Liposome Formulations as Adjuvants for Vaccines.
Journal
Current topics in microbiology and immunology
ISSN: 0070-217X
Titre abrégé: Curr Top Microbiol Immunol
Pays: Germany
ID NLM: 0110513
Informations de publication
Date de publication:
2021
2021
Historique:
pubmed:
10
11
2020
medline:
7
9
2021
entrez:
9
11
2020
Statut:
ppublish
Résumé
Development of liposome-based formulations as vaccine adjuvants has been intimately associated with, and dependent on, and informed by, a fundamental understanding of biochemical and biophysical properties of liposomes themselves. The Walter Reed Army Institute of Research (WRAIR) has a fifty-year history of experience of basic research on liposomes; and development of liposomes as drug carriers; and development of liposomes as adjuvant formulations for vaccines. Uptake of liposomes by phagocytic cells in vitro has served as an excellent model for studying the intracellular trafficking patterns of liposomal antigen. Differential fluorescent labeling of proteins and liposomal lipids, together with the use of inhibitors, has enabled the visualization of physical locations of antigens, peptides, and lipids to elucidate mechanisms underlying the MHC class I and class II pathways in phagocytic APCs. Army Liposome Formulation (ALF) family of vaccine adjuvants, which have been developed and improved since 1986, and which range from nanosize to microsize, are currently being employed in phase 1 studies with different types of candidate vaccines.
Substances chimiques
Adjuvants, Immunologic
0
Antigens
0
Lipids
0
Liposomes
0
Vaccines
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1-28Informations de copyright
© 2021. This is a U.S. government work and not under copyright protection in the U.S.; foreign copyright protection may apply.
Références
Allison AG, Gregoriadis G (1974) Liposomes as immunological adjuvants. Nature 252:252
pubmed: 4424229
doi: 10.1038/252252a0
Alving CR (1984) Natural antibodies against phospholipids and liposomes in humans. Biochem Soc Trans 12:342–344
pubmed: 6724120
doi: 10.1042/bst0120342
Alving CR (1991) Liposomes as carriers of antigens and adjuvants. J Immunol Methods 140:1–13
pubmed: 1712030
doi: 10.1016/0022-1759(91)90120-5
Alving CR (2002) Design and selection of vaccine adjuvants: animal models and human trials. Vaccine 20(Suppl 3):S56–S64
pubmed: 12184368
doi: 10.1016/S0264-410X(02)00174-3
Alving C, Beck Z (2019) Non-toxic adjuvant formulation comprising a monophosphoryl lipid A (MPLA)-containing liposome composition and a saponin. US patent application, 8 Oct 2019
Alving CR, Kinsky SC (1971) The preparation and properties of liposomes in the LA and LAC states. Immunochemistry 8:325–343
pubmed: 5105371
doi: 10.1016/0019-2791(71)90155-8
Alving CR, Wassef NM (1999) Naturally occurring antibodies to cholesterol: a new theory of LDL cholesterol metabolism. Immunol Today 20:362–366
pubmed: 10431156
doi: 10.1016/S0167-5699(99)01496-6
Alving CR, Richards RL, Moss J et al (1986) Effectiveness of liposomes as potential carriers of vaccines: applications to cholera toxin and human malaria sporozoite antigen. Vaccine 4:166–172
pubmed: 3532603
doi: 10.1016/0264-410X(86)90005-8
Alving CR, Koulchin V, Glenn GM et al (1995) Liposomes as carriers of peptide antigens: induction of antibodies and cytotoxic T lymphocytes to conjugated and unconjugated peptides. Immunol Rev 145:5–31
pubmed: 7590830
doi: 10.1111/j.1600-065X.1995.tb00075.x
Alving CR, Peachman KK, Rao M et al (2012) Adjuvants for human vaccines. Curr Opin Immunol 24:310–315
pubmed: 22521140
pmcid: 3383374
doi: 10.1016/j.coi.2012.03.008
Alving CR, Beck Z, Matyas GR et al (2016) Liposomal adjuvants for human vaccines. Expert Opin Drug Deliv 13:807–816
pubmed: 26866300
doi: 10.1517/17425247.2016.1151871
Alving CR, Peachman KK, Matyas GR et al (2020) Army Liposome Formulation (ALF) family of vaccine adjuvants. Expert Rev Vaccines 1–14
Androlewicz MJ, Browning JL, Ware CF (1992) Lymphotoxin is expressed as a heteromeric complex with a distinct 33-kDa glycoprotein on the surface of an activated human T cell hybridoma. J Biol Chem 267:2542–2547
pubmed: 1733951
doi: 10.1016/S0021-9258(18)45914-5
Ballou WR, Hoffman SL, Sherwood JA et al (1987) Safety and efficacy of a recombinant DNA Plasmodium falciparum sporozoite vaccine. Lancet 1:1277–1281
pubmed: 2884410
doi: 10.1016/S0140-6736(87)90540-X
Bangham AD, Standish MM, Watkins JC (1965) Diffusion of univalent ions across the lamellae of swollen phospholipids. J Mol Biol 13:238–252
pubmed: 5859039
doi: 10.1016/S0022-2836(65)80093-6
Bao L, Ding L, Yang M et al (2015) Noninvasive imaging of sialyltransferase activity in living cells by chemoselective recognition. Sci Rep 5:10947
pubmed: 26046317
pmcid: 4456940
doi: 10.1038/srep10947
Beck Z, Matyas GR, Alving CR (2015a) Detection of liposomal cholesterol and monophosphoryl lipid A by QS-21 saponin and Limulus polyphemus amebocyte lysate. Biochim Biophys Acta 1848:775–780
pubmed: 25511587
doi: 10.1016/j.bbamem.2014.12.005
Beck Z, Matyas GR, Jalah R et al (2015b) Differential immune responses to HIV-1 envelope protein induced by liposomal adjuvant formulations containing monophosphoryl lipid A with or without QS21. Vaccine 33:5578–5587
pubmed: 26372857
doi: 10.1016/j.vaccine.2015.09.001
Beck Z, Torres OB, Matyas GR et al (2018) Immune response to antigen adsorbed to aluminum hydroxide particles: effects of co-adsorption of ALF or ALFQ adjuvant to the aluminum-antigen complex. J Control Release 275:12–19
pubmed: 29432824
pmcid: 5878139
doi: 10.1016/j.jconrel.2018.02.006
Bevan MJ (1987) Antigen recognition. Class discrimination in the world of immunology. Nature 325:192–194
pubmed: 2433584
doi: 10.1038/325192b0
Boes M, Van Der Wel N, Peperzak V et al (2005) In vivo control of endosomal architecture by class II-associated invariant chain and cathepsin S. Eur J Immunol 35:2552–2562
pubmed: 16094690
doi: 10.1002/eji.200526323
Bohlson SS, Garred P, Kemper C et al (2019) Complement nomenclature-deconvoluted. Front Immunol 10:1308
pubmed: 31231398
pmcid: 6568193
doi: 10.3389/fimmu.2019.01308
Bonte F, Juliano RL (1986) Interactions of liposomes with serum proteins. Chem Phys Lipids 40:359–372
pubmed: 3742678
doi: 10.1016/0009-3084(86)90079-4
Cawlfield A, Genito CJ, Beck Z et al (2019) Safety, toxicity and immunogenicity of a malaria vaccine based on the circumsporozoite protein (FMP013) with the adjuvant army liposome formulation containing QS21 (ALFQ). Vaccine 37:3793–3803
pubmed: 31151801
doi: 10.1016/j.vaccine.2019.05.059
Cedervall T, Lynch I, Lindman S et al (2007) Understanding the nanoparticle-protein corona using methods to quantify exchange rates and affinities of proteins for nanoparticles. Proc Natl Acad Sci U S A 104:2050–2055
pubmed: 17267609
pmcid: 1892985
doi: 10.1073/pnas.0608582104
Chapman HA (2006) Endosomal proteases in antigen presentation. Curr Opin Immunol 18:78–84
pubmed: 16338127
doi: 10.1016/j.coi.2005.11.011
Chonn A, Cullis PR, Devine DV (1991) The role of surface charge in the activation of the classical and alternative pathways of complement by liposomes. J Immunol 146:4234–4241
pubmed: 2040798
Chonn A, Semple SC, Cullis PR (1992) Association of blood proteins with large unilamellar liposomes in vivo. Relation to circulation lifetimes. J Biol Chem 267:18759–18765
pubmed: 1527006
doi: 10.1016/S0021-9258(19)37026-7
Chulay JD, Schneider I, Cosgriff TM et al (1986) Malaria transmitted to humans by mosquitoes infected from cultured Plasmodium falciparum. Am J Trop Med Hyg 35:66–68
pubmed: 3511753
doi: 10.4269/ajtmh.1986.35.66
Collins DS, Findlay K, Harding CV (1992) Processing of exogenous liposome-encapsulated antigens in vivo generates class I MHC-restricted T cell responses. J Immunol 148:3336–3341
pubmed: 1588035
pmcid: 1588035
Couture A, Garnier A, Docagne F et al (2019) HLA-Class II artificial antigen presenting cells in CD4(+) T cell-based immunotherapy. Front Immunol 10:1081
pubmed: 31156634
pmcid: 6533590
doi: 10.3389/fimmu.2019.01081
Dame JB, Williams JL, Mccutchan TF et al (1984) Structure of the gene encoding the immunodominant surface antigen on the sporozoite of the human malaria parasite Plasmodium falciparum. Science 225:593–599
pubmed: 6204383
doi: 10.1126/science.6204383
pmcid: 6204383
De Serrano LO, Burkhart DJ (2017) Liposomal vaccine formulations as prophylactic agents: design considerations for modern vaccines. J Nanobiotechnol 15:83
doi: 10.1186/s12951-017-0319-9
Didierlaurent AM, Collignon C, Bourguignon P et al (2014) Enhancement of adaptive immunity by the human vaccine adjuvant AS01 depends on activated dendritic cells. J Immunol 193:1920–1930
pubmed: 25024381
doi: 10.4049/jimmunol.1400948
Didierlaurent AM, Laupeze B, Di Pasquale A et al (2017) Adjuvant system AS01: helping to overcome the challenges of modern vaccines. Expert Rev Vaccines 16:55–63
pubmed: 27448771
doi: 10.1080/14760584.2016.1213632
pmcid: 27448771
Edelman R, Wasserman SS, Kublin JG et al (2002) Immediate-type hypersensitivity and other clinical reactions in volunteers immunized with a synthetic multi-antigen peptide vaccine (PfCS-MAP1NYU) against Plasmodium falciparum sporozoites. Vaccine 21:269–280
pubmed: 12450702
doi: 10.1016/S0264-410X(02)00468-1
Enea V, Ellis J, Zavala F et al (1984) DNA cloning of Plasmodium falciparum circumsporozoite gene: amino acid sequence of repetitive epitope. Science 225:628–630
pubmed: 6204384
doi: 10.1126/science.6204384
Engler OB, Schwendener RA, Dai WJ et al (2004) A liposomal peptide vaccine inducing CD8+ T cells in HLA-A2.1 transgenic mice, which recognise human cells encoding hepatitis C virus (HCV) proteins. Vaccine 23:58–68
pubmed: 15519708
doi: 10.1016/j.vaccine.2004.05.009
pmcid: 15519708
Fries LF, Gordon DM, Richards RL et al (1992) Liposomal malaria vaccine in humans: a safe and potent adjuvant strategy. Proc Natl Acad Sci U S A 89:358–362
pubmed: 1729706
pmcid: 48236
doi: 10.1073/pnas.89.1.358
Garcon N, Chomez P, Van Mechelen M (2007) GlaxoSmithKline adjuvant systems in vaccines: concepts, achievements and perspectives. Expert Rev Vaccines 6:723–739
pubmed: 17931153
doi: 10.1586/14760584.6.5.723
pmcid: 17931153
Genito CJ, Beck Z, Phares TW et al (2017) Liposomes containing monophosphoryl lipid A and QS-21 serve as an effective adjuvant for soluble circumsporozoite protein malaria vaccine FMP013. Vaccine 35:3865–3874
pubmed: 28596090
doi: 10.1016/j.vaccine.2017.05.070
pmcid: 28596090
Germain RN, Margulies DH (1993) The biochemistry and cell biology of antigen processing and presentation. Annu Rev Immunol 11:403–450
pubmed: 8476568
doi: 10.1146/annurev.iy.11.040193.002155
pmcid: 8476568
Giodini A, Albert ML (2010) A whodunit: an appointment with death. Curr Opin Immunol 22:94–108
pubmed: 20171862
doi: 10.1016/j.coi.2010.01.023
pmcid: 20171862
Gregoriadis G (1978) Liposomes in therapeutic and preventive medicine: the development of the drug-carrier concept. Ann N Y Acad Sci 308:343–370
pubmed: 100040
doi: 10.1111/j.1749-6632.1978.tb22034.x
pmcid: 100040
Haxby JA, Kinsky CB, Kinsky SC (1968) Immune response of a liposomal model membrane. Proc Natl Acad Sci U S A 61:300–307
pubmed: 5246926
pmcid: 285936
doi: 10.1073/pnas.61.1.300
Haxby JA, Gotze O, Muller-Eberhard HJ et al (1969) Release of trapped marker from liposomes by the action of purified complement components. Proc Natl Acad Sci U S A 64:290–295
pubmed: 5263014
pmcid: 286160
doi: 10.1073/pnas.64.1.290
Henriksen-Lacey M, Bramwell VW, Christensen D et al (2010) Liposomes based on dimethyldioctadecylammonium promote a depot effect and enhance immunogenicity of soluble antigen. J Control Release 142:180–186
pubmed: 19874860
doi: 10.1016/j.jconrel.2009.10.022
pmcid: 19874860
Heppner DG, Gordon DM, Gross M et al (1996) Safety, immunogenicity, and efficacy of Plasmodium falciparum repeatless circumsporozoite protein vaccine encapsulated in liposomes. J Infect Dis 174:361–366
pubmed: 8699067
doi: 10.1093/infdis/174.2.361
pmcid: 8699067
Herzog C, Hartmann K, Kunzi V et al (2009) Eleven years of inflexal V-a virosomal adjuvanted influenza vaccine. Vaccine 27:4381–4387
pubmed: 19450630
doi: 10.1016/j.vaccine.2009.05.029
pmcid: 19450630
Jafari I, Heravi Shargh V, Shahryari M et al (2018) Cationic liposomes formulated with a novel whole Leishmania lysate (WLL) as a vaccine for leishmaniasis in murine model. Immunobiology 223:493–500
pubmed: 29317110
doi: 10.1016/j.imbio.2017.12.003
Joffre OP, Segura E, Savina A et al (2012) Cross-presentation by dendritic cells. Nat Rev Immunol 12:557–569
pubmed: 22790179
doi: 10.1038/nri3254
Kamphuis T, Meijerhof T, Stegmann T et al (2012) Immunogenicity and protective capacity of a virosomal respiratory syncytial virus vaccine adjuvanted with monophosphoryl lipid A in mice. PLoS ONE 7:e36812
pubmed: 22590614
pmcid: 3348902
doi: 10.1371/journal.pone.0036812
Ke PC, Lin S, Parak WJ et al (2017) A decade of the protein corona. ACS Nano 11:11773–11776
pubmed: 29206030
doi: 10.1021/acsnano.7b08008
Kinsky SC, Haxby JA, Zopf DA et al (1969) Complement-dependent damage to liposomes prepared from pure lipids and Forssman hapten. Biochemistry 8:4149–4158
pubmed: 5346393
doi: 10.1021/bi00838a036
Kleijmeer MJ, Kelly A, Geuze HJ et al (1992) Location of MHC-encoded transporters in the endoplasmic reticulum and cis-Golgi. Nature 357:342–344
pubmed: 1589036
doi: 10.1038/357342a0
pmcid: 1589036
Krstic RE (1979) Ultrastructure of the Mammalian Cell. An Atlas. Springer-Verlag, New York
Laborde RJ, Sanchez-Ferras O, Luzardo MC et al (2017) Novel adjuvant based on the pore-forming protein sticholysin II encapsulated into liposomes effectively enhances the antigen-specific CTL-mediated immune response. J Immunol 198:2772–2784
pubmed: 28258198
doi: 10.4049/jimmunol.1600310
pmcid: 28258198
Lal H, Cunningham AL, Godeaux O et al (2015) Efficacy of an adjuvanted herpes zoster subunit vaccine in older adults. N Engl J Med 372:2087–2096
pubmed: 25916341
doi: 10.1056/NEJMoa1501184
pmcid: 25916341
Li S, Paulsson KM, Sjogren HO et al (1999) Peptide-bound major histocompatibility complex class I molecules associate with tapasin before dissociation from transporter associated with antigen processing. J Biol Chem 274:8649–8654
pubmed: 10085102
doi: 10.1074/jbc.274.13.8649
Li M, Du C, Guo N et al (2019) Composition design and medical application of liposomes. Eur J Med Chem 164:640–653
pubmed: 30640028
doi: 10.1016/j.ejmech.2019.01.007
Liang F, Lore K (2016) Local innate immune responses in the vaccine adjuvant-injected muscle. Clin Transl Immunology 5:e74
pubmed: 27195117
pmcid: 4855268
doi: 10.1038/cti.2016.19
Liang F, Ploquin A, Hernandez JD et al (2015) Dissociation of skeletal muscle for flow cytometric characterization of immune cells in macaques. J Immunol Methods 425:69–78
pubmed: 26099800
pmcid: 4604051
doi: 10.1016/j.jim.2015.06.011
Lipsky NG, Pagano RE (1985) A vital stain for the Golgi apparatus. Science 228:745–747
pubmed: 2581316
doi: 10.1126/science.2581316
Liszewski MK, Elvington M, Kulkarni HS et al (2017) Complement’s hidden arsenal: new insights and novel functions inside the cell. Mol Immunol 84:2–9
pubmed: 28196665
pmcid: 5373558
doi: 10.1016/j.molimm.2017.01.004
Lopes LM, Chain BM (1992) Liposome-mediated delivery stimulates a class I-restricted cytotoxic T cell response to soluble antigen. Eur J Immunol 22:287–290
pubmed: 1730255
doi: 10.1002/eji.1830220143
Lubbers R, Van Essen MF, Van Kooten C et al (2017) Production of complement components by cells of the immune system. Clin Exp Immunol 188:183–194
pubmed: 28249350
pmcid: 5383442
doi: 10.1111/cei.12952
Margulies DH, Jiang J, Natarajan K (2020) Structural and dynamic studies of TAPBPR and Tapasin reveal the mechanism of peptide loading of MHC-I molecules. Curr Opin Immunol 64:71–79
pubmed: 32402827
doi: 10.1016/j.coi.2020.04.004
pmcid: 32402827
Matyas GR, Alving CR (2011) Antigen-specific enhancement of natural human IgG antibodies to phosphatidylcholine, phosphatidylglycerol, phosphatidylinositol-4-phosphate, cholesterol, and lipid A by a liposomal vaccine containing lipid A. Vaccine 29:5137–5144
pubmed: 21624414
doi: 10.1016/j.vaccine.2011.05.042
pmcid: 21624414
Matyas GR, Muderhwa JM, Alving CR (2003) Oil-in-water liposomal emulsions for vaccine delivery. Methods Enzymol 373:34–50
pubmed: 14714395
doi: 10.1016/S0076-6879(03)73003-1
Mcelrath MJ (1995) Selection of potent immunological adjuvants for vaccine construction. Semin Cancer Biol 6:375–385
pubmed: 8938276
doi: 10.1016/1044-579X(95)90007-1
Moser C, Muller M, Kaeser MD et al (2013) Influenza virosomes as vaccine adjuvant and carrier system. Expert Rev Vaccines 12:779–791
pubmed: 23885823
doi: 10.1586/14760584.2013.811195
Munz C (2010) Antigen processing via autophagy–not only for MHC class II presentation anymore? Curr Opin Immunol 22:89–93
pubmed: 20149615
pmcid: 3082731
doi: 10.1016/j.coi.2010.01.016
Neefjes JJ, Momburg F, Hammerling GJ (1993) Selective and ATP-dependent translocation of peptides by the MHC-encoded transporter. Science 261:769–771
pubmed: 8342042
doi: 10.1126/science.8342042
Nelson RA Jr, Jensen J, Gigli I et al (1966) Methods for the separation, purification and measurement of nine components of hemolytic complement in guinea-pig serum. Immunochemistry 3:111–135
pubmed: 5960883
doi: 10.1016/0019-2791(66)90292-8
Nisini R, Poerio N, Mariotti S et al (2018) The multirole of liposomes in therapy and prevention of infectious diseases. Front Immunol 9:155
pubmed: 29459867
pmcid: 5807682
doi: 10.3389/fimmu.2018.00155
Nunes-Hasler P, Demaurex N (2017) The ER phagosome connection in the era of membrane contact sites. Biochim Biophys Acta Mol Cell Res 1864:1513–1524
pubmed: 28432021
doi: 10.1016/j.bbamcr.2017.04.007
Pagano RE (1990) The Golgi apparatus: insights from lipid biochemistry. Biochem Soc Trans 18:361–366
pubmed: 2197129
doi: 10.1042/bst0180361
Pagano RE, Sepanski MA, Martin OC (1989) Molecular trapping of a fluorescent ceramide analogue at the Golgi apparatus of fixed cells: interaction with endogenous lipids provides a trans-Golgi marker for both light and electron microscopy. J Cell Biol 109:2067–2079
pubmed: 2478562
doi: 10.1083/jcb.109.5.2067
Peachman KK, Rao M, Palmer DR et al (2004) Functional microtubules are required for antigen processing by macrophages and dendritic cells. Immunol Lett 95:13–24
pubmed: 15325793
doi: 10.1016/j.imlet.2004.05.013
Peachman KK, Rao M, Alving CR et al (2005) Human dendritic cells and macrophages exhibit different intracellular processing pathways for soluble and liposome-encapsulated antigens. Immunobiology 210:321–333
pubmed: 16164039
doi: 10.1016/j.imbio.2005.06.002
Pedersen GK, Andersen P, Christensen D (2018) Immunocorrelates of CAF family adjuvants. Semin Immunol 39:4–13
pubmed: 30396811
doi: 10.1016/j.smim.2018.10.003
Perry DG, Martin WJ 2nd (1995) Fluorescent liposomes as quantitative markers of phagocytosis by alveolar macrophages. J Immunol Methods 181:269–285
pubmed: 7538159
doi: 10.1016/0022-1759(95)00011-X
Pick H, Alves AC, Vogel H (2018) Single-vesicle assays using liposomes and cell-derived vesicles: from modeling complex membrane processes to synthetic biology and biomedical applications. Chem Rev 118:8598–8654
pubmed: 30153012
doi: 10.1021/acs.chemrev.7b00777
Porgador A, Yewdell JW, Deng Y et al (1997) Localization, quantitation, and in situ detection of specific peptide-MHC class I complexes using a monoclonal antibody. Immunity 6:715–726
pubmed: 9208844
doi: 10.1016/S1074-7613(00)80447-1
Ramakrishnan A, Schumack NM, Gariepy CL et al (2019a) Correction for Ramakrishnan et al., “Enhanced immunogenicity and protective efficacy of a Campylobacter jejuni conjugate vaccine coadministered with liposomes containing monophosphoryl lipid A and QS-21”. mSphere 4
Ramakrishnan A, Schumack NM, Gariepy CL et al (2019b) Enhanced immunogenicity and protective efficacy of a Campylobacter jejuni conjugate vaccine coadministered with liposomes containing monophosphoryl lipid A and QS-21. mSphere 4
Ramakrishnan A, Schumack NM, Gariepy CL et al (2019c) Erratum for Ramakrishnan et al., “Enhanced immunogenicity and protective efficacy of a Campylobacter jejuni conjugate vaccine coadministered with liposomes containing monophosphoryl lipid A and QS-21”. mSphere 4
Rao M, Alving CR (2000) Delivery of lipids and liposomal proteins to the cytoplasm and Golgi of antigen-presenting cells. mangala.rao@na.amedd.army.mil. Adv Drug Deliv Rev 41:171–188
pubmed: 10699313
doi: 10.1016/S0169-409X(99)00064-2
Rao M, Rothwell SW, Wassef NM et al (1997) Visualization of peptides derived from liposome-encapsulated proteins in the trans-Golgi area of macrophages. Immunol Lett 59:99–105
pubmed: 9373218
doi: 10.1016/S0165-2478(97)00107-7
Rao M, Matyas GR, Grieder F et al (1999a) Cytotoxic T lymphocytes to Ebola Zaire virus are induced in mice by immunization with liposomes containing lipid A. Vaccine 17:2991–2998
pubmed: 10462234
doi: 10.1016/S0264-410X(99)00170-X
Rao M, Rothwell SW, Wassef NM et al (1999b) Trafficking of liposomal antigen to the trans-Golgi of murine macrophages requires both liposomal lipid and liposomal protein. Exp Cell Res 246:203–211
pubmed: 9882529
doi: 10.1006/excr.1998.4274
Rao M, Bray M, Alving CR et al (2002) Induction of immune responses in mice and monkeys to Ebola virus after immunization with liposome-encapsulated irradiated Ebola virus: protection in mice requires CD4(+) T cells. J Virol 76:9176–9185
pubmed: 12186901
pmcid: 136452
doi: 10.1128/JVI.76.18.9176-9185.2002
Rao M, Matyas GR, Vancott TC et al (2004) Immunostimulatory CpG motifs induce CTL responses to HIV type I oligomeric gp140 envelope protein. Immunol Cell Biol 82:523–530
pubmed: 15479438
doi: 10.1111/j.0818-9641.2004.01283.x
Rao M, Peachman KK, Li Q et al (2011) Highly effective generic adjuvant systems for orphan or poverty-related vaccines. Vaccine 29:873–877
pubmed: 21115053
doi: 10.1016/j.vaccine.2010.11.049
Rao M, Onkar S, Peachman KK et al (2018) Liposome-encapsulated human immunodeficiency virus-1 gp120 induces potent V1V2-specific antibodies in humans. J Infect Dis 218:1541–1550
pubmed: 29893872
doi: 10.1093/infdis/jiy348
Reddy R, Zhou F, Huang L et al (1991) pH sensitive liposomes provide an efficient means of sensitizing target cells to class I restricted CTL recognition of a soluble protein. J Immunol Methods 141:157–163
pubmed: 1880423
doi: 10.1016/0022-1759(91)90142-3
Reddy R, Zhou F, Nair S et al (1992) In vivo cytotoxic T lymphocyte induction with soluble proteins administered in liposomes. J Immunol 148:1585–1589
pubmed: 1538138
Roche PA, Cresswell P (1991) Proteolysis of the class II-associated invariant chain generates a peptide binding site in intracellular HLA-DR molecules. Proc Natl Acad Sci U S A 88:3150–3154
pubmed: 2014234
pmcid: 51403
doi: 10.1073/pnas.88.8.3150
Rothwell SW, Wassef NM, Alving CR et al (2000) Proteasome inhibitors block the entry of liposome-encapsulated antigens into the classical MHC class I pathway. Immunol Lett 74:141–152
pubmed: 10996390
doi: 10.1016/S0165-2478(00)00206-6
Schmidt ST, Olsen CL, Franzyk H et al (2019) Comparison of two different PEGylation strategies for the liposomal adjuvant CAF09: towards induction of CTL responses upon subcutaneous vaccine administration. Eur J Pharm Biopharm 140:29–39
pubmed: 31055066
doi: 10.1016/j.ejpb.2019.04.020
Schwendener RA (2014) Liposomes as vaccine delivery systems: a review of the recent advances. Ther Adv Vaccines 2:159–182
pubmed: 25364509
pmcid: 4212474
doi: 10.1177/2051013614541440
Segal AW, Wills EJ, Richmond JE et al (1974) Morphological observations on the cellular and subcellular destination of intravenously administered liposomes. Br J Exp Pathol 55:320–327
pubmed: 4433467
pmcid: 2072651
Seth L, Bingham Ferlez KM, Kaba SA et al (2017) Development of a self-assembling protein nanoparticle vaccine targeting Plasmodium falciparum circumsporozoite protein delivered in three army liposome formulation adjuvants. Vaccine 35:5448–5454
pubmed: 28274638
doi: 10.1016/j.vaccine.2017.02.040
Singh P, Beck Z, Matyas GR et al (2019) Saturated phospholipids are required for nano- to micron-size transformation of cholesterol-containing liposomes upon QS21 addition. J Liposome Res 29:247–250
pubmed: 30350748
doi: 10.1080/08982104.2018.1538239
Smith GE, Flyer DC, Raghunandan R et al (2013) Development of influenza H7N9 virus like particle (VLP) vaccine: homologous A/Anhui/1/2013 (H7N9) protection and heterologous A/chicken/Jalisco/CPA1/2012 (H7N3) cross-protection in vaccinated mice challenged with H7N9 virus. Vaccine 31:4305–4313
pubmed: 23891795
doi: 10.1016/j.vaccine.2013.07.043
Steers NJ, Alving CR, Rao M (2008) Modulation of immunoproteasome subunits by liposomal lipid A. Vaccine 26:2849–2859
pubmed: 18455279
doi: 10.1016/j.vaccine.2008.03.065
Steers NJ, Ratto-Kim S, De Souza MS et al (2012) HIV-1 envelope resistance to proteasomal cleavage: implications for vaccine induced immune responses. PLoS ONE 7:e42579
pubmed: 22880042
pmcid: 3412807
doi: 10.1371/journal.pone.0042579
Stern LJ, Potolicchio I, Santambrogio L (2006) MHC class II compartment subtypes: structure and function. Curr Opin Immunol 18:64–69
pubmed: 16337363
doi: 10.1016/j.coi.2005.11.005
Tyrrell DA, Heath TD, Colley CM et al (1976) New aspects of liposomes. Biochim Biophys Acta 457:259–302
pubmed: 793635
doi: 10.1016/0304-4157(76)90002-2
Uemura K, Nicolotti RA, Six HR et al (1974) Antibody formation in response to liposomal model membranes sensitized with N-substituted phosphatidylethanolamine derivatives. Biochemistry 13:1572–1578
pubmed: 4831348
doi: 10.1021/bi00705a003
Vandepapeliere P (2018) Vaccine compositions comprising a saponin adjuvant, 4 Dec 2018
Verma JN, Wassef NM, Wirtz RA et al (1991) Phagocytosis of liposomes by macrophages: intracellular fate of liposomal malaria antigen. Biochim Biophys Acta 1066:229–238
pubmed: 1854787
doi: 10.1016/0005-2736(91)90191-A
Voltan AR, Alarcon KM, Fusco-Almeida AM et al (2017) Highlights in endocytosis of nanostructured systems. Curr Med Chem 24:1909–1929
pubmed: 28201970
doi: 10.2174/0929867324666170214111205
Vu VP, Gifford GB, Chen F et al (2019) Immunoglobulin deposition on biomolecule corona determines complement opsonization efficiency of preclinical and clinical nanoparticles. Nat Nanotechnol 14:260–268
pubmed: 30643271
pmcid: 6402998
doi: 10.1038/s41565-018-0344-3
Wagner A, Vorauer-Uhl K (2011) Liposome technology for industrial purposes. J Drug Deliv 2011:591325
pubmed: 21490754
doi: 10.1155/2011/591325
Waite DC, Jacobson EW, Ennis FA et al (2001) Three double-blind, randomized trials evaluating the safety and tolerance of different formulations of the saponin adjuvant QS-21. Vaccine 19:3957–3967
pubmed: 11427271
doi: 10.1016/S0264-410X(01)00142-6
Wang N, Chen M, Wang T (2019) Liposomes used as a vaccine adjuvant-delivery system: from basics to clinical immunization. J Control Release 303:130–150
pubmed: 31022431
pmcid: 7111479
doi: 10.1016/j.jconrel.2019.04.025
Wassef NM, Alving CR (1987) Complement-dependent phagocytosis of liposomes by macrophages. Methods Enzymol 149:124–134
pubmed: 3695956
doi: 10.1016/0076-6879(87)49050-2
Welsby I, Detienne S, N’kuli F et al (2016) Lysosome-dependent activation of human dendritic cells by the vaccine adjuvant QS-21. Front Immunol 7:663
pubmed: 28105029
White K, Krzych U, Gordon DM et al (1993) Induction of cytolytic and antibody responses using Plasmodium falciparum repeatless circumsporozoite protein encapsulated in liposomes. Vaccine 11:1341–1346
pubmed: 7507624
doi: 10.1016/0264-410X(93)90105-7
White WI, Cassatt DR, Madsen J et al (1995) Antibody and cytotoxic T-lymphocyte responses to a single liposome-associated peptide antigen. Vaccine 13:1111–1122
pubmed: 7491819
doi: 10.1016/0264-410X(94)00058-U
Wieczorek L, Krebs SJ, Kalyanaraman V et al (2015) Comparable antigenicity and immunogenicity of oligomeric forms of a novel, acute HIV-1 Subtype C gp145 envelope for use in preclinical and clinical vaccine research. J Virol 89:7478–7493
pubmed: 25972551
pmcid: 4505676
doi: 10.1128/JVI.00412-15
World Health Organization (2018) Malaria vaccine: WHO position paper, January 2016—recommendations. Vaccine 36:3576–3577
doi: 10.1016/j.vaccine.2016.10.047
Young JF, Hockmeyer WT, Gross M et al (1985) Expression of Plasmodium falciparum circumsporozoite proteins in Escherichia coli for potential use in a human malaria vaccine. Science 228:958–962
pubmed: 2988125
doi: 10.1126/science.2988125
Young JF, Ballou WR, Hockmeyer WT (1987) Developing a human malaria sporozoite vaccine. Microb Pathog 2:237–240
pubmed: 3333800
doi: 10.1016/0882-4010(87)90121-5
Zhou F, Watkins SC, Huang L (1994) Characterization and kinetics of MHC class I-restricted presentation of a soluble antigen delivered by liposomes. Immunobiology 190:35–52
pubmed: 8082886
doi: 10.1016/S0171-2985(11)80282-2
Zurbriggen R (2003) Immunostimulating reconstituted influenza virosomes. Vaccine 21:921–924
pubmed: 12547603
doi: 10.1016/S0264-410X(02)00541-8