PLGA microparticle formulations for tunable delivery of a nano-engineered filamentous bacteriophage-based vaccine: in vitro and in silico-supported approach
Journal of Nanostructure in Chemistry - Trang 1-16 - 2023
Tóm tắt
Bacteriophages have attracted great attention in the bioengineering field in diverse research areas from tissue engineering to therapeutic and clinical applications. Recombinant filamentous bacteriophage, carrying multiple copies of foreign peptides on protein capsid has been successfully used in the vaccine delivery setting, even if their plasma instability and degradation have limited their use on the pharmaceutical market. Encapsulation techniques in polymeric materials can be applied to preserve bacteriophage activity, extend its half-life, and finely regulate their release in the target environment. The main goal of this study was to provide tunable formulations of the bacteriophage encapsulated in polymeric microparticles (MPs). We used poly (lactic-co-glycolic-acid) as a biocompatible and biodegradable polymer with ammonium bicarbonate as a porogen to encapsulate bacteriophage expressing OVA (257–264) antigenic peptide. We demonstrate that nano-engineered fdOVA bacteriophages encapsulated in MPs preserve their structure and are immunologically active, inducing a strong immune response towards the delivered peptide. Moreover, MP encapsulation prolongs bacteriophage stability over time also at room temperature. Additionally, in this study, we show the ability of in silico-supported approach to predict and tune the release of bacteriophages. These results lay the framework for a versatile bacteriophage-based vaccine delivery system that could successfully generate robust immune responses in a sustained manner, to be used as a platform against cancer and new emerging diseases. Synopsis: administration of recombinant bacteriophage-loaded PLGA microparticles for antigen delivery. PLGA microparticles release the bacteriophages, inducing activation of dendritic cells and enhancing antigen presentation and specific T cell response. Bacteriophage-encapsulated microneedles potentially can be administered into human body and generate robust immune responses.
Tài liệu tham khảo
Sartorius, R., D’Apice, L., Trovato, M., Cuccaro, F., Costa, V., De Leo, M.G., Marzullo, V.M., Biondo, C., D’Auria, S., De Matteis, M.A., Ciccodicola, A., De Berardinis, P.: Antigen delivery by filamentous bacteriophage fd displaying an anti- DEC -205 single-chain variable fragment confers adjuvanticity by triggering a TLR 9-mediated immune response. EMBO Mol. Med. 7, 973–988 (2015)
Sartorius, R., Bettua, C., D’Apice, L., Caivano, A., Trovato, M., Russo, D., Zanoni, I., Granucci, F., Mascolo, D., Barba, P.: Vaccination with filamentous bacteriophages targeting DEC-205 induces DC maturation and potent anti-tumor T-cell responses in the absence of adjuvants. Eur. J. Immunol. 41, 2573–2584 (2011)
Sartorius, R., D’Apice, L., Barba, P., Cipria, D., Grauso, L., Cutignano, A., De Berardinis, P.: Vectorized delivery of alpha-Galactosylceramide and tumor antigen on filamentous bacteriophage fd induces protective immunity by enhancing tumor-specific T cell response. Front. Immunol. 9, 1496 (2018)
Murgas, P., Bustamante, N., Araya, N., Cruz-Gómez, S., Durán, E., Gaete, D., Oyarce, C., López, E., Herrada, A.A., Ferreira, N.: A filamentous bacteriophage targeted to carcinoembryonic antigen induces tumor regression in mouse models of colorectal cancer. Cancer Immunol. Immunother. 67, 183–193 (2018)
Staquicini, D.I., Tang, F.H.F., Markosian, C., Yao, V.J., Staquicini, F.I., Dodero-Rojas, E., Contessoto, V.G., Davis, D., O’ Brien, P., Habib, N.: Design and proof of concept for targeted phage-based COVID-19 vaccination strategies with a streamlined cold-free supply chain. Proc. Natl. Acad. Sci. 118, 30 (2021).
Dubey, A.K., Kumar Gupta, V., Kujawska, M., Orive, G., Kim, N.Y., Li, C., Kumar Mishra, Y., Kaushik, A.: Exploring nano-enabled CRISPR-Cas-powered strategies for efficient diagnostics and treatment of infectious diseases. J. Nanostruct. Chem. 12, 833–864 (2022)
de da Barros, A.O.S., Pinto, S.R., dos Reis, S.R.R., Ricci-Junior, E., Alencar, L.M.R., Bellei, N.C.J., Janini, L.R.M., Maricato, J.T., Rosa, D.S., Santos-Oliveira, R.: Polymeric nanoparticles and nanomicelles of hydroxychloroquine co-loaded with azithromycin potentiate anti-SARS-CoV-2 effect. J. Nanostruct. Chem. 1–19 (2022). https://doi.org/10.1007/s40097-022-00476-3
Sartorius, R., D’Apice, L., Prisco, A., Berardinis, P.D.: Arming filamentous bacteriophage, a nature-made nanoparticle, for new vaccine and immunotherapeutic strategies. Pharmaceutics. 11, 437 (2019)
Stern, Z., Stylianou, D.C., Kostrikis, L.G.: The development of inovirus-associated vector vaccines using phage-display technologies. Expert Rev. Vaccines. 18, 913–920 (2019)
Jamaledin, R., Sartorius, R., Di Natale, C., Vecchione, R., De Berardinis, P., Netti, P.A.: Recombinant filamentous bacteriophages encapsulated in biodegradable polymeric microparticles for stimulation of innate and adaptive immune responses. Microorganisms. 8, 650 (2020)
González-Mora, A., Hernández-Pérez, J., Iqbal, H., Rito-Palomares, M., Benavides, J.: Bacteriophage-based vaccines: a potent approach for antigen delivery. Vaccines. 8, 504 (2020)
Bartolacci, C., Andreani, C., Curcio, C., Occhipinti, S., Massaccesi, L., Giovarelli, M., Galeazzi, R., Iezzi, M., Tilio, M., Gambini, V.: Phage-based anti-HER2 vaccination can circumvent immune tolerance against breast cancer. Cancer Immunol. Res. 6, 1486–1498 (2018)
Wang, Y., Sheng, J., Chai, J., Zhu, C., Li, X., Yang, W., Cui, R., Ge, T.: Filamentous bacteriophage—a powerful carrier for glioma therapy. Front. Immunol. 12, 3611 (2021)
Foglizzo, V., Marchiò, S.: Bacteriophages as therapeutic and diagnostic vehicles in cancer. Pharmaceuticals. 14, 161 (2021)
Malek-Khatabi, A., Tabandeh, Z., Nouri, A., Mozayan, E., Sartorius, R., Rahimi, S., Jamaledin, R.: Long-Term Vaccine Delivery and Immunological Responses Using Biodegradable Polymer-Based Carriers. ACS Appl. Bio Mater. 5, 5015–5040 (2022)
Di Natale, C., La Manna, S., De Benedictis, I., Brandi, P., Marasco, D.: Perspectives in peptide-based vaccination strategies for syndrome coronavirus 2 pandemic. Front. Pharmacol. 11, 578382 (2020)
Jamaledin, R., Makvandi, P., Yiu, C.K.Y., Agarwal, T., Vecchione, R., Sun, W., Maiti, T.K., Tay, F.R., Netti, P.A.: Engineered microneedle patches for controlled release of active compounds: recent advances in release profile tuning. Adv. Ther. 3, 2000171 (2020)
Li, M., Du, C., Guo, N., Teng, Y., Meng, X., Sun, H., Li, S., Yu, P., Galons, H.: Composition design and medical application of liposomes. Eur. J. Med. Chem. 164, 640–653 (2019)
Colom, J., Cano-Sarabia, M., Otero, J., Aríñez-Soriano, J., Cortés, P., Maspoch, D., Llagostera, M.: Microencapsulation with alginate/CaCO 3: a strategy for improved phage therapy. Sci. Rep. 7, 1–10 (2017)
Zare, E.N., Jamaledin, R., Naserzadeh, P., Afjeh-Dana, E., Ashtari, B., Hosseinzadeh, M., Vecchione, R., Wu, A., Tay, F.R., Borzacchiello, A., Makvandi, P.: Metal-based nanostructures/PLGA nanocomposites: antimicrobial activity, cytotoxicity, and their biomedical applications. ACS Appl. Mater. Interfaces. 12, 3279–3300 (2020).
Malik, D.J., Sokolov, I.J., Vinner, G.K., Mancuso, F., Cinquerrui, S., Vladisavljevic, G.T., Clokie, M.R.J., Garton, N.J., Stapley, A.G.F., Kirpichnikova, A.: Formulation, stabilisation and encapsulation of bacteriophage for phage therapy. Adv. Colloid Interface Sci. 249, 100–133 (2017)
Battisti, M., Vecchione, R., Casale, C., Pennacchio, F.A., Lettera, V., Jamaledin, R., Profeta, M., Di Natale, C., Imparato, G., Urciuolo, F., Netti, P.A.: Non-invasive production of multi-compartmental biodegradable polymer microneedles for controlled intradermal drug release of labile molecules. Front. Bioeng. Biotechnol. 7, 296 (2019)
Wójcik-Pastuszka, D., Krzak, J., Macikowski, B., Berkowski, R., Osiński, B., Musiał, W.: Evaluation of the release kinetics of a pharmacologically active substance from model intra-articular implants replacing the cruciate ligaments of the knee. Materials (Basel) 12, 1202 (2019)
Mircioiu, C., Voicu, V., Anuta, V., Tudose, A., Celia, C., Paolino, D., Fresta, M., Sandulovici, R., Mircioiu, I.: Mathematical modeling of release kinetics from supramolecular drug delivery systems. Pharmaceutics. 11, 140 (2019)
Jakhmola, A., Vecchione, R., Gentile, F., Profeta, M., Manikas, A.C., Battista, E., Celentano, M., Onesto, V., Netti, P.A.: Experimental and theoretical study of biodirected green synthesis of gold nanoflowers. Mater. Today Chem. 14, 100203 (2019)
Bruschi, M.L.: Strategies to modify the drug release from pharmaceutical systems. Woodhead Publishing (2015)
Dash, S., Murthy, P.N., Nath, L., Chowdhury, P.: Kinetic modeling on drug release from controlled drug delivery systems. Acta Pol. Pharm. Drug Res. 67, 217–223 (2010)
Del Pozzo, G., Mascolo, D., Sartorius, R., Citro, A., Barba, P., D’ Apice, L., De Berardinis, P.: Triggering DTH and CTL activity by fd filamentous bacteriophages: role of CD4+ T cells in memory responses. J. Biomed. Biotechnol. 2010, 894971 (2010)
Di Natale, C., Onesto, V., Lagreca, E., Vecchione, R., Netti, P.A.: Tunable release of curcumin with an in silico-supported approach from mixtures of highly porous PLGA microparticles. Materials (Basel) 13, 1807–1808 (2020)
Di Natale, C., De Rosa, D., Profeta, M., Jamaledin, R., Attanasio, A., Lagreca, E., Scognamiglio, P.L., Netti, P.A., Vecchione, R.: Design of biodegradable bi-compartmental microneedles for the stabilization and the controlled release of the labile molecule collagenase for skin healthcare. J. Mater. Chem. B. 9, 392–403 (2021)
Profeta, M., Di Natale, C., Lagreca, E., Mollo, V., Netti, P.A., Vecchione, R.: Cell membrane-coated oil in water nano-emulsions as biomimetic nanocarriers for lipophilic compounds conveyance. Pharmaceutics. 13, 1069 (2021)
Di Natale, C., Celetti, G., Scognamiglio, P.L., Cosenza, C., Battista, E., Causa, F., Netti, P.A.: Molecularly endowed hydrogel with an in silico-assisted screened peptide for highly sensitive small molecule harvesting. Chem. Commun. 54, 10088–10091 (2018)
Celetti, G., Di Natale, C., Causa, F., Battista, E., Netti, P.A.: Functionalized poly (ethylene glycol) diacrylate microgels by microfluidics: in situ peptide encapsulation for in serum selective protein detection. Colloids Surf. B Biointerfaces. 145, 21–29 (2016)
Di Natale, C., Battista, E., Lettera, V., Reddy, N., Pitingolo, G., Vecchione, R., Causa, F., Netti, P.A.: Easy surface functionalization and bioconjugation of peptides as capture agents of a microfluidic biosensing platform for multiplex assay in serum. Bioconjug. Chem. 32.8, 1593–1601 (2021)
Di Natale, C., La Manna, S., Malfitano, A.M., Di Somma, S., Florio, D., Scognamiglio, P.L., Novellino, E., Netti, P.A., Marasco, D.: Structural insights into amyloid structures of the C-terminal region of nucleophosmin 1 in type A mutation of acute myeloid leukemia. Biochim. Biophys. Acta Proteins Proteomics. 1867, 637–644 (2019)
Fotticchia, T., Vecchione, R., Scognamiglio, P.L., Guarnieri, D., Calcagno, V., Di Natale, C., Attanasio, C., De Gregorio, M., Di Cicco, C., Quagliariello, V., Maurea, N., Barbieri, A., Arra, C., Raiola, L., Iaffaioli, R.V., Netti, P.A.: Enhanced drug delivery into cell cytosol via glycoprotein H-derived peptide conjugated nanoemulsions. ACS Nano 11, 9802–9813 (2017)
Di Natale, C., Natale, C.F., Florio, D., Netti, P.A., Morelli, G., Ventre, M., Marasco, D.: Effects of surface nanopatterning on internalization and amyloid aggregation of the fragment 264–277 of nucleophosmin 1. Colloids Surf. B Biointerfaces. 197, 111439 (2020)
Di Natale, C., Florio, D., Di Somma, S., Di Matteo, A., Federici, L., Netti, P.A., Morelli, G., Malfitano, A.M., Marasco, D.: Proteostasis unbalance of nucleophosmin 1 in acute myeloid leukemia: an aggregomic perspective. Int. J. Biol. Macromol. 164, 3501–3507 (2020)
Florio, D., Di Natale, C., Scognamiglio, P.L., Leone, M., La Manna, S., Di Somma, S., Netti, P.A., Malfitano, A.M., Marasco, D.: Self-assembly of bio-inspired heterochiral peptides. Bioorg. Chem. 114, 105047 (2021)
Olofsson, L., Ankarloo, J., Andersson, P.O., Nicholls, I.A.: Filamentous bacteriophage stability in non-aqueous media. Chem. Biol. 8, 661–671 (2001)
Rakonjac, J., Russel, M., Khanum, S., Brooke, S.J., Rajič, M.: Filamentous phage: structure and biology. In: Recombinant antibodies for infectious diseases, pp. 1–20. Springer (2017)
Berardinis, P.D., Sartorius, R., Caivano, A., Mascolo, D., Domingo, G.J., Pozzo, G.D., Gaubin, M., Perham, R.N., Piatier-Tonneau, D., Guardiola, J.: Use of fusion proteins and procaryotic display systems for delivery of HIV-1 antigens: development of novel vaccines for HIV-1 infection. Curr. HIV Res. 1, 441–446 (2003)
Lee, J.H., Yeo, Y.: Controlled drug release from pharmaceutical nanocarriers. Chem. Eng. Sci. 125, 75–84 (2015)
Rabiee, N., Bagherzadeh, M., Ghadiri, A.M., Kiani, M., Ahmadi, S., Jajarmi, V., Fatahi, Y., Aldhaher, A., Tahriri, M., Webster, T.J., Mostafavi, E.: Calcium-based nanomaterials and their interrelation with chitosan: optimization for pCRISPR delivery. J. Nanostruct. Chem. (2021). https://doi.org/10.1007/s40097-021-00446-1
Tabasi, H., Babaei, M., Abnous, K., Taghdisi, S.M., Saljooghi, A.S., Ramezani, M., Alibolandi, M.: Metal–polymer-coordinated complexes as potential nanovehicles for drug delivery. J. Nanostruct. Chem. 11, 501–526 (2021)
Zafar, H., Raza, F., Yousefiasl, S.: T-cell membrane-functionalized nanosystems for viral infectious diseases. Mater. Chem. Horizons. 2, 8 (2023)
Raza, F., Zafar, H., Hatami, K., Khan, A.U.: T-cell membrane-coated nanomaterials in cancer treatment. Mater. Chem. Horizons. 1, 199–217 (2022)
Movagharnezhad, N., Ehsanimehr, S., Najafi Moghadam, P.: Synthesis of poly (N-vinylpyrrolidone)-grafted-magnetite bromoacetylated cellulose via ATRP for drug delivery. Mater. Chem. Horizons. 1, 89–98 (2022)
Yousefiasl, S., Manoochehri, H., Makvandi, P., Afshar, S., Salahinejad, E., Khosraviyan, P., Saidijam, M., Soleimani Asl, S., Sharifi, E.: Chitosan/alginate bionanocomposites adorned with mesoporous silica nanoparticles for bone tissue engineering. J. Nanostruct. Chem. (2022). https://doi.org/10.1007/s40097-022-00507-z
Allahyari, M., Mohit, E.: Peptide/protein vaccine delivery system based on PLGA particles. Hum. Vaccin. Immunother. 12, 806–828 (2016)
Silva, A.L., Soema, P.C., Slütter, B., Ossendorp, F., Jiskoot, W.: PLGA particulate delivery systems for subunit vaccines: linking particle properties to immunogenicity. Hum. Vaccin. Immunother. 12, 1056–1069 (2016)
Lagreca, E., Onesto, V., Di Natale, C., La Manna, S., Netti, P.A., Vecchione, R.: Recent advances in the formulation of PLGA microparticles for controlled drug delivery. Prog. Biomater. 9, 153–174 (2020)
Dong, Y., Su, H., Jiang, H., Zheng, H., Du, Y., Wu, J., Li, D.: Experimental study on the influence of low-frequency and low-intensity ultrasound on the permeability of the Mycobacterium smegmatis cytoderm and potentiation with levofloxacin. Ultrason. Sonochem. 37, 1–8 (2017)
Yoshida, M., Mata, J., Babensee, J.E.: Effect of poly (lactic-co-glycolic acid) contact on maturation of murine bone marrow-derived dendritic cells. J. Biomed. Mater. Res. Part A 80, 7–12 (2007)
Koerner, J., Horvath, D., Groettrup, M.: Harnessing dendritic cells for poly (D, L-lactide-co-glycolide) microspheres (PLGA MS)—Mediated anti-tumor therapy. Front. Immunol. 10, 707 (2019)