Immunotoxicity of poly (lactic-co-glycolic acid) nanoparticles: influence of surface properties on dendritic cell activation

References

• Antonios, D., P. Rousseau, A. Larange, S. Kerdine-Romer, and M. Pallardy. 2010. “Mechanisms of IL-12 Synthesis by Human Dendritic Cells Treated with the Chemical Sensitizer NiSO4.” Journal of Immunology 185 (1): 89–98. doi:10.4049/jimmunol.0901992.
   PubMed Web of Science ®Google Scholar
• Aragao-Santiago, L., H. Hillaireau, N. Grabowski, S. Mura, T. L. Nascimento, S. Dufort, J.-L. Coll, N. Tsapis, and E. Fattal. 2016. “Compared In Vivo Toxicity in Mice of Lung Delivered Biodegradable and Non-biodegradable Nanoparticles.” Nanotoxicology 10 (3): 292–302. doi:10.3109/17435390.2015.1054908.
   PubMed Web of Science ®Google Scholar
• Audran, R., K. Peter, J. Dannull, Y. Men, E. Scandella, M. Groettrup, B. Gander, and G. Corradin. 2003. “Encapsulation of Peptides in Biodegradable Microspheres Prolongs Their MHC class-I Presentation by Dendritic Cells and Macrophages In Vitro.” Vaccine 21 (11–12): 1250–1255. doi:10.1016/S0264-410X(02)00521-2.
   PubMed Web of Science ®Google Scholar
• Babensee, J. E., and A. Paranjpe. 2005. “Differential Levels of Dendritic Cell Maturation on Different Biomaterials Used in Combination Products.” Journal of Biomedical Materials Research Part A 74 (4): 503–510. doi:10.1002/jbm.a.30429.
   PubMed Web of Science ®Google Scholar
• Bala, I., S. Hariharan, and M. N. Kumar. 2004. “PLGA Nanoparticles in Drug Delivery: The State of the Art.” Critical Reviews in Therapeutic Drug Carrier Systems 21 (5): 387–422. doi:10.1615.
   PubMed Web of Science ®Google Scholar
• Banchereau, J., and R. M. Steinman. 1998. “Dendritic Cells and the Control of Immunity.” Nature 392 (6673): 245–252. doi:10.1038/32588.
   PubMed Web of Science ®Google Scholar
• Bhardwaj, V., S. Hariharan, I. Bala, A. Lamprecht, N. Kumar, R. Panchagnula, and M. N. Kumar. 2005. “Pharmaceutical Aspects of Polymeric Nanoparticles for Oral Delivery.” Journal of Biomedical Nanotechnology 1 (3): 235–258. doi:10.1166/jbn.2005.033.
   Web of Science ®Google Scholar
• Bivas-Benita, M., M. Y. Lin, S. M. Bal, K. E. van Meijgaarden, K. L. M. C. Franken, A. H. Friggen, H. E. Junginger, G. Borchard, M. R. Klein, and T. H. M. Ottenhoff. 2009. “Pulmonary Delivery of DNA Encoding Mycobacterium tuberculosis Latency Antigen Rv1733c Associated to PLGA-PEI Nanoparticles Enhances T Cell Responses in a DNA Prime/protein Boost Vaccination Regimen in Mice.” Vaccine 27 (30): 4010–4017. doi:10.1016/j.vaccine.2009.04.033.
   PubMed Web of Science ®Google Scholar
• Blank, F., P. Stumbles, and C. von Garnier. 2011. “Opportunities and Challenges of the Pulmonary Route for Vaccination.” Expert Opinion on Drug Delivery 8 (5): 547–563. doi:10.1517/17425247.2011.565326.
   PubMed Web of Science ®Google Scholar
• Bisht, R., and I. D. Rupenthal. 2016. “PLGA Nanoparticles for Intravitreal Peptide Delivery: Statistical Optimization, Characterization and Toxicity Evaluation.” Pharmaceutical Development and Technology 3: 1–10. doi:10.1080/10837450.2016.1240184.
   Web of Science ®Google Scholar
• Clawson, C., C. T. Huang, D. Futalan, D. Martin Seible, R. Saenz, M. Larsson, W. Ma, et al. 2010. “Delivery of a Peptide via Poly(d,l-lactic-co-glycolic) Acid Nanoparticles Enhances Its Dendritic Cell-Stimulatory Capacity.” Nanomedicine 6 (5): 651–661. doi:10.1016/j.nano.2010.03.001.
   PubMed Web of Science ®Google Scholar
• Chen, X., and G. Changyou. 2018. “Influences of Surface Coating of PLGA Nanoparticles on Immune Activation of Macrophages.” Journal of Materials Chemistry B 6 (14): 2065–2077. doi:10.1039/C7TB03080K.
   PubMed Web of Science ®Google Scholar
• Dailey, L. A., N. Jekel, L. Fink, T. Gessler, T. Schmehl, M. Wittmar, T. Kissel, and W. Seeger. 2006. “Investigation of the Proinflammatory Potential of Biodegradable Nanoparticle Drug Delivery Systems in the Lung.” Toxicology and Applied Pharmacology 215 (1): 100–108. doi:10.1016/j.taap.2006.01.016.
   PubMed Web of Science ®Google Scholar
• DeLoid, G. M., J. M. Cohen, G. Pyrgiotakis, and P. Demokritou. 2017. “Preparation, Characterization, and In Vitro Dosimetry of Dispersed, engineered Nanomaterials.” Nature Protocols 12 (2): 355–371. doi:10.1038/nprot.2016.172.
   PubMed Web of Science ®Google Scholar
• Di Gioacchino, M., C. Petrarca, F. Lazzarin, L. Di Giampaolo, E. Sabbioni, P. Boscolo, R. Mariani-Costantini, and G. Bernardini. 2011. “Immunotoxicity of Nanoparticles.” International Journal of Immunopathology and Pharmacology 24 (1 Suppl): 65S–71S.
   PubMed Web of Science ®Google Scholar
• Diwan, M., P. Elamanchili, H. Lane, A. Gainer, and J. Samuel. 2003. “Biodegradable Nanoparticle Mediated Antigen Delivery to Human Cord Blood Derived Dendritic Cells for Induction of Primary T Cell Responses.” Journal of Drug Targeting 11 (8–10): 495–507. doi:10.1080/10611860410001670026.
   PubMed Web of Science ®Google Scholar
• Dobrovolskaia, M. A., D. R. Germolec, and J. L. Weaver. 2009. “Evaluation of Nanoparticle Immunotoxicity.” Nature Nanotechnology 4 (7): 411–414. doi:10.1038/nnano.2009.175.
   PubMed Web of Science ®Google Scholar
• Dobrovolskaia, M. A., and S. E. McNeil. 2007. “Immunological Properties of Engineered Nanomaterials.” Nature Nanotechnology 2 (8): 469–478. doi:10.1038/nnano.2007.223.
   PubMed Web of Science ®Google Scholar
• Dobrovolskaia, M. A., M. Shurin, and A. Shvedova. 2016. “Current Understanding of Interactions between Nanoparticles and the Immune System.” Toxicology and Applied Pharmacology 299: 78–89. doi:10.1016/j.taap.2015.12.022.
   PubMed Web of Science ®Google Scholar
• El Ali, Z., C. Delomenie, J. Botton, M. Pallardy, and S. Kerdine-Romer. 2017. “Dendritic Cells' Death Induced by Contact Sensitizers Is Controlled by Nrf2 and Depends on Glutathione Levels.” Toxicology and Applied Pharmacology 322: 41–50. doi:10.1016/j.taap.2017.02.014.
   PubMed Web of Science ®Google Scholar
• Elamanchili, P., M. Diwan, M. Cao, and J. Samuel. 2004. “Characterization of Poly(,-Lactic-co-glycolic Acid) based Nanoparticulate System for Enhanced Delivery of Antigens to Dendritic Cells.” Vaccine 22 (19): 2406–2412. doi:10.1016/j.vaccine.2003.12.032.
   PubMed Web of Science ®Google Scholar
• Fischer, S., E. Uetz-von Allmen, Y. Waeckerle-Men, M. Groettrup, H. P. Merkle, and B. Gander. 2007. “The Preservation of Phenotype and Functionality of Dendritic Cells upon Phagocytosis of Polyelectrolyte-coated PLGA Microparticles.” Biomaterials 28 (6): 994–1004. doi:10.1016/j.biomaterials.2006.10.034.
   PubMed Web of Science ®Google Scholar
• Grabowski, N., H. Hillaireau, J. Vergnaud, N. Tsapis, M. Pallardy, S. Kerdine-Römer, and E. Fattal. 2015. “Surface Coating Mediates the Toxicity of Polymeric Nanoparticles towards Human-like Macrophages.” International Journal of Pharmaceutics 482 (1–2): 75–83. doi:10.1016/j.ijpharm.2014.11.042.
   PubMed Web of Science ®Google Scholar
• Guedj AS1, Kell AJ2, Barnes M2, Stals S1, Gonçalves D3, Girard D3, and Lavigne C1. 2015. Preparation, characterization, and safety evaluation of poly(lactide-co-glycolide) nanoparticles for protein delivery into macrophages. Int J Nanomedicine 10: 5965–79. doi:10.2147/IJN.S82205.
   Google Scholar
• Hamdy, S., A. Haddadi, R. W. Hung, and A. Lavasanifar. 2011. “Targeting Dendritic Cells with Nano-Particulate PLGA Cancer Vaccine Formulations.” Advanced Drug Delivery Reviews 63 (10–11): 943–955. doi:10.1016/j.addr.2011.05.021.
   PubMed Web of Science ®Google Scholar
• Hinderliter, P. M., K. R. Minard, G. Orr, W. B. Chrisler, B. D. Thrall, J. G. Pounds, and J. G. Teeguarden. 2010. “ISDD: A Computational Model of Particle Sedimentation, Diffusion and Target Cell Dosimetry for In Vitro Toxicity Studies.” Particle and Fibre Toxicology 7 (1): 36. doi:10.1186/1743-8977-7-36.
   PubMed Web of Science ®Google Scholar
• Ilinskaya, A. N., and M. A. Dobrovolskaia. 2014. “Immunosuppressive and anti-inflammatory Properties of Engineered Nanomaterials.” British Journal of Pharmacology 171 (17): 3988–4000. doi:10.1111/bph.12722.
   PubMed Web of Science ®Google Scholar
• Jilek, S., M. Ulrich, H. P. Merkle, and E. Walter. 2004. “Composition and Surface Charge of DNA-loaded Microparticles Determine Maturation and Cytokine Secretion in Human Dendritic Cells.” Pharmaceutical Research 21 (7): 1240. doi:10.1023/B:PHAM.0000033012.16152.5d.
   PubMed Web of Science ®Google Scholar
• Larange, A., D. Antonios, M. Pallardy, and S. Kerdine-Romer. 2012. “Glucocorticoids Inhibit Dendritic Cell Maturation Induced by Toll-like Receptor 7 and Toll-like Receptor 8.” Journal of Leukocyte Biology 91 (1): 105–117. doi:10.1189/jlb.1110615.
   PubMed Web of Science ®Google Scholar
• Lu, J. M., X. Wang, C. Marin-Muller, H. Wang, P. H. Lin, Q. Yao, and C. Chen. 2009. “Current Advances in Research and Clinical Applications of PLGA-based Nanotechnology.” Expert Review of Molecular Diagnostics 9 (4): 325–341. doi:10.1586/erm.09.15.
   PubMed Web of Science ®Google Scholar
• Lutsiak, M. E., D. R. Robinson, C. Coester, G. S. Kwon, and J. Samuel. 2002. “Analysis of Poly(D,L-lactic-co-glycolic Acid) Nanosphere Uptake by Human Dendritic Cells and Macrophages In Vitro.” Pharmaceutical Research 19 (10): 1480–1487. doi:10.1023/A:1020452531828.
   PubMed Web of Science ®Google Scholar
• Ma, W., T. Smith, V. Bogin, Y. Zhang, C. Ozkan, M. Ozkan, M. Hayden., et al. 2011. “Enhanced Presentation of MHC Class Ia, Ib and Class II-restricted Peptides Encapsulated in Biodegradable Nanoparticles: A Promising Strategy for Tumor Immunotherapy.” Journal of Translational Medicine 9 (1): 34. doi:10.1186/1479-5876-9-34.
   PubMed Web of Science ®Google Scholar
• Menon, J. U., S. Kona, A. S. Wadajkar, F. Desai, A. Vadla, and K. T. Nguyen. 2012. “Effects of Surfactants on the Properties of PLGA Nanoparticles.” Journal of Biomedical Materials Research Part A 100 (8): 1998–2005. doi:0.1002/jbm.a.34040.
   PubMed Web of Science ®Google Scholar
• Mundargi, R. C., V. R. Babu, V. Rangaswamy, P. Patel, and T. M. Aminabhavi. 2008. “Nano/micro Technologies for Delivering Macromolecular Therapeutics Using Poly(D,L-lactide-co-glycolide) and Its Derivatives.” Journal of Controlled Release 125 (3): 193–209. doi:10.1016/j.jconrel.2007.09.013.
   PubMed Web of Science ®Google Scholar
• Mura, S., H. Hillaireau, J. Nicolas, B. Le Droumaguet, C. Gueutin, S. Zanna, N. Tsapis, and E. Fattal. 2011. “Influence of Surface Charge on the Potential Toxicity of PLGA Nanoparticles towards Calu-3 Cells.” International Journal of Nanomedicine 6: 2591–2605. doi:10.2147/IJN.S24552.
   PubMed Web of Science ®Google Scholar
• Mura, S., H. Hillaireau, J. Nicolas, S. Kerdine-Römer, B. Le Droumaguet, C. Deloménie, V. Nicolas, M. Pallardy, N. Tsapis, and E. Fattal. 2011. “Biodegradable Nanoparticles Meet the Bronchial Airway Barrier: How Surface Properties Affect Their Interaction with Mucus and Epithelial Cells.” Biomacromolecules 12 (11): 4136–4143. doi:10.1021/bm201226x.
   PubMed Web of Science ®Google Scholar
• Neves, B. M., M. Gonçalo, A. Figueiredo, C. B. Duarte, M. C. Lopes, and M. T. Cruz. 2011. “Signal Transduction Profile of Chemical Sensitisers in Dendritic Cells: An Endpoint to Be Included in a Cell-based In Vitro Alternative Approach to Hazard Identification?.” Toxicology and Applied Pharmacology 250 (2): 87–95. doi:10.1016/j.taap.2010.10.003.
   PubMed Web of Science ®Google Scholar
• Newman, K. D., P. Elamanchili, G. S. Kwon, and J. Samuel. 2002. “Uptake of Poly(D,L-lactic-co-glycolic Acid) Microspheres by Antigen-presenting Cells In Vivo.” Journal of Biomedical Materials Research 60 (3): 480–486. doi:10.1002/jbm.10019.
   PubMed Web of Science ®Google Scholar
• Newman, K. D., J. Samuel, and G. Kwon. 1998. “Ovalbumin Peptide Encapsulated in Poly(d,l Lactic-co-glycolic Acid) Microspheres Is Capable of Inducing a T Helper Type 1 Immune Response.” Journal of Controlled Release 54 (1): 49–59. doi:10.1016/S0168-3659(97)00142-9.
   PubMed Web of Science ®Google Scholar
• Oostingh, G. J., E. Casals, P. Italiani, R. Colognato, R. Stritzinger, J. Ponti, T. Pfaller., et al. 2011. “Problems and Challenges in the Development and Validation of Human Cell-based Assays to Determine Nanoparticle-induced Immunomodulatory Effects.” Particle and Fibre Toxicology 8 (1): 8. doi:10.1186/1743-8977-8-8.
   PubMed Web of Science ®Google Scholar
• Panyam, J., and V. Labhasetwar. 2003. “Biodegradable Nanoparticles for Drug and Gene Delivery to Cells and Tissue.” Advanced Drug Delivery Reviews 55 (3): 329–347. doi:10.1016/S0169-409X(02)00228-4.
   PubMed Web of Science ®Google Scholar
• Petrarca C, Clemente E, Amato V, Pedata P, Sabbioni E, Bernardini G, Iavicoli I, Cortese S, Niu Q, Otsuki T, Paganelli R. Di Gioacchino M. 2015. Engineered metal based nanoparticles and innate immunity. Clin Mol Allergy 13 (1): 13. doi:10.1186/s12948-015-0020-1.
   Google Scholar
• Platel, A., R. Carpentier, E. Becart, G. Mordacq, D. Betbeder, and F. Nesslany. 2016. “Influence of the Surface Charge of PLGA Nanoparticles on Their In Vitro Genotoxicity, Cytotoxicity, ROS Production and Endocytosis.” Journal of Applied Toxicology: Jat 36 (3): 434–444. doi:10.1002/jat.3247.
   PubMed Web of Science ®Google Scholar
• Semete, B., L. Booysen, Y. Lemmer, L. Kalombo, L. Katata, J. Verschoor, and H. S. Swai. 2010. “In Vivo Evaluation of the Biodistribution and Safety of PLGA Nanoparticles as Drug Delivery Systems.” Nanomedicine: Nanotechnology, Biology, and Medicine 6 (5): 662–671. doi:10.1016/j.nano.2010.02.002.
   PubMed Web of Science ®Google Scholar
• Spek, S., M. Haeuser, M. M. Schaefer, and K. Langer. 2015. “Characterisation of PEGylated PLGA Nanoparticles Comparing the Nanoparticle Bulk to the Particle Surface Using UV/Vis Spectroscopy, SEC, 1H-NMR Spectroscopy, and X-ray Photoelectron Spectroscopy.” Applied Surface Science 347: 78–85. doi:10.1016/j.apsusc.2015.04.071.
   Web of Science ®Google Scholar
• Sun, H., K. G. J. Pollock, and J. M. Brewer. 2003. “Analysis of the Role of Vaccine Adjuvants in Modulating Dendritic Cell Activation and Antigen Presentation In Vitro.” Vaccine 21 (9–10): 849–855. doi:10.1016/S0264-410X(02)00531-5.
   PubMed Web of Science ®Google Scholar
• Tenzer, S., D. Docter, S. Rosfa, A. Wlodarski, J. Kuharev, A. Rekik, S. K. Knauer., et al. 2011. “Nanoparticle Size Is a Critical Physicochemical Determinant of the Human Blood Plasma Corona: A Comprehensive Quantitative Proteomic Analysis.” ACS Na 5 (9): 7155–7167. doi:10.1021/nn201950e.
   PubMed Web of Science ®Google Scholar
• Waeckerle-Men, Y., E. Scandella, E. Uetz-von Allmen, B. Ludewig, S. Gillessen, H. P. Merkle, B. Gander, and M. Groettrup. 2004. “Phenotype and Functional Analysis of Human Monocyte-Derived Dendritic Cells Loaded with Biodegradable Poly(lactide-co-glycolide) Microspheres for Immunotherapy.” Journal of Immunological Methods 287 (1–2): 109–124. doi:10.1016/j.jim.2004.01.010.
   PubMed Web of Science ®Google Scholar
• Walter, E., D. Dreher, M. Kok, L. Thiele, S. G. Kiama, P. Gehr, and H. P. Merkle. 2001. “Hydrophilic Poly(-Lactide-co-glycolide) Microspheres for the Delivery of DNA to Human-derived Macrophages and Dendritic Cells.” Journal of Controlled Release 76 (1–2): 149–168. doi:10.1016/S0168-3659(01)00413-8.
   PubMed Web of Science ®Google Scholar
• Xu, P., E. Gullotti, L. Tong, C. B. Highley, D. R. Errabelli, T. Hasan, J. X. Cheng, D. S. Kohane, and Y. Yeo. 2009. “Intracellular Drug Delivery by Poly(lactic-co-glycolic Acid) Nanoparticles, Revisited.” Molecular Pharmaceutics 6 (1): 190–201. doi:10.1021/mp800137z.
   PubMed Web of Science ®Google Scholar
• Yoshida, M., and J. E. Babensee. 2004. “Poly(lactic-co-glycolic Acid) Enhances Maturation of Human Monocyte-Derived Dendritic Cells.” Journal of Biomedical Materials Research A 71: 45–54. doi:10.1002/jbm.a.30131.
   PubMed Web of Science ®Google Scholar
• Yoshida, M., and J. E. Babensee. 2006a. “Differential Effects of Agarose and Poly(lactic-co-glycolic Acid) on Dendritic Cell Maturation.” Journal of Biomedical Materials Research Part A 79 (2): 393–408. doi:10.1002/jbm.a.30798.
   PubMed Web of Science ®Google Scholar
• Yoshida, M., and J. E. Babensee. 2006b. “Molecular Aspects of Microparticle Phagocytosis by Dendritic Cells.” Journal of Biomaterials Science Polymer Edition 17 (8): 893–907. doi:10.1163/156856206777996844.
   PubMed Web of Science ®Google Scholar
• Yoshida, M., J. Mata, and J. E. Babensee. 2007. “Effect of Poly(lactic-co-glycolic Acid) Contact on Maturation of Murine Bone Marrow-derived Dendritic Cells.” Journal of Biomedical Materials Research Part A 80 (1): 7–12. doi: 10.1002/jbm.a.30832.
   PubMed Web of Science ®Google Scholar
• Yue, Z.-G., W. Wei, P.-P. Lv, H. Yue, L.-Y. Wang, Z.-G. Su, G.-H. Ma. et al. 2011. “Surface Charge Affects Cellular Uptake and Intracellular Trafficking of Chitosan-Based Nanoparticles.” Biomacromolecules 12 (7): 2440–2446. doi:10.1021/bm101482r.
   PubMed Web of Science ®Google Scholar
• Zolnik, B. S., A. Gonzalez-Fernandez, N. Sadrieh, and M. A. Dobrovolskaia. 2010. “Minireview: Nanoparticles and the Immune System.” Endocrinology 151 (2): 458–465. doi:10.1210/en.2009-1082.
   PubMed Web of Science ®Google Scholar