Choice and design of adjuvants for parenteral and mucosal vaccines

Vaccines

Volumn 3, Issue 1, 2015, Pages 148-171

  Savelkoul, Huub F J ^a   Ferro, Valerie A ^b   Strioga, Marius M ^c   Schijns, Virgil E J C ^a,b,d  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b UNIVERSITY OF STRATHCLYDE   (United Kingdom)

^c NATIONAL CANCER INSTITUTE   (Lithuania)

^d ERC Belgium and ERC The Netherlands   (Netherlands)

Author keywords

Adjuvant; Immunology; Mechanisms

Indexed keywords

ADJUVANT; ALUMINUM POTASSIUM SULFATE; BACTERIAL DNA; CD14 ANTIGEN; CHEMOKINE RECEPTOR CXCR4; CHEMOKINE RECEPTOR CXCR5; ENDOTOXIN; GAMMA INTERFERON; HEAT SHOCK PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 18; ISCOM; LECTIN RECEPTOR; LIPOPOLYSACCHARIDE; LIPOSOME; MEDRONIC ACID; MIFAMURTIDE; MITOGEN ACTIVATED PROTEIN KINASE; NUCLEOTIDE BINDING OLIGOMERIZATION DOMAIN LIKE RECEPTOR; NUCLEOTIDE BINDING OLIGOMERIZATION DOMAIN PROTEIN; PEPTIDOGLYCAN; RECEPTOR ACTIVITY MODIFYING PROTEIN 1; SAPONIN; SINGLE STRANDED RNA; T LYMPHOCYTE RECEPTOR; T6 ANTIGEN; UNINDEXED DRUG; VACCINE;

ANTIGEN PRESENTING CELL; CELL DIFFERENTIATION; CELLULAR IMMUNITY; CYTOKINE PRODUCTION; DRUG DESIGN; EMULSION; ENTEROTOXIGENIC ESCHERICHIA COLI; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOGENICITY; IMMUNOMODULATION; IMMUNOSTIMULATION; INFLUENZA; MUCOSAL IMMUNITY; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION;

EID: 85016866277     PISSN: None     EISSN: 2076393X     Source Type: Journal    
DOI: 10.3390/vaccines3010148     Document Type: Review

References (115)

1. O’Hagan, D.T.; Rappuoli, R. The safety of vaccines. Drug Discov. Today 2004, 9, 846-854.
2. Batista-Duharte, A.; Portuondo, D.; Perez, O.; Carlos, I.Z. Systemic immunotoxicity reactions induced by adjuvanted vaccines. Int. Immunopharmacol. 2014, 20, 170-180.
3. Subbarao, K.; Murphy, B.R.; Fauci, A.S. Development of effective vaccines against pandemic influenza. Immunity 2006, 24, 5-9.
4. Lambert, L.C.; Fauci, A.S. Influenza vaccines for the future. N. Engl. J. Med. 2010, 363, 2036-2044.
5. Bodewes, R.; Geelhoed-Mieras, M.M.; Heldens, J.G.; Glover, J.; Lambrecht, B.N.; Fouchier, R.A.; Osterhaus, A.D.; Rimmelzwaan, G.F. The novel adjuvant covaccineht increases the immunogenicity of cell-culture derived influenza a/H5N1 vaccine and induces the maturation of murine and human dendritic cells in vitro. Vaccine 2009, 27, 6833-6839.
6. Lambrecht, B.N.; Kool, M.; Willart, M.A.; Hammad, H. Mechanism of action of clinically approved adjuvants. Curr. Opin. Immunol. 2009, 21, 23-29.
7. Coffman, R.L.; Sher, A.; Seder, R.A. Vaccine adjuvants: Putting innate immunity to work. Immunity 2010, 33, 492-503.
8. Tangye, S.G.; Tarlinton, D.M. Memory B cells: Effectors of long-lived immune responses. Eur. J. Immunol. 2009, 39, 2065-2075.
9. Akbar, A.N.; Fletcher, J.M. Memory T cell homeostasis and senescence during aging. Curr. Opin. Immunol. 2005, 17, 480-485.
10. Tobin, G.J.; Trujillo, J.D.; Bushnell, R.V.; Lin, G.; Chaudhuri, A.R.; Long, J.; Barrera, J.; Pena, L.; Grubman, M.J.; Nara, P.L. Deceptive imprinting and immune refocusing in vaccine design. Vaccine 2008, 26, 6189-6199.
11. Cusi, M.G.; Martorelli, B.; di Genova, G.; Terrosi, C.; Campoccia, G.; Correale, P. Age related changes in T cell mediated immune response and effector memory to respiratory syncytial virus (RSV) in healthy subjects. Immunity Ageing 2010, doi:10.1186/1742-4933-7-14.
12. Schijns, V.E. Immunological concepts of vaccine adjuvant activity. Curr. Opin. Immunol. 2000, 12, 456-463.
13. Schijns, V.E. Mechanisms of vaccine adjuvant activity: Initiation and regulation of immune responses by vaccine adjuvants. Vaccine 2003, 21, 829-831.
14. Schijns, V.E. Induction and direction of immune responses by vaccine adjuvants. Crit. Rev. Immunol. 2001, 21, 75-85.
15. Schijns, V.E. Antigen delivery systems and immunostimulation. Vet. Immunol. Immunopathol. 2002, 87, 195-198.
16. Eksteen, B.; Mora, J.R.; Haughton, E.L.; Henderson, N.C.; Lee-Turner, L.; Villablanca, E.J.; Curbishley, S.M.; Aspinall, A.I.; von Andrian, U.H.; Adams, D.H. Gut homing receptors on CD8 T cells are retinoic acid dependent and not maintained by liver dendritic or stellate cells. Gastroenterology 2009, 137, 320-329.
17. Sigmundsdottir, H.; Pan, J.; Debes, G.F.; Alt, C.; Habtezion, A.; Soler, D.; Butcher, E.C. DCs metabolize sunlight-induced vitamin D3 to “program” T cell attraction to the epidermal chemokine CCL27. Nat. Immunol. 2007, 8, 285-293.
18. Marrack, P.; McKee, A.S.; Munks, M.W. Towards an understanding of the adjuvant action of aluminium. Nat. Rev. Immunol. 2009, 9, 287-293.
19. Bachmann, M.F.; Jennings, G.T. Vaccine delivery: A matter of size, geometry, kinetics and molecular patterns. Nat. Rev. Immunol. 2010, 10, 787-796.
20. Mitchell, D.; Yong, M.; Schroder, W.; Black, M.; Tirrell, M.; Olive, C. Dual stimulation of myd88-dependent toll-like receptors induces synergistically enhanced production of inflammatory cytokines in murine bone marrow-derived dendritic cells. J. Infect. Dis. 2010, 202, 318-329.
21. Li, H.; Willingham, S.B.; Ting, J.P.; Re, F. Cutting edge: Inflammasome activation by alum and alum’s adjuvant effect are mediated by NLRP3. J. Immunol. 2008, 181, 17-21.
22. Ulanova, M.; Tarkowski, A.; Hahn-Zoric, M.; Hanson, L.A. The common vaccine adjuvant aluminum hydroxide up-regulates accessory properties of human monocytes via an interleukin-4-dependent mechanism. Infect. Immunity 2001, 69, 1151-1159.
23. Lindblad, E.B. Aluminium compounds for use in vaccines. Immunol. Cell Biol. 2004, 82, 497-505.
24. Petrovsky, N.; Aguilar, J.C. Vaccine adjuvants: Current state and future trends. Immunol. Cell Biol. 2004, 82, 488-496.
25. Medzhitov, R.; Preston-Hurlburt, P.; Janeway, C.A., Jr. A human homologue of the drosophila toll protein signals activation of adaptive immunity. Nature 1997, 388, 394-397.
26. Petrovsky, N. Freeing vaccine adjuvants from dangerous immunological dogma. Expert Rev. Vaccines 2008, 7, 7-10.
27. Kool, M.; Soullie, T.; van Nimwegen, M.; Willart, M.A.; Muskens, F.; Jung, S.; Hoogsteden, H.C.; Hammad, H.; Lambrecht, B.N. Alum adjuvant boosts adaptive immunity by inducing uric acid and activating inflammatory dendritic cells. J. Exp. Med. 2008, 205, 869-882.
28. Al-Akl, N.S.; Chakhtoura, M.; Kazzi, N.F.; Usta, J.; Chamoun, C.A.; Abdelnoor, A.M. Uric acid: A possible mediator of the adjuvant effect of alum in mice immunized with ovalbumin. World J. Vaccines 2011, 1, 148-155.
29. Vajdy, M.; Srivastava, I.; Polo, J.; Donnelly, J.; O’Hagan, D.; Singh, M. Mucosal adjuvants and delivery systems for protein-, DNA-and RNA-based vaccines. Immunol. Cell Biol. 2004, 82, 617-627.
30. Coban, C.; Kobiyama, K.; Aoshi, T.; Takeshita, F.; Horii, T.; Akira, S.; Ishii, K.J. Novel strategies to improve DNA vaccine immunogenicity. Curr. Gene Ther. 2011, 11, 479-484.
31. Flingai, S.; Czerwonko, M.; Goodman, J.; Kudchodkar, S.B.; Muthumani, K.; Weiner, D.B. Synthetic DNA vaccines: Improved vaccine potency by electroporation and co-delivered genetic adjuvants. Front. Immunol. 2013, doi:10.3389/fimmu.2013.00354.
32. Marichal, T.; Ohata, K.; Bedoret, D.; Mesnil, C.; Sabatel, C.; Kobiyama, K.; Lekeux, P.; Coban, C.; Akira, S.; Ishii, K.J.; et al. DNA released from dying host cells mediates aluminum adjuvant activity. Nat. Med. 2011, 17, 996-1002.
33. Mattsson, J.; Yrlid, U.; Stensson, A.; Schon, K.; Karlsson, M.C.; Ravetch, J.V.; Lycke, N.Y. Complement activation and complement receptors on follicular dendritic cells are critical for the function of a targeted adjuvant. J. Immunol. 2011, 187, 3641-3652.
34. Bhardwaj, N.; Gnjatic, S.; Sawhney, N.B. TLR agonists: Are they good adjuvants? Cancer J. 2010, 16, 382-391.
35. Orr, M.T.; Beebe, E.A.; Hudson, T.E.; Moon, J.J.; Fox, C.B.; Reed, S.G.; Coler, R.N. A dual TLR agonist adjuvant enhances the immunogenicity and protective efficacy of the tuberculosis vaccine antigen ID93. PLOS ONE 2014, 9, e83884.
36. O’Hagan, D.T.; Valiante, N.M. Recent advances in the discovery and delivery of vaccine adjuvants. Nat. Rev. Drug Discov. 2003, 2, 727-735.
37. O’Hagan, D.T. New generation vaccine adjuvants. eLS 2007, doi:10.1002/9780470015902.a0020177.
38. Rappuoli, R.; Mandl, C.W.; Black, S.; de Gregorio, E. Vaccines for the twenty-first century society. Nat. Rev. Immunol. 2011, 11, 865-872.
39. Antonova, G.; Lichtenbeld, H.; Xia, T.; Chatterjee, A.; Dimitropoulou, C.; Catravas, J.D. Functional significance of hsp90 complexes with NOS and sGC in endothelial cells. Clin. Hemorheol. Microcirc. 2007, 37, 19-35.
40. Nishikawa, M.; Takemoto, S.; Takakura, Y. Heat shock protein derivatives for delivery of antigens to antigen presenting cells. Int. J. Pharm. 2008, 354, 23-27.
41. Colaco, C.A.; Bailey, C.R.; Walker, K.B.; Keeble, J. Heat shock proteins: Stimulators of innate and acquired immunity. BioMed Res. Int. 2013, doi:10.1155/2013/461230.
42. Glass, E.J. Genetic variation and responses to vaccines. Anim. Health Res. Rev. 2004, 5, 197-208.
43. Long, A.B.; Ferguson, A.M.; Majumder, P.; Nagarajan, U.M.; Boss, J.M. Conserved residues of the bare lymphocyte syndrome transcription factor RFXAP determine coordinate MHC class II expression. Mol. Immunol. 2006, 43, 395-409.
44. Evans, T.I.; Reeves, R.K. All-trans-retinoic acid imprints expression of the gut-homing marker alpha4beta7 while suppressing lymph node homing of dendritic cells. Clin. Vaccine Immunol. 2013, 20, 1642-1646.
45. Connell, T.D. Cholera toxin, LT-I, LT-IIa and LT-IIb: The critical role of ganglioside binding in immunomodulation by type I and type II heat-labile enterotoxins. Expert Rev. Vaccines 2007, 6, 821-834.
46. Sun, J.B.; Czerkinsky, C.; Holmgren, J. Mucosally induced immunological tolerance, regulatory T cells and the adjuvant effect by cholera toxin B subunit. Scandinavian J. Immunol. 2010, 71, 1-11.
47. Sun, J.B.; Eriksson, K.; Li, B.L.; Lindblad, M.; Azem, J.; Holmgren, J. Vaccination with dendritic cells pulsed in vitro with tumor antigen conjugated to cholera toxin efficiently induces specific tumoricidal CD8+ cytotoxic lymphocytes dependent on cyclic amp activation of dendritic cells. Clin. Immunol. 2004, 112, 35-44.
48. Veglia, F.; Sciaraffia, E.; Riccomi, A.; Pinto, D.; Negri, D.R.; de Magistris, M.T.; Vendetti, S. Cholera toxin impairs the differentiation of monocytes into dendritic cells, inducing professional antigen-presenting myeloid cells. Infect. Immunity 2011, 79, 1300-1310.
49. Gustafsson, T.; Hua, Y.J.; Dahlgren, M.W.; Livingston, M.; Johansson-Lindbom, B.; Yrlid, U. Direct interaction between cholera toxin and dendritic cells is required for oral adjuvant activity. Eur. J. Immunol. 2013, 43, 1779-1788.
50. Yang, Z.; Zhang, X.; Darrah, P.A.; Mosser, D.M. The regulation of th1 responses by the p38 mapk. J. Immunol. 2010, 185, 6205-6213.
51. Matsushita, N.; Komine, H.; Grolleau-Julius, A.; Pilon-Thomas, S.; Mule, J.J. Targeting marco can lead to enhanced dendritic cell motility and anti-melanoma activity. Cancer Immunol. Immunother. 2010, 59, 875-884.
52. Tovey, M.G.; Lallemand, C. Adjuvant activity of cytokines. Methods Mol. Biol. 2010, 626, 287-309.
53. Sharp, F.A.; Ruane, D.; Claass, B.; Creagh, E.; Harris, J.; Malyala, P.; Singh, M.; O’Hagan, D.T.; Petrilli, V.; Tschopp, J.; et al. Uptake of particulate vaccine adjuvants by dendritic cells activates the nalp3 inflammasome. Proc. Natl. Acad. Sci. USA 2009, 106, 870-875.
54. Mathew, S.; Lendlein, A.; Wischke, C. Characterization of protein-adjuvant coencapsulation in microparticles for vaccine delivery. Eur. J. Pharm. Biopharm. 2014, 87, 403-407.
55. Schijns, V.E.; Horzinek, M.C. Cytokines in Veterinary Medicine; CAB International: Wallingford, Oxon, UK; New York, NY, USA, 1998.
56. Schijns, V.E.; Scholtes, N.C.; Zuilekom, H.I.; Sanders, L.E.; Nicolson, L.; Argyle, D.J. Facilitation of antibody forming responses to viral vaccine antigens in young cats by recombinant baculovirus-expressed feline ifn-gamma. Vaccine 2002, 20, 1718-1724.
57. Degen, W.G.; van Zuilekom, H.I.; Scholtes, N.C.; van Daal, N.; Schijns, V.E. Potentiation of humoral immune responses to vaccine antigens by recombinant chicken IL-18 (rCHIL-18). Vaccine 2005, 23, 4212-4218.
58. Tarpey, I.; Davis, P.J.; Sondermeijer, P.; van Geffen, C.; Verstegen, I.; Schijns, V.E.; Kolodsick, J.; Sundick, R. Expression of chicken interleukin-2 by turkey herpesvirus increases the immune response against marek’s disease virus but fails to increase protection against virulent challenge. Avian Pathol. 2007, 36, 69-74.
59. Schijns, V.E.; Degen, W.G. Vaccine immunopotentiators of the future. Clin. Pharmacol. Ther. 2007, 82, 750-755.
60. Perret, R.; Sierro, S.R.; Botelho, N.K.; Corgnac, S.; Donda, A.; Romero, P. Adjuvants that improve the ratio of antigen-specific effector to regulatory t cells enhance tumor immunity. Cancer Res. 2013, 73, 6597-6608.
61. Bayry, J. Regulatory T cells as adjuvant target for enhancing the viral disease vaccine efficacy. Virusdisease 2014, 25, 18-25.
62. Maisonneuve, C.; Bertholet, S.; Philpott, D.J.; de Gregorio, E. Unleashing the potential of nod-and toll-like agonists as vaccine adjuvants. Proc. Natl. Acad. Sci. USA 2014, 111, 12294-12299.
63. Diener, K.R.; Moldenhauer, L.M.; Lyons, A.B.; Brown, M.P.; Hayball, J.D. Human Flt-3-ligand-mobilized dendritic cells require additional activation to drive effective immune responses. Exp. Hematol. 2008, 36, 51-60.
64. Johansen, P.; Mohanan, D.; Martinez-Gomez, J.M.; Kundig, T.M.; Gander, B. Lympho-geographical concepts in vaccine delivery. J. Control. Release 2010, 148, 56-62.
65. Morrow, M.P.; Yan, J.; Pankhong, P.; Ferraro, B.; Lewis, M.G.; Khan, A.S.; Sardesai, N.Y.; Weiner, D.B. Unique Th1/Th2 phenotypes induced during priming and memory phases by use of interleukin-12 (IL-12) or IL-28B vaccine adjuvants in rhesus macaques. Clin. Vaccine Immunol. 2010, 17, 1493-1499.
66. Zhou, Q.; Wang, F.; Yang, F.; Wang, Y.; Zhang, X.; Sun, S. Augmented humoral and cellular immune response of hepatitis b virus DNA vaccine by micro-needle vaccination using Flt3l as an adjuvant. Vaccine 2010, 28, 1357-1362.
67. Kaufman, H.L.; Ruby, C.E.; Hughes, T.; Slingluff, C.L., Jr. Current status of granulocyte-macrophage colony-stimulating factor in the immunotherapy of melanoma. J. Immunother. Cancer 2014, doi:10.1186/2051-1426-2-1.
68. Lee, J.B.; Jang, J.E.; Song, M.K.; Chang, J. Intranasal delivery of cholera toxin induces.
69. Th17-dominated T-cell response to bystander antigens. PLOS ONE 2009, 4, e5190.
70. Thompson, A.L.; Staats, H.F. Cytokines: The future of intranasal vaccine adjuvants. Clin. Dev. Immunol. 2011, 2011, 289597.
71. Tamura, S. Studies on the usefulness of intranasal inactivated influenza vaccines. Vaccine 2010, 28, 6393-6397.
72. Hailemichael, Y.; Dai, Z.; Jaffarzad, N.; Ye, Y.; Medina, M.A.; Huang, X.F.; Dorta-Estremera, S.M.; Greeley, N.R.; Nitti, G.; Peng, W.; et al. Persistent antigen at vaccination sites induces tumor-specific CD8+ T cell sequestration, dysfunction and deletion. Nat. Med. 2013, 19, 465-472.
73. Sandoval, F.; Terme, M.; Nizard, M.; Badoual, C.; Bureau, M.F.; Freyburger, L.; Clement, O.; Marcheteau, E.; Gey, A.; Fraisse, G.; et al. Mucosal imprinting of vaccine-induced CD8+ T cells is crucial to inhibit the growth of mucosal tumors. Sci. Transl. Med. 2013, doi:10.1126/scitranslmed.3004888.
74. Macho-Fernandez, E.; Cruz, L.J.; Ghinnagow, R.; Fontaine, J.; Bialecki, E.; Frisch, B.; Trottein, F.; Faveeuw, C. Targeted delivery of alpha-galactosylceramide to CD8alpha+ dendritic cells optimizes type I NKT cell-based antitumor responses. J. Immunol. 2014, 193, 961-969.
75. Blander, J.M.; Medzhitov, R. Toll-dependent selection of microbial antigens for presentation by dendritic cells. Nature 2006, 440, 808-812.
76. Kasturi, S.P.; Skountzou, I.; Albrecht, R.A.; Koutsonanos, D.; Hua, T.; Nakaya, H.I.; Ravindran, R.; Stewart, S.; Alam, M.; Kwissa, M.; et al. Programming the magnitude and persistence of antibody responses with innate immunity. Nature 2011, 470, 543-547.
77. Salazar, L.G.; Coveler, A.L.; Swensen, R.E.; Gooley, T.A.; Goodell, V.; Schiffman, K.; Disis, M.L. Kinetics of tumor-specific T-cell response development after active immunization in patients with HER-2/neu overexpressing cancers. Clin. Immunol. 2007, 125, 275-280.
78. Hong, C.Y.; Kim, S.Y.; Lee, H.J.; Lee, S.E.; Lim, S.C.; Rhee, J.H.; Lee, J.J. A bacterial flagellin in combination with proinflammatory cytokines activates human monocyte-derived dendritic cells to generate cytotoxic T lymphocytes having increased homing signals to cancer. J. Immunother. 2014, 37, 16-25.
79. Jansen, T.; Hofmans, M.P.; Theelen, M.J.; Manders, F.; Schijns, V.E. Structure-and oil type-based efficacy of emulsion adjuvants. Vaccine 2006, 24, 5400-5405.
80. Jansen, T.; Hofmans, M.P.; Theelen, M.J.; Schijns, V.E. Structure-activity relations of water-in-oil vaccine formulations and induced antigen-specific antibody responses. Vaccine 2005, 23, 1053-1060.
81. Del Giudice, G.; Fragapane, E.; Bugarini, R.; Hora, M.; Henriksson, T.; Palla, E.; O’Hagan, D.; Donnelly, J.; Rappuoli, R.; Podda, A. Vaccines with the MF59 adjuvant do not stimulate antibody responses against squalene. Clin. Vaccine Immunol. 2006, 13, 1010-1013.
82. Lee, S.H. Detection of human papillomavirus (HPV) l1 gene DNA possibly bound to particulate aluminum adjuvant in the hpv vaccine gardasil. J. Inorg. Biochem. 2012, 117, 85-92.
83. Didierlaurent, A.M.; Morel, S.; Lockman, L.; Giannini, S.L.; 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.
84. Hem, S.L.; Hogenesch, H. Relationship between physical and chemical properties of aluminum-containing adjuvants and immunopotentiation. Expert Rev. Vaccines 2007, 6, 685-698.
85. Yang, M.; Hearnden, C.H.; Oleszycka, E.; Lavelle, E.C. NLRP3 inflammasome activation and cytotoxicity induced by particulate adjuvants. Methods Mol. Biol. 2013, 1040, 41-63.
86. Mori, A.; Oleszycka, E.; Sharp, F.A.; Coleman, M.; Ozasa, Y.; Singh, M.; O’Hagan, D.T.; Tajber, L.; Corrigan, O.I.; McNeela, E.A.; et al. The vaccine adjuvant alum inhibits IL-12 by promoting PI3 kinase signaling while chitosan does not inhibit IL-12 and enhances Th1 and Th17 responses. Eur. J. Immunol. 2012, 42, 2709-2719.
87. Harris, J.; Sharp, F.A.; Lavelle, E.C. The role of inflammasomes in the immunostimulatory effects of particulate vaccine adjuvants. Eur. J. Immunol. 2010, 40, 634-638.
88. Lu, F.; Hogenesch, H. Kinetics of the inflammatory response following intramuscular injection of aluminum adjuvant. Vaccine 2013, 31, 3979-3986.
89. Matzinger, P. The danger model: A renewed sense of self. Science 2002, 296, 301-305.
90. Kuroda, E.; Coban, C.; Ishii, K.J. Particulate Adjuvant and Innate Immunity: Past Achievements, Present Findings, and Future Prospects. Int. Rev. Immunol. 2013, 32, 209-220.
91. Miyaji, E.N.; Carvalho, E.; Oliveira, M.L.; Raw, I.; Ho, P.L. Trends in adjuvant development for vaccines: DAMPs and PAMPs as potential new adjuvants. Braz. J. Med. Biol. Res. 2011, 44, 500-513.
92. De Gregorio, E.; Caproni, E.; Ulmer, J.B. Vaccine adjuvants: Mode of action. Front. Immunol. 2013, doi:10.3389/fimmu.2013.00214.
93. Mbow, M.L.; de Gregorio, E.; Valiante, N.M.; Rappuoli, R. New adjuvants for human vaccines. Curr. Opin. Immunol. 2010, 22, 411-416.
94. Miller, R.L.; Meng, T.C.; Tomai, M.A. The antiviral activity of toll-like receptor 7 and 7/8 agonists. Drug News Perspect. 2008, 21, 69-87.
95. Bodera, P.; Stankiewicz, W.; Kocik, J. Synthetic immunostimulatory oligonucleotides in experimental and clinical practice. Pharmacol. Rep. 2012, 64, 1003-1010.
96. Jain, V.; Vyas, S.P.; Kohli, D.V. Well-defined and potent liposomal hepatitis B vaccines adjuvanted with lipophilic mdp derivatives. Nanomed. Nanotechnol. Biol. Med. 2009, 5, 334-344.
97. Siegrist, C.A.; Pihlgren, M.; Tougne, C.; Efler, S.M.; Morris, M.L.; AlAdhami, M.J.; Cameron, D.W.; Cooper, C.L.; Heathcote, J.; Davis, H.L. ; et al. Co-administration of CpG oligonucleotides enhances the late affinity maturation process of human anti-hepatitis B vaccine response. Vaccine 2004, 23, 615-622.
98. Leroux-Roels, G. Unmet needs in modern vaccinology: Adjuvants to improve the immune response. Vaccine 2010, 28, C25-C36.
99. Duthie, M.S.; Windish, H.P.; Fox, C.B.; Reed, S.G. Use of defined TLR ligands as adjuvants within human vaccines. Immunol. Rev. 2011, 239, 178-196.
100. Nierkens, S.; den Brok, M.H.; Garcia, Z.; Togher, S.; Wagenaars, J.; Wassink, M.; Boon, L.; Ruers, T.J.; Figdor, C.G.; Schoenberger, S.P. ; et al. Immune adjuvant efficacy of CpG oligonucleotide in cancer treatment is founded specifically upon tlr9 function in plasmacytoid dendritic cells. Cancer Res. 2011, 71, 6428-6437.
101. Rappuoli, R. Conjugates and reverse vaccinology to eliminate bacterial meningitis. Vaccine 2001, 19, 2319-2322.
102. Levine, O.S.; Knoll, M.D.; Jones, A.; Walker, D.G.; Risko, N.; Gilani, Z. Global status of haemophilus influenzae type B and pneumococcal conjugate vaccines: Evidence, policies, and introductions. Curr. Opin. Infect. Dis. 2010, 23, 236-241.
103. Pasetti, M.F.; Simon, J.K.; Sztein, M.B.; Levine, M.M. Immunology of gut mucosal vaccines. Immunol. Rev. 2011, 239, 125-148.
104. Lundin, B.S.; Johansson, C.; Svennerholm, A.M. Oral immunization with a salmonella enterica serovar Typhi vaccine induces specific circulating mucosa-homing CD4+ and CD8+ T cells in humans. Infect. Immunity 2002, 70, 5622-5627.
105. Mowat, A.M. Dendritic cells and immune responses to orally administered antigens. Vaccine 2005, 23, 1797-1799.
106. Mann, J.F.; Ferro, V.A.; Mullen, A.B.; Tetley, L.; Mullen, M.; Carter, K.C.; Alexander, J.; Stimson, W.H. Optimisation of a lipid based oral delivery system containing a/panama influenza haemagglutinin. Vaccine 2004, 22, 2425-2429.
107. Gebril, A.; Alsaadi, M.; Acevedo, R.; Mullen, A.B.; Ferro, V.A. Optimizing efficacy of mucosal vaccines. Expert Rev. Vaccines 2012, 11, 1139-1155.
108. Rescigno, M. Mucosal immunology and bacterial handling in the intestine. Best Pract. Res. Clin. Gastroenterol. 2013, 27, 17-24.
109. Keijzer, C.; van der Zee, R.; van Eden, W.; Broere, F. Treg inducing adjuvants for therapeutic vaccination against chronic inflammatory diseases. Front. Immunol. 2013, doi:10.3389/fimmu.2013.00245.
110. Chen, K.; Cerutti, A. Vaccination strategies to promote mucosal antibody responses. Immunity 2010, 33, 479-491.
111. Lawson, L.B.; Norton, E.B.; Clements, J.D. Defending the mucosa: Adjuvant and carrier formulations for mucosal immunity. Curr. Opin. Immunol. 2011, 23, 414-420.
112. Read, R.C.; Naylor, S.C.; Potter, C.W.; Bond, J.; Jabbal-Gill, I.; Fisher, A.; Illum, L.; Jennings, R. Effective nasal influenza vaccine delivery using chitosan. Vaccine 2005, 23, 4367-4374.
113. Baaten, B.J.; Clarke, B.; Strong, P.; Hou, S. Nasal mucosal administration of chitin microparticles boosts innate immunity against influenza a virus in the local pulmonary tissue. Vaccine 2010, 28, 4130-4137.
114. Bolhassani, A.; Javanzad, S.; Saleh, T.; Hashemi, M.; Aghasadeghi, M.R.; Sadat, S.M. Polymeric nanoparticles: Potent vectors for vaccine delivery targeting cancer and infectious diseases. Hum. Vaccines Immunother. 2014, 10, 321-332.
115. Rhee, J.H.; Lee, S.E.; Kim, S.Y. Mucosal vaccine adjuvants update. Clin. Exp. Vaccine Res. 2012, 1, 50-63.