An overview of adjuvants utilized in prophylactic vaccine formulation as immunomodulators

References

• O’Hagan DT. New generation vaccine adjuvants. Encyclopedia of Life Sciences. 1–7.
   Google Scholar
• Mohan T, Verma P, Nageswara Rao D. Novel adjuvants & delivery vehicles for vaccines development: A road ahead. Ind J Med Res. 2013;138:779–795.
   PubMed Web of Science ®Google Scholar
• Petrovsky N, Cooper PD. Carbohydrate-based immune adjuvants. Expert Rev Vaccines. 2011;10(4):523–537.
   PubMed Web of Science ®Google Scholar
• Kreuter J. Nanoparticles as adjuvants for vaccines. Chapter: Vaccine Design, Pharmaceutical Biotechnology. 1995;6:463–472.
   PubMedGoogle Scholar
• Chang M, Shi Y, Nail SL, et al. Degree of antigen adsorption in the vaccine or interstitial fluid and its effect on the antibody response in rabbits. Vaccine. 2001;19:2884–2889.
   PubMed Web of Science ®Google Scholar
• Tritto E, Mosca F, De Gregorio E. Mechanism of action of licensed vaccine adjuvants. Vaccine. 2009;27:3331–3334.
   PubMed Web of Science ®Google Scholar
• Vogel FR. Improving vaccine performance with adjuvants. Clin Infect Dis. 2000;30:S266–S270.
   PubMed Web of Science ®Google Scholar
• Coler RN, Bertholet S, Moutaftsi M, et al. Development and characterization of synthetic glucopyranosyl lipid adjuvant system as a vaccine adjuvant. Plos One. 2011;6:e16333.
   PubMed Web of Science ®Google Scholar
• Treuel L, Jiang X, Nienhaus GU. New views on cellular uptake and trafficking of manufactured nanoparticles. J Royal Soc Interface. 2013;10:20120939.
   PubMed Web of Science ®Google Scholar
• Manolova V, Flace A, Bauer M, et al. Nanoparticles target distinct dendritic cell populations according to their size. Eur J Immunol. 2008;38(5):1404–1413.
   PubMed Web of Science ®Google Scholar
• Wang W, Singh M. Selection of adjuvants for enhanced vaccine potency. World J Vaccine. 2011;1:33–78.
   Google Scholar
• Petrovsky N, Aguilar JC. Vaccine adjuvants: current state and future trends. Immunol Cell Biol. 2004;82:488–496.
   PubMed Web of Science ®Google Scholar
• Song X, Hu S. Adjuvant activities of saponins from traditional Chinese medicinal herbs. Vaccine. 2009;27:4883–4890.
   PubMed Web of Science ®Google Scholar
• Sivakumar SM, Safhi MM, Kannadasan M, et al. Vaccine adjuvants – Current status and prospects on controlled release adjuvanticity. Saudi Pharm J. 2011;19:197–206.
   PubMed Web of Science ®Google Scholar
• Edelman R. Vaccine Adjuvants. Res Infect Dis. 1980;2:370–383.
   PubMedGoogle Scholar
• Neutra MR, Pringault E, Kraehenbuhl JP. Antigen sampling across epithelial barriers and induction of mucosal immune responses. Annu Rev Immunol. 1996;14:275–300.
   PubMed Web of Science ®Google Scholar
• Lindblad EB. Aluminium compounds for use in vaccines. Immunol Cell Biol. 2004;82:497–505.
   PubMed Web of Science ®Google Scholar
• Byars NE, Allison AC. Immunologic adjuvants: general properties, advantages and limitations. laboratory methods in immunology. Boca Raton: CRC Press; 1990. p. 39–51.
   Google Scholar
• Burrell LS, White JL, Hem SL. Stability of aluminium-containing adjuvants during aging at room temperature. Vaccine. 2000;18:2188–2192.
   PubMed Web of Science ®Google Scholar
• Wu JY, Gardner BH, Kushner NN, et al. Accessory cell requirements for saponin adjuvant–induced class I MHC antigen–restricted cytotoxic T lymphocytes. Cell Immunol. 1994;154:393–406.
   PubMed Web of Science ®Google Scholar
• Awate S, Babiuk LA, Mutwiri G. Mechanisms of action of adjuvants. Front Immunol. 2013;4:114.
   PubMed Web of Science ®Google Scholar
• Zhou F, Huang L. Liposome-mediated cytoplasmic delivery of proteins: an effective means of accessing the MHC class I–restricted antigen presentation pathway. Immuno-Methods. 1994;4:229–235.
   PubMedGoogle Scholar
• Dupuis M, Murphy TJ, Higgins D, et al. Dendritic cells internalize vaccine adjuvant after intramuscular injection. Cell Immunol. 1998;186:18–27.
   PubMed Web of Science ®Google Scholar
• Newman MJ, Wu YJ, Gardner BH, et al. Saponin adjuvant induction of ovalbumin-specific CD81 cytotoxic T lymphocyte responses. J Immunol. 1992;148:2357–2362.
   PubMed Web of Science ®Google Scholar
• Takahashi H, Takashita T, Morein B, et al. Induction of CD81 cytotoxic cells by immunization with purified HIV1 envelope protein in ISCOMs. Nature. 1990;344:873–875.
   PubMed Web of Science ®Google Scholar
• Babu JS, Nair P, Kanda P, et al. Priming for virus-specific CD81 but notCD41 cytotoxic T lymphocytes with synthetic lipopeptide is influenced by acylation units and liposome encapsulation. Vaccine. 1995;13:1669–1676.
   PubMed Web of Science ®Google Scholar
• Powers DC, Manning MC, Hanscome PJ, et al. Cytotoxic T-lymphocyte responses to a liposome adjuvanted influenza A virus vaccine in the elderly. J Infect Dis. 1995;172:1103–1107.
   PubMed Web of Science ®Google Scholar
• White WI, Cassatt DR, Madsen J, et al. Antibody and cytotoxic T lymphocyte responses to a single liposome-associated peptide antigen. Vaccine. 1995;13:1111–1122.
   PubMed Web of Science ®Google Scholar
• Audibert FM, Lise LD. Adjuvants: current status, clinical perspectives and future prospects. Immunol Today. 1993;14:281–284.
   PubMedGoogle Scholar
• Grun JL, Maurer PH. Different T helper cell subsets elicited in mice utilizing two different adjuvant vehicles: the role of endogenous interleukin 1 in proliferative responses. Cell Immunol. 1989;121:134–145.
   PubMed Web of Science ®Google Scholar
• Xu-Amano J, Kiyono H, Jackson RJ, et al. Helper T cell subsets for immunoglobulin A responses: oral immunization with tetanus toxoid and cholera toxin as adjuvant selectively induces Th2 cells in mucosa associated tissues. J Exp Med. 1993;178:1309–1320.
   PubMed Web of Science ®Google Scholar
• Allison AC. The mode of action of immunological adjuvants. Dev Biol Stand. 1998;92:3–11.
   PubMedGoogle Scholar
• Unkeless JC, Scigliano E, Freedman VH. Structure and function of human and murine receptors for IgG. Annu Rev Immunol. 1988;6:251–281.
   PubMed Web of Science ®Google Scholar
• Phillips NC, Emili A. Enhanced antibody responses to liposome-associated protein antigens: preferential stimulation of IgG2a/b production. Vaccine. 1992;10:151–158.
   PubMed Web of Science ®Google 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. Vaccine. 1999;17:2517–2527.
   PubMed Web of Science ®Google Scholar
• 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. 1997;159:2409–2417.
   PubMed Web of Science ®Google Scholar
• Wilson AD, Robinson A, Irons L, et al. Adjuvant action of cholera toxin and pertussis toxin in the induction of IgA antibody response to orally administered antigen. Vaccine. 1993;11:113–118.
   PubMed Web of Science ®Google Scholar
• Lindsay DS, Parton R, Wardlaw AC. Adjuvant effect of pertussis toxin on the production of anti-ovalbumin IgE in mice and lack of direct correlation between PCA and ELISA. Int Arch Allergy Immunol. 1994;105:281–288.
   PubMed Web of Science ®Google Scholar
• Coffman RL, Sher A, Seder RA. Vaccine adjuvants: putting Innate immunity to work. Immunity. 2010;33(4):492–503.
   PubMed Web of Science ®Google Scholar
• Alpar HO, Bowen JC, Brown MRW. Effectiveness of liposomes as adjuvants of orally and nasally administered tetanus toxoid. Int J Pharm. 1992;88:335–344.
   Web of Science ®Google Scholar
• Walker RI. New strategies for using mucosal vaccination to achieve more effective immunization. Vaccine. 1994;12:387–400.
   PubMed Web of Science ®Google Scholar
• Allison AC, Byars NE. Immunological adjuvants: desirable properties and side-effects. Mol Immunol. 1991;28:279–284.
   PubMed Web of Science ®Google Scholar
• Waters RV, Terrell TG, Jones GH. Uveitis induction in the rabbit by muramyl dipeptides. Infect Immun. 1986;51:816–825.
   PubMed Web of Science ®Google Scholar
• Goldenthal KL, Cavagnaro JA, Alving CR, et al. Safety evaluation of vaccine adjuvants. national cooperative vaccine development working group. AIDS Res Hum Retroviruses. 1993;9:S45–9.
   Web of Science ®Google Scholar
• Petrovsky N. Freeing vaccine adjuvants from dangerous immunological dogma. Expert Rev Vaccines. 2008;7(1):7–10.
   PubMed Web of Science ®Google Scholar
• Butler NR, Voyce MA, Burland WL, et al. Advantages of aluminium hydroxide adsorbed combined diphtheria, tetanus, and pertussis vaccines for the immunization of infants. Br Med J. 1969;1(645):663–666.
   PubMed Web of Science ®Google Scholar
• Cherin P, Gherardi RK. Emergence of a new entity, the macrophagic myofasciitis. GERMMAD study group of the french association against myopathies study and research group on acquired dysimmunity-related muscle disease. Rev Rhum Engl Ed. 1998;65(10):541–542.
   PubMedGoogle Scholar
• Aghazadeh-Habashi A, Kohan MH, Asghar W, et al. Glucosamine dose/concentration-effect correlation in the rat with adjuvant arthritis. J Pharmac Sci. 2014;103(2):760–767.
   PubMed Web of Science ®Google Scholar
• Petrovsky N. Comparative safety of vaccine adjuvants: a summary of current evidence and future needs. Drug Saf. 2015;38(11):1059–1074.
   PubMed Web of Science ®Google Scholar
• Aiyer Harini P, Ashok Kumar HG, Praveen Kumar G, et al. An overview of immunologic adjuvants - a review. J Vaccines Vaccin. 2013;4:167.
   Google Scholar
• Walls RS. Eosinophil response to alum adjuvants. involvement of T cells in non-antigen-dependent mechanisms. Proc Soc Exp Biol Medical. 1977;156:431–435.
   PubMed Web of Science ®Google Scholar
• Relyveld EH, Hencoq E, Raynaud M. Etude de la vaccination antidiphterique de sujets alergiques avec une anatoxine pure adsorbee sur phosphate de calcium. Bull WHO. 1964;30:321–325.
   PubMedGoogle Scholar
• Gupta RK, Siber GR. Adjuvants for human vaccines-current status, problems and future prospects. Vaccine. 1995;13:1263–1276.
   PubMed Web of Science ®Google Scholar
• Relyveld EH. Preparation and use of calcium phosphate adsorbed vaccines. Dev Biol Stand. 1986;65:131–136.
   PubMedGoogle Scholar
• Jackson LR, Fox JG. Institutional policies and guidelines on adjuvants and antibody production. Ilar J. 1995;37:141–150.
   PubMedGoogle Scholar
• Bomford R. The comparative selectivity of adjuvants for humoral and cell-mediated immunity. II. effect on delayed-type hypersensitivity in the mouse and guinea pig, and cell-mediated immunity to tumour antigens in the mouse of Freund’s incomplete and complete adjuvants, alhydrogel, corynebacterium parvum, Bordetella pertussis, muramyl dipeptide and saponin. Clin Exp Immunol. 1980;39:435–441.
   PubMed Web of Science ®Google Scholar
• Orozco-Morales M, Sánchez-García FJ, Guevara-Salazar P, et al. Adjuvant immunotherapy of C6 glioma in rats with pertussis toxin. J Cancer Res Clin Oncol. 2012;138:23–33.
   PubMed Web of Science ®Google Scholar
• Ghose C, Kalsy A, Sheikh A, et al. Transcutaneous immunization with Clostridium difficile toxoid A induces systemic and mucosal immune responses and toxin A-neutralizing antibodies in mice. Infect Immun. 2007;75:2826–2832.
   PubMed Web of Science ®Google Scholar
• Katre NV. Liposome-based depot injection technologies; how versatile are they? Am J Drug Deliv. 2004;2:213–227.
   Google Scholar
• Fossum C, Bergström M, Lövgren K, et al. Effect of ISCOMs and their adjuvant moiety (matrix) on the initial proliferation and IL-2 responses: comparison of spleen cells from mice inoculated with iscoms and/or matrix. Cell Immunol. 1990;129:414–425.
   PubMed Web of Science ®Google Scholar
• Mukherjee C, Mäkinen K, Savolainen J, et al. Chemistry and biology of oligo valent β-(1→2)-linked oligomannosides: new insights into carbohydrate-based adjuvants in immunotherapy. Chemistry. 2013;19:7961–7974.
   PubMed Web of Science ®Google Scholar
• Yang D, Biragyn A, Hoover DM, et al. Multiple roles of antimicrobial defensins, cathelicidins, and eosinophil-derived neurotoxin in host defense. Annu Rev Immunol. 2004;22:181–215.
   PubMed Web of Science ®Google Scholar
• Yang D, Biragyn A, Kwak LW, et al. Mammalian defensins in immunity: more than just microbicidal. Trends Immunol. 2002;23:291–296.
   PubMed Web of Science ®Google Scholar
• Mohan T, Mitra D, Rao DN. Nasal delivery of PLG micro particle encapsulated defensin peptides adjuvanted gp41 antigen confers strong and long-lasting immunoprotective response against HIV-1. Immunol Res. 2014;58(1):139–153.
   Web of Science ®Google Scholar
• LeBon A, Schiavoni G, D’Agostino G, et al. Type-I interferons potently enhance humoral immunity and can promote isotype switching by stimulating dendritic cells in-vivo. Immunity. 2001;14:461–470.
   PubMed Web of Science ®Google Scholar
• Staats HF, Ennis FA, Jr IL-1. is an effective adjuvant for mucosal and systemic immune responses when co-administered with protein immunogens. J Immunol. 1999;162:6141–6147.
   PubMed Web of Science ®Google Scholar
• Huffnagle GB, Strieter RM, McNeil LK, et al. Macrophage inflammatory protein-1α (MIP-1α) is required for the efferent phase of pulmonary cell-mediated immunity to a Cryptococcus neoformans infection. J Immunol. 1997;159:318–327.
   PubMed Web of Science ®Google Scholar
• Eberl M, Beck E, Coulson PS, et al. IL-18 potentiates the adjuvant properties of IL-12 in the induction of a strong Th1 type immune response against a recombinant antigen. Vaccine. 2000;18:2002–2008.
   PubMed Web of Science ®Google Scholar
• Bobanga ID, Petrosiute A, Huang AY. Chemokines as cancer vaccine adjuvants. Vaccines. 2013;1(4):444–462.
   PubMedGoogle Scholar
• Sominskaya I, Skrastina D, Dislers A, et al. Construction and immunological evaluation of multivalent hepatitis B virus (HBV) core virus-like particles carrying HBV and HCV epitopes. Clin Vaccine Immunol. 2010;17:1027–1033.
   PubMed Web of Science ®Google Scholar
• Thomas C, Rawat A, Hope-Weeks L, et al. Aerosolized PLGA nanoparticles enhance humoral, mucosal and cytokine responses to hepatitis B vaccine. Mol Pharm. 2011;8:405–415.
   PubMed Web of Science ®Google Scholar
• Kim SY, Doh HJ, Jang MH, et al. Oral immunization with Helicobacter pylori-loaded poly (d, l-lactide-co-glycolide) nanoparticles. Helicobacter. 1999;4:33–39.
   PubMed Web of Science ®Google Scholar
• Vila A, Sanchez A, Evora C, et al. PEG-PLA nanoparticles as carriers for nasal vaccine delivery. J Aerosol Med. 2004;17:174–185.
   PubMedGoogle Scholar
• Lü J-M, Wang X, Marin-Muller C, et al. Current advances in research and clinical applications of PLGA-based nanotechnology. Expert Rev Mol Diagn. 2009;9:325–341.
   PubMed Web of Science ®Google Scholar
• Demento SL, Cui W, Criscione JM, et al. Role of sustained antigen release from nanoparticle vaccines in shaping the T cell memory phenotype. Biomaterials. 2012;33:4957–4964.
   PubMed Web of Science ®Google Scholar
• Diwan M, Tafaghodi M, Samuel J. Enhancement of immune responses by co-delivery of a CpG oligodeoxynucleotide and tetanus toxoid in biodegradable nanospheres. J Control Release. 2002;85:247–262.
   PubMed Web of Science ®Google Scholar
• Silva AL, Rosalia RA, Sazak A, et al. Optimization of encapsulation of a synthetic long peptide in PLGA nanoparticles: low-burst release is crucial for efficient CD8 (+) T cell activation. Eur J Pharmaceutics Biopharmaceutics. 2013;83:338–345.
   PubMed Web of Science ®Google Scholar
• Akagi T, Baba M, Akashi M, et al. 2012. Biodegradable nanoparticles as vaccine adjuvants and delivery systems: regulation of immune responses by nanoparticle-based vaccine. S. Kunugi, T. Yamaoka (Eds.), Polymers in nanomedicine, Berlin: Springer-Verlag Berlin, pp. 31–64.
   Google Scholar
• Akagi T, Kaneko T, Kida T, et al. Preparation and characterization of biodegradable nanoparticles based on poly (γ-glutamic acid) with l-phenylalanine as a protein carrier. J Control Release. 2005;108:226–236.
   PubMed Web of Science ®Google Scholar
• Kalkanidis M, Pietersz GA, Xiang SD, et al. Methods for nano-particle based vaccine formulation and evaluation of their immunogenicity. Methods. 2006;40:20–29.
   PubMed Web of Science ®Google Scholar
• Sjolander S, Drave D, Davis R, et al. Intranasal immunisation with influenza- ISCOMATRIX adjuvanted influenza vaccine. Vaccine. 2003;21:946–949.
   PubMed Web of Science ®Google Scholar
• Rimmelzwann GF, Baars M, VanAmerongen G, et al. A single dose of an ISCOM influenza vaccine induces long- lasting protective immunity against homologous challenge infection but fails to protect cynomologus macaques against distant drift variants of influenza A (H3N2) viruses. Vaccine. 2001;20:158–163.
   PubMed Web of Science ®Google Scholar
• Freund J. The mode of action of immunologic adjuvants. Adv Tuberc Res. 1956;7:130–148.
   Google Scholar
• Dar P, Kalaivanan R, Sied N, et al. Montanide ISA™ 201 adjuvanted FMD vaccine induces improved immune responses and protection in cattle. Vaccine. 2013;31:3327–3332.
   PubMed Web of Science ®Google Scholar
• Seubert A, Monaci E, Pizza M, et al. The adjuvants aluminium hydroxide and MF59 induce monocyte and granulocyte chemo attractants and enhance monocyte differentiation toward dendritic cells. J Immunol. 2008;180:5402–5412.
   PubMed Web of Science ®Google Scholar
• Didierlaurent AM, Laupèze B, Di Pasquale A, et al. Adjuvant system AS01: helping to overcome the challenges of modern vaccines. Expert Rev Vaccines. 2017;16(1):55–63.
   PubMed Web of Science ®Google Scholar
• Leroux-Roels I, Devaster JM, Leroux-Roels G, et al. Adjuvant system AS02V enhances humoral and cellular immune responses to pneumococcal protein PhtD vaccine in healthy young and older adults: randomised, controlled trials. Vaccine. 2015;33(4):577–584.
   PubMed Web of Science ®Google Scholar
• Garçon N, Vaughn DW, Didierlaurent AM. Development and evaluation of AS03, an adjuvant system containing α-tocopherol and squalene in an oil-in-water emulsion. Expert Rev Vaccines. 2012;11(3):349–366.
   PubMed Web of Science ®Google Scholar
• Didierlaurent AM, Morel S, Lockman L, 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(10):6186–6197.
   PubMed Web of Science ®Google Scholar
• Schmidt ST, Foged C, Korsholm KS, et al. Liposome-based adjuvants for subunit vaccines: formulation strategies for subunit antigens and immunostimulators. Pharmaceutics. 2016;8:7.
   Web of Science ®Google Scholar
• Zhu D, Tuo W. QS-21: A potent vaccine adjuvant. Nat Prod Chem Res. 2016;3(4):e113.
   PubMedGoogle Scholar
• Eng NF, Bhardwaj N, Mulligan R, et al. The potential of 1018 ISS adjuvant in hepatitis B vaccines: HEPLISAV™ review. Hum Vaccin Immunother. 2013;9(8):1661–1672.
   PubMed Web of Science ®Google Scholar
• Olafsdottir TA, Lingnau K, Nagy E, et al. IC31, a two-component novel adjuvant mixed with a conjugate vaccine enhances protective immunity against pneumococcal disease in neonatal mice. Scand J Immunol. 2009;69(3):194–202.
   PubMed Web of Science ®Google Scholar
• Szabo A, Gogolak P, Pazmandi K, et al. The two-component adjuvant IC31® boosts type i interferon production of human monocyte-derived dendritic cells via ligation of endosomal TLRs. Plos One. 2013;8(2):e55264.
   PubMed Web of Science ®Google Scholar
• van Dissel JT, Joosten SA, Hoff ST, et al. A novel liposomal adjuvant system, CAF01, promotes long-lived mycobacterium tuberculosis-specific T-cell responses in human. Vaccine. 2014;32(52):7098–7107.
   PubMed Web of Science ®Google Scholar
• Norton EB, Bauer DL, Weldon WC, et al. The novel adjuvant dmLT promotes dose sparing, mucosal immunity and longevity of antibody responses to the inactivated polio vaccine in a murine model. Vaccine. 2015;33(16):1909–1915.
   PubMed Web of Science ®Google Scholar
• Morelli AB, Becher D, Koernig S, et al. ISCOMATRIX: a novel adjuvant for use in prophylactic and therapeutic vaccines against infectious diseases. J Med Microbiol. 2012;6:935–943.
   Web of Science ®Google Scholar
• Reimer JM, Karlsson KH, Lövgren-Bengtsson K, et al. Matrix-M™ adjuvant induces local recruitment, activation and maturation of central immune cells in absence of antigen. Plos One. 2012;7(7):e41451.
   PubMed Web of Science ®Google Scholar
• Jain S, O’Hagan DT, Singh M. The long-term potential of biodegradable poly(lactide-co-glycolide) microparticles as the next-generation vaccine adjuvant. Expert Rev Vaccines. 2011;10(12):1731–1742.
   PubMed Web of Science ®Google Scholar
• Shim DH, Ko HJ, Volker G, et al. Efficacy of poly [di(sodium carboxylatophenoxy)phosphazene] (PCPP) as mucosal adjuvant to induce protective immunity against respiratory pathogens. Vaccine. 2010;28(11):2311–2317.
   PubMed Web of Science ®Google Scholar
• Bode C, Zhao G, Steinhagen F, et al. CpG DNA as a vaccine adjuvant. Expert Rev Vaccines. 2011;10(4):499–511.
   PubMed Web of Science ®Google Scholar
• Behzad H, Huckriede AL, Haynes L, et al. GLA-SE, a synthetic toll-like receptor 4 agonist, enhances T-cell responses to influenza vaccine in older adults. J Infect Dis. 2012;205(3):466.
   PubMed Web of Science ®Google Scholar
• Lindblad EB. Aluminium Adjuvants. In: Stewart-Tull DES, ed. The theory and practical application of adjuvants. Chichester: John Wiley & Sons Ltd; 1995. p. 21–35.
   Google Scholar
• Schirmbeck R, Melber K, Mertens T, et al. Antibody and cytotoxic T-cell responses to soluble hepatitis B virus (HBV) S antigen in mice: implications for the pathogenesis of HBV-induced hepatitis. J Virol. 1994;68:1418–1425.
   PubMed Web of Science ®Google Scholar
• Traquina P, Morandi M, Contorni M, et al. MF59 adjuvant enhances the antibody response to recombinant hepatitis B surface antigen vaccine in primates. J Infect Dis. 1996;174:1168–1175.
   PubMed Web of Science ®Google Scholar
• Blagowechensky NN. Durée du séjour de l’antigène dans l’organisme et immunité. Rev Immunol París. 1938;4:161.
   Google Scholar
• Gupta RK, Rost BE, Relyveld E, et al. Adjuvant properties of aluminium and calcium compounds. In: Powell MF, Newman MJ eds. Vaccine design: the subunit and adjuvant approach. New York: Plenum Press; 1995. p. 229–248.
   Google Scholar
• Straw BE, MacLachlan NJ, Corbett WT, et al. Comparison of tissue reactions produced by Haemophilus pleuropneumoniae vaccines made with six different adjuvants in swine. Can J Comp Med. 1985;49:149.
   PubMedGoogle Scholar
• Frey S, Poland G, Percell S, et al. Comparison of the safety, tolerability, and immunogenicity of a MF59-adjuvanted influenza vaccine and a non-adjuvanted influenza vaccine in non-elderly adults. Vaccine. 2003;21:4234–4237.
   PubMed Web of Science ®Google Scholar
• Lee JB, Jang JE, Song MK, et al. Intranasal delivery of cholera toxin induces Th17- dominated T-cell response to bystander antigens. Plos One. 2009;4:e5190.
   PubMed Web of Science ®Google Scholar
• Gupta P, Singh MK, Singh Y, et al. Recombinant Shiga toxin B subunit elicits protection against Shiga toxin via mixed Th type immune response in mice. Vaccine None. 2011;29:8094–8100.
   PubMed Web of Science ®Google Scholar
• Lowell GH, Kaminski RW, Grate S, et al. Intranasal and intramuscular proteosome-staphylococcal enterotoxin B (SEB) toxoid vaccines: immunogenicity and efficacy against lethal SEB intoxication in mice. Infect Immun. 1996;64:1706–1713.
   PubMed Web of Science ®Google Scholar
• Qiu HN, Wong CK, Chu IM, et al. Muramyl dipeptide mediated activation of human bronchial epithelial cells interacting with basophils: a novel mechanism of airway inflammation. Clin Exp Immunol. 2013;172:81–94.
   PubMed Web of Science ®Google Scholar
• Bessler WG, Baier W, Esche U, et al. Bacterial lipopeptides constitute efficient novel immunogens and adjuvants in parenteral and oral immunization. Behring Inst Mitt. 1997;98:390–399.
   Google Scholar
• Burt D, Mallett C, Plante M, et al. Proteasome-adjuvanted intranasal influenza vaccines: advantages, progress and future considerations. Expert Rev Vaccines None. 2011;10:365–375.
   PubMed Web of Science ®Google Scholar
• Tomai MA, Johnson AG. T cell and interferon-g involvement in the adjuvant action of a detoxified endotoxin. J Biol Resp Modifiers. 1989;8:625–630.
   PubMedGoogle Scholar
• Ronnberg B, Fekadu M, Morien B. Adjuvant activity of non-toxic Quillaja saponaria Molina components for use in ISCOM matrix. Vaccine. 1995;13:1375–1382.
   PubMed Web of Science ®Google Scholar
• Nambiar JK, Ryan AA, Kong CU, et al. Modulation of pulmonary DC function by vaccine encoded GM-CSF enhances protective immunity against mycobacterium tuberculosis infection. Eur J Immunol. 2010;40:153–161.
   PubMed Web of Science ®Google Scholar
• Abraham E, Shah S. Intranasal immunization with liposomes containing IL-2 enhances bacterial polysaccharide antigen-specific pulmonary secretory antibody response. J Immunol. 1992;49:3719–3726.
   Google Scholar
• Kishimoto T. Interleukin-6: discovery of a pleiotropic cytokine. Arth Res Ther. 2006;8(Suppl 2):S2.
   PubMed Web of Science ®Google Scholar
• Shanmugham LN, Petrarca C, Frydas S, et al. IL-15 an immunoregulatory and anti-cancer cytokine: recent advances. J Exp Clin Can Res. 2006;25:529–536.
   PubMed Web of Science ®Google Scholar
• Seth A, Ritchie FK, Wibowo N, et al. Non-carrier nanoparticles adjuvant modular protein vaccine in a particle-dependent manner. Plos One. 2015;10(3):e0117203.
   PubMed Web of Science ®Google Scholar
• Minigo G, Scholzen A, Tang CK, et al. Poly-l-lysine-coated nanoparticles: a potent delivery system to enhance DNA vaccine efficacy. Vaccine. 2007;25:1316–1327.
   PubMed Web of Science ®Google Scholar
• Peek LJ, Middaugh CR, Berkland C. Nanotechnology in vaccine delivery. Adv Drug Deliv Rev. 2008;60:915–928.
   PubMed Web of Science ®Google Scholar
• Danhier F, Ansorena E, Silva JM, et al. PLGA-based nanoparticles: an overview of biomedical applications. J Control Release. 2012;161:505–522.
   PubMed Web of Science ®Google Scholar
• Manish M, Rahi A, Kaur M, et al. A single-dose PLGA encapsulated protective antigen domain 4 nanoformulation protects mice against Bacillus anthracis spore challenge. Plos ONE. 2013;8:e61885–e61890.
   PubMed Web of Science ®Google Scholar
• Moon JJ, Suh H, Polhemus ME, et al. Antigen-displaying lipid-enveloped PLGA nanoparticles as delivery agents for a plasmodium vivax malaria vaccine. Plos ONE. 2012;7:e31472.
   PubMed Web of Science ®Google Scholar
• Xiang SD, Scholzen A, Minigo G, et al. Pathogen recognition and development of particulate vaccines: does size matter? Methods. 2006 Sep;40(1):1–9.
   PubMed Web of Science ®Google Scholar
• Scheerlinck J-PY, Gloster S, Gamvrellis A, et al. Systemic immune responses in sheep, induced by a novel nano-bead adjuvant. Vaccine. 2006;24:1124–1131.
   PubMed Web of Science ®Google Scholar
• Démoulins T, Bassi I, Thomann-Harwood L, et al. Alginate-coated chitosan nanogel capacity to modulate the effect of TLR ligands on blood dendritic cells. Nanomedicine: Nanotechnology, Biol Med. 2013;9:806–817.
   PubMed Web of Science ®Google Scholar
• Vinogradov S, Batrakova E, Kabanov A. Poly (ethylene glycol)-polyethylene imine NanoGel™ particles: novel drug delivery systems for antisense oligonucleotides. Colloids and Surfaces B: Biointerfaces. 1999;16:291–304.
   Web of Science ®Google Scholar
• Ferreira SA, Gama FM, Vilanova M. Polymeric nanogels as vaccine delivery systems. Nanomedicine: Nanotechnology, Biol Med. 2012;9:159–173.
   PubMed Web of Science ®Google Scholar
• Raemdonck K, Demeester J, De Smedt S. Advanced nanogel engineering for drug delivery. Soft Matter. 2009;5:707–715.
   Web of Science ®Google Scholar
• Nochi T, Yuki Y, Takahashi H, et al. Nanogel antigenic protein-delivery system for adjuvant-free intranasal vaccines. Nat Mater. 2010;9:572–578.
   PubMed Web of Science ®Google Scholar
• Debache K, Kropf C, Schutz CA, et al. Vaccination of mice with chitosan nanogel-associated recombinant NcPDI against challenge infection with Neospora caninum tachyzoites. Parasite Immunol. 2011;33:81–94.
   PubMed Web of Science ®Google Scholar
• Stone JW, Thornburg NJ, Blum DL, et al. Gold nanorod vaccine for respiratory syncytial virus. Nanotechnology. 2013;24:295102.
   PubMed Web of Science ®Google Scholar
• Tao W, Ziemer KS, Gill HS. Gold nanoparticle-M2e conjugate co-formulated with CpG induces protective immunity against influenza A virus. Nanomedicine. 2014;9(2):237–251.
   Web of Science ®Google Scholar
• Xu L, Liu Y, Chen Z, et al. Surface-engineered gold nanorods: promising DNA vaccine adjuvant for HIV-1 treatment. Nano Lett. 2012;12:2003–2012.
   PubMed Web of Science ®Google Scholar
• Chen Y-S, Hung Y-C, Lin W-H, et al. Assessment of gold nanoparticles as a size-dependent vaccine carrier for enhancing the antibody response against synthetic foot-and-mouth disease virus peptide. Nanotechnology. 2010;21:195101–195108.
   PubMed Web of Science ®Google Scholar
• Bianco A, Kostarelos K, Prato M. Applications of carbon nanotubes in drug delivery. Curr Opin Chem Biol. 2005;9:674–679.
   PubMed Web of Science ®Google Scholar
• Wang T, Zou M, Jiang H, et al. Synthesis of a novel kind of carbon nanoparticle with large mesopores and macropores and its application as an oral vaccine adjuvant. Eur J Pharm Sci. 2011;44:653–659.
   PubMed Web of Science ®Google Scholar
• Smart S, Cassady A, Lu G, et al. The biocompatibility of carbon nanotubes. Carbon. 2006;44:1034–1047.
   Web of Science ®Google Scholar
• Villa CH, Dao T, Ahearn I, et al. Single-walled carbon nanotubes deliver peptide antigen into dendritic cells and enhance IgG responses to tumor-associated antigens. ACS Nano. 2011;5:5300–5311.
   PubMed Web of Science ®Google Scholar
• Parra J, Abad-Somovilla A, Mercader JV, et al. Carbon nanotube-protein carriers enhance size-dependent self-adjuvant antibody response to haptens. J Control Release. 2013;170:242–251.
   PubMed Web of Science ®Google Scholar
• Pantarotto D, Partidos CD, Hoebeke J, et al. Immunization with peptide-functionalized carbon nanotubes enhances virus-specific neutralizing antibody responses. Chem Biol. 2003;10:961–966.
   PubMed Web of Science ®Google Scholar
• Ow H, Larson DR, Srivastava M, et al. Bright and stable core-shell fluorescent silica nanoparticles. Nano Lett. 2005;5:113–117.
   PubMed Web of Science ®Google Scholar
• Benezra M, Penate-Medina O, Zanzonico PB, et al. Multimodal silica nanoparticles are effective cancer-targeted probes in a model of human melanoma. J Clin Investig. 2011;121:2768–2780.
   PubMed Web of Science ®Google Scholar
• Niu Y, Popat A, Yu M, et al. Recent advances in the rational design of silica-based nanoparticles for gene therapy. Ther Deliv. 2012;3:1217–1237.
   PubMedGoogle Scholar
• Yu M, Jambhrunkar S, Thorn P, et al. Hyaluronic acid modified mesoporous silica nanoparticles for targeted drug delivery to CD44-overexpressing cancer cells. Nanoscale. 2013;5:178–183.
   PubMed Web of Science ®Google Scholar
• Alshamsan A, Haddadi A, Incani V, et al. Formulation and delivery of siRNA by oleic acid and stearic acid modified polyethylene imine. Mol Pharm. 2008;6:121–133.
   Web of Science ®Google Scholar
• Xia T, Kovochich M, Liong M, et al. Polyethylene imine coating enhances the cellular uptake of mesoporous silica nanoparticles and allows safe delivery of siRNA and DNA constructs. ACS Nano. 2009;3:3273–3286.
   PubMed Web of Science ®Google Scholar
• He -X-X, Wang K, Tan W, et al. Bio-conjugated nanoparticles for DNA protection from cleavage. J Am Chem Soc. 2003;125:7168–7169.
   PubMed Web of Science ®Google Scholar
• Zhai W, He C, Wu L, et al. Degradation of hollow mesoporous silica nanoparticles in human umbilical vein endothelial cells. J Biomed Mater Res B: Appl Biomater. 2012;100B:1397–1403.
   Web of Science ®Google Scholar
• Yamada H, Urata C, Aoyama Y, et al. Preparation of colloidal mesoporous silica nanoparticles with different diameters and their unique degradation behavior in static aqueous systems. Chem Mater. 2012;24:1462–1471.
   Web of Science ®Google Scholar
• Chen K, Zhang J, Gu H. Dissolution from inside: unique degradation behaviour of core-shell magnetic mesoporous silica nanoparticles and the effect of polyethylene imine coating. J Mater Chem. 2012;22:22005–22012.
   Web of Science ®Google Scholar
• Nakanishi T, Kunisawa J, Hayashi A, et al. Positively charged liposomes function as an efficient immunoadjuvant in inducing cell-mediated immune response to soluble proteins. J Control Release. 1999;61:233–240.
   PubMed Web of Science ®Google Scholar
• Campbell JD. Development of the CpG adjuvant 1018: a case study. Methods Mol Biol. 2017;1494:15–27.
   PubMedGoogle Scholar
• Romio S, Weibel D, Dieleman JP, et al. Guillain-Barré syndrome and adjuvanted pandemic influenza A (H1N1) 2009 vaccines: a multinational self-Controlled case series in Europe. Plos One. 2014;9(1):e82222.
   PubMed Web of Science ®Google Scholar