Long-term stability and immunogenicity of lipid nanoparticle COVID-19 mRNA vaccine is affected by particle size

References

• Hajj KA, Whitehead KA. Tools for translation: non-viral materials for therapeutic mRNA delivery. Nat Rev Mater. 2017;2(10):17056. doi:10.1038/natrevmats.2017.56.
   Web of Science ®Google Scholar
• Pardi N, Hogan MJ, Porter FW, Weissman D. mRNA vaccines — a new era in vaccinology. Nat Rev Drug Discov. 2018;17(4):261–11. doi:10.1038/nrd.2017.243.
   PubMed Web of Science ®Google Scholar
• Erasmus JH, Archer J, Fuerte-Stone J, Khandhar AP, Voigt E, Granger B, Bombardi RG, Govero J, Tan Q, Durnell LA. et al. Intramuscular delivery of replicon RNA encoding ZIKV-117 human monoclonal antibody protects against Zika virus infection. Mol Ther Methods Clin Dev. 2020;18:402–14. doi:10.1016/j.omtm.2020.06.011.
   PubMed Web of Science ®Google Scholar
• Schoenmaker L, Witzigmann D, Kulkarni JA, Verbeke R, Kersten G, Jiskoot W, Crommelin DJA. mRNA-lipid nanoparticle COVID-19 vaccines: structure and stability. Int J Pharm. 2021;601:120586. doi:10.1016/j.ijpharm.2021.120586.
   PubMed Web of Science ®Google Scholar
• Hassett KJ, Benenato KE, Jacquinet E, Lee A, Woods A, Yuzhakov O, Himansu S, Deterling J, Geilich BM, Ketova T. et al. Optimization of lipid nanoparticles for intramuscular administration of mRNA vaccines. Mol Ther Nucleic Acids. 2019;15:1–11. doi:10.1016/j.omtn.2019.01.013.
   PubMedGoogle Scholar
• John S, Yuzhakov O, Woods A, Deterling J, Hassett K, Shaw CA, Ciaramella G. Multi-antigenic human cytomegalovirus mRNA vaccines that elicit potent humoral and cell-mediated immunity. Vaccine. 2018;36(12):1689–99. doi:10.1016/j.vaccine.2018.01.029.
   PubMed Web of Science ®Google Scholar
• Schlake T, Thess A, Fotin-Mleczek M, Kallen KJ. Developing mRNA-vaccine technologies. RNA Biol. 2012;9(11):1319–30. doi:10.4161/rna.22269.
   PubMed Web of Science ®Google Scholar
• Sabnis S, Kumarasinghe ES, Salerno T, Mihai C, Ketova T, Senn JJ, Lynn A, Bulychev A, McFadyen I, Chan J. et al. A novel amino lipid series for mRNA delivery: improved endosomal escape and sustained pharmacology and safety in non-human primates. Mol Ther. 2018;26(6):1509–19. doi:10.1016/j.ymthe.2018.03.010.
   PubMed Web of Science ®Google Scholar
• Kose N, Fox JM, Sapparapu G, Bombardi R, Tennekoon RN, de Silva AD, Elbashir SM, Theisen MA, Humphris-Narayanan E, Ciaramella G. et al. A lipid-encapsulated mRNA encoding a potently neutralizing human monoclonal antibody protects against chikungunya infection. Sci Immunol. 2019;4(35):4. doi:10.1126/sciimmunol.aaw6647.
   Web of Science ®Google Scholar
• Pardi N, Secreto AJ, Shan X, Debonera F, Glover J, Yi Y, Muramatsu H, Ni H, Mui BL, Tam YK. et al. Administration of nucleoside-modified mRNA encoding broadly neutralizing antibody protects humanized mice from HIV-1 challenge. Nat Commun. 2017;8(1):14630. doi:10.1038/ncomms14630.
   PubMedGoogle Scholar
• Van Hoecke L, Verbeke R, De Vlieger D, Dewitte H, Roose K, Van Nevel S, Krysko O, Bachert C, Schepens B, Lentacker I. et al. mRNA encoding a bispecific single domain antibody construct protects against influenza a virus infection in mice. Mol Ther Nucleic Acids. 2020;20:777–87. doi:10.1016/j.omtn.2020.04.015.
   PubMedGoogle Scholar
• Baden LR, El Sahly HM, Essink B, Kotloff K, Frey S, Novak R, Diemert D, Spector SA, Rouphael N, Creech CB. et al. Efficacy and safety of the mRNA-1273 SARS-CoV-2 vaccine. N Engl J Med. 2021;384(5):403–16. doi:10.1056/NEJMoa2035389.
   PubMed Web of Science ®Google Scholar
• Deng YQ, Zhang NN, Zhang YF, Zhong X, Xu S, Qiu HY, Wang T-C, Zhao H, Zhou C, Zu S-L. et al. Lipid nanoparticle-encapsulated mRNA antibody provides long-term protection against SARS-CoV-2 in mice and hamsters. Cell Res. 2022;32(4):375–82. doi:10.1038/s41422-022-00630-0.
   PubMed Web of Science ®Google Scholar
• Muramatsu H, Lam K, Bajusz C, Laczko D, Kariko K, Schreiner P, Martin A, Lutwyche P, Heyes J, Pardi N. et al. Lyophilization provides long-term stability for a lipid nanoparticle-formulated, nucleoside-modified mRNA vaccine. Mol Ther. 2022;30(5):1941–51. doi:10.1016/j.ymthe.2022.02.001.
   PubMed Web of Science ®Google Scholar
• Howard GP, Verma G, Ke X, Thayer WM, Hamerly T, Baxter VK, Lee JE, Dinglasan RR, Mao H-Q. Critical size limit of biodegradable nanoparticles for enhanced lymph node trafficking and paracortex penetration. Nano Res. 2019;12(4):837–44. doi:10.1007/s12274-019-2301-3.
   PubMed Web of Science ®Google Scholar
• Crommelin DJA, Anchordoquy TJ, Volkin DB, Jiskoot W, Mastrobattista E. Addressing the cold reality of mRNA vaccine stability. J Pharm Sci. 2021;110(3):997–1001. doi:10.1016/j.xphs.2020.12.006.
   PubMed Web of Science ®Google Scholar
• Oude Blenke E, Örnskov E, Schöneich C, Nilsson GA, Volkin DB, Mastrobattista E, Almarsson Ö, Crommelin DJA. The storage and in-use stability of mRNA vaccines and therapeutics: not a cold case. J Pharm Sci. 2023;112(2):386–403. doi:10.1016/j.xphs.2022.11.001.
   PubMed Web of Science ®Google Scholar
• Wang T, Sung TC, Yu T, Lin HY, Chen YH, Zhu ZW, Gong J, Pan J, Higuchi A. Next-generation materials for RNA–lipid nanoparticles: lyophilization and targeted transfection. J Mater Chem B. 2023;11(23):5083–93. doi:10.1039/D3TB00308F.
   PubMed Web of Science ®Google Scholar
• Poveda C, Biter AB, Bottazzi ME, Strych U. Establishing preferred product characterization for the evaluation of RNA vaccine antigens. Vaccines. 2019;7(4):7. doi:10.3390/vaccines7040131.
   Web of Science ®Google Scholar
• Fan Y, Marioli M, Zhang K. Analytical characterization of liposomes and other lipid nanoparticles for drug delivery. J Pharm Biomed Anal. 2021;192:113642. doi:10.1016/j.jpba.2020.113642.
   PubMed Web of Science ®Google Scholar
• Kim J, Eygeris Y, Gupta M, Sahay G. Self-assembled mRNA vaccines. Adv Drug Deliv Rev. 2021;170:83–112. doi:10.1016/j.addr.2020.12.014.
   PubMed Web of Science ®Google Scholar
• Suzuki Y, Hyodo K, Tanaka Y, Ishihara H. siRNA-lipid nanoparticles with long-term storage stability facilitate potent gene-silencing in vivo. J Control Release. 2015;220:44–50. doi:10.1016/j.jconrel.2015.10.024.
   PubMed Web of Science ®Google Scholar
• Gindy ME, Feuston B, Glass A, Arrington L, Haas RM, Schariter J, Stirdivant SM. Stabilization of Ostwald ripening in low molecular weight amino lipid nanoparticles for systemic delivery of siRNA therapeutics. Mol Pharm. 2014;11(11):4143–53. doi:10.1021/mp500367k.
   PubMedGoogle Scholar
• Suzuki Y, Miyazaki T, Muto H, Kubara K, Mukai Y, Watari R, Sato S, Kondo K, Tsukumo S-I, Yasutomo K. et al. Design and lyophilization of lipid nanoparticles for mRNA vaccine and its robust immune response in mice and nonhuman primates. Mol Ther Nucleic Acids. 2022;30:226–40. doi:10.1016/j.omtn.2022.09.017.
   PubMedGoogle Scholar
• Wang Y, Grainger DW. Lyophilized liposome-based parenteral drug development: reviewing complex product design strategies and current regulatory environments. Adv Drug Deliv Rev. 2019;151-152:56–71. doi:10.1016/j.addr.2019.03.003.
   PubMed Web of Science ®Google Scholar
• Zhao P, Hou X, Yan J, Du S, Xue Y, Li W, Xiang G, Dong Y. Long-term storage of lipid-like nanoparticles for mRNA delivery. Bioact Mater. 2020;5(2):358–63. doi:10.1016/j.bioactmat.2020.03.001.
   PubMed Web of Science ®Google Scholar
• Hald Albertsen C, Kulkarni JA, Witzigmann D, Lind M, Petersson K, Simonsen JB. The role of lipid components in lipid nanoparticles for vaccines and gene therapy. Adv Drug Deliv Rev. 2022;188:114416. doi:10.1016/j.addr.2022.114416.
   PubMed Web of Science ®Google Scholar
• Franzé S, Selmin F, Samaritani E, Minghetti P, Cilurzo F. Lyophilization of liposomal formulations: still necessary, still challenging. Pharmaceutics. 2018;10(3):10. doi:10.3390/pharmaceutics10030139.
   PubMed Web of Science ®Google Scholar
• Jakubek ZJ, Chen S, Zaifman J, Tam YYC, Zou S. Lipid nanoparticle and liposome reference materials: assessment of size homogeneity and long-term −70 °C and 4 °C Storage Stability. Langmuir. 2023;39(7):2509–19. doi:10.1021/acs.langmuir.2c02657.
   PubMedGoogle Scholar
• Lamoot A, Lammens J, De Lombaerde E, Zhong Z, Gontsarik M, Chen Y, De Beer TRM, De Geest BG. Successful batch and continuous lyophilization of mRNA LNP formulations depend on cryoprotectants and ionizable lipids. Biomater Sci. 2023;11(12):4327–34. doi:10.1039/D2BM02031A.
   PubMed Web of Science ®Google Scholar
• Pardi N, Carreno JM, O’Dell G, Tan J, Bajusz C, Muramatsu H, Rijnink W, Strohmeier S, Loganathan M, Bielak D. et al. Development of a pentavalent broadly protective nucleoside-modified mRNA vaccine against influenza B viruses. Nat Commun. 2022;13(1):4677. doi:10.1038/s41467-022-32149-8.
   PubMed Web of Science ®Google Scholar
• Costa VG, Costa SM, Saramago M, Cunha MV, Arraiano CM, Viegas SC, Matos RG. Developing new tools to fight human pathogens: a journey through the advances in RNA technologies. Microorganisms. 2022;10(11):10. doi:10.3390/microorganisms10112303.
   Web of Science ®Google Scholar
• Foged C, Brodin B, Frokjaer S, Sundblad A. Particle size and surface charge affect particle uptake by human dendritic cells in an in vitro model. Int J Pharm. 2005;298(2):315–22. doi:10.1016/j.ijpharm.2005.03.035.
   PubMed Web of Science ®Google Scholar
• Gao X, Liu N, Wang Z, Gao J, Zhang H, Li M, Du Y, Gao X, Zheng A. Development and optimization of chitosan nanoparticle-based intranasal vaccine carrier. Molecules. 2021;27(1):27. doi:10.3390/molecules27010204.
   PubMed Web of Science ®Google Scholar
• Viger-Gravel J, Schantz A, Pinon AC, Rossini AJ, Schantz S, Emsley L. Structure of lipid nanoparticles containing siRNA or mRNA by dynamic nuclear polarization-enhanced NMR spectroscopy. J Phys Chem B. 2018;122(7):2073–81. doi:10.1021/acs.jpcb.7b10795.
   PubMed Web of Science ®Google Scholar
• Yanez Arteta M, Kjellman T, Bartesaghi S, Wallin S, Wu X, Kvist AJ, Dabkowska A, Székely N, Radulescu A, Bergenholtz J. et al. Successful reprogramming of cellular protein production through mRNA delivered by functionalized lipid nanoparticles. Proc Natl Acad Sci U S A. 2018;115(15):E3351–e60. doi:10.1073/pnas.1720542115.
   PubMed Web of Science ®Google Scholar
• Malburet C, Leclercq L, Cotte JF, Thiebaud J, Bazin E, Garinot M, Cottet H. Size and charge characterization of lipid nanoparticles for mRNA vaccines. Anal Chem. 2022;94(11):4677–85. doi:10.1021/acs.analchem.1c04778.
   PubMed Web of Science ®Google Scholar
• Skowronski DM, De Serres G. Safety and efficacy of the BNT162b2 mRNA Covid-19 vaccine. N Engl J Med. 2021;384:1576–7.
   PubMedGoogle Scholar
• Hogan MJ, Pardi N. mRNA vaccines in the COVID-19 pandemic and beyond. Annu Rev Med. 2022;73(1):17–39. doi:10.1146/annurev-med-042420-112725.
   PubMed Web of Science ®Google Scholar
• Meulewaeter S, Nuytten G, Cheng MHY, De Smedt SC, Cullis PR, De Beer T, Lentacker I, Verbeke R. Continuous freeze-drying of messenger RNA lipid nanoparticles enables storage at higher temperatures. J Control Release. 2023;357:149–60. doi:10.1016/j.jconrel.2023.03.039.
   PubMed Web of Science ®Google Scholar
• Muramatsu H, Lam K, Bajusz C, Laczkó D, Karikó K, Schreiner P, Martin A, Lutwyche P, Heyes J, Pardi N. et al. Lyophilization provides long-term stability for a lipid nanoparticle-formulated, nucleoside-modified mRNA vaccine. Mol Ther. 2022;30(5):1941–51. doi:10.1016/j.ymthe.2022.02.001.
   PubMed Web of Science ®Google Scholar