T-cell-dependent mechanisms promote Ebola VLP-induced antibody responses, but are dispensable for vaccine-mediated protection

References

• Wong G, Kobinger GP.Backs against the wall: novel and existing strategies used during the 2014-2015 Ebola virus outbreak. Clin Microbiol Rev 2015;28: 593–601.
   PubMed Web of Science ®Google Scholar
• Marzi A, Feldmann H.Ebola virus vaccines: an overview of current approaches. Expert Rev Vaccines. 2014;13: 521–531.
   PubMed Web of Science ®Google Scholar
• Cooper CL, Bavari S.A race for an Ebola vaccine: promises and obstacles. Trends Microbiol 2015;23: 65–66.
   PubMed Web of Science ®Google Scholar
• De Santis O, Audran R, Pothin Eet al.Safety and immunogenicity of a chimpanzee adenovirus-vectored Ebola vaccine in healthy adults: a randomised, double-blind, placebo-controlled, dose-finding, phase 1/2a study. Lancet Infect Dis 2016;16: 311–320.
   PubMed Web of Science ®Google Scholar
• Huttner A, Dayer JA, Yerly Set al.The effect of dose on the safety and immunogenicity of the VSV Ebola candidate vaccine: a randomised double-blind, placebo-controlled phase 1/2 trial. Lancet Infect Dis 2015;15: 1156–1166.
   PubMed Web of Science ®Google Scholar
• Regules JA, Beigel JH, Paolino KMet al.A recombinant vesicular stomatitis virus ebola vaccine—preliminary report. N Engl J Med 2017;376: 330–341.
   PubMed Web of Science ®Google Scholar
• Martins KA, Jahrling PB, Bavari Set al.Ebola virus disease candidate vaccines under evaluation in clinical trials. Expert Rev Vaccines 2016;15: 1101–1112.
   PubMed Web of Science ®Google Scholar
• Falzarano D, Geisbert TW, Feldmann H.Progress in filovirus vaccine development: evaluating the potential for clinical use. Expert Rev Vaccines 2011;10: 63–77.
   PubMed Web of Science ®Google Scholar
• Krause PR, Bryant PR, Clark Tet al.Immunology of protection from Ebola virus infection. Sci Transl Med 2015;7: 286ps11.
   PubMed Web of Science ®Google Scholar
• Sullivan NJ, Martin JE, Graham BSet al.Correlates of protective immunity for Ebola vaccines: implications for regulatory approval by the animal rule. Nat Rev Microbiol 2009;7: 393–400.
   PubMed Web of Science ®Google Scholar
• Bradfute SB, Bavari S.Correlates of immunity to filovirus infection. Viruses 2011;3: 982–1000.
   PubMed Web of Science ®Google Scholar
• Wong G, Kobinger GP, Qiu X.Characterization of host immune responses in Ebola virus infections. Expert Rev Clin Immunol 2014;10: 781–790.
   PubMed Web of Science ®Google Scholar
• Sullivan NJ, Hensley L, Asiedu Cet al.CD8+ cellular immunity mediates rAd5 vaccine protection against Ebola virus infection of nonhuman primates. Nat Med 2011;17: 1128–1131.
   PubMed Web of Science ®Google Scholar
• Olinger GG, Bailey MA, Dye JMet al.Protective cytotoxic T-cell responses induced by venezuelan equine encephalitis virus replicons expressing Ebola virus proteins. J Virol. 2005;79: 14189–14196.
   PubMed Web of Science ®Google Scholar
• Warfield KL, Olinger GG.Protective role of cytotoxic T lymphocytes in filovirus hemorrhagic fever. J Biomed Biotechnol 2011;2011: 984241.
   PubMedGoogle Scholar
• Wong G, Richardson JS, Pillet Set al.Immune parameters correlate with protection against ebola virus infection in rodents and nonhuman primates. Sci Transl Med 2012;4: 158ra46.
   Web of Science ®Google Scholar
• Marzi A, Engelmann F, Feldmann Fet al.Antibodies are necessary for rVSV/ZEBOV-GP-mediated protection against lethal Ebola virus challenge in nonhuman primates. Proc Natl Acad Sci USA 2013;110: 1893–1898.
   PubMed Web of Science ®Google Scholar
• Jones SM, Stroher U, Fernando Let al.Assessment of a vesicular stomatitis virus-based vaccine by use of the mouse model of Ebola virus hemorrhagic fever. J Infect Dis 2007;196: S404–S412.
   PubMed Web of Science ®Google Scholar
• Martins KA, Cooper CL, Stronsky SMet al.Adjuvant-enhanced CD4 T cell responses are critical to durable vaccine immunity. EBioMedicine 2016;3: 67–78.
   PubMed Web of Science ®Google Scholar
• Martins KA, Steffens JT, van Tongeren SAet al.Toll-like receptor agonist augments virus-like particle-mediated protection from Ebola virus with transient immune activation. PLoS ONE 2014;9: e89735.
   PubMed Web of Science ®Google Scholar
• Warfield KL, Olinger G, Deal EMet al.Induction of humoral and CD8+ T cell responses are required for protection against lethal Ebola virus infection. J Immunol 2005;175: 1184–1191.
   PubMed Web of Science ®Google Scholar
• Blaney JE, Marzi A, Willet Met al.Antibody quality and protection from lethal Ebola virus challenge in nonhuman primates immunized with rabies virus based bivalent vaccine. PLoS Pathog 2013;9: e1003389.
   PubMed Web of Science ®Google Scholar
• Qiu X, Audet J, Wong Get al.Sustained protection against Ebola virus infection following treatment of infected nonhuman primates with ZMAb. Sci Rep 2013;3: 3365.
   PubMed Web of Science ®Google Scholar
• Qiu X, Wong G, Audet Jet al.Reversion of advanced Ebola virus disease in nonhuman primates with ZMapp. Nature 2014;514: 47–53.
   PubMed Web of Science ®Google Scholar
• Pettitt J, Zeitlin L, Kim DHet al.Therapeutic intervention of Ebola virus infection in rhesus macaques with the MB-003 monoclonal antibody cocktail. Sci Transl Med 2013;5: 199ra13.
   Web of Science ®Google Scholar
• McHeyzer-Williams M, Okitsu S, Wang Net al.Molecular programming of B cell memory. Nat Rev Immunol 2012;12: 24–34.
   Web of Science ®Google Scholar
• Mesin L, Ersching J, Victora GD.Germinal center B cell dynamics. Immunity 2016;45: 471–482.
   PubMed Web of Science ®Google Scholar
• Bengtsson KL, Song H, Stertman Let al.Matrix-M adjuvant enhances antibody, cellular and protective immune responses of a Zaire Ebola/Makona virus glycoprotein (GP) nanoparticle vaccine in mice. Vaccine 2016;34: 1927–1935.
   PubMed Web of Science ®Google Scholar
• Warfield KL, Dye JM, Wells JBet al.Homologous and heterologous protection of nonhuman primates by Ebola and Sudan virus-like particles. PLoS ONE 2015;10: e0118881.
   PubMed Web of Science ®Google Scholar
• Warfield KL, Bosio CM, Welcher BCet al.Ebola virus-like particles protect from lethal Ebola virus infection. Proc Natl Acad Sci USA 2003;100: 15889–15894.
   PubMed Web of Science ®Google Scholar
• Warfield KL, Swenson DL, Olinger GGet al.Ebola virus-like particle-based vaccine protects nonhuman primates against lethal Ebola virus challenge. J Infect Dis 2007;196: S430–S437.
   PubMed Web of Science ®Google Scholar
• Cazares LH, Ward MD, Brueggemann EEet al.Development of a liquid chromatography high resolution mass spectrometry method for the quantitation of viral envelope glycoprotein in Ebola virus-like particle vaccine preparations. Clin Proteomics 2016;13: 18.
   PubMed Web of Science ®Google Scholar
• De Silva NS, Klein U.Dynamics of B cells in germinal centres. Nat Rev Immunol 2015;15: 137–148.
   PubMed Web of Science ®Google Scholar
• Ma CS, Deenick EK, Batten Met al.The origins, function, and regulation of T follicular helper cells. J Exp Med 2012;209: 1241–1253.
   PubMed Web of Science ®Google Scholar
• Baumjohann D, Preite S, Reboldi Aet al.Persistent antigen and germinal center B cells sustain T follicular helper cell responses and phenotype. Immunity 2013;38: 596–605.
   PubMed Web of Science ®Google Scholar
• Elgueta R, Benson MJ, de Vries VCet al.Molecular mechanism and function of CD40/CD40L engagement in the immune system. Immunol Rev 2009;229: 152–172.
   PubMed Web of Science ®Google Scholar
• Kawabe T, Naka T, Yoshida Ket al.The immune responses in CD40-deficient mice: impaired immunoglobulin class switching and germinal center formation. Immunity 1994;1: 167–178.
   PubMed Web of Science ®Google Scholar
• Muramatsu M, Kinoshita K, Fagarasan Set al.Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell 2000;102: 553–563.
   PubMed Web of Science ®Google Scholar
• Kitamura D, Roes J, Kuhn Ret al.B cell-deficient mouse by targeted disruption of the membrane exon of the immunoglobulin mu chain gene. Nature 1991;350: 423–426.
   PubMed Web of Science ®Google Scholar
• Allio T.Product development under FDA's animal rule: understanding FDA's expectations and potential implications for traditional development programs. Therap Innov Regul Sci 2016;50: 660–670.
   PubMed Web of Science ®Google Scholar
• Bray M, Davis K, Geisbert Tet al.A mouse model for evaluation of prophylaxis and therapy of Ebola hemorrhagic fever. J Infect Dis 1998;178: 651–661.
   PubMed Web of Science ®Google Scholar
• Nakayama E, Saijo M.Animal models for Ebola and Marburg virus infections. Front Microbiol 2013;4: 267.
   PubMed Web of Science ®Google Scholar
• Bradfute SB, Anthony SM, Stuthman KSet al.Mechanisms of immunity in post-exposure vaccination against Ebola virus infection. PLoS ONE 2015;10: e0118434.
   PubMed Web of Science ®Google Scholar
• Bradfute SB, Warfield KL, Bray M.Mouse models for filovirus infections. Viruses 2012;4: 1477–1508.
   PubMed Web of Science ®Google Scholar
• Furuyama W, Marzi A, Nanbo Aet al.Discovery of an antibody for pan-ebolavirus therapy. Sci Rep 2016;6: 20514.
   PubMed Web of Science ®Google Scholar
• Warfield KL, Perkins JG, Swenson DLet al.Role of natural killer cells in innate protection against lethal ebola virus infection. J Exp Med 2004;200: 169–179.
   PubMed Web of Science ®Google Scholar
• Nanton MR, Way SS, Shlomchik MJet al.Cutting edge: B cells are essential for protective immunity against Salmonella independent of antibody secretion. J Immunol 2012;189: 5503–5507.
   PubMed Web of Science ®Google Scholar
• Misumi I, Whitmire JK.B cell depletion curtails CD4+ T cell memory and reduces protection against disseminating virus infection. J Immunol 2014;192: 1597–1608.
   PubMed Web of Science ®Google Scholar