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Current Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 0929-8673
ISSN (Online): 1875-533X

General Review Article

Lipids as Activators of Innate Immunity in Peptide Vaccine Delivery

Author(s): Stacey Bartlett, Mariusz Skwarczynski* and Istvan Toth

Volume 27, Issue 17, 2020

Page: [2887 - 2901] Pages: 15

DOI: 10.2174/0929867325666181026100849

Price: $65

Abstract

Background: Innate immune system plays an important role in pathogen detection and the recognition of vaccines, mainly through pattern recognition receptors (PRRs) that identify pathogen components (danger signals). One of the typically recognised bacterial components are lipids in conjugation with peptides, proteins and saccharides. Lipidic compounds are readily recognised by the immune system, and thus are ideal candidates for peptide- based vaccine delivery. Thus, bacterial or synthetic lipids mixed with, or conjugated to, antigens have shown adjuvant properties. These systems have many advantages over traditional adjuvants, including low toxicity and good efficacy for stimulating mucosal and systemic immune responses.

Methods: The most recent literature on the role of lipids in stimulation of immune responses was selected for this review. The vast majority of reviewed papers were published in the last decade. Older but significant findings are also cited.

Results: This review focuses on the development of lipopeptide vaccine systems including application of palmitic acid, bacterial lipopeptides, glycolipids and the lipid core peptide and their routes of administration. The use of liposomes as a delivery system that incorporates lipopeptides is discussed. The review also includes a brief description of immune system in relation to vaccinology and discussion on vaccine delivery routes.

Conclusion: Lipids and their conjugates are an ideal frontrunner in the development of safe and efficient vaccines for different immunisation routes.

Keywords: Peptide-based vaccine, lipid, lipopeptide vaccine, mucosal immunity, liposome, innate immune system.

[1]
Cheever, M.A.; Higano, C.S. PROVENGE (Sipuleucel-T) in prostate cancer: the first FDA-approved therapeutic cancer vaccine. Clin. Cancer Res., 2011, 17(11), 3520-3526.
[http://dx.doi.org/10.1158/1078-0432.CCR-10-3126] [PMID: 21471425]
[2]
Greig, S.L. Talimogene Laherparepvec: First Global Approval. Drugs, 2016, 76(1), 147-154.
[http://dx.doi.org/10.1007/s40265-015-0522-7] [PMID: 26620366]
[3]
Zimet, G.D.; Shew, M.L.; Kahn, J.A. Appropriate use of cervical cancer vaccine. Annu. Rev. Med., 2008, 59, 223-236.
[http://dx.doi.org/10.1146/annurev.med.59.092806.131644] [PMID: 18186704]
[4]
Ott, P.A.; Hodi, F.S. Talimogene laherparepvec for the treatment of advanced melanoma. Clin. Cancer Res., 2016, 22(13), 3127-3131.
[http://dx.doi.org/10.1158/1078-0432.CCR-15-2709] [PMID: 27146699]
[5]
Delany, I.; Rappuoli, R.; De Gregorio, E. Vaccines for the 21st century. EMBO Mol. Med., 2014, 6(6), 708-720.
[http://dx.doi.org/10.1002/emmm.201403876] [PMID: 24803000]
[6]
Tomori, O. From smallpox eradication to the future of global health: innovations, application and lessons for future eradication and control initiatives. Vaccine, 2011, 29(4)(Suppl. 4), D145-D148.
[http://dx.doi.org/10.1016/j.vaccine.2011.09.003] [PMID: 22185830]
[7]
Skwarczynski, M.; Toth, I. Peptide-based synthetic vaccines. Chem. Sci. (Camb.), 2016, 7(2), 842-854.
[http://dx.doi.org/10.1039/C5SC03892H] [PMID: 28791117]
[8]
Matthews, L.J.; Davis, R.; Smith, G.P. Immunogenically fit subunit vaccine components via epitope discovery from natural peptide libraries. J. immunol., (Baltimore, Md.: 1950), 2002, 169(2), 837-846.
[9]
Toth, I.; Simerska, P.; Fujita, Y. Recent advances in design and synthesis of self-adjuvanting lipopeptide vaccines. Int. J. Pept. Res. Ther., 2008, 14(4), 333-340.
[http://dx.doi.org/10.1007/s10989-008-9147-y]
[10]
Nevagi, R.; Toth, I.; Skwarczynski, M. Peptide-based Vaccines in Peptide applications in biomedicine, biotechnology and bioengineering; Sotirios, Koutsopoulos., Ed.; Elsevier Inc.: Oxford: United Kingdom, 2018, pp. 327-358.
[http://dx.doi.org/10.1016/B978-0-08-100736-5.00012-0]
[11]
Singh, M.; O’Hagan, D.T. Recent advances in vaccine adjuvants. Pharm. Res., 2002, 19(6), 715-728.
[http://dx.doi.org/10.1023/A:1016104910582] [PMID: 12134940]
[12]
Petrovsky, N.; Aguilar, J.C. Vaccine adjuvants: current state and future trends. Immunol. Cell Biol., 2004, 82(5), 488-496.
[http://dx.doi.org/10.1111/j.0818-9641.2004.01272.x] [PMID: 15479434]
[13]
Azmi, F.; Ahmad Fuaad, A.A.; Skwarczynski, M.; Toth, I. Recent progress in adjuvant discovery for peptide-based subunit vaccines. Hum. Vaccin. Immunother., 2014, 10(3), 778-796.
[http://dx.doi.org/10.4161/hv.27332] [PMID: 24300669]
[14]
Gupta, R.K.; Relyveld, E.H.; Lindblad, E.B.; Bizzini, B.; Ben-Efraim, S.; Gupta, C.K. Adjuvants--a balance between toxicity and adjuvanticity. Vaccine, 1993, 11(3), 293-306.
[http://dx.doi.org/10.1016/0264-410X(93)90190-9] [PMID: 8447157]
[15]
Pérez, O.; Romeu, B.; Cabrera, O.; González, E.; Batista-Duharte, A.; Labrada, A.; Pérez, R.; Reyes, L.M.; Ramírez, W.; Sifontes, S.; Fernández, N.; Lastre, M. Adjuvants are key factors for the development of future vaccines: lessons from the finlay adjuvant platform. Front. Immunol., 2013, 4, 407.
[http://dx.doi.org/10.3389/fimmu.2013.00407] [PMID: 24348475]
[16]
Brewer, J.M.; Conacher, M.; Satoskar, A.; Bluethmann, H.; Alexander, J. In interleukin-4-deficient mice, alum not only generates T helper 1 responses equivalent to freund’s complete adjuvant, but continues to induce T helper 2 cytokine production. Eur. J. Immunol., 1996, 26(9), 2062-2066.
[http://dx.doi.org/10.1002/eji.1830260915] [PMID: 8814247]
[17]
Schirmbeck, R.; Melber, K.; Mertens, T.; Reimann, J. Antibody and cytotoxic T-cell responses to soluble hepatitis B virus (HBV) S antigen in mice: implication for the pathogenesis of HBV-induced hepatitis. J. Virol., 1994, 68(3), 1418-1425.
[http://dx.doi.org/10.1128/JVI.68.3.1418-1425.1994] [PMID: 8107205]
[18]
Zaman, M.; Chandrudu, S.; Toth, I. Strategies for intranasal delivery of vaccines. Drug Deliv. Transl. Res., 2013, 3(1), 100-109.
[http://dx.doi.org/10.1007/s13346-012-0085-z] [PMID: 23316448]
[19]
Moschos, S.A.; Bramwell, V.W.; Somavarapu, S.; Alpar, H.O. Adjuvant synergy: the effects of nasal coadministration of adjuvants. Immunol. Cell Biol., 2004, 82(6), 628-637.
[http://dx.doi.org/10.1111/j.0818-9641.2004.01280.x] [PMID: 15550121]
[20]
Skwarczynski, M.; Toth, I. Recent advances in peptide-based subunit nanovaccines. Nanomedicine (Lond.), 2014, 9(17), 2657-2669.
[http://dx.doi.org/10.2217/nnm.14.187] [PMID: 25529569]
[21]
Banchereau, J.; Palucka, A.K. Dendritic cells as therapeutic vaccines against cancer. Nat. Rev. Immunol., 2005, 5(4), 296-306.
[http://dx.doi.org/10.1038/nri1592] [PMID: 15803149]
[22]
Banchereau, J.; Steinman, R.M. Dendritic cells and the control of immunity. Nature, 1998, 392(6673), 245-252.
[http://dx.doi.org/10.1038/32588] [PMID: 9521319]
[23]
De Temmerman, M-L.; Rejman, J.; Demeester, J.; Irvine, D.J.; Gander, B.; De Smedt, S.C. Particulate vaccines: on the quest for optimal delivery and immune response. Drug Discov. Today, 2011, 16(13-14), 569-582.
[http://dx.doi.org/10.1016/j.drudis.2011.04.006] [PMID: 21570475]
[24]
Hussein, W.M.; Liu, T-Y.; Skwarczynski, M.; Toth, I. Toll-like receptor agonists: a patent review (2011 - 2013). Expert Opin. Ther. Pat., 2014, 24(4), 453-470.
[http://dx.doi.org/10.1517/13543776.2014.880691] [PMID: 24456079]
[25]
Rosa, D.S.; Ribeiro, S.P.; Cunha-Neto, E. CD4+ T cell epitope discovery and rational vaccine design. Arch. Immunol. Ther. Exp. (Warsz.), 2010, 58(2), 121-130.
[http://dx.doi.org/10.1007/s00005-010-0067-0] [PMID: 20155490]
[26]
Marasini, N.; Skwarczynski, M.; Toth, I. Oral delivery of nanoparticle-based vaccines. Expert Rev. Vaccines, 2014, 13(11), 1361-1376.
[http://dx.doi.org/10.1586/14760584.2014.936852] [PMID: 25155636]
[27]
Kraan, H.; Vrieling, H.; Czerkinsky, C.; Jiskoot, W.; Kersten, G.; Amorij, J-P. Buccal and sublingual vaccine delivery. J. Control. Release, 2014, 190, 580-592.
[http://dx.doi.org/10.1016/j.jconrel.2014.05.060] [PMID: 24911355]
[28]
Neutra, M.R.; Kozlowski, P.A. Mucosal vaccines: the promise and the challenge. Nat. Rev. Immunol., 2006, 6(2), 148-158.
[http://dx.doi.org/10.1038/nri1777] [PMID: 16491139]
[29]
Holmgren, J.; Czerkinsky, C. Mucosal immunity and vaccines. Nat. Med., 2005, 11(4)(Suppl.), S45-S53.
[http://dx.doi.org/10.1038/nm1213] [PMID: 15812489]
[30]
Marasini, N.; Giddam, A.K.; Ghaffar, K.A.; Batzloff, M.R.; Good, M.F.; Skwarczynski, M.; Toth, I. Multilayer engineered nanoliposomes as a novel tool for oral delivery of lipopeptide-based vaccines against group A Streptococcus. Nanomedicine (Lond.), 2016, 11(10), 1223-1236.
[http://dx.doi.org/10.2217/nnm.16.36] [PMID: 27077314]
[31]
Han, M.; Watarai, S.; Kobayashi, K.; Yasuda, T. Application of liposomes for development of oral vaccines: study of in vitro stability of liposomes and antibody response to antigen associated with liposomes after oral immunization. J. Vet. Med. Sci., 1997, 59(12), 1109-1114.
[http://dx.doi.org/10.1292/jvms.59.1109] [PMID: 9450240]
[32]
Zhong, W.; Skwarczynski, M.; Toth, I. Lipid core peptide system for gene, drug and vaccine delivery. Aust. J. Chem., 2009, 62(9), 956-967.
[http://dx.doi.org/10.1071/CH09149]
[33]
Skwarczynski, M.; Zaman, M.; Toth, I. Handbook of the Biologically Active Peptides, the, 2nd ed; Kastin, A., Ed.; Elsevier Inc: Burlington, 2013, pp. 571-579.
[http://dx.doi.org/10.1016/B978-0-12-385095-9.00078-6]
[34]
Kovacs-Simon, A.; Titball, R.W.; Michell, S.L. Lipoproteins of bacterial pathogens. Infect. Immun., 2011, 79(2), 548-561.
[http://dx.doi.org/10.1128/IAI.00682-10] [PMID: 20974828]
[35]
Moyle, P.M.; Toth, I. Self-adjuvanting lipopeptide vaccines. Curr. Med. Chem., 2008, 15(5), 506-516.
[http://dx.doi.org/10.2174/092986708783503249] [PMID: 18289006]
[36]
Vitiello, A.; Ishioka, G.; Grey, H.M.; Rose, R.; Farness, P.; LaFond, R.; Yuan, L.; Chisari, F.V.; Furze, J.; Bartholomeuz, R. Development of a lipopeptide-based therapeutic vaccine to treat chronic HBV infection. I. Induction of a primary cytotoxic T lymphocyte response in humans. J. Clin. Invest., 1995, 95(1), 341-349.
[http://dx.doi.org/10.1172/JCI117662] [PMID: 7814635]
[37]
Gahéry-Ségard, H.; Pialoux, G.; Charmeteau, B.; Sermet, S.; Poncelet, H.; Raux, M.; Tartar, A.; Lévy, J-P.; Gras-Masse, H.; Guillet, J-G. Multiepitopic B- and T-cell responses induced in humans by a human immunodeficiency virus type 1 lipopeptide vaccine. J. Virol., 2000, 74(4), 1694-1703.
[http://dx.doi.org/10.1128/JVI.74.4.1694-1703.2000] [PMID: 10644339]
[38]
Renaudet, O.; Dasgupta, G.; Bettahi, I.; Shi, A.; Nesburn, A.B.; Dumy, P.; BenMohamed, L. Linear and branched glyco-lipopeptide vaccines follow distinct cross-presentation pathways and generate different magnitudes of antitumor immunity. PLoS One, 2010, 5(6) e11216
[http://dx.doi.org/10.1371/journal.pone.0011216] [PMID: 20574522]
[39]
Zhang, X.; Chentoufi, A.A.; Dasgupta, G.; Nesburn, A.B.; Wu, M.; Zhu, X.; Carpenter, D.; Wechsler, S.L.; You, S.; BenMohamed, L. A genital tract peptide epitope vaccine targeting TLR-2 efficiently induces local and systemic CD8+ T cells and protects against herpes simplex virus type 2 challenge. Mucosal Immunol., 2009, 2(2), 129-143.
[http://dx.doi.org/10.1038/mi.2008.81] [PMID: 19129756]
[40]
Hayashi, S.; Wu, H.C. Lipoproteins in bacteria. J. Bioenerg. Biomembr., 1990, 22(3), 451-471.
[http://dx.doi.org/10.1007/BF00763177] [PMID: 2202727]
[41]
Wiesmüller, K.H.; Jung, G.; Hess, G. Novel low-molecular-weight synthetic vaccine against foot-and-mouth disease containing a potent B-cell and macrophage activator. Vaccine, 1989, 7(1), 29-33.
[http://dx.doi.org/10.1016/0264-410X(89)90007-8] [PMID: 2470215]
[42]
Zeng, W.; Ghosh, S.; Lau, Y.F.; Brown, L.E.; Jackson, D.C. Highly immunogenic and totally synthetic lipopeptides as self-adjuvanting immunocontraceptive vaccines. J. Immunol., 2002, 169(9), 4905-4912.
[http://dx.doi.org/10.4049/jimmunol.169.9.4905] [PMID: 12391202]
[43]
Chua, B.Y.; Eriksson, E.M.; Brown, L.E.; Zeng, W.; Gowans, E.J.; Torresi, J.; Jackson, D.C. A self-adjuvanting lipopeptide-based vaccine candidate for the treatment of hepatitis C virus infection. Vaccine, 2008, 26(37), 4866-4875.
[http://dx.doi.org/10.1016/j.vaccine.2008.03.032] [PMID: 18455278]
[44]
Gowthaman, U.; Singh, V.; Zeng, W.; Jain, S.; Siddiqui, K.F.; Chodisetti, S.B.; Gurram, R.K.; Parihar, P.; Gupta, P.; Gupta, U.D.; Jackson, D.C.; Agrewala, J.N. Promiscuous peptide of 16 kDa antigen linked to Pam2Cys protects against Mycobacterium tuberculosis by evoking enduring memory T-cell response. J. Infect. Dis., 2011, 204(9), 1328-1338.
[http://dx.doi.org/10.1093/infdis/jir548] [PMID: 21933875]
[45]
Jackson, D.C.; Lau, Y.F.; Le, T.; Suhrbier, A.; Deliyannis, G.; Cheers, C.; Smith, C.; Zeng, W.; Brown, L.E. A totally synthetic vaccine of generic structure that targets Toll-like receptor 2 on dendritic cells and promotes antibody or cytotoxic T cell responses. Proc. Natl. Acad. Sci. USA, 2004, 101(43), 15440-15445.
[http://dx.doi.org/10.1073/pnas.0406740101] [PMID: 15489266]
[46]
Moyle, P.M.; Dai, W.; Zhang, Y.; Batzloff, M.R.; Good, M.F.; Toth, I. Site-specific incorporation of three toll-like receptor 2 targeting adjuvants into semisynthetic, molecularly defined nanoparticles: application to group a streptococcal vaccines. Bioconjug. Chem., 2014, 25(5), 965-978.
[http://dx.doi.org/10.1021/bc500108b] [PMID: 24712905]
[47]
Hussein, W.M.; Liu, T-Y.; Maruthayanar, P.; Mukaida, S.; Moyle, P.M.; Wells, J.W.; Toth, I.; Skwarczynski, M. Double conjugation strategy to incorporate lipid adjuvants into multiantigenic vaccines. Chem. Sci. (Camb.), 2016, 7(3), 2308-2321.
[http://dx.doi.org/10.1039/C5SC03859F] [PMID: 29910921]
[48]
Hussein, W.M.; Mukaida, S.; Azmi, F.; Bartlett, S.; Olivier, C.; Batzloff, M.R.; Good, M.F.; Skwarczynski, M.; Toth, I. Comparison of fluorinated and nonfluorinated lipids in self-adjuvanting delivery systems for peptide-based vaccines. ACS Med. Chem. Lett., 2017, 8(2), 227-232.
[http://dx.doi.org/10.1021/acsmedchemlett.6b00453] [PMID: 28197317]
[49]
Fagan, V.; Hussein, W.M.; Su, M.; Giddam, A.K.; Batzloff, M.R.; Good, M.F.; Toth, I.; Simerska, P. Synthesis, characterization and immunological evaluation of self-adjuvanting Group A Streptococcal vaccine candidates bearing various lipidic adjuvanting moieties. ChemBioChem, 2017, 18(6), 545-553.
[http://dx.doi.org/10.1002/cbic.201600639] [PMID: 28075053]
[50]
Steimle, A.; Autenrieth, I.B.; Frick, J-S. Structure and function: Lipid A modifications in commensals and pathogens. Int. J. Med. Microbiol., 2016, 306(5), 290-301.
[http://dx.doi.org/10.1016/j.ijmm.2016.03.001] [PMID: 27009633]
[51]
Fox, C.B.; Friede, M.; Reed, S.G.; Ireton, G.C. Endotoxins: Structure, Function and Recognition; Wang, X; Quinn, P.J., Ed.; Springer: New York, 2010, Vol. 53, pp. 303-321.
[http://dx.doi.org/10.1007/978-90-481-9078-2_14]
[52]
Casella, C.R.; Mitchell, T.C. Putting endotoxin to work for us: monophosphoryl lipid A as a safe and effective vaccine adjuvant. Cell. Mol. Life Sci., 2008, 65(20), 3231-3240.
[http://dx.doi.org/10.1007/s00018-008-8228-6] [PMID: 18668203]
[53]
Nevagi, R.J.; Toth, I.; Skwarczynski, M. Peptide Applications in Biomedicine, Biotechnology and Bioengineering; Koutsopoulos, S., Ed.; Woodhead Publishing, 2018, pp. 327-358.
[http://dx.doi.org/10.1016/B978-0-08-100736-5.00012-0]
[54]
Fujita, Y.; Abdel-Aal, A-B.M.; Wimmer, N.; Batzloff, M.R.; Good, M.F.; Toth, I. Synthesis and immunological evaluation of self-adjuvanting glycolipopeptide vaccine candidates. Bioorg. Med. Chem., 2008, 16(19), 8907-8913.
[http://dx.doi.org/10.1016/j.bmc.2008.08.064] [PMID: 18789866]
[55]
Toth, I.; Danton, M.; Flinn, N.; Gibbons, W.A. A combined adjuvant and carrier system for enhancing synthetic peptides immunogenicity utilising lipidic amino acids. Tetrahedron Lett., 1993, 34(24), 3925-3928.
[http://dx.doi.org/10.1016/S0040-4039(00)79265-3]
[56]
Olive, C.; Batzloff, M.; Horváth, A.; Clair, T.; Yarwood, P.; Toth, I.; Good, M.F. Potential of lipid core peptide technology as a novel self-adjuvanting vaccine delivery system for multiple different synthetic peptide immunogens. Infect. Immun., 2003, 71(5), 2373-2383.
[http://dx.doi.org/10.1128/IAI.71.5.2373-2383.2003] [PMID: 12704107]
[57]
Moyle, P.M.; Olive, C.; Karpati, L.; Barozzi, N.; Ho, M-F.; Dyer, J.; Sun, H.K.; Good, M.; Toth, I. Synthesis and immunological evaluation of M protein targeted tetra-valent and tri-valent group A streptococcal vaccine candidates based on the lipid-core peptide system. Int. J. Pept. Res. Ther., 2006, 12(3), 317-326.
[http://dx.doi.org/10.1007/s10989-006-9021-8]
[58]
Fuaad, A.A.; Skwarczynski, M.; Toth, I. The use of microwave-assisted solid-phase peptide synthesis and click chemistry for the synthesis of vaccine candidates against hookworm infection. Methods Mol. Biol., 2016, 1403, 639-653.
[http://dx.doi.org/10.1007/978-1-4939-3387-7_36] [PMID: 27076158]
[59]
Skwarczynski, M.; Toth, I. Lipid-core-peptide system for self-adjuvanting synthetic vaccine delivery.Bioconjugation Protocols; Mark, S.S., Ed.; Humana Press, 2011, Vol. 751, pp. 297-308.
[http://dx.doi.org/10.1007/978-1-61779-151-2_18]
[60]
Zhong, G.; Toth, I.; Reid, R.; Brunham, R.C. Immunogenicity evaluation of a lipidic amino acid-based synthetic peptide vaccine for Chlamydia trachomatis. Journal of immunology (Baltimore, Md: 1950), 1993, 151(7), 3728-3736.
[PMID: 7690812]
[61]
Ahmad Fuaad, A.A.; Roubille, R.; Pearson, M.S.; Pickering, D.A.; Loukas, A.C.; Skwarczynski, M.; Toth, I. The use of a conformational cathepsin D-derived epitope for vaccine development against Schistosoma mansoni. Bioorg. Med. Chem., 2015, 23(6), 1307-1312.
[http://dx.doi.org/10.1016/j.bmc.2015.01.033] [PMID: 25684420]
[62]
Zaman, M.; Chandrudu, S.; Giddam, A.K.; Reiman, J.; Skwarczynski, M.; McPhun, V.; Moyle, P.M.; Batzloff, M.R.; Good, M.F.; Toth, I.; Group, A. Group A Streptococcal vaccine candidate: contribution of epitope to size, antigen presenting cell interaction and immunogenicity. Nanomedicine (Lond.), 2014, 9(17), 2613-2624.
[http://dx.doi.org/10.2217/nnm.14.190] [PMID: 25529566]
[63]
Fuaad, A.A.H.A.; Pearson, M.S.; Pickering, D.A.; Becker, L.; Zhao, G.; Loukas, A.C.; Skwarczynski, M.; Toth, I. Lipopeptide nanoparticles: development of vaccines against hookworm parasite. Chem. Med. Chem., 2015, 10(10), 1647-1654.
[http://dx.doi.org/10.1002/cmdc.201500227] [PMID: 26269385]
[64]
Abdel-Aal, A-B.M.; Batzloff, M.R.; Fujita, Y.; Barozzi, N.; Faria, A.; Simerska, P.; Moyle, P.M.; Good, M.F.; Toth, I. Structure-activity relationship of a series of synthetic lipopeptide self-adjuvanting group a streptococcal vaccine candidates. J. Med. Chem., 2008, 51(1), 167-172.
[http://dx.doi.org/10.1021/jm701091d] [PMID: 18072728]
[65]
Chan, A.; Hussein, W.M.; Ghaffar, K.A.; Marasini, N.; Mostafa, A.; Eskandari, S.; Batzloff, M.R.; Good, M.F.; Skwarczynski, M.; Toth, I. Structure-activity relationship of lipid core peptide-based Group A Streptococcus vaccine candidates. Bioorg. Med. Chem., 2016, 24(14), 3095-3101.
[http://dx.doi.org/10.1016/j.bmc.2016.03.063] [PMID: 27246859]
[66]
Zaman, M.; Abdel-Aal, A-B.M.; Fujita, Y.; Ziora, Z.M.; Batzloff, M.R.; Good, M.F.; Toth, I. Structure-activity relationship for the development of a self-adjuvanting mucosally active lipopeptide vaccine against Streptococcus pyogenes. J. Med. Chem., 2012, 55(19), 8515-8523.
[http://dx.doi.org/10.1021/jm301074n] [PMID: 22974133]
[67]
Zhao, G.; Chandrudu, S.; Skwarczynski, M.; Toth, I. The application of self-assembled nanostructures in peptide-based subunit vaccine development. Eur. Polym. J., 2017, 93, 670-681.
[http://dx.doi.org/10.1016/j.eurpolymj.2017.02.014] [PMID: 32226094]
[68]
Skwarczynski, M.; Parhiz, B.H.; Soltani, F.; Srinivasan, S.; Kamaruzaman, K.A.; Lin, I-C.; Toth, I. Lipid peptide core nanoparticles as multivalent vaccine candidates against Streptococcus pyogenes. Aust. J. Chem., 2012, 65, 35-39.
[http://dx.doi.org/10.1071/CH11292]
[69]
Azmi, F.; Ahmad Fuaad, A.A.; Giddam, A.K.; Batzloff, M.R.; Good, M.F.; Skwarczynski, M.; Toth, I. Self-adjuvanting vaccine against group A streptococcus: application of fibrillized peptide and immunostimulatory lipid as adjuvant. Bioorg. Med. Chem., 2014, 22(22), 6401-6408.
[http://dx.doi.org/10.1016/j.bmc.2014.09.042] [PMID: 25438764]
[70]
Marasini, N.; Giddam, A.K.; Khalil, Z.G.; Hussein, W.M.; Capon, R.J.; Batzloff, M.R.; Good, M.F.; Toth, I.; Skwarczynski, M. Double adjuvanting strategy for peptide-based vaccines: trimethyl chitosan nanoparticles for lipopeptide delivery. Nanomedicine (Lond.), 2016, 11(24), 3223-3235.
[http://dx.doi.org/10.2217/nnm-2016-0291] [PMID: 27830630]
[71]
Marasini, N.; Giddam, A.K.; Batzloff, M.R.; Good, M.F.; Skwarczynski, M.; Toth, I. Poly-L-lysine-coated nanoparticles are ineffective in inducing mucosal immunity against group A Streptococcus. Biochemical Compounds, 2017, 5(1), 1.
[http://dx.doi.org/10.7243/2052-9341-5-1]
[72]
Marasini, N.; Khalil, Z.G.; Giddam, A.K.; Ghaffar, K.A.; Hussein, W.M.; Capon, R.J.; Batzloff, M.R.; Good, M.F.; Skwarczynski, M.; Toth, I. Lipid core peptide/poly(lactic-co-glycolic acid) as a highly potent intranasal vaccine delivery system against Group A streptococcus. Int. J. Pharm., 2016, 513(1-2), 410-420.
[http://dx.doi.org/10.1016/j.ijpharm.2016.09.057] [PMID: 27659862]
[73]
Giddam, A.K.; Zaman, M.; Skwarczynski, M.; Toth, I. Liposome-based delivery system for vaccine candidates: constructing an effective formulation. Nanomedicine (Lond.), 2012, 7(12), 1877-1893.
[http://dx.doi.org/10.2217/nnm.12.157] [PMID: 23249332]
[74]
Ghaffar, K.A.; Giddam, A.K.; Zaman, M.; Skwarczynski, M.; Toth, I. Liposomes as nanovaccine delivery systems. Curr. Top. Med. Chem., 2014, 14(9), 1194-1208.
[http://dx.doi.org/10.2174/1568026614666140329232757] [PMID: 24678703]
[75]
Gregoriadis, G. Engineering liposomes for drug delivery: progress and problems. Trends Biotechnol., 1995, 13(12), 527-537.
[http://dx.doi.org/10.1016/S0167-7799(00)89017-4] [PMID: 8595139]
[76]
Chang, D-K.; Chiu, C-Y.; Kuo, S-Y.; Lin, W-C.; Lo, A.; Wang, Y-P.; Li, P-C.; Wu, H-C. Antiangiogenic targeting liposomes increase therapeutic efficacy for solid tumors. J. Biol. Chem., 2009, 284(19), 12905-12916.
[http://dx.doi.org/10.1074/jbc.M900280200] [PMID: 19276080]
[77]
Immordino, M.L.; Dosio, F.; Cattel, L. Stealth liposomes: review of the basic science, rationale, and clinical applications, existing and potential. Int. J. Nanomedicine, 2006, 1(3), 297-315.
[PMID: 17717971]
[78]
Baca-Estrada, M.E.; Foldvari, M.; Snider, M.; van Drunen Littel-van den Hurk, S.; Babiuk, L.A. Effect of IL-4 and IL-12 liposomal formulations on the induction of immune response to bovine herpesvirus type-1 glycoprotein D. Vaccine, 1997, 15(16), 1753-1760.
[http://dx.doi.org/10.1016/S0264-410X(97)00111-4] [PMID: 9364679]
[79]
Demana, P.H.; Fehske, C.; White, K.; Rades, T.; Hook, S. Effect of incorporation of the adjuvant Quil A on structure and immune stimulatory capacity of liposomes. Immunol. Cell Biol., 2004, 82(5), 547-554.
[http://dx.doi.org/10.1111/j.0818-9641.2004.01276.x] [PMID: 15479441]
[80]
Engler, O.B.; Schwendener, R.A.; Dai, W.J.; Wölk, B.; Pichler, W.; Moradpour, D.; Brunner, T.; Cerny, A. 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, 2004, 23(1), 58-68.
[http://dx.doi.org/10.1016/j.vaccine.2004.05.009] [PMID: 15519708]
[81]
Ghaffar, K.A.; Marasini, N.; Giddam, A.K.; Batzloff, M.R.; Good, M.F.; Skwarczynski, M.; Toth, I. Liposome-based intranasal delivery of lipopeptide vaccine candidates against group A streptococcus. Acta Biomater., 2016, 41, 161-168.
[http://dx.doi.org/10.1016/j.actbio.2016.04.012] [PMID: 27063491]
[82]
Bachmann, M.F.; Jennings, G.T. Vaccine delivery: a matter of size, geometry, kinetics and molecular patterns. Nat. Rev. Immunol., 2010, 10(11), 787-796.
[http://dx.doi.org/10.1038/nri2868] [PMID: 20948547]
[83]
Ghaffar, K.A.; Marasini, N.; Giddam, A.K.; Batzloff, M.R.; Good, M.F.; Skwarczynski, M.; Toth, I. The role of size in development of mucosal liposome-lipopeptide vaccine candidates against group A Streptococcus. Med. Chem., 2016, 13(1), 22-27.
[http://dx.doi.org/10.2174/1573406412666160720093138] [PMID: 27449794]
[84]
Hanson, M.C.; Abraham, W.; Crespo, M.P.; Chen, S.H.; Liu, H.; Szeto, G.L.; Kim, M.; Reinherz, E.L.; Irvine, D.J. Liposomal vaccines incorporating molecular adjuvants and intrastructural T-cell help promote the immunogenicity of HIV membrane-proximal external region peptides. Vaccine, 2015, 33(7), 861-868.
[http://dx.doi.org/10.1016/j.vaccine.2014.12.045] [PMID: 25559188]
[85]
Kelly, C.; Jefferies, C.; Cryan, S-A. Targeted liposomal drug delivery to monocytes and macrophages. J. Drug Deliv., 2011, 2011 727241
[http://dx.doi.org/10.1155/2011/727241] [PMID: 21512579]
[86]
Giddam, A.K.; Reiman, J.M.; Zaman, M.; Skwarczynski, M.; Toth, I.; Good, M.F. A semi-synthetic whole parasite vaccine designed to protect against blood stage malaria. Acta Biomater., 2016, 44, 295-303.
[http://dx.doi.org/10.1016/j.actbio.2016.08.020] [PMID: 27544810]

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