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Research Article

PEGylated pH-responsive peptide-mRNA nano self-assemblies enhance the pulmonary delivery efficiency and safety of aerosolized mRNA

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Article: 2219870 | Received 06 Feb 2023, Accepted 02 May 2023, Published online: 19 Jun 2023

References

  • Anderson EJ, Rouphael NG, Widge AT, et al. (2020). Safety and immunogenicity of SARS-CoV-2 mRNA-1273 vaccine in older adults. N Engl J Med 383:1–14.
  • Armbruster N, Jasny E, Petsch B. (2019). Advances in RNA vaccines for preventive indications: a case study of a vaccine against rabies. Vaccines 7:132.
  • Berraondo P, Martini PGV, Avila MA, et al. (2019). Messenger RNA therapy for rare genetic metabolic diseases. Gut 68:1323–30.
  • Bulcha JT, Wang Y, Ma H, et al. (2021). Viral vector platforms within the gene therapy landscape. Signal Transduct Target Ther 6:53.
  • Crommelin DJA, Anchordoquy TJ, Volkin DB, et al. (2021). Addressing the cold reality of mRNA vaccine stability. J Pharm Sci 110:997–1001.
  • Elkhalifa D, Rayan M, Negmeldin AT, et al. (2022). Chemically modified mRNA beyond COVID-19: potential preventive and therapeutic applications for targeting chronic diseases. Biomed Pharmacother 145:112385.
  • Faghfuri E, Pourfarzi F, Faghfouri AH, et al. (2021). Recent developments of RNA-based vaccines in cancer immunotherapy. Expert Opin Biol Ther 21:201–18.
  • Fant K, Esbjörner EK, Jenkins A, et al. (2010). Effects of PEGylation and acetylation of PAMAM dendrimers on DNA binding, cytotoxicity and in vitro transfection efficiency. Mol Pharm 7:1734–46.
  • Gjetting T, Arildsen NS, Christensen CL, et al. (2010). In vitro and in vivo effects of polyethylene glycol (PEG)-modified lipid in DOTAP/cholesterol-mediated gene transfection. Int J Nanomedicine 5:371–83.
  • Gomez-Aguado I, Rodriguez-Castejon J, Vicente-Pascual M, et al. (2020). Nanomedicines to deliver mRNA: state of the art and future perspectives. Nanomaterials 10:364.
  • Gu P, Wang D, Zhang J, et al. (2021). Protective function of interleukin-22 in pulmonary fibrosis. Clin Transl Med 11:e509.
  • Heida R, Hinrichs WL, Frijlink HW. (2022). Inhaled vaccine delivery in the combat against respiratory viruses: a 2021 overview of recent developments and implications for COVID-19. Expert Rev Vaccine 21:957–74.
  • Hellfritzsch M, Scherließ R. (2019). Mucosal vaccination via the respiratory tract. Pharmaceutica 11:375.
  • Huckaby JT, Lai SK. (2018). PEGylation for enhancing nanoparticle diffusion in mucus. Adv Drug Deliv Rev 124:125–39.
  • Iacobucci V, Di Giuseppe F, Bui TT, et al. (2012). Control of pH responsive peptide self-association during endocytosis is required for effective gene transfer. Biochim Biophys Acta 1818:1332–41.
  • Ibba ML, Ciccone G, Esposito CL, et al. (2021). Advances in mRNA non-viral delivery approaches. Adv Drug Deliv Rev 177:113930.
  • Kargaard A, Sluijter JPG, Klumperman B. (2019). Polymeric siRNA gene delivery – transfection efficiency versus cytotoxicity. J Control Release 316:263–91.
  • Kato A, Hulse KE, Tan BK, et al. (2013). B-lymphocyte lineage cells and the respiratory system. J Allergy Clin Immunol 131:933–57; quiz 958.
  • Ke X, Shelton L, Hu Y, et al. (2020). Surface-functionalized PEGylated nanoparticles deliver messenger RNA to pulmonary immune cells. ACS Appl Mater Interfaces 12:35835–44.
  • Khalil IA, Harashima H. (2018). An efficient PEGylated gene delivery system with improved targeting: synergism between octaarginine and a fusogenic peptide. Int J Pharm 538:179–87.
  • Klimek L, Novak N, Hamelmann E, et al. (2021). Severe allergic reactions after COVID-19 vaccination with the Pfizer/BioNTech vaccine in Great Britain and USA. Allergo J Int 30:51–5.
  • Kormann MS, Hasenpusch G, Aneja MK, et al. (2011). Expression of therapeutic proteins after delivery of chemically modified mRNA in mice. Nat Biotechnol 29:154–7.
  • Kubler H, Scheel B, Gnad-Vogt U, et al. (2015). Self-adjuvanted mRNA vaccination in advanced prostate cancer patients: a first-in-man phase I/IIa study. J Immunother Cancer 3:1–14.
  • Kunnapuu K, Veiman KL, Porosk L, et al. (2019). Tumor gene therapy by systemic delivery of plasmid DNA with cell-penetrating peptides. FASEB Bioadv 1:105–14.
  • Lam JK, Liang W, Lan Y, et al. (2012). Effective endogenous gene silencing mediated by pH responsive peptides proceeds via multiple pathways. J Control Release 158:293–303.
  • Lauring AS, Jones JO, Andino R. (2010). Rationalizing the development of live attenuated virus vaccines. Nat Biotechnol 28:573–9.
  • Leppek K, Byeon GW, Kladwang W, et al. (2021). Combinatorial optimization of mRNA structure, stability, and translation for RNA-based therapeutics. Nat Commun 13:1–22.
  • Li Z, Luo G, Hu WP, et al. (2020). Mediated drug release from nanovehicles by black phosphorus quantum dots for efficient therapy of chronic obstructive pulmonary disease. Angew Chem 132:20749–57.
  • Li C, Zhan W, Yang Z, et al. (2022). Broad neutralization of SARS-CoV-2 variants by an inhalable bispecific single-domain antibody. Cell 185:1389–401.e18.
  • Liang W, Chow MY, Lau PN, et al. (2015). Inhalable dry powder formulations of siRNA and pH-responsive peptides with antiviral activity against H1N1 influenza virus. Mol Pharm 12:910–21.
  • Liang W, Kwok PC, Chow MY, et al. (2014). Formulation of pH responsive peptides as inhalable dry powders for pulmonary delivery of nucleic acids. Eur J Pharm Biopharm 86:64–73.
  • Lin YX, Wang Y, Blake S, et al. (2020). RNA nanotechnology-mediated cancer immunotherapy. Theranostics 10:281–99.
  • Lokugamage MP, Vanover D, Beyersdorf J, et al. (2021). Optimization of lipid nanoparticles for the delivery of nebulized therapeutic mRNA to the lungs. Nat Biomed Eng 5:1059–68.
  • Maruggi G, Zhang C, Li J, et al. (2019). mRNA as a transformative technology for vaccine development to control infectious diseases. Mol Ther 27:757–72.
  • Mehta D, Leong N, McLeod VM, et al. (2018). Reducing dendrimer generation and PEG chain length increases drug release and promotes anticancer activity of PEGylated polylysine dendrimers conjugated with doxorubicin via a cathepsin-cleavable peptide linker. Mol Pharm 15:4568–76.
  • Moghimi SM. (2021). Allergic reactions and anaphylaxis to LNP-based COVID-19 vaccines. Mol Ther 29:898–900.
  • Moreno-Fierros L, Garcia-Silva I, Rosales-Mendoza S. (2020). Development of SARS-CoV-2 vaccines: should we focus on mucosal immunity? Expert Opin Biol Ther 20:831–6.
  • Muqier M, Xiao H, Yu X, et al. (2022). Synthesis of PEGylated cationic curdlan derivatives with enhanced biocompatibility. J Biomater Sci Polym Ed 33:465–80.
  • Ndeupen S, Qin Z, Jacobsen S, et al. (2021). The mRNA-LNP platform’s lipid nanoparticle component used in preclinical vaccine studies is highly inflammatory. Iscience 24:103479.
  • Osman G, Rodriguez J, Chan SY, et al. (2018). PEGylated enhanced cell penetrating peptide nanoparticles for lung gene therapy. J Control Release 285:35–45.
  • Peng J, Cai Z, Wang Q, et al. (2022a). Carboxymethyl chitosan modified oxymatrine liposomes for the alleviation of emphysema in mice via pulmonary administration. Molecules 27:3610.
  • Peng B, Nguyen TM, Jayasinghe MK, et al. (2022b). Robust delivery of RIG-I agonists using extracellular vesicles for anti-cancer immunotherapy. J Extracell Vesicles 11:e12187.
  • Polack FP, Thomas SJ, Kitchin N, et al. (2020). Safety and efficacy of the BNT162b2 mRNA Covid-19 vaccine. N Engl J Med 383:2603–15.
  • Pozzi D, Colapicchioni V, Caracciolo G, et al. (2014). Effect of polyethyleneglycol (PEG) chain length on the bio-nano-interactions between PEGylated lipid nanoparticles and biological fluids: from nanostructure to uptake in cancer cells. Nanoscale 6:2782–92.
  • Qin S, Tang X, Chen Y, et al. (2022). mRNA-based therapeutics: powerful and versatile tools to combat diseases. Signal Transduct Target Ther 7:1–35.
  • Qiu Y, Clarke M, Wan LTL, et al. (2021). Optimization of PEGylated KL4 peptide for siRNA delivery with improved pulmonary tolerance. Mol Pharm 18:2218–32.
  • Qiu Y, Man RCH, Liao Q, et al. (2019). Effective mRNA pulmonary delivery by dry powder formulation of PEGylated synthetic KL4 peptide. J Control Release 314:102–15.
  • Rao GA, Tsai R, Roura D, et al. (2008). Evaluation of the transfection property of a peptide ligand for the fibroblast growth factor receptor as part of PEGylated polyethylenimine polyplex. J Drug Target 16:79–89.
  • Sahin U, Kariko K, Tureci O. (2014). mRNA-based therapeutics-developing a new class of drugs. Nat Rev Drug Discov 13:759–80.
  • Sahu I, Haque A, Weidensee B, et al. (2019). Recent developments in mRNA-based protein supplementation therapy to target lung diseases. Mol Ther 27:803–23.
  • Schoenmaker L, Witzigmann D, Kulkarni JA, et al. (2021). mRNA-lipid nanoparticle COVID-19 vaccines: structure and stability. Int J Pharm 601:120586.
  • Sebastian M, Schroder A, Scheel B, et al. (2019). A phase I/IIa study of the mRNA-based cancer immunotherapy CV9201 in patients with stage IIIB/IV non-small cell lung cancer. Cancer Immunol Immunother 68:799–812.
  • Su R, Wang H, Xiao C, et al. (2021). Venetoclax nanomedicine alleviates acute lung injury via increasing neutrophil apoptosis. Biomater Sci 9:4746–54.
  • Tenchov R, Bird R, Curtze AE, et al. (2021). Lipid nanoparticles-from liposomes to mRNA vaccine delivery, a aandscape of research diversity and advancement. ACS Nano 15:16982–7015.
  • Tian X, Bera H, Guo X, et al. (2021). Pulmonary delivery of reactive oxygen species/glutathione-responsive paclitaxel dimeric nanoparticles improved therapeutic indices against metastatic lung cancer. ACS Appl Mater Interfaces 13:56858–72.
  • Uddin MN, Roni MA. (2021). Challenges of storage and stability of mRNA-based COVID-19 vaccines. Vaccines 9:1033.
  • van den Brand D, Gorris MAJ, van Asbeck AH, et al. (2019). Peptide-mediated delivery of therapeutic mRNA in ovarian cancer. Eur J Pharm Biopharm 141:180–90.
  • Veiman KL, Kunnapuu K, Lehto T, et al. (2015). PEG shielded MMP sensitive CPPs for efficient and tumor specific gene delivery in vivo. J Control Release 209:238–47.
  • Vetter V, Denizer G, Friedland LR, et al. (2018). Understanding modern-day vaccines: what you need to know. Ann Med 50:110–20.
  • Wadhwa A, Aljabbari A, Lokras A, et al. (2020). Opportunities and challenges in the delivery of mRNA-based vaccines. Pharmaceutics 12:102.
  • Wang Y, Li J, Oupicky D. (2014). Polymeric plerixafor: effect of PEGylation on CXCR4 antagonism, cancer cell invasion, and DNA transfection. Pharm Res 31:3538–48.
  • Wang Z, Lorenzi JCC, Muecksch F, et al. (2021). Enhanced SARS-CoV-2 neutralization by dimeric IgA. Sci Transl Med 13:eabf1555.
  • Wang P, Zhang L, Liao Y, et al. (2020). Effect of intratracheal instillation of ZnO nanoparticles on acute lung inflammation induced by lipopolysaccharides in mice. Toxicol Sci 173:373–86.
  • Weng Y, Huang Y. (2021). Advances of mRNA vaccines for COVID-19: a new prophylactic revolution begins. Asian J Pharm Sci 16:263–4.
  • Weng Y, Li C, Yang T, et al. (2020). The challenge and prospect of mRNA therapeutics landscape. Biotechnol Adv 40:107534.
  • Wu L, Rodríguez-Rodríguez C, Cun D, et al. (2020). Quantitative comparison of three widely-used pulmonary administration methods in vivo with radiolabeled inhalable nanoparticles. Eur J Pharm Biopharm 152:108–15.
  • Wu L, Wu LP, Wu J, et al. (2021). Poly(lactide-co-glycolide) nanoparticles mediate sustained gene silencing and improved biocompatibility of siRNA delivery systems in mouse lungs after pulmonary administration. ACS Appl Mater Interfaces 13:3722–37.
  • Xu Y, Liang W, Qiu Y, et al. (2016). Incorporation of a nuclear localization signal in pH responsive LAH4-L1 peptide enhances transfection and nuclear uptake of plasmid DNA. Mol Pharm 13:3141–52.
  • Zasheva S, Gugleva V, Andonova V. (2020). Aerosol vaccines–perspectives and therapeutic impact. Scripta Sci Pharmaceut 7:18–25.
  • Zheng Q, Qin F, Luo R, et al. (2021). mRNA-loaded lipid-like nanoparticles for liver base editing via the optimization of central composite design. Adv Funct Mater 31:2011068.