Induction of adaptive immune response by self-aggregating peptides

References

• Akagi T, Baba M, Akashi M. Biodegradable nanoparticles as vaccine adjuvants and delivery systems: regulation of immune responses by nanoparticle-based vaccine. Adv Polym Sci. 2012;247:31–64.
   Google Scholar
• Arnon R, Ben-Yedidia T. Old and new vaccine approaches. Int Immunopharmacol. 2003;3(8):1195–1204.
   PubMed Web of Science ®Google Scholar
• Plummer EM, Manchester M. Viral nanoparticles and virus-like particles: platforms for contemporary vaccine design. Wiley Interdiscip Rev Nanomed Nanobiotechnol. 2011;3(2):174–196.
   PubMed Web of Science ®Google Scholar
• Moron VG, Rueda P, Sedlik C, et al. Dendritic cells can cross-present virus-like particles using an endosome-to-cytosol pathway. J Immunol. 2003;171(5):2242–2250.
   PubMed Web of Science ®Google Scholar
• Ludwig C, Wagner R. Virus-like particles-universal molecular toolboxes. Curr Opin Biotechnol. 2007;18(6):537–545.
   PubMed Web of Science ®Google Scholar
• Grgacic EVL, Anderson DA. Virus-like particles: passport to immune recognition. Methods. 2006;40(1):60–65.
   PubMed Web of Science ®Google Scholar
• Crisci E, Bárcena J, Montoya M. Virus-like particles: the new frontier of vaccines for animal viral infections. Vet Immunol Immunopathol. 2012;148(3–4):211–225.
   PubMed Web of Science ®Google Scholar
• Sharp FA, Ruane D, Claass B, et al.. Uptake of particulate vaccine adjuvants by dendritic cells activates the NALP3 inflammasome. Proc Natl Acad Sci U S A. 2009;106(3):870–875.
   PubMed Web of Science ®Google Scholar
• Spellberg B, Edwards JE. Type 1/Type 2 immunity in infectious diseases. Clin Infect Dis. 2001;32:76–102.
   PubMed Web of Science ®Google Scholar
• Shoenfeld Y, Agmon-Levin N. “ASIA” - Autoimmune/inflammatory syndrome induced by adjuvants. J Autoimmun. 2011;36(1):4–8.
   PubMed Web of Science ®Google Scholar
• Noad R, Roy P. Virus-like particles as immunogens Trends Microbiol. 2003;11(9):438–444.
   PubMed Web of Science ®Google Scholar
• Singh M, Kazzaz J, Ugozzoli M, et al. MF59 oil-in-water emulsion in combination with a synthetic TLR4 agonist (E6020) is a potent adjuvant for a combination Meningococcus vaccine. Hum Vaccin Immunother. 2012;8(4):486–490.
   PubMed Web of Science ®Google Scholar
• Chen J, Pompano RR, Santiago FW, et al.. The use of self-adjuvanting nanofiber vaccines to elicit high-affinity B cell responses to peptide antigens without inflammation. Biomaterials. 2013;34(34):8776–8785.
   PubMed Web of Science ®Google Scholar
• Gazit E. Self assembly of short aromatic peptides into amyloid fibrils and related nanostructures. Prion. 2007;1(1):32–35.
   PubMed Web of Science ®Google Scholar
• Gazit E. Self-assembled peptide nanostructures: the design of molecular building blocks and their technological utilization. Chem Soc Rev. 2007;36(8):1263.
   PubMed Web of Science ®Google Scholar
• Hauser CAE, Zhang S. Designer self-assembling peptide nanofiber biological materials. Chem Soc Rev. 2010;39(8):2780.
   PubMed Web of Science ®Google Scholar
• Fink AL. Protein aggregation: folding aggregates, inclusion bodies and amyloid. Fold Des. 1998;3(1):9–23.
   PubMedGoogle Scholar
• Wang J, Liu K, Xing R, et al.. Peptide self-assembly: thermodynamics and kinetics. Chem Soc Rev. 2016;45(20):5589–5604.
   PubMed Web of Science ®Google Scholar
• Loo Y, Zhang S, Hauser CAE. From short peptides to nanofibers to macromolecular assemblies in biomedicine. Biotechnol Adv. 2012;30(3):593–603.
   PubMed Web of Science ®Google Scholar
• Rad-Malekshahi M, Lempsink L, Amidi M, et al. Biomedical applications of self-assembling peptides. Bioconjug Chem. 2016;27(1):3–18.
   PubMed Web of Science ®Google Scholar
• Cavalli S, Albericio F, Kros A. Amphiphilic peptides and their cross-disciplinary role as building blocks for nanoscience. Chem Soc Rev. 2010;39(1):241–263.
   PubMed Web of Science ®Google Scholar
• Banerji B, Chatterjee M, Pal U, et al. Formation of annular protofibrillar assembly by cysteine tripeptide: unraveling the interactions with NMR, FTIR, and molecular dynamics. J Phys Chem B. 2017;121(26):6367–6379.
   PubMed Web of Science ®Google Scholar
• Sun F, Chen L, Ding X, et al. High-resolution insights into the stepwise self-assembly of nanofiber from bioactive peptides. J Phys Chem B. 2017;121(31):7421–7430.
   PubMed Web of Science ®Google Scholar
• Olsen KW. Internal residue criteria for predicting three-dimensional protein structures. Biochim Biopghysica Acts. 1980;622:259–267.
   PubMedGoogle Scholar
• Durell SR, Ben-Naim A. Hydrophobic-hydrophilic forces in protein folding. Biopolymers. 2017;107:8.
   Web of Science ®Google Scholar
• Damaschun G, Damaschun H, Gast K, et al. Proteins can adopt totally different folded conformations. J Mol Biol. 1999;291:715–725.
   PubMed Web of Science ®Google Scholar
• Rudra JS, Tripathi PK, Hildeman DA, et al.. Immune responses to coiled coil supramolecular biomaterials. Biomaterials. 2010;31(32):8475–8483.
   PubMed Web of Science ®Google Scholar
• Hauser CAE, Deng R, Mishra A, et al.. Natural tri- to hexapeptides self-assemble in water to amyloid-type fiber aggregates by unexpected -helical intermediate structures. Proc Natl Acad Sci. 2011;108(4):1361–1366.
   PubMed Web of Science ®Google Scholar
• Ross CA, Poirier MA. Protein aggregation and neurodegenerative disease. Nat Med. 2004;10(7):S10–S17.
   PubMed Web of Science ®Google Scholar
• Ke PC, Sani M-A, Ding F, Kakinen A, Javed I, Separovic F, et al. Implications of peptide assemblies in amyloid diseases. Chem Soc Rev. 2017
   Web of Science ®Google Scholar
• Fowler DM, Koulov AV, Balch WE, et al. Functional amyloid - from bacteria to humans. Trends Biochem Sci. 2007;32(5):217–224.
   PubMed Web of Science ®Google Scholar
• Maji SK, Perrin MH, Sawaya MR, et al. Functional amyloid as natural storage of peptide hormones in pituitary granules. Science (80-). 2010;325(5938):328–332.
   Web of Science ®Google Scholar
• Jacob RS, Das S, Ghosh S, et al.. Amyloid formation of growth hormone in presence of zinc: relevance to its storage in secretory granules. Sci Rep. 2016;6(1):23370.
   PubMedGoogle Scholar
• Petrlova J, Hansen FC, Van der Plas MJA, et al.. Aggregation of thrombin-derived C-terminal fragments as a previously undisclosed host defense mechanism. Proc Natl Acad Sci. 2017;114(21):E4213–E4222.
   PubMed Web of Science ®Google Scholar
• Pizzi A, Pigliacelli C, Gori A, et al.. Halogenation dictates the architecture of amyloid peptide nanostructures. Nanoscale. 2017;9(28):9805–9810.
   PubMed Web of Science ®Google Scholar
• Xie Y, Wang Y, Qi W, et al. Reconfigurable chiral self-assembly of peptides through control of terminal charges. Small. 2017;13(30):1–8.
   Web of Science ®Google Scholar
• Gilead S, Gazit E. Self-organization of short peptide fragments: from amyloid fibrils to nanoscale supramolecular assemblies. Supramol Chem. 2005;17(1–2):87–92.
   Web of Science ®Google Scholar
• Westermark P, Engström U, Johnson K,A, et al. Islet amyloid polypeptide: pinpointing amino acid residues linked to amyloid fibril formation. Proc Natl Acad Sci U S A. 1990;87:5036–5040.
   PubMed Web of Science ®Google Scholar
• Haspel N, Zanuy D, Ma B, et al. A comparative study of amyloid fibril formation by residues 15–19 of the human calcitonin hormone: a single β-sheet model with a small hydrophobic core. J Mol Biol. 2005;345(5):1213–1227.
   PubMed Web of Science ®Google Scholar
• Adler-Abramovich L, Reches M, Sedman VL, et al. Thermal and chemical stability of diphenylalanine peptide nanotubes: implications for nanotechnological applications. Langmuir. 2006;22(3):1313–1320.
   PubMed Web of Science ®Google Scholar
• Mandal D, Nasrolahi Shirazi A, Parang K. Self-assembly of peptides to nanostructures. Org Biomol Chem. 2014;12(22):3544–3561.
   PubMed Web of Science ®Google Scholar
• Smith AM, Williams RJ, Tang C, et al. Fmoc-diphenylalanine self assembles to a hydrogel via a novel architecture based on π-π interlocked β-sheets. Adv Mater. 2008;20(1):37–41.
   Web of Science ®Google Scholar
• Yamagata N, Chen X, Zhou J, et al.. Enzymatic self-assembly of an immunoreceptor tyrosine-based inhibitory motif (ITIM). Org Biomol Chem. 2017;15(27):5689–5692.
   PubMed Web of Science ®Google Scholar
• Rudra JS, Mishra S, Chong AS, et al.. Self-assembled peptide nanofibers raising durable antibody responses against a malaria epitope. Biomaterials. 2012;33(27):6476–6484.
   PubMed Web of Science ®Google Scholar
• Collier JH, Messersmith PB. Enzymatic modification of self-assembled peptide structures with tissue transglutaminase. Bioconjug Chem. 2003;14(4):748–755.
   PubMed Web of Science ®Google Scholar
• Cjc E-G, Hamley IW. Self-assembly of bioactive peptides, peptide conjugates, and peptide mimetic materials. Org Biomol Chem. 2017;15(28):5867–5876.
   PubMed Web of Science ®Google Scholar
• Lu S, Wang H, Sheng Y, et al.. Molecular binding of self-assembling peptide EAK16-II with anticancer agent EPT and its implication in cancer cell inhibition. J Control Release. 2012;160(1):33–40.
   PubMed Web of Science ®Google Scholar
• Hao R, Zhang J, Xu T, et al.. Characterization and assembly investigation of a dodecapeptide hydrolyzed from the crystalline domain of Bombyx mori silk fibroin. Polym Chem. 2013;4(10):3005.
   Web of Science ®Google Scholar
• Ye Z, Zhang H, Luo H, et al. Temperature and pH effects on biophysical and morphological properties of self-assembling peptide RADA16-I. J Pept Sci. 2008;14:152–162.
   PubMed Web of Science ®Google Scholar
• Paramonov SE, Jun HW, Hartgerink JD. Self-assembly of peptide-amphiphile nanofibers: the roles of hydrogen bonding and amphiphilic packing. J Am Chem Soc. 2006;128(22):7291–7298.
   PubMed Web of Science ®Google Scholar
• Zhao X, Pan F, Xu H, et al.. Molecular self-assembly and applications of designer peptide amphiphiles. Chem Soc Rev. 2010;39(9):3480.
   PubMed Web of Science ®Google Scholar
• Kornmueller K, Lehofer B, Leitinger G, et al. Peptide self-assembly into lamellar phases and the formation of lipid-peptide nanostructures. Nano Res. 2017;1:1–16.
   Google Scholar
• Mishra A, Loo Y, Deng R, et al. Ultrasmall natural peptides self-assemble to strong temperature-resistant helical fibers in scaffolds suitable for tissue engineering. Nano Today. 2011;6(3):232–239.
   Web of Science ®Google Scholar
• Zhou X-R, Cao Y, Zhang Q, et al.. Self-assembly nanostructure controlled sustained release, activity and stability of peptide drugs. Int J Pharm. 2017;528(1–2):723–731.
   PubMed Web of Science ®Google Scholar
• Tu Z, Hao J, Kharidia R, et al. Improved stability and selectivity of lytic peptides through self-assembly. Biochem Biophys Res Commun. 2007;361(3):712–717.
   PubMed Web of Science ®Google Scholar
• Trent A, Marullo R, Lin B, et al.. Structural properties of soluble peptide amphiphile micelles. Soft Matter. 2011;7(20):9572.
   Web of Science ®Google Scholar
• Trent AR, Ulery BD, Black MJ, et al.. Peptide amphiphile micelles self-adjuvant group a streptococcal vaccination. AAPS J. 2015;17(2):380–388.
   PubMed Web of Science ®Google Scholar
• Black M, Trent A, Kostenko Y, et al. Self-assembled peptide amphiphile micelles containing a cytotoxic T-cell epitope promote a protective immune response in vivo. Adv Mater. 2012;24(28):3845–3849.
   PubMed Web of Science ®Google Scholar
• Zaman M, Abm A-A, Fujita Y, et al. Structure-activity relationship for the development of a self-adjuvanting mucosally active lipopeptide vaccine against Streptococcus pyogenes. J Med Chem. 2012;55(19):8515–8523.
   PubMed Web of Science ®Google Scholar
• Abm A-A, Batzloff MR, Fujita Y, et al. Structure-activity relationship of a series of synthetic lipopeptide self-adjuvanting group A streptococcal vaccine candidates. J Med Chem. 2008;51(1):167–172.
   PubMed Web of Science ®Google Scholar
• Zaman M, Chandrudu S, Giddam AK, et al. Group A Streptococcal vaccine candidate: contribution of epitope to size, antigen presenting cell interaction and immunogenicity. Nanomedicine. 2014;9(17):2613–2624.
   PubMed Web of Science ®Google Scholar
• Raman S, Machaidze G, Lustig A, et al. Structure-based design of peptides that self-assemble into regular polyhedral nanoparticles. Nanomedicine Nanotechnology, Biol Med. 2006;2(2):95–102.
   PubMed Web of Science ®Google Scholar
• Kaba SA, Brando C, Guo Q, et al. A non-adjuvanted polypeptide nanoparticle vaccine confers long-lasting protection against rodent malaria. J Immunol. 2009;183(11):7268–7277.
   PubMed Web of Science ®Google Scholar
• Wahome N, Pfeiffer T, Ambiel I, et al. Conformation-specific display of 4E10 and 2F5 epitopes on self-assembling protein nanoparticles as a potential HIV vaccine. Chem Biol Drug Des. 2012;80(3):349–357.
   PubMed Web of Science ®Google Scholar
• Sampieri A, Luz-Madrigal A, Zepeda J, et al.. Identification of fragments from Autographa californica polyhedrin protein essential for self-aggregation and exogenous protein incorporation. BMC Biochem. 2015;16(1):1–12. .
   PubMedGoogle Scholar
• Kamita SG, Maeda S, Hammock BD. High-frequency homologous recombination between baculoviruses involves. DNA Replication †. 2003;77(24):13053–13061.
   Google Scholar
• Vicente T, Roldão A, Peixoto C, et al.. Large-scale production and purification of VLP-based vaccines. J Invertebr Pathol. 2011;107(SUPPL.):S42–8.
   PubMed Web of Science ®Google Scholar
• Slack J, Arif BM. The baculoviruses occlusion-derived virus: virion structure and function. Adv Virus Res. 2006;69(6):99–165.
   Google Scholar
• Hamley IW, Kirkham S, Dehsorkhi A, et al.. Toll-like receptor agonist lipopeptides self-assemble into distinct nanostructures. Chem Commun. 2014;50(100):15948–15951.
   PubMed Web of Science ®Google Scholar
• Vauthey S, Santoso S, Gong H, et al.. Molecular self-assembly of surfactant-like peptides to form nanotubes and nanovesicles. Proc Natl Acad Sci U S A. 2002Apr16; 99(8): 5355–5360.
   PubMed Web of Science ®Google Scholar
• Xiang SD, Scholzen A, Minigo G, et al. Pathogen recognition and development of particulate vaccines: does size matter?. Methods. 2006;40(1):1–9.
   PubMed Web of Science ®Google Scholar
• Xiang SD, Wilson K, Day S, et al.. Methods of effective conjugation of antigens to nanoparticles as non-inflammatory vaccine carriers. Methods. 2013;60(3):232–241.
   PubMed Web of Science ®Google Scholar
• Zhang T, Yu W, Wang Y, et al.. PEGylation of the carrier protein improves the polysaccharide-specific immunogenicity of meningococcal group A polysaccharide conjugate vaccine. Vaccine. 2015;33(28):3208–3214.
   PubMed Web of Science ®Google Scholar
• Rad-Malekshahi M, Fransen MF, Krawczyk M, et al. Self-assembling peptide epitopes as novel platform for anticancer vaccination. Mol Pharm. 2017;14(5):1482–1493.
   PubMed Web of Science ®Google Scholar
• Azmi F, Aah AF, Giddam AK, et al.. Self-adjuvanting vaccine against group A streptococcus: application of fibrillized peptide and immunostimulatory lipid as adjuvant. Bioorganic Med Chem. 2014;22(22):6401–6408.
   PubMed Web of Science ®Google Scholar
• Kawai T, Akira S. Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity. 2011;34(5): 637–650.
   PubMed Web of Science ®Google Scholar
• Takeuchi O, Akira S. Pattern recognition receptors and inflammation. Cell. 2010;140(6): 805–820.
   PubMed Web of Science ®Google Scholar
• Van Duin D, Medzhitov R, Shaw AC. Triggering TLR signaling in vaccination. Trends Immunol. 2006;27(1):49–55.
   PubMed Web of Science ®Google Scholar
• Foster SL, Medzhitov R. Gene-specific control of the TLR-induced inflammatory response. Clin Immunol. 2009;130(1): 7–15.
   PubMed Web of Science ®Google Scholar
• HogenEsch H. Mechanism of immunopotentiation and safety of aluminum adjuvants. Front Immunol. 2012 JAN;3:1–13.
   PubMed Web of Science ®Google Scholar
• Klen J, Goričar K, Janež A, et al.. NLRP3 Inflammasome polymorphism and macrovascular complications in type 2 diabetes patients. J Diabetes Res. 2015;June1–6.
   Web of Science ®Google Scholar
• Wright TH, Brooks AES, Didsbury AJ, et al. Direct peptide lipidation through thiol-ene coupling enables rapid synthesis and evaluation of self-adjuvanting vaccine candidates. Angew Chemie - Int Ed. 2013;52(40):10616–10619.
   PubMed Web of Science ®Google Scholar
• Moussa EM, Panchal JP, Moorthy BS, et al.. Immunogenicity of therapeutic protein aggregates. J Pharm Sci. 2016;105(2):417–430.
   PubMed Web of Science ®Google Scholar
• Bachmann MF, Hoffmann Rohrer U, Kündig TM, et al.. The influence of antigen organization on B cell responsiveness. Source Sci New Ser. 1993;262226229(26):1448–1451.
   Google Scholar
• López-Sagaseta J, Malito E, Rappuoli R, et al.. Self-assembling protein nanoparticles in the design of vaccines. Comput Struct Biotechnol J. 2016;14:58–68.
   PubMedGoogle Scholar
• Ratanji KD, Derrick JP, Dearman RJ, et al.. Immunogenicity of therapeutic proteins: influence of aggregation. J Immunotoxicol. 2014;11(2):99–109.
   PubMed Web of Science ®Google Scholar
• Bawa R, Fung SY, Shiozaki A, et al.. Self-assembling peptide-based nanoparticles enhance cellular delivery of the hydrophobic anticancer drug ellipticine through caveolae-dependent endocytosis. Nanomed Nanotechnol Biol Med. 2012;8(5):647–654.
   PubMed Web of Science ®Google Scholar
• Bachmann MF, Jennings GT. Vaccine delivery: a matter of size, geometry, kinetics and molecular patterns. Nat Rev Immunol. 2010;10(11):787–796.
   PubMed Web of Science ®Google Scholar
• Rudra JS, Tian YF, Jung JP, et al.. A self-assembling peptide acting as an immune adjuvant. Proc Natl Acad Sci. 2010;107(2):622–627.
   PubMed Web of Science ®Google Scholar
• Szabo SJ, Sullivan BM, Peng SL, et al.. Molecular mechanisms regulating Th1 immune responses. Annu Rev Immunol. 2003;21(1):713–758.
   PubMedGoogle Scholar
• Rudra JS, Sun T, Bird KC, et al.. Modulating adaptive immune responses to peptide self-assemblies. ACS Nano. 2012;6(2):1557–1564.
   PubMed Web of Science ®Google Scholar
• Sun T, Han H, Hudalla GA, et al.. Thermal stability of self-assembled peptide vaccine materials. Acta Biomater. 2016;30:62–71.
   PubMed Web of Science ®Google Scholar
• Pimentel TAPF, Yan Z, Jeffers SA, et al.. Peptide nanoparticles as novel immunogens: design and analysis of a prototypic severe acute respiratory syndrome vaccine. Chem Biol. 2009;73(1):53–61.
   Google Scholar
• Chesson CB, Huelsmann EJ, Lacek AT, et al.. Antigenic peptide nanofibers elicit adjuvant-free CD8+ T cell responses. Vaccine. 2014;32(10):1174–1180.
   PubMed Web of Science ®Google Scholar
• Pross S, Lefkowitz D. Cell-mediated immunity. 2007;Cmi:1–4.
   Google Scholar
• El Bissati K, Zhou Y, Dasgupta D, et al.. Effectiveness of a novel immunogenic nanoparticle platform for toxoplasma peptide vaccine in HLA transgenic mice. Vaccine. 2014;32(26):3243–3248.
   PubMed Web of Science ®Google Scholar
• Mccoy ME, Golden HE, Doll TA, et al. Mechanisms of protective immune responses induced by the Plasmodium falciparum protein nanoparticle vaccine. Malar. J. 2013;12:136. doi: 10.1186/1475-2875-12-136.
   Google Scholar
• Kaba SA, McCoy ME, Doll TAPF, et al.. Protective antibody and CD8+ T-cell responses to the Plasmodium falciparum circumsporozoite protein induced by a nanoparticle vaccine. PLoS One. 2012;7(10):e48304.
   PubMed Web of Science ®Google Scholar
• Hermeling S, Crommelin DJA, Schellekens H, et al. Structure-immunogenicity relationships of therapeutic proteins. Pharm Res. 2004;21(6):897–903.
   PubMed Web of Science ®Google Scholar
• Danhier F, Ansorena E, Silva JM, et al.. PLGA-based nanoparticles: an overview of biomedical applications. J Control Release. 2012;161(2):505–522.
   PubMed Web of Science ®Google Scholar
• Fredriksen BN, Sævareid K, McAuley L, et al.. Early immune responses in Atlantic salmon (Salmo salar L.) after immunization with PLGA nanoparticles loaded with a model antigen and β-glucan. Vaccine. 2011;29(46):8338–8349. Oct 26 [cited 2013 Nov 29].
   PubMed Web of Science ®Google Scholar
• Fredriksen BN, Grip J. PLGA/PLA micro- and nanoparticle formulations serve as antigen depots and induce elevated humoral responses after immunization of Atlantic salmon (Salmo salar L.) Jan 11 [cited 2013 Nov 29]. Vaccine. 2012;30(3):656–667.
   PubMed Web of Science ®Google Scholar
• Audran R, Peter K, Dannull J, et al. Encapsulation of peptides in biodegradable microspheres prolongs their MHC class-I presentation by dendritic cells and macrophages in vitro. Vaccine. 2003;21(11–12):1250–1255.
   PubMed Web of Science ®Google Scholar
• Chong CSW, Cao M, Wong WW, et al. Enhancement of T helper type 1 immune responses against hepatitis B virus core antigen by PLGA nanoparticle vaccine delivery. J Control Release. 2005;102(1):85–99.
   PubMed Web of Science ®Google Scholar
• Wilson JT, Postma A, Keller S, et al.. Enhancement of MHC-I antigen presentation via architectural control of pH-responsive, endosomolytic polymer nanoparticles. AAPS J. 2015;17(2):358–369.
   PubMed Web of Science ®Google Scholar
• Keijzer C, Slütter B, Van Der Zee R, et al. PLGA-TMC and TMC-TPP nanoparticles differentially modulate the outcome of nasal vaccination by inducing tolerance or enhancing humoral immunity. PLoS One. 2011;6:11.
   Web of Science ®Google Scholar
• Amidi M, Romeijn SG, Verhoef JC, et al. N-Trimethyl chitosan (TMC) nanoparticles loaded with influenza subunit antigen for intranasal vaccination: biological properties and immunogenicity in a mouse model. Vaccine. 2007;25(1):144–153.
   PubMed Web of Science ®Google Scholar
• Hamdy S, Haddadi A, Hung RW, et al.. Targeting dendritic cells with nano-particulate PLGA cancer vaccine formulations. Adv Drug Deliv Rev. 2011;63(10–11):943–955.
   PubMed Web of Science ®Google Scholar
• Silva AL, Soema PC, Slütter B, et al. PLGA particulate delivery systems for subunit vaccines: linking particle properties to immunogenicity. Hum Vaccines Immunother. 2016;12(4):1056–1069.
   PubMed Web of Science ®Google Scholar
• Kumari A, Yadav SK, Yadav SC. Biodegradable polymeric nanoparticles based drug delivery systems. Colloids Surfaces B Biointerfaces. 2010;75(1):1–18.
   PubMed Web of Science ®Google Scholar