On the use of adenovirus dodecahedron as a carrier for glycoconjugate vaccines.
Adenovirus dodecahedron
Carbohydrate antigen
Glycoconjugate vaccine
Streptococcus pneumoniae
Virus-like particle
Journal
Glycoconjugate journal
ISSN: 1573-4986
Titre abrégé: Glycoconj J
Pays: United States
ID NLM: 8603310
Informations de publication
Date de publication:
08 2021
08 2021
Historique:
received:
23
12
2020
accepted:
08
04
2021
revised:
28
03
2021
pubmed:
15
4
2021
medline:
25
2
2022
entrez:
14
4
2021
Statut:
ppublish
Résumé
Virus-Like Particles (VLPs) have been used as immunogenic molecules in numerous recombinant vaccines. VLPs can also serve as vaccine platform to exogenous antigens, usually peptides incorporated within the protein sequences which compose the VLPs or conjugated to them. We herein described the conjugation of a synthetic tetrasaccharide mimicking the Streptococcus pneumoniae serotype 14 capsular polysaccharide to recombinant adenoviral type 3 dodecahedron, formed by the self-assembling of twelve penton bases and investigated the induced immune response when administered subcutaneously (s.c.). Whether formulated in the form of a dodecahedron or disassembled, the glycoconjugate induced an anti-protein response after two and three immunizations equivalent to that observed when the native dodecahedron was administered. On the other hand, the glycoconjugate induced a weak anti-IgM response which diminishes after two doses but no IgM-to-IgG switch was observed in mice against the serotype 14 capsular polysaccharide. In definitive, the whole conjugation process preserved both particulate nature and immunogenicity of the adenoviral dodecahedron. Further studies are needed to fully exploit adenoviral dodecahedron potential in terms of plasticity towards sequence engineering and of its capacity to stimulate the immune system via the intranasal route of administration as well as to shift the response to the carbohydrate antigen by playing both with the carbohydrate to protein ratio and the length of the synthetic carbohydrate antigen.
Identifiants
pubmed: 33852106
doi: 10.1007/s10719-021-09999-3
pii: 10.1007/s10719-021-09999-3
doi:
Substances chimiques
Glycoconjugates
0
Pneumococcal Vaccines
0
Vaccines, Conjugate
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
437-446Références
Heidelberger, M., Avery, O.T.: The soluble specific substance of pneumococcus. J. Exp. Med. 38(1), 73–79 (1923). https://doi.org/10.1084/jem.38.1.73
doi: 10.1084/jem.38.1.73
pubmed: 19868772
pmcid: 2128423
Rappuoli, R.: Glycoconjugate vaccines: Principles and mechanisms. Sci. Transl. Med. 10(456), 29 (2018). https://doi.org/10.1126/scitranslmed.aat4615
doi: 10.1126/scitranslmed.aat4615
Sun, X., Stefanetti, G., Berti, F., Kasper, D.L.: Polysaccharide structure dictates mechanism of adaptive immune response to glycoconjugate vaccines. Proc. Natl. Acad. Sci. U S A. 116(1), 193–198 (2019). https://doi.org/10.1073/pnas.1816401115
doi: 10.1073/pnas.1816401115
pubmed: 30510007
Bröker, M., Berti, F., Schneider, J., Vojtek, I.: Polysaccharide conjugate vaccine protein carriers as a “neglected valency” - Potential and limitations. Vaccine. 35(25), 3286–3294 (2017). https://doi.org/10.1016/j.vaccine.2017.04.078
doi: 10.1016/j.vaccine.2017.04.078
pubmed: 28487056
Micoli, F., Adamo, R., Costantino, P.: Protein Carriers for Glycoconjugate Vaccines: History, Selection Criteria, Characterization and New Trends. Molecules. 23(6), (2018). https://doi.org/10.3390/molecules23061451
Pinto, V.B., Burden, R., Wagner, A., Moran, E.E., Lee, C.-H.: The development of an experimental multiple serogroups vaccine for Neisseria meningitidis. PLoS One. 8(11), e79304 (2013). https://doi.org/10.1371/journal.pone.0079304
doi: 10.1371/journal.pone.0079304
pubmed: 24244473
pmcid: 3828347
Grandjean, C., Wade, T.K., Ropartz, D., Ernst, L., Wade, W.F.: Acid-detoxified Inaba lipopolysaccharide (pmLPS) is a superior cholera conjugate vaccine immunogen than hydrazine-detoxified lipopolysaccharide and induces vibriocidal and protective antibodies. Pathog. Dis. 67(2), 136–158 (2013). https://doi.org/10.1111/2049-632X.12022
doi: 10.1111/2049-632X.12022
pubmed: 23620159
Woodruff, M.C., Kim, E.H., Luo, W., Pulendran, B.: B Cell Competition for Restricted T Cell Help Suppresses Rare-Epitope Responses. Cell. Rep. 25(2), 321–327.e3 (2018). https://doi.org/10.1016/j.celrep.2018.09.029
doi: 10.1016/j.celrep.2018.09.029
pubmed: 30304673
pmcid: 6235168
Pillot, A., Defontaine, A., Fateh, A., Lambert, A., Prasanna, M., Fanuel, M., Pipelier, M., Csaba, N., Violo, T., Camberlein, E., Grandjean, C.: Site-specific conjugation for fully controlled Glycoconjugate vaccine preparation. Front Chem. 7, 726 (2019). https://doi.org/10.3389/fchem.2019.00726
doi: 10.3389/fchem.2019.00726
pubmed: 31737603
pmcid: 6839274
Gause, K.T., Wheatley, A.K., Cui, J., Yan, Y., Kent, S.J., Caruso, F.: Immunological Principles Guiding the Rational Design of Particles for Vaccine Delivery. ACS Nano. 11(1), 54–68 (2017). https://doi.org/10.1021/acsnano.6b07343
doi: 10.1021/acsnano.6b07343
pubmed: 28075558
Cimica, V., Galarza, J.M.: Adjuvant formulations for virus-like particle (VLP) based vaccines. Clin. Immunol. 183, 99–108 (2017). https://doi.org/10.1016/j.clim.2017.08.004
doi: 10.1016/j.clim.2017.08.004
pubmed: 28780375
pmcid: 5673579
Yan, D., Wei, Y.-Q., Guo, H.-C., Sun, S.-Q.: The application of virus-like particles as vaccines and biological vehicles. Appl. Microbiol. Biotechnol. 99(24), 10415–10432 (2015). https://doi.org/10.1007/s00253-015-7000-8
doi: 10.1007/s00253-015-7000-8
pubmed: 26454868
pmcid: 7080154
Marcandalli, J., et al.: Induction of Potent Neutralizing Antibody Responses by a Designed Protein Nanoparticle Vaccine for Respiratory Syncytial Virus. Cell. 176(6), 1420–1431.e17 (2019). https://doi.org/10.1016/j.cell.2019.01.046
doi: 10.1016/j.cell.2019.01.046
pubmed: 30849373
pmcid: 6424820
Powell, A.E., Zhang, K., Sanyal, M., Tang, S., Weidenbacher, P.A., Li, S., Pham, T.D., Pak, J.E., Chiu, W., Kim, P.S.: A single immunization with spike-functionalized ferritin vaccines elicits neutralizing antibody responses against SARS-CoV-2 in mice. ACS Cent. Sci. 7(1), 183–199 (2021). https://doi.org/10.1021/acscentsci.0c01405
doi: 10.1021/acscentsci.0c01405
pubmed: 33527087
pmcid: 7805605
Sungsuwan, S., Wu, X., Huang, X.: Evaluation of virus-like particle-based tumor-associated carbohydrate Immunogen in a mouse tumor model. Methods Enzymol. 597, 359–376 (2017). https://doi.org/10.1016/bs.mie.2017.06.030
doi: 10.1016/bs.mie.2017.06.030
pubmed: 28935111
pmcid: 5772760
Astronomo, R.D., et al.: Defining criteria for oligomannose immunogens for HIV using icosahedral virus capsid scaffolds. Chem. Biol. 17(4), 357–370 (2010). https://doi.org/10.1016/j.chembiol.2010.03.012
doi: 10.1016/j.chembiol.2010.03.012
pubmed: 20416507
pmcid: 2867452
Polonskaya, Z., et al.: T cells control the generation of nanomolar-affinity anti-glycan antibodies. J. Clin. Invest. 127(4), 1491–1504 (2017). https://doi.org/10.1172/JCI91192
doi: 10.1172/JCI91192
pubmed: 28287405
pmcid: 5373877
Fender, P., Ruigrok, R.W., Gout, E., Buffet, S., Chroboczek, J.: Adenovirus dodecahedron, a new vector for human gene transfer. Nat Biotechnol. 15(1), 52–56 (1997). https://doi.org/10.1038/nbt0197-52
doi: 10.1038/nbt0197-52
pubmed: 9035106
Vivès, R.R., Lortat-Jacob, H., Chroboczek, J., Fender, P.: Heparan sulfate proteoglycan mediates the selective attachment and internalization of serotype 3 human adenovirus dodecahedron. Virology. 321(2), 332–340 (2004). https://doi.org/10.1016/j.virol.2004.01.015
doi: 10.1016/j.virol.2004.01.015
pubmed: 15051392
Fender, P., Schoehn, G., Perron-Sierra, F., Tucker, G.C., Lortat-Jacob, H.: Adenovirus dodecahedron cell attachment and entry are mediated by heparan sulfate and integrins and vary along the cell cycle. Virology. 371(1), 155–164 (2008). https://doi.org/10.1016/j.virol.2007.09.026
doi: 10.1016/j.virol.2007.09.026
pubmed: 17950396
Naskalska, A., Szolajska, E., Andreev, I., Podsiadla, M., Chroboczek, J.: Towards a novel influenza vaccine: engineering of hemagglutinin on a platform of adenovirus dodecahedron. BMC Biotechnol. 13, 50 (2013). https://doi.org/10.1186/1472-6750-13-50
doi: 10.1186/1472-6750-13-50
pubmed: 23767961
pmcid: 3688493
Szurgot, I., et al.: Self-adjuvanting influenza candidate vaccine presenting epitopes for cell-mediated immunity on a proteinaceous multivalent nanoplatform. Vaccine. 31(40), 4338–4346 (2013). https://doi.org/10.1016/j.vaccine.2013.07.021
doi: 10.1016/j.vaccine.2013.07.021
pubmed: 23880363
Vragniau, C., Bufton, J. C., Garzoni, F., Stermann, E., Rabi, F., Terrat, C., Guidetti, M., Josserand, V., Williams, M., Woods, C.J., Viedma, G., Bates, P., Verrier, B., Chaperot, L., Schaffitzel, C., Berger, I., Fender, P. Synthetic self-assembling ADDomer platform for highly efficient vaccination by genetically encoded multiepitope display. Sci. Adv. 5(9), eaaw2853 (2019). https://doi.org/10.1126/sciadv.aaw2853
Szurgot, I., Jedynak, M., Podsiadla-Bialoskorska, M., Piwowarski, J., Szolajska, E., Chroboczek, J.: Adenovirus Dodecahedron, a VLP, Can be Purified by Size Exclusion Chromatography Instead of Time-Consuming Sucrose Density Gradient Centrifugation. Mol. Biotechnol. 57(6), 565–573 (2015). https://doi.org/10.1007/s12033-015-9850-9
Prasanna, M., et al.: Semisynthetic glycoconjugate based on dual role protein/PsaA as a pneumococcal vaccine. Eur. J. Pharm. Sci. 129, 31–41 (2019). https://doi.org/10.1016/j.ejps.2018.12.013
doi: 10.1016/j.ejps.2018.12.013
pubmed: 30572107
Herbert, D., Phipps, P. J., Strange, R. E., Chapter III Chemical Analysis of Microbial Cells. In: Methods in Microbiology, 5, J. R. Norris, D. W. Ribbons, Éd. Academic Press, 209–344 (1971). https://doi.org/10.1016/S0580-9517(08)70641-X
Grandjean, C., Boutonnier, A., Dassy, B., Fournier, J.-M., Mulard, L.A.: Investigation towards bivalent chemically defined glycoconjugate immunogens prepared from acid-detoxified lipopolysaccharide of Vibrio cholerae O1, serotype Inaba. Glycoconj J. 26(1), 41–55 (2009). https://doi.org/10.1007/s10719-008-9160-6
Fuschiotti, P., et al.: Structure of the dodecahedral penton particle from human adenovirus type 3. J. Mol. Biol. 356(2), 510–520 (2006). https://doi.org/10.1016/j.jmb.2005.11.048
doi: 10.1016/j.jmb.2005.11.048
pubmed: 16375921
Safari, D., et al.: Identification of the smallest structure capable of evoking opsonophagocytic antibodies against Streptococcus pneumoniae type 14. Infect. Immun. 76(10), 4615–4623 (2008). https://doi.org/10.1128/IAI.00472-08
doi: 10.1128/IAI.00472-08
pubmed: 18678667
pmcid: 2546832
Kurbatova, E.A., Akhmatova, N.K., Akhmatova, E.A., Egorova, N.B., Yastrebova, N.E., Sukhova, E.V., Yashunsky, D.V., Tsvetkov, Y.E., Gening, M.L., Nifantiev, N.E.: Neoglycoconjugate of Tetrasaccharide representing one repeating unit of the Streptococcus pneumoniae type 14 capsular polysaccharide induces the production of opsonizing IgG1 antibodies and possesses the highest protective activity as compared to Hexa- and Octasaccharide conjugates. Front. Immunol. 8, 659 (2017). https://doi.org/10.3389/fimmu.2017.00659
doi: 10.3389/fimmu.2017.00659
pubmed: 28626461
pmcid: 5454037
Pozsgay, V., Chu, C., Pannell, L., Wolfe, J., Robbins, J.B., Schneerson, R.: Protein conjugates of synthetic saccharides elicit higher levels of serum IgG lipopolysaccharide antibodies in mice than do those of the O-specific polysaccharide from Shigella dysenteriae type 1. Proc. Natl. Acad. Sci. U S A. 96(9), 5194–5197 (1999). https://doi.org/10.1073/pnas.96.9.5194
doi: 10.1073/pnas.96.9.5194
pubmed: 10220442
pmcid: 21840
Carboni, F., et al.: Evaluation of Immune Responses to Group B Streptococcus Type III Oligosaccharides Containing a Minimal Protective Epitope. J. Infect. Dis. 221(6), 943–947 (2020). https://doi.org/10.1093/infdis/jiz551
doi: 10.1093/infdis/jiz551
pubmed: 31641758
Mawas, F., Niggemann, J., Jones, C., Corbel, M.J., Kamerling, J.P., Vliegenthart, J.F.G.: Immunogenicity in a mouse model of a conjugate vaccine made with a synthetic single repeating unit of type 14 pneumococcal polysaccharide coupled to CRM197. Infect. Immun. 70(9), 5107–5114 (2002). https://doi.org/10.1128/iai.70.9.5107-5114.2002
doi: 10.1128/iai.70.9.5107-5114.2002
pubmed: 12183560
pmcid: 128223
Milhomme, O., et al.: Synthesis and immunochemical evaluation of a non-methylated disaccharide analogue of the anthrax tetrasaccharide. Org. Biomol. Chem. 10(42), 8524–8532 (2012). https://doi.org/10.1039/c2ob26131f
doi: 10.1039/c2ob26131f
pubmed: 23010801
Khurana, J.M., Gogia, A.: Synthetically Useful Reactions with Nickel Boride. a Review. Org. Preparations Proced. Int. 29(1), 1–32 (1997). https://doi.org/10.1080/00304949709355171
doi: 10.1080/00304949709355171
Pettersen, E.F., et al.: UCSF Chimera--a visualization system for exploratory research and analysis. J. Comput. Chem. 25(13), 1605–1612 (2004). https://doi.org/10.1002/jcc.20084
doi: 10.1002/jcc.20084
Szolajska, E., et al.: The structural basis for the integrity of adenovirus Ad3 dodecahedron. PLoS One. 7(9), e46075 (2012). https://doi.org/10.1371/journal.pone.0046075
doi: 10.1371/journal.pone.0046075
pubmed: 23049939
pmcid: 3457955
Wang, X., et al.: Immune protection efficacy of FAdV-4 surface proteins fiber-1, fiber-2, hexon and penton base. Virus Res. 245, 1–6 (2018). https://doi.org/10.1016/j.virusres.2017.12.003
doi: 10.1016/j.virusres.2017.12.003
pubmed: 29233649
Bal, H.P., Chroboczek, J., Schoehn, G., Ruigrok, R.W., Dewhurst, S.: Adenovirus type 7 penton purification of soluble pentamers from Escherichia coli and development of an integrin-dependent gene delivery system. Eur J Biochem. 267(19), 6074–6081 (2000). https://doi.org/10.1046/j.1432-1327.2000.01684.x
doi: 10.1046/j.1432-1327.2000.01684.x
pubmed: 10998069
« Default of the coating can be ruled out since a response has been observed for positive controls - positive sera from previous immunizations - which are added in every tested ELISA plate »
Peeters, C.C., Tenbergen-Meekes, A.M., Poolman, J.T., Zegers, B.J., Rijkers, G.T.: Immunogenicity of a Streptococcus pneumoniae type 4 polysaccharide--protein conjugate vaccine is decreased by admixture of high doses of free saccharide. Vaccine. 10(12), 833–840 (1992). https://doi.org/10.1016/0264-410x(92)90046-m
doi: 10.1016/0264-410x(92)90046-m
pubmed: 1455909
Rodriguez, M.E., et al.: Immunogenicity of Streptococcus pneumoniae type 6B and 14 polysaccharide-tetanus toxoid conjugates and the effect of uncoupled polysaccharide on the antigen-specific immune response. Vaccine. 16(20), 1941–1949 (1998). https://doi.org/10.1016/s0264-410x(98)00129-7
doi: 10.1016/s0264-410x(98)00129-7
pubmed: 9796048
Ma, Z., Zhang, H., Wang, P.G., Liu, X.-W., Chen, M.: Peptide adjacent to glycosylation sites impacts immunogenicity of glycoconjugate vaccine. Oncotarget. 9(1), 75–82 (2018). https://doi.org/10.18632/oncotarget.19944
doi: 10.18632/oncotarget.19944
pubmed: 29416597
Pecetta, S., et al.: Carrier priming with CRM 197 or diphtheria toxoid has a different impact on the immunogenicity of the respective glycoconjugates: biophysical and immunochemical interpretation. Vaccine. 33(2), 314–320 (2015). https://doi.org/10.1016/j.vaccine.2014.11.026
doi: 10.1016/j.vaccine.2014.11.026
pubmed: 25448110
Vinuesa, C.G., Linterman, M.A., Yu, D., MacLennan, I.C.M.: Follicular Helper T Cells. Annu. Rev. Immunol. 34, 335–368 (2016). https://doi.org/10.1146/annurev-immunol-041015-055605
doi: 10.1146/annurev-immunol-041015-055605
pubmed: 26907215
Sterrett, S., et al.: Peripheral CD4 T follicular cells induced by a conjugated pneumococcal vaccine correlate with enhanced opsonophagocytic antibody responses in younger individuals. Vaccine. 38(7), 1778–1786 (2020). https://doi.org/10.1016/j.vaccine.2019.12.023
doi: 10.1016/j.vaccine.2019.12.023
pubmed: 31911030
pmcid: 8040292
Hong, S., et al.: B Cells Are the Dominant Antigen-Presenting Cells that Activate Naive CD4+ T Cells upon Immunization with a Virus-Derived Nanoparticle Antigen. Immunity. 49(4), 695–708.e4 (2018). https://doi.org/10.1016/j.immuni.2018.08.012
doi: 10.1016/j.immuni.2018.08.012
pubmed: 30291027