Development of chitosan–pullulan composite nanoparticles for nasal delivery of vaccines: optimisation and cellular studies

References

• Almeida AJ, Alpar HO. Nasal delivery of vaccines. J Drug Target, 1996;3:455–67
   PubMed Web of Science ®Google Scholar
• Alpar HO, Eyles JE, Williamson ED, Somavarapu S. Intranasal vaccination against plague, tetanus and diphtheria. Adv Drug Deliver Rev, 2001;51:173–201
   PubMed Web of Science ®Google Scholar
• Alpar HO, Somavarapu S, Atuah KN, Bramwell V. Biodegradable mucoadhesive particulates for nasal and pulmonary antigen and DNA delivery. Adv Drug Deliver Rev, 2005;57:411–30
   PubMed Web of Science ®Google Scholar
• Amidi M, Romeijn SG, Borchard G, Junginger HE, Hennink WE, Jiskoot W. Preparation and characterization of protein-loaded N-trimethyl chitosan nanoparticles as nasal delivery system. J Control Release, 2006;111:107–16
   PubMed Web of Science ®Google Scholar
• Amidi M, Romeijn SG, Verhoef JC, Junginger HE, Bungener L, Huckriede A, Crommelin DJA, Jiskoot W. N-Trimethyl chitosan (TMC) nanoparticles loaded with influenza subunit antigen for intranasal vaccination: Biological properties and immunogenicity in a mouse model. Vaccine, 2007;25:144–53
   PubMed Web of Science ®Google Scholar
• Amidi M, Mastrobattista E, Jiskoot W, Hennink WE. Chitosan-based delivery systems for protein therapeutics and antigens. Adv Drug Deliv Rev, 2010;62:59–82
   PubMed Web of Science ®Google Scholar
• Artursson P, Lindmark T, Davis SS, Illum L. Effect of chitosan on the permeability of monolayers of intestinal epithelial-cells (Caco-2). Pharm Res, 1994;11:1358–61
   PubMed Web of Science ®Google Scholar
• Bakeev KN, Izumrudov VA, Kuchanov SI, Zezin AB, Kabanov VA. Kinetics and mechanism of interpolyelectrolyte exchange and addition-reactions. Macromolecules, 1992;25:4249–54
   Web of Science ®Google Scholar
• Borchard G. Calu-3 cells, a valid model for the airway epithelium? STP Pharm Sci, 2002;12:205–11
   Google Scholar
• Borges O, Tavares J, de Sousa A, Borchard G, Junginger HE, Cordeiro-Da-Silva A. Evaluation of the immune response following a short oral vaccination schedule with hepatitis B antigen encapsulated into alginate-coated chitosan nanoparticles. Eur J Pharm Sci, 2007;32:278–90
   PubMed Web of Science ®Google Scholar
• Carreno-Gomez B, Duncan R. Evaluation of the biological properties of soluble chitosan and chitosan microspheres. Int J Pharm, 1997;148:231–40
   Web of Science ®Google Scholar
• Chen Q, Hu Y, Chen Y, Jiang XQ, Yang YH. Microstructure formation and property of chitosan-poly(acrylic acid) nanoparticles prepared by macromolecular complex. Macromol Biosci, 2005;5:993–1000
   PubMed Web of Science ®Google Scholar
• Choi NW, Verbridge SS, Williams RM, Chen J, Kim J-Y, Schmehl R, Farnum CE, Zipfel WR, Fischbach C, Stroock AD. Phosphorescent nanoparticles for quantitative measurements of oxygen profiles in vitro and in vivo. Biomaterials, 2012;33:2710–22
   PubMed Web of Science ®Google Scholar
• Chopra S, Mahdi S, Kaur J, Iqbal Z, Talegaonkar S, Ahmad FJ. Advances and potential applications of chitosan derivatives as mucoadhesive biomaterials in modern drug delivery. J Pharm Pharmacol, 2006;58:1021–32
   PubMed Web of Science ®Google Scholar
• Costalat M, Alcouffe P, David L, Delair T. Controlling the complexation of polysaccharides into multi-functional colloidal assemblies for nanomedicine. J Colloid Interf Sci, 2014;430:147–56
   PubMed Web of Science ®Google Scholar
• Csaba N, Köping-Höggård M, Fernandez-Megia E, Novoa-Carballal R, Riguera R, Alonso MJ. Ionically crosslinked chitosan nanoparticles as gene delivery systems: Effect of PEGylation degree on in vitro and in vivo gene transfer. J Biomed Nanotechnol, 2009;5:162–71
   PubMed Web of Science ®Google Scholar
• Davis SS. Nasal vaccines. Adv Drug Deliver Rev, 2001;51:21–42
   PubMed Web of Science ®Google Scholar
• Davis SS. The use of soluble polymers and polymer microparticles to provide improved vaccine responses after parenteral and mucosal delivery. Vaccine, 2006;24:S7–10
   Web of Science ®Google Scholar
• de Vasconcelos CL, Bezerril PM, dos Santos DES, Dantas TNC, Pereira MR, Fonseca JLC. Effect of molecular weight and ionic strength on the formation of polyelectrolyte complexes based on poly(methacrylic acid) and chitosan. Biomacromolecules, 2006;7:1245–52
   PubMed Web of Science ®Google Scholar
• Freitas S, Merkle HP, Gander B. Microencapsulation by solvent extraction/evaporation: Reviewing the state of the art of microsphere preparation process technology. J Control Release, 2005;102:313–32
   PubMed Web of Science ®Google Scholar
• Fujimura Y, Akisada T, Harada T, Haruma K. Uptake of microparticles into the epithelium of human nasopharyngeal lymphoid tissue. Med Mol Morphol, 2006;39:181–6
   PubMed Web of Science ®Google Scholar
• Gaspar R, Duncan R. Polymeric carriers: Preclinical safety and the regulatory implications for design and development of polymer therapeutics. Adv Drug Deliv Rev, 2009;61:220–31
   Web of Science ®Google Scholar
• Glinel K, Sauvage JP, Oulyadi H, Huguet J. Determination of substituents distribution in carboxymethyl pullulans by NMR spectroscopy. Carbohydr Res, 2000;328:343–54
   PubMed Web of Science ®Google Scholar
• Gupta M, Gupta AK. Hydrogel pullulan nanoparticles encapsulating pBUDLacZ plasmid as an efficient gene delivery carrier. J Control Release, 2004;99:157–66
   PubMed Web of Science ®Google Scholar
• Harding SE, Varum KM, Stokke BT, Smidsrod O. 1991. Molecular weight determination of polysaccharides. In: White CA, ed. Advances in carbohydrate analysis. Vol. 1. Birmingham, UK: JAI Press Ltd, pp. 63–144
   Google Scholar
• Hartig SM, Greene RR, Dikov MM, Prokop A, Davidson JM. Multifunctional nanoparticulate polyelectrolyte complexes. Pharm Res, 2007;24:2353–69
   PubMed Web of Science ®Google Scholar
• Hasegawa T, Hirota K, Tomoda K, Ito F, Inagawa H, Kochi C, Soma G, Makino K, Terada H. Phagocytic activity of alveolar macrophages toward polystyrene latex microspheres and PLGA microspheres loaded with anti-tuberculosis agent. Colloids Surf B Biointerfaces, 2007;60:221–8
   PubMed Web of Science ®Google Scholar
• 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;31:3657–66
   PubMed Web of Science ®Google Scholar
• Hirota K, Terada H. 2012. Endocytosis of particle formulations by macrophages ain its application to clinical treatment. In: Ceresa B, ed. Molecular regulation of endocytosis. Croatia: Intech Open Acces, pp. 413–28
   Google Scholar
• Honary S, Zahir F. Effect of zeta potential on the properties of nano-drug delivery systems -- A review (Part 1). Trop J Pharm Res, 2013;12:255–64
   Web of Science ®Google Scholar
• Horie K, Sakagami M, Kuramochi K, Hanasaki K, Hamana H, Ito T. Enhanced accumulation of sialyl Lewis X-carboxymethylpullulan conjugate in acute inflammatory lesion. Pharm Res, 1999;16:314–20
   PubMed Web of Science ®Google Scholar
• Illum L, Jabbal-Gill I, Hinchcliffe M, Fisher AN, Davis SS. Chitosan as a novel nasal delivery system for vaccines. Adv Drug Deliver Rev, 2001;51:81–96
   PubMed Web of Science ®Google Scholar
• Jiang WL, Gupta RK, Deshpande MC, Schwendeman SP. Biodegradable poly(lactic-co-glycolic acid) microparticles for injectable delivery of vaccine antigens. Adv Drug Deliver Rev, 2005;57:391–410
   PubMed Web of Science ®Google Scholar
• Kamide K, Dobashi T. 2000. Physical chemistry of polymer solutions. Theoretical background. Amsterdam, The Netherlands: Elsevier B.V
   Google Scholar
• Kammona O, Kiparissides C. Recent advances in nanocarrier-based mucosal delivery of biomolecules. J Control Release, 2012;161:781--94
   Google Scholar
• Katas H, Alpar HO. Development and characterisation of chitosan nanoparticles for siRNA delivery. J Control Release, 2006;115:216–25
   PubMed Web of Science ®Google Scholar
• Kean T, Roth S, Thanou M. Trimethylated chitosans as non-viral gene delivery vectors: Cytotoxicity and transfection efficiency. J Control Release, 2005;103:643–53
   PubMed Web of Science ®Google Scholar
• Kensil CR, Mo AXY, Truneh A. Current vaccine adjuvants: An overview of a diverse class. Fron Biosci, 2004;9:2972–88
   PubMed Web of Science ®Google Scholar
• Kotze AF, Luessen HL, deLeeuw BJ, deBoer BG, Verhoef JC, Junginger HE. N-trimethyl chitosan chloride as a potential absorption enhancer across mucosal surfaces: In vitro evaluation in intestinal epithelial cells (Caco-2). Pharm Res, 1997;14:1197–202
   PubMed Web of Science ®Google Scholar
• Kuper CF, Koornstra PJ, Hameleers DMH, Biewenga J, Spit BJ, Duijvestijn AM, Vriesman PJC, Sminia T. The role of nasopharyngeal lymphoid-tissue. Immunol Today, 1992;13:219–24
   PubMedGoogle Scholar
• Leathers TD. Biotechnological production and applications of pullulan. Appl Microbiol Biotechnol, 2003;62:468–73
   PubMed Web of Science ®Google Scholar
• Lin YH, Chung CK, Chen CT, Liang HF, Chen SC, Sung HW. Preparation of nanoparticles composed of chitosan/poly-gamma-glutamic acid and evaluation of their permeability through Caco-2 cells. Biomacromolecules, 2005;6:1104–12
   PubMed Web of Science ®Google Scholar
• Lin YH, Mi FL, Chen CT, Chang WC, Peng SF, Liang HF, Sung HW. Preparation and characterization of nanoparticles shelled with chitosan for oral insulin delivery. Biomacromolecules, 2007;8:146–52
   PubMed Web of Science ®Google Scholar
• Liu Q, Zhang C, Zheng X, Shao X, Zhang X, Zhang Q, Jiang X. Preparation and evaluation of antigen/N trimethylaminoethylmethacrylate chitosan conjugates for nasal immunization. Vaccine, 2014;32:2582--90
   Google Scholar
• Makino K, Yamamoto N, Higuchi K, Harada N, Ohshima H, Terada H. Phagocytic uptake of polystyrene microspheres by alveolar macrophages: Effects of the size and surface properties of the microspheres. Colloids Surf B Biointerfaces, 2003;27:33–9
   Web of Science ®Google Scholar
• Mangal S, Pawar D, Garg NK, Jain AK, Vyas SP, Raman Rao DSV, Jaganathan KS. Pharmaceutical and immunological evaluation of mucoadhesive nanoparticles based delivery system(s) administered intranasally. Vaccine, 2011;29:4953--62
   Google Scholar
• Mao S, Shuai X, Unger F, Wittmar M, Xie X, Kissel T. Synthesis, characterization and cytotoxicity of poly(ethylene glycol)-graft-trimethyl chitosan block copolymers. Biomaterials, 2005;26:6343–56
   PubMed Web of Science ®Google Scholar
• Masuda K, Sakagami M, Horie K, Nogusa H, Hamana H, Hirano K. Evaluation of carboxymethyl pullulan as a novel carrier for targeting immune tissues. Pharm Res, 2001;18:217–23
   PubMed Web of Science ®Google Scholar
• McKeever DJ, Rege JEO. Vaccines and diagnostic tools for animal health: The influence of biotechnology. Livest Prod Sci, 1999;59:257–64
   Google Scholar
• Mi FL, Wu YY, Chiu YL, Chen MC, Sung HW, Yu SH, Shyu SS, Huang MF. Synthesis of a novel glycoconjugated chitosan and preparation of its derived nanoparticles for targeting HepG2 cells. Biomacromolecules, 2007;8:892–8
   PubMed Web of Science ®Google Scholar
• Mi FL, Wu YY, Lin YH, Sonaje K, Ho YC, Chen CT, Juang JH, Sung HW. Oral delivery of peptide drugs using nanoparticles self-assembled by poly(γ-glutamic acid) and a chitosan derivative functionalized by trimethylation. Bioconjug Chem, 2008;19:1248–55
   PubMed Web of Science ®Google Scholar
• Mitani S, Yamamoto A, Ikegami H, Usui M, Matuhasi T. Immunoglobulin E-suppressing and immunoglobulin G-enhancing tetanus toxoid prepared by conjugation with pullulan. Infect Immun, 1982;36:971–6
   PubMed Web of Science ®Google Scholar
• Mutsaers SE, Papadimitriou JM. Surface charge of macrophages and their interaction with charged particles. J Leukoc Biol, 1988;44:17–26
   PubMed Web of Science ®Google Scholar
• O'Hagan DT, Valiante NM. Recent advances in the discovery and delivery of vaccine adjuvants. Nat Rev Drug Discov, 2003;2:727–35
   PubMed Web of Science ®Google Scholar
• Ohno N, Kurachi K, Yadomae T. Physicochemical properties and antitumor activities of carboxymethylated derivatives of glucan from sclerotinia-sclerotiorum. Chem Pharm Bull, 1988;36:1016–25
   PubMed Web of Science ®Google Scholar
• Pandit S, Cevher E, Zariwala MG, Somavarapu S, Alpar HO. 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
   PubMed Web of Science ®Google Scholar
• Polnok A, Borchard G, Verhoef JC, Sarisuta N, Junginger HE. Influence of methylation process on the degree of quaternization of N-trimethyl chitosan chloride. Eur J Pharm Biopharm, 2004;57:77–83
   PubMed Web of Science ®Google Scholar
• Ramasamy T, Tran TH, Cho HJ, Kim JH, Kim YI, Jeon JY, Choi H-G, Yong CS, Kim JO. Chitosan-based polyelectrolyte complexes as potential nanoparticulate carriers: Physicochemical and biological characterization. Pharm Res, 2014;31:1302–14
   PubMed Web of Science ®Google Scholar
• Rekha MR, Chandra PS. Pullulan as a promising biomaterial for biomedical applications: A perspective. Trends Biomater Artif Organs, 2007;20:116–21
   Google Scholar
• Rodrigues S, Dionísio M, López CR, Grenha A. Biocompatibility of chitosan carriers with application in drug delivery. J Funct Biomater, 2012;3:615–41
   PubMedGoogle Scholar
• Sayın B, Somavarapu S, Li XW, Sesardic D, Şenel S, Alpar HO. TMC–MCC (N-trimethyl chitosan–mono-N-carboxymethyl chitosan) nanocomplexes for mucosal delivery of vaccines. Eur J Pharm Sci, 2009;38:362–9
   PubMed Web of Science ®Google Scholar
• Schatz C, Domard A, Viton C, Pichot C, Delair T. Versatile and efficient formation of colloids of biopolymer-based polyelectrolyte complexes. Biomacromolecules, 2004;5:1882–92
   PubMed Web of Science ®Google Scholar
• Sieval AB, Thanou M, Kotze AF, Verhoef JE, Brussee J, Junginger HE. Preparation and NMR characterization of highly substituted N-trimethyl chitosan chloride. Carbohydr Polym, 1998;36:157–65
   Web of Science ®Google Scholar
• Singla AK, Chawla M. Chitosan: Some pharmaceutical and biological aspects – An update. J Pharm Pharmacol, 2001;53:1047–67
   PubMed Web of Science ®Google Scholar
• Slütter B, Bal S, Keijzer C, Mallants R, Hagenaars N, Que I, Kaijzel E, van Eden W, Augustijns P, Löwik C, 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
   Google Scholar
• Subbiah R, Ramalingam P, Ramasundaram S, Kim do Y, Park K, Ramasamy MK, Choi KJ. N,N,N-Trimethyl chitosan nanoparticles for controlled intranasal delivery of HBV surface antigen. Carbohydr Polym, 2012;89:1289--97
   Google Scholar
• Sugumaran KR, Sindhu RV, Sukanya S, Aiswarya N, Ponnusami V. Statistical studies on high molecular weight pullulan production in solid state fermentation using jack fruit seed. Carbohydr Polym, 2013;98:854–60
   PubMed Web of Science ®Google Scholar
• Tabata Y, Ikada Y. Effect of the size and surface charge of polymer microspheres on their phagocytosis by macrophage. Biomaterials, 1988;9:356–62
   PubMed Web of Science ®Google Scholar
• Tafaghodi M, Saluja V, Kersten GF, Kraan H, Slütter B, Amorij JP, Jiskoot W. Hepatitis B surface antigen nanoparticles coated with chitosan and trimethyl chitosan: Impact of formulation on physicochemical and immunological characteristics. Vaccine, 2012;30:5341--8
   Google Scholar
• Tafaghodi M, Tabassi SAS, Jaafari MR. Induction of systemic and mucosal immune responses by intranasal administration of alginate microspheres encapsulated with tetanus toxoid and CpG-ODN. Int J Pharm, 2006;319:37–43
   PubMed Web of Science ®Google Scholar
• Thanou M, Verhoef JC, Junginger HE. Oral drug absorption enhancement by chitosan and its derivatives. Adv Drug Deliver Rev, 2001;52:117–26
   PubMed Web of Science ®Google Scholar
• Tripathy S, Das S, Chakraborty SP, Sahu SK, Pramanik P, Roy S. Synthesis, characterization of chitosan–tripolyphosphate conjugated chloroquine nanoparticle and its in vivo anti-malarial efficacy against rodent parasite: A dose and duration dependent approach. Int J Pharm, 2012;434:292–305
   PubMed Web of Science ®Google Scholar
• Tsuji K, Fujimoto M, Masuko F, Nagase T. 1978. Carboxymethylated pullulan and method for producing same. US Patent 4090016
   Google Scholar
• Ulmer JB. Enhancement of vaccine potency through improved delivery. Expert Opin Bioll Ther, 2004;4:1045–51
   PubMed Web of Science ®Google Scholar
• Vajdy M, Srivastava I, Polo J, Donnelly J, O'Hagan D, Singh M. Mucosal adjuvants and delivery systems for protein-, DNA- and RNA-based vaccines. Immunol Cell Biol, 2004;82:617–27
   PubMed Web of Science ®Google Scholar
• van der Lubben IM, Kersten G, Fretz MM, Beuvery C, Verhoef JC, Junginger HE. Chitosan microparticles for mucosal vaccination against diphtheria: Oral and nasal efficacy studies in mice. Vaccine, 2003;21:1400–8
   PubMed Web of Science ®Google Scholar
• van der Lubben IM, Verhoef JC, Fretz MM, Van Opdorp FAC, Mesu I, Kersten G, Junginger HE. Trimethyl chitosan chloride (TMC) as a novel excipient for oral and nasal immunisation against diphtheria. STP Pharm Sci, 2002;12:235–42
   Google Scholar
• van der Merwe SM, Verhoef JC, Verheijden JHM, Kotze AF, Junginger HE. Trimethylated chitosan as polymeric absorption enhancer for improved peroral delivery of peptide drugs. Eur J Pharm Biopharm, 2004;58:225–35
   PubMed Web of Science ®Google Scholar
• Venkatesan C, Vimal S, Sahul Hameed AS. Synthesis and characterization of chitosan tripolyphosphate nanoparticles and its encapsulation efficiency containing Russell's viper snake venom. J Biochem Mol Toxicol, 2013;27:406–11
   PubMed Web of Science ®Google Scholar
• Vila A, Sanchez A, Janes K, Behrens I, Kissel T, Jato JLV, Alonso MJ. Low molecular weight chitosan nanoparticles as new carriers for nasal vaccine delivery in mice. Eur J Pharm Biopharm, 2004;57:123–31
   PubMed Web of Science ®Google Scholar
• Wang TW, Xu Q, Wu Y, Zeng AJ, Li M, Gao X. Quaternized chitosan (QCS/poly(aspartic acid) nanoparticles as a protein drug delivery system. Carbohydr Res, 2009;344:908–14
   PubMed Web of Science ®Google Scholar
• Yamaya S, Yamamoto A, Komiya T, Mizuguchi J, Matuhasi T. Preparation of a diphtheria-toxin pullulan conjugate that elicits good IgG antibody production with poor IgE synthesis. Vaccine, 1990;8:65–9
   PubMed Web of Science ®Google Scholar
• Yang Y-W, Hsu PY-J. The effect of poly(d,l-lactide-co-glycolide) microparticles with polyelectrolyte self-assembled multilayer surfaces on the cross-presentation of exogenous antigens. Biomaterials, 2008;29:2516–26
   PubMed Web of Science ®Google Scholar
• Yeh M-K, Cheng K-M, Hu C-S, Huang Y-C, Young J-J. Novel protein-loaded chondroitin sulfate–chitosan nanoparticles: Preparation and characterization. Acta Biomater, 2011;7:3804–12
   PubMed Web of Science ®Google Scholar