Bordetella pertussis antigens encapsulated into N-trimethyl chitosan nanoparticulate systems as a novel intranasal pertussis vaccine

References

• Kilgore PE, Salim AM, Zervos MJ, et al. Pertussis: microbiology, disease, treatment, and prevention. Clin Microbiol Rev. 2016;29:449–486.
   PubMed Web of Science ®Google Scholar
• Melvin JA, Scheller EV, Miller JF, et al. Bordetella pertussis pathogenesis: current and future challenges. Nat Rev Microbiol. 2014;12:274–288.
   PubMed Web of Science ®Google Scholar
• Siegel SJ, Weiser JN. Mechanisms of bacterial colonization of the respiratory tract. Annu Rev Microbiol. 2015;69:425–444.
   PubMed Web of Science ®Google Scholar
• Solans L, Locht C. The role of mucosal immunity in pertussis. Front Immunol. 2018;9:3068.
   PubMed Web of Science ®Google Scholar
• Berbers GA, de Greeff SC, Mooi F. Improving pertussis vaccination. Hum Vaccin. 2009;5:497–503.
   PubMed Web of Science ®Google Scholar
• Storsaeter J, Wolter J, Locht C. Pertussis vaccines. In Locht C, editor. Bordetella molecular microbiology. Norfolk, UK: Horizon Press; 2007. p. 245–288.
   Google Scholar
• Kuchar E, Karlikowska-Skwarnik M, Han S, et al. Pertussis: history of the disease and current prevention failure. In: Pokorski M, editor. Pulmonary dysfunction and disease. Cham, Switzerland: Springer International Publishing; 2016. p. 77–82.
   Google Scholar
• Poolman JT, Hallander H. Acellular pertussis vaccines and the role of pertactin and fimbriae. Expert Rev Vacc. 2007;6:47–56.
   PubMed Web of Science ®Google Scholar
• Locht C, Mielcarek N, Microbiology M. New pertussis vaccination approaches: en route to protect newborns? FEMS Immunol Med Microbiol. 2012;66:121–133.
   PubMed Web of Science ®Google Scholar
• Klein NP, Bartlett J, Rowhani-Rahbar A, et al. Waning protection after fifth dose of acellular pertussis vaccine in children. N Engl J Med. 2012;367:1012–1019.
   PubMed Web of Science ®Google Scholar
• Warfel JM, Zimmerman LI, Merkel T. Acellular pertussis vaccines protect against disease but fail to prevent infection and transmission in a nonhuman primate model. PNAS. 2014;111:787–792.
   PubMed Web of Science ®Google Scholar
• Burdin N, Handy LK, Plotkin S. What is wrong with pertussis vaccine immunity? Cold Spring Harb Perspect Biol. 2017;9:a029454.
   PubMed Web of Science ®Google Scholar
• Locht C. Pertussis: where did we go wrong and what can we do about it? J Infect. 2016;72:S34–S40.
   PubMed Web of Science ®Google Scholar
• van den Berg BM, Beekhuizen H, Willems RJ, et al. Role of Bordetella pertussis virulence factors in adherence to epithelial cell lines derived from the human respiratory tract. Infect. Immun 1999;67:1056–1062.
   PubMed Web of Science ®Google Scholar
• van den Berg BM, Beekhuizen H, Mooi FR, et al. Role of antibodies against Bordetella pertussis virulence factors in adherence of Bordetella pertussis and Bordetella parapertussis to human bronchial epithelial cells. Infect Immun. 1999;67:1050–1055.
   PubMed Web of Science ®Google Scholar
• Ugwoke MI, Agu RU, Verbeke N, et al. Nasal mucoadhesive drug delivery: background, applications, trends and future perspectives. Adv Drug Deliv Rev. 2005;57:1640–1665.
   PubMed Web of Science ®Google Scholar
• Illum L. Nasal drug delivery—possibilities, problems and solutions. J Contr Rel. 2003;87:187–198.
   PubMed Web of Science ®Google Scholar
• Perrie Y, Mohammed AR, Kirby DJ, et al. Vaccine adjuvant systems: enhancing the efficacy of sub-unit protein antigens. Int J Pharm. 2008;364:272–280.
   PubMed Web of Science ®Google Scholar
• Akagi T, Baba M, Akashi M. Biodegradable nanoparticles as vaccine adjuvants and delivery systems: regulation of immune responses by nanoparticle-based vaccine. In Polymers in nanomedicine. Berlin, Heidelberg: Springer; 2011. p. 31–64.
   Google Scholar
• Marasini N, Skwarczynski M, Toth I. Intranasal delivery of nanoparticle-based vaccines. Ther Deliv. 2017;8:151–167.
   PubMed Web of Science ®Google Scholar
• Calvo P, Remunan‐Lopez C, Vila‐Jato JL, et al. Novel hydrophilic chitosan‐polyethylene oxide nanoparticles as protein carriers. J Appl Polym Sci. 1997;63:125–132.
   Web of Science ®Google Scholar
• Slütter B, Bal S, Keijzer 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;28:6282–6291.
   PubMed Web of Science ®Google Scholar
• Smith PK, Krohn RI, Hermanson G, et al. Measurement of protein using bicinchoninic acid. Anal Biochem. 1985;150:76–85.
   PubMed Web of Science ®Google Scholar
• Chen F, Zhang Z-R, Huang Y. Evaluation and modification of N-trimethyl chitosan chloride nanoparticles as protein carriers. Int J Pharm. 2007;336:166–173.
   PubMed Web of Science ®Google Scholar
• Shi W, Kou Y, Jiang H, et al. Novel intranasal pertussis vaccine based on bacterium-like particles as a mucosal adjuvant. Immunol Lett. 2018;198:26–32.
   PubMed Web of Science ®Google Scholar
• Higgs R, Higgins S, Ross P, et al. Immunity to the respiratory pathogen Bordetella pertussis. Mucos Immunol. 2012;5:485.
   PubMed Web of Science ®Google Scholar
• Ross PJ, Sutton CE, Higgins S, et al. Relative contribution of Th1 and Th17 cells in adaptive immunity to Bordetella pertussis: towards the rational design of an improved acellular pertussis vaccine. PLoS One. 2013;9:e1003264.
   Google Scholar
• Allen AC, Wilk MM, Misiak A, et al. Sustained protective immunity against Bordetella pertussis nasal colonization by intranasal immunization with a vaccine-adjuvant combination that induces IL-17-secreting T RM cells. Mucos Immunol. 2018;11:1763.
   PubMed Web of Science ®Google Scholar
• Mehrabi M, Montazeri H, Mohamadpour Dounighi N, et al. Chitosan-based nanoparticles in mucosal vaccine delivery. Arch Razi Inst. 2018;73:165–176.
   PubMedGoogle Scholar
• Jabbal-Gill I, Watts P, Smith A. Chitosan-based delivery systems for mucosal vaccines. Expert Opin Drug Deliv. 2012;9:1051–1067.
   PubMed Web of Science ®Google Scholar
• Choi C, Nam JP, Nah JW, et al. Application of chitosan and chitosan derivatives as biomaterials. J Ind Eng Chem. 2016;33:1–10.
   Web of Science ®Google Scholar
• Verheul RJ, Amidi M, van der Wal S, et al. Synthesis, characterization and in vitro biological properties of O-methyl free N, N, N-trimethylated chitosan. Biomaterials. 2008;29:3642–3649.
   PubMed Web of Science ®Google Scholar
• Vila A, Sanchez A, Evora C, et al. PLA-PEG particles as nasal protein carriers: the influence of the particle size. Int J Pharm. 2005;292:43–52.
   PubMed Web of Science ®Google Scholar
• Gutierro I, Hernández RM, Igartua M, et al. Size dependent immune response after subcutaneous, oral and intranasal administration of BSA loaded nanospheres. Vaccine. 2002;21:67–77.
   PubMed Web of Science ®Google Scholar
• Neutra MR, Kozlowski P. Mucosal vaccines: the promise and the challenge. Nat Rev Immunol. 2006;6:148.
   PubMed Web of Science ®Google Scholar
• Pardeshi CV, Belgamwar VS. Controlled synthesis of N,N,N-trimethyl chitosan for modulated bioadhesion and nasal membrane permeability. Int J Biol Macromol. 2016;82:933–944.
   PubMed Web of Science ®Google Scholar
• Slütter B, Plapied L, Fievez V, et al. Mechanistic study of the adjuvant effect of biodegradable nanoparticles in mucosal vaccination. J Contr Rel. 2009;138:113–121.
   PubMed 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;25:144–153.
   PubMed Web of Science ®Google Scholar
• Dabaghian M, Latifi AM, Tebianian M, et al. Nasal vaccination with r4M2e. HSP70c antigen encapsulated into N-trimethyl chitosan (TMC) nanoparticulate systems: Preparation and immunogenicity in a mouse model. Vaccine. 2018;36:2886–2895.
   PubMed Web of Science ®Google Scholar
• Amini Y, Tebianian M, Mosavari N, et al. Development of an effective delivery system for intranasal immunization against Mycobacterium tuberculosis ESAT-6 antigen. Artific Cells, Nanomed, Biotech. 2017;45:291–296.
   PubMed Web of Science ®Google Scholar
• Subbiah R, Ramalingam P, Ramasundaram S, et al. N,N,N-Trimethyl chitosan nanoparticles for controlled intranasal delivery of HBV surface antigen . Carbohydr Polym. 2012;89:1289–1297.
   PubMed Web of Science ®Google Scholar
• Vllasaliu D, Exposito-Harris R, Heras A, et al. Tight junction modulation by chitosan nanoparticles: comparison with chitosan solution. Int J Pharmac. 2010;400:183–193.
   PubMed Web of Science ®Google Scholar
• Ramvikas M, Arumugam M, Chakrabarti SR, et al. Nasal Vaccine Delivery. In Skwarczynski M, Toth I, editors. Micro and nanotechnology in vaccine development. Norwich, NY: William Andrew Publishing; 2017. p. 279–301.
   Google Scholar
• Hellwig SM, van Spriel AB, Schellekens JF, et al. Immunoglobulin A-mediated protection against Bordetella pertussis infection. Infect Immun. 2001;69:4846–4850.
   PubMed Web of Science ®Google Scholar
• Jabbal-Gill I, Fisher AN, Rappuoli R, et al. Stimulation of mucosal and systemic antibody responses against Bordetella pertussis filamentous haemagglutinin and recombinant pertussis toxin after nasal administration with chitosan in mice. Vaccine. 1998;16:2039–2046.
   PubMed Web of Science ®Google Scholar
• Cropley I, Douce G, Roberts M, et al. Mucosal and systemic immunogenicity of a recombinant, non-ADP-ribosylating pertussis toxin: effects of formaldehyde treatment. Vaccine. 1995;13:1643–1648.
   PubMed Web of Science ®Google Scholar