NAVIGATING THE LANDSCAPE OF ADJUVANTS FOR SUBUNIT VACCINES: RECENT ADVANCES AND FUTURE PERSPECTIVES
DOI:
https://doi.org/10.22159/ijap.2024v16i1.49563Keywords:
Adjuvants, Delivery systems, Immune response, Subunit vaccinesAbstract
The development of effective subunit vaccines relies on the incorporation of adjuvants to enhance immune responses and improve vaccine efficacy. This paper provides a comprehensive review of the various adjuvants employed in subunit vaccine development, with an emphasis on liposome-based, carbohydrate-based, polymer-based, and nanoparticle-based adjuvants. Additionally, the general concept of vaccine adjuvants, their classification into different types, and the underlying molecular mechanisms by which they exert their immunostimulatory effects are discussed. The use of adjuvants in subunit vaccine development has revolutionized immunization strategies by enhancing vaccine efficacy and inducing robust immune responses. Further research is needed to understand the safety profiles of adjuvants, elucidate the underlying molecular mechanisms, and optimize the adjuvant formulations. By harnessing the power of adjuvants, we can advance the development of effective subunit vaccines against infectious diseases and malignancies, thereby contributing to global health outcomes.
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Powell MF, Newman MJ. Vaccine design: the subunit and adjuvant approach. Springer; 2012. p. 977.
Skwarczynski M, Toth I. Peptide-based synthetic vaccines. Chem Sci. 2016 Feb 1;7(2):842-54. doi: 10.1039/c5sc03892h, PMID 28791117.
Skwarczynski M, Toth I. Recent advances in peptide-based subunit nanovaccines. Nanomedicine (Lond). 2014 Dec;9(17):2657-69. doi: 10.2217/nnm.14.187, PMID 25529569.
Nevagi RJ, Toth I, Skwarczynski M. 12-peptide-based vaccines. In: Woodhead publishing. Peptide applications in biomedicine, biotechnology and bioengineering; 2018. p. 327-58. Available from: https://www.sciencedirect.com/science/article/pii/B9780081007365000120. [Last accessed on 02 Jul 2023]
Azmi F, Ahmad Fuaad AAH, Skwarczynski M, Toth I. Recent progress in adjuvant discovery for peptide-based subunit vaccines. Hum Vaccin Immunother. 2014 Mar 1;10(3):778-96. doi: 10.4161/hv.27332, PMID 24300669.
Singh M, O’Hagan DT. Recent advances in vaccine adjuvants. Pharm Res. 2002 Jun 1;19(6):715-28. doi: 10.1023/a:1016104910582, PMID 12134940.
Pashine A, Valiante NM, Ulmer JB. Targeting the innate immune response with improved vaccine adjuvants. Nat Med. 2005 Apr;11(4)Suppl:S63-8. doi: 10.1038/nm1210, PMID 15812492.
Shah RR, Hassett KJ, Brito LA. Overview of vaccine adjuvants: introduction, history, and current status. In: New York: Springer; 2017. p. 1-13. doi: 10.1007/978-1-4939-6445-1_1.
Olive C. Pattern recognition receptors: sentinels in innate immunity and targets of new vaccine adjuvants. Expert Rev Vaccines. 2012 Feb 1;11(2):237-56. doi: 10.1586/erv.11.189, PMID 22309671.
Brito LA, Malyala P, O’Hagan DT. Vaccine adjuvant formulations: a pharmaceutical perspective. Semin Immunol. 2013 Apr 1;25(2):130-45. doi: 10.1016/j.smim.2013.05.007, PMID 23850011.
Petrovsky N. Comparative safety of vaccine adjuvants: a summary of current evidence and future needs. Drug Saf. 2015 Nov 1;38(11):1059-74. doi: 10.1007/s40264-015-0350-4, PMID 26446142.
Corradin G, Giudice GD. Novel adjuvants for vaccines. CMCAIAA. 2005;4(2):185-91. doi: 10.2174/1568014053507113.
Cross RTK, Alan S. Adjuvants for the future. In: New generation vaccines. 4th ed. CRC Press; 2010.
Peek LJ, Middaugh CR, Berkland C. Nanotechnology in vaccine delivery. Adv Drug Deliv Rev. 2008 May 22;60(8):915-28. doi: 10.1016/j.addr.2007.05.017, PMID 18325628.
He P, Zou Y, Hu Z. Advances in aluminum hydroxide-based adjuvant research and its mechanism. Hum Vaccin Immunother. 2015 Feb 1;11(2):477-88. doi: 10.1080/21645515.2014.1004026, PMID 25692535.
Garcia A, De Sanctis JB. An overview of adjuvant formulations and delivery systems. APMIS. 2014;122(4):257-67. doi: 10.1111/apm.12143, PMID 23919674.
Tritto E, Mosca F, De Gregorio E. Mechanism of action of licensed vaccine adjuvants. Vaccine. 2009 May 26;27(25-26):3331-4. doi: 10.1016/j.vaccine.2009.01.084, PMID 19200813.
Crooke SN, Ovsyannikova IG, Poland GA, Kennedy RB. Immunosenescence and human vaccine immune responses. Immun Ageing. 2019 Sep 13;16(1):25. doi: 10.1186/s12979-019-0164-9, PMID 31528180.
Mahedi MRA, Rawat A, Rabbi F, Babu KS, Tasayco ES, Areche FO. Understanding the global transmission and demographic distribution of Nipah virus (NiV). Res J Pharm Technol. 2023 Aug 31;16(8):3588-94.
Petkar KC, Patil SM, Chavhan SS, Kaneko K, Sawant KK, Kunda NK. An overview of nanocarrier-based adjuvants for vaccine delivery. Pharmaceutics. 2021 Apr;13(4):455. doi: 10.3390/pharmaceutics13040455, PMID 33801614.
Facciola A, Visalli G, Lagana A, Di Pietro A. An overview of vaccine adjuvants: current evidence and future perspectives. Vaccines. 2022 May;10(5):819. doi: 10.3390/vaccines10050819, PMID 35632575.
Henriksen Lacey M, Korsholm KS, Andersen P, Perrie Y, Christensen D. Liposomal vaccine delivery systems. Expert Opin Drug Deliv. 2011 Apr;8(4):505-19. doi: 10.1517/17425247.2011.558081, PMID 21413904.
Schwendener RA. Liposomes as vaccine delivery systems: a review of the recent advances. Ther Adv Vaccines. 2014 Nov;2(6):159-82. doi: 10.1177/2051013614541440, PMID 25364509.
Sanders MT, Brown LE, Deliyannis G, Pearse MJ. ISCOM-based vaccines: the second decade. Immunol Cell Biol. 2005 Apr;83(2):119-28. doi: 10.1111/j.1440-1711.2005.01319.x, PMID 15748208.
Pearse MJ, Drane D. ISCOMATRIX adjuvant for antigen delivery. Adv Drug Deliv Rev. 2005 Jan 10;57(3):465-74. doi: 10.1016/j.addr.2004.09.006, PMID 15560952.
Baz Morelli A, Becher D, Koernig S, Silva A, Drane D, Maraskovsky E. ISCOMATRIX: a novel adjuvant for use in prophylactic and therapeutic vaccines against infectious diseases. J Med Microbiol. 2012 Jul;61(7):935-43. doi: 10.1099/jmm.0.040857-0, PMID 22442293.
Apostolico Jde S, Lunardelli VAS, Coirada FC, Boscardin SB, Rosa DS. Adjuvants: classification, modus operandi, and licensing. J Immunol Res. 2016;2016:1459394. doi: 10.1155/2016/1459394, PMID 27274998.
Stephen J, Scales HE, Benson RA, Erben D, Garside P, Brewer JM. Neutrophil swarming and extracellular trap formation play a significant role in Alum adjuvant activity. NPJ Vaccines. 2017 Jan 23;2(1):1. doi: 10.1038/s41541-016-0001-5, PMID 29263862.
Nkolola JP, Cheung A, Perry JR, Carter D, Reed S, Schuitemaker H. Comparison of multiple adjuvants on the stability and immunogenicity of a clade C HIV-1 gp140 trimer. Vaccine. 2014 Apr 11;32(18):2109-16. doi: 10.1016/j.vaccine.2014.02.001, PMID 24556505.
Querec T, Bennouna S, Alkan S, Laouar Y, Gorden K, Flavell R. Yellow fever vaccine YF-17D activates multiple dendritic cell subsets via TLR2, 7, 8, and 9 to stimulate polyvalent immunity. J Exp Med. 2006 Feb 20;203(2):413-24. doi: 10.1084/jem.20051720, PMID 16461338.
Kim YG. Microbiota influences vaccine and mucosal adjuvant efficacy. Immune Netw. 2017 Feb;17(1):20-4. doi: 10.4110/in.2017.17.1.20, PMID 28261017.
Didierlaurent AM, Morel S, Lockman L, Giannini SL, Bisteau M, Carlsen H. Garçon N. AS04, an aluminum salt-and TLR4 agonist-based adjuvant system, induces a transient localized innate immune response leading to enhanced adaptive immunity. J Immunol Baltim Md. 2009;183(10):6186-97.
Cekic C, Casella CR, Eaves CA, Matsuzawa A, Ichijo H, Mitchell TC. Selective activation of the p38 MAPK pathway by synthetic monophosphoryl lipid A. J Biol Chem. 2009 Nov 13;284(46):31982-91. doi: 10.1074/jbc.M109.046383, PMID 19759006.
Mosca F, Tritto E, Muzzi A, Monaci E, Bagnoli F, Iavarone C. Molecular and cellular signatures of human vaccine adjuvants. Proc Natl Acad Sci USA. 2008 Jul 29;105(30):10501-6. doi: 10.1073/pnas.0804699105, PMID 18650390.
De Gregorio E, Caproni E, Ulmer JB. Vaccine adjuvants: mode of action. Front Immunol. 2013;4:214. doi: 10.3389/fimmu.2013.00214, PMID 23914187.
Seubert A, Monaci E, Pizza M, O’Hagan DT, Wack A. The adjuvants aluminum hydroxide and MF59 induce monocyte and granulocyte chemoattractants and enhance monocyte differentiation toward dendritic cells. J Immunol. 2008;180(8):5402-12. doi: 10.4049/jimmunol.180.8.5402, PMID 18390722.
BP, RA. Immunological mechanisms of vaccination. Nat Immunol. 2011 Jun;12(6). Available from: https://pubmed.ncbi.nlm.nih.gov/21739679.
Burny W, Callegaro A, Bechtold V, Clement F, Delhaye S, Fissette L. Different adjuvants induce common innate pathways that are associated with enhanced adaptive responses against a model antigen in humans. Front Immunol. 2017;8:943. doi: 10.3389/fimmu.2017.00943, PMID 28855902.
Pulendran B, Oh JZ, Nakaya HI, Ravindran R, Kazmin DA. Immunity to viruses: learning from successful human vaccines. Immunol Rev. 2013 Sep;255(1):243-55. doi: 10.1111/imr.12099, PMID 23947360.
Ho NI, Huis in’t Veld LGM, Raaijmakers TK, Adema GJ. Adjuvants enhancing cross-presentation by dendritic cells: the key to more effective vaccines? Front Immunol. 2018;9:2874. doi: 10.3389/fimmu.2018.02874, PMID 30619259.
Toussi DN, Massari P. Immune adjuvant effect of molecularly defined toll-like receptor ligands. Vaccines. 2014 Apr 25;2(2):323-53. doi: 10.3390/vaccines2020323, PMID 26344622.
Cimica V, Boigard H, Bhatia B, Fallon JT, Alimova A, Gottlieb P. Novel respiratory syncytial virus-like particle vaccine composed of the postfusion and prefusion conformations of the F glycoprotein. Clin Vaccine Immunol. 2016 Jun;23(6):451-9. doi: 10.1128/CVI.00720-15, PMID 27030590.
Mastelic B, Ahmed S, Egan WM, Del Giudice G, Golding H, Gust I. Mode of action of adjuvants: implications for vaccine safety and design. Biologicals. 2010 Sep;38(5):594-601. doi: 10.1016/j.biologicals.2010.06.002, PMID 20659806.
Bolhassani A. Lipid-based delivery systems in development of genetic and subunit vaccines. Mol Biotechnol. 2023 May 1;65(5):669-98. doi: 10.1007/s12033-022-00624-8, PMID 36462102.
Raoufi E, Bahramimeimandi B, Salehi Shadkami M, Chaosri P, Mozafari MR. Methodical design of viral vaccines based on avant-garde nanocarriers: a multi-domain narrative review. Biomedicines. 2021 May 6;9(5):520. doi: 10.3390/biomedicines9050520, PMID 34066608.
Okay S, Ozge Ozcan O, Karahan M. Nanoparticle-based delivery platforms for mRNA vaccine development. AIMS Biophys. 2020;7(4):323-38. doi: 10.3934/biophy.2020023.
Tretiakova DS, Vodovozova EL. Liposomes as adjuvants and vaccine delivery systems. Biochem (Mosc) Suppl Ser A Membr Cell Biol. 2022 Mar 1;16(1):1-20. doi: 10.1134/S1990747822020076, PMID 35194485.
Luwi NM, Ahmad S, Azlyna AN, Nordin A, Sarmiento ME, Acosta A. Liposomes as immunological adjuvants and delivery systems in the development of tuberculosis vaccine: a review. Asian Pac J Trop Med. 2022 Jan;15(1):7. doi: 10.4103/1995-7645.332806.
Fobian SF, Cheng Z, Ten Hagen TLM. Smart lipid-based nanosystems for therapeutic immune induction against cancers: perspectives and outlooks. Pharmaceutics. 2021;14(1):26. doi: 10.3390/pharmaceutics14010026, PMID 35056922.
De Serrano LO, Burkhart DJ. Liposomal vaccine formulations as prophylactic agents: design considerations for modern vaccines. J Nanobiotechnology. 2017 Nov 17;15(1):83. doi: 10.1186/s12951-017-0319-9, PMID 29149896.
Khademi F, Taheri RA, Momtazi Borojeni AA, Farnoosh G, Johnston TP, Sahebkar A. Potential of cationic liposomes as adjuvants/delivery systems for tuberculosis subunit vaccines. Rev Physiol Biochem Pharmacol. 2018;175:47-69. doi: 10.1007/112_2018_9, PMID 29700609.
Tang J, Cai L, Xu C, Sun S, Liu Y, Rosenecker J. Nanotechnologies in delivery of DNA and mRNA vaccines to the nasal and pulmonary mucosa. Nanomaterials (Basel). 2022 Jan 11;12(2):226. doi: 10.3390/nano12020226, PMID 35055244.
Bashiri S, Koirala P, Toth I, Skwarczynski M. Carbohydrate immune adjuvants in subunit vaccines. Pharmaceutics. 2020 Oct;12(10):965. doi: 10.3390/pharmaceutics12100965, PMID 33066594.
Sun B, Yu S, Zhao D, Guo S, Wang X, Zhao K. Polysaccharides as vaccine adjuvants. Vaccine. 2018 Aug 23;36(35):5226-34. doi: 10.1016/j.vaccine.2018.07.040, PMID 30057282.
Geijtenbeek TBH, Van Kooyk Y. Pathogens target DC-SIGN to influence their fate DC-SIGN functions as a pathogen receptor with broad specificity. APMIS. 2003;111(7-8):698-714. doi: 10.1034/j.1600-0463.2003.11107803.x, PMID 12974773.
Yamasaki S, Matsumoto M, Takeuchi O, Matsuzawa T, Ishikawa E, Sakuma M. C-type lectin Mincle is an activating receptor for pathogenic fungus, Malassezia. Proc Natl Acad Sci USA. 2009 Feb 10;106(6):1897-902. doi: 10.1073/pnas.0805177106, PMID 19171887.
Zhang C, Shi G, Zhang J, Song H, Niu J, Shi S. Targeted antigen delivery to dendritic cell via functionalized alginate nanoparticles for cancer immunotherapy. J Control Release. 2017 Jun 28;256:170-81. doi: 10.1016/j.jconrel.2017.04.020, PMID 28414151.
Zhu D, Hu C, Fan F, Qin Y, Huang C, Zhang Z. Co-delivery of antigen and dual agonists by programmed mannose-targeted cationic lipid-hybrid polymersomes for enhanced vaccination. Biomaterials. 2019 Jun;206:25-40. doi: 10.1016/j.biomaterials.2019.03.012, PMID 30925286.
He LZ, Crocker A, Lee J, Mendoza Ramirez J, Wang XT, Vitale LA. Antigenic targeting of the human mannose receptor induces tumor immunity. J Immunol. 2007 May 15;178(10):6259-67. doi: 10.4049/jimmunol.178.10.6259, PMID 17475854.
Dabaghian M, Latifi AM, Tebianian M, Najmi Nejad H, Ebrahimi SM. Nasal vaccination with r4M2e.HSP70c antigen encapsulated into N-trimethyl chitosan (TMC) nanoparticulate systems: preparation and immunogenicity in a mouse model. Vaccine. 2018 May 11;36(20):2886-95. doi: 10.1016/j.vaccine.2018.02.072, PMID 29627234.
Dalle Vedove E, Costabile G, Merkel OM. Mannose and mannose-6-phosphatereceptor–targeted drug delivery systems and their application in cancer therapy. Adv Healthc Mater. 2018;7(14):e1701398. doi: 10.1002/adhm.201701398, PMID 29719138.
Glaffig M, Stergiou N, Hartmann S, Schmitt E, Kunz H. A synthetic MUC1 anticancer vaccine containing mannose ligands for targeting macrophages and dendritic cells. Chem Med Chem. 2018;13(1):25-9. doi: 10.1002/cmdc.201700646, PMID 29193802.
Cordeiro AS, Alonso MJ. Recent advances in vaccine delivery. Pharm Pat Anal. 2016;5(1):49-73. doi: 10.4155/ppa.15.38, PMID 26667309.
GO, ES. Oral macrophage-mediated gene delivery system. Tech Conn Briefs. 2007;2:378-81.
Goodridge HS, Reyes CN, Becker CA, Katsumoto TR, Ma J, Wolf AJ. Activation of the innate immune receptor dectin-1 upon formation of a ‘phagocytic synapse’ Nature. 2011 Apr;472(7344):471-5. doi: 10.1038/nature10071, PMID 21525931.
Dedloff MR, Effler CS, Holban AM, Gestal MC. Use of biopolymers in mucosally-administered vaccinations for respiratory disease. Materials (Basel). 2019 Jan;12(15):2445. doi: 10.3390/ma12152445, PMID 31370286.
Kagimura FY, da Cunha MAA, Barbosa AM, Dekker RFH, Malfatti CRM. Biological activities of derivatized d-glucans: a review. Int J Biol Macromol. 2015 Jan 1;72:588-98. doi: 10.1016/j.ijbiomac.2014.09.008, PMID 25239192.
Jin JW, Peng WL, Tang SQ, Rong MZ, Zhang MQ. Antigen uptake and immunoadjuvant activity of pathogen-mimetic hollow silica particles conjugated with β-glucan. J Mater Chem B. 2018 Oct 10;6(39):6288-301. doi: 10.1039/c8tb02129e, PMID 32254619.
Kim S, Patel DS, Park S, Slusky J, Klauda JB, Widmalm G. Bilayer properties of lipid a from various gram-negative bacteria. Biophys J. 2016 Oct 18;111(8):1750-60. doi: 10.1016/j.bpj.2016.09.001, PMID 27760361.
Persing DH, Coler RN, Lacy MJ, Johnson DA, Baldridge JR, Hershberg RM. Taking toll: lipid a mimetics as adjuvants and immunomodulators. Trends Microbiol. 2002 Oct 1;10(10)Suppl:S32-7. doi: 10.1016/s0966-842x(02)02426-5, PMID 12377566.
Patil HP, Murugappan S, Ter Veer W, Meijerhof T, de Haan A, Frijlink HW. Evaluation of monophosphoryl lipid as adjuvant for pulmonary delivered influenza vaccine. J Control Release. 2014 Jan 28;174:51-62. doi: 10.1016/j.jconrel.2013.11.013, PMID 24269505.
Chong CSW, Cao M, Wong WW, Fischer KP, Addison WR, Kwon GS. Enhancement of T helper type 1 immune responses against hepatitis B virus core antigen by PLGA nanoparticle vaccine delivery. J Control Release. 2005 Jan 20;102(1):85-99. doi: 10.1016/j.jconrel.2004.09.014, PMID 15653136.
Hu X, Liu R, Zhu N. Enhancement of humoral and cellular immune responses by monophosphoryl lipid a (MPLA) as an adjuvant to the rabies vaccine in BALB/c mice. Immunobiology. 2013 Dec;218(12):1524-8. doi: 10.1016/j.imbio.2013.05.006, PMID 23816301.
Golkar M, Shokrgozar MA, Rafati S, Musset K, Assmar M, Sadaie R. Evaluation of protective effect of recombinant dense granule antigens GRA2 and GRA6 formulated in monophosphoryl lipid a (MPL) adjuvant against toxoplasma chronic infection in mice. Vaccine. 2007 May 22;25(21):4301-11. doi: 10.1016/j.vaccine.2007.02.057, PMID 17418457.
Van Dissel JT, Joosten SA, Hoff ST, Soonawala D, Prins C, Hokey DA. A novel liposomal adjuvant system, CAF01, promotes long-lived mycobacterium tuberculosis-specific t-cell responses in human. Vaccine. 2014 Dec 12;32(52):7098-107. doi: 10.1016/j.vaccine.2014.10.036, PMID 25454872.
Braganza CD, Teunissen T, Timmer MSM, Stocker BL. Identification and biological activity of synthetic macrophage inducible c-type lectin ligands. Front Immunol. 2017;8:1940. doi: 10.3389/fimmu.2017.01940, PMID 29387054. Available from: https://www.frontiersin.org/articles/10.3389/fimmu.2017.01940.
Smith AJ, Miller SM, Buhl C, Child R, Whitacre M, Schoener R. Species-specific structural requirements of alpha-branched trehalose diester mincle agonists. Front Immunol. 2019;10:338. doi: 10.3389/fimmu.2019.00338, PMID 30873180. Available from: https://www.frontiersin.org/articles/10.3389/fimmu.2019.00338.
Gram GJ, Karlsson I, Agger EM, Andersen P, Fomsgaard A. A novel liposome-based adjuvant CAF01 for induction of CD8(+) cytotoxic T-lymphocytes (CTL) to HIV-1 minimal CTL peptides in HLA-A*0201 transgenic mice. PLOS ONE. 2009 Sep 11;4(9):e6950. doi: 10.1371/journal.pone.0006950, PMID 19759892.
Kamstrup S, San Martin R, Doberti A, Grande H, Dalsgaard K. Preparation and characterisation of quillaja saponin with less heterogeneity than quil-a. Vaccine. 2000 Apr 1;18(21):2244-9. doi: 10.1016/s0264-410x(99)00560-5, PMID 10717344.
Fernández Tejada A, Tan DS, Gin DY. Development of improved vaccine adjuvants based on the saponin natural product QS-21 through chemical synthesis. Acc Chem Res. 2016 Sep 20;49(9):1741-56. doi: 10.1021/acs.accounts.6b00242, PMID 27568877.
Pink JR, Kieny MP. 4th. Meeting on novel adjuvants currently in/close to human clinical testing. 2004 Jun 2;22(17-18):2097-102. doi: 10.1016/j.vaccine.2004.01.021.
Marciani DJ. Is fucose the answer to the immunomodulatory paradox of Quillaja saponins? Int Immunopharmacol. 2015 Dec;29(2):908-13. doi: 10.1016/j.intimp.2015.10.028, PMID 26603552.
Oda K, Matsuda H, Murakami T, Katayama S, Ohgitani T, Yoshikawa M. Adjuvant and haemolytic activities of 47 saponins derived from medicinal and food plants. Biol Chem. 2000 Jan 28;381(1):67-74. doi: 10.1515/BC.2000.009, PMID 10722052.
Sun H, Chen L, Wang J, Wang K, Zhou J.Structure–function relationship of the saponins from the roots of platycodon grandiflorum for hemolytic and adjuvant activity. Int Immunopharmacol. 2011 Dec 1;11(12):2047-56. doi: 10.1016/j.intimp.2011.08.018, PMID 21945665.
Moghimipour E, Saponin HS. Properties, methods of evaluation and applications. Annu Res Rev Biol. 2015:207-20.
Kashala O, Amador R, Valero MV, Moreno A, Barbosa A, Nickel B. Safety, tolerability and immunogenicity of new formulations of the plasmodium falciparum malaria peptide vaccine SPf66 combined with the immunological adjuvant QS-21. Vaccine. 2002 May 22;20(17-18):2263-77. doi: 10.1016/s0264-410x(02)00115-9, PMID 12009282.
Fujii SI, Shimizu K, Smith C, Bonifaz L, Steinman RM. Activation of natural killer T cells by alpha-galactosylceramide rapidly induces the full maturation of dendritic cells in vivo and thereby acts as an adjuvant for combined CD4 and CD8 T cell immunity to a coadministered protein. J Exp Med. 2003 Jul 21;198(2):267-79. doi: 10.1084/jem.20030324, PMID 12874260.
Reilly EC, Thompson EA, Aspeslagh S, Wands JR, Elewaut D, Brossay L. Activated iNKT cells promote memory CD8+T cell differentiation during viral infection. PLOS ONE. 2012 May 23;7(5):e37991. doi: 10.1371/journal.pone.0037991, PMID 22649570.
Kawano T, Cui J, Koezuka Y, Toura I, Kaneko Y, Motoki K. CD1d-restricted and TCR-mediated activation of valpha14 NKT cells by glycosylceramides. Science. 1997 Nov 28;278(5343):1626-9. doi: 10.1126/science.278.5343.1626, PMID 9374463.
Wang S, Liu H, Zhang X, Qian F. Intranasal and oral vaccination with protein-based antigens: advantages, challenges and formulation strategies. Protein Cell. 2015 Jul 1;6(7):480-503. doi: 10.1007/s13238-015-0164-2, PMID 25944045.
Ko SY, Ko HJ, Chang WS, Park SH, Kweon MN, Kang CY. Alpha-galactosylceramide can act as a nasal vaccine adjuvant, inducing protective immune responses against viral infection and tumor. J Immunol. 2005;175(5):3309-17. doi: 10.4049/jimmunol.175.5.3309, PMID 16116223.
Moschos SA, Bramwell VW, Somavarapu S, Alpar HO. Adjuvant synergy: the effects of nasal coadministration of adjuvants. Immunol Cell Biol. 2004 Dec;82(6):628-37. doi: 10.1111/j.0818-9641.2004.01280.x, PMID 15550121.
Kawai T, Akira S. The role of pattern-recognition receptors in innate immunity: update on toll-like receptors. Nat Immunol. 2010 May;11(5):373-84. doi: 10.1038/ni.1863, PMID 20404851.
Maisonneuve C, Bertholet S, Philpott DJ, De Gregorio E. Unleashing the potential of NOD and toll-like agonists as vaccine adjuvants. Proc Natl Acad Sci USA. 2014 Aug 26;111(34):12294-9. doi: 10.1073/pnas.1400478111, PMID 25136133.
Orosco FL. Current progress in diagnostics, therapeutics, and vaccines for African swine fever virus. VIS. 2023 Jun 19;21(3):751-81. doi: 10.12982/VIS.2023.054.
Zhou CJ, Chen J, Hou JB, Zheng Y, Yu YN, He H. The immunological functions of muramyl dipeptide compound adjuvant on humoral, cellular-mediated and mucosal immune responses to PEDV inactivated vaccine in mice. Protein Pept Lett. 2018;25(10):908-13. doi: 10.2174/0929866525666180917160926, PMID 30227812.
Orosco FL. Immune evasion mechanisms of porcine epidemic diarrhea virus: a comprehensive review. Vet Integr Sci. 2024;22(1):171-92.
Bacon A, Makin J, Sizer PJ, Jabbal Gill I, Hinchcliffe M, Illum L. Carbohydrate biopolymers enhance antibody responses to mucosally delivered vaccine antigens. Infect Immun. 2000 Oct;68(10):5764-70. doi: 10.1128/IAI.68.10.5764-5770.2000, PMID 10992483.
Nevagi RJ, Skwarczynski M, Toth I. Polymers for subunit vaccine delivery. Eur Polym J. 2019 May 1;114:397-410. doi: 10.1016/j.eurpolymj.2019.03.009.
Netea MG, Gow NAR, Munro CA, Bates S, Collins C, Ferwerda G. Immune sensing of Candida albicans requires cooperative recognition of mannans and glucans by lectin and toll-like receptors. J Clin Invest. 2006 Jun;116(6):1642-50. doi: 10.1172/JCI27114, PMID 16710478.
Bartheldyova E, Turanek Knotigova P, Zachova K, Masek J, Kulich P, Effenberg R. N-oxy lipid-based click chemistry for orthogonal coupling of mannan onto nanoliposomes prepared by microfluidic mixing: synthesis of lipids, characterisation of mannan-coated nanoliposomes and in vitro stimulation of dendritic cells. Carbohydr Polym. 2019 Mar 1;207:521-32. doi: 10.1016/j.carbpol.2018.10.121, PMID 30600036.
François Heude M, Mendez Ardoy A, Cendret V, Lafite P, Daniellou R, Ortiz Mellet C. Synthesis of high-mannose oligosaccharide analogues through click chemistry: true functional mimics of their natural counterparts against lectins? Chemistry. 2015;21(5):1978-91. doi: 10.1002/chem.201405481, PMID 25483029.
Han J, Zhao D, Li D, Wang X, Jin Z, Zhao K. Polymer-based nanomaterials and applications for vaccines and drugs. Polymers. 2018 Jan;10(1):31. doi: 10.3390/polym10010031, PMID 30966075.
Zhang X, Qi C, Guo Y, Zhou W, Zhang Y. Toll-like receptor 4-related immunostimulatory polysaccharides: primary structure, activity relationships, and possible interaction models. Carbohydr Polym. 2016 Sep 20;149:186-206. doi: 10.1016/j.carbpol.2016.04.097, PMID 27261743.
Wu Y, Yan C, He J, Xiong W, Wu S, Liu S. Reversible mannosylation as a covalent binding adjuvant enhances immune responses for porcine circovirus type 2 vaccine. ACS Omega. 2018 Dec 31;3(12):17341-7. doi: 10.1021/acsomega.8b02264.
Sarmento B, Das NJ. Chitosan-based systems for biopharmaceuticals: delivery, targeting and polymer therapeutics. John Wiley & Sons; 2012. p. 691.
Zhang J, Xia W, Liu P, Cheng Q, Tahirou T, Gu W. Chitosan modification and pharmaceutical/biomedical applications. Mar Drugs. 2010 Jul;8(7):1962-87. doi: 10.3390/md8071962, PMID 20714418.
Zaharoff DA, Rogers CJ, Hance KW, Schlom J, Greiner JW. Chitosan solution enhances both humoral and cell-mediated immune responses to subcutaneous vaccination. Vaccine. 2007 Mar 1;25(11):2085-94. doi: 10.1016/j.vaccine.2006.11.034, PMID 17258843.
Li X, Min M, Du N, Gu Y, Hode T, Naylor M. Chitin, chitosan, and glycated chitosan regulate immune responses: the novel adjuvants for cancer vaccine. Clin Dev Immunol. 2013:387023. doi: 10.1155/2013/387023, PMID 23533454.
Marasini N, Skwarczynski M, Toth I. Intranasal delivery of nanoparticle-based vaccines. Ther Deliv. 2017 Mar;8(3):151-67. doi: 10.4155/tde-2016-0068, PMID 28145824.
Jain S, Khomane K, Jain AK, Dani P. Nanocarriers for transmucosal vaccine delivery. Curr Nanosci. 2011;7(2):160-77. doi: 10.2174/157341311794653541.
Sui Z, Chen Q, Fang F, Zheng M, Chen Z. Cross-protection against influenza virus infection by intranasal administration of M1-based vaccine with chitosan as an adjuvant. Vaccine. 2010 Nov 10;28(48):7690-8. doi: 10.1016/j.vaccine.2010.09.019, PMID 20870054.
Otterlei M, Ostgaard K, Skjak Braek G, Smidsrod O, Soon Shiong P, Espevik T. Induction of cytokine production from human monocytes stimulated with alginate. J Immunother. 1991 Aug;10(4):286-91. doi: 10.1097/00002371-199108000-00007, PMID 1931864.
Farjaha A, Owlia P, Siadat SD, Mousavi SF, Shafieeardestani M. Conjugation of alginate to a synthetic peptide containing T- and B-cell epitopes as an induction for protective immunity against Pseudomonas Aeruginosa. J Biotechnol. 2014 Dec 20;192(A):240-7. doi: 10.1016/j.jbiotec.2014.10.025, PMID 25449544.
Kogan G, Soltes L, Stern R, Gemeiner P. Hyaluronic acid: a natural biopolymer with a broad range of biomedical and industrial applications. Biotechnol Lett. 2007 Jan;29(1):17-25. doi: 10.1007/s10529-006-9219-z, PMID 17091377.
Necas J, Bartosikova L, Brauner P, Kolar J. Hyaluronic acid (hyaluronan): a review. Vet Med. 2008 Aug 31;53(8):397-411. doi: 10.17221/1930-VETMED.
Kong WH, Sung DK, Kim H, Yang JA, Ieronimakis N, Kim KS. Self-adjuvanted hyaluronate–antigenic peptide conjugate for transdermal treatment of muscular dystrophy. Biomaterials. 2016 Mar 1;81:93-103. doi: 10.1016/j.biomaterials.2015.12.007, PMID 26724457.
Termeer C, Benedix F, Sleeman J, Fieber C, Voith U, Ahrens T. Oligosaccharides of hyaluronan activate dendritic cells via toll-like receptor 4. J Exp Med. 2002 Jan 7;195(1):99-111. doi: 10.1084/jem.20001858, PMID 11781369.
Gariboldi S, Palazzo M, Zanobbio L, Selleri S, Sommariva M, Sfondrini L. Low molecular weight hyaluronic acid increases the self-defense of skin epithelium by induction of β-defensin 2 via TLR2 and TLR4. J Immunol. 2008 Aug 1;181(3):2103-10. doi: 10.4049/jimmunol.181.3.2103, PMID 18641349.
Lees A, Finkelman F, Inman JK, Witherspoon K, Johnson P, Kennedy J. Enhanced immunogenicity of protein-dextran conjugates: I. Rapid stimulation of enhanced antibody responses to poorly immunogenic molecules. Vaccine. 1994 Jan 1;12(13):1160-6. doi: 10.1016/0264-410x(94)90237-2, PMID 7530886.
Shinchi H, Crain B, Yao S, Chan M, Zhang SS, Ahmadiiveli A. Enhancement of the immunostimulatory activity of a TLR7 ligand by conjugation to polysaccharides. Bioconjug Chem. 2015 Jan 1;26(8):1713-23. doi: 10.1021/acs.bioconjchem.5b00285, PMID 26193334.
Zhang W, An M, Xi J, Liu H. Targeting CpG adjuvant to lymph node via dextran conjugate enhances antitumor immunotherapy. Bioconjug Chem. 2017 Jan 1;28(7):1993-2000. doi: 10.1021/acs.bioconjchem.7b00313, PMID 28644608.
Luo M, Shao B, Nie W, Wei XW, Li YL, Wang BL. Antitumor and adjuvant activity of λ-carrageenan by stimulating immune response in cancer immunotherapy. Sci Rep. 2015 Jun 22;5:11062. doi: 10.1038/srep11062, PMID 26098663.
Zhang YQ, Tsai YC, Monie A, Hung CF, Wu TC. Carrageenan as an adjuvant to enhance peptide-based vaccine potency. Vaccine. 2010 Jul 19;28(32):5212-9. doi: 10.1016/j.vaccine.2010.05.068, PMID 20541583.
Sinha VR, Bansal K, Kaushik R, Kumria R, Trehan A. Poly-ε-caprolactone microspheres and nanospheres: an overview. Int J Pharm. 2004 Jun 18;278(1):1-23. doi: 10.1016/j.ijpharm.2004.01.044, PMID 15158945.
Jameela SR, Suma N, Misra A, Raghuvanshi R, Ganga S, Jayakrishnan A. Poly(ε-caprolactone) microspheres as a vaccine carrier. Curr Sci. 1996;70(7):669-71.
Slobbe L, Medlicott N, Lockhart E, Davies N, Tucker I, Razzak M. A prolonged immune response to antigen delivered in poly (epsilon-caprolactone) microparticles. Immunol Cell Biol. 2003 Jun;81(3):185-91. doi: 10.1046/j.1440-1711.2003.01155.x, PMID 12752682.
Cruz LJ, Tacken PJ, Eich C, Rueda F, Torensma R, Figdor CG. Controlled release of antigen and toll-like receptor ligands from PLGA nanoparticles enhances immunogenicity. Nanomedicine (Lond). 2017 Mar;12(5):491-510. doi: 10.2217/nnm-2016-0295, PMID 28181470.
Hamdy S, Haddadi A, Hung RW, Lavasanifar A. Targeting dendritic cells with nano-particulate PLGA cancer vaccine formulations. Adv Drug Deliv Rev. 2011 Sep 10;63(10-11):943-55. doi: 10.1016/j.addr.2011.05.021, PMID 21679733.
Bailey BA, Desai KH, Ochyl LJ, Ciotti SM, Moon JJ, Schwendeman SP. Self-encapsulating poly(lactic-co-glycolic acid) (PLGA) microspheres for intranasal vaccine delivery. Mol Pharm. 2017 Sep 5;14(9):3228-37. doi: 10.1021/acs.molpharmaceut.7b00586, PMID 28726424.
Inbaraj BS, Chen BH. In vitro removal of toxic heavy metals by poly(γ-glutamic acid)-coated superparamagnetic nanoparticles. Int J Nanomedicine. 2012;7:4419-32. doi: 10.2147/IJN.S34396, PMID 22927758.
Matsusaki M, Hiwatari K, Higashi M, Kaneko T, Akashi M. Stably-dispersed and surface-functional bionanoparticles prepared by self-assembling amphipathic polymers of hydrophilic poly(γ-glutamic acid) bearing hydrophobic amino acids. Chem Lett. 2004 Apr;33(4):398-9. doi: 10.1246/cl.2004.398.
Uto T, Wang X, Sato K, Haraguchi M, Akagi T, Akashi M. Targeting of antigen to dendritic cells with poly(γ-glutamic acid) nanoparticles induces antigen-specific humoral and cellular immunity. J Immunol. 2007 Mar 1;178(5):2979-86. doi: 10.4049/jimmunol.178.5.2979, PMID 17312143.
Akagi T, Wang X, Uto T, Baba M, Akashi M. Protein direct delivery to dendritic cells using nanoparticles based on amphiphilic poly(amino acid) derivatives. Biomaterials. 2007 Aug 1;28(23):3427-36. doi: 10.1016/j.biomaterials.2007.04.023, PMID 17482261.
Bettencourt A, Almeida AJ. Poly(methyl methacrylate) particulate carriers in drug delivery. J Microencapsul. 2012 Jun 1;29(4):353-67. doi: 10.3109/02652048.2011.651500, PMID 22251239.
Kreuter J, Speiser PP. New adjuvants on a polymethylmethacrylate base. Infect Immun. 1976 Jan;13(1):204-10. doi: 10.1128/iai.13.1.204-210.1976, PMID 1248871.
Eldridge JH, Hammond CJ, Meulbroek JA, Staas JK, Gilley RM, Tice TR. Controlled vaccine release in the gut-associated lymphoid tissues. I. Orally administered biodegradable microspheres target the Peyer’s patches. J Control Release. 1990 Jan 1;11(1-3):205-14. doi: 10.1016/0168-3659(90)90133-E.
Voltan R, Castaldello A, Brocca Cofano E, Altavilla G, Caputo A, Laus M. Preparation and characterization of innovative protein-coated poly(methylmethacrylate) core-shell nanoparticles for vaccine purposes. Pharm Res. 2007 Oct 1;24(10):1870-82. doi: 10.1007/s11095-007-9310-8, PMID 17476465.
Wusiman A, Gu P, Liu Z, Xu S, Zhang Y, Hu Y. Cationic polymer modified PLGA nanoparticles encapsulating Alhagi honey polysaccharides as a vaccine delivery system for ovalbumin to improve immune responses. Int J Nanomedicine. 2019 Dec 31;14:3221-34. doi: 10.2147/IJN.S203072, PMID 31123399.
Duran V, Yasar H, Becker J, Thiyagarajan D, Loretz B, Kalinke U. Preferential uptake of chitosan-coated PLGA nanoparticles by primary human antigen-presenting cells. Nanomedicine. 2019 Oct;21:102073. doi: 10.1016/j.nano.2019.102073, PMID 31376570.
Cappellano G, Comi C, Chiocchetti A, Dianzani U. Exploiting PLGA-based biocompatible nanoparticles for next-generation tolerogenic vaccines against autoimmune disease. Int J Mol Sci. 2019 Jan 8;20(1):204. doi: 10.3390/ijms20010204, PMID 30626016.
Pati R, Shevtsov M, Sonawane A. Nanoparticle vaccines against infectious diseases. Front Immunol. 2018;9:2224. doi: 10.3389/fimmu.2018.02224, PMID 30337923.
Khalaj Hedayati A, Chua CLL, Smooker P, Lee KW. Nanoparticles in influenza subunit vaccine development: immunogenicity enhancement. Influenza Other Respir Viruses. 2020;14(1):92-101. doi: 10.1111/irv.12697, PMID 31774251.
Fritze D. Taxonomy of the genus bacillus and related genera: the aerobic endospore-forming bacteria. Phytopathology. 2004 Nov;94(11):1245-8. doi: 10.1094/PHYTO.2004.94.11.1245, PMID 18944461.
McKenney PT, Driks A, Eichenberger P. The Bacillus subtilis endospore: assembly and functions of the multilayered coat. Nat Rev Microbiol. 2013 Jan;11(1):33-44. doi: 10.1038/nrmicro2921, PMID 23202530.
Zhao G, Miao Y, Guo Y, Qiu H, Sun S, Kou Z. Development of a heat-stable and orally delivered recombinant M2e-expressing B. subtilis spore-based influenza vaccine. Hum Vaccin Immunother. 2014;10(12):3649-58. doi: 10.4161/hv.36122, PMID 25483702.
Ferreira LCS, Ferreira RCC, Schumann W. Bacillus subtilis as a tool for vaccine development: from antigen factories to delivery vectors. An Acad Bras Cienc. 2005 Mar;77(1):113-24. doi: 10.1590/s0001-37652005000100009, PMID 15692682.
Ciabattini A, Parigi R, Isticato R, Oggioni MR, Pozzi G. Oral priming of mice by recombinant spores of Bacillus subtilis. Vaccine. 2004 Oct 22;22(31-32):4139-43. doi: 10.1016/j.vaccine.2004.05.001, PMID 15474704.
Grgacic EVL, Anderson DA. Virus-like particles: passport to immune recognition. Methods. 2006 Sep;40(1):60-5. doi: 10.1016/j.ymeth.2006.07.018, PMID 16997714.
Young KR, Ross TM. Particle-based vaccines for HIV-1 infection. Curr Drug Targets Infect Disord. 2003 Jun;3(2):151-69. doi: 10.2174/1568005033481213, PMID 12769792.
Wang BZ, Quan FS, Kang SM, Bozja J, Skountzou I, Compans RW. Incorporation of membrane-anchored flagellin into influenza virus-like particles enhances the breadth of immune responses. J Virol. 2008 Dec;82(23):11813-23. doi: 10.1128/JVI.01076-08, PMID 18786995.
Kovacsovics Bankowski M, Clark K, Benacerraf B, Rock KL. Efficient major histocompatibility complex class I presentation of exogenous antigen upon phagocytosis by macrophages. Proc Natl Acad Sci USA. 1993 Jun;90(11):4942-6. doi: 10.1073/pnas.90.11.4942, PMID 8506338.
Zhao Q, Li S, Yu H, Xia N, Modis Y. Virus-like particle-based human vaccines: quality assessment based on structural and functional properties. Trends Biotechnol. 2013 Nov;31(11):654-63. doi: 10.1016/j.tibtech.2013.09.002, PMID 24125746.
Tao P, Zhu J, Mahalingam M, Batra H, Rao VB. Bacteriophage T4 nanoparticles for vaccine delivery against infectious diseases. Adv Drug Deliv Rev. 2019 May;145:57-72. doi: 10.1016/j.addr.2018.06.025, PMID 29981801.
Deng X, Wang L, You X, Dai P, Zeng Y. Advances in the T7 phage display system review. Mol Med Rep. 2018 Jan;17(1):714-20. doi: 10.3892/mmr.2017.7994, PMID 29115536.
Almeida J, Edwards DC, Brand C, Heath T. Formation of virosomes from influenza subunits and liposomes. Lancet. 1975 Nov 8;306(7941):899-901. doi: 10.1016/S0140-6736(75)92130-3.
Stegmann T, Morselt HW, Booy FP, van Breemen JF, Scherphof G, Wilschut J. Functional reconstitution of influenza virus envelopes. EMBO J. 1987 Sep;6(9):2651-9. doi: 10.1002/j.1460-2075.1987.tb02556.x, PMID 3678202.
Cryz SJ, Que JU, Glück R. A virosome vaccine antigen delivery system does not stimulate an antiphospholipid antibody response in humans. Vaccine. 1996 Oct;14(14):1381-3. doi: 10.1016/s0264-410x(96)00040-0, PMID 9004449.
Huckriede A, Bungener L, Stegmann T, Daemen T, Medema J, Palache AM. The virosome concept for influenza vaccines. Vaccine. 2005 Jul 8;23Suppl 1:S26-38. doi: 10.1016/j.vaccine.2005.04.026, PMID 16026906.
Moser C, Amacker M, Kammer AR, Rasi S, Westerfeld N, Zurbriggen R. Influenza virosomes as a combined vaccine carrier and adjuvant system for prophylactic and therapeutic immunizations. Expert Rev Vaccines. 2007 Oct;6(5):711-21. doi: 10.1586/14760584.6.5.711, PMID 17931152.
Mischler R, Metcalfe IC. Inflexal V a trivalent virosome subunit influenza vaccine: production. Vaccine. 2002 Dec 20;20Suppl 5:B17-23. doi: 10.1016/s0264-410x(02)00512-1, PMID 12477413.
Lövgren K, Morein B. The requirement of lipids for the formation of immunostimulating complexes (iscoms). Biotechnol Appl Biochem. 1988 Apr;10(2):161-72. doi: 10.1111/j.1470-8744.1988.tb00012.x, PMID 2838046.
Kersten GF, Spiekstra A, Beuvery EC, Crommelin DJ. On the structure of immune-stimulating saponin-lipid complexes (iscoms). Biochim Biophys Acta. 1991 Feb 25;1062(2):165-71. doi: 10.1016/0005-2736(91)90388-o, PMID 2004105.
Skene CD, Sutton P. Saponin-adjuvanted particulate vaccines for clinical use. Methods. 2006 Sep;40(1):53-9. doi: 10.1016/j.ymeth.2006.05.019, PMID 16997713.
Zhu D, Tuo W. QS-21: a potent vaccine adjuvant. Nat Prod Chem Res. 2016 Apr;3(4):e113. doi: 10.4172/2329-6836.1000e113, PMID 27213168.
Sambhara S, Kurichh A, Miranda R, Tumpey T, Rowe T, Renshaw M. Heterosubtypic immunity against human influenza a viruses, including recently emerged avian H5 and H9 viruses, induced by FLU-ISCOM vaccine in mice requires both cytotoxic T-lymphocyte and macrophage function. Cell Immunol. 2001 Aug 1;211(2):143-53. doi: 10.1006/cimm.2001.1835, PMID 11591118.
Lövgren Bengtsson K, Morein B, Osterhaus AD. ISCOM technology-based Matrix M™ adjuvant: success in future vaccines relies on formulation. Expert Rev Vaccines. 2011 Apr;10(4):401-3. doi: 10.1586/erv.11.25, PMID 21506635.
Lin Y, Hamme AT. Gold nanoparticle labeling based icp-ms detection/measurement of bacteria and their quantitative photothermal destruction. J Mater Chem B. 2015 May 7;3(17):3573-82. doi: 10.1039/C5TB00223K, PMID 26417447.
Tao W, Ziemer KS, Gill HS. Gold nanoparticle-M2e conjugate coformulated with CpG induces protective immunity against influenza a virus. Nanomedicine (Lond). 2014 Feb;9(2):237-51. doi: 10.2217/nnm.13.58, PMID 23829488.
Ingrole RS, Tao W, Tripathy JN, Gill HS. Synthesis and immunogenicity assessment of elastin-like polypeptide-m2e construct as an influenza antigen. Nano Life. 2014 Jun 1;4(2):1450004. doi: 10.1142/s1793984414500044, PMID 25825595.
Orosco FL. Advancing the frontiers: revolutionary control and prevention paradigms against Nipah virus. Open Vet J. 2023 Oct;13(9):1056. doi: 10.5455/OVJ.2023.v13.i9.1, PMID 37842102.
Wang C, Zhu W, Luo Y, Wang BZ. Gold nanoparticles conjugating recombinant influenza hemagglutinin trimers and flagellin enhanced mucosal cellular immunity. Nanomedicine. 2018 Jun;14(4):1349-60. doi: 10.1016/j.nano.2018.03.007, PMID 29649593.
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