The impact of size on particulate vaccine adjuvants

References

• 1 Kommareddy S, Amiji M. Biodistribution and pharmacokinetic analysis of long-circulating thiolated gelatin nanoparticles following systemic administration in breast cancer-bearing mice. J. Pharm. Sci. 96(2), 397–407 (2007).
  Medline CASGoogle Scholar
• 2 Xu J, Gattacceca F, Amiji M. Biodistribution and pharmacokinetics of EGFR-targeted thiolated gelatin nanoparticles following systemic administration in pancreatic tumor-bearing mice. Mol. Pharm. 10(5), 2031–2044 (2013).
  Medline CASGoogle Scholar
• 3 Van Vlerken LE, Vyas TK, Amiji MM. Poly(ethylene glycol)-modified nanocarriers for tumor-targeted and intracellular delivery. Pharm. Res. 24(8), 1405–1414 (2007).
  Medline CASGoogle Scholar
• 4 Panyam J, Labhasetwar V. Biodegradable nanoparticles for drug and gene delivery to cells and tissue. Adv. Drug Deliv. Rev. 55(3), 329–347 (2003).
  Medline CASGoogle Scholar
• 5 Cho K, Wang X, Nie S, Chen Z, Shin DM. Therapeutic nanoparticles for drug delivery in cancer. Clin. Cancer Res. 14(5), 1310–1316 (2008).
  Medline CASGoogle Scholar
• 6 Barenholz Y. Doxil^® – the first FDA-approved nano-drug: lessons learned. J. Control. Release 160(2), 117–134 (2012).
  Medline CASGoogle Scholar
• 7 Kreuter J. Nanoparticles and microparticles for drug and vaccine delivery. J. Anat. 189(Pt 3), 503–505 (1996).
  Medline CASGoogle Scholar
• 8 O'Hagan DT. The intestinal uptake of particles and the implications for drug and antigen delivery. J. Anat. 189(Pt 3), 477–482 (1996).
  MedlineGoogle Scholar
• 9 Hans ML, Lowman AM. Biodegradable nanoparticles for drug delivery and targeting. Curr. Opin. Solid State Mater. Sci. 6(4), 319–327 (2002).
  CASGoogle Scholar
• 10 Gindy ME, Prud'homme RK. Multifunctional nanoparticles for imaging, delivery and targeting in cancer therapy. Expert Opin. Drug Deliv. 6(8), 865–878 (2009).
  Medline CASGoogle Scholar
• 11 Gradishar WJ, Tjulandin S, Davidson N et al. Phase III trial of nanoparticle albumin-bound paclitaxel compared with polyethylated castor oil-based paclitaxel in women with breast cancer. J. Clin. Oncol. 23(31), 7794–7803 (2005).
  Medline CASGoogle Scholar
• 12 Bachmann MF, Jennings GT. Vaccine delivery: a matter of size, geometry, kinetics and molecular patterns. Nat. Rev. Immunol. 10(11), 787–796 (2010).
  Medline CASGoogle Scholar
• 13 Manolova V, Flace A, Bauer M, Schwarz K, Saudan P, Bachmann MF. Nanoparticles target distinct dendritic cell populations according to their size. Eur. J. Immunol. 38(5), 1404–1413 (2008).
  Medline CASGoogle Scholar
• 14 Xiang SD, Scholzen A, Minigo G et al. Pathogen recognition and development of particulate vaccines: does size matter? Methods 40(1), 1–9 (2006).
  Medline CASGoogle Scholar
• 15 Gamvrellis A, Leong D, Hanley JC, Xiang SD, Mottram P, Plebanski M. Vaccines that facilitate antigen entry into dendritic cells. Immunol. Cell Biol. 82(5), 506–516 (2004).
  Medline CASGoogle Scholar
• 16 Fifis T, Gamvrellis A, Crimeen-Irwin B et al. Size-dependent immunogenicity: therapeutic and protective properties of nano-vaccines against tumors. J. Immunol. 173(5), 3148–3154 (2004).
  Medline CASGoogle Scholar
• 17 Delany I, Rappuoli R, De Gregorio E. Vaccines for the 21st century. EMBO Mol. Med. 6(6), 708–720 (2014).
  Medline CASGoogle Scholar
• 18 Foged C, Hansen J, Agger EM. License to kill: Formulation requirements for optimal priming of CD8(⁺) CTL responses with particulate vaccine delivery systems. Eur. J. Pharm. Sci. 45(4), 482–491 (2012).
  Medline CASGoogle Scholar
• 19 Reed SG, Orr MT, Fox CB. Key roles of adjuvants in modern vaccines. Nat. Med. 19(12), 1597–1608 (2013).
  Medline CASGoogle Scholar
• 20 Shah R, Brito L, O'Hagan D, Amiji M. Emulsions as vaccine adjuvants. In: Subunit Vaccine Delivery. Foged C, Rades TH, Perrie Y, Hook S (Eds). Springer, NY, USA (2015).
  Google Scholar
• 21 Gupta RaR, Bradford. Aluminium compounds as vaccine adjuvants. In: Vaccine Adjuvants Preparation Methods and Res. Protocols. O'Hagan D (Ed.). Humana, NJ, USA, 65–89 (2000).
  Google Scholar
• 22 Hem SL, Hogenesch H. Relationship between physical and chemical properties of aluminum-containing adjuvants and immunopotentiation. Expert Rev. Vaccines 6(5), 685–698 (2007).
  Medline CASGoogle Scholar
• 23 De Gregorio E, Caproni E, Ulmer JB. Vaccine adjuvants: mode of action. Front. Immunol. 4, 214 (2013).
  MedlineGoogle Scholar
• 24 De Gregorio E, D'oro U, Wack A. Immunology of TLR-independent vaccine adjuvants. Curr. Opin. Immunol. 21(3), 339–345 (2009).
  Medline CASGoogle Scholar
• 25 De Gregorio E, Tritto E, Rappuoli R. Alum adjuvanticity: unraveling a century old mystery. Eur. J. Immunol. 38(8), 2068–2071 (2008).
  Medline CASGoogle Scholar
• 26 Lambrecht BN, Kool M, Willart MA, Hammad H. Mechanism of action of clinically approved adjuvants. Curr. Opin. Immunol. 21(1), 23–29 (2009).
  Medline CASGoogle Scholar
• 27 Marrack P, Mckee AS, Munks MW. Towards an understanding of the adjuvant action of aluminium. Nat. Rev. Immunol. 9(4), 287–293 (2009).
  Medline CASGoogle Scholar
• 28 Kool M, Petrilli V, De Smedt T et al. Cutting edge: alum adjuvant stimulates inflammatory dendritic cells through activation of the NALP3 inflammasome. J. Immunol. 181(6), 3755–3759 (2008).
  Medline CASGoogle Scholar
• 29 Eisenbarth SC, Colegio OR, O'Connor W, Sutterwala FS, Flavell RA. Crucial role for the Nalp3 inflammasome in the immunostimulatory properties of aluminium adjuvants. Nature 453(7198), 1122–1126 (2008).
  Medline CASGoogle Scholar
• 30 Hem SL, White JL. Structure and properties of aluminum-containing adjuvants. Pharm. Biotechnol. 6, 249–276 (1995).
  Medline CASGoogle Scholar
• 31 Romero Mendez IZ, Shi Y, Hogenesch H, Hem SL. Potentiation of the immune response to non-adsorbed antigens by aluminum-containing adjuvants. Vaccine 25(5), 825–833 (2007).
  Medline CASGoogle Scholar
• 32 Morefield GL, Sokolovska A, Jiang D, Hogenesch H, Robinson JP, Hem SL. Role of aluminum-containing adjuvants in antigen internalization by dendritic cells in vitro. Vaccine 23(13), 1588–1595 (2005).
  Medline CASGoogle Scholar
• 33 Li X, Aldayel AM, Cui Z. Aluminum hydroxide nanoparticles show a stronger vaccine adjuvant activity than traditional aluminum hydroxide microparticles. J. Control. Release 173, 148–157 (2014).
  Medline CASGoogle Scholar
• 34 O'Hagan DT, Ott GS, Nest GV, Rappuoli R, Giudice GD. The history of MF59((R)) adjuvant: a phoenix that arose from the ashes. Expert Rev. Vaccines 12(1), 13–30 (2013).
  MedlineGoogle Scholar
• 35 Morel S, Didierlaurent A, Bourguignon P et al. Adjuvant System AS03 containing alpha-tocopherol modulates innate immune response and leads to improved adaptive immunity. Vaccine 29(13), 2461–2473 (2011).
  Medline CASGoogle Scholar
• 36 Ott G, Barchfeld GL, Van Nest G. Enhancement of humoral response against human influenza vaccine with the simple submicron oil/water emulsion adjuvant MF59. Vaccine 13(16), 1557–1562 (1995).
  Medline CASGoogle Scholar
• 37 Allison AC. Squalene and squalane emulsions as adjuvants. Methods 19(1), 87–93 (1999).
  Medline CASGoogle Scholar
• 38 Vesikari T, Karvonen A, Tilman S et al. Immunogenicity and safety of MF59-adjuvanted H5N1 influenza vaccine from infancy to adolescence. Pediatrics 126(4), e762–e770 (2010).
  MedlineGoogle Scholar
• 39 Villa M, Black S, Groth N et al. Safety of MF59-adjuvanted influenza vaccination in the elderly: results of a comparative study of MF59-adjuvanted vaccine versus nonadjuvanted influenza vaccine in Northern Italy. Am. J. Epidemiol. 178(7), 1139–1145 (2013).
  MedlineGoogle Scholar
• 40 Whitehouse MW, Orr KJ, Beck FW, Pearson CM. Freund's adjuvants: relationship of arthritogenicity and adjuvanticity in rats to vehicle composition. Immunology 27(2), 311–330 (1974).
  Medline CASGoogle Scholar
• 41 Stills HF Jr. Adjuvants and antibody production: dispelling the myths associated with Freund's complete and other adjuvants. ILAR J. 46(3), 280–293 (2005).
  Medline CASGoogle Scholar
• 42 Stuewart-Tull DE, Shimono T, Kotani S, Knights BA. Immunosuppressive effect in mycobacterial adjuvant emulsions of mineral oils containing low molecular weight hydrocarbons. Int. Arch. Allergy Appl. Immunol. 52(1–4), 118–128 (1976).
  Medline CASGoogle Scholar
• 43 Murray R, Cohen P, Hardegree MC. Mineral oil adjuvants: biological and chemical studies. Ann. Allergy 30(3), 146–151 (1972).
  Medline CASGoogle Scholar
• 44 Bovier PA. Epaxal: a virosomal vaccine to prevent hepatitis A infection. Expert Rev. Vaccines 7(8), 1141–1150 (2008).
  Medline CASGoogle Scholar
• 45 Herzog C, Hartmann K, Kunzi V et al. Eleven years of Inflexal V-a virosomal adjuvanted influenza vaccine. Vaccine 27(33), 4381–4387 (2009).
  Medline CASGoogle Scholar
• 46 Henson D, Van Dissel J, Joosten S et al. Vaccination with a Hybrid 1 (H1) fusion protein combined with a liposomal adjuvant (CAF01) induced antigen specific T-cells 3 years post vaccination in a human clinical trial. (VAC7P.971). J. Immunol. 192(1 Suppl.), 141.116 (2014).
  Google Scholar
• 47 Watson DS, Endsley AN, Huang L. Design considerations for liposomal vaccines: influence of formulation parameters on antibody and cell-mediated immune responses to liposome associated antigens. Vaccine 30(13), 2256–2272 (2012).
  Medline CASGoogle Scholar
• 48 Brewer JM, Tetley L, Richmond J, Liew FY, Alexander J. Lipid vesicle size determines the Th1 or Th2 response to entrapped antigen. J. Immunol. 161(8), 4000–4007 (1998).
  Medline CASGoogle Scholar
• 49 Mann JF, Shakir E, Carter KC, Mullen AB, Alexander J, Ferro VA. Lipid vesicle size of an oral influenza vaccine delivery vehicle influences the Th1/Th2 bias in the immune response and protection against infection. Vaccine 27(27), 3643–3649 (2009).
  Medline CASGoogle Scholar
• 50 Brewer JM, Pollock KG, Tetley L, Russell DG. Vesicle size influences the trafficking, processing, and presentation of antigens in lipid vesicles. J. Immunol. 173(10), 6143–6150 (2004).
  Medline CASGoogle Scholar
• 51 Henriksen-Lacey M, Devitt A, Perrie Y. The vesicle size of DDA:TDB liposomal adjuvants plays a role in the cell-mediated immune response but has no significant effect on antibody production. J. Control. Release 154(2), 131–137 (2011).
  Medline CASGoogle Scholar
• 52 Christensen D, Korsholm KS, Rosenkrands I, Lindenstrom T, Andersen P, Agger EM. Cationic liposomes as vaccine adjuvants. Expert Rev. Vaccines 6(5), 785–796 (2007).
  Medline CASGoogle Scholar
• 53 Vangasseri DP, Cui Z, Chen W, Hokey DA, Falo LD Jr, Huang L. Immunostimulation of dendritic cells by cationic liposomes. Mol. membrane Biol. 23(5), 385–395 (2006).
  Medline CASGoogle Scholar
• 54 Christensen D, Agger EM, Andreasen LV, Kirby D, Andersen P, Perrie Y. Liposome-based cationic adjuvant formulations (CAF): past, present, and future. J. liposome Res. 19(1), 2–11 (2009).
  Medline CASGoogle Scholar
• 55 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 10(12), 1731–1742 (2011).
  Medline CASGoogle Scholar
• 56 Oyewumi MO, Kumar A, Cui Z. Nano-microparticles as immune adjuvants: correlating particle sizes and the resultant immune responses. Expert Rev. Vaccines 9(9), 1095–1107 (2010).
  Medline CASGoogle Scholar
• 57 Kreuter J, Berg U, Liehl E, Soliva M, Speiser PP. Influence of the particle size on the adjuvant effect of particulate polymeric adjuvants. Vaccine 4(2), 125–129 (1986).
  Medline CASGoogle Scholar
• 58 Joshi VB, Geary SM, Salem AK. Biodegradable particles as vaccine delivery systems: size matters. AAPS J. 15(1), 85–94 (2013).
  Medline CASGoogle Scholar
• 59 Li X, Sloat BR, Yanasarn N, Cui Z. Relationship between the size of nanoparticles and their adjuvant activity: data from a study with an improved experimental design. Eur. J. Pharm. bioPharm. 78(1), 107–116 (2011).
  Medline CASGoogle Scholar
• 60 Foged C, Brodin B, Frokjaer S, Sundblad A. Particle size and surface charge affect particle uptake by human dendritic cells in an in vitro model. Int. J. Pharm. 298(2), 315–322 (2005).
  Medline CASGoogle Scholar
• 61 Gamvrellis A, Gloster S, Jefferies M et al. Characterisation of local immune responses induced by a novel nano-particle based carrier-adjuvant in sheep. Vet. Immunol. Immunopathol. 155(1–2), 21–29 (2013).
  Medline CASGoogle Scholar
• 62 Scheerlinck J-PY, Gloster S, Gamvrellis A, Mottram PL, Plebanski M. Systemic immune responses in sheep, induced by a novel nano-bead adjuvant. Vaccine 24(8), 1124–1131 (2006).
  Medline CASGoogle Scholar
• 63 Gutierro I, Hernandez RM, Igartua M, Gascon AR, Pedraz JL. Size dependent immune response after subcutaneous, oral and intranasal administration of BSA loaded nanospheres. Vaccine 21(1–2), 67–77 (2002).
  Medline CASGoogle Scholar
• 64 Nagamoto T, Hattori Y, Takayama K, Maitani Y. Novel chitosan particles and chitosan-coated emulsions inducing immune response via intranasal vaccine delivery. Pharm. Res. 21(4), 671–674 (2004).
  Medline CASGoogle Scholar
• 65 Wendorf J, Chesko J, Kazzaz J et al. A comparison of anionic nanoparticles and microparticles as vaccine delivery systems. Hum. Vaccin. 4(1), 44–49 (2008).
  Medline CASGoogle Scholar
• 66 Singh M, Li XM, Wang H et al. Controlled release microparticles as a single dose diphtheria toxoid vaccine: immunogenicity in small animal models. Vaccine 16(4), 346–352 (1998).
  Medline CASGoogle Scholar
• 67 Wendorf J, Singh M, Chesko J et al. A practical approach to the use of nanoparticles for vaccine delivery. J. Pharm. Sci. 95(12), 2738–2750 (2006).
  Medline CASGoogle Scholar
• 68 Galloway AL, Murphy A, Desimone JM et al. Development of a nanoparticle-based influenza vaccine using the PRINT technology. NanoMed. 9(4), 523–531 (2013).
  Medline CASGoogle Scholar
• 69 Calabro S, Tritto E, Pezzotti A et al. The adjuvant effect of MF59 is due to the oil-in-water emulsion formulation, none of the individual components induce a comparable adjuvant effect. Vaccine 31(33), 3363–3369 (2013).
  Medline CASGoogle Scholar
• 70 Brar SK, Verma M. Measurement of nanoparticles by light-scattering techniques. Trends Anal. Chem. 30(1), 4–17 (2011).
  CASGoogle Scholar
• 71 Gaumet M, Vargas A, Gurny R, Delie F. Nanoparticles for drug delivery: the need for precision in reporting particle size parameters. Eur. J. Pharm. BioPharm. 69(1), 1–9 (2008).
  Medline CASGoogle Scholar