Biocompatibility assessment of functionalized magnetic mesoporous silica nanoparticles in human HepaRG cells

References

• Antherieu, S., C. Chesne, R. Li, C. Guguen-Guillouzo, and A. Guillouzo. 2012. “Optimization of the HepaRG Cell Model for Drug Metabolism and Toxicity Studies.” Toxicology in Vitro : An International Journal Published in Association with Bibra 26: 1278–1285.
   PubMed Web of Science ®Google Scholar
• Ashley, C. E., E. C. Carnes, G. K. Phillips, D. Padilla, P. N. Durfee, P. A. Brown, T. N. Hanna, et al. 2011. “The Targeted Delivery of Multicomponent Cargos to Cancer Cells by Nanoporous Particle-Supported Lipid Bilayers.” Nature Materials 10: 389–397.
   PubMed Web of Science ®Google Scholar
• Atienzar, F. A., H. Gerets, K. Tilmant, G. Toussaint, and S. Dhalluin. 2013. “Evaluation of Impedance-Based Label-Free Technology as a Tool for Pharmacology and Toxicology Investigations.” Biosensors 3: 132–156.
   PubMedGoogle Scholar
• Bangham, A., M. M. Standish, and J. Watkins. 1965. “Diffusion of Univalent Ions Across the Lamellae of Swollen Phospholipids.” Journal of Molecular Biology 13: 238–252.
   PubMed Web of Science ®Google Scholar
• Beigneux, A. P., A. H. Moser, J. K. Shigenaga, C. Grunfeld, and K. R. Feingold. 2002. “Reduction in Cytochrome P-450 Enzyme Expression is Associated with Repression of CAR (Constitutive Androstane Receptor) and PXR (Pregnane X Receptor) in Mouse Liver During the Acute Phase Response.” Biochemical and Biophysical Research Communications 293: 145–149.
   PubMed Web of Science ®Google Scholar
• Bouchoucha, M., M.-F. Côté, R. C. Gaudreault, M.-A. Fortin, and F. Kleitz. 2016. “Size-Controlled Functionalized Mesoporous Silica Nanoparticles for Tunable Drug Release and Enhanced Anti-Tumoral Activity.” Chemistry of Materials 28: 4243–4258.
   Web of Science ®Google Scholar
• Brown, G., and J. Butler. 1997. “New Method for the Characterization of Domain Morphology of Polymer Blends Using Ruthenium Tetroxide Staining and Low Voltage Scanning Electron Microscopy (LVSEM).” Polymer 38: 3937–3945.
   Web of Science ®Google Scholar
• Cedervall, T., I. Lynch, S. Lindman, T. Berggård, E. Thulin, H. Nilsson, K. A. Dawson, and S. Linse. 2007. “Understanding the Nanoparticle–Protein Corona Using Methods to Quantify Exchange Rates and Affinities of Proteins for Nanoparticles.” Proceedings of the National Academy of Sciences 104: 2050–2055.
   PubMed Web of Science ®Google Scholar
• Danhier, F., E. Ansorena, J. M. Silva, R. Coco, A. Le Breton, and V. Préat. 2012. “PLGA-Based Nanoparticles: An Overview of Biomedical Applications.” Journal of Controlled Release 161: 505–522.
   PubMed Web of Science ®Google Scholar
• Deodhar, G. V., M. L. Adams, and B. G. Trewyn.2017. “Controlled Release and Intracellular Protein Delivery from Mesoporous Silica Nanoparticles.” Biotechnology Journal 12(1). doi: 10.1002/biot.201600408.
   PubMed Web of Science ®Google Scholar
• Durfee, P. N., Y.-S. Lin, D. R. Dunphy, A. J. Muñiz, K. S. Butler, K. R. Humphrey, A. J. Lokke, et al. 2016. “Mesoporous Silica Nanoparticle-Supported Lipid Bilayers (Protocells) for Active Targeting and Delivery to Individual Leukemia Cells.” ACS Nano 10: 8325–8345.
   PubMed Web of Science ®Google Scholar
• Edwards, S. W., Y.-M. Tan, D. L. Villeneuve, M. E. Meek, and C. A. Mcqueen. 2016. “Adverse Outcome Pathways—Organizing Toxicological Information to Improve Decision Making.” Journal of Pharmacology and Experimental Therapeutics 356: 170–181.
   PubMed Web of Science ®Google Scholar
• Guillouzo, A. 1998. “Liver Cell Models in In Vitro Toxicology.” Environmental Health Perspectives 106(Suppl 2): 511–532.
   PubMed Web of Science ®Google Scholar
• Guillouzo, A., A. Corlu, C. Aninat, D. Glaise, F. Morel, and C. Guguen-Guillouzo. 2007. “The Human Hepatoma HepaRG cells: A Highly Differentiated Model for Studies of Liver Metabolism and Toxicity of Xenobiotics.” Chemico-Biological Interactions 168: 66–73.
   PubMed Web of Science ®Google Scholar
• Hart, S. N., Y. Li, K. Nakamoto, E. A. Subileau, D. Steen, and X. B. Zhong. 2010. “A Comparison of Whole Genome Gene Expression Profiles of HepaRG Cells and HepG2 Cells to Primary Human Hepatocytes and Human Liver Tissues.” Drug Metabolism and Disposition 38: 988–994.
   PubMed Web of Science ®Google Scholar
• Hartung, T. 2010. “Food for Thought… on Alternative Methods for Nanoparticle Safety Testing.” Altex 27: 87–95.
   PubMedGoogle Scholar
• Hartung, T. 2017. “Utility of the Adverse Outcome Pathway Concept in Drug Development.” Expert Opinion on Drug Metabolism & Toxicology 13: 1–3.
   PubMed Web of Science ®Google Scholar
• He, Q., Z. Zhang, F. Gao, Y. Li, and J. Shi. 2011. “In vivo Biodistribution and Urinary Excretion of Mesoporous Silica Nanoparticles: Effects of Particle Size and PEGylation.” Small 7: 271–280.
   PubMed Web of Science ®Google Scholar
• Hild, W., K. Pollinger, A. Caporale, C. Cabrele, M. Keller, N. Pluym, A. Buschauer, et al. 2010. “G Protein-Coupled Receptors Function as Logic Gates for Nanoparticle Binding and Cell Uptake.” Proceedings of the National Academy of Sciences of the United States of America 107: 10667–10672.
   PubMed Web of Science ®Google Scholar
• Hudson, S. P., R. F. Padera, R. Langer, and D. S. Kohane. 2008. “The Biocompatibility of Mesoporous Silicates.” Biomaterials 29: 4045–4055.
   PubMed Web of Science ®Google Scholar
• Jennen, D. G. J., C. Magkoufopoulou, H. B. Ketelslegers, M. H. M. Van Herwijnen, J. C. S. Kleinjans, and J. H. M. Van Delft. 2010. “Comparison of HepG2 and HepaRG by Whole-Genome Gene Expression Analysis for the Purpose of Chemical Hazard Identification.” Toxicological Sciences 115: 66–79.
   PubMed Web of Science ®Google Scholar
• Jennings, P., A. Limonciel, L. Felice, and M. O. Leonard. 2013. “An Overview of Transcriptional Regulation in Response to Toxicological Insult.” Archives of Toxicology 87: 49–72.
   PubMed Web of Science ®Google Scholar
• Kanebratt, K. P., and T. B. Andersson. 2008. “HepaRG Cells as an in Vitro Model for Evaluation of Cytochrome P450 Induction in Humans.” Drug Metabolism and Disposition 36: 137–145.
   PubMed Web of Science ®Google Scholar
• Kim, J. A., A. Salvati, C. Aberg, and K. A. Dawson. 2014. “Suppression of Nanoparticle Cytotoxicity Approaching In Vivo Serum Concentrations: Limitations of In Vitro Testing for Nanosafety.” Nanoscale 6: 14180–14184.
   PubMed Web of Science ®Google Scholar
• Li, T., X. Shen, Y. Geng, Z. Chen, L. Li, S. Li, H. Yang, C. Wu, H. Zeng, and Y. Liu. 2016. “Folate-Functionalized Magnetic-Mesoporous Silica Nanoparticles for Drug/Gene Codelivery To Potentiate the Antitumor Efficacy.” ACS Applied Materials & Interfaces 8: 13748–13758.
   PubMed Web of Science ®Google Scholar
• Li, Z., J. C. Barnes, A. Bosoy, J. F. Stoddart, and J. I. Zink. 2012. “Mesoporous Silica Nanoparticles in Biomedical Applications.” Chemical Society Reviews 41: 2590–2605.
   PubMed Web of Science ®Google Scholar
• Lison, D., L. C. Thomassen, V. Rabolli, L. Gonzalez, D. Napierska, J. W. Seo, M. Kirsch-Volders, P. Hoet, C. E. Kirschhock, and J. A. Martens. 2008. “Nominal and Effective Dosimetry of Silica Nanoparticles in Cytotoxicity Assays.” Toxicological Sciences 104: 155–162.
   PubMed Web of Science ®Google Scholar
• Liu, T., L. Li, X. Teng, X. Huang, H. Liu, D. Chen, J. Ren, J. He, and F. Tang. 2011. “Single and Repeated Dose Toxicity of Mesoporous Hollow Silica Nanoparticles in Intravenously Exposed Mice.” Biomaterials 32: 1657–1668.
   PubMed Web of Science ®Google Scholar
• Lobenhofer, E. K., X. Cui, L. Bennett, P. L. Cable, B. A. Merrick, G. A. Churchill, and C. A. Afshari. 2004. “Exploration of Low-Dose Estrogen Effects: Identification of No Observed Transcriptional Effect Level (NOTEL).” Toxicologic Pathology 32: 482–492.
   PubMed Web of Science ®Google Scholar
• Lu, J., M. Liong, Z. Li, J. I. Zink, and F. Tamanoi. 2010. “Biocompatibility, Biodistribution, and Drug-Delivery Efficiency of Mesoporous Silica Nanoparticles for Cancer Therapy in Animals.” Small 6: 1794–1805.
   PubMed Web of Science ®Google Scholar
• Miao, J., S. Fang, J. Lee, C. Comstock, K. E. Knudsen, and J. K. Kemper. 2009. “Functional Specificities of Brm and Brg-1 Swi/Snf ATPases in the Feedback Regulation of Hepatic Bile Acid Biosynthesis.” Molecular and Cellular Biology 29: 6170–6181.
   PubMed Web of Science ®Google Scholar
• Nyalosaso, J., E. Rascol, C. Pisani, C. Dorandeu, X. Dumail, M. Maynadier, M. Gary-Bobo, et al. 2016. “Synthesis, Decoration, and Cellular Effects of Magnetic Mesoporous Silica Nanoparticles.” RSC Advances 6: 57275–57283.
   Web of Science ®Google Scholar
• Perry, J. L., K. G. Reuter, M. P. Kai, K. P. Herlihy, S. W. Jones, J. C. Luft, M. Napier, J. E. Bear, and J. M. Desimone. 2012. “PEGylated PRINT Nanoparticles: The Impact of PEG Density on Protein Binding, Macrophage Association, Biodistribution, and Pharmacokinetics.” Nano Letters 12: 5304–5310.
   PubMed Web of Science ®Google Scholar
• Pisani, C., J.-C. Gaillard, M. Odorico, J. L. Nyalosaso, C. Charnay, Y. Guari, J. Chopineau, J.-M. Devoisselle, J. Armengaud, and O. Prat. 2017a. “The timeline of corona formation around silica nanocarriers highlights the role of the protein interactome.” Nanoscale 9: 1840–1851.
   PubMed Web of Science ®Google Scholar
• Pisani, C., J. C. Gaillard, V. Nouvel, M. Odorico, J. Armengaud, and O. Prat. 2015. “High-Throughput, Quantitative Assessment of the Effects of Low-Dose Silica Nanoparticles on Lung Cells: Grasping Complex Toxicity with a Great Depth of Field.” BMC Genomics 16: 315.
   PubMed Web of Science ®Google Scholar
• Pisani, C., E. Rascol, C. Dorandeu, J.-C. Gaillard, C. Charnay, Y. Guari, J. Chopineau, J. Armengaud, J.-M. Devoisselle, and O. Prat. 2017b. “The Species Origin of the Serum in the Culture Medium Influences the In Vitro Toxicity of Silica Nanoparticles to HepG2 cells.” PLoS One 12: e0182906.
   PubMed Web of Science ®Google Scholar
• Rascol, E., M. Daurat, A. Da Silva, M. Maynadier, C. Dorandeu, C. Charnay, M. Garcia, et al. 2017. “Biological Fate of Fe3O4 Core-Shell Mesoporous Silica Nanoparticles Depending on Particle Surface Chemistry.” Nanomaterials 7: 162.
   Web of Science ®Google Scholar
• Rho, W.-Y., H.-M. Kim, S. Kyeong, Y.-L. Kang, D.-H. Kim, H. Kang, C. Jeong, D.-E. Kim, Y.-S. Lee, and B.-H. Jun. 2014. “Facile Synthesis of Monodispersed Silica-Coated Magnetic Nanoparticles.” Journal of Industrial and Engineering Chemistry 20: 2646–2649.
   Web of Science ®Google Scholar
• Rushmore, T. H., and A. Tony Kong. 2002. “Pharmacogenomics, Regulation and Signaling Pathways of Phase I and II Drug Metabolizing Enzymes.” Current Drug Metabolism 3: 481–490.
   PubMed Web of Science ®Google Scholar
• Russell, W. M. S., and R. L. Burch. 1959. The Principles of Humane Experimental Technique. London, UK: Methuen & Co., Ltd.
   Google Scholar
• Savarala, S., S. Ahmed, M. A. Ilies, and S. L. Wunder. 2010. “Formation and Colloidal Stability of DMPC Supported Lipid Bilayers on SiO2 Nanobeads.” Langmuir 26: 12081–12088.
   PubMed Web of Science ®Google Scholar
• Sergent, J.-A., V. Paget, and S. Chevillard. 2012. “Toxicity and Genotoxicity of Nano-SiO2 on Human Epithelial Intestinal HT-29 Cell Line.” Annals of Occupational Hygiene 56: 622–630.
   PubMed Web of Science ®Google Scholar
• Turpeinen, M., A. Tolonen, C. Chesne, A. Guillouzo, J. Uusitalo, and O. Pelkonen. 2009. “Functional Expression, Inhibition and Induction of CYP Enzymes in HepaRG Cells.” Toxicology in Vitro 23: 748–753.
   PubMed Web of Science ®Google Scholar
• Uz, M., V. Bulmus, and S. Alsoy Altinkaya. 2016. “Effect of PEG Grafting Density and Hydrodynamic Volume on Gold Nanoparticle–Cell Interactions: An Investigation on Cell Cycle, Apoptosis, and DNA Damage.” Langmuir 32: 5997–6009.
   PubMed Web of Science ®Google Scholar
• Vallet-Regí, M., F. Balas, and D. Arcos. 2007. “Mesoporous Materials for Drug Delivery.” Angewandte Chemie International Edition 46: 7548–7558.
   PubMed Web of Science ®Google Scholar
• Vinken, M. 2016. “The Adverse Outcome Pathway for Cholestatic Liver Injury: From Mechanisms to Predictive Human Toxicology.” Toxicology Letters 258:S47.
   Web of Science ®Google Scholar
• Vivero-Escoto, J. L., I. Slowing, B. G. Trewyn, and V. S. Lin. 2010. “Mesoporous Silica Nanoparticles for Intracellular Controlled Drug Delivery.” Small 6: 1952–1967.
   PubMed Web of Science ®Google Scholar
• Witasp, E., N. Kupferschmidt, L. Bengtsson, K. Hultenby, C. Smedman, S. Paulie, A. E. Garcia-Bennett, and B. Fadeel. 2009. “Efficient Internalization of Mesoporous Silica Particles of Different Sizes by Primary Human Macrophages without Impairment of Macrophage Clearance of Apoptotic or Antibody-Opsonized Target Cells.” Toxicology and Applied Pharmacology 239: 306–319.
   PubMed Web of Science ®Google Scholar
• Wright, W. R., K. Parzych, D. Crawford, C. Mein, J. A. Mitchell, and M. J. Paul-Clark. 2012. “Inflammatory Transcriptome Profiling of Human Monocytes Exposed Acutely to Cigarette Smoke.” PLoS One 7: e30120.
   PubMed Web of Science ®Google Scholar
• Xie, J., S. Lee, and X. Chen. 2010. “Nanoparticle-Based Theranostic Agents.” Advanced Drug Delivery Reviews 62: 1064–1079.
   PubMed Web of Science ®Google Scholar
• Yang, P., S. Gai, and J. Lin. 2012. “Functionalized Mesoporous Silica Materials for Controlled Drug Delivery.” Chemical Society Reviews 41: 3679–3698.
   PubMed Web of Science ®Google Scholar
• Zarbl, H., M. A. Gallo, J. Glick, K. Y. Yeung, and P. Vouros. 2010. “The Vanishing Zero Revisited: Thresholds in the Age of Genomics.” Chemico-Biological Interactions 184: 273–278.
   PubMed Web of Science ®Google Scholar
• Zollner, G., P. Fickert, R. Zenz, A. Fuchsbichler, C. Stumptner, L. Kenner, P. Ferenci, et al. 2001. “Hepatobiliary Transporter Expression in Percutaneous Liver Biopsies of Patients with Cholestatic Liver Diseases.” Hepatology 33: 633–646.
   PubMed Web of Science ®Google Scholar
• Zollner, G., H.-U. Marschall, M. Wagner, and M. Trauner. 2006. “Role of Nuclear Receptors in the Adaptive Response to Bile Acids and Cholestasis: Pathogenetic and Therapeutic Considerations.” Molecular Pharmaceutics 3: 231–251.
   PubMed Web of Science ®Google Scholar