Subunit-based mucosal vaccine delivery systems for pulmonary delivery - Are they feasible?

References

• http://www.who.int/news-room/fact-sheets/detail/the-top-10-causes-of-death. 2018.
   Google Scholar
• Carter NJ, Curran MP. Live attenuated influenza vaccine (FluMist(R); Fluenz): a review of its use in the prevention of seasonal influenza in children and adults. Drugs. 2011;71:1591–1622.
   PubMed Web of Science ®Google Scholar
• Rappuoli R, Pizza M, Del Giudice G, et al. Vaccines, new opportunities for a new society. Proc Natl Acad Sci USA. 2014;111:12288–12293.
   PubMed Web of Science ®Google Scholar
• Taddio A, Appleton M, Bortolussi R, et al. Reducing the pain of childhood vaccination: an evidence-based clinical practice guideline. CMAJ. 2010;182:E843–E855.
   PubMed Web of Science ®Google Scholar
• van Aalst S, Ludwig IS, van Kooten PJS, et al. Dynamics of APC recruitment at the site of injection following injection of vaccine adjuvants. Vaccine. 2017;35:1622–1629.
   PubMed Web of Science ®Google Scholar
• Marasini N, Skwarczynski M, Toth I. Oral delivery of nanoparticle-based vaccines. Expert Rev Vaccines. 2014;13:1361–1376.
   PubMed Web of Science ®Google Scholar
• Giudice EL, Campbell JD. Needle-free vaccine delivery. Adv Drug Deliv Rev. 2006;58:68–89. 20
   PubMed Web of Science ®Google Scholar
• Holt PG, Strickland DH, Wikström ME, et al. Regulation of immunological homeostasis in the respiratory tract. Nat Rev Immunol. 2008;8:142.
   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
• Cerutti A, Chen K, Chorny A. Immunoglobulin responses at the mucosal interface. Annu Rev Immunol. 2011;29:273–293.
   PubMed Web of Science ®Google Scholar
• Vissers M, Ahout IM, de Jonge MI, et al. Mucosal IgG levels correlate better with respiratory syncytial virus load and inflammation than plasma IgG levels. Clin Vaccine Immunol. 2015;23:243–245.
   PubMed Web of Science ®Google Scholar
• Wang YY, Kannan A, Nunn KL, et al. IgG in cervicovaginal mucus traps HSV and prevents vaginal herpes infections. Mucosal Immunol. 2014;7:1036–1044.
   PubMed Web of Science ®Google Scholar
• Marasini N, Haque S, Kaminskas LM. Polymer-drug conjugates as inhalable drug delivery systems: a review. Curr Opin Colloid Interface Sci. 2017;31:18–29.
   Web of Science ®Google Scholar
• Sato S, Kiyono H. The mucosal immune system of the respiratory tract. Curr Opin Virol. 2012;2:225–232.
   PubMed Web of Science ®Google Scholar
• Rogan MP, Geraghty P, Greene CM, et al. Antimicrobial proteins and polypeptides in pulmonary innate defence. Respir Res. 2006;7:29.
   PubMed Web of Science ®Google Scholar
• Reed KD, Chapter 84 - respiratory tract infections: a clinical approach. In: Tang Y-W, Sussman M, Liu D, et al., editors. Molecular medical microbiology (Second Edition). Boston: Academic Press; 2015. p. 1499–1506.
   Google Scholar
• Bosch AATM, Biesbroek G, Trzcinski K, et al. Viral and bacterial interactions in the upper respiratory tract. PLOS Pathog. 2013;9:e1003057.
   PubMed Web of Science ®Google Scholar
• Bienenstock J, McDermott MR. Bronchus- and nasal-associated lymphoid tissues. Immunol Rev. 2005;206:22–31.
   PubMed Web of Science ®Google Scholar
• Zuercher AW, Coffin SE, Thurnheer MC, et al. Nasal-associated lymphoid tissue is a mucosal inductive site for virus-specific humoral and cellular immune responses. J Immunol. 2002;168:1796–1803.
   PubMed Web of Science ®Google Scholar
• Plotnicky-Gilquin H, Robert A, Chevalet L, et al. CD4(+) T-cell-mediated antiviral protection of the upper respiratory tract in BALB/c mice following parenteral immunization with a recombinant respiratory syncytial virus G protein fragment. J Virol. 2000;74:3455.
   PubMed Web of Science ®Google Scholar
• Wiley JA, Hogan RJ, Woodland DL, et al. Antigen-specific CD8(+) T cells persist in the upper respiratory tract following influenza virus infection. J Immunol. 2001;167:3293.
   PubMed Web of Science ®Google Scholar
• Kim DY, Sato A, Fukuyama S, et al. The airway antigen sampling system: respiratory M cells as an alternative gateway for inhaled antigens. J Immunol. 2011;186:4253–4262.
   PubMed Web of Science ®Google Scholar
• Saleem I, Petkar K, Somavarapu S. Chapter nineteen - rationale for pulmonary vaccine delivery: formulation and device considerations. In: Skwarczynski M, Toth I, editors. Micro and nanotechnology in vaccine development: William Andrew Publishing; 2017. p. 357–371.
   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
• Blom RAM, Amacker M, van Dijk RM, et al. Pulmonary delivery of virosome-bound antigen enhances antigen-specific CD4+ T cell proliferation compared to liposome-bound or soluble antigen. Front Immunol. 2017;8:359.
   PubMed Web of Science ®Google Scholar
• Shikina T, Hiroi T, Iwatani K, et al. IgA class switch occurs in the organized nasopharynx- and gut-associated lymphoid tissue, but not in the diffuse lamina propria of airways and gut. J Immunol. 2004;172:6259.
   PubMed Web of Science ®Google Scholar
• Nguyen CT, Hong SH, Ung TT, et al. Intranasal immunization with a flagellin-adjuvanted peptide anticancer vaccine prevents tumor development by enhancing specific cytotoxic T lymphocyte response in a mouse model. Clin Exp Vaccine Res. 2013;2:128–134.
   PubMedGoogle Scholar
• Chen X, Liu S, Goraya MU, et al. Host immune response to influenza A virus infection. Front Immunol. 2018; 9:320.
   PubMed Web of Science ®Google Scholar
• Pizzolla A, Wang Z, Groom JR, et al. Nasal-associated lymphoid tissues (NALTs) support the recall but not priming of influenza virus-specific cytotoxic T cells. Proc Natl Acad Sci USA. 2017;114:5225–5230.
   PubMed Web of Science ®Google Scholar
• Martin TR, Frevert CW. Innate immunity in the lungs. Proc Am Thorac Soc. 2005;2:403–411.
   PubMedGoogle Scholar
• Suzuki T, Chow CW, Downey GP. Role of innate immune cells and their products in lung immunopathology. Int J Biochem Cell Biol. 2008;40:1348–1361.
   PubMed Web of Science ®Google Scholar
• Tomioka H, Tatano Y, Maw WW, et al. Characteristics of suppressor macrophages induced by mycobacterial and protozoal infections in relation to alternatively activated M2 macrophages. Clin Dev Immunol. 2012; 635451.
   PubMedGoogle Scholar
• Zhou X, Moore BB. Adoptive transfer of lung antigen presenting cells. Bio-protocol. 2017;7:e2182.
   PubMedGoogle Scholar
• Kirby AC, Coles MC, Kaye PM. Alveolar macrophages transport pathogens to lung draining lymph nodes. J Immunol. 2009;183:1983–1989.
   PubMed Web of Science ®Google Scholar
• Desch AN, Henson PM, Jakubzick CV. Pulmonary dendritic cell development and antigen acquisition. Immunol Res. 2013;55:178–186.
   PubMed Web of Science ®Google Scholar
• von Garnier C, Filgueira L, Wikstrom M, et al. Anatomical location determines the distribution and function of dendritic cells and other APCs in the respiratory tract. J Immunol. 2005;175:1609–1618.
   PubMed Web of Science ®Google Scholar
• El-Sherbiny IM, El-Baz NM, Yacoub MH. Inhaled nano- and microparticles for drug delivery. Glob Cardiol Sci Pract. 2015; 2015:2.
   PubMedGoogle Scholar
• Blank F, Stumbles PA, Seydoux E, et al. Size-dependent uptake of particles by pulmonary antigen-presenting cell populations and trafficking to regional lymph nodes. Am J Respir Cell Mol Biol. 2013;49:67–77.
   PubMed Web of Science ®Google Scholar
• Hardy CL, Lemasurier JS, Mohamud R, et al. Differential uptake of nanoparticles and microparticles by pulmonary APC subsets induces discrete immunological imprints. J Immunol. 2013;191:5278–5290.
   PubMed Web of Science ®Google Scholar
• Thakkar SG, Ruwona TB, Williams RO, et al. The immunogenicity of thin-film freeze-dried, aluminum salt-adjuvanted vaccine when exposed to different temperatures. Hum Vaccin Immunother. 2017;13:936–946.
   PubMed Web of Science ®Google Scholar
• Hatley RHM, Byrne SM. Variability in delivered dose and respirable delivered dose from nebulizers: are current regulatory testing guidelines sufficient to produce meaningful information? Mder. 2017;10:17–28.
   Google Scholar
• Amorij JP, Saluja V, Petersen AH, et al. Pulmonary delivery of an inulin-stabilized influenza subunit vaccine prepared by spray-freeze drying induces systemic, mucosal humoral as well as cell-mediated immune responses in BALB/c mice. Vaccine. 2007;25:8707–8717.
   PubMed Web of Science ®Google Scholar
• McAdams D, Chen D, Kristensen D. Spray drying and vaccine stabilization. Expert Rev Vaccines. 2012;11:1211–1219.
   PubMed Web of Science ®Google Scholar
• Kanojia G, Have R, Soema PC, et al. Developments in the formulation and delivery of spray dried vaccines. Hum Vaccin Immunother. 2017;13:2364–2378.
   PubMed Web of Science ®Google Scholar
• Sou T, Morton DA, Williamson M, et al. Spray-dried influenza antigen with trehalose and leucine produces an aerosolizable powder vaccine formulation that induces strong systemic and mucosal immunity after pulmonary administration. J Aerosol Med Pulm Drug Deliv. 2015;28:361–371.
   PubMed Web of Science ®Google Scholar
• Azmi F, Ahmad Fuaad AA, Skwarczynski M, et al. Recent progress in adjuvant discovery for peptide-based subunit vaccines. Hum Vaccin Immunother. 2014;10:778–796.
   PubMed Web of Science ®Google Scholar
• Di Pasquale A, Preiss S, Tavares Da Silva F, et al. Vaccine adjuvants: from 1920 to 2015 and beyond. Vaccines (Basel). 2015;3:320–343.
   PubMed Web of Science ®Google Scholar
• Lee S, Nguyen MT. Recent advances of vaccine adjuvants for infectious diseases. Immune Netw. 2015;15:51–57.
   PubMed Web of Science ®Google Scholar
• Mohan T, Verma P, Rao DN. Novel adjuvants & delivery vehicles for vaccines development: a road ahead. Indian J Med Res. 2013;138:779–795.
   PubMed Web of Science ®Google Scholar
• Lewis DJM, Huo Z, Barnett S, et al. Transient facial nerve paralysis (Bell's palsy) following intranasal delivery of a genetically detoxified mutant of Escherichia coli heat labile toxin. Plos One. 2009;4:e6999.
   PubMed Web of Science ®Google Scholar
• Zeng L. Mucosal adjuvants: opportunities and challenges. Hum Vaccin Immunother. 2016;12:2456–2458.
   PubMed Web of Science ®Google Scholar
• Royal JM, Matoba N. Therapeutic potential of cholera toxin B subunit for the treatment of inflammatory diseases of the mucosa. Toxins. 2017;9:379.
   Web of Science ®Google Scholar
• Ahmed T, Bhuiyan TR, Zaman K, et al. Vaccines for preventing enterotoxigenic Escherichia coli (ETEC) diarrhoea. Cochrane Database Syst Rev. 2013; 5:Cd009029.
   Google Scholar
• Bergquist C, Johansson EL, Lagergard T, et al. Intranasal vaccination of humans with recombinant cholera toxin B subunit induces systemic and local antibody responses in the upper respiratory tract and the vagina. Infect Immun. 1997;65:2676–2684.
   PubMed Web of Science ®Google Scholar
• Wiedinger K, Pinho D, Bitsaktsis C. Utilization of cholera toxin B as a mucosal adjuvant elicits antibody-mediated protection against S. pneumoniae infection in mice. Ther Adv Vaccines. 2017;5:15–24.
   PubMedGoogle Scholar
• Marasini N, Ghaffar KA, Skwarczynski M, et al. Chapter twelve - liposomes as a vaccine delivery system. In: Skwarczynski M, Toth I, editors. Micro and nanotechnology in vaccine development: William Andrew Publishing; 2017. p. 221–239.
   Google Scholar
• Rudokas M, Najlah M, Alhnan MA, et al. Liposome delivery systems for inhalation: a critical review highlighting formulation issues and anticancer applications. Med Princ Pract. 2016;25: 60–72.
   PubMed Web of Science ®Google Scholar
• Haque S, Whittaker MR, McIntosh MP, et al. Disposition and safety of inhaled biodegradable nanomedicines: opportunities and challenges. Nanomedicine. 2016;12:1703–1724.
   PubMed Web of Science ®Google Scholar
• Moser C, Amacker M, Zurbriggen R. Influenza virosomes as a vaccine adjuvant and carrier system. Expert Rev Vaccines. 2011;10:437–446.
   PubMed Web of Science ®Google Scholar
• Shafique M, Meijerhof T, Wilschut J, et al. Evaluation of an intranasal virosomal vaccine against respiratory syncytial virus in mice: effect of TLR2 and NOD2 ligands on induction of systemic and mucosal immune responses. Plos One. 2013;8:e61287.
   PubMed Web of Science ®Google Scholar
• Kim K-H, Lee Y-T, Hwang HS, et al. Virus-like particle vaccine containing the F protein of respiratory syncytial virus confers protection without pulmonary disease by modulating specific subsets of dendritic cells and effector T cells. J Virol. 2015;89:11692–11705.
   PubMed Web of Science ®Google Scholar
• Chesson CB, Zloza A. Nanoparticles: augmenting tumor antigen presentation for vaccine and immunotherapy treatments of cancer. Nanomedicine (London). 2017;12:2693–2706.
   PubMed Web of Science ®Google Scholar
• Xia X, Mai J, Xu R, et al. Porous silicon microparticle potentiates anti-tumor immunity by enhancing cross-presentation and inducing type I interferon response. Cell Rep. 2015;11:957–966.
   PubMed Web of Science ®Google Scholar
• Reddy ST, van der Vlies AJ, Simeoni E, et al. Exploiting lymphatic transport and complement activation in nanoparticle vaccines. Nat Biotechnol. 2007;25:1159.
   PubMed Web of Science ®Google Scholar
• Gause KT, Wheatley AK, Cui J, et al. Immunological principles guiding the rational design of particles for vaccine delivery. ACS Nano. 2017;11:54–68.
   PubMed Web of Science ®Google Scholar
• Ryan GM, Bischof RJ, Enkhbaatar P, et al. A comparison of the pharmacokinetics and pulmonary lymphatic exposure of a generation 4 PEGylated dendrimer following intravenous and aerosol administration to rats and sheep. Pharm Res. 2016;33:510–525.
   PubMed Web of Science ®Google Scholar
• Ghaffar KA, Marasini N, Giddam AK, et al. The role of size in development of mucosal liposome-lipopeptide vaccine candidates against group A Streptococcus. Med Chem. 2016;13:22–27.
   PubMed Web of Science ®Google Scholar
• Mant A, Chinnery F, Elliott T, et al. The pathway of cross-presentation is influenced by the particle size of phagocytosed antigen. Immunology. 2012;136:163–175.
   PubMed Web of Science ®Google Scholar
• Thomas C, Gupta V, Ahsan F. Particle size influences the immune response produced by hepatitis B vaccine formulated in inhalable particles. Pharm Res. 2010;27:905–919.
   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;40:1–9.
   PubMed Web of Science ®Google Scholar
• Slütter B, Jiskoot W. Sizing the optimal dimensions of a vaccine delivery system: a particulate matter. Expert Opin Drug Deliv. 2016;13:167–170.
   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, Suzuki H, Takahashi S, et al. Nasal vaccination with pneumococcal surface protein A in combination with cationic liposomes consisting of DOTAP and DC-chol confers antigen-mediated protective immunity against Streptococcus pneumoniae infections in mice. Int Immunopharmacol. 2018;61:385–393.
   PubMed Web of Science ®Google Scholar
• Ghaffar KA, Marasini N, Giddam AK, et al. Liposome-based intranasal delivery of lipopeptide vaccine candidates against group A Streptococcus. Acta Biomater. 2016;41:161–168.
   PubMed Web of Science ®Google Scholar
• Marasini N, Ghaffar KA, Giddam AK, et al. Highly immunogenic trimethyl chitosan-based delivery system for intranasal lipopeptide vaccines against group A Streptococcus. Curr Drug Deliv. 2017;14:701–708.
   PubMed Web of Science ®Google Scholar
• Marasini N, Giddam AK, Khalil ZG, et al. Double adjuvanting strategy for peptide-based vaccines: trimethyl chitosan nanoparticles for lipopeptide delivery. Nanomedicine (London). 2016;11:3223–3235.
   PubMed Web of Science ®Google Scholar
• Marasini N, Khalil ZG, Giddam AK, et al. Lipid core peptide/poly(lactic-co-glycolic acid) as a highly potent intranasal vaccine delivery system against Group A Streptococcus. Int J Pharm. 2016;513:410–420.
   PubMed Web of Science ®Google Scholar
• Thomas C, Gupta V, Ahsan F. Influence of surface charge of PLGA particles of recombinant hepatitis B surface antigen in enhancing systemic and mucosal immune responses. Int J Pharm. 2009;379:41–50.
   PubMed Web of Science ®Google Scholar
• Fromen CA, Robbins GR, Shen TW, et al. Controlled analysis of nanoparticle charge on mucosal and systemic antibody responses following pulmonary immunization. Proc Natl Acad Sci USA. 2015;112:488–493.
   PubMed Web of Science ®Google Scholar
• Fromen CA, Rahhal TB, Robbins GR, et al. Nanoparticle surface charge impacts distribution, uptake and lymph node trafficking by pulmonary antigen-presenting cells. Nanomedicine. 2016;12:677–687.
   PubMed Web of Science ®Google Scholar
• Bal SM, Slütter B, Verheul R, et al. Adjuvanted, antigen loaded N-trimethyl chitosan nanoparticles for nasal and intradermal vaccination: adjuvant- and site-dependent immunogenicity in mice. Eur J Pharm Sci. 2012;45:475–481.
   PubMed Web of Science ®Google Scholar
• Hagan D, Singh M, Ugozzoli M, et al. Induction of potent immune responses by cationic microparticles with adsorbed human immunodeficiency virus DNA vaccines. J Virol. 2001;75:9037.
   PubMed Web of Science ®Google Scholar
• Barnier-Quer C, Elsharkawy A, Romeijn S, et al. Adjuvant effect of cationic liposomes for subunit influenza vaccine: influence of antigen loading method, cholesterol and immune modulators. Pharmaceutics. 2013;5:392–410.
   PubMedGoogle Scholar
• Liu L, Ma P, Wang H, et al. Immune responses to vaccines delivered by encapsulation into and/or adsorption onto cationic lipid-PLGA hybrid nanoparticles. J Control Release. 2016;225:230–239.
   PubMed Web of Science ®Google Scholar
• Ulery BD, Kumar D, Ramer-Tait AE, et al. Design of a protective single-dose intranasal nanoparticle-based vaccine platform for respiratory infectious diseases. Plos One. 2011;6:e17642.
   PubMed Web of Science ®Google Scholar
• Shen TW, Fromen CA, Kai MP, et al. Distribution and cellular uptake of PEGylated polymeric particles in the lung towards cell-specific targeted delivery. Pharm Res. 2015;32:3248–3260.
   PubMed Web of Science ®Google Scholar
• Nembrini C, Stano A, Dane KY, et al. Nanoparticle conjugation of antigen enhances cytotoxic T-cell responses in pulmonary vaccination. Proc Natl Acad Sci USA. 2011;108:E989–E997.
   PubMed Web of Science ®Google Scholar
• Doshi N, Mitragotri S. Macrophages recognize size and shape of their targets. Plos One. 2010;5:e10051.
   PubMed Web of Science ®Google Scholar
• Benne N, van Duijn J, Kuiper J, et al. Orchestrating immune responses: how size, shape and rigidity affect the immunogenicity of particulate vaccines. J Control Release. 2016;234:124–134.
   PubMed Web of Science ®Google Scholar
• Kumar S, Anselmo AC, Banerjee A, et al. Shape and size-dependent immune response to antigen-carrying nanoparticles. J Control Release. 2015;220:141–148.
   PubMed Web of Science ®Google Scholar
• Fadeel B. Clear and present danger? Engineered nanoparticles and the immune system. Swiss Med Wkly. 2012;142:w13609.
   PubMed Web of Science ®Google Scholar
• Moyano DF, Goldsmith M, Solfiell DJ, et al. Nanoparticle hydrophobicity dictates immune response. J Am Chem Soc. 2012;134:3965–3967.
   PubMed Web of Science ®Google Scholar
• Li B, Xie J, Yuan Z, et al. Mitigation of inflammatory immune responses with hydrophilic nanoparticles. Angew Chem Int Ed. 2018;57:4527–4531.
   PubMed Web of Science ®Google Scholar
• Vaccines Licensed for Use in the United States [Internet]. 2018. Available from: https://www.fda.gov/BiologicsBloodVaccines/Vaccines/ApprovedProducts/ucm093833.htm.
   Google Scholar
• Jia Y, Krishnan L, Omri A. Nasal and pulmonary vaccine delivery using particulate carriers. Expert Opin Drug Deliv. 2015;12:993–1008.
   PubMed Web of Science ®Google Scholar