416
Views
26
CrossRef citations to date
0
Altmetric
Special Report

Cationic liposomal vaccine adjuvants in animal challenge models: overview and current clinical status

, &
Pages 561-577 | Published online: 09 Jan 2014

References

  • Gall D. The adjuvant activity of aliphatic nitrogenous bases. Immunology 11(4), 369–386 (1966).
  • Veronesi R, Corrêa A, Alterio D. Single dose immunization against tetanus. Promising results in human trials. Rev. Inst. Med. Trop. Sao Paulo 12(1), 46–54 (1970).
  • Stanfield JP, Gall D, Bracken PM. Single-dose antenatal tetanus immunisation. Lancet 1(7797), 215–219 (1973).
  • Allison AG, Gregoriadis G. Liposomes as immunological adjuvants. Nature 252(5480), 252 (1974).
  • Latif N, Bachhawat BK. The effect of surface charges of liposomes in immunopotentiation. Biosci. Rep. 4(2), 99–107 (1984).
  • Christensen D, Korsholm KS, Andersen P, Agger EM. Cationic liposomes as vaccine adjuvants. Expert Rev. Vaccines 10(4), 513–521 (2011).
  • Tanaka T, Legat A, Adam E et al. DiC14-amidine cationic liposomes stimulate myeloid dendritic cells through Toll-like receptor 4. Eur. J. Immunol. 38(5), 1351–1357 (2008).
  • Foged C, Arigita C, Sundblad A, Jiskoot W, Storm G, Frokjaer S. Interaction of dendritic cells with antigen-containing liposomes: effect of bilayer composition. Vaccine 22(15-16), 1903–1913 (2004).
  • Korsholm KS, Agger EM, Foged C et al. The adjuvant mechanism of cationic dimethyldioctadecylammonium liposomes. Immunology 121(2), 216–226 (2007).
  • Maestrelli F, González-Rodríguez ML, Rabasco AM, Mura P. Effect of preparation technique on the properties of liposomes encapsulating ketoprofen–cyclodextrin complexes aimed for transdermal delivery. Int. J. Pharm. 312(1–2), 53–60 (2006).
  • McNeil SE, Rosenkrands I, Agger EM, Andersen P, Perrie Y. Subunit vaccines: distearoylphosphatidylcholine-based liposomes entrapping antigen offer a neutral alternative to dimethyldioctadecylammonium-based cationic liposomes as an adjuvant delivery system. J. Pharm. Sci. 100(5), 1856–1865 (2011).
  • Kirby DJ, Rosenkrands I, Agger EM, Andersen P, Coombes AG, Perrie Y. Liposomes act as stronger sub-unit vaccine adjuvants when compared to microspheres. J. Drug Target. 16(7), 543–554 (2008).
  • Nordly P, Rose F, Christensen D et al. Immunity by formulation design: induction of high CD8+ T-cell responses by poly(I:C) incorporated into the CAF01 adjuvant via a double emulsion method. J. Control. Release 150(3), 307–317 (2011).
  • Chen W, Huang L. Induction of cytotoxic T-lymphocytes and antitumor activity by a liposomal lipopeptide vaccine. Mol. Pharm. 5(3), 464–471 (2008).
  • Henriksen-Lacey M, Christensen D, Bramwell VW et al. Liposomal cationic charge and antigen adsorption are important properties for the efficient deposition of antigen at the injection site and ability of the vaccine to induce a CMI response. J. Control. Release 145(2), 102–108 (2010).
  • Henriksen-Lacey M, Bramwell VW, Christensen D, Agger EM, Andersen P, Perrie Y. Liposomes based on dimethyldioctadecylammonium promote a depot effect and enhance immunogenicity of soluble antigen. J. Control. Release 142(2), 180–186 (2010).
  • Henriksen-Lacey M, Christensen D, Bramwell VW et al. Comparison of the depot effect and immunogenicity of liposomes based on dimethyldioctadecylammonium (DDA), 3b-[N-(N´,N´-dimethylaminoethane)carbomyl] cholesterol (DC-Chol), and 1,2-dioleoyl-3-trimethylammonium propane (DOTAP): prolonged liposome retention mediates stronger Th1 responses. Mol. Pharm. 8(1), 153–161 (2011).
  • Kaur R, Bramwell VW, Kirby DJ, Perrie Y. Pegylation of DDA:TDB liposomal adjuvants reduces the vaccine depot effect and alters the Th1/Th2 immune responses. J. Control. Release 158(1), 72–77 (2012).
  • Tamaddon AM, Shirazi FH, Moghimi HR. Modeling cytoplasmic release of encapsulated oligonucleotides from cationic liposomes. Int. J. Pharm. 336(1), 174–182 (2007).
  • Zelphati O, Szoka FC Jr. Intracellular distribution and mechanism of delivery of oligonucleotides mediated by cationic lipids. Pharm. Res. 13(9), 1367–1372 (1996).
  • Okada N, Saito T, Mori K et al. Effects of lipofectin-antigen complexes on major histocompatibility complex class I-restricted antigen presentation pathway in murine dendritic cells and on dendritic cell maturation. Biochim. Biophys. Acta 1527(3), 97–101 (2001).
  • Hui SW, Langner M, Zhao YL, Ross P, Hurley E, Chan K. The role of helper lipids in cationic liposome-mediated gene transfer. Biophys. J. 71(2), 590–599 (1996).
  • Friend DS, Papahadjopoulos D, Debs RJ. Endocytosis and intracellular processing accompanying transfection mediated by cationic liposomes. Biochim. Biophys. Acta 1278(1), 41–50 (1996).
  • Zuhorn IS, Hoekstra D. On the mechanism of cationic amphiphile-mediated transfection. To fuse or not to fuse: is that the question? J. Membr. Biol. 189(3), 167–179 (2002).
  • Zaks K, Jordan M, Guth A et al. Efficient immunization and cross-priming by vaccine adjuvants containing TLR3 or TLR9 agonists complexed to cationic liposomes. J. Immunol. 176(12), 7335–7345 (2006).
  • Hansen J, Lindenstrøm T, Lindberg-Levin J, Aagaard C, Andersen P, Agger EM. CAF05: cationic liposomes that incorporate synthetic cord factor and poly(I:C) induce CTL immunity and reduce tumor burden in mice. Cancer Immunol. Immunother. doi:10.1007/s00262-011-1156-6 (2011) (Epub ahead of print).
  • Bennett MJ, Nantz MH, Balasubramaniam RP, Gruenert DC, Malone RW. Cholesterol enhances cationic liposome-mediated DNA transfection of human respiratory epithelial cells. Biosci. Rep. 15(1), 47–53 (1995).
  • Perrie Y, Frederik PM, Gregoriadis G. Liposome-mediated DNA vaccination: the effect of vesicle composition. Vaccine 19(23-24), 3301–3310 (2001).
  • Lonez C, Lensink MF, Kleiren E, Vanderwinden JM, Ruysschaert JM, Vandenbranden M. Fusogenic activity of cationic lipids and lipid shape distribution. Cell. Mol. Life Sci. 67(3), 483–494 (2010).
  • Ramesh R. Nanoparticle-mediated gene delivery to the lung. Methods Mol. Biol. 433, 301–331 (2008).
  • Ramesh R, Saeki T, Templeton NS et al. Successful treatment of primary and disseminated human lung cancers by systemic delivery of tumor suppressor genes using an improved liposome vector. Mol. Ther. 3(3), 337–350 (2001).
  • Lu Y, Kawakami S, Yamashita F, Hashida M. Development of an antigen-presenting cell-targeted DNA vaccine against melanoma by mannosylated liposomes. Biomaterials 28(21), 3255–3262 (2007).
  • Semple SC, Chonn A, Cullis PR. Influence of cholesterol on the association of plasma proteins with liposomes. Biochemistry 35(8), 2521–2525 (1996).
  • Devaraj GN, Parakh SR, Devraj R, Apte SS, Rao BR, Rambhau D. Release studies on niosomes containing fatty alcohols as bilayer stabilizers instead of cholesterol. J. Colloid Interface Sci. 251(2), 360–365 (2002).
  • Duthie MS, Windish HP, Fox CB, Reed SG. Use of defined TLR ligands as adjuvants within human vaccines. Immunol. Rev. 239(1), 178–196 (2011).
  • Slütter B, Bal SM, Ding Z, Jiskoot W, Bouwstra JA. Adjuvant effect of cationic liposomes and CpG depends on administration route. J. Control. Release 154(2), 123–130 (2011).
  • Mohanan D, Slütter B, Henriksen-Lacey M et al. Administration routes affect the quality of immune responses: a cross-sectional evaluation of particulate antigen-delivery systems. J. Control. Release 147(3), 342–349 (2010).
  • Johansen P, Mohanan D, Martinez-Gomez JM, Kundig TM, Gander B. Lympho-geographical concepts in vaccine delivery. J. Control. Release 148(1), 56–62 (2010).
  • Christensen D, Henriksen-Laceyb M, Kamath AT et al. A cationic vaccine adjuvant based on a saturated quaternary ammonium lipid have different in vivo distribution kinetics and display a distinct CD4 T cell-inducing capacity compared to its unsaturated analog. J. Control. Release doi:10.1016/j.jconrel.2012.03.016 (2012) (Epub ahead of print).
  • Pialoux G, Hocini H, Pérusat S et al.; ANRS VAC14 Study Group. Phase I study of a candidate vaccine based on recombinant HIV-1 gp160 (MN/LAI) administered by the mucosal route to HIV-seronegative volunteers: the ANRS VAC14 study. Vaccine 26(21), 2657–2666 (2008).
  • Smith LR, Wloch MK, Ye M et al. Phase 1 clinical trials of the safety and immunogenicity of adjuvanted plasmid DNA vaccines encoding influenza A virus H5 hemagglutinin. Vaccine 28(13), 2565–2572 (2010).
  • Porter KR, Ewing D, Chen L et al. Immunogenicity and protective efficacy of a vaxfectin-adjuvanted tetravalent dengue DNA vaccine. Vaccine 30(2), 336–341 (2012).
  • Joseph A, Itskovitz-Cooper N, Samira S et al. A new intranasal influenza vaccine based on a novel polycationic lipid–ceramide carbamoyl-spermine (CCS) I. Immunogenicity and efficacy studies in mice. Vaccine 24(18), 3990–4006(2006).
  • Even-Or O, Joseph A, Itskovitz-Cooper N 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. Vaccine 29(13), 2474–2486 (2011).
  • Even-Or O, Samira S, Rochlin E et al. Immunogenicity, protective efficacy and mechanism of novel CCS adjuvanted influenza vaccine. Vaccine 28(39), 6527–6541 (2010).
  • Sanchez V, Gimenez S, Haensler J et al. Formulations of single or multiple H. pylori antigens with DC Chol adjuvant induce protection by the systemic route in mice. Optimal prophylactic combinations are different from therapeutic ones. FEMS Immunol. Med. Microbiol. 30(2), 157–165 (2001).
  • Cheng JY, Huang HN, Tseng WC et al. Transcutaneous immunization by lipoplex-patch based DNA vaccines is effective vaccination against Japanese encephalitis virus infection. J. Control. Release 135(3), 242–249 (2009).
  • Woodard LF, Toone NM, McLaughlin CA. Comparison of muramyl dipeptide, trehalose dimycolate, and dimethyl dioctadecyl ammonium bromide as adjuvants in Brucella abortus 45/20 vaccines. Infect. Immun. 30(2), 409–412 (1980).
  • Willers JM, Bloksma N, van der Meer C et al. Regulation of the immune response by macrophages. Antonie Van Leeuwenhoek 45(1), 41–48 (1979).
  • Desowitz RS, Barnwell JW. Effect of selenium and dimethyl dioctadecyl ammonium bromide on the vaccine-induced immunity of Swiss–Webster mice against malaria (Plasmodiumberghei). Infect. Immun. 27(1), 87–89 (1980).
  • McColm AA, Bomford R, Dalton L. A comparison of saponin with other adjuvants for the potentiation of protective immunity by a killed Plasmodium yoelii vaccine in the mouse. Parasite Immunol. 4(5), 337–347 (1982).
  • Silva RA, Pais TF, Appelberg R. Effects of interleukin-12 in the long-term protection conferred by a Mycobacterium avium subunit vaccine. Scand. J. Immunol. 52(6), 531–533 (2000).
  • Katz D, Inbar I, Samina I, Peleg BA, Heller DE. Comparison of dimethyl dioctadecyl ammonium bromide, Freund’s complete adjuvant and mineral oil for induction of humoral antibodies, cellular immunity and resistance to Newcastle disease virus in chickens. FEMS Immunol. Med. Microbiol. 7(4), 303–313 (1993).
  • Kathaperumal K, Kumanan V, McDonough S et al. Evaluation of immune responses and protective efficacy in a goat model following immunization with a coctail of recombinant antigens and a polyprotein of Mycobacterium avium subsp. paratuberculosis. Vaccine 27(1), 123–135 (2009).
  • van Rooij EM, Glansbeek HL, Hilgers LA et al. Protective antiviral immune responses to pseudorabies virus induced by DNA vaccination using dimethyldioctadecylammonium bromide as an adjuvant. J. Virol. 76(20), 10540–10545 (2002).
  • Klinguer-Hamour C, Libon C, Plotnicky-Gilquin H et al. DDA adjuvant induces a mixed Th1/Th2 immune response when associated with BBG2Na, a respiratory syncytial virus potential vaccine. Vaccine 20(21–22), 2743–2751 (2002).
  • Klinguer C, Beck A, De-Lys P et al. Lipophilic quaternary ammonium salt acts as a mucosal adjuvant when co-administered by the nasal route with vaccine antigens. Vaccine 19(30), 4236–4244 (2001).
  • Kraaijeveld CA, Snippe H, Harmsen M, Khader Boutahar-Trouw B. Dimethyl dioctadecyl ammoniumbromide as an adjuvant for delayed type hypersensitivity and cellular immunity against Semliki Forest virus in mice. Arch. Virol. 65(3–4), 211–217 (1980).
  • Dascher CC, Hiromatsu K, Xiong X et al. Immunization with a mycobacterial lipid vaccine improves pulmonary pathology in the guinea pig model of tuberculosis. Int. Immunol. 15(8), 915–925 (2003).
  • Sharma AK, Verma I, Tewari R, Khuller GK. Adjuvant modulation of T-cell reactivity to 30-kDa secretory protein of Mycobacterium tuberculosis H37Rv and its protective efficacy against experimental tuberculosis. J. Med. Microbiol. 48(8), 757–763 (1999).
  • Giri PK, Sable SB, Verma I, Khuller GK. Comparative evaluation of intranasal and subcutaneous route of immunization for development of mucosal vaccine against experimental tuberculosis. FEMS Immunol. Med. Microbiol. 45(1), 87–93 (2005).
  • Giri PK, Verma I, Khuller GK. Enhanced immunoprotective potential of Mycobacterium tuberculosis Ag85 complex protein based vaccine against airway Mycobacterium tuberculosis challenge following intranasal administration. FEMS Immunol. Med. Microbiol. 47(2), 233–241 (2006).
  • Olsen AW, Williams A, Okkels LM, Hatch G, Andersen P. Protective effect of a tuberculosis subunit vaccine based on a fusion of antigen 85B and ESAT-6 in the aerosol guinea pig model. Infect. Immun. 72(10), 6148–6150 (2004).
  • Jaafari MR, Badiee A, Khamesipour A et al. The role of CpG ODN in enhancement of immune response and protection in BALB/c mice immunized with recombinant major surface glycoprotein of Leishmania (rgp63) encapsulated in cationic liposome. Vaccine 25(32), 6107–6117 (2007).
  • Cortesi R, Argnani R, Esposito E et al. Cationic liposomes as potential carriers for ocular administration of peptides with anti-herpetic activity. Int. J. Pharm. 317(1), 90–100 (2006).
  • Leal IS, Smedegård B, Andersen P, Appelberg R. Failure to induce enhanced protection against tuberculosis by increasing T-cell-dependent interferon-gamma generation. Immunology 104(2), 157–161 (2001).
  • Lindblad EB, Elhay MJ, Silva R, Appelberg R, Andersen P. Adjuvant modulation of immune responses to tuberculosis subunit vaccines. Infect. Immun. 65(2), 623–629 (1997).
  • Rosenkrands I, Agger EM, Olsen AW et al. Cationic liposomes containing mycobacterial lipids: a new powerful Th1 adjuvant system. Infect. Immun. 73(9), 5817–5826 (2005).
  • Li Q, Yu H, Zhang Y et al. Immunogenicity and protective efficacy of a fusion protein vaccine consisting of antigen Ag85B and HspX against Mycobacterium tuberculosis infection in mice. Scand. J. Immunol. 73(6), 568–576 (2011).
  • Luo Y, Wang B, Hu L et al. Fusion protein Ag85B-MPT64(190-198)-Mtb8.4 has higher immunogenicity than Ag85B with capacity to boost BCG-primed immunity against Mycobacterium tuberculosis in mice. Vaccine 27(44), 6179–6185 (2009).
  • Andersen CA, Rosenkrands I, Olsen AW et al. Novel generation mycobacterial adjuvant based on liposome-encapsulated monomycoloyl glycerol from Mycobacterium bovis bacillus Calmette–Guérin. J. Immunol. 183(4), 2294–2302 (2009).
  • Yu H, Karunakaran KP, Jiang X, Shen C, Andersen P, Brunham RC. Chlamydia muridarum T cell antigens and adjuvants that induce protective immunity in mice. Infect. Immun. 80(4), 1510–1518 (2012).
  • Holten-Andersen L, Doherty TM, Korsholm KS, Andersen P. Combination of the cationic surfactant dimethyl dioctadecyl ammonium bromide and synthetic mycobacterial cord factor as an efficient adjuvant for tuberculosis subunit vaccines. Infect. Immun. 72(3), 1608–1617 (2004).
  • Parra M, Pickett T, Delogu G et al. The mycobacterial heparin-binding hemagglutinin is a protective antigen in the mouse aerosol challenge model of tuberculosis. Infect. Immun. 72(12), 6799–6805 (2004).
  • Sable SB, Verma I, Khuller GK. Multicomponent antituberculous subunit vaccine based on immunodominant antigens of Mycobacterium tuberculosis. Vaccine 23(32), 4175–4184 (2005).
  • Langermans JA, Doherty TM, Vervenne RA et al. Protection of macaques against Mycobacterium tuberculosis infection by a subunit vaccine based on a fusion protein of antigen 85B and ESAT-6. Vaccine 23(21), 2740–2750 (2005).
  • Lee SH, Lillehoj HS, Jang SI et al. Embryo vaccination of chickens using a novel adjuvant formulation stimulates protective immunity against Eimeria maxima infection. Vaccine 28(49), 7774–7778 (2010).
  • Ridpath JF, Dominowski P, Mannan R et al. Evaluation of three experimental bovine viral diarrhea virus killed vaccines adjuvanted with combinations of Quil A cholesterol and dimethyldioctadecylammonium (DDA) bromide. Vet. Res. Commun. 34(8), 691–702 (2010).
  • Gonggrijp R, Antonissen AC, van den Bosch JF, van Boven CP. Ribonuclease-sensitive ribosomal vaccines. Antonie Van Leeuwenhoek 50(5–6), 763–774 (1984).
  • Yu H, Jiang X, Shen C et al. Chlamydia muridarum T-cell antigens formulated with the adjuvant DDA/TDB induce immunity against infection that correlates with a high frequency of gamma interferon (IFN-gamma)/tumor necrosis factor alpha and IFN-gamma/interleukin-17 double-positive CD4+ T cells. Infect. Immun. 78(5), 2272–2282 (2010).
  • Agger EM, Rosenkrands I, Hansen J et al. Cationic liposomes formulated with synthetic mycobacterial cordfactor (CAF01): a versatile adjuvant for vaccines with different immunological requirements. PLoS ONE 3(9), e3116 (2008).
  • Hansen J, Jensen KT, Follmann F, Agger EM, Theisen M, Andersen P. Liposome delivery of Chlamydia muridarum major outer membrane protein primes a Th1 response that protects against genital chlamydial infection in a mouse model. J. Infect. Dis. 198(5), 758–767 (2008).
  • Olsen AW, Theisen M, Christensen D, Follmann F, Andersen P. Protection against Chlamydia promoted by a subunit vaccine (CTH1) compared with a primary intranasal infection in a mouse genital challenge model. PLoS ONE 5(5), e10768 (2010).
  • Hitzler I, Oertli M, Becher B, Agger EM, Müller A. Dendritic cells prevent rather than promote immunity conferred by a helicobacter vaccine using a mycobacterial adjuvant. Gastroenterology 141(1), 186–196, 196.e1 (2011).
  • Fomsgaard A, Karlsson I, Gram G et al. Development and preclinical safety evaluation of a new therapeutic HIV-1 vaccine based on 18 T-cell minimal epitope peptides applying a novel cationic adjuvant CAF01. Vaccine 29(40), 7067–7074 (2011).
  • Martel CJ, Agger EM, Poulsen JJ et al. CAF01 potentiates immune responses and efficacy of an inactivated influenza vaccine in ferrets. PLoS ONE 6(8), e22891 (2011).
  • Rosenkrands I, Vingsbo-Lundberg C, Bundgaard TJ et al. Enhanced humoral and cell-mediated immune responses after immunization with trivalent influenza vaccine adjuvanted with cationic liposomes. Vaccine 29(37), 6283–6291 (2011).
  • Kamath AT, Rochat AF, Christensen D et al. A liposome-based mycobacterial vaccine induces potent adult and neonatal multifunctional T cells through the exquisite targeting of dendritic cells. PLoS ONE 4(6), e5771 (2009).
  • Christensen D, Lindenstrøm T, van de Wijdeven G, Andersen P, Agger EM. Syringe free vaccination with CAF01 Adjuvated Ag85B-ESAT-6 in Bioneedles provides strong and prolonged protection against tuberculosis. PLoS ONE 5(11), e15043 (2010).
  • Lindenstrøm T, Agger EM, Korsholm KS et al. Tuberculosis subunit vaccination provides long-term protective immunity characterized by multifunctional CD4 memory T cells. J. Immunol. 182(12), 8047–8055 (2009).
  • Aagaard CS, Hoang TT, Vingsbo-Lundberg C, Dietrich J, Andersen P. Quality and vaccine efficacy of CD4+ T cell responses directed to dominant and subdominant epitopes in ESAT-6 from Mycobacterium tuberculosis. J. Immunol. 183(4), 2659–2668 (2009).
  • Niu H, Hu L, Li Q et al. Construction and evaluation of a multistage Mycobacterium tuberculosis subunit vaccine candidate Mtb10.4-HspX. Vaccine 29(51), 9451–9458 (2011).
  • Dietrich J, Billeskov R, Doherty TM, Andersen P. Synergistic effect of bacillus calmette guerin and a tuberculosis subunit vaccine in cationic liposomes: increased immunogenicity and protection. J. Immunol. 178(6), 3721–3730 (2007).
  • Wedlock DN, Denis M, Painter GF et al. Enhanced protection against bovine tuberculosis after coadministration of Mycobacterium bovis BCG with a Mycobacterial protein vaccine-adjuvant combination but not after coadministration of adjuvant alone. Clin. Vaccine Immunol. 15(5), 765–772 (2008).
  • Cai H, Tian X, Hu XD, Li SX, Yu DH, Zhu YX. Combined DNA vaccines formulated either in DDA or in saline protect cattle from Mycobacterium bovis infection. Vaccine 23(30), 3887–3895 (2005).
  • Roh HJ, Sung HW, Kwon HM. Effects of DDA, CpG-ODN, and plasmid-encoded chicken IFN-gamma on protective immunity by a DNA vaccine against IBDV in chickens. J. Vet. Sci. 7(4), 361–368 (2006).
  • Bu J, Song Y, Rompato G, Burgess DJ, Garmendia AE. Co-delivery of IL-2 or liposomes augment the responses of mice to a DNA vaccine for pseudorabies virus IE180. Comp. Immunol. Microbiol. Infect. Dis. 26(3), 175–187 (2003).
  • Jacquet A, Vanderschrick JF, Vandenbranden M et al. Vaccination with the recombinant allergen ProDer p 1 complexed with the cationic lipid DiC14-amidine prevents allergic responses to house dust mite. Mol. Ther. 11(6), 960–968 (2005).
  • Chen W, Yan W, Huang L. A simple but effective cancer vaccine consisting of an antigen and a cationic lipid. Cancer Immunol. Immunother. 57(4), 517–530 (2008).
  • Vasievich EA, Chen W, Huang L. Enantiospecific adjuvant activity of cationic lipid DOTAP in cancer vaccine. Cancer Immunol. Immunother. 60(5), 629–638 (2011).
  • Yan W, Chen W, Huang L. Mechanism of adjuvant activity of cationic liposome: phosphorylation of a MAP kinase, ERK and induction of chemokines. Mol. Immunol. 44(15), 3672–3681 (2007).
  • Yan W, Chen W, Huang L. Reactive oxygen species play a central role in the activity of cationic liposome based cancer vaccine. J. Control. Release 130(1), 22–28 (2008).
  • Yan W, Huang L. The effects of salt on the physicochemical properties and immunogenicity of protein based vaccine formulated in cationic liposome. Int J Pharm 368(1–2), 56–62 (2009).
  • Heravi Shargh V, Jaafari MR, Khamesipour A et al. Cationic liposomes containing soluble Leishmania antigens (SLA) plus CpG ODNs induce protection against murine model of leishmaniasis. Parasitol. Res. doi:10.1007/s00436-011-2806-5(2012) (Epub ahead of print).
  • Cheng G, Zhao X, Yan W et al. Alpha interferon is a powerful adjuvant for a recombinant protein vaccine against foot-and-mouth disease virus in swine, and an effective stimulus of in vivo immune response. Vaccine 25(28), 5199–5208 (2007).
  • Fernandez-Alonso M, Rocha A, Coll JM. DNA vaccination by immersion and ultrasound to trout viral haemorrhagic septicaemia virus. Vaccine 19(23–24), 3067–3075 (2001).
  • Zhang YY, Taylor MG, Gregoriadis G, McCrossan MV, Bickle QD. Immunogenicity of plasmid DNA encoding the 62 kDa fragment of Schistosoma japonicum myosin. Vaccine 18(20), 2102–2109 (2000).
  • Rosada RS, de la Torre LG, Frantz FG et al. Protection against tuberculosis by a single intranasal administration of DNA-hsp65 vaccine complexed with cationic liposomes. BMC Immunol. 9, 38 (2008).
  • Chen R, Lu SH, Tong QB et al. Protective effect of DNA-mediated immunization with liposome-encapsulated GRA4 against infection of Toxoplasma gondii. J. Zhejiang Univ. Sci. B 10(7), 512–521 (2009).
  • Harpin S, Hurley DJ, Mbikay M, Talbot B, Elazhary Y. Vaccination of cattle with a DNA plasmid encoding the bovine viral diarrhoea virus major glycoprotein E2. J. Gen. Virol. 80(Pt 12), 3137–3144 (1999).
  • Whitmore M, Li S, Huang L. LPD lipopolyplex initiates a potent cytokine response and inhibits tumor growth. Gene Ther. 6(11), 1867–1875 (1999).
  • Chang S, Warner J, Liang L, Fairman J. A novel vaccine adjuvant for recombinant flu antigens. Biologicals 37(3), 141–147 (2009).
  • Dong L, Liu F, Fairman J et al. Cationic liposome-DNA complexes (CLDC) adjuvant enhances the immunogenicity and cross-protective efficacy of a pre-pandemic influenza A H5N1 vaccine in mice. Vaccine 30(2), 254–264 (2012).
  • Lay M, Callejo B, Chang S et al. Cationic lipid/DNA complexes (JVRS-100) combined with influenza vaccine (fluzone) increases antibody response, cellular immunity, and antigenically drifted protection. Vaccine 27(29), 3811–3820 (2009).
  • Morrey JD, Motter NE, Chang S, Fairman J. Breaking B and T cell tolerance using cationic lipid–DNA complexes (CLDC) as a vaccine adjuvant with hepatitis B virus (HBV) surface antigen in transgenic mice expressing HBV. Antiviral Res. 90(3), 227–230 (2011).
  • Bernstein DI, Cardin RD, Bravo FJ et al. Potent adjuvant activity of cationic liposome-DNA complexes for genital herpes vaccines. Clin. Vaccine Immunol. 16(5), 699–705 (2009).
  • Bernstein DI, Earwood JD, Bravo FJ et al. Effects of herpes simplex virus type 2 glycoprotein vaccines and CLDC adjuvant on genital herpes infection in the guinea pig. Vaccine 29(11), 2071–2078 (2011).
  • Bernstein DI, Farley N, Bravo FJ et al. The adjuvant CLDC increases protection of a herpes simplex type 2 glycoprotein D vaccine in guinea pigs. Vaccine 28(21), 3748–3753 (2010).
  • Cote PJ, Butler SD, George AL et al. Rapid immunity to vaccination with woodchuck hepatitis virus surface antigen using cationic liposome-DNA complexes as adjuvant. J. Med. Virol. 81(10), 1760–1772 (2009).
  • Henderson A, Propst K, Kedl R, Dow S. Mucosal immunization with liposome-nucleic acid adjuvants generates effective humoral and cellular immunity. Vaccine 29(32), 5304–5312 (2011).
  • Hong DK, Chang S, Botham CM, Giffon TD, Fairman J, Lewis DB. Cationic lipid/DNA complex-adjuvanted influenza A virus vaccination induces robust cross-protective immunity. J. Virol. 84(24), 12691–12702 (2010).
  • Jones A, Bosio C, Duffy A, Goodyear A, Schriefer M, Dow S. Protection against pneumonic plague following oral immunization with a non-replicating vaccine. Vaccine 28(36), 5924–5929 (2010).
  • Schleiss MR, Stroup G, Pogorzelski K, McGregor A. Protection against congenital cytomegalovirus (CMV) disease, conferred by a replication-disabled, bacterial artificial chromosome (BAC)-based DNA vaccine. Vaccine 24(37–39), 6175–6186 (2006).
  • Sakaguchi M, Nakamura H, Sonoda K, Hamada F, Hirai K. Protection of chickens from Newcastle disease by vaccination with a linear plasmid DNA expressing the F protein of Newcastle disease virus. Vaccine 14(8), 747–752 (1996).
  • Yokoyama M, Zhang J, Whitton JL. DNA immunization: effects of vehicle and route of administration on the induction of protective antiviral immunity. FEMS Immunol. Med. Microbiol. 14(4), 221–230 (1996).
  • Franke ED, Corradin G, Hoffman SL. Induction of protective CTL responses against the Plasmodium yoelii circumsporozoite protein by immunization with peptides. J. Immunol. 159(7), 3424–3433 (1997).
  • Jimenez GS, Planchon R, Wei Q et al. Vaxfectin-formulated influenza DNA vaccines encoding NP and M2 viral proteins protect mice against lethal viral challenge. Hum. Vaccin. 3(5), 157–164 (2007).
  • Vilalta A, Jimenez G, Rusalov D et al. Vaccination with polymerase chain reaction-generated linear expression cassettes protects mice against lethal influenza A challenge. Hum. Gene Ther. 18(8), 763–771 (2007).
  • Lalor PA, Webby RJ, Morrow J et al. Plasmid DNA-based vaccines protect mice and ferrets against lethal challenge withA/Vietnam/1203/04 (H5N1) influenza virus. J. Infect. Dis. 197(12), 1643–1652 (2008).
  • Pan CH, Jimenez GS, Nair N et al. Use of Vaxfectin adjuvant with DNA vaccine encoding the measles virus hemagglutinin and fusion proteins protects juvenile and infant rhesus macaques against measles virus. Clin. Vaccine Immunol. 15(8), 1214–1221 (2008).
  • Locher CP, Witt SA, Ashlock BM et al. Human immunodeficiency virus type 2 DNA vaccine provides partial protection from acute baboon infection. Vaccine 22(17–18), 2261–2272 (2004).
  • Lima KM, Bonato VL, Faccioli LH et al. Comparison of different delivery systems of vaccination for the induction of protection against tuberculosis in mice. Vaccine 19(25–26), 3518–3525 (2001).
  • Afrin F, Ali N. Adjuvanticity and protective immunity elicited by Leishmania donovani antigens encapsulated in positively charged liposomes. Infect. Immun. 65(6), 2371–2377 (1997).
  • Mazumder S, Maji M, Ali N. Potentiating effects of MPL on DSPC bearing cationic liposomes promote recombinant GP63 vaccine efficacy: high immunogenicity and protection. PLoS Negl. Trop. Dis. 5(12), e1429 (2011).
  • Ravindran R, Maji M, Ali N. Vaccination with liposomal leishmanial antigens adjuvanted with monophosphoryl lipid-trehalose dicorynomycolate (MPL-TDM) confers long-term protection against visceral leishmaniasis through a human administrable route. Mol. Pharm. 9(1), 59–70 (2012).
  • Ravindran R, Bhowmick S, Das A, Ali N. Comparison of BCG, MPL and cationic liposome adjuvant systems in leishmanial antigen vaccine formulations against murine visceral leishmaniasis. BMC Microbiol. 10, 181 (2010).
  • Bhowmick S, Mazumdar T, Sinha R, Ali N. Comparison of liposome based antigen delivery systems for protection against Leishmania donovani. J. Control. Release 141(2), 199–207 (2010).
  • Bhowmick S, Ali N. Identification of novel Leishmania donovani antigens that help define correlates of vaccine-mediated protection in visceral leishmaniasis. PLoS ONE 4(6), e5820 (2009).
  • Bhowmick S, Ravindran R, Ali N. gp63 in stable cationic liposomes confers sustained vaccine immunity to susceptible BALB/c mice infected with Leishmania donovani. Infect. Immun. 76(3), 1003–1015 (2008).
  • Afrin F, Rajesh R, Anam K, Gopinath M, Pal S, Ali N. Characterization of Leishmania donovani antigens encapsulated in liposomes that induce protective immunity in BALB/c mice. Infect. Immun. 70(12), 6697–6706 (2002).
  • Mazumder S, Ravindran R, Banerjee A, Ali N. Non-coding pDNA bearing immunostimulatory sequences co-entrapped with leishmanial antigens in cationic liposomes elicits almost complete protection against experimental visceral leishmaniasis in BALB/c mice. Vaccine 25(52), 8771–8781 (2007).
  • Commander NJ, Brewer JM, Wren BW, Spencer SA, Macmillan AP, Stack JA. Liposomal delivery of p-ialB and p-omp25 DNA vaccines improves immunogenicity but fails to provide full protection against B. melitensis challenge. Genet. Vaccines Ther. 8, 5 (2010).
  • Usui T, Konnai S, Tajima S et al. Protective effects of vaccination with bovine leukemia virus (BLV) Tax DNA against BLV infection in sheep. J. Vet. Med. Sci. 65(11), 1201–1205 (2003).
  • Davidsen J, Rosenkrands I, Christensen D et al. Characterization of cationic liposomes based on dimethyldioctadecylammonium and synthetic cord factor from M. tuberculosis (trehalose 6,6´-dibehenate) – a novel adjuvant inducing both strong CMI and antibody responses. Biochim Biophys Acta 1718(1–2), 22–31 (2005).
  • Nordly P, Korsholm KS, Pedersen EA et al. Incorporation of a synthetic mycobacterial monomycoloyl glycerol analogue stabilizes dimethyldioctadecylammonium liposomes and potentiates their adjuvant effect in vivo. Eur J Pharm Biopharm 77(1), 89–98 (2011).

Websites

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.