1,355
Views
409
CrossRef citations to date
0
Altmetric
Review

Nano-microparticles as immune adjuvants: correlating particle sizes and the resultant immune responses

, &
Pages 1095-1107 | Published online: 09 Jan 2014

References

  • Davis JP. Experience with hepatitis A and B vaccines. Am. J. Med.118(10 Suppl. 1), 7–15 (2005).
  • Look M, Bandyopadhyay A, Blum JS, Fahmy TM. Application of nanotechnologies for improved immune response against infectious diseases in the developing world. Adv. Drug Deliv. Rev.62(4–5), 378–393 (2009).
  • O’Hagan DT, Valiante NM. Recent advances in the discovery and delivery of vaccine adjuvants. Nat. Rev. Drug Discov.2(9), 727–735 (2003).
  • Perrie Y, Mohammed AR, Kirby DJ, McNeil SE, Bramwell VW. Vaccine adjuvant systems: enhancing the efficacy of sub-unit protein antigens. Int. J. Pharm.364(2), 272–280 (2008).
  • Copland MJ, Baird MA, Rades T et al. Liposomal delivery of antigen to human dendritic cells. Vaccine21(9–10), 883–890 (2003).
  • Schijns V. Immunological concepts for vaccine adjuvant activity. Curr. Opin. Immunol.12(4), 456–463 (2000).
  • Caputo A, Sparnacci K, Ensoli B, Tondelli L. Functional polymeric nano/microparticles for surface adsorption and delivery of protein and DNA vaccines. Curr. Drug Deliv.5(4), 230–242 (2008).
  • Petrovsky N, Aguilar JC. Vaccine adjuvants: current state and future trends. Immunol. Cell Biol.82(5), 488–496 (2004).
  • Chang S, Warner J, Liang L, Fairman J. A novel vaccine adjuvant for recombinant flu antigens. Biologicals37(3), 141–147 (2009).
  • Singh M, Briones M, Ott G, O’Hagan DT. Cationic microparticles: a potent delivety system for DNA vaccines. Proc. Natl Acad. Sci. USA97, 811–816 (2000).
  • Kalkanidis M, Pietersz GA, Xiang SD et al. Methods for nano-particle based vaccine formulation and evaluation of their immunogenicity. Methods40(1), 20–29 (2006).
  • Peek LJ, Middaugh CR, Berkland C. Nanotechnology in vaccine delivery. Adv. Drug Deliv. Rev.60(8), 915–928 (2008).
  • Scheerlinck J-PY, Greenwood DLV. Virus-sized vaccine delivery systems. Drug Discov. Today13(19–20), 882–887 (2008).
  • Aguilar JC, Rodríguez EG. Vaccine adjuvants revisited. Vaccine25(19), 3752–3762 (2007).
  • O’Hagan DT, Singh M. Microparticles as vaccine adjuvants and delivery systems. Expert Rev. Vaccines2, 269–283 (2003).
  • Schmidt CS, Morrow WJW, Sheikh NA. Smart adjuvants. Expert Rev. Vaccines6, 391–400 (2007).
  • SayIn B, Somavarapu S, Li XW, Sesardic D, Senel S, Alpar OH. TMC-MCC (N-trimethyl chitosan-mono-N-carboxymethyl chitosan) nanocomplexes for mucosal delivery of vaccines. Eur. J. Pharm. Sci.38(4), 362–369 (2009).
  • Gómez S, Gamazo C, San Roman B et al. A novel nanoparticulate adjuvant for immunotherapy with Lolium perenne. J. Immunol. Methods348(1–2), 1–8 (2009).
  • Gunaseelan S, Gunaseelan K, Deshmukh M, Zhang X, Sinko PJ. Surface modifications of nanocarriers for effective intracellular delivery of anti-HIV drugs. Adv. Drug Deliv. Rev.62(4–5), 518–531 (2010).
  • Reed SG, Bertholet S, Coler RN, Friede M. New horizons in adjuvants for vaccine development. Trends Immunol.30(1), 23–32 (2009).
  • Jones KS. Biomaterials as vaccine adjuvants. Biotechnol. Progress24(4), 807–814 (2008).
  • Mallapragada SK, Narasimhan B. Immunomodulatory biomaterials. Int. J. Pharm.364(2), 265–271 (2008).
  • Thomas C, Gupta V, Ahsan F. Influence of surface charge of PLGA particles of recombinant hepatitis B surface antigen in enhancing systemic and mucosal immune responses. Int. J. Pharm.379(1), 41–50 (2009).
  • Reddy ST, Rehor A, Schmoekel HG, Hubbell JA, Swartz MA. In vivo targeting of dendritic cells in lymph nodes with poly(propylene sulfide) nanoparticles. J. Controlled Release112(1), 26–34 (2006).
  • Walter E, Dreher D, Kok M et al. Hydrophilic poly(D,L-lactide-co-glycolide) microspheres for the delivery of DNA to human-derived macrophages and dendritic cells. J. Controlled Release76(1–2), 149–168 (2001).
  • Rice-Ficht AC, Arenas-Gamboa AM, Kahl-McDonagh MM, Ficht TA. Polymeric particles in vaccine delivery. Curr. Opin. Microbiol.13(1), 106–112 (2009).
  • Thomasin C, Corradin G, Men Y, Merkle HP, Gander B. Tetanus toxoid and synthetic malaria antigen containing poly(lactide)/poly(lactide-co-glycolide) microspheres: importance of polymer degradation and antigen release for immune response. J. Controlled Release41(1–2), 131–145 (1996).
  • Slütter B, Soema PC, Ding Z, Verheul R, Hennink W, Jiskoot W. Conjugation of ovalbumin to trimethyl chitosan improves immunogenicity of the antigen. J. Controlled Release143(2), 207–214 (2010).
  • O’Hagan DT. Microparticles and polymers for the mucosal delivery of vaccines. Adv. Drug Deliv. Rev.34(2–3), 305–320 (1998).
  • Kazzaz J, Neidleman J, Singh M, Ott G, O’Hagan DT. Novel anionic microparticles are a potent adjuvant for the induction of cytotoxic T lymphocytes against recombinant p55 gag from HIV-1. J. Controlled Release67(2–3), 347–356 (2000).
  • Jain S, Yap WT, Irvine DJ. Synthesis of protein-loaded hydrogel particles in an aqueous two-phase system for coincident antigen and CpG oligonucleotide delivery to antigen-presenting cells. Biomacromolecules6(5), 2590–2600 (2005).
  • Shen Z, Reznikoff G, Dranoff G, Rock K. Cloned dendritic cells can present exogenous antigens on both MHC class I and class II molecules. J. Immunol.158(6), 2723–2730 (1997).
  • Sharma S, Mukkur TKS, Benson HAE, Chen Y. Pharmaceutical aspects of intranasal delivery of vaccines using particulate systems. J. Pharm. Sci.98(3), 812–843 (2009).
  • Katare YK, Muthukumaran T, Panda AK. Influence of particle size, antigen load, dose and additional adjuvant on the immune response from antigen loaded PLA microparticles. Int. J. Pharm.301(1–2), 149–160 (2005).
  • 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).
  • Gutierro I, Hernández RM, Igartua M, Gascón AR, Pedraz JL. Size dependent immune response after subcutaneous, oral and intranasal administration of BSA loaded nanospheres. Vaccine21(1–2), 67–77 (2002).
  • Jung T, Kamm W, Breitenbach A, Hungerer K-D, Hundt E, Kissel T. Tetanus toxoid loaded nanoparticles from sulfobutylated poly(vinyl alcohol)-graft-poly(lactide-co-glycolide): evaluation of antibody response after oral and nasal application in mice. Pharm. Res.18(3), 352–360 (2001).
  • Vila A, Sanchez A, Evora C, Soriano I, Jato J, Alonso M. PEG-PLA nanoparticles as carriers for nasal vaccine delivery. J. Aerosol Med.17, 174–185 (2004).
  • 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).
  • Manocha M, Pal PC, Chitralekha KT et al. Enhanced mucosal and systemic immune response with intranasal immunization of mice with HIV peptides entrapped in PLG microparticles in combination with Ulex Europaeus-I lectin as M cell target. Vaccine23(48–49), 5599–5617 (2005).
  • Ying M, Gander B, Merkle HP, Corradin G. Induction of sustained and elevated immune responses to weakly immunogenic synthetic malarial peptides by encapsulation in biodegradable polymer microspheres. Vaccine14(15), 1442–1450 (1996).
  • Panyam J, Labhasetwar V. Biodegradable nanoparticles for drug and gene delivery to cells and tissue. Adv. Drug Deliv. Rev.55(3), 329–347 (2003).
  • Elamanchili P, Diwan M, Cao M, Samuel J. Characterization of poly(D,L,-lactic-co-glycolic acid) based nanoparticulate system for enhanced delivery of antigens to dendritic cells. Vaccine22(19), 2406–2412 (2004).
  • Cui Z, Mumper RJ. Topical immunization using nanoengineered genetic vaccines. J. Controlled Release81(1–2), 173–184 (2002).
  • Cui Z, Mumper RJ. Genetic Immunization Using nanoparticles engineered from microemulsion precursors. Pharm. Res.19(7), 939–946 (2002).
  • Sloat BR, Sandoval MA, Hau AM, He Y, Cui Z. Strong antibody responses induced by protein antigens conjugated onto the surface of lecithin-based nanoparticles. J. Controlled Release141(1), 93–100 (2010).
  • Tobío M, Gref R, Sánchez A, Langer R, Alonso MJ. Stealth PLA-PEG nanoparticles as protein carriers for nasal administration. Pharm. Res.15(2), 270–275 (1998).
  • Rieger J, Freichels H, Imberty A et al. Polyester nanoparticles presenting mannose residues: toward the development of new vaccine delivery systems combining biodegradability and targeting properties. Biomacromolecules10(3), 651–657 (2009).
  • Andrianov AK, Marin A, Roberts BE. Polyphosphazene polyelectrolytes: a link between the formation of noncovalent complexes with antigenic proteins and immunostimulating activity. Biomacromolecules6(3), 1375–1379 (2005).
  • Zwiorek K, Bourquin C, Battiany J et al. Delivery by cationic gelatin nanoparticles strongly increases the immunostimulatory effects of CpG oligonucleotides. Pharm. Res.25(3), 551–562 (2008).
  • Coppi G, Iannuccelli V, Sala N, Bondi M. Alginate microparticles for polymyxin B Peyer’s patches uptake: microparticles for antibiotic oral administration. J. Microencap. Micro Nano Carriers21(8), 829–839 (2004).
  • Okada H, Toguchi H. Biodegradable microspheres in drug delivery. Crit. Rev. Ther. Drug Carrier Syst.12(1), 1–99 (1995).
  • Florindo HF, Pandit S, Lacerda L, Gonçalves LMD, Alpar HO, Almeida AJ. The enhancement of the immune response against S. equi antigens through the intranasal administration of poly-[var e]-caprolactone-based nanoparticles. Biomaterials30(5), 879–891 (2009).
  • Freitas S, Merkle HP, Gander B. Microencapsulation by solvent extraction/evaporation: reviewing the state of the art of microsphere preparation process technology. J. Controlled Release102(2), 313–332 (2005).
  • 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).
  • Sharp F, Ruane D, Claas B et al. Uptake of particulate vaccine adjuvants by dendritic cells activates the NALP3 inflammasome. Proc. Natl Acad. Sci. USA106, 870–875 (2009).
  • Kreuter J. Nanoparticles and microparticles for drug and vaccine delivery. J. Anat.189, 503–505 (1996).
  • Mumper RJ, Cui Z, Oyewumi MO. Nanotemplate engineering of cell specific nanoparticles. J. Dispers. Sci. Technol.24(3), 569–588 (2003).
  • Monfardini C, Veronese M. Stabilization of substances in circulation. Bioconjug. Chem.9, 418–450 (1998).
  • Kim GJ, Nie S. Targeted cancer nanotherapy. Mater. Today8(8 Suppl. 1), 28–33 (2005).
  • Wu NZ, Da D, Rudoll TL, Needham D, Whorton AR, Dewhirst MW. Increased microvascular permeability contributes to preferential accumulation of stealth liposomes in tumor tissue. Cancer Res.53(16), 3765–3770 (1993).
  • Xiang SD, Scholzen A, Minigo G et al. Pathogen recognition and development of particulate vaccines: does size matter? Methods40(1), 1–9 (2006).
  • Kanchan V, Panda AK. Interactions of antigen-loaded polylactide particles with macrophages and their correlation with the immune response. Biomaterials28(35), 5344–5357 (2007).
  • Johansen P, Estevez F, Zurbriggen R et al. Towards clinical testing of a single-administration tetanus vaccine based on PLA/PLGA microspheres. Vaccine19(9–10), 1047–1054 (2000).
  • Johansen P, Gander B, Merkle HP, Sesardic D. Ambiguities in the preclinical quality assessment of microparticulate vaccines. Trends Biotechnol.18(5), 203–211 (2000).
  • Caputo A, Brocca-Cofano E, Castaldello A et al. Characterization of immune responses elicited in mice by intranasal co-immunization with HIV-1 Tat, gp140 DV2Env and/or SIV Gag proteins and the nontoxicogenic heat-labile Escherichia coli enterotoxin. Vaccine26(9), 1214–1227 (2008).
  • Mann JFS, 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. Vaccine27(27), 3643–3649 (2009).
  • Cruz LJ, Tacken PJ, Fokkink R et al. Targeted PLGA nano- but not microparticles specifically deliver antigen to human dendritic cells via DC-SIGN in vitro. J. Controlled Release (2010) (In Press).
  • Newman KD, Elamanchili P, Kwon GS, Samuel J. Uptake of poly(D,L-lactic-co-glycolic acid) microspheres by antigen-presenting cells in vivoJ. Biomed. Mater. Res.60(3), 480–486 (2002).
  • Tabata Y, Inoue Y, Ikada Y. Size effect on systemic and mucosal immune responses induced by oral administration of biodegradable microspheres. Vaccine14(17–18), 1677–1685 (1996).
  • Panyam J, Labhasetwar V. Dynamics of endocytosis and exocytosis ofpoly(D,L-lactide-co-glycolide) nanoparticles in vascular smooth muscle cells. Pharm. Res.20(2), 212–220 (2003).
  • Horisawa E, Kubota K, Tuboi I et al. Size-dependency of D,L-lactide/glycolide copolymer particulates for intra-articular delivery system on phagocytosis in rat synovium. Pharm. Res.19(2), 132–139 (2002).
  • Doe B, Selby M, Barnett S, Baenziger J, Walker CM. Induction of cytotoxic T lymphocytes by intramuscular immunization with plasmid DNA is facilitated by bone marrow-derived cells. Proc. Natl Acad. Sci. USA16, 8578–8583 (1996).
  • Zinkernagel RM, Ehl S, Aichele P, Oehen S, Kündig T, Hengartner H. Antigen localisation regulates immune responses in a dose- and time-dependent fashion: a geographical view of immune reactivity. Immunol. Rev.156(1), 199–209 (1997).
  • Bramwell VW, Perrie Y. Particulate delivery systems for vaccines: what can we expect? J. Pharm. Pharmacol.58, 717–728 (2006).
  • Brewer JM, Pollock KGJ, Tetley L, Russell DG. Vesicle size influences the trafficking, processing, and presentation of antigens in lipid vesicles. J. Immunol.173(10), 6143–6150 (2004).
  • Mottram PL, Leong D, Crimeen-Irwin B et al. Type 1 and 2 immunity following vaccination is influenced by nanoparticle size: formulation of a model vaccine for respiratory syncytial virus. Mol. Pharm.4(1), 73–84 (2006).
  • Audran R, Peter K, Dannull J et al. Encapsulation of peptides in biodegradable microspheres prolongs their MHC class-I presentation by dendritic cells and macrophages in vitro. Vaccine21(11–12), 1250–1255 (2003).
  • Balasse E, Odot J, Gatouillat G, Andry M-C, Madoulet C. Enhanced immune response induced by BSA loaded in hydroxyethylstarch microparticles. Int. J. Pharm.353(1–2), 131–138 (2008).
  • Reddy ST, van der Vlies AJ, Simeoni E et al. Exploiting lymphatic transport and complement activation in nanoparticle vaccines. Nat. Biotech.25(10), 1159–1164 (2007).
  • Manolova V, Flace A, Bauer M, Schwarz K, Saudan P, Bachmann Martin F. Nanoparticles target distinct dendritic cell populations according to their size. Eur. J. Immunol.38(5), 1404–1413 (2008).
  • Mutwiri G, Benjamin P, Soita H, Babiuk LA. Co-administration of polyphosphazenes with CpG oligodeoxynucleotides strongly enhances immune responses in mice immunized with Hepatitis B virus surface antigen. Vaccine26(22), 2680–2688 (2008).
  • Briones M, Singh M, Ugozzoli M et al. The preparation, characterization, and evaluation of cationic microparticles for DNA vaccine delivery. Pharm. Res.18(5), 709–712 (2001).
  • O’Hagan D, Singh M, Ugozzoli M et al. Induction of potent immune responses by cationic microparticles with adsorbed human immunodeficiency virus DNA vaccines. J. Virol.75(19), 9037–9043 (2001).
  • Borges O, Borchard G, Verhoef JC, de Sousa A, Junginger HE. Preparation of coated nanoparticles for a new mucosal vaccine delivery system. Int. J. Pharm.299(1–2), 155–166 (2005).
  • 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).
  • Neutra MR, Kozlowski PA. Mucosal vaccines: the promise and the challenge. Nat. Rev. Immunol.6(2), 148–158 (2006).
  • Nakaoka R, Inoue Y, Tabata Y, Ikada Y. Size effect on the antibody production induced by biodegradable microspheres containing antigen. Vaccine14(13), 1251–1256 (1996).
  • Mohammed AR, Bramwell VW, Coombes AGA, Perrie Y. Lyophilisation and sterilisation of liposomal vaccines to produce stable and sterile products. Methods40(1), 30–38 (2006).
  • Memisoglu-Bilensoy E, Hincal AA. Sterile, injectable cyclodextrin nanoparticles: Effects of γ irradiation and autoclaving. Int. J. Pharm.311(1–2), 203–208 (2006).
  • Konan YN, Cerny R, Favet J, Berton M, Gurny R, Allémann E. Preparation and characterization of sterile sub-200 nm meso-tetra(4-hydroxylphenyl)porphyrin-loaded nanoparticles for photodynamic therapy. Eur. J. Pharm. Biopharm.55(1), 115–124 (2003).
  • Konan YN, Gurny R, Allémann E. Preparation and characterization of sterile and freeze-dried sub-200 nm nanoparticles. Int. J. Pharm.233(1–2), 239–252 (2002).
  • Masson V, Maurin F, Fessi H, Devissaguet JP. Influence of sterilization processes on poly([var e]-caprolactone) nanospheres. Biomaterials18(4), 327–335 (1997).
  • Sintzel MB, Merkli A, Tabatabay C, Gurny R. Influence of irradiation sterilization on polymers used as drug carriers: a review. Drug Develop. Industrial Pharm.23(9), 857–878 (1997).
  • Mehnert W, Mäder K. Solid lipid nanoparticles: production, characterization and applications. Adv. Drug Deliv. Rev.47(2–3), 165–196 (2001).
  • Rollot JM, Couvreur P, Roblot-Treupel L, Puisieux F. Physicochemical and morphological characterization of polyisobutyl cyanoacrylate nanocapsules. J. Pharm. Sci.75(4), 361–364 (1986).
  • Bozdag S, Dillen K, Vandervoort J, Ludwig A. The effect of freeze-drying with different cryoprotectants and γ-irradiation sterilization on the characteristics of ciprofloxacin HCl-loaded poly(D,L-lactide-glycolide) nanoparticles. J. Pharm. Pharmacol.57, 699–708 (2005).
  • Quintanar-Guerrero D, Ganem-Quintanar A, Allemann E, Fessi H, Doelker E. Influence of the stabilizer coating layer on the purification and freeze-drying of poly(D,L-lactic acid) nanoparticles prepared by an emulsion-diffusion technique. J. Microencapsul.15(1), 107–119 (1998).
  • Glavas-Dodov M, Fredro-Kumbaradzi E, Goracinova K et al. The effects of lyophilization on the stability of liposomes containing 5-FU. Int. J. Pharm.291(1–2), 79–86 (2005).
  • Chen D, Kristensen D. Opportunities and challenges of developing thermostable vaccines. Expert Rev. Vaccines8, 547–557 (2009).
  • Sloat BS, Sandoval MA, Cui Z. Towards preserving the immunogenicity of protein antigens carried by nanoparticles while avoiding the cold chain. Int. J. Pharm.393(1–2), 197–202 (2010).
  • Nixon DF, Hioe C, Chen P-D et al. Synthetic peptides entrapped in microparticles can elicit cytotoxic T cell activity. Vaccine14(16), 1523–1530 (1996).
  • 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).
  • Igartua M, Hernández RM, Esquisabel A, Gascón AR, Calvo MB, Pedraz JL. Enhanced immune response after subcutaneous and oral immunization with biodegradable PLGA microspheres. J. Controlled Release56(1–3), 63–73 (1998).

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.