Cationic DDA/TDB liposome as a mucosal vaccine adjuvant for uptake by dendritic cells in vitro induces potent humoural immunity

References

• Rappuoli R. Reverse vaccinology. Curr Opin Microbiol. 2000;3:445–450.
   PubMed Web of Science ®Google Scholar
• Rappuoli R, Mandl CW, Black S, et al. Vaccines for the twenty-first century society. Nat Rev Immunol. 2011;11:865–872.
   PubMed Web of Science ®Google Scholar
• McNeil SE, Rosenkrands I, Agger EM, et al. Subunit vaccines: distearoylphosphatidylcholine-based liposomes entrapping antigen of fer a neutral alternative to dimethyldioctadecylammonium-based cationic liposomes as an adjuvant delivery system. J Pharm Sci. 2011;100:1856–1865.
   PubMed Web of Science ®Google Scholar
• Amorij JP, Kersten GF, Saluja V, et al. Towards tailored vaccine delivery: needs, challenges and perspectives. J Control Release. 2012;161:363–376.
   PubMed Web of Science ®Google Scholar
• Lindblad EB, Elhay MJ, Silva R, et al. Adjuvant modulation of immune responses to tuberculosis subunit vaccines. Infect Immun. 1997;65:623–629.
   PubMed Web of Science ®Google Scholar
• Bhavsar MD, Amiji MM. Development of novel biodegradable polymeric nanoparticles-in-microsphere formulation for local plasmid DNA delivery in the gastrointestinal tract. AAPS PharmSciTech. 2008;9:288–294.
   PubMed Web of Science ®Google Scholar
• Schwendener RA. Liposomes as vaccine delivery systems: a review of the recent advances. Ther Adv Vaccines. 2014;2:159–182.
   PubMedGoogle Scholar
• Kakhi Z, Frisch B, Heurtault B, et al. Liposomal constructs for antitumoral vaccination by the nasal route. Biochimie. 2016;130:14–22.
   PubMed Web of Science ®Google Scholar
• Tyagi RK, Garg NK, Jadon R, et al. Elastic liposome-mediated transdermal immunization enhanced the immunogenicity of P. falciparum surface antigen, MSP-119. Vaccine. 2015;33:4630–4638.
   PubMed Web of Science ®Google Scholar
• Tada R, Hidaka A, Iwase N, et al. Intranasal immunization with DOTAP cationic liposomes combined with DC-cholesterol induces potent antigen-specific mucosal and systemic immune responses in mice. PLoS One. 2015;10:e0139785.
   PubMed Web of Science ®Google Scholar
• Christensen D, Korsholm KS, Andersen P, et al. Cationic liposomes as vaccine adjuvants. Expert Rev Vaccines. 2011;10:513–521.
   PubMed Web of Science ®Google Scholar
• Tada R, Muto S, Iwata T, et al. Attachment of class B CpG ODN onto DOTAP/DC-chol liposome in nasal vaccine formulations augments antigen-specific immune responses in mice. BMC Res Notes. 2017;10:68.
   PubMedGoogle Scholar
• Andersen P. Effective vaccination of mice against Mycobacterium tuberculosis infection with a soluble mixture of secreted mycobacterial proteins. Infect Immunity. 1994;62:2536–2544.
   PubMed Web of Science ®Google Scholar
• Lemaire G, Tenu J-P, Petit J-F. Natural and synthetic trehalose diesters as immunomodulators. Med Res Rev. 1986;6:243–274.
   PubMed Web of Science ®Google Scholar
• Kirby DJ, Kaur R, Agger EM, et al. Developing solid particulate vaccine adjuvants – surface bound antigen favouring a humoural response, whereas entrapped antigen shows a tendency for cell mediated immunity. Cdd. 2013;10:268–278.
   PubMed Web of Science ®Google Scholar
• Henriksen-Lacey M, Bramwell VW, Christensen D, et al. Liposomes based on dimethyldioctadecylammonium promote a depot effect and enhance immunogenicity of soluble antigen. J Control Release. 2010;142:180–186.
   PubMed Web of Science ®Google Scholar
• Korsholm KS, Petersen RV, Agger EM, et al. T-helper 1 and T-helper 2 adjuvants induce distinct differences in the magnitude, quality and kinetics of the early inflammatory response at the site of injection. Immunology. 2009;129:75–86.
   PubMed Web of Science ®Google Scholar
• Henriksen-Lacey M, Devitt A, Perrie Y. The vesicle size of DDA:TDB liposomal adjuvants plays a role in the cell-mediated immune response but has no significant effect on antibody production. J Control Release. 2011;154:131–137.
   PubMed Web of Science ®Google Scholar
• Kaur R, Henriksen-Lacey M, Wilkhu J, et al. Effect of incorporating cholesterol into DDA:TDB liposomal adjuvants on bilayer properties, biodistribution, and immune responses. Mol Pharm. 2014;11:197–207.
   PubMed Web of Science ®Google Scholar
• Gebert A, Steinmetz I, Fassbender S, et al. Antigen transport into Peyer's patches: increased uptake by constant numbers of M cells. Am J Pathol. 2004;164:65–72.
   PubMed Web of Science ®Google Scholar
• Kim SH, Jang YS. The development of mucosal vaccines for both mucosal and systemic immune induction and the roles played by adjuvants. Clin Exp Vaccine Res. 2017;6:15–21.
   PubMed Web of Science ®Google Scholar
• Lycke N. Recent progress in mucosal vaccine development: potential and limitations. Nat Rev Immunol. 2012;12:592–605.
   PubMed Web of Science ®Google Scholar
• Jiang PL, Lin HJ, Wang HW, et al. Galactosylated liposome as a dendritic cell-targeted mucosal vaccine for inducing protective anti-tumor immunity. Acta Biomater. 2015;11:356–367.
   PubMed Web of Science ®Google Scholar
• Asanuma H, Thompson AH, Iwasaki T, et al. Isolation and characterization of mouse nasal-associated lymphoid tissue. J Immunol Methods. 1997;202:123–131.
   PubMed Web of Science ®Google Scholar
• Kuper CF, Koornstra PJ, Hameleers DMH, et al. The role of nasopharyngeal lymphoid tissue. Immunol Today. 1992;13:219–224.
   PubMedGoogle Scholar
• Zavari-Nematabad A, Alizadeh-Ghodsi M, Hamishehkar H, et al. Development of quantum-dot-encapsulated liposome-based optical nanobiosensor for detection of telomerase activity without target amplification. Anal Bioanal Chem. 2016;409:1301–1310.
   PubMed Web of Science ®Google Scholar
• Qu W, Zuo W, Li N, et al. Design of multifunctional liposome-quantum dot hybrid nanocarriers and their biomedical application. J Drug Target. 2017;25:1–12.
   PubMed Web of Science ®Google Scholar
• Bangham AD, Standish MM, Watkins JC. Diffusion of univalent ions across the lamellae of swollen phospholipids. J Mol Biol. 1965;13:238–252.
   PubMed Web of Science ®Google Scholar
• Inaba K, Inaba M, Romani N, et al. Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor. J Exp Med. 1992;176:1693–1702.
   PubMed Web of Science ®Google Scholar
• Wang H-W, Jiang P-L, Lin S-F, et al. Application of galactose-modified liposomes as a potent antigen presenting cell targeted carrier for intranasal immunization. Acta Biomater. 2013;9:5681–5688.
   PubMed Web of Science ®Google Scholar
• Perrie Y, Kastner E, Kaur R, et al. A case-study investigating the physicochemical characteristics that dictate the function of a liposomal adjuvant. Hum Vaccin Immunother. 2013;9:1374–1381.
   PubMed Web of Science ®Google Scholar
• Ingvarsson PT, Rasmussen IS, Viaene M, et al. The surface charge of liposomal adjuvants is decisive for their interactions with the Calu-3 and A549 airway epithelial cell culture models. Eur J Pharm Biopharm. 2014;87:480–488.
   PubMed Web of Science ®Google Scholar
• Korsholm KS, Agger EM, Foged C, et al. The adjuvant mechanism of cationic dimethyldioctadecylammonium liposomes. Immunology. 2007;121:216–226.
   PubMed Web of Science ®Google Scholar
• Ma Y, Poisson L, Sanchez-Schmitz G, et al. Assessing the immunopotency of Toll-like receptor agonists in an in vitro tissue-engineered immunological model. Immunology. 2010;130:374–387.
   PubMed Web of Science ®Google Scholar
• Morel PA, Butterfiel LH. Dendritic cell control of immune responses. Front Immunol. 2015;6:1–2.
   PubMed Web of Science ®Google Scholar
• Swartz MA, Hubbell JA, Reddy ST. Lymphatic drainage function and its immunological implications: from dendritic cell homing to vaccine design. Semin Immunol. 2008;20:147–156.
   PubMed Web of Science ®Google Scholar
• Hinshaw VS, Webster RG, Easterday BC, et al. Replication of avian influenza a viruses in mammals. Infect Immun. 1981;34:354–361.
   PubMed Web of Science ®Google Scholar
• Doherty PC, Turner SJ, Webby RG, et al. Influenza and the challenge for immunology. Nat Immunol. 2006;7:449–455.
   PubMed Web of Science ®Google Scholar
• Tasaniyananda N, Chaisri U, Tungtrongchitr A, et al. Mouse model of cat allergic rhinitis and intranasal liposome-adjuvanted refined Fel d 1 vaccine. PLoS One. 2016;11:e0150463.
   PubMed Web of Science ®Google Scholar
• Agger EM, Rosenkrand S, Hansen J, et al. Cationic liposomes formulated with synthetic MycobacterialCordfactor (CAF01) a versatile adjuvant for vaccines with different immunological requirements. PLoS One. 2008;3:e3116.
   PubMed Web of Science ®Google Scholar
• Christensen D, Foged C, Rosenkrands I, et al. CAF01 liposomes as a mucosal vaccine adjuvant: in vitro and in vivo investigations. Int J Pharm. 2010;390:19–24.
   PubMed Web of Science ®Google Scholar
• Werninghaus K, Babiak A, Gross O, et al. Adjuvanticity of a synthetic cord factor analogue for subunit Mycobacterium tuberculosis vaccination requires FcRgamma-Syk-Card9-dependent innate immune activation. J Exp Med. 2009;206:89–97.
   PubMed Web of Science ®Google Scholar