Vaccine adjuvants: Putting innate immunity to work

Immunity

Volumn 33, Issue 4, 2010, Pages 492-503

  Coffman, Robert L ^a   Sher, Alan ^b   Seder, Robert A ^b  

^a Dynavax Technologies Corporation   (United States)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALUMINUM POTASSIUM SULFATE; AS 01; AS 01B; AS 02; AS 02A; AS 03; AS 04; CAF 01; CORD FACTOR; CPG OLIGODEOXYNUCLEOTIDE; FLAGELLIN; FREUND ADJUVANT; HYBRID PROTEIN; IC 31; IMIQUIMOD; IMMUNOLOGICAL ADJUVANT; INFLAMMASOME; ISCOM; LIPOSOME; LIQUID PARAFFIN; MINERAL OIL; MYELOID DIFFERENTIATION FACTOR 88; N ACETYLMURAMYLALANYL DEXTRO ISOGLUTAMINYLALANYL DIPALMITOYLPHOSPHATIDYLETHANOLAMINE; PATTERN RECOGNITION RECEPTOR; PHOSPHORYL LIPID A; POLYINOSINIC POLYCYTIDYLIC ACID; QB 10; QS 21; QUIL A; SAPONIN DERIVATIVE; SQUALENE; SURFACTANT; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 5; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 8; TOLL LIKE RECEPTOR 9; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1; UNCLASSIFIED DRUG; UNINDEXED DRUG;

ADAPTIVE IMMUNITY; ANTIBODY RESPONSE; ANTIGEN PRESENTING CELL; CELLULAR IMMUNITY; CYTOKINE PRODUCTION; DRUG EFFECT; DRUG MECHANISM; DRUG RESPONSE; EMULSION; HUMAN; INNATE IMMUNITY; NONHUMAN; PRIORITY JOURNAL; REVIEW;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; ANTIGEN-PRESENTING CELLS; HUMANS; IMMUNITY, CELLULAR; IMMUNITY, HUMORAL; IMMUNITY, INNATE; MODELS, ANIMAL; RNA HELICASES; TOLL-LIKE RECEPTORS; VACCINES;

EID: 77958498224     PISSN: 10747613     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.immuni.2010.10.002     Document Type: Review

References (118)

1. Alexopoulou L., Holt A.C., Medzhitov R., Flavell R.A. Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 2001, 413:732-738.
2. Amanna I.J., Carlson N.E., Slifka M.K. Duration of humoral immunity to common viral and vaccine antigens. N. Engl. J. Med. 2007, 357:1903-1915.
3. Antonelli L.R., Gigliotti Rothfuchs A., Goncalves R., Roffe E., Cheever A.W., Bafica A., Salazar A.M., Feng C.G., Sher A. Intranasal Poly-IC treatment exacerbates tuberculosis in mice through the pulmonary recruitment of a pathogen-permissive monocyte/macrophage population. J. Clin. Invest. 2010, 120:1674-1682.
4. Banzhoff A., Gasparini R., Laghi-Pasini F., Staniscia T., Durando P., Montomoli E., Capecchi P.L., di Giovanni P., Sticchi L., Gentile C., et al. MF59-adjuvanted H5N1 vaccine induces immunologic memory and heterotypic antibody responses in non-elderly and elderly adults. PLoS ONE 2009, 4:e4384.
5. Bedoui S., Whitney P.G., Waithman J., Eidsmo L., Wakim L., Caminschi I., Allan R.S., Wojtasiak M., Shortman K., Carbone F.R., et al. Cross-presentation of viral and self antigens by skin-derived CD103+ dendritic cells. Nat. Immunol. 2009, 10:488-495.
6. Beran J. Safety and immunogenicity of a new hepatitis B vaccine for the protection of patients with renal insufficiency including pre-haemodialysis and haemodialysis patients. Expert Opin. Biol. Ther. 2008, 8:235-247.
7. Beutler B.A. TLRs and innate immunity. Blood 2009, 113:1399-1407.
8. Blanco P., Palucka A.K., Gill M., Pascual V., Banchereau J. Induction of dendritic cell differentiation by IFN-alpha in systemic lupus erythematosus. Science 2001, 294:1540-1543.
9. Blander J.M., Medzhitov R. Toll-dependent selection of microbial antigens for presentation by dendritic cells. Nature 2006, 440:808-812.
10. Blasius A.L., Beutler B. Intracellular toll-like receptors. Immunity 2010, 32:305-315.
11. Boyle J., Eastman D., Millar C., Camuglia S., Cox J., Pearse M., Good J., Drane D. The utility of ISCOMATRIX adjuvant for dose reduction of antigen for vaccines requiring antibody responses. Vaccine 2007, 25:2541-2544.
12. Campbell J.D., Cho Y., Foster M.L., Kanzler H., Kachura M.A., Lum J.A., Ratcliffe M.J., Sathe A., Leishman A.J., Bahl A., et al. CpG-containing immunostimulatory DNA sequences elicit TNF-alpha-dependent toxicity in rodents but not in humans. J. Clin. Invest. 2009, 119:2564-2576.
13. Casella C.R., Mitchell T.C. Putting endotoxin to work for us: monophosphoryl lipid A as a safe and effective vaccine adjuvant. Cell. Mol. Life Sci. 2008, 65:3231-3240.
14. Chen W.H., Kozlovsky B.F., Effros R.B., Grubeck-Loebenstein B., Edelman R., Sztein M.B. Vaccination in the elderly: an immunological perspective. Trends Immunol. 2009, 30:351-359.
15. Davey G.M., Wojtasiak M., Proietto A.I., Carbone F.R., Heath W.R., Bedoui S. Cutting edge: Priming of CD8 T cell immunity to herpes simplex virus type 1 requires cognate TLR3 expression in vivo. J. Immunol. 2010, 184:2243-2246.
16. Davis I.D., Chen W., Jackson H., Parente P., Shackleton M., Hopkins W., Chen Q., Dimopoulos N., Luke T., Murphy R., et al. Recombinant NY-ESO-1 protein with ISCOMATRIX adjuvant induces broad integrated antibody and CD4(+) and CD8(+) T cell responses in humans. Proc. Natl. Acad. Sci. USA 2004, 101:10697-10702.
17. 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.
18. Diebold S.S., Kaisho T., Hemmi H., Akira S., Reis e Sousa C. Innate antiviral responses by means of TLR7-mediated recognition of single-stranded RNA. Science 2004, 303:1529-1531.
19. Dupuis M., Murphy T.J., Higgins D., Ugozzoli M., van Nest G., Ott G., McDonald D.M. Dendritic cells internalize vaccine adjuvant after intramuscular injection. Cell. Immunol. 1998, 186:18-27.
20. Eisenbarth S.C., Colegio O.R., O'Connor W., Sutterwala F.S., Flavell R.A. Crucial role for the Nalp3 inflammasome in the immunostimulatory properties of aluminium adjuvants. Nature 2008, 453:1122-1126.
21. Fearon D.T., Locksley R.M. The instructive role of innate immunity in the acquired immune response. Science 1996, 272:50-53.
22. Fritz J.H., Le Bourhis L., Sellge G., Magalhaes J.G., Fsihi H., Kufer T.A., Collins C., Viala J., Ferrero R.L., Girardin S.E., Philpott D.J. Nod1-mediated innate immune recognition of peptidoglycan contributes to the onset of adaptive immunity. Immunity 2007, 26:445-459.
23. Gale M., Foy E.M. Evasion of intracellular host defence by hepatitis C virus. Nature 2005, 436:939-945.
24. 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. USA 2009, 106:7962-7967.
25. Galli G., Medini D., Borgogni E., Zedda L., Bardelli M., Malzone C., Nuti S., Tavarini S., Sammicheli C., Hilbert A.K., et al. Adjuvanted H5N1 vaccine induces early CD4+ T cell response that predicts long-term persistence of protective antibody levels. Proc. Natl. Acad. Sci. USA 2009, 106:3877-3882.
26. Gavin A.L., Hoebe K., Duong B., Ota T., Martin C., Beutler B., Nemazee D. Adjuvant-enhanced antibody responses in the absence of toll-like receptor signaling. Science 2006, 314:1936-1938.
27. Gorden K.B., Gorski K.S., Gibson S.J., Kedl R.M., Kieper W.C., Qiu X., Tomai M.A., Alkan S.S., Vasilakos J.P. Synthetic TLR agonists reveal functional differences between human TLR7 and TLR8. J. Immunol. 2005, 174:1259-1268.
28. Gowen B.B., Wong M.H., Jung K.H., Sanders A.B., Mitchell W.M., Alexopoulou L., Flavell R.A., Sidwell R.W. TLR3 is essential for the induction of protective immunity against Punta Toro Virus infection by the double-stranded RNA (dsRNA), poly(I:C12U), but not Poly(I:C): Differential recognition of synthetic dsRNA molecules. J. Immunol. 2007, 178:5200-5208.
29. *0201 transgenic mice. PLoS ONE 2009, 4:e6950.
30. Haas T., Metzger J., Schmitz F., Heit A., Muller T., Latz E., Wagner H. The DNA sugar backbone 2' deoxyribose determines Toll-like receptor 9 activation. Immunity 2008, 28:315-323.
31. Halperin S.A., Dobson S., McNeil S., Langley J.M., Smith B., McCall-Sani R., Levitt D., Nest G.V., Gennevois D., Eiden J.J. Comparison of the safety and immunogenicity of hepatitis B virus surface antigen co-administered with an immunostimulatory phosphorothioate oligonucleotide and a licensed hepatitis B vaccine in healthy young adults. Vaccine 2006, 24:20-26.
32. Heil F., Ahmad-Nejad P., Hemmi H., Hochrein H., Ampenberger F., Gellert T., Dietrich H., Lipford G., Takeda K., Akira S., et al. The Toll-like receptor 7 (TLR7)-specific stimulus loxoribine uncovers a strong relationship within the TLR7, 8 and 9 subfamily. Eur. J. Immunol. 2003, 33:2987-2997.
33. Heil F., Hemmi H., Hochrein H., Ampenberger F., Kirschning C., Akira S., Lipford G., Wagner H., Bauer S. Species-specific recognition of single-stranded RNA via toll-like receptor 7 and 8. Science 2004, 303:1526-1529.
34. Heit A., Maurer T., Hochrein H., Bauer S., Huster K.M., Busch D.H., Wagner H. Cutting edge: Toll-like receptor 9 expression is not required for CpG DNA-aided cross-presentation of DNA-conjugated antigens but essential for cross-priming of CD8 T cells. J. Immunol. 2003, 170:2802-2805.
35. Hemmi H., Kaisho T., Takeuchi O., Sato S., Sanjo H., Hoshino K., Horiuchi T., Tomizawa H., Takeda K., Akira S. Small anti-viral compounds activate immune cells via the TLR7 MyD88-dependent signaling pathway. Nat. Immunol. 2002, 3:196-200.
36. Hornung V., Bauernfeind F., Halle A., Samstad E.O., Kono H., Rock K.L., Fitzgerald K.A., Latz E. Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nat. Immunol. 2008, 9:847-856.
37. Hou B., Reizis B., DeFranco A.L. Toll-like receptors activate innate and adaptive immunity by using dendritic cell-intrinsic and -extrinsic mechanisms. Immunity 2008, 29:272-282.
38. Huleatt J.W., Jacobs A.R., Tang J., Desai P., Kopp E.B., Huang Y., Song L., Nakaar V., Powell T.J. Vaccination with recombinant fusion proteins incorporating Toll-like receptor ligands induces rapid cellular and humoral immunity. Vaccine 2007, 25:763-775.
39. Ishikawa E., Ishikawa T., Morita Y.S., Toyonaga K., Yamada H., Takeuchi O., Kinoshita T., Akira S., Yoshikai Y., Yamasaki S. Direct recognition of the mycobacterial glycolipid, trehalose dimycolate, by C-type lectin Mincle. J. Exp. Med. 2009, 206:2879-2888.
40. Iwasaki A., Medzhitov R. Toll-like receptor control of the adaptive immune responses. Nat. Immunol. 2004, 5:987-995.
41. Iwasaki A., Medzhitov R. Regulation of adaptive immunity by the innate immune system. Science 2010, 327:291-295.
42. Iyer S.S., Pulskens W.P., Sadler J.J., Butter L.M., Teske G.J., Ulland T.K., Eisenbarth S.C., Florquin S., Flavell R.A., Leemans J.C., Sutterwala F.S. Necrotic cells trigger a sterile inflammatory response through the Nlrp3 inflammasome. Proc. Natl. Acad. Sci. USA 2009, 106:20388-20393.
43. Jarrossay D., Napolitani G., Colonna M., Sallusto F., Lanzavecchia A. Specialization and complementarity in microbial molecule recognition by human myeloid and plasmacytoid dendritic cells. Eur. J. Immunol. 2001, 31:3388-3393.
44. Jennings G.T., Bachmann M.F. Immunodrugs: Therapeutic VLP-based vaccines for chronic diseases. Annu. Rev. Pharmacol. Toxicol. 2009, 49:303-326.
45. Joffre O., Nolte M.A., Sporri R., Reis e Sousa C. Inflammatory signals in dendritic cell activation and the induction of adaptive immunity. Immunol. Rev. 2009, 227:234-247.
46. Jongbloed S.L., Kassianos A.J., McDonald K.J., Clark G.J., Ju X., Angel C.E., Chen C.J., Dunbar P.R., Wadley R.B., Jeet V., et al. Human CD141+ (BDCA-3)+ dendritic cells (DCs) represent a unique myeloid DC subset that cross-presents necrotic cell antigens. J. Exp. Med. 2010, 207:1247-1260.
47. Jurk M., Heil F., Vollmer J., Schetter C., Krieg A.M., Wagner H., Lipford G., Bauer S. Human TLR7 or TLR8 independently confer responsiveness to the antiviral compound R-848. Nat. Immunol. 2002, 3:499.
48. Kadowaki N., Ho S., Antonenko S., Malefyt R.W., Kastelein R.A., Bazan F., Liu Y.J. Subsets of human dendritic cell precursors express different toll-like receptors and respond to different microbial antigens. J. Exp. Med. 2001, 194:863-869.
49. Kato H., Takeuchi O., Sato S., Yoneyama M., Yamamoto M., Matsui K., Uematsu S., Jung A., Kawai T., Ishii K.J., et al. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 2006, 441:101-105.
50. Kato H., Takeuchi O., Mikamo-Satoh E., Hirai R., Kawai T., Matsushita K., Hiiragi A., Dermody T.S., Fujita T., Akira S. Length-dependent recognition of double-stranded ribonucleic acids by retinoic acid-inducible gene-I and melanoma differentiation-associated gene 5. J. Exp. Med. 2008, 205:1601-1610.
51. Kawai T., Akira S. The role of pattern-recognition receptors in innate immunity: Update on Toll-like receptors. Nat. Immunol. 2010, 11:373-384.
52. Kenney R.T., Cross A.S. Adjuvants for the future. New Generation Vaccines 2010, 250-262. Informa Healthcare USA, Inc., New York. M.M. Levine, G. Dougan, M.F. Good, M.A. Liu, G.J. Nabel, J.P. Nataro, R. Rappuoli (Eds.).
53. Kester K.E., Cummings J.F., Ofori-Anyinam O., Ockenhouse C.F., Krzych U., Moris P., Schwenk R., Nielsen R.A., Debebe Z., Pinelis E., et al. Randomized, double-blind, phase 2a trial of falciparum malaria vaccines RTS,S/AS01B and RTS,S/AS02A in malaria-naive adults: Safety, efficacy, and immunologic associates of protection. J. Infect. Dis. 2009, 200:337-346.
54. Khurana S., Chearwae W., Castellino F., Manischewitz J., King L.R., Honorkiewicz A., Rock M.T., Edwards K.M., Del Giudice G., Rappuoli R., Golding H. Vaccines with MF59 adjuvant expand the antibody repertoire to target protective sites of pandemic avian H5N1 influenza virus. Sci. Transl. Med. 2010, 2:15ra15.
55. Klechevsky E., Morita R., Liu M., Cao Y., Coquery S., Thompson-Snipes L., Briere F., Chaussabel D., Zurawski G., Palucka A.K., et al. Functional specializations of human epidermal Langerhans cells and CD14+ dermal dendritic cells. Immunity 2008, 29:497-510.
56. Kobayashi H., Horner A.A., Takabayashi K., Nguyen M.D., Huang E., Cinman N., Raz E. Immunostimulatory DNA pre-priming: A novel approach for prolonged Th1-biased immunity. Cell. Immunol. 1999, 198:69-75.
57. 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.
58. Lambrecht B.N., Kool M., Willart M.A., Hammad H. Mechanism of action of clinically approved adjuvants. Curr. Opin. Immunol. 2009, 21:23-29.
59. Le Bon A., Thompson C., Kamphuis E., Durand V., Rossmann C., Kalinke U., Tough D.F. Cutting edge: Enhancement of antibody responses through direct stimulation of B and T cells by type I IFN. J. Immunol. 2006, 176:2074-2078.
60. Leroux-Roels I., Roman F., Forgus S., Maes C., De Boever F., Drame M., Gillard P., van der Most R., Van Mechelen M., Hanon E., Leroux-Roels G. Priming with AS03 A-adjuvanted H5N1 influenza vaccine improves the kinetics, magnitude and durability of the immune response after a heterologous booster vaccination: An open non-randomised extension of a double-blind randomised primary study. Vaccine 2010, 28:849-857.
61. Levy H.B., Baer G., Baron S., Buckler C.E., Gibbs C.J., Iadarola M.J., London W.T., Rice J. A modified polyriboinosinic-polyribocytidylic acid complex that induces interferon in primates. J. Infect. Dis. 1975, 132:434-439.
62. Li H., Nookala S., Re F. Aluminum hydroxide adjuvants activate caspase-1 and induce IL-1beta and IL-18 release. J. Immunol. 2007, 178:5271-5276.
63. Longhi M.P., Trumpfheller C., Idoyaga J., Caskey M., Matos I., Kluger C., Salazar A.M., Colonna M., Steinman R.M. Dendritic cells require a systemic type I interferon response to mature and induce CD4+ Th1 immunity with poly IC as adjuvant. J. Exp. Med. 2009, 206:1589-1602.
64. Lore K., Betts M.R., Brenchley J.M., Kuruppu J., Khojasteh S., Perfetto S., Roederer M., Seder R.A., Koup R.A. Toll-like receptor ligands modulate dendritic cells to augment cytomegalovirus- and HIV-1-specific T cell responses. J. Immunol. 2003, 171:4320-4328.
65. Lund J.M., Alexopoulou L., Sato A., Karow M., Adams N.C., Gale N.W., Iwasaki A., Flavell R.A. Recognition of single-stranded RNA viruses by Toll-like receptor 7. Proc. Natl. Acad. Sci. USA 2004, 101:5598-5603.
66. Malherbe L., Mark L., Fazilleau N., McHeyzer-Williams L.J., McHeyzer-Williams M.G. Vaccine adjuvants alter TCR-based selection thresholds. Immunity 2008, 28:698-709.
67. Maraskovsky E., Schnurr M., Wilson N.S., Robson N.C., Boyle J., Drane D. Development of prophylactic and therapeutic vaccines using the ISCOMATRIX adjuvant. Immunol. Cell Biol. 2009, 87:371-376.
68. Marrack P., McKee A.S., Munks M.W. Towards an understanding of the adjuvant action of aluminium. Nat. Rev. Immunol. 2009, 9:287-293.
69. Marshall J.D., Higgins D., Abbate C., Yee P., Teshima G., Ott G., dela Cruz T., Passmore D., Fearon K.L., Tuck S., Van Nest G. Polymyxin B enhances ISS-mediated immune responses across multiple species. Cell. Immunol. 2004, 229:93-105.
70. Martinon F., Mayor A., Tschopp J. The inflammasomes: Guardians of the body. Annu. Rev. Immunol. 2009, 27:229-265.
71. Mascola J.R., Stiegler G., VanCott T.C., Katinger H., Carpenter C.B., Hanson C.E., Beary H., Hayes D., Frankel S.S., Birx D.L., Lewis M.G. Protection of macaques against vaginal transmission of a pathogenic HIV-1/SIV chimeric virus by passive infusion of neutralizing antibodies. Nat. Med. 2000, 6:207-210.
72. Mata-Haro V., Cekic C., Martin M., Chilton P.M., Casella C.R., Mitchell T.C. The vaccine adjuvant monophosphoryl lipid A as a TRIF-biased agonist of TLR4. Science 2007, 316:1628-1632.
73. Mbow M.L., De Gregorio E., Valiante N.M., Rappuoli R. New adjuvants for human vaccines. Curr. Opin. Immunol. 2010, 22:411-416.
74. McCartney S., Vermi W., Gilfillan S., Cella M., Murphy T.L., Schreiber R.D., Murphy K.M., Colonna M. Distinct and complementary functions of MDA5 and TLR3 in poly(I:C)-mediated activation of mouse NK cells. J. Exp. Med. 2009, 206:2967-2976.
75. McDonald W.F., Huleatt J.W., Foellmer H.G., Hewitt D., Tang J., Desai P., Price A., Jacobs A., Takahashi V.N., Huang Y., et al. A West Nile virus recombinant protein vaccine that coactivates innate and adaptive immunity. J. Infect. Dis. 2007, 195:1607-1617.
76. McKee A.S., Munks M.W., Marrack P. How do adjuvants work? Important considerations for new generation adjuvants. Immunity 2007, 27:687-690.
77. McKee A.S., MacLeod M.K., Kappler J.W., Marrack P. Immune mechanisms of protection: Can adjuvants rise to the challenge?. BMC Biol. 2010, 8:37.
78. Miao E.A., Warren S.E. Innate immune detection of bacterial virulence factors via the NLRC4 inflammasome. J. Clin. Immunol. 2010, 30:502-506.
79. Moorthy V.S., Ballou W.R. Immunological mechanisms underlying protection mediated by RTS,S: A review of the available data. Malar. J. 2009, 8:312.
80. Moreira L.O., Smith A.M., DeFreitas A.A., Qualls J.E., El Kasmi K.C., Murray P.J. Modulation of adaptive immunity by different adjuvant-antigen combinations in mice lacking Nod2. Vaccine 2008, 26:5808-5813.
81. Mosca F., Tritto E., Muzzi A., Monaci E., Bagnoli F., Iavarone C., O'Hagan D., Rappuoli R., De Gregorio E. Molecular and cellular signatures of human vaccine adjuvants. Proc. Natl. Acad. Sci. USA 2008, 105:10501-10506.
82. O'Hagan D.T., De Gregorio E. The path to a successful vaccine adjuvant-'The long and winding road'. Drug Discov. Today 2009, 14:541-551.
83. O'Neill L.A., Bowie A.G. Sensing and signaling in antiviral innate immunity. Curr. Biol. 2010, 20:R328-R333.
84. Ott G., Barchfeld G.L., Chernoff D., Radhakrishnan R., van Hoogevest P., Van Nest G. MF59. Design and evaluation of a safe and potent adjuvant for human vaccines. Pharm. Biotechnol. 1995, 6:277-296.
85. Palm N.W., Medzhitov R. Immunostimulatory activity of haptenated proteins. Proc. Natl. Acad. Sci. USA 2009, 106:4782-4787.
86. Pasare C., Medzhitov R. Toll pathway-dependent blockade of CD4+CD25+ T cell-mediated suppression by dendritic cells. Science 2003, 299:1033-1036.
87. Pellegrini M., Nicolay U., Lindert K., Groth N., Della Cioppa G. MF59-adjuvanted versus non-adjuvanted influenza vaccines: Integrated analysis from a large safety database. Vaccine 2009, 27:6959-6965.
88. Plotkin S.A. Correlates of protection induced by vaccination. Clin. Vaccine Immunol. 2010, 17:1055-1065.
89. Podda A. The adjuvanted influenza vaccines with novel adjuvants: Experience with the MF59-adjuvanted vaccine. Vaccine 2001, 19:2673-2680.
90. Poulin L.F., Salio M., Griessinger E., Anjos-Afonso F., Craciun L., Chen J.L., Keller A.M., Joffre O., Zelenay S., Nye E., et al. Characterization of human DNGR-1+ BDCA3+ leukocytes as putative equivalents of mouse CD8alpha+ dendritic cells. J. Exp. Med. 2010, 207:1261-1271.
91. Pulendran B., Powell J., Flavell R.A. Modulating vaccine responses with innate immunity. New Generation Vaccines 2010, 183-190. Informa Healthcare USA, Inc., New York. M.M. Levine, G. Dougan, M.F. Good, M.A. Liu, G.J. Nabel, J.P. Nataro, R. Rappuoli (Eds.).
92. Querec T., Bennouna S., Alkan S., Laouar Y., Gorden K., Flavell R., Akira S., Ahmed R., Pulendran B. Yellow fever vaccine YF-17D activates multiple dendritic cell subsets via TLR2, 7, 8, and 9 to stimulate polyvalent immunity. J. Exp. Med. 2006, 203:413-424.
93. Qureshi N., Takayama K., Ribi E. Purification and structural determination of nontoxic lipid A obtained from the lipopolysaccharide of Salmonella typhimurium. J. Biol. Chem. 1982, 257:11808-11815.
94. Rosenberg S.A., Yang J.C., Restifo N.P. Cancer immunotherapy: Moving beyond current vaccines. Nat. Med. 2004, 10:909-915.
95. Sanders C.J., Moore D.A., Williams I.R., Gewirtz A.T. Both radioresistant and hemopoietic cells promote innate and adaptive immune responses to flagellin. J. Immunol. 2008, 180:7184-7192.
96. Schnurr M., Orban M., Robson N.C., Shin A., Braley H., Airey D., Cebon J., Maraskovsky E., Endres S. ISCOMATRIX adjuvant induces efficient cross-presentation of tumor antigen by dendritic cells via rapid cytosolic antigen delivery and processing via tripeptidyl peptidase II. J. Immunol. 2009, 182:1253-1259.
97. Schoenen H., Bodendorfer B., Hitchens K., Manzanero S., Werninghaus K., Nimmerjahn F., Agger E.M., Stenger S., Andersen P., Ruland J., et al. Cutting edge: Mincle is essential for recognition and adjuvanticity of the mycobacterial cord factor and its synthetic analog trehalose-dibehenate. J. Immunol. 2010, 184:2756-2760.
98. Schulz O., Diebold S.S., Chen M., Naslund T.I., Nolte M.A., Alexopoulou L., Azuma Y.T., Flavell R.A., Liljestrom P., Reis e Sousa C. Toll-like receptor 3 promotes cross-priming to virus-infected cells. Nature 2005, 433:887-892.
99. Schwarz T.F., Horacek T., Knuf M., Damman H.G., Roman F., Drame M., Gillard P., Jilg W. Single dose vaccination with AS03-adjuvanted H5N1 vaccines in a randomized trial induces strong and broad immune responsiveness to booster vaccination in adults. Vaccine 2009, 27:6284-6290.
100. Serre K., Mohr E., Toellner K.M., Cunningham A.F., Granjeaud S., Bird R., MacLennan I.C. Molecular differences between the divergent responses of ovalbumin-specific CD4 T cells to alum-precipitated ovalbumin compared to ovalbumin expressed by Salmonella. Mol. Immunol. 2008, 45:3558-3566.
101. Seubert A., Monaci E., Pizza M., O'Hagan D.T., Wack A. The adjuvants aluminum hydroxide and MF59 induce monocyte and granulocyte chemoattractants and enhance monocyte differentiation toward dendritic cells. J. Immunol. 2008, 180:5402-5412.
102. Shenderov K., Barber D., Mayer K., Jankovic D., White S., Caspar P., Hieny S., Trinchieri G., Besra G., Cerundolo V., Sher A. Inflammasome-dependent IL-1{beta} production is critical for complete Freund's adjuvant-induced helper T cell polarization. J. Immunol. 2010, 184. 136.44.
103. Sporri R., Reis e Sousa C. Inflammatory mediators are insufficient for full dendritic cell activation and promote expansion of CD4+ T cell populations lacking helper function. Nat. Immunol. 2005, 6:163-170.
104. Stahl-Hennig C., Eisenblatter M., Jasny E., Rzehak T., Tenner-Racz K., Trumpfheller C., Salazar A.M., Uberla K., Nieto K., Kleinschmidt J., et al. Synthetic double-stranded RNAs are adjuvants for the induction of T helper 1 and humoral immune responses to human papillomavirus in rhesus macaques. PLoS Pathog. 2009, 5:e1000373.
105. Stoute J.A., Slaoui M., Heppner D.G., Momin P., Kester K.E., Desmons P., Wellde B.T., Garcon N., Krzych U., Marchand M. A preliminary evaluation of a recombinant circumsporozoite protein vaccine against Plasmodium falciparum malaria. RTS,S Malaria Vaccine Evaluation Group. N. Engl. J. Med. 1997, 336:86-91.
106. Su S.B., Silver P.B., Grajewski R.S., Agarwal R.K., Tang J., Chan C.C., Caspi R.R. Essential role of the MyD88 pathway, but nonessential roles of TLRs 2, 4, and 9, in the adjuvant effect promoting Th1-mediated autoimmunity. J. Immunol. 2005, 175:6303-6310.
107. Takeuchi O., Akira S. Pattern recognition receptors and inflammation. Cell 2010, 140:805-820.
108. Teleshova N., Kenney J., Van Nest G., Marshall J., Lifson J.D., Sivin I., Dufour J., Bohm R., Gettie A., Robbiani M. Local and systemic effects of intranodally injected CpG-C immunostimulatory-oligodeoxyribonucleotides in macaques. J. Immunol. 2006, 177:8531-8541.
109. Tighe H., Takabayashi K., Schwartz D., Van Nest G., Tuck S., Eiden J.J., Kagey-Sobotka A., Creticos P.S., Lichtenstein L.M., Spiegelberg H.L., Raz E. Conjugation of immunostimulatory DNA to the short ragweed allergen Amb a 1 enhances its immunogenicity and reduces its allergenicity. J. Allergy Clin. Immunol. 2000, 106:124-134.
110. Trinchieri G., Sher A. Cooperation of Toll-like receptor signals in innate immune defence. Nat. Rev. Immunol. 2007, 7:179-190.
111. Trumpfheller C., Caskey M., Nchinda G., Longhi M.P., Mizenina O., Huang Y., Schlesinger S.J., Colonna M., Steinman R.M. The microbial mimic poly IC induces durable and protective CD4+ T cell immunity together with a dendritic cell targeted vaccine. Proc. Natl. Acad. Sci. USA 2008, 105:2574-2579.
112. Vandepapeliere P., Horsmans Y., Moris P., Van Mechelen M., Janssens M., Koutsoukos M., Van Belle P., Clement F., Hanon E., Wettendorff M., et al. Vaccine adjuvant systems containing monophosphoryl lipid A and QS21 induce strong and persistent humoral and T cell responses against hepatitis B surface antigen in healthy adult volunteers. Vaccine 2008, 26:1375-1386.
113. Verstraeten T., Descamps D., David M.P., Zahaf T., Hardt K., Izurieta P., Dubin G., Breuer T. Analysis of adverse events of potential autoimmune aetiology in a large integrated safety database of AS04 adjuvanted vaccines. Vaccine 2008, 26:6630-6638.
114. Wang Y., Cella M., Gilfillan S., Colonna M. Cutting edge: Polyinosinic:polycytidylic acid boosts the generation of memory CD8 T cells through melanoma differentiation-associated protein 5 expressed in stromal cells. J. Immunol. 2010, 184:2751-2755.
115. Wille-Reece U., Flynn B.J., Lore K., Koup R.A., Kedl R.M., Mattapallil J.J., Weiss W.R., Roederer M., Seder R.A. HIV Gag protein conjugated to a Toll-like receptor 7/8 agonist improves the magnitude and quality of Th1 and CD8+ T cell responses in nonhuman primates. Proc. Natl. Acad. Sci. USA 2005, 102:15190-15194.
116. Wille-Reece U., Flynn B.J., Lore K., Koup R.A., Miles A.P., Saul A., Kedl R.M., Mattapallil J.J., Weiss W.R., Roederer M., Seder R.A. Toll-like receptor agonists influence the magnitude and quality of memory T cell responses after prime-boost immunization in nonhuman primates. J. Exp. Med. 2006, 203:1249-1258.
117. Wu C.C., Hayashi T., Takabayashi K., Sabet M., Smee D.F., Guiney D.D., Cottam H.B., Carson D.A. Immunotherapeutic activity of a conjugate of a Toll-like receptor 7 ligand. Proc. Natl. Acad. Sci. USA 2007, 104:3990-3995.
118. Zandman-Goddard G., Shoenfeld Y. Infections and SLE. Autoimmunity 2005, 38:473-485.