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Review

Nanocarriers: a Versatile Approach for Mucosal Vaccine Delivery

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Pages 231-245 | Published online: 18 Feb 2015

References

  • Wang J Thorson L Stokes RW Santosuosso M Huygen K Zganiacz A et al. Single mucosal, but not parenteral, immunization with recombinant adenoviral-based vaccine provides potent protection from pulmonary tuberculosis. J. Immunol.173 (10), 6357–6365 (2004).
  • Neutra MR Kozlowski PA . Mucosal vaccines: the promise and the challenge. Nat. Rev. Immunol.6 (2), 148–158 (2006).
  • Chadwick S Kriegel C Amiji M . Nanotechnology solutions for mucosal immunization. Adv. Drug Del. Rev.62 (4–5), 394–407 (2010).
  • Hobson P Barnfield C Barnes A Klavinskis LS . Mucosal immunization with DNA vaccines. Methods31 (3), 217–224 (2003).
  • Csaba N Garcia-Fuentes M Alonso MJ . Nanoparticles for nasal vaccination. Adv. Drug Deliv. Rev.61 (2), 140–157 (2009).
  • Jain S Khomane K Jain AK Dani P . Nanocarriers for transmucosal vaccine delivery. Current Nanosci.7, 160–177 (2011).
  • Amorij JP Saluja V Petersen AH Hinrichs WL Huckriede JA 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. Vaccine25 (52), 8707–8717 (2007).
  • Vyas SP Gupta PN . Implication of nanoparticles/microparticles in mucosal vaccine delivery. Expert Rev. Vaccines6 (3), 401–418 (2007).
  • Corr S Gahan CCGM Hill C . M-cells: origin, morphology and role in mucosal immunity and microbial pathogenesis. FEMS Immunol. Med. Microbiol.52 (1), 2–12 (2008).
  • Lawson LB Norton EB Clements JD . Defending the mucosa: adjuvant and carrier formulations for mucosal immunity. Currt. Opinion Immunol.23 (3), 414–420 (2011).
  • Cesta MF . Normal structure, function, and histology of mucosa-associated lymphoid tissue. Toxicol. Pathol.34 (5), 599–608 (2006).
  • Kunisawa J Nochi T Kiyono H . Immunological commonalities and distinctions between airway and digestive immunity. Trends Immunol.29 (11), 505–513 (2008).
  • Chen W Patel GB Yan H Zhang J . Recent advances in the development of novel mucosal adjuvants and antigen delivery systems. Hum. Vaccin.6 (9), 781–794 (2010).
  • Mowat AM Millington OR Chirdo FG . Anatomical and cellular basis of immunity and tolerance in the intestine. J. Pediatr. Gastroenterol. Nutr.39 (Suppl.3), s723–s724 (2004).
  • Lycke N . Recent progress in mucosal vaccine development: potential and limitations. Nature Rev. Immunol.12 (8), 592–605 (2012).
  • Czerkinsky C Holmgren J . Mucosal delivery routes for optimal immunization: targeting immunity to the right tissues. Curr. Top. Microbiol. Immunol.354, 1–18 (2010).
  • Levine MM . Immunogenicity and efficacy of oral vaccines in developing countries: lessons from a live cholera vaccine. BMC Biol. doi:10.1186/1741-7007-8-129 (2010) ( Epub).
  • Kasturi SP Skountzou I Albrecht RA Koutsonanos D Hua TH Nakaya HI et al. Programming the magnitude and persistence of antibody responses with innate immunity. Nature470 (7335), 543–547 (2011).
  • Laroui H Wilson DS Dalmasso G Salaita K Murthy N Sitaraman SV et al. Nanomedicine in GI. Am. J. Physiol. Gastrointest. Liver Physiol.300 (3), g371–g383 (2011).
  • Cario E . Nanotechnology-based drug delivery in mucosal immune diseases: hype or hope?Mucosal Immuno.5, 2–3 (2012).
  • Farokhzad OC Langer R . Impact of nanotechnology on drug delivery. ACS Nano.3 (1), 16–20 (2009).
  • Gupta PN Mahor S Rawat A Khatri K Goyal A Vyas SP . Lectin anchored stabilized biodegradable nanoparticles for oral immunization 1. Development and in vitro evaluation. Int. J. Pharm.318 (1–2), 163–173 (2006).
  • Shahiwala A Vyas TK Amiji MM . Nanocarriers for systemic and mucosal vaccine delivery. Recent Pat. Drug Deliv. Formul.1 (1), 1–9 (2007).
  • Csaba N Garcia-Fuentes M Alonso MJ . The performance of nanocarriers for transmucosal drug delivery. Expert Opin. Drug Deliv.3 (4), 463–478 (2006).
  • Stuart LM Ezekowitz RAB . Phagocytosis elegant complexity. Immunity22 (5), 539–550 (2005).
  • Rajapaksa TE Lo DD . Microencapsulation of vaccine antigens and adjuvants for mucosal targeting. Curr. Immunol. Rev.6 (1), 29–37 (2010).
  • Hartikka J Bozoukova V Ferrari M Sukhu L Enas J Sawdey M et al. Vaxfectin enhances the humoral immune response to plasmid DNA-encoded antigens. Vaccine19 (15–16), 1911–1923 (2001).
  • Thanou M Verhoef JC Junginger HE . Chitosan and its derivatives as intestinal absorption enhancers. Adv. Drug Deliv. Rev.50 (Suppl.1), s91–s101 (2001).
  • Jabbal-Gill I Lin W Kistner O Davis SS Illum L . Polymeric lamellar substrate particles for intranasal vaccination. Adv. Drug Deliv. Rev.51 (1–3), 97–111 (2001).
  • Hejazi R Amiji M . Chitosan-based gastrointestinal delivery systems. J. Control Release89, 151–165 (2003).
  • Ye T Yue Y Fan X Dong C Xu W Xiong S . M cell-targeting strategy facilitates mucosal immune response and enhances protection against CVB3-induced viral myocarditis elicited by chitosan DNA vaccine. Vaccine32 (35), 4457–4465 (2014).
  • Vila A Sanchez A Evora C Soriano I Jato JLV Alonso MJ . PEG-PLA nanoparticles as carriers for nasal vaccine delivery. J. Aerosol Med.17, 174–185 (2004).
  • Primard C Poecheim J Heuking S Sublet E Esmaeili F Gerrit Borchard . Multifunctional PLGA-based nanoparticles encapsulating simultaneously hydrophilic antigen and hydrophobic immunomodulator for mucosal immunization. Mol. Pharm.10 (8), 2996–3004 (2013).
  • Mangal S Pawar D Agrawal U Jain AK Vyas SP . Evaluation of mucoadhesive carrier adjuvant: toward an oral anthrax vaccine. Artif. Cells Nanomed. Biotechnol.42 (1), 47–57 (2014).
  • Mishra N Khatri K Gupta M Vyas SP . Development and characterization of LTA-appended chitosan nanoparticles for mucosal immunization against hepatitis B. Artif. Cells Nanomed. Biotechnol.42 (4), 245–255 (2014).
  • Flanary S Hoffman AS Stayton PS . Antigen delivery with poly(propylacrylic acid) conjugation enhances MHC-1 presentation and T-cell activation. Bioconjug. Chem.20 (2), 241–248 (2009).
  • Hubbell JA Thomas SN Swartz MA . Materials engineering for immunomodulation. Nature462 (7272), 449–460 (2009).
  • Watson Douglas S Aaron N Huang EL . Design considerations for liposomal vaccines: Influence of formulation parameters on antibody and cell-mediated immune responses to liposome associated antigens. Vaccine30 (13), 2256–2272 (2012).
  • Nordly P Madsen HB Nielsen HM Foged C . Status and future prospects of lipid-based particulate delivery systems as vaccine adjuvants and their combination with immunostimulators. Expert Opin. Drug Deliv.6 (7), 657–672 (2009).
  • Zhou F Neutra MR . Antigen delivery to mucosa-associated lymphoid tissues using liposomes as a carrier. Biosci. Rep.22 (2), 355–369 (2002).
  • Espuelas S Roth A Thumann C et al. Effect of synthetic lipopeptides formulated in liposomes on the maturation of human dendritic cells. Mol. Immunol.42 (6), 721–729 (2005).
  • Heurtault B Frisch B Pons F . Liposomes as delivery systems for nasal vaccination: strategies and outcomes. Expert Opin. Drug Deliv.7 (7), 829–844 (2010).
  • Gupta PN Vyas SP . Investigation of lectinized liposomes as M-cell targeted carrier-adjuvant for mucosal immunization. Colloids Surf. B. Biointerfaces82 (1), 118–125 (2011).
  • Tiwari S Agrawal GP Vyas SP . Molecular basis of the mucosal immune system: from fundamental concepts to advances in liposome-based vaccines. Nanomedicine (Lond).5 (10), 1617–1640 (2010).
  • Tiwari S Verma SK Agrawal GP Vyas SP . Viral protein complexed liposomes for intranasal delivery of hepatitis B surface antigen. Inter. J. Pharma.413, 211–219 (2011).
  • Zhuang Y Ma Y Wang C Hai L Yan C Zhang Y et al. PEGylated cationic liposomes robustly augment vaccine-induced immune responses: role of lymphatic trafficking and biodistribution. J. Control Release159 (1), 135–142 (2012).
  • Senchi KM Hasegawa S Kimura H Ryo H . Development of oligomannose-coated liposome-based nasal vaccine against human parainfluenza virus type 3. Front Microbiol.26 (4), 346 (2013).
  • Henderson A Propst K Kedl R Dow S . Mucosal immunization with liposome-nucleic acid adjuvants generates effective humoral and cellular immunity. Vaccine29 (32), 5304–5312 (2011).
  • Wang HW Jiang PL Lin S Lin HJ Liang Ou K Deng W et al. Application of galactose-modified liposomes as a potent antigen presenting cell targeted carrier for intranasal immunization. Acta Biomater.9 (3), 5681–5688 (2013).
  • Watarai S Iwase T Tajima T Yuba E Kono K Sekiya Y . Application of pH-sensitive fusogenic polymer-modified liposomes for development of mucosal vaccines. Vet. Immunol. Immunopathol.158 (1–2), 62–72 (2014).
  • de Veer M Neeland M Burke M et al. Cell recruitment and antigen trafficking in afferent lymph after injection of antigen and poly(I:C) containing liposomes, in aqueous or oil-based formulations. Vaccine31 (7), 1012–1018 (2013).
  • Herzog C Hartmann K Kunzi V Kursteiner O Mischler R Lazar H et al. Eleven years of Inflexal V-a virosomal adjuvanted influenza vaccine. Vaccine27 (33), 4381–4387 (2009).
  • Kursteiner O Mischler R Metcalfe IC . Inflexal V a trivalent virosome subunit influenza vaccine: production. Vaccine20 (Suppl.5), b17–b23 (2002).
  • Bovier PA . Epaxal: a virosomal vaccine to prevent hepatitis A infection. Expert Rev. Vaccines7 (8), 1141–1150 (2008).
  • Usonis V Bakasenas V Valentelis R Katiliene G Vidzeniene D Herzog C . Antibody titres after primary and booster vaccination of infants and young children with a virosomal hepatitis A vaccine (Epaxal). Vaccine21 (31), 4588–4592 (2003).
  • Butts C Murray N Maksymiuk A Goss G Marshall E Soulieres D et al. Randomized phase IIB trial of BLP25 liposome vaccine in stage IIIB and IV non-small-cell lung cancer. J. Clin. Oncol.23 (27), 6674–6681 (2005).
  • North S Butts C . Vaccination with BLP25 liposome vaccine to treat non-small cell lung and prostate cancers. Expert Rev. Vaccines4 (3), 249–257 (2005).
  • Regules JA Cummings JF Ockenhouse CF . The RTS, S vaccine candidate for malaria. Expert Rev. Vaccines10 (5), 589–599 (2011).
  • Agnandji ST Asante KP Lyimo J Vekemans J Soulanoudjingar SS Owusu R et al. Evaluation of the safety and immunogenicity of the RTS,S/AS01E malaria candidate vaccine when integrated in the expanded program of immunization. J. Infect. Dis.202 (7), 1076–1087 (2010).
  • Schoenen H Bodendorfer B Hitchens K Manzanero S Werninghaus K Nimmerjahn F et al. Cutting edge: mincle is essential for recognition and adjuvanticity of the mycobacterial cord factor and its synthetic analog trehalose-dibehenate. J. Immunol.184 (6), 2756–2760 (2010).
  • Even-Or O Joseph A Itskovitz-Cooper N Samira S Rochlin E Eliyahu H et al. A new intranasal influenza vaccine based on a novel polycationic lipid-ceramide carbamoyl-spermine (CCS). II. Studies in mice and ferrets and mechanism of adjuvanticity. Vaccine29 (13), 2474–2486 (2011).
  • Even-Or O Samira S Rochlin E Balasingam S Mann AJ Lambkin-Williams R et al. Immunogenicity, protective efficacy and mechanism of novel CCS adjuvanted influenza vaccine. Vaccine28 (39), 6527–6541 (2010).
  • Lay M Callejo B Chang S Hong DK Lewis DB Carroll TD et al. Cationic lipid/DNA complexes (JVRS-100) combined with influenza vaccine (Fluzone) increases antibody response, cellular immunity, and antigenically drifted protection. Vaccine27 (29), 3811–3820 (2009).
  • Sullivan SM Doukas J Hartikka J Smith L Rolland A . Vaxfectin: a versatile adjuvant for plasmid DNA- and protein-based vaccines. Expert Opin. Drug Deliv.7 (12), 1433–1446 (2010).
  • Jain S Singh P Mishra V Vyas SP . Mannosylated niosomes as adjuvant–carrier system for oral genetic immunization against hepatitis B. Immunol. Lett.101 (1), 41–49 (2005).
  • Wilkhu JS McNeil SE Anderson DE Perrie Y . Characterization and optimization of bilosomes for oral vaccine delivery. J. Drug Target.21 (3), 291–299 (2013).
  • Shilpa S Srinivasan BP Chauhan M . Niosomes as vesicular carriers for delivery of proteins and biologicals. Inter. J. Drug Deliv.3 (1), 14–24 (2011).
  • Cortesi R Ravani L Rinaldi F Marconi P Drechsler M Manservigi M et al. Intranasal immunization in mice with non-ionic surfactants vesicles containing HSV immunogens: a preliminary study as possible vaccine against genital herpes. Int. J. Pharm.440 (2), 229–237 (2013).
  • Pardakhty A Shakibaie M Daneshvar H Khamesipour A Mohammadi-Khorsand T Forootanfar H . Preparation and evaluation of niosomes containing autoclaved Leishmania major: a preliminary study. J. Microencapsul.29 (3), 219–224 (2012).
  • Jain S Vyas SP . Mannosylated niosomes as adjuvant-carrier system for oral mucosal immunization. J. Liposome Res.16 (4), 331–345 (2006).
  • Katare R Gupta PN Mahor S et al. Development of polysaccharide-capped niosomes for oral immunization of tetanus toxoid. J. Drug Deliv. Sci. Technol.16 (3), 167–172 (2006).
  • Mann JFS Ferro VA Mullen AB Tetley L Mullen M Carter KC Alexander J Stimson WH . Optimisation of a lipid based oral delivery system containing A/Panama influenza haemagglutinin. Vaccine22 (19), 2425–2429 (2004).
  • Mann JFS Scales HE Shakir E Alexander J Cartera KC Mullen AB et al. Oral delivery of tetanus toxoid using vesicles containing bile salts (bilosomes) induces significant systemic and mucosal immunity. Methods38 (2), 90–95 (2006).
  • Conacher M Alexander J Brewer J . Oral immunisation with peptide and protein antigens by formulation in lipid vesicles incorporating bile salts (bilosomes). Vaccine19 (20–22), 2965–2974 (2001).
  • Arora D Khurana B Murugesan SM Vyas SP . Oral immunization against hepatitis B virus using mannosylated bilosomes. Inter. J. Recent Adv. Pharma. Res.1, 45–51 (2011).
  • Premanand B Prabakaran M Kiener TK Kwang J . Recombinant baculovirus associated with bilosomes as an oral vaccine candidate against HEV71 infection in mice. PLoS ONE8 (2), e55536 (2013).
  • Jain S Harde H Indulkar A Agrawal AK . Improved stability and immunological potential of tetanus toxoid containing surface engineered bilosomes following oral administration. Nanomedicine10 (2), 431–440 (2014).
  • Wilschut J . Influenza vaccines: the virosome concept. Immunol. Lett.122 (2), 118–121 (2009).
  • Huckriede A Bungener L Stegmann T Daemen T Medema J Palache AM Wilschut J . The virosome concept for influenza vaccines. Vaccine23 (Supple.1), s26–s38 (2005).
  • Durrer P Glück U Spyr C Lang AB Zurbriggen R Herzog C et al. Mucosal antibody response induced with a nasal virosome-based influenza vaccine. Vaccine21 (27–30), 4328–4334 (2003).
  • Lambkin R Oxford JS Bossuyt S Mann A Metcalfe IC Herzog C et al. Strong local and systemic protective immunity induced in the ferret model by an intranasal virosome-formulated influenza subunit vaccine. Vaccine22 (31–32), 4390–4396 (2004).
  • Morgane B Daniela T Drillet AS Alfsen A Ganor Y Roger MG et al. Immunization with HIV-1 gp41 subunit virosomes induces mucosal antibodies protecting nonhuman primates against vaginal HIV. Immunity34 (2), 269–280 (2011).
  • Liu J Gong T Fu H Wang C Wang X Chen Q Zhang Q He Q Zhang Z . Solid lipid nanoparticles for pulmonary delivery of insulin. Int. J. Pharm.356 (1–2), 333–344 (2006).
  • Pedersen N Hansen S Heydenreich AV Kristensen HG Poulsen HS . Solid lipid nanoparticles can effectively bind DNA, streptavidin and biotinylated ligands. Eur. J. Pharm. Biopharm.62 (2), 155–162 (2006).
  • Zhang N Ping Q Huang G Hu W Cheng Y Han X . Lectin-modified solid lipid nanoparticles as carriers for oral administration of insulin. Int. J. Pharm.327 (1–2), 153–159 (2006).
  • Saraf S Mishra D Asthana A Jain R Singh S Jain NK . Lipid microparticles for mucosal immunization against hepatitis B. Vaccine24 (1), 45–56 (2006).
  • Pushechnikov A Jalisatgi AA Hawthorne MF . Dendritic closomers: novel spherical hybrid dendrimers. Chem. Commun (Camb).49 (34), 3579–3581 (2013).
  • Misumi S Masuyama M Takamune N Nakayama D Mitsumata R Matsumoto H Urata N Takahashi Y Muneoka A Sukamoto T Fukuzaki K Shoji S . Targeted delivery of immunogen to primate m cells with tetragalloyl lysine dendrimer. J. Immunol.182 (10), 6061–6070 (2009).
  • Solans C Izquierdo P Nolla J Azemar N Garcia-Celma MJ . Nano-emulsions. Curr. Opin. Colloid Interface Sci.10 (3–4), 102–110 (2005).
  • Muller RH Mader K Gohla S . Solid lipid nanoparticles for controlled drug delivery–a review of the state of the art. Eur. J. Pharm. Biopharm.50 (1), 161–177 (2000).
  • Baker JR Bielinska A Landers J Janczak K Cao P . Enhanced systemic and mucosal immune responses in mice immunized with recombinant Bacillus anthracis protective antigen (rPA) using a novel nanoemulsion adjuvant. J. Allergy Clin. Immunol.113 (2), 292–292 (2004).
  • Makidon PE Bielinska AU Nigavekar SS Janczak KW Knowlton J . Pre-clinical evaluation of a novel nanoemulsion-based hepatitis B mucosal vaccine. PLoS ONE3 (8), e2954 (2008).

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