Abstract
In recent years, there have been a number of reports on the successful use of immunostimulatory complexes with saponins and viral glycoproteins as veterinary vaccines and in clinical trials for human medicine. The saponins Algiox, Sapanox and Pangisan were isolated and purified by HPLC from Allochrusa gypsophiloides, Saponaria officinalis and Gypsophila paniculata plants in Kazakhstan and they proved to have low toxicity in experiments with mice, chickens and chicken embryos. Algiox, Sapanox and Pangisan can be used to create immunostimulatory complexes (ISCOMs) similar to saponin-Quil-A-containing ISCOMs both in structure and in immunostimulatory efficiency. The adjuvant effect of the obtained saponins was studied by subcutaneous injection of mice with ISCOMs containing these herbal saponins and lipids and glycoproteins of H7N1 influenza virus. Sapanox, Pangisan and Algiox from Kazakhstani plants of the family Caryophyllaceae could be considered an additional source of highly effective adjuvants not only for veterinary vaccines but also for human medicine.
Similar content being viewed by others
References
Alving CR, Peachman KK, Rao M, Reed SG (2012) Adjuvants for human vaccines. Curr Opin Immunol 24:310–315. doi:10.1016/j.coi.2012.03.008
Greenwood B, Salisbury D, Hill AVS (2011) Vaccines and global health. Philos Trans R Soc Lond B Biol Sci 366(1579):2733–2742. doi:10.1098/rstb.2011.0076
Gregory AE, Titball R, Williamson D (2013) Vaccine delivery using nanoparticles. Front Cell Infect Microbiol 3:13
Dalsgaard K (1974) Saponin adjuvants. III. Isolation of a substance from Quillaja saponaria Molina with adjuvant activity in foot-and-mouth disease vaccines. Arch Gesamte Virusfopsch 44:243–254
Paepenmüller T, Müller-Goymann CC (2014) Influence of Quil A on liposomal membranes. Int J Pharm 475:138–146
Camussone CM, Pujato N, Renna MS et al (2014) Immune response and functional role of antibodies raised in heifers against a Staphylococcus aureus CP5 lysate and recombinant antigens vaccine formulated with Iscom Matrix adjuvant. Vet Immunol Immunopathol 162:96–107
Cox RJ, Major D, Pedersen G et al (2015) Matrix M H5N1 vaccine induces cross-H5 clade humoral immune responses in a randomized clinical trial and provides protection from highly pathogenic influenza challenge in ferrets. PLoS ONE 10(7):e0131652. doi:10.1371/journal.pone.0131652
Morein B, Lovgren К, Ronnberg B et al (1995) Immunostimulating complexes: clinical potential in vaccine development. Clin Immunother 3:461–475
Rajput ZI, Hu SH, Xiao ChW et al (2007) Adjuvant effects of saponins on animal immune responses. J Zhejiang Univ Sci B 8(3):153–161
Sun HX, Xie Y, Ye YP (2009) ISCOMs and ISCOMATRIX. Vaccine 27:4388–4401. doi:10.1016/j.vaccine.2009.05.032
Rönnberg B, Fekadu M, Morein B (1995) Adjuvant activity of non-toxic Quillaja saponaria Molina components for use in ISCOM matrix. Vaccine 13:1375–1382
Chung KY, Coyle EM, Jani D et al (2015) ISCOMATRIX™ adjuvant promotes epitope spreading and antibody affinity maturation of influenza A H7N9 virus like particle vaccine that correlate with virus neutralization in humans. Vaccine 33:3953–3962
Hägglund S, Hu K, Blodörn K et al (2014) Characterization of an experimental vaccine for bovine respiratory syncytial virus. Clin Vaccine Immunol 21:997–1004
Fossum C, Hjertner B, Ahlberg V et al (2014) Early inflammatory response to the saponin adjuvant Matrix-M in the pig. Vet Immunol Immunopathol 158:53–61
Magnusson SE, Karlsson KH, Reimer JM et al (2014) Matrix-M™ adjuvanted envelope protein vaccine protects against lethal lineage 1 and 2 West Nile virus infection in mice. Vaccine 32:800–808
(2007) Novavax revealed preclinical data of virus-like particle HIV vaccine. Expert Rev Vaccines 6:654-655. doi:10.1586/14760584.6.5.653
Katselis GS, Estrada A, Gorecki DKJ, Barl B (2007) Adjuvant activities of saponins from the root of Polygala senega L. Can J Physiol Pharmacol 85(11):1184–1194. doi:10.1139/Y07-109
Hong F, Xiao W, Ragupathi G et al (2011) The known immunologically active components of Astragalus account for only a small proportion of the immunological adjuvant activity when combined with conjugate vaccines. Planta Med 77(8):817–824. doi:10.1055/s-0030-1250574
Berezin VE, Bogoyavlenskiy AP, Turmagambetova AS et al (2013) Nanoparticles from plant saponins as delivery system for mucosal influenza vaccine. Am J Infect Dis Microbiol 1:1–4
Tiwari N, Gupta VK, Pandey P et al (2017) Adjuvant effect of Asparagus racemosus Willd. derived saponins in antibody production, allergic response and pro-inflammatory cytokine modulation. Biomed Pharmacother 86:555–561
Berezin VE, Zaides VM, Isaeva ES, Artamonov AF, Zhdanov VM (1988) Controlled organization of multimolecular complexes of enveloped virus glycoproteins: study of immunogenicity. Vaccine 6:450–456
Klimov A, Balish A, Veguilla V et al (2012) Influenza virus titration, antigenic characterization, and serological methods for antibody detection. Methods Mol Biol 865:25–51. doi:10.1007/978-1-61779-621-0_3
Carlsson N, Borde A, Wölfel S, Åkerman B, Larsson A (2011) Quantification of protein concentration by the Bradford method in the presence of pharmaceutical polymers. Anal Biochem 411:116–121
Uematsu Y, Hirata K, Saito K (2000) Spectrophotometric determination of saponin in Yucca extract used as food additive. J AOAC Int 83(6):1451–1454
Stepanenko AA, Dmitrenko VV (2015) Pitfalls of the MTT assay: direct and off-target effects of inhibitors can result in over/underestimation of cell viability. Gene 574:193–203
Bomford R (1980) Saponin and other haemolysins (vitamin A, aliphatic amines, polyene antibiotics) as adjuvants for SRBC in the mouse. Evidence for a role for cholesterol-binding in saponin adjuvanticity. Int Arch Allergy Appl Immunol 63(2):170–177
Ozel M, Hoglund S, Gelderblom H, Morein B (1989) Quaternary structure of the immunostimulating complex (iscom). J Ultrastruct Mol Struct Res 102:240–248
Natarajan S, Remick DG (2013) ELISA rescue protocol: Recovery of sample concentrations from an assay with an unsuccessful standard curve. Methods 61:69–72
Verschoor CP, Singh P, Russell ML et al (2016) Correction: microneutralization assay titres correlate with protection against seasonal influenza H1N1 and H3N2 in children. PLOS ONE 11(9):e0163830
Baltina LA (2003) Chemical modification of glycyrrhizic acid as a route to new bioactive compounds for medicine. Curr Med Chem 10:155–171
Bauer R, Hoheisel O, Stuhlfauth I, Wolf H (1999) Extract of the Echinacea purpurea herb: an allopathic phytoimmunostimulant. Wien Med Wochenschr 149:185–189
Bedir E, Pugh N, Calis I, Pasco DS, Khan IA (2000) Immunostimulatory effects of cycloartane-type triterpene glycosides from Astragalus species. Biol Pharm Bull 23:834–837
Desbène S, Hanquet B, Shoyama Y, Wagner H, Lacaille-Dubois MA (1999) Biologically active triterpene saponins from callus tissue of Polygala amarella. J Nat Prod 62:923–926
Quan F, Compans R, Cho Y, Kang S (2007) Ginseng and Salviae herbs play a role as immune activators and modulate immune responses during influenza virus infection. Vaccine 25:272–282
Morein B, Hu KF, Abasugra I (2004) Current status and potential application of ISCOMs in veterinary medicine. Adv Drug Deliv Rev 56:1367–1382
Evans TG, McElrath MJ, Matthews T et al (2001) QS-21 promotes an adjuvant effect allowing for reduced antigen dose during HIV-1 envelope subunit immunization in humans. Vaccine 19:2080–2091. doi:10.1016/S0264-410X(00)00415-1
Vogel FR (2000) Improving vaccine performance with adjuvants. Clin Infect Dis 30:S266–S270
Lafaille JJ (1998) The role of helper T cell subsets in autoimmune diseases. Cytokine Growth Factor Rev 9:139–151
Acknowledgements
This work was supported by the Ministry of Education and Science of the Republic of Kazakhstan (Grant numbers: 0114RK00274, 0115RK01097 and 0115RK01098).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.
Informed consent
Not applicable.
Additional information
Handling Editor: Sheela Ramamoorthy
Rights and permissions
About this article
Cite this article
Turmagambetova, A.S., Alexyuk, P.G., Bogoyavlenskiy, A.P. et al. Adjuvant activity of saponins from Kazakhstani plants on the immune responses to subunit influenza vaccine. Arch Virol 162, 3817–3826 (2017). https://doi.org/10.1007/s00705-017-3560-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00705-017-3560-5