β-glucan as a new tool in vaccine development

Vaclav Vetvicka, Luca Vannucci, Petr Sima, Vaclav Vetvicka, Luca Vannucci, Petr Sima

Abstract

Vaccination constitutes one of the major breakthroughs in human medicine. At the same time, development of more immunogenic vaccine alternatives to using aluminium-based adjuvants is one of the most important phases of vaccination development. Among different sources of carbohydrate polymers, including plants, microbes and synthetic sources tested, glucans were found to be the most promising vaccine adjuvant, as they alone stimulate various immune reactions including antibody production without any negative side effects. The use of glucan particles as a delivery system is a viable option based on the documented efficient antigen loading and receptor-targeted uptake in antigen-presenting cells. In addition to particles, soluble glucans can be used as novel hydrogels or as direct immunocyte-targeting delivery systems employing novel complexes with oligodeoxynucleotides. This review focuses on recent advances in glucan-based vaccine development from glucan-based conjugates to a glucan-based delivery and adjuvant platform.

Keywords: cancer; diseases; experimental animals; processes; subject; vaccination.

© 2019 The Scandinavian Foundation for Immunology.

References

REFERENCES

    1. Borchers AT, Stern JS, Hackman RM, Keen CL, Gershwin ME. Mushrooms, tumors, and immunity. Proc Soc Exp Biol Med. 1999;221:281-293.
    1. Brown GD, Gordon S. Fungal beta-glucans and mammalian immunity. Immunity. 2003;19:311-315.
    1. Novak M, Vetvicka V. Beta-glucans, history, and the present: immunomodulatory aspects and mechanisms of action. J Immunotoxicol. 2008;5:47-57.
    1. Torrence PF. Biological Response Modifiers: New Approaches to Disease Intervention. Orlando: Academic Press; 1985.
    1. Soto E, Ostroff G. Glucan particles as an efficient siRNA delivery vehicle. NSTI-Nanotech 2008. Techn Proc. 2008;2008(2):332-335.
    1. Thornton BP, Vetvicka V, Pitman M, Goldman RC, Ross GD. Analysis of the sugar specificity and molecular location of the beta-glucan-binding lectin site of complement receptor type 3 (CD11b/CD18). J Immunol. 1996;156:1235-1246.
    1. Yan J, Vetvicka V, Xia Y, et al. Beta-glucan, a "specific" biologic response modifier that uses antibodies to target tumors for cytotoxic recognition by leukocyte complement receptor type 3 (CD11b/CD18). J Immunol. 1999;163:3045-3052.
    1. Taylor PR, Brown GD, Reid DM, et al. The beta-glucan receptor, dectin-1, is predominantly expressed on the surface of cells of the monocyte/macrophage and neutrophil lineages. J Immunol. 2002;169:3876-3882.
    1. Czop JK, Austen KF. Properties of glycans that activate the human alternative complement pathway and interact with the human monocyte beta-glucan receptor. J Immunol. 1985;135:3388-3393.
    1. Al Tuwaijri AS, Mahmoud AA, Al Mofleh IA, Al Khuwaitir SA. Effect of glucan on Leishmania major infection in BALB/c mice. J Med Microbiol. 1987;23:363-365.
    1. Cook JA, Holbrook TW. Immunogenicity of soluble and particulate antigens from Leishmania donovani: effect of glucan as an adjuvant. Infect Immun. 1983;40:1038-1043.
    1. Aoyagi K, Itoh N, Abe F, et al. Enhancement by ubenimex (bestatin) of host resistance to Candida albicans infection. J Antibiot. 1992;45:1778-1784.
    1. Bousquet M, Escoula L, Pipy B, Bessieres MH, Chavant L, Seguela JP. [Enhancement of resistance of mice Toxoplasma gondii by 2 polysaccharides beta 1-3, beta 1-6 (PSAT and Scleroglucan)]. Ann Parasitol Hum Comp. 1988;63:398-409.
    1. Dritz SS, Shi J, Kielian TL, et al. Influence of dietary beta-glucan on growth performance, nonspecific immunity, and resistance to Streptococcus suis infection in weanling pigs. J Anim Sci. 1995;73:3341-3350.
    1. Kumar P, Ahmad S. Glucan-induced immunity in mice against Plasmodium berghei. Ann Trop Med Parasitol. 1985;79:211-213.
    1. Liang J, Melican D, Cafro L, et al. Enhanced clearance of a multiple antibiotic resistant Staphylococcus aureus in rats treated with PGG-glucan is associated with increased leukocyte counts and increased neutrophil oxidative burst activity. Int J Immunopharmacol. 1998;20:595-614.
    1. Rasmussen LT, Seljelid R. Dynamics of blood components and peritoneal fluid during treatment of murine E. coli sepsis with beta-1,3-D-polyglucose derivatives. I. Cells. Scand J Immunol. 1990;32:321-331.
    1. White TR, Thompson RC, Penhale WJ, Chihara G. The effect of lentinan on the resistance of mice to Mesocestoides corti. Parasitol Res. 1988;74:563-568.
    1. Williams DL, Yaeger RG, Pretus HA, Browder IW, McNamee RB, Jones EL. Immunization against Trypanosoma cruzi: adjuvant effect of glucan. Int J Immunopharmacol. 1989;11:403-410.
    1. Vetvicka V, Terayam K, Mandeville R, Brousseau P, Kournikakis B, Ostroff G. Pilot study: Orally-administered yeast β1,3-glucan prophylactically protects against anthrax infectin and cancer in mice. JANA. 2002;5:1-5.
    1. Cisneros RL, Gibson FC 3rd, Tzianabos AO. Passive transfer of poly-(1-6)-beta-glucotriosyl-(1-3)-beta-glucopyranose glucan protection against lethal infection in an animal model of intra-abdominal sepsis. Infect Immun. 1996;64:2201-2205.
    1. Kimura Y, Tojima H, Fukase S, Takeda K. Clinical evaluation of sizofilan as assistant immunotherapy in treatment of head and neck cancer. Acta Otolaryngol Suppl. 1994;511:192-195.
    1. Matsuoka H, Seo Y, Wakasugi H, Saito T, Tomoda H. Lentinan potentiates immunity and prolongs the survival time of some patients. Anticancer Res. 1997;17:2751-2755.
    1. Takeshita K, Saito N, Sato Y, et al. [Diversity of complement activation by lentinan, an antitumor polysaccharide, in gastric cancer patients]. Nihon Geka Gakkai. Zasshi. 1991;92:5-11.
    1. Patchen ML, MacVittie TJ. Dose-dependent responses of murine pluripotent stem cells and myeloid and erythroid progenitor cells following administration of the immunomodulating agent glucan. Immunopharmacology. 1983;5:303-313.
    1. Patchen ML, MacVittie TJ. Stimulated hemopoiesis and enhanced survival following glucan treatment in sublethally and lethally irradiated mice. Int J Immunopharmacol. 1985;7:923-932.
    1. Wagnerova J, Liskova A, Navarova J, Kristofova A, Trnovec T, Ferencik M. The effect of two glucan carboxymethyl derivatives with various substitution degrees on cyclophosphamide immunosuppression in mice. Immunopharmacol Immunotoxicol. 1993;15:227-242.
    1. Hanaue H, Tokuda Y, Machimura T, et al. Effects of oral lentinan on T-cell subsets in peripheral venous blood. Clin Ther. 1989;11:614-622.
    1. Suzuki I, Sakurai T, Hashimoto K, et al. Inhibition of experimental pulmonary metastasis of Lewis lung carcinoma by orally administered beta-glucan in mice. Chem Pharm Bull. 1991;39:1606-1608.
    1. Suzuki I, Tanaka H, Kinoshita A, Oikawa S, Osawa M, Yadomae T. Effect of orally administered beta-glucan on macrophage function in mice. Int J Immunopharmacol. 1990;12:675-684.
    1. Cheung NK, Modak S, Vickers A, Knuckles B. Orally administered beta-glucans enhance anti-tumor effects of monoclonal antibodies. Cancer Immunol Immunother. 2002;51:557-564.
    1. Tsukada C, Yokoyama H, Miyaji C, Ishimoto Y, Kawamura H, Abo T. Immunopotentiation of intraepithelial lymphocytes in the intestine by oral administrations of beta-glucan. Cell Immunol. 2003;221:1-5.
    1. Nabel GJ. Designing tomorrow's vaccines. N Engl J Med. 2013;368:551-560.
    1. Centers for Disease Control and Prevention (CDC). Outbreak of poliomyelitis-Dominican Republic and Haiti, 2000. MMWR Morb Mortal Wkly Rep. 2000;49:1094-1103.
    1. McNeela EA, Lavelle EC. Recent advances in microparticle and nanoparticle delivery vehicles for mucosal vaccination. Curr Top Microbiol Immunol. 2012;354:75-99.
    1. Garçon N, Hem S, Friede M. Evolution of adjuvants across the centuries. In: Plotkin S, Orenstein W, Offit P, eds. Vaccines. Philadelphia, PA: Elsevier Saunders; 2012:58-70.
    1. Olafsdottir T, Lindqvist M, Harandi AM. Molecular signatures of vaccine adjuvants. Vaccine. 2015;33:5302-5307.
    1. Reed SG, Orr MT, Fox CB. Key roles of adjuvants in modern vaccines. Nat Med. 2013;19:1597-1608.
    1. He Y, Rappuoli R, De Groot AS, Chen RT. Emerging vaccine informatics. J Biomed Biotechnol. 2010;2010:218590.
    1. Sayers S, Ulysse G, Xiang Z, He Y. Vaxjo: a web-based vaccine adjuvant database and its application for analysis of vaccine adjuvants and their uses in vaccine development. J Biomed Biotechnol. 2012;2012:831486.
    1. Newsted D, Fallahi F, Golshani A, Azizi A. Advances and challenges in mucosal adjuvant technology. Vaccine. 2015;33:2399-2405.
    1. Kagimura FY, da Cunha MA, Barbosa AM, Dekker RF, Malfatti CR. Biological activities of derivatized D-glucans: a review. Int J Biol Macromol. 2015;72:588-598.
    1. Moreno-Mendieta S, Guillen D, Hernandez-Pando R, Sanchez S, Rodriguez-Sanoja R. Potential of glucans as vaccine adjuvants: a review of the alpha-glucans case. Carbohydr Polym. 2017;165:103-114.
    1. Li P, Wang F. Polysaccharides: candidates of promising vaccine adjuvants. Drug Discov Ther. 2015;9:88-93.
    1. Goodridge HS, Wolf AJ, Underhill DM. Beta-glucan recognition by the innate immune system. Immunol Rev. 2009;230:38-50.
    1. Gallin EK, Green SW, Patchen ML. Comparative effects of particulate and soluble glucan on macrophages of C3H/HeN and C3H/HeJ mice. Int J Immunopharmacol. 1992;14:173-183.
    1. Hunter KW Jr, DuPre S, Redelman D. Microparticulate beta-glucan upregulates the expression of B7.1, B7.2, B7-H1, but not B7-DC on cultured murine peritoneal macrophages. Immunol Lett. 2004;93:71-78.
    1. Hunter KW Jr, Gault RA, Berner MD. Preparation of microparticulate beta-glucan from Saccharomyces cerevisiae for use in immune potentiation. Lett Appl Microbiol. 2002;35:267-271.
    1. Berner MD, Sura ME, Alves BN, Hunter KW Jr. IFN-gamma primes macrophages for enhanced TNF-alpha expression in response to stimulatory and non-stimulatory amounts of microparticulate beta-glucan. Immunol Lett. 2005;98:115-122.
    1. Berner VK, Sura ME, Hunter KW Jr. Conjugation of protein antigen to microparticulate beta-glucan from Saccharomyces cerevisiae: a new adjuvant for intradermal and oral immunizations. Appl Microbiol Biotechnol. 2008;80:1053-1061.
    1. Hoffman OA, Olson EJ, Limper AH. Fungal beta-glucans modulate macrophage release of tumor necrosis factor-alpha in response to bacterial lipopolysaccharide. Immunol Lett. 1993;37:19-25.
    1. Abel G, Czop JK. Stimulation of human monocyte beta-glucan receptors by glucan particles induces production of TNF-alpha and IL-1 beta. Int J Immunopharmacol. 1992;14:1363-1373.
    1. Vetvicka V, Vannucci L, Sima P. The effects of beta - glucan on fish immunity. N Am J Med Sci. 2013;5:580-588.
    1. Diao J, Ye H-B, Yu X-Q, et al. Adjuvant and immunostimulatory effects of LPS and β-glucan on immune response in Japanese flounder, Paralichthys olivaceus. Vet Immunol Immunopathol. 2013;156:167-175.
    1. Wang M, Yang R, Zhang L, et al. Sulfated glucan can improve the immune efficacy of Newcastle disease vaccine in chicken. Int J Biol Macromol. 2014;70:193-198.
    1. Ferwerda G, Meyer-Wentrup F, Kullberg BJ, Netea MG, Adema GJ. Dectin-1 synergizes with TLR2 and TLR4 for cytokine production in human primary monocytes and macrophages. Cell Microbiol. 2008;10:2058-2066.
    1. Li P, Zhang X, Cheng Y, et al. Preparation and in vitro immunomodulatory effect of curdlan sulfate. Carbohydr Polym. 2014;102:852-861.
    1. Skov J, Kania PW, Holten-Andersen L, Fouz B, Buchmann K. Immunomodulatory effects of dietary beta-1,3-glucan from Euglena gracilis in rainbow trout (Oncorhynchus mykiss) immersion vaccinated against Yersinia ruckeri. Fish Shellfish Immunol. 2012;33:111-120.
    1. Rodriguez FE, Valenzuela B, Farias A, Sandino AM, Imarai M. beta-1,3/1,6-Glucan-supplemented diets antagonize immune inhibitory effects of hypoxia and enhance the immune response to a model vaccine. Fish Shellfish Immunol. 2016;59:36-45.
    1. Li P, Tan H, Xu D, et al. Effect and mechanisms of curdlan sulfate on inhibiting HBV infection and acting as an HB vaccine adjuvant. Carbohydr Polym. 2014;110:446-455.
    1. Wang M, Zhang L, Yang R, et al. Improvement of immune responses to influenza vaccine (H5N1) by sulfated yeast beta-glucan. Int J Biol Macromol. 2016;93:203-207.
    1. Vetvicka V, Vetvickova J. Glucan supplementation enhances the immune response against an influenza challenge in mice. Ann Transl Med. 2015;3:22.
    1. Clemons KV, Antonysamy MA, Danielson ME, et al. Whole glucan particles as a vaccine against systemic coccidioidomycosis. J Med Microbiol. 2015;64:1237-1243.
    1. Specht CA, Lee CK, Huang H, et al. Vaccination with recombinant cryptococcus proteins in glucan particles protects mice against cryptococcosis in a manner dependent upon mouse strain and Cryptococcal species. MBio. 2017;8:piii: e01872-17.
    1. Mirza Z, Soto ER, Dikengil F, Levitz SM, Ostroff GR. Beta-glucan particles as vaccine adjuvant carriers. In: Kalkum M, Semis M, eds. Vaccines for Invasive Fungal Infections: Methods and Protocols. New York, NY: Humana Press; 2017:143-157.
    1. Huang H, Ostroff GR, Lee CK, Specht CA, Levitz SM. Robust stimulation of humoral and cellular immune responses following vaccination with antigen-loaded beta-glucan particles. MBio. 2010;1:piii: e00164-10.
    1. Huang H, Ostroff GR, Lee CK, Wang JP, Specht CA, Levitz SM. Distinct patterns of dendritic cell cytokine release stimulated by fungal beta-glucans and toll-like receptor agonists. Infect Immun. 2009;77:1774-1781.
    1. Miyamoto N, Mochizuki S, Fujii S, Yoshida K, Sakurai K. Adjuvant activity enhanced by cross-Linked CpG-oligonucleotides in beta-glucan nanogel and its antitumor effect. Bioconjug Chem. 2017;28:565-573.
    1. Liu H, Jia Z, Yang C, et al. Aluminum hydroxide colloid vaccine encapsulated in yeast shells with enhanced humoral and cellular immune responses. Biomaterials. 2018;167:32-43.
    1. Capper D, Jones D, Sill M, et al. DNA methylation-based classification of central nervous system tumours. Nature. 2018;555:469-474.
    1. Singh PK, Srivastava AK, Dev A, Kaundal B, Choudhury SR, Karmakar S. 1, 3beta-Glucan anchored, paclitaxel loaded chitosan nanocarrier endows enhanced hemocompatibility with efficient anti-glioblastoma stem cells therapy. Carbohydr Polym. 2018;180:365-375.
    1. Zhu K, Chen X, Yu D, He Y, Song G. Preparation and characterisation of a novel hydrogel based on Auricularia polytricha beta-glucan and its bio-release property for vitamin B12 delivery. J Sci Food Agric. 2018;98:2617-2623.
    1. Cordeiro AS, Alonso MJ, de la Fuente M. Nanoengineering of vaccines using natural polysaccharides. Biotechnol Adv. 2015;33:1279-1293.
    1. Yang Z, Xu M, Jia Z, et al. A novel antigen delivery system induces strong humoral and CTL immune responses. Biomaterials. 2017;134:51-63.
    1. Soares E, Jesus S, Borges O. Oral hepatitis B vaccine: chitosan or glucan based delivery systems for efficient HBsAg immunization following subcutaneous priming. Int J Pharm. 2018;535:261-271.
    1. De Smet R, Demoor T, Verschuere S, et al. beta-Glucan microparticles are good candidates for mucosal antigen delivery in oral vaccination. J Control Release. 2013;172:671-678.
    1. Huang H, Ostroff GR, Lee CK, Specht CA, Levitz SM. Characterization and optimization of the glucan particle-based vaccine platform. Clin Vaccine Immunol. 2013;20:1585-1591.
    1. Pan Y, Li X, Kang T, et al. Efficient delivery of antigen to DCs using yeast-derived microparticles. Sci Rep. 2015;5:10687.
    1. Wang J, Guo C, Yue T, Yuan Y, Liu X, Kennedy JF. Cationization of Ganoderma lucidum polysaccharides in concentrated alkaline solutions as gene carriers. Carbohyd Polym. 2012;88:966-972.
    1. Mochizuki S, Sakurai K. Dectin-1 targeting delivery of TNF-alpha antisense ODNs complexed with beta-1,3-glucan protects mice from LPS-induced hepatitis. J Control Release. 2011;151:155-161.
    1. Kobiyama K, Temizoz B, Kanuma T, et al. Species-dependent role of type I IFNs and IL-12 in the CTL response induced by humanized CpG complexed with beta-glucan. Eur J Immunol. 2016;46:1142-1151.
    1. Fujiwara N, Izumi H, Morimoto Y, Sakurai K, Mochizuki S. Complex consisting of antisense DNA and beta-glucan promotes internalization into cell through Dectin-1 and hybridizes with target mRNA in cytosol. Cancer Gene Ther. 2019;26:32-40.
    1. Mochizuki S, Morishita H, Sakurai K. Complex consisting of beta-glucan and antigenic peptides with cleavage site for glutathione and aminopeptidases induces potent cytotoxic T lymphocytes. Bioconjug Chem. 2017;28:2246-2253.
    1. Lee DY, Nurunnabi M, Kang SH, et al. Oral gavage delivery of PR8 antigen with beta-glucan-conjugated GRGDS carrier to enhance M-cell targeting ability and induce immunity. Biomacromol. 2017;18:1172-1179.
    1. Ludwig C, Wagner R. Virus-like particles-universal molecular toolboxes. Curr Opin Biotechnol. 2007;18:537-545.
    1. Perrie Y, Obrenovic M, McCarthy D, Gregoriadis G. Liposome (Lipodine)-mediated DNA vaccination by the oral route. J Liposome Res. 2002;12:185-197.
    1. Shi Y, Huang G. Recent developments of biodegradable and biocompatible materials based micro/nanoparticles for delivering macromolecular therapeutics. Crit Rev Ther Drug Carrier Syst. 2009;26:29-84.
    1. De Smet R, Allais L, Cuvelier CA. Recent advances in oral vaccine development: yeast-derived beta-glucan particles. Hum Vaccin Immunother. 2014;10:1309-1318.
    1. Cevher E, Salomon SK, Makrakis A, Li XW, Brocchini S, Alpar HO. Development of chitosan-pullulan composite nanoparticles for nasal delivery of vaccines: optimisation and cellular studies. J Microencapsul. 2015;32:755-768.
    1. Baert K, De Geest BG, De Greve H, Cox E, Devriendt B. Duality of beta-glucan microparticles: antigen carrier and immunostimulants. Int J Nanomedicine. 2016;11:2463-2469.
    1. Baert K, de Geest BG, de Rycke R, et al. beta-glucan microparticles targeted to epithelial APN as oral antigen delivery system. J Control Release. 2015;220:149-159.
    1. des Rieux A, Fievez V, Garinot M, Schneider YJ, Préat V. Nanoparticles as potential oral delivery systems of proteins and vaccines: a mechanistic approach. J Control Release. 2006;116:1-27.
    1. Jones DH, Corris S, McDonald S, Clegg JC, Farrar GH. Poly(DL-lactide-co-glycolide)-encapsulated plasmid DNA elicits systemic and mucosal antibody responses to encoded protein after oral administration. Vaccine. 1997;15:814-817.
    1. Holmgren J, Svennerholm AM. Vaccines against mucosal infections. Curr Opin Immunol. 2012;24:343-353.
    1. Tesz GJ, Aouadi M, Prot M, et al. Glucan particles for selective delivery of siRNA to phagocytic cells in mice. Biochem J. 2011;436:351-362.
    1. Brandtzaeg P. Function of mucosa-associated lymphoid tissue in antibody formation. Immunol Invest. 2010;39:303-355.
    1. Brayden DJ, Jepson MA, Baird AW. Keynote review: intestinal Peyer's patch M cells and oral vaccine targeting. Drug Discov Today. 2005;10:1145-1157.

Source: PubMed

3
S'abonner