Peptide/protein vaccine delivery system based on PLGA particles

Human Vaccines and Immunotherapeutics

Volumn 12, Issue 3, 2016, Pages 806-828

  Allahyari, Mojgan ^a   Mohit, Elham ^b  

^a PASTEUR INSTITUTE OF IRAN   (Iran)

^b SHAHID BEHESHTI UNIVERSITY OF MEDICAL SCIENCES   (Iran)

Author keywords

delivery system; micro nano particles; PLGA particle; protein peptide vaccine; TLR ligands

Indexed keywords

CHITOSAN; POLYGLACTIN; SMALL INTERFERING RNA; BIOMATERIAL; DRUG CARRIER; LACTIC ACID; POLYGLYCOLIC ACID; POLYLACTIC ACID-POLYGLYCOLIC ACID COPOLYMER; PROTEIN; SUBUNIT VACCINE;

ALLERGY; CHLAMYDIASIS; COACERVATION; DRUG DELIVERY SYSTEM; ENCAPSULATION; GAMMA IRRADIATION; HEPATITIS B; HUMAN; IMMUNOGENICITY; IMMUNOMODULATION; LEISHMANIASIS; MALARIA; MOUSE; NONHUMAN; PARTICLE SIZE; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PHASE SEPARATION; PROTEIN DEGRADATION; PROTEIN SECRETION; PROTEIN VACCINE DELIVERY SYSTEM; REVIEW; TOXOPLASMOSIS; TUBERCULOSIS; IMMUNOLOGY;

BIOCOMPATIBLE MATERIALS; DRUG CARRIERS; HUMANS; LACTIC ACID; POLYGLYCOLIC ACID; PROTEINS; VACCINES, SUBUNIT;

EID: 84976513957     PISSN: 21645515     EISSN: 2164554X     Source Type: Journal    
DOI: 10.1080/21645515.2015.1102804     Document Type: Review

References (133)

1. S.Jain, D.T.O'Hagan, M.Singh. The long-term potential of biodegradable poly(lactide-co-glycolide) microparticles as the next-generation vaccine adjuvant. Expert Rev Vaccines 2011; 10:1731-42; PMID:22085176; http://dx.doi.org/10.1586/erv.11.126
2. I.Amjadi, M.Rabiee, M.S.Hosseini. Anticancer Activity of Nanoparticles Based on PLGA and its Co-polymer: In-vitro Evaluation. Iran J Pharm Res 2013; 12:623-34; PMID:24523742
3. H.K.Makadia, S.J.Siegel. Poly lactic-co-glycolic acid (PLGA) as biodegradable controlled drug delivery carrier. Polymers 2011; 3:1377-97; PMID:22577513; http://dx.doi.org/10.3390/polym3031377
4. B.Semete, L.Booysen, Y.Lemmer, L.Kalombo, L.Katata, J.Verschoor, H.S.Swai. In vivo evaluation of the biodistribution and safety of PLGA nanoparticles as drug delivery systems. Nanomedicine 2010; 6:662-71; http://dx.doi.org/10.1016/j.nano.2010.02.002
5. A.Mahboubian, S.K.Hashemein, S.Moghadam, F.Atyabi, R.Dinarvand. Preparation and in-vitro evaluation of controlled release PLGA microparticles containing triptoreline. Iran J Pharm Res 2010; 9:369; PMID:24381601
6. Y.Waeckerle-Men, M.Groettrup. PLGA microspheres for improved antigen delivery to dendritic cells as cellular vaccines. Adv Drug Deliv Rev 2005; 57:475-82; PMID:15560953; http://dx.doi.org/10.1016/j.addr.2004.09.007
7. S.Hamdy, A.Haddadi, R.W.Hung, A.Lavasanifar. Targeting dendritic cells with nano-particulate PLGA cancer vaccine formulations. Adv Drug Deliv Rev 2011; 63:943-55; PMID:21679733; http://dx.doi.org/10.1016/j.addr.2011.05.021
8. P.Malyala, D.T.O'Hagan, M.Singh. Enhancing the therapeutic efficacy of CpG oligonucleotides using biodegradable microparticles. Adv Drug Deliv Rev 2009; 61:218-25; PMID:19168103; http://dx.doi.org/10.1016/j.addr.2008.12.009
9. S.Bhatnagar, R.A.Naqvi, R.Ali, D.N.Rao. Preparation of peptide microspheres using tumor antigen-derived peptides. Methods Mol Biol 2014; 1139:443-52; PMID:24619698; http://dx.doi.org/10.1007/978-1-4939-0345-0_34
10. M.van de Weert, W.E.Hennink, W.Jiskoot. Protein instability in poly (lactic-co-glycolic acid) microparticles. Pharm Res 2000; 17:1159-67; PMID:11145219; http://dx.doi.org/10.1023/A:1026498209874
11. L.R.Brown. Commercial challenges of protein drug delivery. Expert Opin Drug Deliv 2005; 2:29-42; PMID:16296733; http://dx.doi.org/10.1517/17425247.2.1.29
12. A.Salvador, M.Igartua, R.M.Hernández, J.L.Pedraz. An overview on the field of micro-and nanotechnologies for synthetic peptide-based vaccines. J Drug Deliv 2011; 2011:181646; PMID:21773041; http://dx.doi.org/10.1155/2011/181646
13. D.Quintanar-Guerrero, E.Allemann, H.Fessi, E.Doelker. Preparation techniques and mechanisms of formation of biodegradable nanoparticles from preformed polymers. Drug Dev Ind Pharm 1998; 24:1113-28; PMID:9876569; http://dx.doi.org/10.3109/03639049809108571
14. V.Kanchan, A.K.Panda. Interactions of antigen-loaded polylactide particles with macrophages and their correlation with the immune response. Biomaterials 2007; 28:5344-57; PMID:17825905; http://dx.doi.org/10.1016/j.biomaterials.2007.08.015
15. R.C.Mundargi, V.R.Babu, V.Rangaswamy, P.Patel, T.M.Aminabhavi. Nano/micro technologies for delivering macromolecular therapeutics using poly (d, l-lactide-< i>co-glycolide) and its derivatives. J Control Release 2008; 125:193-209; PMID:18083265; http://dx.doi.org/10.1016/j.jconrel.2007.09.013
16. J.Wendorf, J.Chesko, J.Kazzaz, M.Ugozzoli, M.Vajdy, D.O'Hagan, M.Singh. A comparison of anionic nanoparticles and microparticles as vaccine delivery systems. Hum Vaccin 2008; 4:44-9; PMID:18438105; http://dx.doi.org/10.4161/hv.4.1.4886
17. M.L.Tan, P.F.Choong, C.R.Dass. Recent developments in liposomes, microparticles and nanoparticles for protein and peptide drug delivery. Peptides 2010; 31:184-93; PMID:19819278; http://dx.doi.org/10.1016/j.peptides.2009.10.002
18. M.Vert, K.-H.Hellwich, M.Hess, P.Hodge, P.Kubisa, M.Rinaudo, et al. Terminology for biorelated polymers and applications (IUPAC Recommendations 2012). Pure Applied Chem 2012; 84:377-410; http://dx.doi.org/10.1351/PAC-REC-10-12-04
19. A.Kumari, S.K.Yadav, S.C.Yadav. Biodegradable polymeric nanoparticles based drug delivery systems. Colloids Surf B Biointerfaces 2010; 75:1-18; http://dx.doi.org/10.1016/j.colsurfb.2009.09.001
20. Y.Zhang, H.F.Chan, K.W.Leong. Advanced materials and processing for drug delivery: the past and the future. Adv Drug Deliv Rev 2013; 65:104-20; PMID:23088863; http://dx.doi.org/10.1016/j.addr.2012.10.003
21. U.Bilati, E.Allémann, E.Doelker. Strategic approaches for overcoming peptide and protein instability within biodegradable nano-and microparticles. Eur J Pharm Biopharm 2005; 59:375-88; PMID:15760718; http://dx.doi.org/10.1016/j.ejpb.2004.10.006
22. V.Sinha, A.Trehan. Biodegradable microspheres for protein delivery. J Control Release 2003; 90:261-80; PMID:12880694; http://dx.doi.org/10.1016/S0168-3659(03)00194-9
23. Q.Xu, M.Hashimoto, T.T.Dang, T.Hoare, D.S.Kohane, G.M.Whitesides, R.Langer, D.G.Anderson. Preparation of monodisperse biodegradable polymer microparticles using a microfluidic flow‐focusing device for controlled drug delivery. Small 2009; 5:1575-81; PMID:19296563; http://dx.doi.org/10.1002/smll.200801855
24. J.Xu, D.H.Wong, J.D.Byrne, K.Chen, C.Bowerman, J.M.DeSimone. Future of the particle replication in nonwetting templates (PRINT) technology. Angew Chem Int Ed 2013; 52:6580-9; http://dx.doi.org/10.1002/anie.201209145
25. A.L.Galloway, A.Murphy, J.M.DeSimone, J.Di, J.P.Herrmann, M.E.Hunter, J.P.Kindig, F.J.Malinoski, M.A.Rumley, D.M.Stoltz, et al. Development of a nanoparticle-based influenza vaccine using the PRINT technology. Nanomedicine 2013; 9:523-31; PMID:23178283; http://dx.doi.org/10.1016/j.nano.2012.11.001
26. R.S.Raghuvanshi, Y.K.Katare, K.Lalwani, M.M.Ali, O.Singh, A.K.Panda. Improved immune response from biodegradable polymer particles entrapping tetanus toxoid by use of different immunization protocol and adjuvants. Int J Pharm 2002; 245:109-21; PMID:12270248; http://dx.doi.org/10.1016/S0378-5173(02)00342-3
27. S.Shi, A.J.Hickey. PLGA microparticles in respirable sizes enhance an in vitro T cell response to recombinant Mycobacterium tuberculosis antigen TB10.4-Ag85B. Pharm Res 2010; 27:350-60; PMID:20024670; http://dx.doi.org/10.1007/s11095-009-0028-7
28. S.P.Kasturi, I.Skountzou, R.A.Albrecht, D.Koutsonanos, T.Hua, H.I.Nakaya, R.Ravindran, S.Stewart, M.Alam, M.Kwissa, et al. Programming the magnitude and persistence of antibody responses with innate immunity. Nature 2011; 470:543-7; PMID:21350488; http://dx.doi.org/10.1038/nature09737
29. P.Sales-Junior, F.Guzman, M.Vargas, S.Sossai, C.González, J.Patarroyo. Use of biodegradable PLGA microspheres as a slow release delivery system for the Boophilus microplus synthetic vaccine SBm7462. Vet Immunol Immunopathol 2005; 107:281-90; PMID:16002149; http://dx.doi.org/10.1016/j.vetimm.2005.05.004
30. J.E.Rosas, R.M.Hernandez, A.R.Gascon, M.Igartua, F.Guzman, M.E.Patarroyo, J.L.Pedraz. Biodegradable PLGA microspheres as a delivery system for malaria synthetic peptide SPf66. Vaccine 2001; 19:4445-51; PMID:11483270; http://dx.doi.org/10.1016/S0264-410X(01)00192-X
31. A.Salvador, M.Igartua, R.M.Hernandez, J.L.Pedraz. Combination of immune stimulating adjuvants with poly(lactide-co-glycolide) microspheres enhances the immune response of vaccines. Vaccine 2012; 30:589-96; PMID:22119926; http://dx.doi.org/10.1016/j.vaccine.2011.11.057
32. W.Quintilio, C.S.Takata, O.A.Sant'Anna, M.H.B.da Costa, I.Raw. Evaluation of a diphtheria and tetanus PLGA microencapsulated vaccine formulation without stabilizers. Curr Drug Deliv 2009; 6:297-304; PMID:19604144; http://dx.doi.org/10.2174/156720109788680886
33. Y.Waeckerle-Men, E.Uetz-von Allmen, B.Gander, E.Scandella, E.Schlosser, G.Schmidtke, H.P.Merkle, M.Groettrup. Encapsulation of proteins and peptides into biodegradable poly (D, L-lactide-co-glycolide) microspheres prolongs and enhances antigen presentation by human dendritic cells. Vaccine 2006; 24:1847-57; PMID:16288821; http://dx.doi.org/10.1016/j.vaccine.2005.10.032
34. S.S.Huang, I.H.Li, P.D.Hong, M.K.Yeh. Development of Yersinia pestis F1 antigen-loaded microspheres vaccine against plague. Int J Nanomedicine 2014; 9:813-22; PMID:24550673
35. Y.-R.Lee, Y.-H.Lee, S.-A.Im, K.Kim, C.-K.Lee. Formulation and Characterization of Antigen-loaded PLGA Nanoparticles for Efficient Cross-priming of the Antigen. Immune Netw 2011; 11:163-8; PMID:21860609; http://dx.doi.org/10.4110/in.2011.11.3.163
36. L.Feng, X.R.Qi, X.J.Zhou, Y.Maitani, S.C.Wang, Y.Jiang, T.Nagai. Pharmaceutical and immunological evaluation of a single-dose hepatitis B vaccine using PLGA microspheres. J Controlled Release 2006; 112:35-42; PMID:16516999; http://dx.doi.org/10.1016/j.jconrel.2006.01.012
37. C.Thomas, V.Gupta, F.Ahsan. Influence of surface charge of PLGA particles of recombinant hepatitis B surface antigen in enhancing systemic and mucosal immune responses. Int J Pharm 2009; 379:41-50; PMID:19524654; http://dx.doi.org/10.1016/j.ijpharm.2009.06.006
38. S.-C.Chuang, J.-C.Ko, C.-P.Chen, J.-T.Du, C.-D.Yang. Induction of long-lasting protective immunity against Toxoplasma gondii in BALB/c mice by recombinant surface antigen 1 protein encapsulated in poly (lactide-co-glycolide) microparticles. Parasit Vectors 2013; 6:34; PMID:23398973; http://dx.doi.org/10.1186/1756-3305-6-34
39. S.-C.Chuang, J.-C.Ko, C.-P.Chen, J.-T.Du, C.-D.Yang. Encapsulation of chimeric protein rSAG1/2 into poly (lactide-co-glycolide) microparticles induces long-term protective immunity against Toxoplasma gondii in mice. Exp Parasitol 2013; 134:430-7; PMID:23624036; http://dx.doi.org/10.1016/j.exppara.2013.04.002
40. J.Kazzaz, M.Singh, M.Ugozzoli, J.Chesko, E.Soenawan, D.T.O'Hagan. Encapsulation of the immune potentiators MPL and RC529 in PLG microparticles enhances their potency. J Control Release 2006; 110:566-73; PMID:16360956; http://dx.doi.org/10.1016/j.jconrel.2005.10.010
41. J.Chesko, J.Kazzaz, M.Ugozzoli, D.T.O'Hagan, M.Singh. An investigation of the factors controlling the adsorption of protein antigens to anionic PLG microparticles. J Pharm Sci 2005; 94:2510-9; PMID:16200615; http://dx.doi.org/10.1002/jps.20472
42. J.Kazzaz, J.Neidleman, M.Singh, G.Ott, D.O'Hagan. Novel anionic microparticles are a potent adjuvant for the induction of cytotoxic T lymphocytes against recombinant p55 gag from HIV-1. J Control Release 2000; 67:347-56; PMID:10825566; http://dx.doi.org/10.1016/S0168-3659(00)00226-1
43. M.Singh, J.Kazzaz, J.Chesko, E.Soenawan, M.Ugozzoli, M.Giuliani, M.Pizza, R.Rappouli, D.T.O'Hagan. Anionic microparticles are a potent delivery system for recombinant antigens from Neisseria meningitidis serotype B. J Pharm Sci 2004; 93:273-82; PMID:14705185; http://dx.doi.org/10.1002/jps.10538
44. T.G.Park, H.Y.Lee, Y.S.Nam. A new preparation method for protein loaded poly (D, L-lactic-co-glycolic acid) microspheres and protein release mechanism study. J Control Release 1998; 55:181-91; PMID:9795050; http://dx.doi.org/10.1016/S0168-3659(98)00050-9
45. S.Calis, R.Jeyanthi, T.Tsai, R.C.Mehta, P.P.DeLuca. Adsorption of salmon calcitonin to PLGA microspheres. Pharm Res 1995; 12:1072-6; PMID:7494805; http://dx.doi.org/10.1023/A:1016278902839
46. S.Mao, J.Xu, C.Cai, O.Germershaus, A.Schaper, T.Kissel. Effect of WOW process parameters on morphology and burst release of FITC-dextran loaded PLGA microspheres. Int J Pharm 2007; 334:137-48; PMID:17196348; http://dx.doi.org/10.1016/j.ijpharm.2006.10.036
47. B.S.Zolnik, D.J.Burgess. Effect of acidic pH on PLGA microsphere degradation and release. J Control Release 2007; 122:338-44; PMID:17644208; http://dx.doi.org/10.1016/j.jconrel.2007.05.034
48. J.M.Anderson, M.S.Shive. Biodegradation and biocompatibility of PLA and PLGA microspheres. Adv Drug Deliv Rev 2012; 64:72-82; http://dx.doi.org/10.1016/j.addr.2012.09.004
49. J.Schakenraad, M.Hardonk, J.Feijen, I.Molenaar, P.Nieuwenhuis. Enzymatic activity toward poly (L‐lactic acid) implants. J Biomed Mater Res 1990; 24:529-45; PMID:2324125; http://dx.doi.org/10.1002/jbm.820240502
50. S.L.Demento, W.Cui, J.M.Criscione, E.Stern, J.Tulipan, S.M.Kaech, T.M.Fahmy. Role of sustained antigen release from nanoparticle vaccines in shaping the T cell memory phenotype. Biomaterials 2012; 33:4957-64; PMID:22484047; http://dx.doi.org/10.1016/j.biomaterials.2012.03.041
51. S.Fredenberg, M.Wahlgren, M.Reslow, A.Axelsson. The mechanisms of drug release in poly (lactic-co-glycolic acid)-based drug delivery systems—a review. Int J Pharm 2011; 415:34-52; PMID:21640806; http://dx.doi.org/10.1016/j.ijpharm.2011.05.049
52. C.Wischke, S.P.Schwendeman. Principles of encapsulating hydrophobic drugs in PLA/PLGA microparticles. Int J Pharm 2008; 364:298-327; PMID:18621492; http://dx.doi.org/10.1016/j.ijpharm.2008.04.042
53. K.Makino, T.Mogi, N.Ohtake, M.Yoshida, S.Ando, T.Nakajima, et al. Pulsatile drug release from poly (lactide-co-glycolide) microspheres: how does the composition of the polymer matrices affect the time interval between the initial burst and the pulsatile release of drugs? Colloids and Surfaces B: Biointerfaces 2000; 19:173-9; http://dx.doi.org/10.1016/S0927-7765(00)00148-X
54. Y.Chen, V.J.Mohanraj, F.Wang, H.A.Benson. Designing chitosan-dextran sulfate nanoparticles using charge ratios. AAPS PharmSciTech 2007; 8:E98; PMID:18181558; http://dx.doi.org/10.1208/pt0804098
55. A.Giteau, M.-C.Venier-Julienne, A.Aubert-Pouëssel, J.-P.Benoit. How to achieve sustained and complete protein release from PLGA-based microparticles? Int J Pharm 2008; 350:14-26; PMID:18162341; http://dx.doi.org/10.1016/j.ijpharm.2007.11.012
56. M.A.Tracy, K.L.Ward, L.Firouzabadian, Y.Wang, N.Dong, R.Qian, Y.Zhang. Factors affecting the degradation rate of poly(lactide-co-glycolide) microspheres in vivo and in vitro. Biomaterials 1999; 20:1057-62; PMID:10378806; http://dx.doi.org/10.1016/S0142-9612(99)00002-2
57. K.Lima, J.Rodrigues Júnior. Poly-DL-lactide-co-glycolide microspheres as a controlled release antigen delivery system. Braz J Med Biol Res 1999; 32:171-80
58. V.Saini, V.Jain, M.S.Sudheesh, K.S.Jaganathan, P.K.Murthy, D.V.Kohli. Comparison of humoral and cell-mediated immune responses to cationic PLGA microspheres containing recombinant hepatitis B antigen. Int J Pharm 2011; 408:50-7; PMID:21291968; http://dx.doi.org/10.1016/j.ijpharm.2011.01.045
59. T.G.Park. Degradation of poly (lactic-co-glycolic acid) microspheres: effect of copolymer composition. Biomaterials 1995; 16:1123-30; PMID:8562787; http://dx.doi.org/10.1016/0142-9612(95)93575-X
60. N.Passerini, D.Craig. An investigation into the effects of residual water on the glass transition temperature of polylactide microspheres using modulated temperature DSC. J Control Release 2001; 73:111-5; PMID:11337064; http://dx.doi.org/10.1016/S0168-3659(01)00245-0
61. J.S.Wiggins, M.K.Hassan, K.A.Mauritz, R.F.Storey. Hydrolytic degradation of poly (d, l-lactide) as a function of end group: carboxylic acid vs. hydroxyl. Polymer 2006; 47:1960-9; http://dx.doi.org/10.1016/j.polymer.2006.01.021
62. A.Silva, R.Rosalia, A.Sazak, M.Carstens, F.Ossendorp, J.Oostendorp, W.Jiskoot. Optimization of encapsulation of a synthetic long peptide in PLGA nanoparticles: Low-burst release is crucial for efficient CD8+T cell activation. Eur J Pharm Biopharm 2013; 83:338-45; PMID:23201055; http://dx.doi.org/10.1016/j.ejpb.2012.11.006
63. J.Panyam, V.Labhasetwar. Biodegradable nanoparticles for drug and gene delivery to cells and tissue. Adv Drug Deliv Rev 2003; 55:329-47; PMID:12628320; http://dx.doi.org/10.1016/S0169-409X(02)00228-4
64. J.Siepmann, K.Elkharraz, F.Siepmann, D.Klose. How autocatalysis accelerates drug release from PLGA-based microparticles: a quantitative treatment. Biomacromolecules 2005; 6:2312-9; PMID:16004477; http://dx.doi.org/10.1021/bm050228k
65. Q.Yang, G.Owusu-Ababio. Biodegradable progesterone microsphere delivery system for osteoporosis therapy. Drug Dev Ind Pharm 2000; 26:61-70; PMID:10677811; http://dx.doi.org/10.1081/DDC-100100328
66. M.Sandor, D.Enscore, P.Weston, E.Mathiowitz. Effect of protein molecular weight on release from micron-sized PLGA microspheres. J Control Release 2001; 76:297-311; PMID:11578744; http://dx.doi.org/10.1016/S0168-3659(01)00446-1
67. K.D.Newman, P.Elamanchili, G.S.Kwon, J.Samuel. Uptake of poly (D, L‐lactic‐co‐glycolic acid) microspheres by antigen‐presenting cells in vivo. J Biomed Mater Res 2002; 60:480-6; PMID:11920673; http://dx.doi.org/10.1002/jbm.10019
68. E.van Riet, A.Ainai, T.Suzuki, G.Kersten, H.Hasegawa. Combatting infectious diseases; nanotechnology as a platform for rational vaccine design. Adv Drug Deliv Rev 2014; 74:28-34; PMID:24862579; http://dx.doi.org/10.1016/j.addr.2014.05.011
69. D.Mohanan, B.Slütter, M.Henriksen-Lacey, W.Jiskoot, J.A.Bouwstra, Y.Perrie, T.M.Kündig, B.Gander, P.Johansen. Administration routes affect the quality of immune responses: a cross-sectional evaluation of particulate antigen-delivery systems. J Control Release 2010; 147:342-9; PMID:20727926; http://dx.doi.org/10.1016/j.jconrel.2010.08.012
70. D.T.O'Hagan, M.Singh, J.B.Ulmer. Microparticle-based technologies for vaccines. Methods 2006; 40:10-9; http://dx.doi.org/10.1016/j.ymeth.2006.05.017
71. M.Garinot, V.Fiévez, V.Pourcelle, F.Stoffelbach, A.des Rieux, L.Plapied, I.Theate, H.Freichels, C.Jérôme, J.Marchand-Brynaert, et al. PEGylated PLGA-based nanoparticles targeting M cells for oral vaccination. J Control Release 2007; 120:195-204; PMID:17586081; http://dx.doi.org/10.1016/j.jconrel.2007.04.021
72. M.A.Conway, L.Madrigal-Estebas, S.McClean, D.J.Brayden, K.H.Mills. Protection against Bordetella pertussis infection following parenteral or oral immunization with antigens entrapped in biodegradable particles: effect of formulation and route of immunization on induction of Th1 and Th2 cells. Vaccine 2001; 19:1940-50; PMID:11228364; http://dx.doi.org/10.1016/S0264-410X(00)00433-3
73. I.Gutierro, R.Hernandez, M.Igartua, A.Gascon, J.Pedraz. Size dependent immune response after subcutaneous, oral and intranasal administration of BSA loaded nanospheres. Vaccine 2002; 21:67-77; PMID:12443664; http://dx.doi.org/10.1016/S0264-410X(02)00435-8
74. A.M.Carcaboso, R.M.Hernandez, M.Igartua, J.E.Rosas, M.E.Patarroyo, J.L.Pedraz. Potent, long lasting systemic antibody levels and mixed Th1/Th2 immune response after nasal immunization with malaria antigen loaded PLGA microparticles. Vaccine 2004; 22:1423-32; PMID:15063565; http://dx.doi.org/10.1016/j.vaccine.2003.10.020
75. C.Thomas, V.Gupta, F.Ahsan. Particle size influences the immune response produced by hepatitis B vaccine formulated in inhalable particles. Pharm Res 2010; 27:905-19; PMID:20232117; http://dx.doi.org/10.1007/s11095-010-0094-x
76. L.J.Cruz, P.J.Tacken, R.Fokkink, B.Joosten, M.C.Stuart, F.Albericio, R.Torensma, C.G.Figdor. Targeted PLGA nano-but not microparticles specifically deliver antigen to human dendritic cells via DC-SIGN in vitro. J Control Release 2010; 144:118-26; PMID:20156497; http://dx.doi.org/10.1016/j.jconrel.2010.02.013
77. D.T.O'Hagan, H.Jeffery, S.Davis. Long-term antibody responses in mice following subcutaneous immunization with ovalbumin entrapped in biodegradable microparticles. Vaccine 1993; 11:965-9; PMID:8212845; http://dx.doi.org/10.1016/0264-410X(93)90387-D
78. J.H.Eldridge, J.Staas, J.Meulbroek, T.Tice, R.Gilley. Biodegradable and biocompatible poly (DL-lactide-co-glycolide) microspheres as an adjuvant for staphylococcal enterotoxin B toxoid which enhances the level of toxin-neutralizing antibodies. Infect Immun 1991; 59:2978-86; PMID:1879922
79. V.Manolova, A.Flace, M.Bauer, K.Schwarz, P.Saudan, M.F.Bachmann. Nanoparticles target distinct dendritic cell populations according to their size. Eur J Immunol 2008; 38:1404-13; PMID:18389478; http://dx.doi.org/10.1002/eji.200737984
80. K.S.Jaganathan, P.Singh, D.Prabakaran, V.Mishra, S.P.Vyas. Development of a single-dose stabilized poly(D,L-lactic-co-glycolic acid) microspheres-based vaccine against hepatitis B. J Pharm Pharmacol 2004; 56:1243-50; PMID:15482638; http://dx.doi.org/10.1211/0022357044418
81. J.E.Rosas, J.L.Pedraz, R.M.Hernandez, A.R.Gascon, M.Igartua, F.Guzman, R.Rodríguez, J.Cortés, M.E.Patarroyo. Remarkably high antibody levels and protection against P. falciparum malaria in Aotus monkeys after a single immunisation of SPf66 encapsulated in PLGA microspheres. Vaccine 2002; 20:1707-10; PMID:11906756; http://dx.doi.org/10.1016/S0264-410X(01)00508-4
82. V.B.Joshi, A.Adamcakova-Dodd, X.Jing, A.Wongrakpanich, K.N.Gibson-Corley, P.S.Thorne, A.K.Salem. Development of a poly (lactic-co-glycolic acid) particle vaccine to protect against house dust mite induced allergy. AAPS J 2014; 16:975-85; PMID:24981892; http://dx.doi.org/10.1208/s12248-014-9624-5
83. X.Xiao, X.Zeng, X.Zhang, L.Ma, X.Liu, H.Yu, L.Mei, Z.Liu. Effects of Caryota mitis profilin-loaded PLGA nanoparticles in a murine model of allergic asthma. Int J Nanomedicine 2013; 8:4553; PMID:24376349
84. C.Thomas, A.Rawat, L.Hope-Weeks, F.Ahsan. Aerosolized PLA and PLGA nanoparticles enhance humoral, mucosal and cytokine responses to hepatitis B vaccine. Mol Pharm 2011; 8:405-15; PMID:21189035; http://dx.doi.org/10.1021/mp100255c
85. M.Tafaghodi, M.Eskandari, M.Kharazizadeh, A.Khamesipour, M.Jaafari. Immunization against leishmaniasis by PLGA nanospheres loaded with an experimental autoclaved Leishmania major (ALM) and Quillaja saponins. Tropical biomedicine 2010; 27:639-50; PMID:21399606
86. D.M.Santos, M.W.Carneiro, T.R.de Moura, K.Fukutani, J.Clarencio, M.Soto, S.Espuelas, C.Brodskyn, A.Barral, M.Barral-Netto, et al. Towards development of novel immunization strategies against leishmaniasis using PLGA nanoparticles loaded with kinetoplastid membrane protein-11. Int J Nanomedicine 2012; 7:2115-27; PMID:22619548
87. D.M.Santos, M.W.Carneiro, T.R.de Moura, M.Soto, N.F.Luz, D.B.Prates, J.M.Irache, C.Brodskyn, A.Barral, M.Barral-Netto, et al. PLGA nanoparticles loaded with KMP-11 stimulate innate immunity and induce the killing of< i>Leishmania. Nanomedicine 2013; 9:985-95; http://dx.doi.org/10.1016/j.nano.2013.04.003
88. D.J.Kirby, I.Rosenkrands, E.M.Agger, P.Andersen, A.G.Coombes, Y.Perrie. PLGA microspheres for the delivery of a novel subunit TB vaccine. J Drug Target 2008; 16:282-93; PMID:18446607; http://dx.doi.org/10.1080/10611860801900462
89. C.Wang, P.Muttil, D.Lu, A.A.Beltran-Torres, L.Garcia-Contreras, A.J.Hickey. Screening for potential adjuvants administered by the pulmonary route for tuberculosis vaccines. AAPS J 2009; 11:139-47; PMID:19277872; http://dx.doi.org/10.1208/s12248-009-9089-0
90. M.A.Taha, S.R.Singh, V.A.Dennis. Biodegradable PLGA85/15 nanoparticles as a delivery vehicle for Chlamydia trachomatis recombinant MOMP-187 peptide. Nanotechnology 2012; 23:325101; PMID:22824940; http://dx.doi.org/10.1088/0957-4484/23/32/325101
91. S.J.Fairley, S.R.Singh, A.N.Yilma, A.B.Waffo, P.Subbarayan, S.Dixit, M.A.Taha, C.D.Cambridge, V.A.Dennis. Chlamydia trachomatis recombinant MOMP encapsulated in PLGA nanoparticles triggers primarily T helper 1 cellular and antibody immune responses in mice: a desirable candidate nanovaccine. Int J Nanomedicine 2013; 8:2085-99; PMID:23785233
92. P.J.Tacken, I.S.Zeelenberg, L.J.Cruz, M.A.van Hout-Kuijer, G.van de Glind, R.G.Fokkink, A.J.Lambeck, C.G.Figdor. Targeted delivery of TLR ligands to human and mouse dendritic cells strongly enhances adjuvanticity. Blood 2011; 118:6836-44; PMID:21967977; http://dx.doi.org/10.1182/blood-2011-07-367615
93. C.Wischke, J.Zimmermann, B.Wessinger, A.Schendler, H.H.Borchert, J.H.Peters, T.Nesselhut, D.R.Lorenzen. Poly(I:C) coated PLGA microparticles induce dendritic cell maturation. Int J Pharm 2009; 365:61-8; PMID:18812217; http://dx.doi.org/10.1016/j.ijpharm.2008.08.039
94. A.M.Hafner, B.Corthésy, H.P.Merkle. Particulate formulations for the delivery of poly (I: C) as vaccine adjuvant. Adv Drug Deliv Rev 2013; 65:1386-99; PMID:23751781; http://dx.doi.org/10.1016/j.addr.2013.05.013
95. A.Salvador, M.Igartua, R.M.Hernandez, J.L.Pedraz. Designing improved poly lactic-co-glycolic acid microspheres for a malarial vaccine: incorporation of alginate and polyinosinic-polycytidilic acid. J Microencapsul 2014; 31:560-6; PMID:24697189; http://dx.doi.org/10.3109/02652048.2014.885608
96. C.S.Chong, M.Cao, W.W.Wong, K.P.Fischer, W.R.Addison, G.S.Kwon, D.L.Tyrrell, J.Samuel. Enhancement of T helper type 1 immune responses against hepatitis B virus core antigen by PLGA nanoparticle vaccine delivery. J Control Release 2005; 102:85-99; PMID:15653136; http://dx.doi.org/10.1016/j.jconrel.2004.09.014
97. H.Xie, I.Gursel, B.E.Ivins, M.Singh, D.T.O'Hagan, J.B.Ulmer, D.M.Klinman. CpG oligodeoxynucleotides adsorbed onto polylactide-co-glycolide microparticles improve the immunogenicity and protective activity of the licensed anthrax vaccine. Infect Immun 2005; 73:828-33; PMID:15664922; http://dx.doi.org/10.1128/IAI.73.2.828-833.2005
98. J.M.Martinez Gomez, S.Fischer, N.Csaba, T.M.Kundig, H.P.Merkle, B.Gander, P.Johansen. A protective allergy vaccine based on CpG- and protamine-containing PLGA microparticles. Pharm Res 2007; 24:1927-35; PMID:17541735; http://dx.doi.org/10.1007/s11095-007-9318-0
99. M.Tafaghodi, A.Khamesipour, M.R.Jaafari. Immunization against leishmaniasis by PLGA nanospheres encapsulated with autoclaved Leishmania major (ALM) and CpG-ODN. Parasitol Res 2011; 108:1265-73; PMID:21125294; http://dx.doi.org/10.1007/s00436-010-2176-4
100. Y.-R.Lee, Y.-H.Lee, K.-H.Kim, S.-A.Im, C.-K.Lee. Induction of potent antigen-specific cytotoxic T cell response by PLGA-nanoparticles containing antigen and TLR agonist. Immune Netw 2013; 13:30-3; PMID:23559898; http://dx.doi.org/10.4110/in.2013.13.1.30
101. P.Elamanchili, M.Diwan, M.Cao, J.Samuel. Characterization of poly (D, L-lactic-co-glycolic acid) based nanoparticulate system for enhanced delivery of antigens to dendritic cells. Vaccine 2004; 22:2406-12; PMID:15193402; http://dx.doi.org/10.1016/j.vaccine.2003.12.032
102. Q.Wang, M.T.Tan, B.P.Keegan, M.A.Barry, M.J.Heffernan. Time course study of the antigen-specific immune response to a PLGA microparticle vaccine formulation. Biomaterials 2014; 35(29):8385-93
103. P.Malyala, J.Chesko, M.Ugozzoli, A.Goodsell, F.Zhou, M.Vajdy, D.T.O'Hagan, M.Singh. The potency of the adjuvant, CpG oligos, is enhanced by encapsulation in PLG microparticles. J Pharm Sci 2008; 97:1155-64; PMID:17683059; http://dx.doi.org/10.1002/jps.21065
104. B.San Roman, J.M.Irache, S.Gomez, N.Tsapis, C.Gamazo, M.S.Espuelas. Co-encapsulation of an antigen and CpG oligonucleotides into PLGA microparticles by TROMS technology. Eur J Pharm Biopharm 2008; 70:98-108; http://dx.doi.org/10.1016/j.ejpb.2008.03.015
105. S.Fischer, E.Schlosser, M.Mueller, N.Csaba, H.P.Merkle, M.Groettrup, B.Gander. Concomitant delivery of a CTL-restricted peptide antigen and CpG ODN by PLGA microparticles induces cellular immune response. J Drug Target 2009; 17:652-61; PMID:19622019; http://dx.doi.org/10.1080/10611860903119656
106. R.M.Rubsamen, C.V.Herst, P.M.Lloyd, D.E.Heckerman. Eliciting cytotoxic T-lymphocyte responses from synthetic vectors containing one or two epitopes in a C57BL/6 mouse model using peptide-containing biodegradable microspheres and adjuvants. Vaccine 2014; 32:4111-6; PMID:24912025; http://dx.doi.org/10.1016/j.vaccine.2014.05.071
107. A.Bershteyn, M.C.Hanson, M.P.Crespo, J.J.Moon, A.V.Li, H.Suh, D.J.Irvine. Robust IgG responses to nanograms of antigen using a biomimetic lipid-coated particle vaccine. J Control Release 2012; 157:354-65; PMID:21820024; http://dx.doi.org/10.1016/j.jconrel.2011.07.029
108. J.J.Moon, H.Suh, M.E.Polhemus, C.F.Ockenhouse, A.Yadava, D.J.Irvine. Antigen-displaying lipid-enveloped PLGA nanoparticles as delivery agents for a Plasmodium vivax malaria vaccine. PloS one 2012; 7:e31472; PMID:22328935; http://dx.doi.org/10.1371/journal.pone.0031472
109. K.Jaganathan, S.P.Vyas. Strong systemic and mucosal immune responses to surface-modified PLGA microspheres containing recombinant hepatitis B antigen administered intranasally. Vaccine 2006; 24:4201-11; PMID:16446012; http://dx.doi.org/10.1016/j.vaccine.2006.01.011
110. S.Pandit, E.Cevher, M.G.Zariwala, S.Somavarapu, H.O.Alpar. Enhancement of immune response of HBsAg loaded poly (L-lactic acid) microspheres against hepatitis B through incorporation of alum and chitosan. J Microencapsul 2007; 24:539-52; PMID:17654174; http://dx.doi.org/10.1080/02652040701443700
111. B.Semete, L.Booysen, L.Kalombo, J.D.Venter, L.Katata, B.Ramalapa, J.A.Verschoor, H.Swai. In vivo uptake and acute immune response to orally administered chitosan and PEG coated PLGA nanoparticles. Toxicol Appl Pharmacol 2010; 249:158-65; PMID:20851137; http://dx.doi.org/10.1016/j.taap.2010.09.002
112. D.Pawar, A.K.Goyal, S.Mangal, N.Mishra, B.Vaidya, S.Tiwari, A.K.Jain, S.P.Vyas. Evaluation of mucoadhesive PLGA microparticles for nasal immunization. AAPS J 2010; 12:130-7; PMID:20077052; http://dx.doi.org/10.1208/s12248-009-9169-1
113. B.Slutter, S.Bal, C.Keijzer, R.Mallants, N.Hagenaars, I.Que, E.Kaijzel, W.van Eden, P.Augustijns, C.Löwik, et al. Nasal vaccination with N-trimethyl chitosan and PLGA based nanoparticles: nanoparticle characteristics determine quality and strength of the antibody response in mice against the encapsulated antigen. Vaccine 2010; 28:6282-91; PMID:20638455; http://dx.doi.org/10.1016/j.vaccine.2010.06.121
114. C.Primard, J.Poecheim, S.Heuking, E.Sublet, F.Esmaeili, G.Borchard. Multifunctional PLGA-based nanoparticles encapsulating simultaneously hydrophilic antigen and hydrophobic immunomodulator for mucosal immunization. Mol Pharm 2013; 10:2996-3004; PMID:23869898; http://dx.doi.org/10.1021/mp400092y
115. N.Brandhonneur, F.Chevanne, V.Vié, B.Frisch, R.Primault, M.-F.Le Potier, P.Le Corre. Specific and non-specific phagocytosis of ligand-grafted PLGA microspheres by macrophages. Eur J Pharm Sci 2009; 36:474-85; PMID:19110055; http://dx.doi.org/10.1016/j.ejps.2008.11.013
116. J.M.Martínez Gómez, N.Csaba, S.Fischer, A.Sichelstiel, T.M.Kündig, B.Gander, P.Johansen. Surface coating of PLGA microparticles with protamine enhances their immunological performance through facilitated phagocytosis. J Control Release 2008; 130:161-7; http://dx.doi.org/10.1016/j.jconrel.2008.06.003
117. R.Han, J.Zhu, X.Yang, H.Xu. Surface modification of poly(D,L-lactic-co-glycolic acid) nanoparticles with protamine enhanced cross-presentation of encapsulated ovalbumin by bone marrow-derived dendritic cells. J Biomed Mater Res A 2011; 96:142-9; PMID:21105162; http://dx.doi.org/10.1002/jbm.a.32860
118. F.Sarti, G.Perera, F.Hintzen, K.Kotti, V.Karageorgiou, O.Kammona, C.Kiparissides, A.Bernkop-Schnürch. In vivo evidence of oral vaccination with PLGA nanoparticles containing the immunostimulant monophosphoryl lipid A. Biomaterials 2011; 32:4052-7; PMID:21377204; http://dx.doi.org/10.1016/j.biomaterials.2011.02.011
119. S.Jain, H.Harde, A.Indulkar, A.K.Agrawal. Improved stability and immunological potential of tetanus toxoid containing surface engineered bilosomes following oral administration. Nanomedicine 2014; 10:431-40; http://dx.doi.org/10.1016/j.nano.2013.08.012
120. P.N.Gupta, K.Khatri, A.K.Goyal, N.Mishra, S.P.Vyas. M-cell targeted biodegradable PLGA nanoparticles for oral immunization against hepatitis B. J Drug Target 2007; 15:701-13; PMID:18041638; http://dx.doi.org/10.1080/10611860701637982
121. V.Fievez, L.Plapied, A.des Rieux, V.Pourcelle, H.Freichels, V.Wascotte, M.L.Vanderhaeghen, C.Jerôme, A.Vanderplasschen, J.Marchand-Brynaert, et al. Targeting nanoparticles to M cells with non-peptidic ligands for oral vaccination. Eur J Pharm Biopharm 2009; 73:16-24; PMID:19409989; http://dx.doi.org/10.1016/j.ejpb.2009.04.009
122. N.Mishra, S.Tiwari, B.Vaidya, G.P.Agrawal, S.P.Vyas. Lectin anchored PLGA nanoparticles for oral mucosal immunization against hepatitis B. J Drug Target 2011; 19:67-78; PMID:20334603; http://dx.doi.org/10.3109/10611861003733946
123. T.Ma, L.Wang, T.Yang, G.Ma, S.Wang. M-cell targeted polymeric lipid nanoparticles containing a Toll-like receptor agonist to boost oral immunity. Int J Pharm 2014; 473:296-303; PMID:24984067; http://dx.doi.org/10.1016/j.ijpharm.2014.06.052
124. T.Jiang, B.Singh, H.-S.Li, Y.-K.Kim, S.-K.Kang, J.-W.Nah, Y.J.Choi, C.S.Cho. Targeted oral delivery of BmpB vaccine using porous PLGA microparticles coated with M cell homing peptide-coupled chitosan. Biomaterials 2014; 35:2365-73; PMID:24342722; http://dx.doi.org/10.1016/j.biomaterials.2013.11.073
125. S.S.Saluja, D.J.Hanlon, F.A.Sharp, E.Hong, D.Khalil, E.Robinson, R.Tigelaar, T.M.Fahmy, R.L.Edelson. Targeting human dendritic cells via DEC-205 using PLGA nanoparticles leads to enhanced cross-presentation of a melanoma-associated antigen. Int J Nanomedicine 2014; 9:5231-46; PMID:25419128
126. D.T O'Hagan, M.Singh, R.K.Gupta. Poly (lactide-co-glycolide) microparticles for the development of single-dose controlled-release vaccines. Adv Drug Deliv Rev 1998; 32:225-46; PMID:10837646; http://dx.doi.org/10.1016/S0169-409X(98)00012-X
127. F.Danhier, E.Ansorena, J.M.Silva, R.Coco, A.Le Breton, V.Préat. PLGA-based nanoparticles: an overview of biomedical applications. J Control Release 2012; 161:505-22; PMID:22353619; http://dx.doi.org/10.1016/j.jconrel.2012.01.043
128. J.K.Vasir, V.Labhasetwar. Biodegradable nanoparticles for cytosolic delivery of therapeutics. Adv Drug Deliv Rev 2007; 59:718-28; PMID:17683826; http://dx.doi.org/10.1016/j.addr.2007.06.003
129. L.J.Cruz, R.A.Rosalia, J.W.Kleinovink, F.Rueda, C.W.Lowik, F.Ossendorp. Targeting nanoparticles to CD40, DEC-205 or CD11c molecules on dendritic cells for efficient CD8(+) T cell response: a comparative study. J Control Release 2014; 192:209-18; PMID:25068703; http://dx.doi.org/10.1016/j.jconrel.2014.07.040
130. S.Fischer, E.Uetz-von Allmen, Y.Waeckerle-Men, M.Groettrup, H.P.Merkle, B.Gander. The preservation of phenotype and functionality of dendritic cells upon phagocytosis of polyelectrolyte-coated PLGA microparticles. Biomaterials 2007; 28:994-1004; PMID:17118442; http://dx.doi.org/10.1016/j.biomaterials.2006.10.034
131. M.B.Heo, M.Y.Cho, Y.T.Lim. Polymer nanoparticles for enhanced immune response: combined delivery of tumor antigen and small interference RNA for immunosuppressive gene to dendritic cells. Acta biomaterialia 2014; 10:2169-76; PMID:24394635; http://dx.doi.org/10.1016/j.actbio.2013.12.050
132. M.B.Heo, Y.T.Lim. Programmed nanoparticles for combined immunomodulation, antigen presentation and tracking of immunotherapeutic cells. Biomaterials 2014; 35:590-600; PMID:24125775; http://dx.doi.org/10.1016/j.biomaterials.2013.10.009
133. L.A.Brito, D.T.O'Hagan. Designing and building the next generation of improved vaccine adjuvants. J Control Release 2014; 190:563-79; PMID:24998942; http://dx.doi.org/10.1016/j.jconrel.2014.06.027