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Review

The long-term potential of biodegradable poly(lactideco-glycolide) microparticles as the next-generation vaccine adjuvant

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Pages 1731-1742 | Published online: 09 Jan 2014

References

  • Poland GA, Murray D, Bonilla-Guerrero R. New vaccine development. BMJ324(7349), 1315–1319 (2002).
  • Rappuoli R, Miller HI, Falkow S. Medicine. The intangible value of vaccination. Science297(5583), 937–939 (2002).
  • Bonanni P. Demographic impact of vaccination: a review. Vaccine17(Suppl. 3), S120–S125 (1999).
  • Samant Y, Lanjewar H, Parker D, Block L, Tomar GS, Stein B. Evaluation of the cold-chain for oral polio vaccine in a rural district of India. Pub. Health Rep.122(1), 112–121 (2007).
  • O’Hagan DT, De Gregorio E. The path to a successful vaccine adjuvant – ‘The long and winding road’. Drug Discov. Today.14(11–12), 541–551 (2009).
  • Pasare C, Medzhitov R. Toll-like receptors: balancing host resistance with immune tolerance. Curr. Opin. Immunol.15(6), 677–682 (2003).
  • Dorner F, Barrett PN. Vaccine technology: looking to the future. Ann. Med.31(1), 51–60 (1999).
  • Casella CR, Mitchell TC. Putting endotoxin to work for us: monophosphoryl lipid A as a safe and effective vaccine adjuvant. Cell Mol. Life Sci.65(20), 3231–3240 (2008).
  • Mullen GED, Aebig JA, Dobrescu G et al. Enhanced antibody production in mice to the malaria antigen AMA 1 by CPG 7909 requires physical association of CpG and antigen. Vaccine25(29), 5343–5347 (2007).
  • Hogenesch H. Mechanisms of stimulation of the immune response by aluminum adjuvants. Vaccine20, S34–S39 (2002).
  • Langer R. Polymeric delivery systems for controlled drug release. Chem. Eng. Communicat.6(1–3), 1–48 (1980).
  • Wischke C, Schwendeman SP. Principles of encapsulating hydrophobic drugs in PLA/PLGA microparticles. Int. J. Pharm.364(2), 298–327 (2008).
  • Saez V, Hernandez JR, Peniche C. Microspheres as delivery systems for the controlled release of peptides and proteins. Biotecnol. Aplicada24, 108–116 (2007).
  • Brown LR. Commercial challenges of protein drug delivery. Exp. Opin. Drug Deliv.2(1), 29–42 (2005).
  • Bramwell VW, Eyles JE, Alpar HO. Particulate delivery systems for biodefense subunit vaccines. Adv. Drug Deliv. Rev.57(9), 1247–1265 (2005).
  • Johansen P, Men Y, Merkle HP, Gander B. Revisiting PLA/PLGA microspheres: an analysis of their potential in parenteral vaccination. Eur. J. Pharm. Biopharm.50(1), 129–146 (2000).
  • Gupta RK, Singh M, O’Hagan DT. Poly(lactide-co-glycolide) microparticles for the development of single-dose controlled-release vaccines. Adv. Drug Deliv. Rev.32(3), 225–246 (1998).
  • Johansen P, Corradin G, Merkle HP, Gander B. Release of tetanus toxoid from adjuvants and PLGA microspheres: how experimental set-up and surface adsorption fool the pattern. J. Control. Release56(1–3), 209–217 (1998).
  • 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).
  • Singh M, Li XM, Wang H et al. Immunogenicity and protection in small-animal models with controlled-release tetanus toxoid microparticles as a single-dose vaccine. Infect. Immun.65(5), 1716–1721 (1997).
  • Peyre M, Sesardic D, Merkle HP, Gander B, Johansen P. An experimental divalent vaccine based on biodegradable microspheres induces protective immunity against tetanus and diphtheria. J. Pharm. Sci.92(5), 957–966 (2003).
  • Singh M, Li XM, Mcgee JP et al. Controlled release microparticles as a single dose hepatitis B vaccine: evaluation of immunogenicity in mice. Vaccine15(5), 475–481 (1997).
  • Shi L, Caulfield MJ, Chern RT, Wilson RR, Sanyal G, Volkin DB. Pharmaceutical and immunological evaluation of a single-shot hepatitis B vaccine formulated with PLGA microspheres. J. Pharm. Sci.91(4), 1019–1035 (2002).
  • Feng L, Qi XR, Zhou XJ et al. Pharmaceutical and immunological evaluation of a single-dose hepatitis B vaccine using PLGA microspheres. J. Control. Release112(1), 35–42 (2006).
  • Johansen P, Tamber H, Merkle HP, Gander B. Diphtheria and tetanus toxoid microencapsulation into conventional and end-group alkylated PLA/PLGAs. Eur. J. Pharm. Biopharm.47(3), 193–201 (1999).
  • Singh M, Singh A, Talwar GP. Controlled delivery of diphtheria toxoid using biodegradable poly(D,L-lactide) microcapsules. Pharm. Res.8(7), 958–961 (1991).
  • Singh M, Li XM, Wang H et al. Controlled release microparticles as a single dose diphtheria toxoid vaccine: immunogenicity in small animal models. Vaccine16(4), 346–352 (1998).
  • Tacket CO, Reid RH, Boedeker EC et al. Enteral immunization and challenge of volunteers given enterotoxigenic E. coli CFA/II encapsulated in biodegradable microspheres. Vaccine12(14), 1270–1274 (1994).
  • Crotts G, Park TG. Protein delivery from poly(lactic-co-glycolic acid) biodegradable microspheres: release kinetics and stability issues. J. Microencapsulat.15(6), 699–713 (1998).
  • Xie JW, Wang CH. Encapsulation of proteins in biodegradable polymeric microparticles using electrospray in the Taylor Cone-Jet mode. Biotechnol. Bioeng.97(5), 1278–1290 (2007).
  • Houchin ML, Topp EM. Chemical degradation of peptides and proteins in PLGA: a review of reactions and mechanisms. J. Pharmaceut. Sci.97(7), 2395–2404 (2008).
  • Park TG, Mok H, Park JW. Microencapsulation of PEGylated adenovirus within PLGA microspheres for enhanced stability and gene transfection efficiency. Pharmaceut. Res.24(12), 2263–2269 (2007).
  • Igartua M, Hernandez RM, Esquisabel A, Gascon AR, Calvo MB, Pedraz JL. Stability of BSA encapsulated into PLGA microspheres using PAGE and capillary electrophoresis. Intl J. Pharmaceut.169(1), 45–54 (1998).
  • Perez C, Griebenow K. Improved activity and stability of lysozyme at the water/CH2Cl2 interface: enzyme unfolding and aggregation and its prevention by polyols. J. Pharm. Pharmacol.53(9), 1217–1226 (2001).
  • Zhu GZ, Mallery SR, Schwendeman SP. Stabilization of proteins encapsulated in injectable poly (lactide-co-glycolide). Nat. Biotechnol.18(1), 52–57 (2000).
  • Jaganathan KS, Singh P, Prabakaran D, Mishra V, Vyas SP. Development of a single-dose stabilized poly(D,L-lactic-co-glycolic acid) microspheres-based vaccine against hepatitis B. J. Pharm. Pharmacol.56(10), 1243–1250 (2004).
  • Ding AG, Schwendeman SP. Acidic Microclimate pH Distribution in PLGA microspheres monitored by confocal laser scanning microscopy. Pharmaceut. Res.25(9), 2041–2052 (2008).
  • Langer R. Drug delivery and targeting. Nature392(6679), 5–10 (1998).
  • Oyewumi MO, Kumar A, Cui Z. Nano-microparticles as immune adjuvants: correlating particle sizes and the resultant immune responses. Expert Rev. Vaccines9(9), 1095–1107 (2010).
  • Zhao X, Jain S, Benjamin Larman H, Gonzalez S, Irvine DJ. Directed cell migration via chemoattractants released from degradable microspheres. Biomaterials26(24), 5048–5063 (2005).
  • Singh M, Singh O, Talwar GP. Biodegradable delivery system for a birth control vaccine: immunogenicity studies in rats and monkeys. Pharm. Res.12(11), 1796–1800 (1995).
  • Jain RA. The manufacturing techniques of various drug loaded biodegradable poly(lactide-co-glycolide) (PLGA) devices. Biomaterials21(23), 2475–2490 (2000).
  • Van De Weert M, Hennink WE, Jiskoot W. Protein instability in poly(lactic-co-glycolic acid) microparticles. Pharm. Res.17(10), 1159–1167 (2000).
  • Zhu G, Schwendeman SP. Stabilization of proteins encapsulated in cylindrical poly(lactide-co-glycolide) implants: mechanism of stabilization by basic additives. Pharm. Res.17(3), 351–357 (2000).
  • Jabbal-Gill I, Lin W, Jenkins P et al. Potential of polymeric lamellar substrate particles (PLSP) as adjuvants for vaccines. Vaccine18(3–4), 238–250 (1999).
  • Jiang W, Schwendeman SP. Stabilization of a model formalinized protein antigen encapsulated in poly(lactide-co-glycolide)-based microspheres. J. Pharm. Sci.90(10), 1558–1569 (2001).
  • Jiang W, Schwendeman SP. Stabilization of tetanus toxoid encapsulated in PLGA microspheres. Mol. Pharm.5(5), 808–817 (2008).
  • Singh M, Chesko J, Kazzaz J et al. Adsorption of a novel recombinant glycoprotein from HIV (Env gp120dV2 SF162) to anionic PLG microparticles retains the structural integrity of the protein, whereas encapsulation in PLG microparticles does not. Pharm. Res.21(12), 2148–2152 (2004).
  • Singh M, Kazzaz J, Chesko J et al. Anionic microparticles are a potent delivery system for recombinant antigens from Neisseria meningitidis serotype B. J. Pharm. Sci.93(2), 273–282 (2004).
  • Singh M, Kazzaz J, Ugozzoli M, Malyala P, Chesko J, O’Hagan DT. Polylactide-co-glycolide microparticles with surface adsorbed antigens as vaccine delivery systems. Curr. Drug Deliv.3(1), 115–120 (2006).
  • Chesko J, Kazzaz J, Ugozzoli M, O’Hagan DT, Singh M. An investigation of the factors controlling the adsorption of protein antigens to anionic PLG microparticles. J. Pharm. Sci.94(11), 2510–2519 (2005).
  • Jain S, Malyala P, Pallaoro M et al. A two-stage strategy for sterilization of poly(lactide-co-glycolide) particles by γ-irradiation does not impair their potency for vaccine delivery. J. Pharm. Sci.100(2), 646–654 (2011).
  • Lamalle-Bernard D, Munier S, Compagnon C et al. Coadsorption of HIV-1 p24 and gp120 proteins to surfactant-free anionic PLA nanoparticles preserves antigenicity and immunogenicity. J. Control. Release115(1), 57–67 (2006).
  • Luten J, Van Nostrum CF, De Smedt SC, Hennink WE. Biodegradable polymers as non-viral carriers for plasmid DNA delivery. J. Control. Release126(2), 97–110 (2008).
  • Denis-Mize KS, Dupuis M, Mackichan ML et al. Plasmid DNA adsorbed onto cationic microparticles mediates target gene expression and antigen presentation by dendritic cells. Gene. Ther.7(24), 2105–2112 (2000).
  • Mollenkopf HJ, Dietrich G, Fensterle J et al. Enhanced protective efficacy of a tuberculosis DNA vaccine by adsorption onto cationic PLG microparticles. Vaccine22(21–22), 2690–2695 (2004).
  • O’Hagan DT, Singh M, Dong C et al. Cationic microparticles are a potent delivery system for a HCV DNA vaccine. Vaccine23(5), 672–680 (2004).
  • O’Hagan DT, Singh M, Ulmer JB. Microparticles for the delivery of DNA vaccines. Immunol. Rev.199, 191–200 (2004).
  • Singh M, Briones M, Ott G, O’Hagan D. Cationic microparticles: a potent delivery system for DNA vaccines. Proc. Natl Acad. Sci. USA97(2), 811–816 (2000).
  • Singh M, Vajdy M, Gardner J, Briones M, O’Hagan D. Mucosal immunization with HIV-1 gag DNA on cationic microparticles prolongs gene expression and enhances local and systemic immunity. Vaccine20(3–4), 594–602 (2001).
  • Walter E, Moelling K, Pavlovic J, Merkle HP. Microencapsulation of DNA using poly(D,L-lactide-co-glycolide): stability issues and release characteristics. J. Control. Release61(3), 361–374 (1999).
  • Ando S, Putnam D, Pack DW, Langer R. PLGA microspheres containing plasmid DNA: preservation of supercoiled DNA via cryopreparation and carbohydrate stabilization. J. Pharmaceut. Sci.88(1), 126–130 (1999).
  • Briones M, Singh M, Ugozzoli M et al. The preparation, characterization, and evaluation of cationic microparticles for DNA vaccine delivery. Pharmaceut. Res.18(5), 709–712 (2001).
  • Spearman P, Lally MA, Elizaga M et al. A trimeric, V2-Deleted HIV-1 envelope glycoprotein vaccine elicits potent neutralizing antibodies but limited breadth of neutralization in human volunteers. J. Infect. Discov.203(8), 1165–1173 (2011).
  • Hayakawa I, Kajihara J, Morikawa K, Oda M, Fujio Y. Denaturation of bovine serum-albumin (Bsa) and ovalbumin by high-pressure, heat and chemicals. J. Food Sci.57(2), 288–292 (1992).
  • Stern AM, Markel H. The history of vaccines and immunization: familiar patterns, new challenges. Health Affairs24(3), 611–621 (2005).
  • Athanasiou KA, Niederauer GG, Agrawal CM. Sterilization, toxicity, biocompatibility and clinical applications of polylactic acid polyglycolic acid copolymers. Biomaterials17(2), 93–102 (1996).
  • Carrascosa C, Espejo L, Torrado S, Torrado JJ. Effect of γ-sterilization process on PLGA microspheres loaded with insulin-like growth factor-I (IGF-I). J. Biomater. Applicat.18(2), 95–108 (2003).
  • Alonso MJ, Gupta RK, Min C, Siber GR, Langer R. Biodegradable microspheres as controlled-release tetanus toxoid delivery systems. Vaccine12(4), 299–306 (1994).
  • Guillon C, Mayol K, Terrat C et al. Formulation of HIV-1 tat and p24 antigens by PLA nanoparticles or MF59 impacts the breadth, but not the magnitude, of serum and faecal antibody responses in rabbits. Vaccine25(43), 7491–7501 (2007).
  • Quintilio W, Takata CS, Sant’anna OA, Da Costa MH, Raw I. Evaluation of a diphtheria and tetanus PLGA microencapsulated vaccine formulation without stabilizers. Curr. Drug Deliv.6(3), 297–304 (2009).
  • O’Hagan DT, Wack A, Podda A. MF59 is a safe and potent vaccine adjuvant for flu vaccines in humans: what did we learn during its development? Clin. Pharmacol. Therapeut.82(6), 740–744 (2007).
  • O’Hagan DT. MF59 is a safe and potent vaccine adjuvant that enhances protection against influenza virus infection. Expert Rev. Vaccines6(5), 699–710 (2007).
  • Paschke R, Pollok M, Geiger H et al. Increased immunogenicity with an MF59-adjuvanted influenza vaccine compared to a conventional sub-unit vaccine in renal transplant recipients. J. Prevent. Med. Hygiene44, 79–84 (2003).
  • Esposito S, Pugni L, Daleno C et al. Influenza A/H1N1 MF59-adjuvanted vaccine in preterm and term children aged 6 to 23 months. Pediatrics127(5), E1161–E1168 (2011).
  • Kazzaz J, Singh M, Ugozzoli M, Chesko J, Soenawan E, O’Hagan DT. Encapsulation of the immune potentiators MPL and RC529 in PLG microparticles enhances their potency. J. Control. Release110(3), 566–573 (2006).
  • Stone GW, Barzee S, Snarsky V et al. Nanoparticle-delivered multimeric soluble CD40L DNA combined with toll-like receptor agonists as a treatment for melanoma. PLoS One4(10), e7334 (2009).
  • 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).
  • Hamdy S, Molavi O, Ma Z et al. Co-delivery of cancer-associated antigen and toll-like receptor 4 ligand in PLGA nanoparticles induces potent CD8+ T cell-mediated anti-tumor immunity. Vaccine26(39), 5046–5057 (2008).
  • Diwan M, Elamanchili P, Cao M, Samuel J. Dose sparing of CpG oligodeoxynucleotide vaccine adjuvants by nanoparticle delivery. Curr. Drug Deliv.1(4), 405–412 (2004).
  • Malyala P, O’hagan DT, Singh M. Enhancing the therapeutic efficacy of CpG oligonucleotides using biodegradable microparticles. Adv. Drug Deliv. Rev.61(3), 218–225 (2009).
  • Tel J, Lambeck AJ, Cruz LJ, Tacken PJ, De Vries IJ, Figdor CG. Human plasmacytoid dendritic cells phagocytose, process, and present exogenous particulate antigen. J. Immunol.184(8), 4276–4283 (2010).
  • Heit A, Schmitz F, Haas T, Busch DH, Wagner H. Antigen co-encapsulated with adjuvants efficiently drive protective T cell immunity. Eur. J. Immunol.37(8), 2063–2074 (2007).
  • Kasturi SP, Skountzou I, Albrecht RA et al. Programming the magnitude and persistence of antibody responses with innate immunity. Nature470(7335), 543–547 (2011).
  • Westwood A, Elvin SJ, Healey GD, Williamson ED, Eyles JE. Immunological responses after immunisation of mice with microparticles containing antigen and single stranded RNA (polyuridylic acid). Vaccine24(11), 1736–1743 (2006).
  • Wischke C, Zimmermann J, Wessinger B et al. Poly(I:C) coated PLGA microparticles induce dendritic cell maturation. Int. J. Pharm.365(1–2), 61–68 (2009).
  • Lee YR, Lee YH, Im SA et al. Biodegradable nanoparticles containing TLR3 or TLR9 agonists together with antigen enhance MHC-restricted presentation of the antigen. Arch. Pharm. Res.33(11), 1859–1866 (2010).
  • Lima KM, Santos SA, Lima VM, Coelho-Castelo AA, Rodrigues JM Jr, Silva CL. Single dose of a vaccine based on DNA encoding mycobacterial hsp65 protein plus TDM-loaded PLGA microspheres protects mice against a virulent strain of Mycobacterium tuberculosis. Gene Ther.10(8), 678–685 (2003).
  • Van Duin D, Medzhitov R, Shaw AC. Triggering TLR signaling in vaccination. Trends Immunol.27(1), 49–55 (2006).
  • O’Hagan DT, Valiante NM. Recent advances in the discovery and delivery of vaccine adjuvants. Nat. Rev. Drug Discov.2(9), 727–735 (2003).
  • Mutwiri G, Gerdts V, Van Drunen Littel-Van Den Hurk SV et al. Combination adjuvants: the next generation of adjuvants? Expert Rev. Vaccines10(1), 95–107 (2011).
  • Reed SG, Bertholet S, Coler RN, Friede M. New horizons in adjuvants for vaccine development. Trends Immunol.30(1), 23–32 (2009).
  • Dunne A, Marshall NA, Mills KH. TLR based therapeutics. Curr. Opin. Pharmacol.11(4), 404–411 (2011).
  • Weissburg RP, Berman PW, Cleland JL et al. Characterization of the MN gp120 HIV-1 vaccine: antigen binding to alum. Pharm. Res.12(10), 1439–1446 (1995).
  • Elamanchili P, Lutsiak CM, Hamdy S, Diwan M, Samuel J. “Pathogen-mimicking” nanoparticles for vaccine delivery to dendritic cells. J. Immunother.30(4), 378–395 (2007).
  • Groettrup M, Schlosser E, Mueller M et al. TLR ligands and antigen need to be coencapsulated into the same biodegradable microsphere for the generation of potent cytotoxic T lymphocyte responses. Vaccine26(13), 1626–1637 (2008).
  • O’Hagan DT, Singh M. Microparticles as vaccine adjuvants and delivery systems. Expert Rev. Vaccines2(2), 269–283 (2003).
  • 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.183(10), 6186–6197 (2009).
  • Singh M, Chakrapani A, O’Hagan D. Nanoparticles and microparticles as vaccine-delivery systems. Expert Rev. Vaccines6(5), 797–808 (2007).
  • Wesselinova D. Current major cancer targets for nanoparticle systems. Curr. Cancer Drug Targets11(2), 164–183 (2011).
  • Cella M, Sallusto F, Lanzavecchia A. Origin, maturation and antigen presenting function of dendritic cells. Curr. Opin. Immunol.9(1), 10–16 (1997).
  • Desai MP, Labhasetwar V, Walter E, Levy RJ, Amidon Gl. The mechanism of uptake of biodegradable microparticles in Caco-2 cells is size dependent. Pharmaceut. Res.14(11), 1568–1573 (1997).
  • 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).
  • 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. Pharmaceut.301(1–2), 149–160 (2005).
  • Ohagan DT, Jeffery H, Davis SS. Long-term antibody-responses in mice following subcutaneous immunization with ovalbumin entrapped in biodegradable microparticles. Vaccine11(9), 965–969 (1993).
  • Xiang SD, Scholzen A, Minigo G et al. Pathogen recognition and development of particulate vaccines: does size matter? Methods40(1), 1–9 (2006).
  • Bachmann MF, Manolova V, Flace A, Bauer M, Schwarz K, Saudan P. Nanoparticles target distinct dendritic cell populations according to their size. Eur. J. Immunol.38(5), 1404–1413 (2008).
  • Bachmann MF, Jennings GT. Vaccine delivery: a matter of size, geometry, kinetics and molecular patterns. Nat. Rev. Immunol.10(11), 787–796 (2010).
  • Samuelsen M, Nygaard UC, Lovik M. Particle size determines activation of the innate immune system in the lung. Scand. J. Immunol.69(5), 421–428 (2009).
  • 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).
  • Gutierro I, Hernandez RM, Igartua M, Gascon AR, Pedraz JL. Size dependent immune response after subcutaneous, oral and intranasal administration of BSA loaded nanospheres. Vaccine21(1–2), 67–77 (2002).
  • Kanchan V, Panda AK. Interactions of antigen-loaded polylactide particles with macrophages and their correlation with the immune response. Biomaterials28(35), 5344–5357 (2007).
  • Wendorf J, Chesko J, Kazzaz J et al. A comparison of anionic nanoparticles and microparticles as vaccine delivery systems. Hum. Vacc.4(1), 44–49 (2008).
  • Mohanan D, Slutter B, Henriksen-Lacey M et al. Administration routes affect the quality of immune responses: a cross-sectional evaluation of particulate antigen-delivery systems. J. Control. Release147(3), 342–349.
  • Newman KD, Elamanchili P, Kwon GS, Samuel J. Uptake of poly(D,L-lactic-co-glycolic acid) microspheres by antigen-presenting cells in vivo.J. Biomed. Mater. Res.60(3), 480–486 (2002).
  • Reddy ST, Van Der Vlies AJ, Simeoni E et al. Exploiting lymphatic transport and complement activation in nanoparticle vaccines. Nat. Biotechnol.25(10), 1159–1164 (2007).
  • Bhaskar S, Pollock KM, Yoshida M, Lahann J. Towards designer microparticles: simultaneous control of anisotropy, shape, and size. Small6(3), 404–411 (2010).
  • Glangchai LC, Caldorera-Moore M, Shi L, Roy K. Nanoimprint lithography based fabrication of shape-specific, enzymatically-triggered smart nanoparticles. J. Control. Release125(3), 263–272 (2008).
  • Gratton SE, Ropp PA, Pohlhaus PD et al. The effect of particle design on cellular internalization pathways. Proc. Natl Acad. Sci. USA105(33), 11613–11618 (2008).
  • Champion JA, Katare YK, Mitragotri S. Particle shape: a new design parameter for micro- and nanoscale drug delivery carriers. J. Control. Release121(1–2), 3–9 (2007).
  • Steele RH, Limaye S, Cleland B, Chow J, Suranyi MG. Hypersensitivity reactions to the polysorbate contained in recombinant erythropoietin and darbepoietin. Nephrology (Carlton)10(3), 317–320 (2005).
  • Yang CS, Wang YC, Wu YT, Huang HY. Surfactant-free formulation of poly(lactic/glycolic) acid nanoparticles encapsulating functional polypeptide: a technical note. Aaps. Pharmscitech10(4), 1263–1267 (2009).
  • 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. Control. Release67(2–3), 347–356 (2000).
  • O’Hagan DT, Jeffery H, Roberts MJ, Mcgee JP, Davis SS. Controlled release microparticles for vaccine development. Vaccine9(10), 768–771 (1991).
  • Kovaiou RD, Herndler-Brandstetter D, Grubeck-Loebenstein B. Age-related changes in immunity: implications for vaccination in the elderly. Exp. Rev. Mol. Med.9(3), 1–17 (2007).
  • Casares S, Brumeanu TD, Richie TL. The RTS,S malaria vaccine. Vaccine28(31), 4880–4894 (2010).
  • Allison AC, Gregoria G. Liposomes as immunological adjuvants. Nature252(5480), 252–252 (1974).
  • Morein B, Sundquist B, Hoglund S, Dalsgaard K, Osterhaus A. Iscom, a novel structure for antigenic presentation of membrane-proteins from enveloped viruses. Nature308(5958), 457–460 (1984).
  • Ennis FA, Cruz J, Jameson J, Klein M, Burt D, Thipphawong J. Augmentation of human influenza A virus-specific cytotoxic T lymphocyte memory by influenza vaccine and adjuvanted carriers (ISCOMS). Virology259(2), 256–261 (1999).
  • Sun HX, Xie Y, Ye YP. ISCOMs and ISCOMATRIX (TM). Vaccine27(33), 4388–4401 (2009).
  • Okada H, Heya T, Ogawa Y, Toguchi H, Shimamoto T. Sustained pharmacological activities in rats following single and repeated administration of once-a-month injectable microspheres of leuprolide acetate. Pharmaceut. Res.8(5), 584–587 (1991).
  • Dean RL. The preclinical development of medisorb naltrexone, a once a month long acting injection, for the treatment of alcohol dependence. Front. Biosci.10, 643–655 (2005).
  • Quarmby V. Immunogenicity in biotherapeutic development: utility of preclinical data. Presented at: Workshop on Protein Aggregation and Immunogenicity/ Breckenridge, CO, USA, 20 July 2010.
  • Chesko J, Kazzaz J, Ugozzoli M et al. Characterization of antigens adsorbed to anionic PLG microparticles by XPS and TOF-SIMS. J. Pharm. Sci.97(4), 1443–1453 (2008).

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