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Current Drug Delivery

Editor-in-Chief

ISSN (Print): 1567-2018
ISSN (Online): 1875-5704

Review Article

Carbohydrates in Vaccine Development

Author(s): Salwa Aljohani, Waleed M. Hussein, Istvan Toth and Pavla Simerska*

Volume 16, Issue 7, 2019

Page: [609 - 617] Pages: 9

DOI: 10.2174/1567201816666190702153612

Price: $65

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Abstract

Despite advances in the development of new vaccines, there are still some diseases with no vaccine solutions. Therefore, further efforts are required to more comprehensively discern the different antigenic components of these microorganisms on a molecular level. This review summarizes advancement in the development of new carbohydrate-based vaccines. Following traditional vaccine counterparts, the carbohydrate-based vaccines introduced a new approach in fighting infectious diseases. Carbohydrates have played various roles in the development of carbohydrate-based vaccines, which are described in this review, including carbohydrates acting as antigens, carriers or targeting moieties. Carbohydrate-based vaccines against infectious diseases, such as group A streptococcus, meningococcal meningitis and human immunodeficiency virus, are also discussed. A number of carbohydrate- based vaccines, such as Pneumovax 23, Menveo and Pentacel, have been successfully marketed in the past few years and there is a promising standpoint for many more to come in the near future.

Keywords: Carbohydrates, vaccines, glycans, polysaccharides, glycoconjugates, immunity.

Graphical Abstract
[1]
Plotkin, S.A.; Orenstein, W.A.; Offit, P.A. Vaccines, 6th Ed.,; Elsevier, 2013.
[2]
Reche, P.A.; Fernandez-Caldas, E.; Flower, D.R.; Fridkis-Hareli, M.; Hoshino, Y. Peptide-based immunotherapeutics and vaccines. J. Immunol. Res., 2014.2014256784
[http://dx.doi.org/10.1155/2014/256784] [PMID: 24741581]
[3]
Francis, D.P. Successes and failures: Worldwide vaccine development and application. Biologicals, 2010, 38(5), 523-528.
[http://dx.doi.org/10.1016/j.biologicals.2010.06.003] [PMID: 20685134]
[4]
Wong, L.K.S.; Muthupalaniappen, L.; Tie, S.T. Knowledge, belief and barriers to adult influenza and pneumococcal vaccination among primary care doctors in sarawak. Med. Health, 2017, 12, 275-285.
[5]
Vogel, F.R. Adjuvants in perspective.Modulation of the immune response to vaccine antigens, 92, F. In: Brown and L.R. Haaheim, eds. (Basel: Karger: Development in Biological Standardization), ; , 1998, 92, pp. 241-248.
[6]
Sun, X.; Stefanetti, G.; Berti, F.; Kasper, D.L. Polysaccharide structure dictates mechanism of adaptive immune response to glycoconjugate vaccines. Proc. Natl. Acad. Sci. USA, 2019, 116(1), 193-198.
[http://dx.doi.org/10.1073/pnas.1816401115] [PMID: 30510007]
[7]
Portillo, S.; Zepeda, B.G.; Iniguez, E.; Olivas, J.J.; Karimi, N.H.; Moreira, O.C.; Marques, A.F.; Michael, K.; Maldonado, R.A.; Almeida, I.C. A prophylactic α-Gal-based glycovaccine effectively protects against murine acute Chagas disease. NPJ Vaccines, 2019, 4, 13.
[http://dx.doi.org/10.1038/s41541-019-0107-7] [PMID: 30911415]
[8]
Harding, C.M.; Nasr, M.A.; Scott, N.E.; Goyette-Desjardins, G.; Nothaft, H.; Mayer, A.E.; Chavez, S.M.; Huynh, J.P.; Kinsella, R.L.; Szymanski, C.M.; Stallings, C.L.; Segura, M.; Feldman, M.F. A platform for glycoengineering a polyvalent pneumococcal bioconjugate vaccine using E. coli as a host. Nat. Commun., 2019, 10(1), 891.
[http://dx.doi.org/10.1038/s41467-019-08869-9] [PMID: 30792408]
[9]
Obaro, S.; Adegbola, R. The Pneumococcus: carriage, disease and conjugate vaccines. J. Med. Microbiol., 2002, 51(2), 98-104.
[http://dx.doi.org/10.1099/0022-1317-51-2-98] [PMID: 11863272]
[10]
Moisa, A.A.; Kolesanova, E.F. Synthetic Peptide Vaccines. Biomed. Khim., 2011, 57(1), 14-30.
[11]
Jones, L.H. Recent advances in the molecular design of synthetic vaccines. Nat. Chem., 2015, 7(12), 952-960.
[http://dx.doi.org/10.1038/nchem.2396] [PMID: 26587710]
[12]
Hu, J.; Qiu, L.; Wang, X.; Zou, X.; Lu, M.; Yin, J. Carbohydrate-based vaccine adjuvants - discovery and development. Expert Opin. Drug Discov., 2015, 10(10), 1133-1144.
[http://dx.doi.org/10.1517/17460441.2015.1067198] [PMID: 26372693]
[13]
Xu, X.; Jin, Z.; Liu, Y.; Gong, H.; Sun, Q.; Zhang, W.; Zhao, L. Carbohydrate-based adjuvants activate tumor-specific Th1 and CD8+ T-cell responses and reduce the immunosuppressive activity of MDSCs. Cancer Lett., 2019, 440-441, 94-105.
[http://dx.doi.org/10.1016/j.canlet.2018.10.013] [PMID: 30352261]
[14]
Simerska, P.; Abdel-Aal, A.B.M.; Fujita, Y.; Moyle, P.M.; McGeary, R.P.; Batzloff, M.R.; Olive, C.; Good, M.F.; Toth, I. Development of a liposaccharide-based delivery system and its application to the design of group A Streptococcal vaccines. J. Med. Chem., 2008, 51(5), 1447-1452.
[http://dx.doi.org/10.1021/jm701410p] [PMID: 18278857]
[15]
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]
[16]
King, W.J.; MacDonald, N.E.; Wells, G.; Huang, J.; Allen, U.; Chan, F.; Ferris, W.; Diaz-Mitoma, F.; Ashton, F. Total and functional antibody response to a quadrivalent meningococcal polysaccharide vaccine among children. J. Pediatr., 1996, 128(2), 196-202.
[http://dx.doi.org/10.1016/S0022-3476(96)70389-X] [PMID: 8636811]
[17]
Bacon, A.; Makin, J.; Sizer, P.J.; Jabbal-Gill, I.; Hinchcliffe, M.; Illum, L.; Chatfield, S.; Roberts, M. Carbohydrate biopolymers enhance antibody responses to mucosally delivered vaccine antigens. Infect. Immun., 2000, 68(10), 5764-5770.
[http://dx.doi.org/10.1128/IAI.68.10.5764-5770.2000] [PMID: 10992483]
[18]
Hölemann, A.; Seeberger, P.H. Carbohydrate diversity: synthesis of glycoconjugates and complex carbohydrates. Curr. Opin. Biotechnol., 2004, 15(6), 615-622.
[http://dx.doi.org/10.1016/j.copbio.2004.10.001] [PMID: 15560990]
[19]
Astronomo, R.D.; Burton, D.R. Carbohydrate vaccines: developing sweet solutions to sticky situations? Nat. Rev. Drug Discov., 2010, 9(4), 308-324.
[http://dx.doi.org/10.1038/nrd3012] [PMID: 20357803]
[20]
Lindberg, B.; Lindqvist, B.; Lönngren, J.; Powell, D.A. Structural studies of the capsular polysaccharide from Streptococcus pneumoniae type 1. Carbohydr. Res., 1980, 78(1), 111-117.
[http://dx.doi.org/10.1016/S0008-6215(00)83664-2] [PMID: 7351025]
[21]
Klugman, K.P.; Gilbertson, I.T.; Koornhof, H.J.; Robbins, J.B.; Schneerson, R.; Schulz, D.; Cadoz, M.; Armand, J. Protective activity of Vi capsular polysaccharide vaccine against typhoid fever. Lancet, 1987, 2(8569), 1165-1169.
[http://dx.doi.org/10.1016/S0140-6736(87)91316-X] [PMID: 2890805]
[22]
Geno, K.A.; Gilbert, G.L.; Song, J.Y.; Skovsted, I.C.; Klugman, K.P.; Jones, C.; Konradsen, H.B.; Nahm, M.H. Pneumococcal capsules and their types: Past, present, and future. Clin. Microbiol. Rev., 2015, 28(3), 871-899.
[http://dx.doi.org/10.1128/CMR.00024-15] [PMID: 26085553]
[23]
Mawas, F.; Newman, G.; Burns, S.; Corbel, M.J. Suppression and modulation of cellular and humoral immune responses to Haemophilus influenzae type B (Hib) conjugate vaccine in hib-diphtheria-tetanus toxoids-acellular pertussis combination vaccines: a study in a rat model. J. Infect. Dis., 2005, 191(1), 58-64.
[http://dx.doi.org/10.1086/426396] [PMID: 15593004]
[24]
Whitney, C.G.; Pilishvili, T.; Farley, M.M.; Schaffner, W.; Craig, A.S.; Lynfield, R.; Nyquist, A.C.; Gershman, K.A.; Vazquez, M.; Bennett, N.M.; Reingold, A.; Thomas, A.; Glode, M.P.; Zell, E.R.; Jorgensen, J.H.; Beall, B.; Schuchat, A. Effectiveness of seven-valent pneumococcal conjugate vaccine against invasive pneumococcal disease: a matched case-control study. Lancet, 2006, 368(9546), 1495-1502.
[http://dx.doi.org/10.1016/S0140-6736(06)69637-2] [PMID: 17071283]
[25]
Bröker, M.; Dull, P.M.; Rappuoli, R.; Costantino, P. Chemistry of a new investigational quadrivalent meningococcal conjugate vaccine that is immunogenic at all ages. Vaccine, 2009, 27(41), 5574-5580.
[http://dx.doi.org/10.1016/j.vaccine.2009.07.036] [PMID: 19619500]
[26]
Durando, P.; Faust, S.N.; Fletcher, M.; Krizova, P.; Torres, A.; Welte, T. Experience with pneumococcal polysaccharide conjugate vaccine (conjugated to CRM197 carrier protein) in children and adults. Clin. Microbiol. Infect., 2013, 19(Suppl. 1), 1-9.
[http://dx.doi.org/10.1111/1469-0691.12320] [PMID: 24083785]
[27]
Fradin, C.; Bernardes, E.S.; Jouault, T. Candida albicans phospholipomannan: a sweet spot for controlling host response/inflammation. Semin. Immunopathol., 2015, 37(2), 123-130.
[http://dx.doi.org/10.1007/s00281-014-0461-5] [PMID: 25394861]
[28]
Maue, A.C.; Poly, F.; Guerry, P. A capsule conjugate vaccine approach to prevent diarrheal disease caused by Campylobacter jejuni. Hum. Vaccin. Immunother., 2014, 10(6), 1499-1504.
[http://dx.doi.org/10.4161/hv.27985] [PMID: 24632556]
[29]
Auzanneau, F-I.; Borrelli, S.; Pinto, B.M. Synthesis and immunological activity of an oligosaccharide-conjugate as a vaccine candidate against Group A Streptococcus. Bioorg. Med. Chem. Lett., 2013, 23(22), 6038-6042.
[http://dx.doi.org/10.1016/j.bmcl.2013.09.042] [PMID: 24103300]
[30]
Ada, G.; Isaacs, D. Carbohydrate-protein conjugate vaccines. Clin. Microbiol. Infect., 2003, 9(2), 79-85.
[http://dx.doi.org/10.1046/j.1469-0691.2003.00530.x] [PMID: 12588327]
[31]
Zou, W.; Jennings, H.J. Preparation of glycoconjugate vaccines., 2008.
[http://dx.doi.org/10.1002/9780470473283.ch2]
[32]
Simerska, P.; Abdel-Aal, A.B.M.; Fujita, Y.; Batzloff, M.R.; Good, M.F.; Toth, I. Synthesis and in vivo studies of carbohydrate-based vaccines against group A streptococcus. Biopolymers, 2008, 90(5), 611-616.
[http://dx.doi.org/10.1002/bip.20992] [PMID: 18381625]
[33]
Slovin, S.F.; Ragupathi, G.; Musselli, C.; Olkiewicz, K.; Verbel, D.; Kuduk, S.D.; Schwarz, J.B.; Sames, D.; Danishefsky, S.; Livingston, P.O.; Scher, H.I. Fully synthetic carbohydrate-based vaccines in biochemically relapsed prostate cancer: clinical trial results with alpha-N-acetylgalactosamine-O-serine/threonine conjugate vaccine. J. Clin. Oncol., 2003, 21(23), 4292-4298.
[http://dx.doi.org/10.1200/JCO.2003.04.112] [PMID: 14645418]
[34]
Zhou, Z.; Liao, G.; Mandal, S.S.; Suryawanshi, S.; Guo, Z. A fully synthetic self-adjuvanting globo H-Based vaccine elicited strong T cell-mediated antitumor immunity. Chem. Sci. (Camb.), 2015, 6(12), 7112-7121.
[http://dx.doi.org/10.1039/C5SC01402F] [PMID: 26918109]
[35]
Simerska, P.; Lu, H.; Toth, I. Synthesis of a Streptococcus pyogenes vaccine candidate based on the M protein PL1 epitope. Bioorg. Med. Chem. Lett., 2009, 19(3), 821-824.
[http://dx.doi.org/10.1016/j.bmcl.2008.12.013] [PMID: 19097790]
[36]
Egleton, R.D.; Davis, T.P. Development of neuropeptide drugs that cross the blood-brain barrier. NeuroRx, 2005, 2(1), 44-53.
[http://dx.doi.org/10.1602/neurorx.2.1.44] [PMID: 15717056]
[37]
Negri, L.; Lattanzi, R.; Tabacco, F.; Scolaro, B.; Rocchi, R. Glycodermorphins: opioid peptides with potent and prolonged analgesic activity and enhanced blood-brain barrier penetration. Br. J. Pharmacol., 1998, 124(7), 1516-1522.
[http://dx.doi.org/10.1038/sj.bjp.0701971] [PMID: 9723966]
[38]
Varamini, P.; Mansfeld, F.M.; Blanchfield, J.T.; Wyse, B.D.; Smith, M.T.; Toth, I. Synthesis and biological evaluation of an orally active glycosylated endomorphin-1. J. Med. Chem., 2012, 55(12), 5859-5867.
[http://dx.doi.org/10.1021/jm300418d] [PMID: 22680612]
[39]
Nomoto, M.; Yamada, K.; Haga, M.; Hayashi, M. Improvement of intestinal absorption of peptide drugs by glycosylation: transport of tetrapeptide by the sodium ion-dependent D-glucose transporter. J. Pharm. Sci., 1998, 87(3), 326-332.
[http://dx.doi.org/10.1021/js970269p] [PMID: 9523986]
[40]
Susaki, H.; Suzuki, K.; Yamada, H.; Okuno, S.; Watanabe, H.K. Renal targeting of arginine-vasopressin by modification with carbohydrates at the tyrosine side chain. Biol. Pharm. Bull., 1999, 22(10), 1094-1098.
[http://dx.doi.org/10.1248/bpb.22.1094] [PMID: 10549862]
[41]
Suzuki, K.; Susaki, H.; Okuno, S.; Yamada, H.; Watanabe, H.K.; Sugiyama, Y. Specific renal delivery of sugar-modified low-molecular-weight peptides. J. Pharmacol. Exp. Ther., 1999, 288(2), 888-897.
[PMID: 9918603]
[42]
Szabó, T.G.; Palotai, R.; Antal, P.; Tokatly, I.; Tóthfalusi, L.; Lund, O.; Nagy, G.; Falus, A.; Buzás, E.I. Critical role of glycosylation in determining the length and structure of T cell epitopes. Immunome Res., 2009, 5, 4.
[http://dx.doi.org/10.1186/1745-7580-5-4] [PMID: 19778434]
[43]
Martinez-Pomares, L. The mannose receptor. J. Leukoc. Biol., 2012, 92(6), 1177-1186.
[http://dx.doi.org/10.1189/jlb.0512231] [PMID: 22966131]
[44]
Kragol, G.; Otvos, L. Orthogonal solid-phase synthesis of tetramannosylated peptide constructs carrying three independent branched epitopes. Tetrahedron, 2001, 57, 957-966.
[http://dx.doi.org/10.1016/S0040-4020(00)01087-5]
[45]
Liu, M.; Borgert, A.; Barany, G.; Live, D. Conformational consequences of protein glycosylation: preparation of O-mannosyl serine and threonine building blocks, and their incorporation into glycopeptide sequences derived from alpha-dystroglycan. Biopolymers, 2008, 90(3), 358-368.
[http://dx.doi.org/10.1002/bip.20847] [PMID: 17868094]
[46]
Levitz, S.M.; Specht, C.A. The molecular basis for the immunogenicity of Cryptococcus neoformans mannoproteins. FEMS Yeast Res., 2006, 6(4), 513-524.
[http://dx.doi.org/10.1111/j.1567-1364.2006.00071.x] [PMID: 16696647]
[47]
Taylor, P.R.; Gordon, S.; Martinez-Pomares, L. The mannose receptor: linking homeostasis and immunity through sugar recognition. Trends Immunol., 2005, 26(2), 104-110.
[http://dx.doi.org/10.1016/j.it.2004.12.001] [PMID: 15668126]
[48]
Sheng, K.C.; Pouniotis, D.S.; Wright, M.D.; Tang, C.K.; Lazoura, E.; Pietersz, G.A.; Apostolopoulos, V. Mannan derivatives induce phenotypic and functional maturation of mouse dendritic cells. Immunology, 2006, 118(3), 372-383.
[http://dx.doi.org/10.1111/j.1365-2567.2006.02384.x] [PMID: 16827898]
[49]
Sedaghat, B.; Stephenson, R.; Toth, I. Targeting the mannose receptor with mannosylated subunit vaccines. Curr. Med. Chem., 2014, 21(30), 3405-3418.
[http://dx.doi.org/10.2174/0929867321666140826115552] [PMID: 25174924]
[50]
Bundle, D.R.; Smith, I.C.P.; Jennings, H.J. Determination of the structure and conformation of bacterial polysaccharides by carbon 13 nuclear magnetic resonance. Studies on the group-specific antigens of Neisseria meningitidis serogroups A and X. J. Biol. Chem., 1974, 249(7), 2275-2281.
[PMID: 4206552]
[51]
Napoletano, C.; Zizzari, I.G.; Rughetti, A.; Rahimi, H.; Irimura, T.; Clausen, H.; Wandall, H.H.; Belleudi, F.; Bellati, F.; Pierelli, L.; Frati, L.; Nuti, M. Targeting of macrophage galactose-type C-type lectin (MGL) induces DC signaling and activation. Eur. J. Immunol., 2012, 42(4), 936-945.
[http://dx.doi.org/10.1002/eji.201142086] [PMID: 22531918]
[52]
Vukman, K.V.; Ravidà, A.; Aldridge, A.M.; O’Neill, S.M. Mannose receptor and macrophage galactose-type lectin are involved in Bordetella pertussis mast cell interaction. J. Leukoc. Biol., 2013, 94(3), 439-448.
[http://dx.doi.org/10.1189/jlb.0313130] [PMID: 23794711]
[53]
Bhatia, S.; Dimde, M.; Haag, R. Multivalent glycoconjugates as vaccines and potential drug candidates. MedChemComm, 2014, 5, 862-878.
[http://dx.doi.org/10.1039/C4MD00143E]
[54]
Buskas, T.; Li, Y.; Boons, G.J. The immunogenicity of the tumor-associated antigen Lewis(y) may be suppressed by a bifunctional cross-linker required for coupling to a carrier protein. Chemistry, 2004, 10(14), 3517-3524.
[http://dx.doi.org/10.1002/chem.200400074] [PMID: 15252797]
[55]
Wang, Q.; Zhang, J.; Guo, Z. Efficient glycoengineering of GM3 on melanoma cell and monoclonal antibody-mediated selective killing of the glycoengineered cancer cell. Bioorg. Med. Chem., 2007, 15(24), 7561-7567.
[http://dx.doi.org/10.1016/j.bmc.2007.09.005] [PMID: 17892942]
[56]
Coler, R.N.; Baldwin, S.L.; Shaverdian, N.; Bertholet, S.; Reed, S.J.; Raman, V.S.; Lu, X.; DeVos, J.; Hancock, K.; Katz, J.M.; Vedvick, T.S.; Duthie, M.S.; Clegg, C.H.; Van Hoeven, N.; Reed, S.G. A synthetic adjuvant to enhance and expand immune responses to influenza vaccines. PLoS One, 2010, 5(10)e13677
[http://dx.doi.org/10.1371/journal.pone.0013677] [PMID: 21060869]
[57]
Jansson, P.E.; Lindberg, B.; Anderson, M.; Lindquist, U.; Henrichsen, J. Structural studies of the capsular polysaccharide from Streptococcus pneumoniae type 2, a reinvestigation. Carbohydr. Res., 1988, 182(1), 111-117.
[http://dx.doi.org/10.1016/0008-6215(88)84095-3] [PMID: 3242800]
[58]
Carapetis, J.R.; Steer, A.C.; Mulholland, E.K.; Weber, M. The global burden of group A streptococcal diseases. Lancet Infect. Dis., 2005, 5(11), 685-694.
[http://dx.doi.org/10.1016/S1473-3099(05)70267-X] [PMID: 16253886]
[59]
Johnson, M.A.; Pinto, B.M. Saturation transfer difference 1D-TOCSY experiments to map the topography of oligosaccharides recognized by a monoclonal antibody directed against the cell-wall polysaccharide of group A streptococcus. J. Am. Chem. Soc., 2002, 124(51), 15368-15374.
[http://dx.doi.org/10.1021/ja020983v] [PMID: 12487612]
[60]
Kabanova, A.; Margarit, I.; Berti, F.; Romano, M.R.; Grandi, G.; Bensi, G.; Chiarot, E.; Proietti, D.; Swennen, E.; Cappelletti, E.; Fontani, P.; Casini, D.; Adamo, R.; Pinto, V.; Skibinski, D.; Capo, S.; Buffi, G.; Gallotta, M.; Christ, W.J.; Campbell, A.S.; Pena, J.; Seeberger, P.H.; Rappuoli, R.; Costantino, P. Evaluation of a Group A Streptococcus synthetic oligosaccharide as vaccine candidate. Vaccine, 2010, 29(1), 104-114.
[http://dx.doi.org/10.1016/j.vaccine.2010.09.018] [PMID: 20870056]
[61]
Wyle, F.A.; Artenstein, M.S.; Brandt, B.L.; Tramont, E.C.; Kasper, D.L.; Altieri, P.L.; Berman, S.L.; Lowenthal, J.P. Immunologic response of man to group B meningococcal polysaccharide vaccines. J. Infect. Dis., 1972, 126(5), 514-521.
[http://dx.doi.org/10.1093/infdis/126.5.514] [PMID: 4197754]
[62]
Weynants, V.; Denoël, P.; Devos, N.; Janssens, D.; Feron, C.; Goraj, K.; Momin, P.; Monnom, D.; Tans, C.; Vandercammen, A.; Wauters, F.; Poolman, J.T. Genetically modified L3,7 and L2 lipooligosaccharides from Neisseria meningitidis serogroup B confer a broad cross-bactericidal response. Infect. Immun., 2009, 77(5), 2084-2093.
[http://dx.doi.org/10.1128/IAI.01108-08] [PMID: 19289516]
[63]
Snape, M.D.; Pollard, A.J. Meningococcal polysaccharide-protein conjugate vaccines. Lancet Infect. Dis., 2005, 5(1), 21-30.
[http://dx.doi.org/10.1016/S1473-3099(04)01251-4] [PMID: 15620558]
[64]
Scanlan, C.N.; Offer, J.; Zitzmann, N.; Dwek, R.A. Exploiting the defensive sugars of HIV-1 for drug and vaccine design. Nature, 2007, 446(7139), 1038-1045.
[http://dx.doi.org/10.1038/nature05818] [PMID: 17460665]
[65]
Tsai, C.C.; Emau, P.; Jiang, Y.; Agy, M.B.; Shattock, R.J.; Schmidt, A.; Morton, W.R.; Gustafson, K.R.; Boyd, M.R. Cyanovirin-N inhibits AIDS virus infections in vaginal transmission models. AIDS Res. Hum. Retroviruses, 2004, 20(1), 11-18.
[http://dx.doi.org/10.1089/088922204322749459] [PMID: 15000694]
[66]
Scanlan, C.N.; Pantophlet, R.; Wormald, M.R.; Ollmann Saphire, E.; Stanfield, R.; Wilson, I.A.; Katinger, H.; Dwek, R.A.; Rudd, P.M.; Burton, D.R. The broadly neutralizing anti-human immunodeficiency virus type 1 antibody 2G12 recognizes a cluster of alpha1-->2 mannose residues on the outer face of gp120. J. Virol., 2002, 76(14), 7306-7321.
[http://dx.doi.org/10.1128/JVI.76.14.7306-7321.2002] [PMID: 12072529]
[67]
Galonić, D.P.; Gin, D.Y. Chemical glycosylation in the synthesis of glycoconjugate antitumour vaccines. Nature, 2007, 446(7139), 1000-1007.
[http://dx.doi.org/10.1038/nature05813] [PMID: 17460660]
[68]
Kensil, C. R.; Patel, U.; Lennick, M.; Marciani, D. Separation and characterization of saponins with adjuvant activity from Quillaja saponaria Molina cortex. J. Immunol. (Baltimore, Md. : 1950), 1991, 146, 431-437.
[69]
Wang, L.X. Synthetic carbohydrate antigens for HIV vaccine design. Curr. Opin. Chem. Biol., 2013, 17(6), 997-1005.
[http://dx.doi.org/10.1016/j.cbpa.2013.10.001] [PMID: 24466581]
[70]
Agrawal, A.; Murphy, T.F. Haemophilus influenzae infections in the H. influenzae type B conjugate vaccine era. J. Clin. Microbiol., 2011, 49(11), 3728-3732.
[http://dx.doi.org/10.1128/JCM.05476-11] [PMID: 21900515]
[71]
Verez-Bencomo, V.; Fernández-Santana, V.; Hardy, E.; Toledo, M.E.; Rodríguez, M.C.; Heynngnezz, L.; Rodriguez, A.; Baly, A.; Herrera, L.; Izquierdo, M.; Villar, A.; Valdés, Y.; Cosme, K.; Deler, M.L.; Montane, M.; Garcia, E.; Ramos, A.; Aguilar, A.; Medina, E.; Toraño, G.; Sosa, I.; Hernandez, I.; Martínez, R.; Muzachio, A.; Carmenates, A.; Costa, L.; Cardoso, F.; Campa, C.; Diaz, M.; Roy, R. A synthetic conjugate polysaccharide vaccine against Haemophilus influenzae type b. Science, 2004, 305(5683), 522-525.
[http://dx.doi.org/10.1126/science.1095209] [PMID: 15273395]

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