The impact of size for liposomes modified with pH-responsive β-glucan derivatives on the initiation of cellular and humoral immune responses in murine models

References

• Cheng ZJ, Shan J. 2019 Novel coronavirus: where we are and what we know. Infection. 2020;48(2):1–13. doi: 10.1007/s15010-020-01401-y.
   PubMed Web of Science ®Google Scholar
• Li M, Wang H, Tian L, et al. COVID-19 vaccine development: milestones, lessons and prospects. Signal Transduct Target Ther. 2022;7:146.
   PubMed Web of Science ®Google Scholar
• Zheng J, Deng Y, Zhao Z, et al. Characterization of SARS-CoV-2-specific humoral immunity and its potential applications and therapeutic prospects. Cell Mol Immunol. 2022;19(2):150–157. doi: 10.1038/s41423-021-00774-w.
   PubMed Web of Science ®Google Scholar
• Ruterbusch M, Pruner KB, Shehata L, et al. In vivo CD4+ T cell differentiation and function: revisiting the Th1/Th2 paradigm. Annu Rev Immunol. 2020;38:705–725.
   PubMed Web of Science ®Google Scholar
• Ong DSY, Fragkou PC, Schweitzer VA, et al. How to interpret and use COVID-19 serology and immunology tests. Clin Microbiol Infect. 2021;27:981–986.
   PubMed Web of Science ®Google Scholar
• Aleebrahim-Dehkordi E, Molavi B, Mokhtari M, et al. T helper type (Th1/Th2) responses to SARS-CoV-2 and influenza A (H1N1) virus: from cytokines produced to immune responses. Transpl Immunol. 2022;70:101495.
   PubMed Web of Science ®Google Scholar
• Koh CH, Lee S, Kwak M, et al. CD8 T-cell subsets: heterogeneity, functions, and therapeutic potential. Exp Mol Med. 2023;55(11):2287–2299. doi: 10.1038/s12276-023-01105-x.
   PubMed Web of Science ®Google Scholar
• Auladell M, Jia X, Hensen L, et al. Recalling the future: immunological memory toward unpredictable influenza viruses. Front Immunol. 2019;10:1400. doi: 10.3389/fimmu.2019.01400.
   PubMed Web of Science ®Google Scholar
• Kaseke C, Tano-Menka R, Senjobe F, et al. The emerging role for CTL epitope specificity in HIV cure efforts. J Infect Dis. 2021;223:32–37.
   PubMed Web of Science ®Google Scholar
• Schwendener RA. Liposomes as vaccine delivery systems: a review of the recent advances. Ther Adv Vaccines. 2014;2(6):159–182. doi: 10.1177/2051013614541440.
   PubMedGoogle Scholar
• Riaz MK, Riaz MA, Zhang X, et al. Surface functionalization and targeting strategies of liposomes in solid tumor therapy: a review. Int J Mol Sci. 2018;19:195.
   PubMed Web of Science ®Google Scholar
• Inglut CT, Sorrin AJ, Kuruppu T, et al. Immunological and toxicological considerations for the design of liposomes. Nanomaterials. 2020;10(2):190. doi: 10.3390/nano10020190.
   Web of Science ®Google Scholar
• Brewer JM, Tetley L, Richmond J, et al. Lipid vesicle size determines the Th1 or Th2 response to entrapped antigen. J Immunol. 1998;161(8):4000–4007. doi: 10.4049/jimmunol.161.8.4000.
   PubMed Web of Science ®Google Scholar
• Matsuoka Y, Onohara E, Kojima N, et al. Importance of particle size of oligomannose-coated liposomes for induction of Th1 immunity. Int Immunopharmacol. 2021;99:108068.
   PubMed Web of Science ®Google Scholar
• Badiee A, Khamesipour A, Samiei A, et al. The role of liposome size on the type of immune response induced in BALB/c mice against leishmaniasis: rgp63 as a model antigen. Exp Parasitol. 2012;132:403–409.
   PubMed Web of Science ®Google Scholar
• Mann JFS, Shakir E, Carter KC, et al. Lipid vesicle size of an oral influenza vaccine delivery vehicle influences the Th1/Th2 bias in the immune response and protection against infection. Vaccine. 2009;27(27):3643–3649. doi: 10.1016/j.vaccine.2009.03.040.
   PubMed Web of Science ®Google Scholar
• Yamamoto S, Ishida T, Inoue A, et al. HEPC-based liposomes trigger cytokine release from peripheral blood cells: effects of liposomal size, dose and lipid composition. Int J Pharm. 2002;236(1–2):125–133. doi: 10.1016/s0378-5173(02)00026-1.
   PubMedGoogle Scholar
• Yuba E, Yamaguchi A, Yoshizaki Y, et al. Bioactive polysaccharide-based pH-sensitive polymers for cytoplasmic delivery of antigen and activation of antigen-specific immunity. Biomaterials. 2017;120:32–45. doi: 10.1016/j.biomaterials.2016.12.021.
   PubMed Web of Science ®Google Scholar
• Okubo M, Miyazaki M, Yuba E, et al. Chondroitin sulfate-based pH-Sensitive polymer-modified liposomes for intracellular antigen delivery and induction of cancer immunity. Bioconjug Chem. 2019;30:1518–1529.
   PubMed Web of Science ®Google Scholar
• Yanagihara S, Kasho N, Sasaki K, et al. pH-Sensitive branched β-glucan-modified liposomes for activation of antigen presenting cells and induction of antitumor immunity. J Mater Chem B. 2021;9:7713–7724.
   PubMed Web of Science ®Google Scholar
• Miyazaki M, Yuba E, Hayashi H, et al. Development of pH-responsive hyaluronic acid-Based antigen carriers for induction of antigen-specific cellular immune responses. ACS Biomater Sci Eng. 2019;5(11):5790–5797. doi: 10.1021/acsbiomaterials.9b01278.
   PubMed Web of Science ®Google Scholar
• Yuba E, Tajima N, Yoshizaki Y, et al. Dextran derivative-based pH-sensitive liposomes for cancer immunotherapy. Biomaterials. 2014;35(9):3091–3101. doi: 10.1016/j.biomaterials.2013.12.024.
   PubMed Web of Science ®Google Scholar
• Yanagihara S, Kitayama Y, Yuba E, et al. Preparing size-controlled liposomes modified with polysaccharide derivatives for pH-responsive drug delivery applications. Life. 2023;13(11):2158. doi: 10.3390/life13112158.
   PubMedGoogle Scholar
• Sultan H, Wu J, Fesenkova VI, et al. Poly-IC enhances the effectiveness of cancer immunotherapy by promoting T cell tumor infiltration. J Immunother Cancer. 2020;8(2):e001224. doi: 10.1136/jitc-2020-001224.
   PubMed Web of Science ®Google Scholar
• Zhang X, Qi C, Guo Y, et al. Toll-like receptor 4-related immunostimulatory polysaccharides: primary structure, activity relationships, and possible interaction models. Carbohydr Polym. 2016;149:186–206.
   PubMed Web of Science ®Google Scholar
• Ikeda A, Akiyama M, Sugikawa K, et al. Formation of β-(1,3-1,6)-d-glucan-complexed [70]fullerene and its photodynamic activity towards macrophages. Org Biomol Chem. 2017;15(45):9734. doi: 10.1039/c7ob90179h.
   PubMed Web of Science ®Google Scholar
• Gu Z, Da Silva CG, Van der Maaden K, et al. Liposome-based drug delivery systems in cancer immunotherapy. Pharmaceutics. 2020;12(11):1054. doi: 10.3390/pharmaceutics12111054.
   PubMed Web of Science ®Google Scholar
• Thapa Magar K, Boafo GF, Li X, et al. Liposome-based delivery of biological drugs. Chin Chem Lett. 2022;33:587–596.
   Web of Science ®Google Scholar
• Lou G, Anderluzzi G, Woods S, et al. A novel microfluidic-based approach to formulate size-tuneable large unilamellar cationic liposomes: formulation, cellular uptake and biodistribution investigations. Eur J Pharm Biopharm. 2019;143:51–60. doi: 10.1016/j.ejpb.2019.08.013.
   PubMed Web of Science ®Google Scholar
• Chono S, Tanino T, Seki T, et al. Uptake characteristics of liposomes by rat alveolar macrophages: influence of particle size and surface mannose modification. J Pharm Pharmacol. 2007;59(1):75–80. doi: 10.1211/jpp.59.1.0010.
   PubMed Web of Science ®Google Scholar
• Garrett WS, Chen LM, Kroschewski R, et al. Developmental control of endocytosis in dendritic cells by Cdc42. Cell. 2000;102(3):325–334. doi: 10.1016/s0092-8674(00)00038-6.
   PubMed Web of Science ®Google Scholar
• Oussoren C, Zuidema J, Crommelin DJA, et al. Lymphatic uptake and biodistribution of liposomes after subcutaneous injection. II. Influence of liposomal size, lipid composition and lipid dose. Biochim Biophys Acta Biomembr. 1997;1328:261–272.
   PubMed Web of Science ®Google Scholar
• Dahlgren MW, Plumb AW, Niss K, et al. Type I interferons promote germinal centers through B cell intrinsic signaling and dendritic cell dependent Th1 and tfh cell lineages. Front Immunol. 2022;13:932388. doi: 10.3389/fimmu.2022.932388.
   PubMed Web of Science ®Google Scholar
• Szeponik L, Akeus P, Rodin W, et al. Regulatory T cells specifically suppress conventional CD8αβ T cells in intestinal tumors of APCMin/+ mice. Cancer Immunol Immunother. 2020;69(7):1279–1292. doi: 10.1007/s00262-020-02540-9.
   PubMed Web of Science ®Google Scholar
• Ahnstedt H, McCullough LD. The impact of sex and age on T cell immunity and ischemic stroke outcomes. Cell Immunol. 2019;345:103960.
   PubMed Web of Science ®Google Scholar
• Schaefer AL, Ceesay M, Leier JA, et al. Factors contributing to sex differences in mice inhaling Aspergillus fumigatus. Int J Environ Res Public Health. 2020;17(23):8851. doi: 10.3390/ijerph17238851.
   PubMed Web of Science ®Google Scholar
• Bleul T, Zhuang X, Hildebrand A, et al. Different innate immune responses in BALB/c and C57BL/6 strains following corneal transplantation. J Innate Immun. 2021;13(1):49–59. doi: 10.1159/000509716.
   PubMed Web of Science ®Google Scholar
• Van Hoecke L, Van Lint S, Roose K, et al. Treatment with mRNA coding for the necroptosis mediator MLKL induces antitumor immunity directed against neo-epitopes. Nat Commun. 2018;9(1):3417. doi: 10.1038/s41467-018-05979-8.
   PubMed Web of Science ®Google Scholar
• Sagiv-Barfi I, Czerwinski DK, Shree T, et al. Intratumoral immunotherapy relies on B and T cell collaboration. Sci Immunol. 2022;7(71):eabn5859. doi: 10.1126/sciimmunol.abn5859.
   PubMed Web of Science ®Google Scholar