Nanoparticle vaccines

Vaccine

Volumn 32, Issue 3, 2014, Pages 327-337

  Zhao, Liang ^a   Seth, Arjun ^a   Wibowo, Nani ^a   Zhao, Chun Xia ^a   Mitter, Neena ^a   Yu, Chengzhong ^a   Middelberg, Anton P J ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Adjuvant; Nanoparticle; Nanotechnology; Nanovaccinology; Vaccine

Indexed keywords

ANTIGEN; GOLD NANOPARTICLE; INORGANIC NANOPARTICLE; ISCOM; LIPOSOME; NANOPARTICLE; NANOROD; POLYMER; POLYMERIC NANOPARTICLE; PROTEIN; SELF ASSEMBLED PROTEIN; UNCLASSIFIED DRUG; VACCINE;

ANTIGEN PRESENTING CELL; DRUG DELIVERY SYSTEM; EMULSION; HUMAN; IMMUNOCOMPETENT CELL; IMMUNOSTIMULATION; IN VIVO STUDY; LIPOSOMAL DELIVERY; NANOMEDICINE; NANOVACCINOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; REVIEW; VIRUS LIKE AGENT;

ADJUVANT; NANOPARTICLE; NANOTECHNOLOGY; NANOVACCINOLOGY; VACCINE;

ADJUVANTS, IMMUNOLOGIC; HUMANS; NANOPARTICLES; VACCINATION; VACCINES;

EID: 84891024912     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2013.11.069     Document Type: Review

References (205)

1. Oberg A.L., Kennedy R.B., Li P., Ovsyannikova I.G., Poland G.A. Systems biology approaches to new vaccine development. Current Opinion in Immunology 2011, 23:436-443.
2. Rappuoli R., Mandl C.W., Black S., De Gregorio E. Vaccines for the twenty-first century society. Nature Reviews Immunology 2011, 11:865-872.
3. Mamo T., Poland G.A. Nanovaccinology: the next generation of vaccines meets 21st century materials science and engineering. Vaccine 2012, 30:6609-6611.
4. Couvreur P., Vauthier C. Nanotechnology: intelligent design to treat complex disease. Pharmaceutical Research 2006, 23:1417-1450.
5. Moghimi S.M., Hunter A.C., Murray J.C. Nanomedicine: current status and future prospects. The FASEB Journal 2005, 19:311-330.
6. Treuel L., Jiang X., Nienhaus G.U. New views on cellular uptake and trafficking of manufactured nanoparticles. Journal of the Royal Society Interface 2013, 10:20120939.
7. Wagner V., Dullaart A., Bock A.-K., Zweck A. The emerging nanomedicine landscape. Nature Biotechnology 2006, 24:1211-1217.
8. Global Industry Analysts Inc. Nanomedicine - a global market report 2009.
9. Tissot A.C., Maurer P., Nussberger J., Sabat R., Pfister T., Ignatenko S., et al. Effect of immunisation against angiotensin II with CYT006-AngQb on ambulatory blood pressure: a double-blind, randomized, placebo-controlled phase IIa study. The Lancet 2008, 371:821-827.
10. Pankhurst Q.A., Connolly J., Jones S.K., Dobson J. Applications of magnetic nanoparticles in biomedicine. Journal of Physics D: Applied Physics 2003, 36:R167-R181.
11. Maurer P., Jennings G.T., Willers J., Rohner F., Lindman Y., Roubicek K., et al. A therapeutic vaccine for nicotine dependence: preclinical efficacy, and phase I safety and immunogenicity. European Journal of Immunology 2005, 35:2031-2040.
12. Dobrovolskaia M.A., McNeil S.E. Immunological properties of engineered nanomaterials. Nature Nanotechnology 2007, 2:469-478.
13. Roldao A., Mellado M.C.M., Castilho L.R., Carrondo M.J., Alves P.M. Virus-like particles in vaccine development. Expert Review of Vaccines 2010, 9:1149-1176.
14. Bolhassani A., Safaiyan S., Rafati S. Improvement of different vaccine delivery systems for cancer therapy. Molecular Cancer 2011, 10:3-22.
15. Krishnamachari Y., Geary S., Lemke C., Salem A. Nanoparticle delivery systems in cancer vaccines. Pharmaceutical Research 2011, 28:215-236.
16. Hamdy S., Haddadi A., Hung R.W., Lavasanifar A. Targeting dendritic cells with nano-particulate PLGA cancer vaccine formulations. Advanced Drug Delivery Reviews 2011, 63:943-955.
17. Chackerian B. Virus-like particle based vaccines for Alzheimer disease. Human Vaccines 2010, 6:926-930.
18. Correia-Pinto J.F., Csaba N., Alonso M.J. Vaccine delivery carriers: insights and future perspectives. International Journal of Pharmaceutics 2013, 440:27-38.
19. Kushnir N., Streatfield S.J., Yusibov V. Virus-like particles as a highly efficient vaccine platform: diversity of targets and production systems and advances in clinical development. Vaccine 2012, 31:58-83.
20. Plummer E.M., Manchester M. Viral nanoparticles and virus-like particles: platforms for contemporary vaccine design. Wiley Interdisciplinary Reviews: Nanomedicine and Nanobiotechnology 2011, 3:174-196.
21. Food and Drug Administration US Considering whether an FDA-regulated product involves the application of nanotechnology 2011, http://wwwfdagov/regulatoryinformation/guidances/ucm257698htm.
22. Thomas C., Rawat A., Hope-Weeks L., Ahsan F. Aerosolized PLGA nanoparticles enhance humoral, mucosal and cytokine responses to hepatitis B vaccine. Molecular Pharmaceutics 2011, 8:405-415.
23. Kim S.Y., Doh H.J., Jang M.H., Ha Y.J., Chung S.I., Park H.J. Oral immunization with Helicobacter pylori-loaded poly(d,l-lactide-co-glycolide) nanoparticles. Helicobacter 1999, 4:33-39.
24. Vila A., Sanchez A., Evora C., Soriano I., Vila Jato J., Alonso M. PEG-PLA nanoparticles as carriers for nasal vaccine delivery. Journal of Aerosol Medicine 2004, 17:174-185.
25. Lü J-M., Wang X., Marin-Muller C., Wang H., Lin P.H., Yao Q., et al. Current advances in research and clinical applications of PLGA-based nanotechnology. Expert Review of Molecular Diagnostics 2009, 9:325-341.
26. Demento S.L., Cui W., Criscione J.M., Stern E., Tulipan J., Kaech S.M., et al. Role of sustained antigen release from nanoparticle vaccines in shaping the T cell memory phenotype. Biomaterials 2012, 33:4957-4964.
27. Diwan M., Tafaghodi M., Samuel J. Enhancement of immune responses by co-delivery of a CpG oligodeoxynucleotide and tetanus toxoid in biodegradable nanospheres. Journal of Controlled Release 2002, 85:247-262.
28. Silva A.L., Rosalia R.A., Sazak A., Carstens M.G., Ossendorp F., Oostendorp J., et al. Optimization of encapsulation of a synthetic long peptide in PLGA nanoparticles: low-burst release is crucial for efficient CD8(+) T cell activation. European Journal of Pharmaceutics and Biopharmaceutics 2013, 83:338-345.
29. Manish M., Rahi A., Kaur M., Bhatnagar R., Singh S. A single-dose PLGA encapsulated protective antigen domain 4 nanoformulation protects mice against Bacillus anthracis spore challenge. PLoS ONE 2013, 8:e61885-e61890.
30. Lutsiak M., Kwon G.S., Samuel J. Biodegradable nanoparticle delivery of a Th2-biased peptide for induction of Th1 immune responses. Journal of Pharmacy and Pharmacology 2006, 58:739-747.
31. Akagi T., Baba M., Akashi M. Biodegradable nanoparticles as vaccine adjuvants and delivery systems: regulation of immune responses by nanoparticle-based vaccine. Polymers in nanomedicine 2012, 31-64. Springer-Verlag Berlin, Berlin. S. Kunugi, T. Yamaoka (Eds.).
32. Akagi T., Kaneko T., Kida T., Akashi M. Preparation and characterization of biodegradable nanoparticles based on poly (γ-glutamic acid) with l-phenylalanine as a protein carrier. Journal of Controlled Release 2005, 108:226-236.
33. Kalkanidis M., Pietersz G.A., Xiang S.D., Mottram P.L., Crimeen-Irwin B., Ardipradja K., et al. Methods for nano-particle based vaccine formulation and evaluation of their immunogenicity. Methods 2006, 40:20-29.
34. Minigo G., Scholzen A., Tang C.K., Hanley J.C., Kalkanidis M., Pietersz G.A., et al. Poly-l-lysine-coated nanoparticles: a potent delivery system to enhance DNA vaccine efficacy. Vaccine 2007, 25:1316-1327.
35. Peek L.J., Middaugh C.R., Berkland C. Nanotechnology in vaccine delivery. Advanced Drug Delivery Reviews 2008, 60:915-928.
36. Danhier F., Ansorena E., Silva J.M., Coco R., Le Breton A., Préat V. PLGA-based nanoparticles: an overview of biomedical applications. Journal of Controlled Release 2012, 161:505-522.
37. Moon J.J., Suh H., Polhemus M.E., Ockenhouse C.F., Yadava A., Irvine D.J. Antigen-displaying lipid-enveloped PLGA nanoparticles as delivery agents for a Plasmodium vivax malaria vaccine. PloS ONE 2012, 7:e31472.
38. Scheerlinck J.-P.Y., Gloster S., Gamvrellis A., Mottram P.L., Plebanski M. Systemic immune responses in sheep, induced by a novel nano-bead adjuvant. Vaccine 2006, 24:1124-1131.
39. Uenaka A., Wada H., Isobe M., Saika T., Tsuji K., Sato E., et al. T cell immunomonitoring and tumor responses in patients immunized with a complex of cholesterol-bearing hydrophobized pullulan (CHP) and NY-ESO-1 protein. Cancer Immunity: A Journal of the Academy of Cancer Immunology 2007, 7:9-19.
40. Hasegawa K., Noguchi Y., Koizumi F., Uenaka A., Tanaka M., Shimono M., et al. In vitro stimulation of CD8 and CD4T cells by dendritic cells loaded with a complex of cholesterol-bearing hydrophobized pullulan and NY-ESO-1 protein: identification of a new HLA-DR15-binding CD4 T-cell epitope. Clinical Cancer Research 2006, 12:1921-1927.
41. Li P., Luo Z., Liu P., Gao N., Zhang Y., Pan H., et al. Bioreducible alginate-poly (ethylenimine) nanogels as an antigen-delivery system robustly enhance vaccine-elicited humoral and cellular immune responses. Journal of Controlled Release 2013, 168:271-279.
42. Honda-Okubo Y., Saade F., Petrovsky N. Advax™ a polysaccharide adjuvant derived from delta inulin, provides improved influenza vaccine protection through broad-based enhancement of adaptive immune responses. Vaccine 2012, 30:5373-5381.
43. Saade F., Honda-Okubo Y., Trec S., Petrovsky N. A novel hepatitis B vaccine containing Advax™, a polysaccharide adjuvant derived from delta inulin, induces robust humoral and cellular immunity with minimal reactogenicity in preclinical testing. Vaccine 2013, 31:1999-2007.
44. Feng G., Jiang Q., Xia M., Lu Y., Qiu W., Zhao D., et al. Enhanced immune response and protective effects of nano-chitosan-based DNA vaccine encoding T cell epitopes of Esat-6 and FL against Mycobacterium tuberculosis infection. PLoS ONE 2013, 8:e61135.
45. Thomann-Harwood L.J., Kaeuper P., Rossi N., Milona P., Herrmann B., McCullough K.C. Nanogel vaccines targeting dendritic cells: contributions of the surface decoration and vaccine cargo on cell targeting and activation. Journal of Controlled Release 2013, 166:95-105.
46. Zhao F., Zhang X., Liu S., Zeng T., Yu J., Gu W., et al. Assessment of the immune responses to Treponema pallidum Gpd DNA vaccine adjuvanted with IL-2 and chitosan nanoparticles before and after Treponema pallidum challenge in rabbits. Science China-Life Sciences 2013, 56:174-180.
47. Nanda R.K., Edao B.M., Hajam I.A., Sekar S.C., Ganesh K., Bhanuprakash V., et al. An effective mannosylated chitosan nanoparticle DNA vaccine for FMD virus. Virologica Sinica 2012, 27:373-376.
48. Zhao K., Chen G., Shi X.-m., Gao T.-t., Li W., Zhao Y., et al. Preparation and efficacy of a live Newcastle disease virus vaccine encapsulated in chitosan nanoparticles. PLoS ONE 2012, 7:e53314.
49. Borges O., Cordeiro-da-Silva A., Tavares J., Santarém N., de Sousa A., Borchard G., et al. Immune response by nasal delivery of hepatitis B surface antigen and codelivery of a CpG ODN in alginate coated chitosan nanoparticles. European Journal of Pharmaceutics and Biopharmaceutics 2008, 69:405-416.
50. Chua B.Y., Al Kobaisi M., Zeng W.G., Mainwaring D., Jackson D.C. Chitosan microparticles and nanoparticles as biocompatible delivery vehicles for peptide and protein-based immunocontraceptive vaccines. Molecular Pharmaceutics 2012, 9:81-90.
51. Arca H.Ç., Günbeyaz M., Şenel S. Chitosan-based systems for the delivery of vaccine antigens. Expert Review of Vaccines 2009, 8:937-953.
52. Götze O., Müller-Eberhard H.J. The C3-activator system: an alternate pathway of complement activation. Journal of Experimental Medicine 1971, 134:90-108.
53. Démoulins T., Bassi I., Thomann-Harwood L., Jandus C., Kaeuper P., Simon H.-U., et al. Alginate-coated chitosan nanogel capacity to modulate the effect of TLR ligands on blood dendritic cells. Nanomedicine: Nanotechnology, Biology and Medicine 2013, 9:806-817.
54. Vinogradov S., Batrakova E., Kabanov A. Poly(ethylene glycol)-polyethyleneimine NanoGel™ particles: novel drug delivery systems for antisense oligonucleotides. Colloids and Surfaces B: Biointerfaces 1999, 16:291-304.
55. Ferreira S.A., Gama F.M., Vilanova M. Polymeric nanogels as vaccine delivery systems. Nanomedicine: Nanotechnology, Biology and Medicine 2012, 9:159-173.
56. Raemdonck K., Demeester J., De Smedt S. Advanced nanogel engineering for drug delivery. Soft Matter 2009, 5:707-715.
57. Nochi T., Yuki Y., Takahashi H., Sawada S.-i., Mejima M., Kohda T., et al. Nanogel antigenic protein-delivery system for adjuvant-free intranasal vaccines. Nature Materials 2010, 9:572-578.
58. Debache K., Kropf C., Schutz C.A., Harwood L.J., Kauper P., Monney T., et al. Vaccination of mice with chitosan nanogel-associated recombinant NcPDI against challenge infection with Neospora caninum tachyzoites. Parasite Immunology 2011, 33:81-94.
59. Niikura K., Matsunaga T., Suzuki T., Kobayashi S., Yamaguchi H., Orba Y., et al. Gold nanoparticles as a vaccine platform: influence of size and shape on immunological responses in vitro and in vivo. ACS Nano 2013, 7:3926-3938.
60. Gregory A.E., Titball R., Williamson D. Vaccine delivery using nanoparticles. Frontiers in Cellular and Infection Microbiology 2013, 3:13.
61. Marradi M., Chiodo F., Garcia I., Penades S. Glyconanoparticles as multifunctional and multimodal carbohydrate systems. Chemical Society Reviews 2013, 42:4728-4745.
62. Stone J.W., Thornburg N.J., Blum D.L., Kuhn S.J., Wright D.W., Crowe J.E. Gold nanorod vaccine for respiratory syncytial virus. Nanotechnology 2013, 24:295102.
63. Tao W., Ziemer K.S., Gill H.S. Gold nanoparticle-M2e conjugate coformulated with CpG induces protective immunity against influenza A virus. Nanomedicine 2013, 1-16. [Epub ahead of print]. 10.2217/nnm.13.58.
64. Chen Y.-S., Hung Y.-C., Lin W.-H., Huang G.S. Assessment of gold nanoparticles as a size-dependent vaccine carrier for enhancing the antibody response against synthetic foot-and-mouth disease virus peptide. Nanotechnology 2010, 21:195101-195108.
65. Xu L., Liu Y., Chen Z., Li W., Liu Y., Wang L., et al. Surface-engineered gold nanorods: promising DNA vaccine adjuvant for HIV-1 treatment. Nano Letters 2012, 12:2003-2012.
66. Bianco A., Kostarelos K., Prato M. Applications of carbon nanotubes in drug delivery. Current Opinion in Chemical Biology 2005, 9:674-679.
67. Wang T., Zou M., Jiang H., Ji Z., Gao P., Cheng G. Synthesis of a novel kind of carbon nanoparticle with large mesopores and macropores and its application as an oral vaccine adjuvant. European Journal of Pharmaceutical Sciences 2011, 44:653-659.
68. Smart S., Cassady A., Lu G., Martin D. The biocompatibility of carbon nanotubes. Carbon 2006, 44:1034-1047.
69. Villa C.H., Dao T., Ahearn I., Fehrenbacher N., Casey E., Rey D.A., et al. Single-walled carbon nanotubes deliver peptide antigen into dendritic cells and enhance IgG responses to tumor-associated antigens. ACS Nano 2011, 5:5300-5311.
70. Parra J., Abad-Somovilla A., Mercader J.V., Taton T.A., Abad-Fuentes A. Carbon nanotube-protein carriers enhance size-dependent self-adjuvant antibody response to haptens. Journal of Controlled Release 2013, 170:242-251.
71. Pantarotto D., Partidos C.D., Hoebeke J., Brown F., Kramer E., Briand J.-P., et al. Immunization with peptide-functionalized carbon nanotubes enhances virus-specific neutralizing antibody responses. Chemistry and Biology 2003, 10:961-966.
72. Ow H., Larson D.R., Srivastava M., Baird B.A., Webb W.W., Wiesner U. Bright and stable core-shell fluorescent silica nanoparticles. Nano Letters 2005, 5:113-117.
73. Benezra M., Penate-Medina O., Zanzonico P.B., Schaer D., Ow H., Burns A., et al. Multimodal silica nanoparticles are effective cancer-targeted probes in a model of human melanoma. Journal of Clinical Investigation 2011, 121:2768-2780.
74. Niu Y., Popat A., Yu M., Karmakar S., Gu W., Yu C. Recent advances in the rational design of silica-based nanoparticles for gene therapy. Therapeutic Delivery 2012, 3:1217-1237.
75. Yu M., Jambhrunkar S., Thorn P., Chen J., Gu W., Yu C. Hyaluronic acid modified mesoporous silica nanoparticles for targeted drug delivery to CD44-overexpressing cancer cells. Nanoscale 2013, 5:178-183.
76. Alshamsan A., Haddadi A., Incani V., Samuel J., Lavasanifar A., Uludag H. Formulation and delivery of siRNA by oleic acid and stearic acid modified polyethylenimine. Molecular Pharmaceutics 2008, 6:121-133.
77. Xia T., Kovochich M., Liong M., Meng H., Kabehie S., George S., et al. Polyethyleneimine coating enhances the cellular uptake of mesoporous silica nanoparticles and allows safe delivery of siRNA and DNA constructs. ACS Nano 2009, 3:3273-3286.
78. He X.-x., Wang K., Tan W., Liu B., Lin X., He C., et al. Bioconjugated nanoparticles for DNA protection from cleavage. Journal of the American Chemical Society 2003, 125:7168-7169.
79. Mody K.T., Popat A., Mahony D., Cavallaro A.S., Yu C., Mitter N. Mesoporous silica nanoparticles as antigen carriers and adjuvants for vaccine delivery. Nanoscale 2013, 5:5167-5179.
80. Carvalho L.V., Ruiz R.d.C., Scaramuzzi K., Marengo E.B., Matos J.R., Tambourgi D.V., et al. Immunological parameters related to the adjuvant effect of the ordered mesoporous silica SBA-15. Vaccine 2010, 28:7829-7836.
81. Mahony D., Cavallaro A.S., Stahr F., Mahony T.J., Qiao S.Z., Mitter N. Mesoporous silica nanoparticles act as a self-adjuvant for ovalbumin model antigen in mice. Small 2013, 9:3138-3146.
82. Guo H.-C., Feng X.-M., Sun S.-Q., Wei Y.-Q., Sun D.-H., Liu X.-T., et al. Immunization of mice by hollow mesoporous silica nanoparticles as carriers of porcine circovirus type 2 ORF2 protein. Virology Journal 2012, 9:108.
83. Cheng K., El-Boubbou K., Landry C.C. Binding of HIV-1 gp120 glycoprotein to silica nanoparticles modified with CD4 glycoprotein and CD4 peptide fragments. ACS Applied Materials & Interfaces 2011, 4:235-243.
84. Manzano M., Aina V., Arean C., Balas F., Cauda V., Colilla M., et al. Studies on MCM-41 mesoporous silica for drug delivery: effect of particle morphology and amine functionalization. Chemical Engineering Journal 2008, 137:30-37.
85. Zhai W., He C., Wu L., Zhou Y., Chen H., Chang J., et al. Degradation of hollow mesoporous silica nanoparticles in human umbilical vein endothelial cells. Journal of Biomedical Materials Research Part B: Applied Biomaterials 2012, 100B:1397-1403.
86. Yamada H., Urata C., Aoyama Y., Osada S., Yamauchi Y., Kuroda K. Preparation of colloidal mesoporous silica nanoparticles with different diameters and their unique degradation behavior in static aqueous systems. Chemistry of Materials 2012, 24:1462-1471.
87. Chen K., Zhang J., Gu H. Dissolution from inside: a unique degradation behaviour of core-shell magnetic mesoporous silica nanoparticles and the effect of polyethyleneimine coating. Journal of Materials Chemistry 2012, 22:22005-22012.
88. He Q., Mitchell A.R., Johnson S.L., Wagner-Bartak C., Morcol T., Bell S.J.D. Calcium phosphate nanoparticle adjuvant. Clinical and Diagnostic Laboratory Immunology 2000, 7:899-903.
89. He Q., Mitchell A., Morcol T., Bell S.J. Calcium phosphate nanoparticles induce mucosal immunity and protection against herpes simplex virus type 2. Clinical and Diagnostic Laboratory Immunology 2002, 9:1021-1024.
90. Joyappa D.H., Ashok Kumar C., Banumathi N., Reddy G.R., Suryanarayana V.V. Calcium phosphate nanoparticle prepared with foot and mouth disease virus P1-3CD gene construct protects mice and guinea pigs against the challenge virus. Veterinary Microbiology 2009, 139:58-66.
91. Giddam A.K., Zaman M., Skwarczynski M., Toth I. Liposome-based delivery system for vaccine candidates: constructing an effective formulation. Nanomedicine 2012, 7:1877-1893.
92. Sharma S., Mukkur T., Benson H.A., Chen Y. Pharmaceutical aspects of intranasal delivery of vaccines using particulate systems. Journal of Pharmaceutical Sciences 2009, 98:812-843.
93. Khatri K., Goyal A.K., Gupta P.N., Mishra N., Mehta A., Vyas S.P. Surface modified liposomes for nasal delivery of DNA vaccine. Vaccine 2008, 26:2225-2233.
94. Glück R., Moser C., Metcalfe I.C. Influenza virosomes as an efficient system for adjuvanted vaccine delivery. Expert Opinion on Biological Therapy 2004, 4:1139-1145.
95. Li S., Rizzo M., Bhattacharya S., Huang L. Characterization of cationic lipid-protamine-DNA (LPD) complexes for intravenous gene delivery. Gene Therapy 1998, 5:930-937.
96. Li S., Huang L. In vivo gene transfer via intravenous administration of cationic lipid-protamine-DNA (LPD) complexes. Gene Therapy 1997, 4:891-900.
97. Moon J.J., Suh H., Bershteyn A., Stephan M.T., Liu H., Huang B., et al. Interbilayer-crosslinked multilamellar vesicles as synthetic vaccines for potent humoral and cellular immune responses. Nature Materials 2011, 10:243-251.
98. Watson D.S., Endsley A.N., Huang L. Design considerations for liposomal vaccines: influence of formulation parameters on antibody and cell-mediated immune responses to liposome associated antigens. Vaccine 2012, 30:2256-2272.
99. Homhuan A., Prakongpan S., Poomvises P., Maas R.A., Crommelin D.J., Kersten G.F., et al. Virosome and ISCOM vaccines against Newcastle disease: preparation, characterization and immunogenicity. European Journal of Pharmaceutical Sciences 2004, 22:459-468.
100. Aguilar J., Rodriguez E. Vaccine adjuvants revisited. Vaccine 2007, 25:3752-3762.
101. Morein B., Sundquist B., Hoglund S., Dalsgaard K., Osterhaus A. ISCOM a novel structure for antigenic presentation of membrane proteins from enveloped viruses. Nature 1984, 308:457-460.
102. Pearse M.J., Drane D. ISCOMATRIX™ adjuvant: a potent inducer of humoral and cellular immune responses. Vaccine 2004, 22:2391-2395.
103. Sambhara S., Woods S., Arpino R., Kurichh A., Tamane A., Underdown B., et al. Heterotypic protection against influenza by immunostimulating complexes is associated with the induction of cross-reactive cytotoxic T lymphocytes. Journal of Infectious Diseases 1998, 177:1266-1274.
104. ® adjuvanted influenza vaccine. Vaccine 2003, 21:946-949.
105. Mohamedi S., Brewer J., Alexander J., Heath A., Jennings R. Antibody responses, cytokine levels and protection of mice immunized with HSV-2 antigens formulated into NISV or ISCOM delivery systems. Vaccine 2000, 18:2083-2094.
106. Agrawal L., Haq W., Hanson C.V., Rao D.N. Generating neutralizing antibodies, Th1 response and MHC non restricted immunogenicity of HIV-I env and gag peptides in liposomes and ISCOMs with in-built adjuvanticity. Journal of Immune Based Therapies and Vaccines 2003, 1:5-26.
107. Noad R., Roy P. Virus-like particles as immunogens. Trends in Microbiology 2003, 11:438-444.
108. Grgacic E.V., Anderson D.A. Virus-like particles: passport to immune recognition. Methods 2006, 40:60-65.
109. Zhang L.F., Zhou J., Chen S., Cai L.L., Bao Q.Y., Zheng F.Y., et al. HPV6b virus like particles are potent immunogens without adjuvant in man. Vaccine 2000, 18:1051-1058.
110. Andre F.E. Overview of a 5-year clinical-experience with a yeast-derived hepatitis-B vaccine. Vaccine 1990, 8:S74-S78.
111. Cutts F.T., Franceschi S., Goldie S., Castellsague X., de Sanjose S., Garnett G., et al. Human papillomavirus and HPV vaccines: a review. Bulletin of the World Health Organization 2007, 85:719-726.
112. Bin Park S. Hepatitis E vaccine debuts. Nature 2012, 491:21-22.
113. Pushko P., Pumpens P., Grens E. Development of virus-like particle technology from small highly symmetric to large complex virus-like particle structures. Intervirology 2013, 56:141-165.
114. Pattenden L.K., Middelberg A.P.J., Niebert M., Lipin D.I. Towards the preparative and large-scale precision manufacture of virus-like particles. Trends in Biotechnology 2005, 23:523-529.
115. Campbell S., Vogt V.M. In vitro assembly of virus-like particles with Rous sarcoma virus Gag deletion mutants: identification of the p10 domain as a morphological determinant in the formation of spherical particles. Journal of Virology 1997, 71:4425-4435.
116. Sánchez-Rodríguez S.P., Münch-Anguiano L., Echeverría O., Vázquez-Nin G., Mora-Pale M., Dordick J.S., et al. Human parvovirus B19 virus-like particles: in vitro assembly and stability. Biochimie 2012, 94:870-878.
117. Zhang W., Carmichael J., Ferguson J., Inglis S., Ashrafian H., Stanley M. Expression of human papillomavirus type 16 L1 protein in Escherichia coli: denaturation, renaturation, and self-assembly of virus-like particles in vitro. Virology 1998, 243:423-431.
118. Liew M.W.O., Chuan Y.P., Middelberg A.P.J. High-yield and scalable cell-free assembly of virus-like particles by dilution. Biochemical Engineering Journal 2012, 67:88-96.
119. Lu Y., Welsh J.P., Chan W., Swartz J.R. Escherichia coli-based cell free production of flagellin and ordered flagellin display on virus-like particles. Biotechnology and Bioengineering 2013, 110:2073-2085.
120. Chuan Y.P., Lua L.H.L., Middelberg A.P.J. Virus-like particle bioprocessing 2012, 139-163. Biopharmaceutical Production Technology: Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim, Germany.
121. Lua L.H.L., Connors N.K., Sainsbury F., Chuan Y.P., Wibowo N., Middelberg A.P.J. Bioengineering virus-like particles as vaccines. Biotechnology and Bioengineering 2013, 10.1002/bit.25159.
122. Tissot A.C., Renhofa R., Schmitz N., Cielens I., Meijerink E., Ose V., et al. Versatile virus-like particle carrier for epitope based vaccines. PLoS ONE 2010, 5:e9809.
123. Middelberg A.P.J., Rivera-Hernandez T., Wibowo N., Lua L.H.L., Fan Y., Magor G., et al. A microbial platform for rapid and low-cost virus-like particle and capsomere vaccines. Vaccine 2011, 29:7154-7162.
124. Neirynck S., Deroo T., Saelens X., Vanlandschoot P., Jou W.M., Fiers W. A universal influenza A vaccine based on the extracellular domain of the M2 protein. Nature Medicine 1999, 5:1157-1163.
125. Ionescu R.M., Przysiecki C.T., Liang X., Garsky V.M., Fan J., Wang B., et al. Pharmaceutical and immunological evaluation of human papillomavirus virus like particle as an antigen carrier. Journal of Pharmaceutical Sciences 2006, 95:70-79.
126. Kanekiyo M., Wei C.-J., Yassine H.M., McTamney P.M., Boyington J.C., Whittle J.R., et al. Self-assembling influenza nanoparticle vaccines elicit broadly neutralizing H1N1 antibodies. Nature 2013, 499:102-106.
127. Champion C.I., Kickhoefer V.A., Liu G., Moniz R.J., Freed A.S., Bergmann L.L., et al. A vault nanoparticle vaccine induces protective mucosal immunity. PLoS ONE 2009, 4:e5409.
128. Shah P., Bhalodia D., Shelat P. Nanoemulsion: a pharmaceutical review. Systematic Reviews in Pharmacy 2010, 1:24-32.
129. Aucouturier J., Dupuis L., Ganne V. Adjuvants designed for veterinary and human vaccines. Vaccine 2001, 19:2666-2672.
130. O'Hagan D.T. MF59 is a safe and potent vaccine adjuvant that enhances protection against influenza virus infection. Expert Review of Vaccines 2007, 6:699-710.
131. De Donato S., Granoff D., Minutello M., Lecchi G., Faccini M., Agnello M., et al. Safety and immunogenicity of MF59-adjuvanted influenza vaccine in the elderly. Vaccine 1999, 17:3094-3101.
132. Nicholson K.G., Colegate A.E., Podda A., Stephenson I., Wood J., Ypma E., et al. Safety and antigenicity of non-adjuvanted and MF59-adjuvanted influenza A/Duck/Singapore/97 (H5N3) vaccine: a randomized trial of two potential vaccines against H5N1 influenza. The Lancet 2001, 357:1937-1943.
133. Aucouturier J., Dupuis L., Deville S., Ascarateil S., Ganne V. Montanide ISA 720 and 51: a new generation of water in oil emulsions as adjuvants for human vaccines. Expert Review of Vaccines 2002, 1:111-118.
134. Kumar S., Jones T.R., Oakley M.S., Zheng H., Kuppusamy S.P., Taye A., et al. CpG oligodeoxynucleotide and Montanide ISA 51 adjuvant combination enhanced the protective efficacy of a subunit malaria vaccine. Infection and Immunity 2004, 72:949-957.
135. Oliveira G.A., Wetzel K., Calvo-Calle J.M., Nussenzweig R., Schmidt A., Birkett A., et al. Safety and enhanced immunogenicity of a hepatitis B core particle plasmodium falciparum malaria vaccine formulated in adjuvant Montanide ISA 720 in a phase I trial. Infection and Immunity 2005, 73:3587-3597.
136. Dar P., Kalaivanan R., Sied N., Mamo B., Kishore S., Suryanaryana V.S., et al. Montanide ISA™ 201 adjuvanted FMD vaccine induces improved immune responses and protection in cattle. Vaccine 2013, 31:3327-3332.
137. Chuan Y.P., Zeng B.Y., O'Sullivan B., Thomas R., Middelberg A.P.J. Co-delivery of antigen and a lipophilic anti-inflammatory drug to cells via a tailorable nanocarrier emulsion. Journal of Colloid and Interface Science 2012, 368:616-624.
138. Zeng B.J., Chuan Y.P., O'Sullivan B., Caminschi I., Lahoud M.H., Thomas R., et al. Receptor-specific delivery of protein antigen to dendritic cells by a nanoemulsion formed using top-down non-covalent click self-assembly. Small 2013, 9:3736-3742.
139. Oyewumi M.O., Kumar A., Cui Z. Nano-microparticles as immune adjuvants: correlating particle sizes and the resultant immune responses. Expert Review of Vaccines 2010, 9:1095-1107.
140. Wendorf J., Singh M., Chesko J., Kazzaz J., Soewanan E., Ugozzoli M., et al. A practical approach to the use of nanoparticles for vaccine delivery. Journal of Pharmaceutical Sciences 2006, 95:2738-2750.
141. Stieneker F., Kreuter J., Lower J. High antibody-titers in mice with polymethylmethacrylate nanoparticles as adjuvant for HIV vaccines. AIDS 1991, 5:431-435.
142. Slütter B., Soema P.C., Ding Z., Verheul R., Hennink W., Jiskoot W. Conjugation of ovalbumin to trimethyl chitosan improves immunogenicity of the antigen. Journal of Controlled Release 2010, 143:207-214.
143. Morel S., Didierlaurent A., Bourguignon P., Delhaye S., Baras B., Jacob V., et al. Adjuvant System AS03 containing [alpha]-tocopherol modulates innate immune response and leads to improved adaptive immunity. Vaccine 2011, 29:2461-2473.
144. O'Hagan D.T., Ott G.S., Van Nest G. Recent advances in vaccine adjuvants: the development of MF59 emulsion and polymeric microparticles. Molecular Medicine Today 1997, 3:69-75.
145. Wibowo N. Engineering viral capsomeres as a vaccine platform 2012, 85-107. Australian Institute for Bioengineering & Nanotechnology, The University of Queensland, [Ph.D. thesis].
146. Vallhov H., Kupferschmidt N., Gabrielsson S., Paulie S., Strømme M., Garcia-Bennett A.E., et al. Adjuvant properties of mesoporous silica particles tune the development of effector T cells. Small 2012, 8:2116-2124.
147. Vallhov H., Gabrielsson S., StrÃ̧mme M., Scheynius A., Garcia-Bennett A.E. Mesoporous silica particles induce size dependent effects on human dendritic cells. Nano Letters 2007, 7:3576-3582.
148. Reddy S.T., Swartz M.A., Hubbell J.A. Targeting dendritic cells with biomaterials: developing the next generation of vaccines. Trends in Immunology 2006, 27:573-579.
149. Jones K.S. Biomaterials as vaccine adjuvants. Biotechnology Progress 2008, 24:807-814.
150. Abensee J.E.B. Interaction of dendritic cells with biomaterials. Seminars in Immunology 2008, 20:101-108.
151. Bachmann M.F., Jennings G.T. Vaccine delivery: a matter of size, geometry, kinetics and molecular patterns. Nature Reviews Immunology 2010, 10:787-796.
152. Scheerlinck J.-P.Y., Greenwood D.L.V. Virus-sized vaccine delivery systems. Drug Discovery Today 2008, 13:882-887.
153. Zolnik B.S., Gonzalez-Fernandez A., Sadrieh N., Dobrovolskaia M.A. Minireview: nanoparticles and the immune system. Endocrinology 2010, 151:458-465.
154. Dobrovolskaia M.A., Aggarwal P., Hall J.B., McNeil S.E. Preclinical studies to understand nanoparticle interaction with the immune system and its potential effects on nanoparticle biodistribution. Molecular Pharmaceutics 2008, 5:487-495.
155. Kumari A., Yadav S.K. Cellular interactions of therapeutically delivered nanoparticles. Expert Opinion on Drug Delivery 2011, 8:141-151.
156. Xiang S.D., Scholzen A., Minigo G., David C., Apostolopoulos V., Mottram P.L., et al. Pathogen recognition and development of particulate vaccines: does size matter. Methods 2006, 40:1-9.
157. Akagi T., Wang X., Uto T., Baba M., Akashi M. Protein direct delivery to dendritic cells using nanoparticles based on amphiphilic poly(amino acid) derivatives. Biomaterials 2007, 28:3427-3436.
158. Uto T., Wang X., Sato K., Haraguchi M., Akagi T., Akashi M., et al. Targeting of antigen to dendritic cells with poly(gamma-glutamic acid) nanoparticles induces antigen-specific humoral and cellular immunity. Journal of Immunology 2007, 178:2979-2986.
159. Copland M.J., Baird M.A., Rades T., McKenzie J.L., Becker B., Reck F., et al. Liposomal delivery of antigen to human dendritic cells. Vaccine 2003, 21:883-890.
160. 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. Vaccine 2004, 22:2406-2412.
161. Lutsiak M.E.C., Robinson D.R., Coester C., Kwon G.S., Samuel J. Analysis of poly(d,l-lactic-co-glycolic acid) nanosphere uptake by human dendritic cells and macrophages in vitro. Pharmaceutical Research 2002, 19:1480-1487.
162. Lin A.Y., Lunsford J., Bear A.S., Young J.K., Eckels P., Luo L., et al. High-density sub-100-nm peptide-gold nanoparticle complexes improve vaccine presentation by dendritic cells in vitro. Nanoscale Research Letters 2013, 8:72.
163. 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. International Journal of Pharmaceutics 2005, 298:315-322.
164. Joshi V.B., Geary S.M., Salem A.K. Biodegradable particles as vaccine delivery systems: size matters. AAPS Journal 2013, 15:85-94.
165. Kanchan V., Panda A.K. Interactions of antigen-loaded polylactide particles with macrophages and their correlation with the immune response. Biomaterials 2007, 28:5344-5357.
166. Kim H., Uto T., Akagi T., Baba M., Akashi M. Amphiphilic poly(amino acid) nanoparticles induce size-dependent dendritic cell maturation. Advanced Functional Materials 2010, 20:3925-3931.
167. Cohen J.A., Beaudette T.T., Tseng W.W., Bachelder E.M., Mende I., Engleman E.G., et al. T-cell activation by antigen-loaded pH-sensitive hydrogel particles in vivo: the effect of particle size. Bioconjugate Chemistry 2009, 20:111-119.
168. Yan S., Gu W., Xu Z.P. Re-considering how particle size and other properties of antigen-adjuvant complexes impact on the immune responses. Journal of Colloid and Interface Science 2013, 395:1-10.
169. Thiele L., Merkle H.P., Walter E. Phagocytosis and phagosomal fate of surface-modified microparticles in dendritic cells and macrophages. Pharmaceutical Research 2003, 20:221-228.
170. Wischke C., Borchert H.-H., Zimmermann J., Siebenbrodt I., Lorenzen D.R. Stable cationic microparticles for enhanced model antigen delivery to dendritic cells. Journal of Controlled Release 2006, 114:359-368.
171. Nakanishi T., Kunisawa J., Hayashi A., Tsutsumi Y., Kubo K., Nakagawa S., et al. Positively charged liposome functions as an efficient immunoadjuvant in inducing cell-mediated immune response to soluble proteins. Journal of Controlled Release 1999, 61:233-240.
172. Yotsumoto S., Aramaki Y., Kakiuchi T., Tsuchiya S. Induction of antigen-dependent interleukin-12 production by negatively charged liposomes encapsulating antigens. Vaccine 2004, 22:3503-3509.
173. Goodman C.M., McCusker C.D., Yilmaz T., Rotello V.M. Toxicity of gold nanoparticles functionalized with cationic and anionic side chains. Bioconjugate Chemistry 2004, 15:897-900.
174. Champion J.A., Mitragotri S. Role of target geometry in phagocytosis. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:4930-4934.
175. Champion J.A., Mitragotri S. Shape induced inhibition of phagocytosis of polymer particles. Pharmaceutical Research 2009, 26:244-249.
176. Hillaireau H., Couvreur P. Nanocarriers' entry into the cell: relevance to drug delivery. Cellular and Molecular Life Sciences 2009, 66:2873-2896.
177. Raghuvanshi R.S., Katare Y.K., Lalwani K., Ali M.M., Singh O., Panda A.K. Improved immune response from biodegradable polymer particles entrapping tetanus toxoid by use of different immunization protocol and adjuvants. International Journal of Pharmaceutics 2002, 245:109-121.
178. Aggarwal P., Hall J.B., McLeland C.B., Dobrovolskaia M.A., McNeil S.E. Nanoparticle interaction with plasma proteins as it relates to particle biodistribution, biocompatibility and therapeutic efficacy. Advanced Drug Delivery Reviews 2009, 61:428-437.
179. Nel A.E., Mädler L., Velegol D., Xia T., Hoek E.M., Somasundaran P., et al. Understanding biophysicochemical interactions at the nano-bio interface. Nature Materials 2009, 8:543-557.
180. Moon J.J., Suh H., Li A.V., Ockenhouse C.F., Yadava A., Irvine D.J. Enhancing humoral responses to a malaria antigen with nanoparticle vaccines that expand Tfh cells and promote germinal center induction. Proceedings of the National Academy of Sciences 2012, 109:1080-1085.
181. Reddy S.T., van der Vlies A.J., Simeoni E., Angeli V., Randolph G.J., O'Neill C.P., et al. Exploiting lymphatic transport and complement activation in nanoparticle vaccines. Nature Biotechnology 2007, 25:1159-1164.
182. Seubert A., Monaci E., Pizza M., O'Hagan D.T., Wack A. The adjuvants aluminum hydroxide and MF59 induce monocyte and granulocyte chemoattractants and enhance monocyte differentiation toward dendritic cells. Journal of Immunology 2008, 180:5402-5412.
183. Oussoren C., Storm G. Lymphatic uptake and biodistribution of liposomes after subcutaneous injection. 3. Influence of surface modification with poly(ethyleneglycol). Pharmaceutical Research 1997, 14:1479-1484.
184. Swartz M.A. The physiology of the lymphatic system. Advanced Drug Delivery Reviews 2001, 50:3-20.
185. Cubas R., Zhang S., Kwon S.K., Sevick-Muraca E.M., Li M., Chen C.Y., et al. Virus-like particle (VLP) lymphatic trafficking and immune response generation after immunization by different routes. Journal of Immunotherapy 2009, 32:118-128.
186. Dane K.Y., Nembrini C., Tomei A.A., Eby J.K., O'Neil C.P., Velluto D., et al. Nano-sized drug-loaded micelles deliver payload to lymph node immune cells and prolong allograft survival. Journal of Controlled Release 2011, 156:154-160.
187. Fifis T., Gamvrellis A., Crimeen-Irwin B., Pietersz G.A., Li J., Mottram P.L., et al. Size-dependent immunogenicity: therapeutic and protective properties of nano-vaccines against tumors. Journal of Immunology 2004, 173:3148-3154.
188. De Temmerman M.-L., Rejman J., Demeester J., Irvine D.J., Gander B., De Smedt S.C. Particulate vaccines: on the quest for optimal delivery and immune response. Drug Discovery Today 2011, 16:569-582.
189. Manolova V., Flace A., Bauer M., Schwarz K., Saudan P., Bachmann M.F. Nanoparticles target distinct dendritic cell populations according to their size. European Journal of Immunology 2008, 38:1404-1413.
190. Allen T., Hansen C., Guo L. Subcutaneous administration of liposomes: a comparison with the intravenous and intraperitoneal routes of injection. Biochimica et Biophysica Acta (BBA)-Biomembranes 1993, 1150:9-16.
191. Longmire M., Choyke P.L., Kobayashi H. Clearance properties of nano-sized particles and molecules as imaging agents: considerations and caveats. Nanomedicine 2008, 3:703-717.
192. Soo Choi H., Liu W., Misra P., Tanaka E., Zimmer J.P., Itty Ipe B., et al. Renal clearance of quantum dots. Nature Biotechnology 2007, 25:1165-1170.
193. Ohlson M., Sörensson J., Haraldsson B. A gel-membrane model of glomerular charge and size selectivity in series. American Journal of Physiology Renal Physiology 2001, 280:F396-F405.
194. William M.D., Matthew J.L., Bryan D.M. Structural determinants of glomerular permeability. American Journal of Physiology - Renal Physiology 2001, 281:579-596.
195. Almeida J.P.M., Chen A.L., Foster A., Drezek R. In vivo biodistribution of nanoparticles. Nanomedicine 2011, 6:815-835.
196. Arora S., Rajwade J.M., Paknikar K.M. Nanotoxicology and in vitro studies: the need of the hour. Toxicology and Applied Pharmacology 2012, 258:151-165.
197. He C., Hu Y., Yin L., Tang C., Yin C. Effects of particle size and surface charge on cellular uptake and biodistribution of polymeric nanoparticles. Biomaterials 2010, 31:3657-3666.
198. Huang X., Li L., Liu T., Hao N., Liu H., Chen D., et al. The shape effect of mesoporous silica nanoparticles on biodistribution, clearance, and biocompatibility in vivo. ACS Nano 2011, 5:5390-5399.
199. Sulek S., Mammadov B., Mahcicek D.I., Sozeri H., Atalar E., Tekinay A.B., et al. Peptide functionalized superparamagnetic iron oxide nanoparticles as MRI contrast agents. Journal of Materials Chemistry 2011, 21:15157-15162.
200. Lee H., Lee E., Kim D.K., Jang N.K., Jeong Y.Y., Jon S. Antibiofouling polymer-coated superparamagnetic iron oxide nanoparticles as potential magnetic resonance contrast agents for in vivo cancer imaging. Journal of the American Chemical Society 2006, 128:7383-7389.
201. Sun G., Xu J., Hagooly A., Rossin R., Li Z., Moore D.A., et al. Strategies for optimized radiolabeling of nanoparticles for in vivo PET imaging. Advanced Materials 2007, 19:3157-3162.
202. Wang K., He X., Yang X., Shi H. Functionalized silica nanoparticles: a platform for fluorescence imaging at the cell and small animal levels. Accounts of Chemical Research 2013, 46:1367-1376.
203. Judenhofer M.S., Wehrl H.F., Newport D.F., Catana C., Siegel S.B., Becker M., et al. Simultaneous PET-MRI: a new approach for functional and morphological imaging. Nature Medicine 2008, 14:459-465.
204. Hafner A.M., Corthésy B., Merkle H.P. Particulate formulations for the delivery of poly(I:C) as vaccine adjuvant. Advanced Drug Delivery Reviews 2013, 65:1386-1399.
205. Zhao C.X., He L.Z., Qiao S.Z., Middelberg A.P.J. Nanoparticle synthesis in microreactors. Chemical Engineering Science 2011, 66:1463-1479.