Abstract
Pulmonary vaccine delivery has gained significant attention as an alternate route for vaccination without the use of needles. Immunization through the pulmonary route induces both mucosal and systemic immunity, and the delivery of antigens in a dry powder state can overcome some challenges such as cold-chain and availability of medical personnel compared to traditional liquid-based vaccines. Antigens formulated as nanoparticles (NPs) reach the respiratory airways of the lungs providing greater chance of uptake by relevant immune cells. In addition, effective targeting of antigens to the most ‘professional’ antigen presenting cells (APCs), the dendritic cells (DCs) yields an enhanced immune response and the use of an adjuvant further augments the generated immune response thus requiring less antigen/dosage to achieve vaccination. This review discusses the pulmonary delivery of vaccines, methods of preparing NPs for antigen delivery and targeting, the importance of targeting DCs and different techniques involved in formulating dry powders suitable for inhalation.
Abbreviations
- AMs:
-
alveolar macrophages
- APCs:
-
antigen presenting cells
- BAL:
-
bronchoalveolar lavage
- CLRs:
-
C-type lectin receptors
- DCs:
-
dendritic cells
- DPI:
-
dry powder inhalations
- FD:
-
freeze-drying
- HLA:
-
human leukocyte antigen
- ILs:
-
interleukins
- LN:
-
lymph node
- MHC:
-
major histocompatibility complex
- MN:
-
mannan
- NPs:
-
nanoparticles
- PCL:
-
poly-ε-caprolactone
- PEG:
-
polyethylene glycol
- PEI:
-
polyethyleneimine
- PLA:
-
polylactide or poly-L-lactic acid
- PLGA:
-
poly lactic-co-glycolic-acid
- PRRs:
-
pattern recognition receptors
- PVA:
-
polyvinyl alcohol
- SCF:
-
supercritical fluid
- SD:
-
spray-drying
- SFD:
-
spray-freeze drying
- TLRs:
-
toll-like receptors
- TMC:
-
N-trimethyl chitosan
- VLPs:
-
virus-like particles
References
Brown LR. Commercial challenges of protein drug delivery. Expet Opin Drug Deliv. 2005;2:29–42.
Sullivan VJ, Mikszta JA, Laurent P, Huang J, Ford B. Noninvasive delivery technologies: respiratory delivery of vaccines. Expet Opin Drug Deliv. 2006;3:87–95.
Sou T, Meeusen EN, de Veer M, Morton DAV, Kaminskas LM, McIntosh MP. New developments in dry powder pulmonary vaccine delivery. Trends Biotechnol. 2011;29:191–8.
Galindo-Rodriguez S, Allémann E, Fessi H, Doelker E. Physicochemical parameters associated with nanoparticle formation in the salting-out, emulsification-diffusion, and nanoprecipitation methods. Pharm Res. 2004;21:1428–39.
Rossi S, Sandri G, Caramella C. Buccal delivery systems for peptides: recent advances. Am J Drug Deliv. 2005;3:215–25.
Shojaei AH, Chang RK, Guo X, Burnside BA, Couch RA. Systemic drug delivery via the buccal mucosal route. Pharm Tech:70–81 (2001).
Kumria Rand GG. Emerging trends in insulin delivery: Buccal route. J Diabetol. 2011;2:1–9.
Ozsoy Y, Gungor S, Cevher E. Nasal delivery of high molecular weight drugs. Molecules. 2009;14:3754–79.
Patel VF, Liu F, Brown MB. Advances in oral transmucosal drug delivery. J Control Release. 2011;153:106–16.
Kalluriand H, Banga A. Transdermal delivery of proteins. AAPS PharmSciTech. 2011;12:431–41.
Carstens MG. Opportunities and challenges in vaccine delivery. Eur J Pharm Sci. 2009;36:605–8.
Maurice J, Davey S. State of the world’s vaccines and immunization. http://www.unicef.org/media/files/SOWVI_full_report_english_LR1.pdf (accessed 17/02/2012 2012).
W.H. Organization. World Health Statistics 2011 in WHO Statistical Information System (WHOSIS). http://www.who.int/whosis/whostat/2011/en/index.html (accessed 17/04 2012).
Blank F, Stumbles P, von Garnier C. Opportunities and challenges of the pulmonary route for vaccination. Expet Opin Drug Deliv. 2011;8:547–63.
Holmgren J, Czerkinsky C. Mucosal immunity and vaccines. Nat Med (2005).
Labiris NR, Dolovich MB. Pulmonary drug delivery. Part II: The role of inhalant delivery devices and drug formulations in therapeutic effectiveness of aerosolized medications. Br J Clin Pharmacol. 2003;56:600–12.
Sanders M. Inhalation therapy: an historical review. Prim Care Respir J. 2007;16:71–81.
Mack GS. Pfizer dumps Exubera. Nat Biotech. 2007;25:1331–2.
Onoue S, Hashimoto N, Yamada S. Dry powder inhalation systems for pulmonary delivery of therapeutic peptides and proteins. Expert Opin Ther Pat. 2008;18:429–42.
de Swart RL, LiCalsi C, Quirk AV, van Amerongen G, Nodelman V, Alcock R, et al. Measles vaccination of macaques by dry powder inhalation. Vaccine. 2007;25:1183–90.
Fourie P, Germishuizen W, Wong Y-L, Edwards D. Spray drying TB vaccines for pulmonary administration. Expert Opin Biol Ther. 2008;8:857–63.
LiCalsi C, Maniaci MJ, Christensen T, Phillips E, Ward GH, Witham C. A powder formulation of measles vaccine for aerosol delivery. Vaccine. 2001;19:2629–36.
Amorij JP, Saluja V, Petersen AH, Hinrichs WLJ, Huckriede A, Frijlink HW. 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;25:8707–17.
Thomas C, Rawat A, Hope-Weeks L, Ahsan F. Aerosolized PLA and PLGA Nanoparticles Enhance Humoral. Mucosal and Cytokine Responses to Hepatitis B Vaccine. Mol Pharm. 2010;8:405–15.
Effros RM. Anatomy, development, and physiology of the lungs. GI Motility online. 1: (2006).
Kleinstreuer C, Zhang Z, Li Z. Modeling airflow and particle transport/deposition in pulmonary airways. Respir Physiol Neurobiol. 2008;163:128–38.
Kleinstreuer C, Zhang Z, Donohue JF. Targeted drug-aerosol delivery in the human respiratory system. Annu Rev Biomed Eng. 2008;10:195–220.
Gehr P. Annexe A. Anatomy and morphology of the respiratory tract. Ann ICRP. 1994;24:121–66.
Scheuch G, Kohlhaeufl MJ, Brand P, Siekmeier R. Clinical perspectives on pulmonary systemic and macromolecular delivery. Adv Drug Deliv Rev. 2006;58:996–1008.
Shen X, Lagergård T, Yang Y, Lindblad M, Fredriksson M, Holmgren J. Systemic and Mucosal Immune Responses in Mice after Mucosal Immunization with Group B Streptococcus Type III Capsular Polysaccharide-Cholera Toxin B Subunit Conjugate Vaccine. Infect Immun. 2000;68:5749–55.
Ballester M, Nembrini C, Dhar N, de Titta A, de Piano C, Pasquier M, et al. Nanoparticle conjugation and pulmonary delivery enhance the protective efficacy of Ag85B and CpG against tuberculosis. Vaccine. 2011;29:6959–66.
Muttil P, Pulliam B, Garcia-Contreras L, Fallon J, Wang C, Hickey A, et al. Pulmonary immunization of Guinea Pigs with diphtheria CRM-197 antigen as nanoparticle aggregate dry powders enhance local and systemic immune responses. AAPS J. 2010;12:699–707.
Alpar HO, Somavarapu S, Atuah KN, Bramwell VW. Biodegradable mucoadhesive particulates for nasal and pulmonary antigen and DNA delivery. Adv Drug Deliv Rev. 2005;57:411–30.
Vermaelen K, Pauwels R. Pulmonary Dendritic Cells. Am J Respir Crit Care Med. 2005;172:530–51.
Banchereau J, Steinman RM. Dendritic cells and the control of immunity. Nature. 1998;392:245–52.
Nobelprize.org. The Nobel Prize in Physiology or Medicine 2011. http://www.nobelprize.org/nobel_prizes/medicine/laureates/2011/ (accessed 19 Apr 2012).
Lassila O, Vainio O, Matzinger P. Can B cells turn on virgin T cells? Nature. 1988;334:253–5.
Banchereau J, Briere F, Caux C, Davoust J, Lebecque S, Liu Y-J, et al. Immunobiology of Dendritic Cells. Annu Rev Immunol. 2000;18:767–811.
Guermonprez P, Valladeau J, Zitvogel L, Théry C, Amigorena S. Antigen Presentation and T Cell Stimulation by Dendritic Cells. Annu Rev Immunol. 2002;20:621–67.
Foged C, Sundblad A, Hovgaard L. Targeting Vaccines to Dendritic Cells. Pharm Res. 2002;19:229–38.
Lambrecht BN, Hammad H. Biology of Lung dendritic cells at the origin of asthma. Immunity. 2009;31:412–24.
GeurtsvanKessel CH, Lambrecht BN. Division of labor between dendritic cell subsets of the lung. Mucosal Immunol. 2008;1:442–50.
Lommatzsch M, Bratke K, Bier A, Julius P, Kuepper M, Luttmann W, et al. Airway dendritic cell phenotypes in inflammatory diseases of the human lung. Eur Respir J. 2007;30:878–86.
Ba-Omar T, Al-Riyami B. Microscopic study of human alveolar macrophages. Microsc Microanal. 2008;14:1518–9.
Kiama SG, Cochand L, Karlsson L, Nicod LP, Gehr P. Evaluation of phagocytic activity in human monocyte-derived dendritic cells. J Aerosol Med. 2001;14:289–99.
von Garnier C, Nicod LP. Immunology taught by lung dendritic cells. Swiss Med Wkly. 2009;139:186–92.
Demedts IK, Brusselle GG, Vermaelen KY, Pauwels RA. Identification and characterization of human pulmonary dendritic cells. Am J Respir Cell Mol Biol. 2005;32:177–84.
Gallucci S, Matzinger P. Danger signals: SOS to the immune system. Curr Opin Immunol. 2001;13:114–9.
Copland MJ, Baird MA, Rades T, McKenzie JL, Becker B, Reck F, et al. Liposomal delivery of antigen to human dendritic cells. Vaccine. 2003;21:883–90.
Burgdorf S, Lukacs-Kornek V, Kurts C. The mannose receptor mediates uptake of soluble but not of cell-associated antigen for cross-presentation. J Immunol. 2006;176:6770–6.
Platt CD, Ma JK, Chalouni C, Ebersold M, Bou-Reslan H, Carano RAD, et al. Mature dendritic cells use endocytic receptors to capture and present antigens. Proc Natl Acad Sci. 2010;107:4287–92.
Thornton EE, Looney MR, Bose O, Sen D, Sheppard D, Locksley R, Huang X, Krummel MF. Spatiotemporally separated antigen uptake by alveolar dendritic cells and airway presentation to T cells in the lung. The Journal of Experimental Medicine (2012).
Foged C, Brodin B, Frokjaer S, Sundblad A. Particle size and surface charge affect particle uptake by human dendritic cells in an in vitro model. Int J Pharm. 2005;298:315–22.
Manolova V, Flace A, Bauer M, Schwarz K, Saudan P, Bachmann MF. Nanoparticles target distinct dendritic cell populations according to their size. Eur J Immunol. 2008;38:1404–13.
Reddy ST, Swartz MA, Hubbell JA. Targeting dendritic cells with biomaterials: developing the next generation of vaccines. Trends Immunol. 2006;27:573–9.
Cruz LJ, Tacken PJ, Pots JM, Torensma R, Buschow SI, Figdor CG. Comparison of antibodies and carbohydrates to target vaccines to human dendritic cells via DC-SIGN. Biomaterials. 2012;33:4229–39.
Caminschi I, Maraskovsky E, Heath WR. Targeting dendritic cells in vivo for cancer therapy. Frontiers in Immunology. 3: (2012).
Carrillo-Conde B, Song E-H, Chavez-Santoscoy A, Phanse Y, Ramer-Tait AE, Pohl NLB, et al. Mannose-functionalized “Pathogen-like” polyanhydride nanoparticles target c-type lectin receptors on dendritic cells. Mol Pharm. 2011;8:1877–86.
Geijtenbeek TBH, Gringhuis SI. Signalling through C-type lectin receptors: shaping immune responses. Nat Rev Immunol. 2009;9:465–79.
Sung JC, Pulliam BL, Edwards DA. Nanoparticles for drug delivery to the lungs. Trends Biotechnol. 2007;25:563–70.
Bailey MM, Berkland CJ. Nanoparticle formulations in pulmonary drug delivery. Med Res Rev. 2009;29:196–212.
Smola M, Vandamme T, Sokolowski A. Nanocarriers as pulmonary drug delivery systems to treat and to diagnose respiratory and non respiratory diseases. Int J Nanomedicine. 2008;3:1–19.
Smyth HDC, Smyth HH, Hickey AJ. Macro and Microstructure of the Airways for Drug Delivery in Controlled Pulmonary Drug Delivery, Springer, 2011.
Heffernan MJ, Kasturi SP, Yang SC, Pulendran B, Murthy N. The stimulation of CD8+ T cells by dendritic cells pulsed with polyketal microparticles containing ion-paired protein antigen and poly(inosinic acid)–poly(cytidylic acid). Biomaterials. 2009;30:910–8.
Rice-Ficht AC, Arenas-Gamboa AM, Kahl-McDonagh MM, Ficht TA. Polymeric particles in vaccine delivery. Curr Opin Microbiol. 2010;13:106–12.
Panyam J, Labhasetwar V. Biodegradable nanoparticles for drug and gene delivery to cells and tissue. Adv Drug Deliv Rev. 2003;55:329–47.
Rytting E, Nguyen J, Wang X, Kissel T. Biodegradable polymeric nanocarriers for pulmonary drug delivery. Expet Opin Drug Deliv. 2008;5:629–39.
Kumari A, Yadav SK, Yadav SC. Biodegradable polymeric nanoparticles based drug delivery systems. Colloids Surf B Biointerfaces. 2010;75:1–18.
Bolhassani A, Safaiyan S, Rafati S. Improvement of different vaccine delivery systems for cancer therapy. Mol Cancer. 2011;10:3.
Doria-Rose NA, Haigwood NL. DNA vaccine strategies: candidates for immune modulation and immunization regimens. Methods. 2003;31:207–16.
Bivas-Benita M, van Meijgaarden KE, Franken KLMC, Junginger HE, Borchard G, Ottenhoff THM, et al. Pulmonary delivery of chitosan-DNA nanoparticles enhances the immunogenicity of a DNA vaccine encoding HLA-A*0201-restricted T-cell epitopes of Mycobacterium tuberculosis. Vaccine. 2004;22:1609–15.
Jain JRA. The manufacturing techniques of various drug loaded biodegradable poly(lactide-co-glycolide) (PLGA) devices. Biomaterials. 2000;21:2475–90.
Anderson JM, Shive MS. Biodegradation and biocompatibility of PLA and PLGA microspheres. Adv Drug Deliv Rev. 1997;28:5–24.
Fiore VF, Lofton MC, Roser-Page S, Yang SC, Roman J, Murthy N, et al. Polyketal microparticles for therapeutic delivery to the lung. Biomaterials. 2010;31:810–7.
Muttil P, Prego C, Garcia-Contreras L, Pulliam B, Fallon J, Wang C, et al. Immunization of Guinea Pigs with Novel Hepatitis B Antigen as Nanoparticle Aggregate Powders Administered by the Pulmonary Route. AAPS J. 2010;12:330–7.
Heffernan MJ, Murthy N. Polyketal nanoparticles: a new pH-sensitive biodegradable drug delivery vehicle. Bioconjug Chem. 2005;16:1340–2.
Yang SC, Bhide M, Crispe IN, Pierce RH, Murthy N. Polyketal copolymers: a new acid-sensitive delivery vehicle for treating acute inflammatory diseases. Bioconjug Chem. 2008;19:1164–9.
Pinto Reis C, Neufeld RJ, Ribeiro AJ, Veiga F. Nanoencapsulation I. Methods for preparation of drug-loaded polymeric nanoparticles. Nanomedicine Nanotechnol Biol Med. 2006;2:8–21.
Singh J, Pandit S, Bramwell VW, Alpar HO. Diphtheria toxoid loaded poly-(ε-caprolactone) nanoparticles as mucosal vaccine delivery systems. Methods. 2006;38:96–105.
Mahapatro A, Singh D. Biodegradable nanoparticles are excellent vehicle for site directed in-vivo delivery of drugs and vaccines. J Nanobiotechnology. 2011;9:55.
Dinarvand R, Sepehri N, Manoochehri S, Rouhani H, Atyabi F. Polylactide-co-glycolide nanoparticles for controlled delivery of anticancer agents. Int J Nanomedicine. 2011;6:877–95.
Lee JS, Hwang SJ, Lee DS, Kim SC, Kim DJ. Formation of Poly(ethylene glycol)-Poly(ε-caprolactone) Nanoparticles via Nanoprecipitation. Macromol Res. 2009;17:72–8.
Ranjan AP, Zeglam K, Mukerjee A, Thamake S, Vishwanatha JK. A sustained release formulation of chitosan modified PLCL:poloxamer blend nanoparticles loaded with optical agent for animal imaging. Nanotechnology. 2011;22:1–10.
Allémann E, Gurny R, Doelker E. Preparation of aqueous polymeric nanodispersions by a reversible salting-out process: influence of process parameters on particle size. Int J Pharm. 1992;87:247–53.
Muthu M. Nanoparticles based on PLGA and its co-polymer: An overview, 2009.
Konan YN, Gurny R, Allémann E. Preparation and characterization of sterile and freeze-dried sub-200 nm nanoparticles. Int J Pharm. 2002;233:239–52.
Soppimath KS, Aminabhavi TM, Kulkarni AR, Rudzinski WE. Biodegradable polymeric nanoparticles as drug delivery devices. J Control Release. 2001;70:1–20.
Bivas-Benita M, Romeijn S, Junginger HE, Borchard G. PLGA–PEI nanoparticles for gene delivery to pulmonary epithelium. Eur J Pharm Biopharm. 2004;58:1–6.
Bivas-Benita M, Lin MY, Bal SM, van Meijgaarden KE, Franken KLMC, Friggen AH, et al. Pulmonary delivery of DNA encoding Mycobacterium tuberculosis latency antigen Rv1733c associated to PLGA–PEI nanoparticles enhances T cell responses in a DNA prime/protein boost vaccination regimen in mice. Vaccine. 2009;27:4010–7.
Pulliam B, Sung JC, Edwards DA. Design of nanoparticle-based dry powder pulmonary vaccines. Expet Opin Drug Deliv. 2007;4:651–63.
Allen TM, Cullis PR. Drug delivery systems: entering the mainstream. Science. 2004;303:1818–22.
Petrovsky N, Aguilar JC. Vaccine adjuvants: current state and future trends. Immunol Cell Biol. 2004;82:488–96.
O’Hagan DT, MacKichan ML, Singh M. Recent developments in adjuvants for vaccines against infectious diseases. Biomol Eng. 2001;18:69–85.
Wilson-Welder JH, Torres MP, Kipper MJ, Mallapragada SK, Wannemuehler MJ, Narasimhan B. Vaccine adjuvants: current challenges and future approaches. J Pharm Sci. 2009;98:1278–316.
Amorij J-P, Kersten GFA, Saluja V, Tonnis WF, Hinrichs WLJ, Slütter B, Bal SM, Bouwstra JA, Huckriede A, Jiskoot W. Towards tailored vaccine delivery: Needs, challenges and perspectives. Journal of Controlled Release.
Sekaly R-P. The failed HIV Merck vaccine study: a step back or a launching point for future vaccine development? J Exp Med. 2008;205:7–12.
Lewis DJM, Huo Z, Barnett S, Kromann I, Giemza R, Galiza E, 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.
Vajdy M. Immunomodulatory properties of vitamins, flavonoids and plant oils and their potential as vaccine adjuvants and delivery systems. Expert Opin Biol Ther. 2011;11:1501–13.
Skountzou I, Quan F-S, Jacob J, Compans RW, Kang S-M. Transcutaneous immunization with inactivated influenza virus induces protective immune responses. Vaccine. 2006;24:6110–9.
Nottenburg C. Types of adjuvants: In Introduction to Adjuvant Patent Landscape. http://www.patentlens.net/daisy/adjuvants/Background/Adjuvant_types.html (accessed 14th April 2012).
Wee JLK, Scheerlinck JPY, Snibson KJ, Edwards S, Pearse M, Quinn C, et al. Pulmonary delivery of ISCOMATRIX influenza vaccine induces both systemic and mucosal immunity with antigen dose sparing. Mucosal Immunol. 2008;1:489–96.
Vauthier C, Bouchemal K. Methods for the preparation and manufacture of polymeric nanoparticles. Pharm Res. 2009;26:1025–58.
LiCalsi C, Christensen T, Bennett JV, Phillips E, Witham C. Dry powder inhalation as a potential delivery method for vaccines. Vaccine. 1999;17:1796–803.
Mansour HM, Rhee Y, Wu X. Nanomedicine in pulmonary delivery. Int J Nanomedicine. 2009;4:299–319.
Pilcer G, Amighi K. Formulation strategy and use of excipients in pulmonary drug delivery. Int J Pharm. 2010;392:1–19.
Abdelwahed W, Degobert G, Stainmesse S, Fessi H. Freeze-drying of nanoparticles: formulation, process and storage considerations. Adv Drug Deliv Rev. 2006;58:1688–713.
Anhorn MG, Mahler H-C, Langer K. Freeze drying of human serum albumin (HSA) nanoparticles with different excipients. Int J Pharm. 2008;363:162–9.
Hirsjärvi S, Peltonen L, Hirvonen J. Effect of sugars, surfactant, and tangential flow filtration on the freeze-drying of Poly(lactic acid) nanoparticles. AAPS PharmSciTech. 2009;10:488–94.
Malcolmson RJ, Embleton JK. Dry powder formulations for pulmonary delivery. Pharmaceut Sci Tech Today. 1998;1:394–8.
Peltonen L, Valo H, Kolakovic R, Laaksonen T, Hirvonen J. Electrospraying, spray drying and related techniques for production and formulation of drug nanoparticles. Expet Opin Drug Deliv. 2010;7:705–19.
Heng D, Lee SH, Ng WK, Tan RB. The nano spray dryer B-90. Expet Opin Drug Deliv. 2011;8:965–72.
Amorij JP, Huckriede A, Wilschut J, Frijlink H, Hinrichs W. Development of stable influenza vaccine powder formulations: challenges and possibilities. Pharm Res. 2008;25:1256–73.
Shoyele SA, Cawthorne S. Particle engineering techniques for inhaled biopharmaceuticals. Adv Drug Deliv Rev. 2006;58:1009–29.
Al-fagih IM, Alanazi FK, Hutcheon GA, Saleem IY. Recent advances using supercritical fluid techniques for pulmonary administration of macromolecules via dry powder formulations. Drug Deliv Lett. 2011;1:128–34.
Okamoto H, Danjo K. Application of supercritical fluid to preparation of powders of high-molecular weight drugs for inhalation. Adv Drug Deliv Rev. 2008;60:433–46.
Byrappa K, Ohara S, Adschiri T. Nanoparticles synthesis using supercritical fluid technology – towards biomedical applications. Adv Drug Deliv Rev. 2008;60:299–327.
Kenji M. Biodegradable particle formation for drug and gene delivery using supercritical fluid and dense gas. Adv Drug Deliv Rev. 2008;60:411–32.
Pasquali I, Bettini R, Giordano F. Supercritical fluid technologies: an innovative approach for manipulating the solid-state of pharmaceuticals. Adv Drug Deliv Rev. 2008;60:399–410.
Amidi M, Pellikaan HC, Hirschberg H, de Boer AH, Crommelin DJA, Hennink WE, et al. Diphtheria toxoid-containing microparticulate powder formulations for pulmonary vaccination: preparation, characterization and evaluation in guinea pigs. Vaccine. 2007;25:6818–29.
W.H. Organization. Pneumonia. http://www.who.int/mediacentre/factsheets/fs331/en/index.html (accessed 17/04 2012).
Ghotbi Z, Haddadi A, Hamdy S, Hung RW, Samuel J, Lavasanifar A. Active targeting of dendritic cells with mannan-decorated PLGA nanoparticles. J Drug Target. 2011;19:281–92.
Bandyopadhyay A, Fine RL, Demento S, Bockenstedt LK, Fahmy TM. The impact of nanoparticle ligand density on dendritic-cell targeted vaccines. Biomaterials. 2011;32:3094–105.
Cruz LJ, Tacken PJ, Fokkink R, Joosten B, Stuart MC, Albericio F, et al. Targeted PLGA nano- but not microparticles specifically deliver antigen to human dendritic cells via DC-SIGN in vitro. J Control Release. 2010;144:118–26.
Kwon YJ, James E, Shastri N, Fréchet JMJ. In vivo targeting of dendritic cells for activation of cellular immunity using vaccine carriers based on pH-responsive microparticles. Proc Natl Acad Sci U S A. 2005;102:18264–8.
Kempf M, Mandal B, Jilek S, Thiele L, Vörös J, Textor M, et al. Improved stimulation of human dendritic cells by receptor engagement with surface-modified microparticles. J Drug Target. 2003;11:11–8.
Sheng K-C, Kalkanidis M, Pouniotis DS, Esparon S, Tang CK, Apostolopoulos V, et al. Delivery of antigen using a novel mannosylated dendrimer potentiates immunogenicity in vitro and in vivo. Eur J Immunol. 2008;38:424–36.
White KL, Rades T, Furneaux RH, Tyler PC, Hook S. Mannosylated liposomes as antigen delivery vehicles for targeting to dendritic cells. J Pharm Pharmacol. 2006;58:729–37.
Jain S, Vyas SP. Mannosylated niosomes as adjuvant-carrier system for oral mucosal immunization. J Liposome Res. 2006;16:331–45.
Hao J, Kwissa M, Pulendran B, Murthy N. Peptide crosslinked micelles: a new strategy for the design and synthesis of peptide vaccines. Int J Nanomedicine. 2006;1:97–103.
Lu D, Hickey AJ. Liposomal dry powders as aerosols for pulmonary delivery of proteins. AAPS PharmSciTech. 2005;6:E641–8.
Barnier Quer C, Robson Marsden H, Romeijn S, Zope H, Kros A, Jiskoot W. Polymersomes enhance the immunogenicity of influenza subunit vaccine. Polym Chem. 2011;2:1482–5.
Matinkhoo S, Lynch KH, Dennis JJ, Finlay WH, Vehring R. Spray-dried respirable powders containing bacteriophages for the treatment of pulmonary infections. J Pharm Sci. 2011;100:5197–205.
Saluja V, Amorij JP, Kapteyn JC, de Boer AH, Frijlink HW, Hinrichs WLJ. A comparison between spray drying and spray freeze drying to produce an influenza subunit vaccine powder for inhalation. J Control Release. 2010;144:127–33.
Jin TH, Tsao E, Goudsmit J, Dheenadhayalan V, Sadoff J. Stabilizing formulations for inhalable powders of an adenovirus 35-vectored tuberculosis (TB) vaccine (AERAS-402). Vaccine. 2010;28:4369–75.
Garcia-Contreras L, Wong Y-L, Muttil P, Padilla D, Sadoff J, DeRousse J, et al. Immunization by a bacterial aerosol. Proc Natl Acad Sci. 2008;105:4656–60.
Lu D, Garcia-Contreras L, Muttil P, Padilla D, Xu D, Liu J, et al. Pulmonary Immunization Using Antigen 85-B Polymeric Microparticles to Boost Tuberculosis Immunity. AAPS J. 2010;12:338–47.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Kunda, N.K., Somavarapu, S., Gordon, S.B. et al. Nanocarriers Targeting Dendritic Cells for Pulmonary Vaccine Delivery. Pharm Res 30, 325–341 (2013). https://doi.org/10.1007/s11095-012-0891-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11095-012-0891-5