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Review

Improving vaccines by incorporating immunological coadjuvants

, , &
Pages 559-578 | Published online: 09 Jan 2014

References

  • Bramwell VW, Perrie Y. The rational design of vaccines. Drug Discov. Today10(22), 1527–1534 (2005).
  • Ramon G. Sur la toxine et surranatoxine diphtheriques. Ann. Inst. Pasteur38, 1–7 (1924).
  • Singh M, O’Hagan DT. Recent advances in vaccine adjuvants. Pharm. Res.19(6), 715–728 (2002).
  • WHO. Immunological adjuvants. Technical report series No. 595, Geneva, Switzerland (1976).
  • Barr TA, Carlring J, Heath AW. Co-stimulatory agonists as immunological adjuvants. Vaccine24(17), 3399–3407 (2006).
  • Ball R. Methods of ensuring vaccine safety. Expert Rev. Vaccines1(2), 161–168 (2002).
  • Pashine A, Valiante NM, Ulmer JB. Targeting the innate immune response with improved vaccine adjuvants. Nat. Med.11(4 Suppl.), S63–S68 (2005).
  • Ulmer JB, Valley U, Rappuoli R. Vaccine manufacturing: challenges and solutions. Nat. Biotechnol.24(11), 1377–1383 (2006).
  • Petrovsky N, Aguilar JC. Vaccine adjuvants: current state and future trends. Immunol. Cell Biol.82(5), 488–496 (2004).
  • Creagh EM, O’Neill LA. TLRs, NLRs and RLRs: a trinity of pathogen sensors that co-operate in innate immunity. Trends Immunol.27(8), 352–357 (2006).
  • Trinchieri G, Sher A. Cooperation of Toll-like receptor signals in innate immune defence. Nat. Rev. Immunol.7(3), 179–190 (2007).
  • Verstak B, Hertzog P, Mansell A. Toll-like receptor signalling and the clinical benefits that lie within. Inflamm. Res.56(1), 1–10 (2007).
  • Akira S, Uematsu S, Takeuchi O. Pathogen recognition and innate immunity. Cell124(4), 783–801 (2006).
  • Kawai T, Akira S. Pathogen recognition with Toll-like receptors. Curr. Opin. Immunol.17(4), 338–344 (2005).
  • Fritz JH, Ferrero RL, Philpott DJ, Girardin SE. Nod-like proteins in immunity, inflammation and disease. Nat. Immunol.7(12), 1250–1257 (2006).
  • Delbridge LM, O’Riordan MX. Innate recognition of intracellular bacteria. Curr. Opin. Immunol.19(1), 10–16 (2007).
  • Martinon F, Tschopp J. NLRs join TLRs as innate sensors of pathogens. Trends Immunol.26(8), 447–454 (2005).
  • Agostini L, Martinon F, Burns K, McDermott MF, Hawkins PN, Tschopp J. NALP3 forms an IL-1β-processing inflammasome with increased activity in Muckle–Wells autoinflammatory disorder. Immunity20(3), 319–325 (2004).
  • Kawai T, Akira S. Innate immune recognition of viral infection. Nat. Immunol.7(2), 131–137 (2006).
  • Kato H, Takeuchi O, Sato S et al. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature441(7089), 101–105 (2006).
  • Hornung V, Ellegast J, Kim S et al. 5´-triphosphate RNA is the ligand for RIG-I. Science314(5801), 994–997 (2006).
  • Pichlmair A, Schulz O, Tan CP et al. RIG-I-mediated antiviral responses to single-stranded RNA bearing 5´-phosphates. Science314(5801), 997–1001 (2006).
  • Janeway CA Jr, Medzhitov R. Innate immune recognition. Annu. Rev. Immunol.20, 197–216 (2002).
  • Foti M, Granucci F, Pelizzola M, Beretta O, Ricciardi-Castagnoli P. Dendritic cells in pathogen recognition and induction of immune responses: a functional genomics approach. J. Leukoc. Biol.79(5), 913–916 (2006).
  • Shortman K, Naik SH. Steady-state and inflammatory dendritic-cell development. Nat. Rev. Immunol.7(1), 19–30 (2007).
  • Bell D, Young JW, Banchereau J. Dendritic cells. Adv. Immunol.72, 255–324 (1999).
  • Vremec D, Pooley J, Hochrein H, Wu L, Shortman K. CD4 and CD8 expression by dendritic cell subtypes in mouse thymus and spleen. J. Immunol.164(6), 2978–2986 (2000).
  • Heath WR, Belz GT, Behrens GM et al. Cross-presentation, dendritic cell subsets, and the generation of immunity to cellular antigens. Immunol. Rev.199, 9–26 (2004).
  • Yewdell JW, Haeryfar SM. Understanding presentation of viral antigens to CD8+ T cells in vivo: the key to rational vaccine design. Annu. Rev. Immunol.23, 651–682 (2005).
  • Liu YJ. IPC: professional type 1 interferon-producing cells and plasmacytoid dendritic cell precursors. Annu. Rev. Immunol.23, 275–306 (2005).
  • Katze MG, He Y, Gale M Jr. Viruses and interferon: a fight for supremacy. Nat. Rev. Immunol.2(9), 675–687 (2002).
  • Biron CA, Nguyen KB, Pien GC, Cousens LP, Salazar-Mather TP. Natural killer cells in antiviral defense: function and regulation by innate cytokines. Annu. Rev. Immunol.17, 189–220 (1999).
  • Le Bon A, Durand V, Kamphuis E et al. Direct stimulation of T cells by type I IFN enhances the CD8+ T cell response during cross-priming. J. Immunol.176(8), 4682–4689 (2006).
  • Gavin AL, Hoebe K, Duong B et al. Adjuvant-enhanced antibody responses in the absence of Toll-like receptor signaling. Science314(5807), 1936–1938 (2006).
  • Pulendran B. Division of labor and cooperation between dendritic cells. Nat. Immunol.7(7), 699–700 (2006).
  • Schlecht G, Garcia S, Escriou N, Freitas AA, Leclerc C, Dadaglio G. Murine plasmacytoid dendritic cells induce effector/memory CD8+ T-cell responses in vivo after viral stimulation. Blood104(6), 1808–1815 (2004).
  • Krug A, Veeraswamy R, Pekosz A et al. Interferon-producing cells fail to induce proliferation of naive T cells but can promote expansion and T helper 1 differentiation of antigen-experienced unpolarized T cells. J. Exp. Med.197(7), 899–906 (2003).
  • Reis e Sousa C. Activation of dendritic cells: translating innate into adaptive immunity. Curr. Opin. Immunol.16(1), 21–25 (2004).
  • Lund JM, Linehan MM, Iijima N, Iwasaki A. Cutting edge: plasmacytoid dendritic cells provide innate immune protection against mucosal viral infection in situ. J. Immunol.177(11), 7510–7514 (2006).
  • Allan RS, Smith CM, Belz GT et al. Epidermal viral immunity induced by CD8α+ dendritic cells but not by Langerhans cells. Science301(5641), 1925–1928 (2003).
  • Allan RS, Waithman J, Bedoui S et al. Migratory dendritic cells transfer antigen to a lymph node-resident dendritic cell population for efficient CTL priming. Immunity25(1), 153–162 (2006).
  • Williams MA, Bevan MJ. Effector and memory CTL differentiation. Annu. Rev. Immunol.25, 171–192 (2007).
  • Mescher MF, Curtsinger JM, Agarwal P et al. Signals required for programming effector and memory development by CD8+ T cells. Immunol. Rev.211, 81–92 (2006).
  • Chang JT, Palanivel VR, Kinjyo I et al. Asymmetric T lymphocyte division in the initiation of adaptive immune responses. Science315(5819), 1687–1691 (2007).
  • Romagnani S. Regulation of the T cell response. Clin. Exp. Allergy36(11), 1357–1366 (2006).
  • Pulendran B, Ahmed R. Translating innate immunity into immunological memory: implications for vaccine development. Cell124(4), 849–863 (2006).
  • Kaech SM, Ahmed R. Memory CD8+ T cell differentiation: initial antigen encounter triggers a developmental program in naive cells. Nat. Immunol.2(5), 415–422 (2001).
  • van Stipdonk MJ, Lemmens EE, Schoenberger SP. Naive CTLs require a single brief period of antigenic stimulation for clonal expansion and differentiation. Nat. Immunol.2(5), 423–429 (2001).
  • Bevan MJ, Fink PJ. The CD8 response on autopilot. Nat. Immunol.2(5), 381–382 (2001).
  • Wherry EJ, Barber DL, Kaech SM, Blattman JN, Ahmed R. Antigen-independent memory CD8 T cells do not develop during chronic viral infection. Proc. Natl Acad. Sci. USA101(45), 16004–16009 (2004).
  • Bajenoff M, Wurtz O, Guerder S. Repeated antigen exposure is necessary for the differentiation, but not the initial proliferation, of naive CD4(+) T cells. J. Immunol.168(4), 1723–1729 (2002).
  • Obst R, van Santen HM, Mathis D, Benoist C. Antigen persistence is required throughout the expansion phase of a CD4(+) T cell response. J. Exp. Med.201(10), 1555–1565 (2005).
  • Shrikant P, Khoruts A, Mescher MF. CTLA-4 blockade reverses CD8+ T cell tolerance to tumor by a CD4+ T cell- and IL-2-dependent mechanism. Immunity11(4), 483–493 (1999).
  • Quezada SA, Jarvinen LZ, Lind EF, Noelle RJ. CD40/CD154 interactions at the interface of tolerance and immunity. Annu. Rev. Immunol.22, 307–328 (2004).
  • Janssen EM, Lemmens EE, Wolfe T, Christen U, von Herrath MG, Schoenberger SP. CD4+ T cells are required for secondary expansion and memory in CD8+ T lymphocytes. Nature421(6925), 852–856 (2003).
  • Sun JC, Williams MA, Bevan MJ. CD4+ T cells are required for the maintenance, not programming, of memory CD8+ T cells after acute infection. Nat. Immunol.5(9), 927–933 (2004).
  • Snapper CM, Paul WE. Interferon-γ and B cell stimulatory factor-1 reciprocally regulate Ig isotype production. Science236(4804), 944–947 (1987).
  • Cazac BB, Roes J. TGF-β receptor controls B cell responsiveness and induction of IgA in vivo. Immunity13(4), 443–451 (2000).
  • Coffman RL, Lebman DA, Shrader B. Transforming growth factor β specifically enhances IgA production by lipopolysaccharide-stimulated murine B lymphocytes. J. Exp. Med.170(3), 1039–1044 (1989).
  • Sonoda E, Matsumoto R, Hitoshi Y et al. Transforming growth factor β induces IgA production and acts additively with interleukin 5 for IgA production. J. Exp. Med.170(4), 1415–1420 (1989).
  • Schittek B, Rajewsky K. Maintenance of B-cell memory by long-lived cells generated from proliferating precursors. Nature346(6286), 749–751 (1990).
  • Maruyama M, Lam KP, Rajewsky K. Memory B-cell persistence is independent of persisting immunizing antigen. Nature407(6804), 636–642 (2000).
  • McHeyzer-Williams LJ, McHeyzer-Williams MG. Antigen-specific memory B cell development. Annu. Rev. Immunol.23, 487–513 (2005).
  • Kleindienst P, Brocker T. Concerted antigen presentation by dendritic cells and B cells is necessary for optimal CD4 T-cell immunity in vivo. Immunology115(4), 556–564 (2005).
  • Dooms H, Abbas AK. Control of CD4+ T-cell memory by cytokines and costimulators. Immunol. Rev.211, 23–38 (2006).
  • Rogers PR, Song J, Gramaglia I, Killeen N, Croft M. OX40 promotes Bcl-xL and Bcl-2 expression and is essential for long-term survival of CD4 T cells. Immunity15(3), 445–455 (2001).
  • Ramon G. Sur l’augmentation anormale de l’antitoxine chez leschevaux producteurs de serum antidiphterique. Bull. Soc. Centr. Med. Vet.101, 227–234 (1925).
  • Kumar S, Jones TR, Oakley MS et al. CpG oligodeoxynucleotide and Montanide ISA 51 adjuvant combination enhanced the protective efficacy of a subunit malaria vaccine. Infect. Immun.72(2), 949–957 (2004).
  • Cooper CL, Davis HL, Morris ML et al. CPG 7909, an immunostimulatory TLR9 agonist oligodeoxynucleotide, as adjuvant to Engerix-B HBV vaccine in healthy adults: a double-blind Phase I/II study. J. Clin. Immunol.24(6), 693–701 (2004).
  • Storni T, Ruedl C, Schwarz K, Schwendener RA, Renner WA, Bachmann MF. Nonmethylated CG motifs packaged into virus-like particles induce protective cytotoxic T cell responses in the absence of systemic side effects. J. Immunol.172(3), 1777–1785 (2004).
  • Boland G, Beran J, Lievens M et al. Safety and immunogenicity profile of an experimental hepatitis B vaccine adjuvanted with AS04. Vaccine23(3), 316–320 (2004).
  • Skeiky YA, Alderson MR, Ovendale PJ et al. Differential immune responses and protective efficacy induced by components of a tuberculosis polyprotein vaccine, Mtb72F, delivered as naked DNA or recombinant protein. J. Immunol.172(12), 7618–7628 (2004).
  • Schellack C, Prinz K, Egyed A et al. IC31, a novel adjuvant signaling via TLR9, induces potent cellular and humoral immune responses. Vaccine24(26), 5461–5472 (2006).
  • Agger EM, Rosenkrands I, Olsen AW et al. Protective immunity to tuberculosis with Ag85B-ESAT-6 in a synthetic cationic adjuvant system IC31. Vaccine24(26), 5452–5460 (2006).
  • Eickhoff TC, Myers M. Workshop summary. Aluminum in vaccines. Vaccine20(Suppl. 3), S1–S4 (2002).
  • Lindblad EB. Aluminium adjuvants – in retrospect and prospect. Vaccine22(27–28), 3658–3668 (2004).
  • HogenEsch H. Mechanisms of stimulation of the immune response by aluminum adjuvants. Vaccine20(Suppl. 3), S34–S39 (2002).
  • Brewer JM. (How) do aluminium adjuvants work? Immunol. Lett.102(1), 10–15 (2006).
  • Gupta RK, Chang AC, Griffin P, Rivera R, Siber GR. In vivo distribution of radioactivity in mice after injection of biodegradable polymer microspheres containing 14C-labeled tetanus toxoid. Vaccine14(15), 1412–1416 (1996).
  • Gallucci S, Lolkema M, Matzinger P. Natural adjuvants: endogenous activators of dendritic cells. Nat. Med.5(11), 1249–1255 (1999).
  • Near KA, Stowers AW, Jankovic D, Kaslow DC. Improved immunogenicity and efficacy of the recombinant 19-kilodalton merozoite surface protein 1 by the addition of oligodeoxynucleotide and aluminum hydroxide gel in a murine malaria vaccine model. Infect. Immun.70(2), 692–701 (2002).
  • Xiao Y, Aldaz-Carroll L, Ortiz AM et al. A protein-based smallpox vaccine protects mice from vaccinia and ectromelia virus challenges when given as a prime and single boost. Vaccine25(7), 1214–1224 (2007).
  • Weeratna R, Comanita L, Davis HL. CPG ODN allows lower dose of antigen against hepatitis B surface antigen in BALB/c mice. Immunol. Cell Biol.81(1), 59–62 (2003).
  • Alderson MR, McGowan P, Baldridge JR, Probst P. TLR4 agonists as immunomodulatory agents. J. Endotoxin Res.12(5), 313–319 (2006).
  • Nevens F, Zuckerman JN, Burroughs AK et al. Immunogenicity and safety of an experimental adjuvanted hepatitis B candidate vaccine in liver transplant patients. Liver Transpl.12(10), 1489–1495 (2006).
  • Hasan MS, Agosti JM, Reynolds KK , Tanzman E, Treanor JJ, Evans TG. Granulocyte macrophage colony-stimulating factor as an adjuvant for hepatitis B vaccination of healthy adults. J. Infect. Dis.180(6), 2023–2026 (1999).
  • Evans TG, Hasan M, Galibert L, Caron D. The use of Flt3 ligand as an adjuvant for hepatitis B vaccination of healthy adults. Vaccine21(3–4), 322–329 (2002).
  • Giannini SL, Hanon E, Moris P et al. Enhanced humoral and memory B cellular immunity using HPV16/18 L1 VLP vaccine formulated with the MPL/aluminium salt combination (AS04) compared to aluminium salt only. Vaccine24(33–34), 5937–5949 (2006).
  • Frazer I. God’s gift to women: the human papillomavirus vaccine. Immunity25(2), 179–184 (2006).
  • Stanberry LR, Spruance SL, Cunningham AL et al. Glycoprotein-D-adjuvant vaccine to prevent genital herpes. N. Engl. J. Med.347(21), 1652–1661 (2002).
  • Moschos SA, Bramwell VW, Somavarapu S, Alpar HO. Modulating the adjuvanticity of alum by co-administration of muramyl di-peptide (MDP) or Quil-A. Vaccine24(8), 1081–1086 (2006).
  • Edell D, Bruce E, Hale K, Khoshoo V. Reduced long-term respiratory morbidity after treatment of respiratory syncytial virus bronchiolitis with ribavirin in previously healthy infants: a preliminary report. Pediatr. Pulmonol.25(3), 154–158 (1998).
  • Puri N, Sinko PJ. Adjuvancy enhancement of muramyl dipeptide by modulating its release from a physicochemically modified matrix of ovalbumin microspheres. II. In vivo investigation. J. Control Release69(1), 69–80 (2000).
  • Inohara N, Nunez G. NODs: intracellular proteins involved in inflammation and apoptosis. Nat. Rev. Immunol.3(5), 371–382 (2003).
  • Car BD, Eng VM, Lipman JM, Anderson TD. The toxicology of interleukin-12: a review. Toxicol. Pathol.27(1), 58–63 (1999).
  • Salem ML, Gillanders WE, Kadima AN et al. Review: novel nonviral delivery approaches for interleukin-12 protein and gene systems: curbing toxicity and enhancing adjuvant activity. J. Interferon Cytokine Res.26(9), 593–608 (2006).
  • Jankovic D, Caspar P, Zweig M et al. Adsorption to aluminum hydroxide promotes the activity of IL-12 as an adjuvant for antibody as well as type 1 cytokine responses to HIV-1 gp120. J. Immunol.159(5), 2409–2417 (1997).
  • Wang S, Liu X, Caulfield MJ. Adjuvant synergy in the response to hepatitis B vaccines. Vaccine21(27–30), 4297–4306 (2003).
  • O’Hagan DT, Rappuoli R. Novel approaches to vaccine delivery. Pharm. Res.21(9), 1519–1530 (2004).
  • Granoff DM, McHugh YE, Raff HV, Mokatrin AS, Van Nest GA. MF59 adjuvant enhances antibody responses of infant baboons immunized with Haemophilus influenzae type b and Neisseria meningitidis group C oligosaccharide-CRM197 conjugate vaccine. Infect. Immun.65(5), 1710–1715 (1997).
  • Podda A, Del Giudice G. MF59-adjuvanted vaccines: increased immunogenicity with an optimal safety profile. Expert Rev. Vaccines2(2), 197–203 (2003).
  • Aucouturier J, Dupuis L, Deville S, Ascarateil S, Ganne V. Montanide ISA 720 and 51: a new generation of water in oil emulsions as adjuvants for human vaccines. Expert Rev. Vaccines1(1), 111–118 (2002).
  • Dupuis M, McDonald DM, Ott G. Distribution of adjuvant MF59 and antigen gD2 after intramuscular injection in mice. Vaccine18(5–6), 434–439 (1999).
  • Dupuis M, Murphy TJ, Higgins D et al. Dendritic cells internalize vaccine adjuvant after intramuscular injection. Cell Immunol.186(1), 18–27 (1998).
  • Vajdy M, Selby M, Medina-Selby A et al. Hepatitis C virus polyprotein vaccine formulations capable of inducing broad antibody and cellular immune responses. J. Gen. Virol.87(Pt 8), 2253–2262 (2006).
  • O’Hagan DT, Singh M, Kazzaz J et al. Synergistic adjuvant activity of immunostimulatory DNA and oil/water emulsions for immunization with HIV p55 gag antigen. Vaccine20(27–28), 3389–3398 (2002).
  • Graham BS, Keefer MC, McElrath MJ et al. Safety and immunogenicity of a candidate HIV-1 vaccine in healthy adults: recombinant glycoprotein (rgp) 120. A randomized, double-blind trial. NIAID AIDS Vaccine Evaluation Group. Ann. Intern. Med.125(4), 270–279 (1996).
  • Ahlers JD, Belyakov IM, Terabe M et al. A push–pull approach to maximize vaccine efficacy: abrogating suppression with an IL-13 inhibitor while augmenting help with granulocyte/macrophage colony-stimulating factor and CD40L. Proc. Natl Acad. Sci. USA99(20), 13020–13025 (2002).
  • Jeamwattanalert P, Mahakunkijcharoen Y, Kittigul L, Mahannop P, Pichyangkul S, Hirunpetcharat C. Long-lasting protective immune response to the 19-kilodalton carboxy-terminal fragment of plasmodium yoelii merozoite surface protein 1 in mice. Clin. Vaccine Immunol.14(4), 342–347 (2007).
  • Roohvand F, Aghasadeghi MR, Sadat SM, Budkowska A, Khabiri AR. HCV core protein immunization with Montanide/CpG elicits strong Th1/Th2 and long-lived CTL responses. Biochem. Biophys. Res. Commun.354(3), 641–649 (2007).
  • Ahlers JD, Belyakov IM, Matsui S, Berzofsky JA. Signals delivered through TCR instruct IL-12 receptor (IL-12R) expression: IL-12 and tumor necrosis factor-α synergize for IL-12R expression at low antigen dose. Int. Immunol.13(11), 1433–1442 (2001).
  • Skene CD, Sutton P. Saponin-adjuvanted particulate vaccines for clinical use. Methods40(1), 53–59 (2006).
  • 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).
  • Newman MJ, Wu JY, Gardner BH et al. Induction of cross-reactive cytotoxic T-lymphocyte responses specific for HIV-1 gp120 using saponin adjuvant (QS-21) supplemented subunit vaccine formulations. Vaccine15(9), 1001–1007 (1997).
  • Kim YJ, Wang P, Navarro-Villalobos M, Rohde BD, Derryberry J, Gin DY. Synthetic studies of complex immunostimulants from Quillaja saponaria: synthesis of the potent clinical immunoadjuvant QS-21Aapi. J. Am. Chem. Soc.128(36), 11906–11915 (2006).
  • Macete E, Aponte JJ, Guinovart C et al. Safety and immunogenicity of the RTS,S/AS02A candidate malaria vaccine in children aged 1–4 in Mozambique. Trop. Med. Int. Health12(1), 37–46 (2007).
  • Stewart VA, McGrath SM, Walsh DS et al. Pre-clinical evaluation of new adjuvant formulations to improve the immunogenicity of the malaria vaccine RTS,S/AS02A. Vaccine24(42–43), 6483–6492 (2006).
  • Ha SJ, Park SH, Kim HJ et al. Enhanced immunogenicity and protective efficacy with the use of interleukin-12-encapsulated microspheres plus AS01B in tuberculosis subunit vaccination. Infect. Immun.74(8), 4954–4959 (2006).
  • Sanders MT, Brown LE, Deliyannis G, Pearse MJ. ISCOM-based vaccines: the second decade. Immunol. Cell Biol.83(2), 119–128 (2005).
  • Andersen CS, Dietrich J, Agger EM, Lycke NY, Lovgren K, Andersen P. The combined CTA1-DD/ISCOMs vector is an effective intranasal adjuvant for boosting prior Mycobacterium bovis BCG immunity to Mycobacterium tuberculosis. Infect. Immun.75(1), 408–416 (2007).
  • Boyle J, Eastman D, Millar C et al. The utility of ISCOMATRIX™ adjuvant for dose reduction of antigen for vaccines requiring antibody responses. Vaccine25(14), 2541–2544 (2007).
  • Smith RE, Donachie AM, Grdic D, Lycke N, Mowat AM. Immune-stimulating complexes induce an IL-12-dependent cascade of innate immune responses. J. Immunol.162(9), 5536–5546 (1999).
  • Robson NC, Beacock-Sharp H, Donachie AM, Mowat AM. Dendritic cell maturation enhances CD8+ T-cell responses to exogenous antigen via a proteasome-independent mechanism of major histocompatibility complex class I loading. Immunology109(3), 374–383 (2003).
  • Windon RG, Chaplin PJ, Beezum L et al. Induction of lymphocyte recruitment in the absence of a detectable immune response. Vaccine19(4–5), 572–578 (2000).
  • Warger T, Osterloh P, Rechtsteiner G et al. Synergistic activation of dendritic cells by combined Toll-like receptor ligation induces superior CTL responses in vivo. Blood108(2), 544–550 (2006).
  • Ahonen CL, Doxsee CL, McGurran SM et al. Combined TLR and CD40 triggering induces potent CD8+ T cell expansion with variable dependence on type I IFN. J. Exp. Med.199(6), 775–784 (2004).
  • Chavan R, Marfatia KA, An IC, Garber DA, Feinberg MB. Expression of CCL20 and granulocyte-macrophage colony-stimulating factor, but not Flt3-L, from modified vaccinia virus ankara enhances antiviral cellular and humoral immune responses. J. Virol.80(15), 7676–7687 (2006).
  • Ahlers JD, Belyakov IM, Matsui S, Berzofsky JA. Mechanisms of cytokine synergy essential for vaccine protection against viral challenge. Int. Immunol.13(7), 897–908 (2001).
  • Jiang W, Baker HJ, Smith BF. Mucosal immunization with helicobacter, CpG DNA, and cholera toxin is protective. Infect. Immun.71(1), 40–46 (2003).
  • Berry LJ, Hickey DK, Skelding KA et al. Transcutaneous immunization with combined cholera toxin and CpG adjuvant protects against Chlamydia muridarum genital tract infection. Infect. Immun.72(2), 1019–1028 (2004).
  • Vajdy M. Generation and maintenance of mucosal memory B cell responses? Curr. Med. Chem.13(25), 3023–3037 (2006).
  • Peppoloni S, Ruggiero P, Contorni M et al. Mutants of the Escherichia coli heat-labile enterotoxin as safe and strong adjuvants for intranasal delivery of vaccines. Expert Rev. Vaccines2(2), 285–293 (2003).
  • Baudner BC, Balland O, Giuliani MM et al. Enhancement of protective efficacy following intranasal immunization with vaccine plus a nontoxic LTK63 mutant delivered with nanoparticles. Infect. Immun.70(9), 4785–4790 (2002).
  • Singh M, Briones M, O’Hagan DT. A novel bioadhesive intranasal delivery system for inactivated influenza vaccines. J. Control Release70(3), 267–276 (2001).
  • Kang SM, Yao Q, Guo L, Compans RW. Mucosal immunization with virus-like particles of simian immunodeficiency virus conjugated with cholera toxin subunit B. J. Virol.77(18), 9823–9830 (2003).
  • Agren L, Sverremark E, Ekman L et al. The ADP-ribosylating CTA1-DD adjuvant enhances T cell-dependent and independent responses by direct action on B cells involving anti-apoptotic Bcl-2- and germinal center-promoting effects. J. Immunol.164(12), 6276–6286 (2000).
  • Mowat AM, Donachie AM, Jagewall S et al. CTA1-DD-immune stimulating complexes: a novel, rationally designed combined mucosal vaccine adjuvant effective with nanogram doses of antigen. J. Immunol.167(6), 3398–3405 (2001).
  • Wiker HG, Mustafa T, Malen H, Riise AM. Vaccine approaches to prevent tuberculosis. Scand. J. Immunol.64(3), 243–250 (2006).
  • Skeiky YA, Sadoff JC. Advances in tuberculosis vaccine strategies. Nat. Rev. Microbiol.4(6), 469–476 (2006).
  • Staats HF, Bradney CP, Gwinn WM et al. Cytokine requirements for induction of systemic and mucosal CTL after nasal immunization. J. Immunol.167(9), 5386–5394 (2001).
  • Bradney CP, Sempowski GD, Liao HX, Haynes BF, Staats HF. Cytokines as adjuvants for the induction of anti-human immunodeficiency virus peptide immunoglobulin G (IgG) and IgA antibodies in serum and mucosal secretions after nasal immunization. J. Virol.76(2), 517–524 (2002).
  • Staats HF, Ennis FA Jr. IL-1 is an effective adjuvant for mucosal and systemic immune responses when coadministered with protein immunogens. J. Immunol.162(10), 6141–6147 (1999).
  • Moschos SA, Bramwell VW, Somavarapu S, Alpar HO. Comparative immunomodulatory properties of a chitosan-MDP adjuvant combination following intranasal or intramuscular immunisation. Vaccine23(16), 1923–1930 (2005).
  • van der Lubben IM, Verhoef JC, Borchard G, Junginger HE. Chitosan and its derivatives in mucosal drug and vaccine delivery. Eur. J. Pharm. Sci.14(3), 201–207 (2001).
  • Zaharoff DA, Rogers CJ, Hance KW, Schlom J, Greiner JW. Chitosan solution enhances both humoral and cell-mediated immune responses to subcutaneous vaccination. Vaccine25(11), 2085–2094 (2007).
  • Gurunathan S, Klinman DM, Seder RA. DNA vaccines: immunology application, and optimization. Annu. Rev. Immunol.18, 927–974 (2000).
  • Polack FP, Lee SH, Permar S et al. Successful DNA immunization against measles: neutralizing antibody against either the hemagglutinin or fusion glycoprotein protects rhesus macaques without evidence of atypical measles. Nat. Med.6(7), 776–781 (2000).
  • Barouch DH. Rational design of gene-based vaccines. J. Pathol.208(2), 283–289 (2006).
  • Corr M, Tighe H. Plasmid DNA vaccination: mechanism of antigen presentation. Springer Semin. Immunopathol.19(2), 139–145 (1997).
  • Sumida SM, McKay PF, Truitt DM et al. Recruitment and expansion of dendritic cells in vivo potentiate the immunogenicity of plasmid DNA vaccines. J. Clin. Invest.114(9), 1334–1342 (2004).
  • Encke J, Bernardin J, Geib J, Barbakadze G, Bujdoso R, Stremmel W. Genetic vaccination with Flt3-L and GM-CSF as adjuvants: Enhancement of cellular and humoral immune responses that results in protective immunity in a murine model of hepatitis C virus infection. World J. Gastroenterol.12(44), 7118–7125 (2006).
  • Pulendran B, Banchereau J, Burkeholder S et al. Flt3-ligand and granulocyte colony-stimulating factor mobilize distinct human dendritic cell subsets in vivo. J. Immunol.165(1), 566–572 (2000).
  • Mwangi W, Brown WC, Lewin HA et al. DNA-encoded fetal liver tyrosine kinase 3 ligand and granulocyte macrophage-colony-stimulating factor increase dendritic cell recruitment to the inoculation site and enhance antigen-specific CD4+ T cell responses induced by DNA vaccination of outbred animals. J. Immunol.169(7), 3837–3846 (2002).
  • Iwasaki A, Stiernholm BJ, Chan AK, Berinstein NL, Barber BH. Enhanced CTL responses mediated by plasmid DNA immunogens encoding costimulatory molecules and cytokines. J. Immunol.158(10), 4591–4601 (1997).
  • Robinson HL, Montefiori DC, Villinger F et al. Studies on GM-CSF DNA as an adjuvant for neutralizing Ab elicited by a DNA/MVA immunodeficiency virus vaccine. Virology352(2), 285–294 (2006).
  • Ahlers JD, Belyakov IM, Berzofsky JA. Cytokine, chemokine, and costimulatory molecule modulation to enhance efficacy of HIV vaccines. Curr. Mol. Med.3(3), 285–301 (2003).
  • Burger JA, Mendoza RB, Kipps TJ. Plasmids encoding granulocyte–macrophage colony-stimulating factor and CD154 enhance the immune response to genetic vaccines. Vaccine19(15–16), 2181–2189 (2001).
  • Kennedy NJ, Spithill TW, Tennent J, Wood PR, Piedrafita D. DNA vaccines in sheep: CTLA-4 mediated targeting and CpG motifs enhance immunogenicity in a DNA prime/protein boost strategy. Vaccine24(7), 970–979 (2006).
  • Ramshaw IA, Andrew ME, Phillips SM, Boyle DB, Coupar BE. Recovery of immunodeficient mice from a vaccinia virus/IL-2 recombinant infection. Nature329(6139), 545–546 (1987).
  • Dale CJ, De Rose R, Wilson KM et al. Evaluation in macaques of HIV-1 DNA vaccines containing primate CpG motifs and fowlpoxvirus vaccines co-expressing IFNγ or IL-12. Vaccine23(2), 188–197 (2004).
  • Bembridge GP, Lopez JA, Cook R, Melero JA, Taylor G. Recombinant vaccinia virus coexpressing the F protein of respiratory syncytial virus (RSV) and interleukin-4 (IL-4) does not inhibit the development of RSV-specific memory cytotoxic T lymphocytes, whereas priming is diminished in the presence of high levels of IL-2 or γ interferon. J. Virol.72(5), 4080–4087 (1998).
  • Konig P, Beer M, Makoschey B et al. Recombinant virus-expressed bovine cytokines do not improve efficacy of a bovine herpesvirus 1 marker vaccine strain. Vaccine22(2), 202–212 (2003).
  • Cooper DA, Workman C, Puls RL et al. Randomised, placebo-controlled, Phase1/2a evaluation of the safety, biological activity and antiretroviral properties of an avipox virus vaccine expressing HIV gag–pol and interferon-γ in HIV-1 infected subjects. In: 11th Annual Conference on the Retroviruses and Opportunistic Infections. CA, USA (2004).
  • Emery S, Workman C, Puls RL et al. Randomized, placebo-controlled, Phase I/IIa evaluation of the safety and immunogenicity of fowlpox virus expressing HIV gag–pol and interferon-γ in HIV-1 infected subjects. Hum. Vaccin.1(6), 232–238 (2005).
  • Abaitua F, Rodriguez JR, Garzon A, Rodriguez D, Esteban M. Improving recombinant MVA immune responses: potentiation of the immune responses to HIV-1 with MVA and DNA vectors expressing Env and the cytokines IL-12 and IFN-γ. Virus Res.116(1–2), 11–20 (2006).
  • Oh S, Berzofsky JA, Burke DS, Waldmann TA, Perera LP. Coadministration of HIV vaccine vectors with vaccinia viruses expressing IL-15 but not IL-2 induces long-lasting cellular immunity. Proc. Natl Acad. Sci. USA100(6), 3392–3397 (2003).
  • Hovav AH, Fishman Y, Bercovier H. γ interferon and monophosphoryl lipid A- trehalose dicorynomycolate are efficient adjuvants for Mycobacterium tuberculosis multivalent acellular vaccine. Infect. Immun.73(1), 250–257 (2005).
  • Bennekov T, Dietrich J, Rosenkrands I , Stryhn A, Doherty TM, Andersen P. Alteration of epitope recognition pattern in Ag85B and ESAT-6 has a profound influence on vaccine-induced protection against Mycobacterium tuberculosis. Eur. J. Immunol.36(12), 3346–3355 (2006).
  • Naito T, Kaneko Y, Kozbor D. Oral vaccination with modified vaccinia virus Ankara attached covalently to TMPEG-modified cationic liposomes overcomes pre-existing poxvirus immunity from recombinant vaccinia immunization. J. Gen. Virol.88(Pt 1), 61–70 (2007).
  • Grgacic EV, Anderson DA. Virus-like particles: passport to immune recognition. Methods40(1), 60–65 (2006).
  • Young KR, McBurney SP, Karkhanis LU, Ross TM. Virus-like particles: designing an effective AIDS vaccine. Methods40(1), 98–117 (2006).
  • Wagner R, Teeuwsen VJ, Deml L et al. Cytotoxic T cells and neutralizing antibodies induced in rhesus monkeys by virus-like particle HIV vaccines in the absence of protection from SHIV infection. Virology245(1), 65–74 (1998).
  • O’Neill E, Martinez I, Villinger F et al. Protection by SIV VLP DNA prime/protein boost following mucosal SIV challenge is markedly enhanced by IL-12/GM-CSF co-administration. J. Med. Primatol.31(4–5), 217–227 (2002).
  • Oh YK, Sohn T, Park JS et al. Enhanced mucosal and systemic immunogenicity of human papillomavirus-like particles encapsidating interleukin-2 gene adjuvant. Virology328(2), 266–273 (2004).
  • Toka FN, Gierynska M, Suvas S, Schoenberger SP, Rouse BT. Rescue of memory CD8+ T cell reactivity in peptide/TLR9 ligand immunization by codelivery of cytokines or CD40 ligation. Virology331(1), 151–158 (2005).
  • Myers L, Lee SW, Rossi RJ et al. Combined CD137 (4–1BB) and adjuvant therapy generates a developing pool of peptide-specific CD8 memory T cells. Int. Immunol.18(2), 325–333 (2006).
  • Bolesta E, Kowalczyk A, Wierzbicki A et al. Increased level and longevity of protective immune responses induced by DNA vaccine expressing the HIV-1 Env glycoprotein when combined with IL-21 and IL-15 gene delivery. J. Immunol.177(1), 177–191 (2006).
  • Holm C, Nyvold CG, Paludan SR, Thomsen AR, Hokland M. Interleukin-21 mRNA expression during virus infections. Cytokine33(1), 41–45 (2006).
  • WHO. Meeting of the Immunization Strategic Advisory Group of Experts, November 2006 – conclusions and recommendations. Wkly Epidemiol. Rec.82(1–2), 1–16 (2007).
  • Young D, Dye C. The development and impact of tuberculosis vaccines. Cell124(4), 683–687 (2006).
  • McMichael AJ. HIV vaccines. Annu. Rev. Immunol.24, 227–255 (2006).
  • Bembridge GP, Rodriguez N, Garcia-Beato R, Nicolson C, Melero JA, Taylor G. Respiratory syncytial virus infection of gene gun vaccinated mice induces Th2-driven pulmonary eosinophilia even in the absence of sensitisation to the fusion (F) or attachment (G) protein. Vaccine19(9–10), 1038–1046 (2000).
  • Kornbluth RS, Stone GW. Immunostimulatory combinations: designing the next generation of vaccine adjuvants. J. Leukoc. Biol.80(5), 1084–1102 (2006).

Website

  • GlaxoSmithKline. GSK reports significant advance in H5N1 pandemic influenza vaccine programme. Press Release. July 26, 2006, London, UK and Rixensart, Belgium www.gsk.com/controllerservlet?appid=4&pageid=402&newsid=868

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