Lofano G, Bacconi M, Tavarini S, Sammicheli C, Arcidiacono L, Giraldi M, Galletti B, Rossi Paccani S, et al. MF59- and Al(OH)3-Adjuvanted Staphylococcus aureus (4C-Staph) Vaccines Induce Sustained Protective Humoral and Cellular Immune Responses, with a Critical Role for Effector CD4 T Cells at Low Antibody Titers. Front Immunol. 2015;6:439. doi:10.3389/fimmu.2015.00439.
   PubMed Web of Science ®Google Scholar
• Vaccari M, Gordon SN, Fourati S, Schifanella L, Liyanage NP, Cameron M, Keele BF, Shen X, Tomaras GD, Billings E, et al. Adjuvant-dependent innate and adaptive immune signatures of risk of SIVmac251 acquisition. Nat Med. 2016;22:762–770. doi:10.1038/nm.4105.
   PubMed Web of Science ®Google Scholar
• Wack A, Baudner BC, Hilbert AK, Manini I, Nuti S, Tavarini S, Scheffczik H, Ugozzoli M, Singh M, Kazzaz J, et al. Combination adjuvants for the induction of potent, long-lasting antibody and T-cell responses to influenza vaccine in mice. Vaccine. 2008;26:552–561. doi:10.1016/j.vaccine.2007.11.054.
   PubMed Web of Science ®Google Scholar
• Baudner BC, Ronconi V, Casini D, Tortoli M, Kazzaz J, Singh M, Hawkins LD, Wack A, O'Hagan DT. MF59 emulsion is an effective delivery system for a synthetic TLR4 agonist (E6020). Pharm Res. 2009;26:1477–1485. doi:10.1007/s11095-009-9859-5.
   PubMed Web of Science ®Google Scholar
• Singh M, Kazzaz J, Ugozzoli M, Baudner B, Pizza M, Giuliani M, Hawkins LD, Otten G, O'Hagan DT. MF59 oil-in-water emulsion in combination with a synthetic TLR4 agonist (E6020) is a potent adjuvant for a combination Meningococcus vaccine. Hum Vaccin Immunother. 2012;8:486–490. doi:10.4161/hv.19229.
   PubMed Web of Science ®Google Scholar
• Lai RP, Seaman MS, Tonks P, Wegmann F, Seilly DJ, Frost SD, LaBranche CC, Montefiori DC, Dey AK, Srivastava IK, et al. Mixed adjuvant formulations reveal a new combination that elicit antibody response comparable to Freund’s adjuvants. PLoS One. 2012;7:e35083. doi:10.1371/journal.pone.0035083.
   PubMed Web of Science ®Google Scholar
• Dey AK, Burke B, Sun Y, Hartog K, Heeney JL, Montefiori D, Srivastava IK, Barnett SW. Use of a polyanionic carbomer, Carbopol971P, in combination with MF59, improves antibody responses to HIV-1 envelope glycoprotein. Vaccine. 2012;30:2749–2759. doi:10.1016/j.vaccine.2012.02.027.
   PubMed Web of Science ®Google Scholar