Combination vaccines: synergistic simultaneous induction of antibody and T-cell immunity

References

• Nossal GJ. The Global Alliance for Vaccines and Immunization – a millennial challenge. Nat. Immunol.1(1), 5–8 (2000).
   PubMed Web of Science ®Google Scholar
• Nossal GJ. A healthier climate for the funding of vaccine research. Nat. Immunol.5(5), 457–459 (2004).
   PubMedGoogle Scholar
• Hanke T, McMichael AJ, Mwau M et al. Development of a DNA-MVA/HIVA vaccine for Kenya. Vaccine20(15), 1995–1998 (2002).
   PubMed Web of Science ®Google Scholar
• Moore AC, Hill AV. Progress in DNA-based heterologous prime–boost immunization strategies for malaria.Immunol. Rev.199, 126–143 (2004).
   PubMed Web of Science ®Google Scholar
• Schneider J, Gilbert SC, Blanchard TJ et al. Enhanced immunogenicity for CD8+ T cell induction and complete protective efficacy of malaria DNA vaccination by boosting with modified vaccinia virus Ankara. Nat. Med.4(4), 397–402 (1998).
   PubMed Web of Science ®Google Scholar
• Good MF, Doolan DL. Immune effector mechanisms in malaria. Curr. Opin. Immunol.11(4), 412–419 (1999).
   PubMed Web of Science ®Google Scholar
• Letvin NL, Barouch DH, Montefiori DC. Prospects for vaccine protection against HIV-1 infection and AIDS. Ann. Rev. Immunol.20, 73–99 (2002).
   PubMed Web of Science ®Google Scholar
• Igietseme JU, Eko FO, He H, Black CM. Antibody regulation of T-cell immunity: implications for vaccine strategies against intracellular pathogens. Expert Rev. Vaccines3(1), 23–34 (2003).
   Google Scholar
• Houghton AN, Gold JS, Blachere NE. Immunity against cancer: lessons learned from melanoma. Curr. Opin. Immunol.13(2), 134–140 (2001).
   PubMed Web of Science ®Google Scholar
• Sedegah M, Weiss W, Sacci JB Jr et al. Improving protective immunity induced by DNA-based immunization: priming with antigen and GM-CSF-encoding plasmid DNA and boosting with antigen-expressing recombinant poxvirus. J. Immunol.164(11), 5905–5912 (2000).
   PubMed Web of Science ®Google Scholar
• Srivastava IK, Liu MA. Gene vaccines. Ann. Intern. Med.138(7), 550–559 (2003).
   PubMed Web of Science ®Google Scholar
• Hutchings CL, Gilbert SC, Hill AV, Moore AC. Novel protein and poxvirus-based vaccine combinations for simultaneous induction of humoral and cell-mediated immunity. J. Immunol.175(1), 599–606 (2005).
   PubMed Web of Science ®Google Scholar
• Gallup JL, Sachs JD. The economic burden of malaria. Am. J. Trop. Med. Hyg.64(Suppl. 1–2), 85–96 (2001).
   PubMed Web of Science ®Google Scholar
• Snow RW, Guerra CA, Noor AM, Myint HY, Hay SI. The global distribution of clinical episodes of Plasmodium falciparum malaria. Nature434(7030), 214–217 (2005).
   PubMed Web of Science ®Google Scholar
• Marshall E. Malaria. A renewed assault on an old and deadly foe. Science290(5491), 428–430 (2000).
   PubMed Web of Science ®Google Scholar
• Plebanski M, Hill AV. The immunology of malaria infection. Curr. Opin. Immunol.12(4), 437–441 (2000).
   PubMed Web of Science ®Google Scholar
• Bull PC, Lowe BS, Kortok M et al. Parasite antigens on the infected red cell surface are targets for naturally acquired immunity to malaria. Nat. Med.4(3), 358–360 (1998).
   PubMed Web of Science ®Google Scholar
• Dodoo D, Staalsoe T, Giha H et al. Antibodies to variant antigens on the surfaces of infected erythrocytes are associated with protection from malaria in Ghanaian children. Infect. Immun.69(6), 3713–3718 (2001).
   PubMed Web of Science ®Google Scholar
• Clyde DF, Most H, McCarthy VC, Vanderberg JP. Immunization of man against sporozite-induced Falciparum malaria. Am. J. Med. Sci.266(3), 169–177 (1973).
   PubMed Web of Science ®Google Scholar
• Nussenzweig RS, Vanderberg J, Most H, Orton C. Protective immunity produced by the injection of x-irradiated sporozoites of Plasmodium berghei.Nature216(5111), 160–162 (1967).
   PubMed Web of Science ®Google Scholar
• Webster DP, Dunachie S, Vuola JM et al. Enhanced T cell-mediated protection against malaria in human challenges by using the recombinant poxviruses FP9 and modified vaccinia virus Ankara. Proc. Natl Acad. Sci. USA102(13), 4836–4841 (2005).
   PubMed Web of Science ®Google Scholar
• Trombetta ES, Mellman I. Cell biology of antigen processing in vitro and in vivo.Ann. Rev. Immunol.23, 975–1028 (2005).
   PubMed Web of Science ®Google Scholar
• Kutubuddin M, Simons J, Chow M. Poliovirus-specific major histocompatibility complex class I-restricted cytolytic T-cell epitopes in mice localize to neutralizing antigenic regions. J. Virol.66(10), 5967–5974 (1992).
   PubMedGoogle Scholar
• Schirmbeck R, Melber K, Mertens T, Reimann J. Antibody and cytotoxic T-cell responses to soluble hepatitis B virus (HBV) S antigen in mice: implication for the pathogenesis of HBV-induced hepatitis. J. Virol.68(3), 1418–1425 (1994).
   PubMed Web of Science ®Google Scholar
• Wraith DC, Vessey AE, Askonas BA. Purified influenza virus nucleoprotein protects mice from lethal infection. J. Gen. Virol.68(Pt 2), 433–440 (1987).
   PubMed Web of Science ®Google Scholar
• Yamada A, Ziese MR, Young JF, Yamada YK, Ennis FA. Influenza virus hemagglutinin-specific cytotoxic T cell response induced by polypeptide produced in Escherichia coli.J. Exp. Med.162(2), 663–674 (1985).
   PubMedGoogle Scholar
• Moore A, McCarthy L, Mills KH. The adjuvant combination monophosphoryl lipid A and QS21 switches T cell responses induced with a soluble recombinant HIV protein from Th2 to Th1. Vaccine17(20–21), 2517–2527 (1999).
   PubMed Web of Science ®Google Scholar
• Nair S, Zhou X, Huang L, Rouse BT. Class I restricted CTL recognition of a soluble protein delivered by liposomes containing lipophilic polylysines. J. Immunol. Methods152(2), 237–243 (1992).
   PubMed Web of Science ®Google Scholar
• Mowat AM, Donachie AM, Reid G, Jarrett O. Immune-stimulating complexes containing Quil A and protein antigen prime class I MHC-restricted T lymphocytes in vivo and are immunogenic by the oral route. Immunology72(3), 317–322 (1991).
   PubMed Web of Science ®Google Scholar
• Takahashi H, Takeshita T, Morein B et al. Induction of CD8+ cytotoxic T cells by immunization with purified HIV-1 envelope protein in ISCOMs. Nature344(6269), 873–875 (1990).
   PubMed Web of Science ®Google Scholar
• van Binnendijk RS, van Baalen CA, Poelen MC et al. Measles virus transmembrane fusion protein synthesized de novo or presented in immunostimulating complexes is endogenously processed for HLA class I- and class II-restricted cytotoxic T cell recognition. J. Exp. Med.176(1), 119–128 (1992).
   PubMed Web of Science ®Google Scholar
• Pashine A, Valiante NM, Ulmer JB. Targeting the innate immune response with improved vaccine adjuvants. Nat. Med.11(Suppl. 4), S63–S68 (2005).
   PubMed Web of Science ®Google Scholar
• Alonso PL, Sacarlal J, Aponte JJ et al. Duration of protection with RTS,S/AS02A malaria vaccine in prevention of Plasmodium falciparum disease in Mozambican children: single-blind extended follow-up of a randomised controlled trial. Lancet366(9502), 2012–2018 (2005).
   PubMed Web of Science ®Google Scholar
• Alonso PL, Sacarlal J, Aponte JJ et al. Efficacy of the RTS,S/AS02A vaccine against Plasmodium falciparum infection and disease in young African children: randomised controlled trial. Lancet364(9443), 1411–1420 (2004).
   PubMed Web of Science ®Google Scholar
• Garcon N, Heppner DG, Cohen J. Development of RTS,S/AS02: a purified subunit-based malaria vaccine candidate formulated with a novel adjuvant. Expert Rev. Vaccines2(2), 231–238 (2003).
   PubMedGoogle Scholar
• Heppner DG Jr, Kester KE, Ockenhouse CF et al. Towards an RTS,S-based, multi-stage, multi-antigen vaccine against falciparum malaria: progress at the Walter Reed Army Institute of Research. Vaccine23(17–18), 2243–2250 (2005).
   PubMed Web of Science ®Google Scholar
• Lalvani A, Moris P, Voss G et al. Potent induction of focused Th1-type cellular and humoral immune responses by RTS,S/SBAS2, a recombinant Plasmodium falciparum malaria vaccine. J. Infect. Dis.180(5), 1656–1664 (1999).
   PubMed Web of Science ®Google Scholar
• Reece WH, Pinder M, Gothard PK et al. A CD4(+) T-cell immune response to a conserved epitope in the circumsporozoite protein correlates with protection from natural Plasmodium falciparum infection and disease. Nat. Med.10(4), 406–410 (2004).
   PubMed Web of Science ®Google Scholar
• Hill AV. Pre-erythrocytic malaria vaccines: towards greater efficacy. Nat. Rev. Immunol.6(1), 21–32 (2006).
   PubMed Web of Science ®Google Scholar
• Birkett A, Lyons K, Schmidt A et al. A modified hepatitis B virus core particle containing multiple epitopes of the Plasmodium falciparum circumsporozoite protein provides a highly immunogenic malaria vaccine in preclinical analyses in rodent and primate hosts. Infect. Immun.70(12), 6860–6870 (2002).
   PubMed Web of Science ®Google Scholar
• Nardin EH, Oliveira GA, Calvo-Calle JM et al. Phase I testing of a malaria vaccine composed of hepatitis B virus core particles expressing Plasmodium falciparum circumsporozoite epitopes. Infect. Immun.72(11), 6519–6527 (2004).
   PubMed Web of Science ®Google Scholar
• Oliveira GA, Wetzel K, Calvo-Calle JM et al. Safety and enhanced immunogenicity of a hepatitis B core particle Plasmodium falciparum malaria vaccine formulated in adjuvant Montanide ISA 720 in a Phase I trial. Infect. Immun.73(6), 3587–3597 (2005).
   PubMed Web of Science ®Google Scholar
• Walther M, Dunachie S, Keating S et al. Safety, immunogenicity and efficacy of a pre-erythrocytic malaria candidate vaccine, ICC-1132 formulated in Seppic ISA 720. Vaccine23(7), 857–864 (2005).
   PubMed Web of Science ®Google Scholar
• Lopez JA, Weilenman C, Audran R et al. A synthetic malaria vaccine elicits a potent CD8(+) and CD4(+) T lymphocyte immune response in humans. Implications for vaccination strategies. Eur. J. Immunol.31(7), 1989–1998 (2001).
   PubMed Web of Science ®Google Scholar
• Donnelly JJ, Ulmer JB, Shiver JW, Liu MA. DNA vaccines. Ann. Rev. Immunol.15, 617–648 (1997).
   PubMed Web of Science ®Google Scholar
• Donnelly JJ, Wahren B, Liu MA. DNA vaccines: progress and challenges. J. Immunol.175(2), 633–639 (2005).
   PubMed Web of Science ®Google Scholar
• Ulmer JB, Deck RR, DeWitt CM et al. Protective immunity by intramuscular injection of low doses of influenza virus DNA vaccines. Vaccine12(16), 1541–1544 (1994).
   PubMed Web of Science ®Google Scholar
• Ulmer JB, Donnelly JJ, Parker SE et al. Heterologous protection against influenza by injection of DNA encoding a viral protein. Science259(5102), 1745–1749 (1993).
   PubMed Web of Science ®Google Scholar
• Wolff JA, Malone RW, Williams P et al. Direct gene transfer into mouse muscle in vivo.Science247(4949 Pt 1), 1465–1468 (1990).
   PubMed Web of Science ®Google Scholar
• Moore AC, Kong WP, Chakrabarti BK, Nabel GJ. Effects of antigen and genetic adjuvants on immune responses to human immunodeficiency virus DNA vaccines in mice. J. Virol.76(1), 243–250 (2002).
   PubMed Web of Science ®Google Scholar
• Sedegah M, Hedstrom R, Hobart P, Hoffman SL. Protection against malaria by immunization with plasmid DNA encoding circumsporozoite protein. Proc. Natl Acad. Sci. USA91(21), 9866–9870 (1994).
   PubMed Web of Science ®Google Scholar
• Degano P, Schneider J, Hannan CM, Gilbert SC, Hill AV. Gene gun intradermal DNA immunization followed by boosting with modified vaccinia virus Ankara: enhanced CD8+ T cell immunogenicity and protective efficacy in the influenza and malaria models. Vaccine18(7–8), 623–632 (1999).
   PubMed Web of Science ®Google Scholar
• Leitner WW, Seguin MC, Ballou WR et al. Immune responses induced by intramuscular or gene gun injection of protective deoxyribonucleic acid vaccines that express the circumsporozoite protein from Plasmodium berghei malaria parasites. J. Immunol.159(12), 6112–6119 (1997).
   PubMedGoogle Scholar
• Calarota S, Bratt G, Nordlund S et al. Cellular cytotoxic response induced by DNA vaccination in HIV-1-infected patients. Lancet351(9112), 1320–1325 (1998).
   PubMed Web of Science ®Google Scholar
• MacGregor RR, Boyer JD, Ugen KE et al. First human trial of a DNA-based vaccine for treatment of human immunodeficiency virus type 1 infection: safety and host response. J. Infect. Dis.178(1), 92–100 (1998).
   PubMed Web of Science ®Google Scholar
• Wang R, Doolan DL, Le TP et al. Induction of antigen-specific cytotoxic T lymphocytes in humans by a malaria DNA vaccine. Science282(5388), 476–480 (1998).
   PubMed Web of Science ®Google Scholar
• McConkey SJ, Reece WH, Moorthy VS et al. Enhanced T-cell immunogenicity of plasmid DNA vaccines boosted by recombinant modified vaccinia virus Ankara in humans. Nat. Med.9(6), 729–735 (2003).
   PubMed Web of Science ®Google Scholar
• Anderson RJ, Hannan CM, Gilbert SC et al. Enhanced CD8+ T cell immune responses and protection elicited against Plasmodium berghei malaria by prime boost immunization regimens using a novel attenuated fowlpox virus. J. Immunol.172(5), 3094–3100 (2004).
   PubMed Web of Science ®Google Scholar
• Ockenhouse CF, Sun PF, Lanar DE et al. Phase I/IIa safety, immunogenicity, and efficacy trial of NYVAC-Pf7, a pox-vectored, multiantigen, multistage vaccine candidate for Plasmodium falciparum malaria. J. Infect. Dis.177(6), 1664–1673 (1998).
   PubMed Web of Science ®Google Scholar
• Amara RR, Villinger F, Staprans SI et al. Different patterns of immune responses but similar control of a simian–human immunodeficiency virus 89.6P mucosal challenge by modified vaccinia virus Ankara (MVA) and DNA/MVA vaccines. J. Virol.76(15), 7625–7631 (2002).
   PubMed Web of Science ®Google Scholar
• Keating SM, Bejon P, Berthoud T et al. Durable human memory T cells quantifiable by cultured enzyme-linked immunospot assays are induced by heterologous prime boost immunization and correlate with protection against malaria. J. Immunol.175(9), 5675–5680 (2005).
   PubMed Web of Science ®Google Scholar
• Letvin NL, Huang Y, Chakrabarti BK et al. Heterologous envelope immunogens contribute to AIDS vaccine protection in rhesus monkeys. J. Virol.78(14), 7490–7497 (2004).
   PubMed Web of Science ®Google Scholar
• McShane H, Behboudi S, Goonetilleke N, Brookes R, Hill AV. Protective immunity against Mycobacterium tuberculosis induced by dendritic cells pulsed with both CD8(+)- and CD4(+)-T-cell epitopes from antigen 85A. Infect. Immun.70(3), 1623–1626 (2002).
   PubMed Web of Science ®Google Scholar
• Moorthy VS, Imoukhuede EB, Keating S et al. Phase I evaluation of 3 highly immunogenic prime-boost regimens, including a 12-month reboosting vaccination, for malaria vaccination in Gambian men. J. Infect. Dis.189(12), 2213–2219 (2004).
   PubMed Web of Science ®Google Scholar
• Moorthy VS, Pinder M, Reece WH et al. Safety and immunogenicity of DNA/modified vaccinia virus ankara malaria vaccination in African adults. J. Infect. Dis.188(8), 1239–1244 (2003).
   PubMed Web of Science ®Google Scholar
• Vuola JM, Keating S, Webster DP et al. Differential immunogenicity of various heterologous prime–boost vaccine regimens using DNA and viral vectors in healthy volunteers. J. Immunol.174(1), 449–455 (2005).
   PubMed Web of Science ®Google Scholar
• Sullivan NJ, Geisbert TW, Geisbert JB et al. Accelerated vaccination for Ebola virus haemorrhagic fever in non-human primates. Nature424(6949), 681–684 (2003).
   PubMed Web of Science ®Google Scholar
• Dunachie SJ, Walther M, Vuola JM et al. A clinical trial of immunisation with the candidate malaria vaccines RTS,S/AS02A and MVA-CS. Vaccine24(15), 2850–2859 (2006).
   PubMed Web of Science ®Google Scholar
• Boudet F, Chevalier M, Jourdier TM, Tartaglia J, Moste C. Modulation of the antibody response to the HIV envelope subunit by co-administration of infectious or heat-inactivated canarypoxvirus (ALVAC) preparations. Vaccine19(30), 4267–4275 (2001).
   PubMedGoogle Scholar
• Phumiamorn S, Sato H, Kamiyama T, Kurokawa M, Shiraki K. Induction of humoral and cell-mediated immunity to hepatitis B surface antigen by a novel adjuvant activity of Oka varicella vaccine. J. Gen. Virol.84(Pt 2), 287–291 (2003).
   PubMed Web of Science ®Google Scholar
• Ramirez JC, Gherardi MM, Esteban M. Biology of attenuated modified vaccinia virus Ankara recombinant vector in mice: virus fate and activation of B- and T-cell immune responses in comparison with the Western Reserve strain and advantages as a vaccine. J. Virol.74(2), 923–933 (2000).
   PubMed Web of Science ®Google Scholar
• Cassese G, Arce S, Hauser AE et al. Plasma cell survival is mediated by synergistic effects of cytokines and adhesion-dependent signals. J. Immunol.171(4), 1684–1690 (2003).
   PubMed Web of Science ®Google Scholar
• Guyre PM, Graziano RF, Goldstein J et al. Increased potency of Fc-receptor-targeted antigens. Cancer Immunol. Immunother.45(3–4), 146–148 (1997).
   PubMed Web of Science ®Google Scholar
• Moore T, Ekworomadu CO, Eko FO et al. Fc receptor-mediated antibody regulation of T cell immunity against intracellular pathogens. J. Infect. Dis.188(4), 617–624 (2003).
   PubMed Web of Science ®Google Scholar
• Fanger NA, Voigtlaender D, Liu C et al. Characterization of expression, cytokine regulation, and effector function of the high affinity IgG receptor Fc γ RI (CD64) expressed on human blood dendritic cells. J. Immunol.158(7), 3090–3098 (1997).
   PubMed Web of Science ®Google Scholar
• Geissmann F, Launay P, Pasquier B et al. A subset of human dendritic cells expresses IgA Fc receptor (CD89), which mediates internalization and activation upon cross-linking by IgA complexes. J. Immunol.166(1), 346–352 (2001).
   PubMed Web of Science ®Google Scholar
• Gosselin EJ, Wardwell K, Gosselin DR et al. Enhanced antigen presentation using human Fc γ receptor (monocyte/macrophage)-specific immunogens. J. Immunol.149(11), 3477–3481 (1992).
   PubMed Web of Science ®Google Scholar
• Regnault A, Lankar D, Lacabanne V et al. Fcγ receptor-mediated induction of dendritic cell maturation and major histocompatibility complex class I-restricted antigen presentation after immune complex internalization. J. Exp. Med.189(2), 371–380 (1999).
   PubMed Web of Science ®Google Scholar
• Mills KH. Immunity to Bordetella pertussis.Microbes Infect.3(8), 655–677 (2001).
   PubMed Web of Science ®Google Scholar
• Moore A, McGuirk P, Adams S et al. Immunization with a soluble recombinant HIV protein entrapped in biodegradable microparticles induces HIV-specific CD8+ cytotoxic T lymphocytes and CD4+ Th1 cells. Vaccine13(18), 1741–1749 (1995).
   PubMed Web of Science ®Google Scholar
• Singh M, Kazzaz J, Ugozzoli M et al. Polylactide-co-glycolide microparticles with surface adsorbed antigens as vaccine delivery systems. Curr. Drug Deliv.3(1), 115–120 (2006).
   PubMedGoogle Scholar
• Westerfeld N, Zurbriggen R. Peptides delivered by immunostimulating reconstituted influenza virosomes. J. Pept. Sci.11(11), 707–712 (2005).
   PubMed Web of Science ®Google Scholar
• Mayr A. [Historical review of smallpox, the eradication of smallpox and the attenuated smallpox MVA vaccine]. Berl. Munch. Tierarztl. Wochenschr.112(9), 322–328 (1999).
   PubMed Web of Science ®Google Scholar
• Paoletti E. Applications of pox virus vectors to vaccination: an update. Proc. Natl Acad. Sci. USA93(21), 11349–11353 (1996).
   PubMed Web of Science ®Google Scholar
• Gilbert SC, Schneider J, Hannan CM et al. Enhanced CD8 T cell immunogenicity and protective efficacy in a mouse malaria model using a recombinant adenoviral vaccine in heterologous prime–boost immunisation regimes. Vaccine20(7–8), 1039–1045 (2002).
   PubMed Web of Science ®Google Scholar
• Tatsis N, Ertl HC. Adenoviruses as vaccine vectors. Mol. Ther.10(4), 616–629 (2004).
   PubMed Web of Science ®Google Scholar
• Schneider J, Langermans JA, Gilbert SC et al. A prime-boost immunisation regimen using DNA followed by recombinant modified vaccinia virus Ankara induces strong cellular immune responses against the Plasmodium falciparum TRAP antigen in chimpanzees. Vaccine19(32), 4595–4602 (2001).
   PubMed Web of Science ®Google Scholar
• McShane H, Pathan AA, Sander CR et al. Recombinant modified vaccinia virus Ankara expressing antigen 85A boosts BCG-primed and naturally acquired antimycobacterial immunity in humans. Nat. Med.10(11), 1240–1244 (2004).
   PubMed Web of Science ®Google Scholar
• Sullivan NJ, Sanchez A, Rollin PE, Yang ZY, Nabel GJ. Development of a preventive vaccine for Ebola virus infection in primates. Nature408(6812), 605–609 (2000).
   PubMed Web of Science ®Google Scholar