Impact of physico-chemical properties on the toxicological potential of reduced graphene oxide in human bronchial epithelial cells

References

• Achawi, S., J. Pourchez, B. Feneon, and V. Forest. 2021. “Graphene-Based Materials in Vitro Toxicity and Their Structure-Activity Relationships: A Systematic Literature Review.” Chemical Research in Toxicology 34 (9): 2003–2018. https://doi.org/10.1021/acs.chemrestox.1c00243
   PubMed Web of Science ®Google Scholar
• Aimonen, K., M. Imani, M. Hartikainen, S. Suhonen, E. Vanhala, C. Moreno, O. J. Rojas, et al. 2022. “Surface Functionalization and Size Modulate the Formation of Reactive Oxygen Species and Genotoxic Effects of Cellulose Nanofibrils.” Particle and Fibre Toxicology 19 (1): 19. https://doi.org/10.1186/s12989-022-00460-3
   PubMed Web of Science ®Google Scholar
• Akhavan, O., E. Ghaderi, and A. Akhavan. 2012. “Size-Dependent Genotoxicity of Graphene Nanoplatelets in Human Stem Cells.” Biomaterials 33 (32): 8017–8025. https://doi.org/10.1016/j.biomaterials.2012.07.040
   PubMed Web of Science ®Google Scholar
• Anichini, C., and P. Samorì. 2021. “Graphene-Based Hybrid Functional Materials.” Small 17 (33): e2100514. https://doi.org/10.1002/smll.202100514
   PubMed Web of Science ®Google Scholar
• Bengtson, S., K. Kling, A. M. Madsen, A. W. Noergaard, N. R. Jacobsen, P. A. Clausen, B. Alonso, et al. 2016. “No Cytotoxicity or Genotoxicity of Graphene and Graphene Oxide in Murine Lung Epithelial FE1 Cells in Vitro.” Environmental and Molecular Mutagenesis 57 (6): 469–482. https://doi.org/10.1002/em.22017
   PubMed Web of Science ®Google Scholar
• Bianco, A., H.-M. Cheng, T. Enoki, Y. Gogotsi, R. H. Hurt, N. Koratkar, T. Kyotani, et al. 2013. “All in the Graphene Family – A Recommended Nomenclature for Two-Dimensional Carbon Materials.” Carbon 65: 1–6. https://doi.org/10.1016/j.carbon.2013.08.038
   Web of Science ®Google Scholar
• Bianco, A., and M. Prato. 2015. “Safety Concerns on Graphene and 2D Materials: A Flagship Perspective.” 2D Materials 2 (3): 030201–030201. https://doi.org/10.1088/2053-1583/2/3/030201
   Google Scholar
• Brownson, D. A. C., D. K. Kampouris, and C. E. Banks. 2011. “An Overview of Graphene in Energy Production and Storage Applications.” Journal of Power Sources 196 (11): 4873–4885. https://doi.org/10.1016/j.jpowsour.2011.02.022
   Web of Science ®Google Scholar
• Burgum, M. J., M. J. D. Clift, S. J. Evans, N. Hondow, M. Miller, S. B. Lopez, A. Williams, et al. 2021. “In Vitro Primary-Indirect Genotoxicity in Bronchial Epithelial Cells Promoted by Industrially Relevant Few-Layer Graphene.” Small 17 (15): e2002551. https://doi.org/10.1002/smll.202002551
   PubMed Web of Science ®Google Scholar
• Cebadero-Dominguez, Ó., C. Medrano-Padial, M. Puerto, S. Sánchez-Ballester, A. M. Cameán, and Á. Jos. 2023. “Genotoxicity Evaluation of Graphene Derivatives by a Battery of in Vitro Assays.” Chemico-Biological Interactions 372: 110367. https://doi.org/10.1016/j.cbi.2023.110367
   PubMed Web of Science ®Google Scholar
• Chatterjee, N., H. J. Eom, and J. Choi. 2014. “A Systems Toxicology Approach to the Surface Functionality Control of Graphene-Cell Interactions.” Biomaterials 35 (4): 1109–1127. https://doi.org/10.1016/j.biomaterials.2013.09.108
   PubMed Web of Science ®Google Scholar
• Chatterjee, N., J. S. Yang, K. Park, S. M. Oh, J. Park, and J. Choi. 2015. “Screening of Toxic Potential of Graphene Family Nanomaterials Using in Vitro and Alternative in Vivo Toxicity Testing Systems.” Environmental Health and Toxicology 30: e2015007. https://doi.org/10.5620/eht.e2015007
   PubMedGoogle Scholar
• Chee, S. Y., H. L. Poh, C. K. Chua, F. Šaněk, Z. Sofer, and M. Pumera. 2012. “Influence of Parent Graphite Particle Size on the Electrochemistry of Thermally Reduced Graphene Oxide.” Physical Chemistry Chemical Physics 14 (37): 12794–12799. https://doi.org/10.1039/c2cp41462g
   PubMed Web of Science ®Google Scholar
• Chee, W. K., H. N. Lim, Z. Zainal, N. M. Huang, I. Harrison, and Y. Andou. 2016. “Flexible Graphene-Based Supercapacitors: A Review.” The Journal of Physical Chemistry C 120 (8): 4153–4172. in pp https://doi.org/10.1021/acs.jpcc.5b10187
   Web of Science ®Google Scholar
• Dekkers, S., A. G. Oomen, E. A. J. Bleeker, R. J. Vandebriel, C. Micheletti, J. Cabellos, G. Janer, et al. 2016. “Towards a Nanospecific Approach for Risk Assessment.” Regulatory Toxicology and Pharmacology 80: 46–59. https://doi.org/10.1016/j.yrtph.2016.05.037
   PubMed Web of Science ®Google Scholar
• Domenech, J., A. Hernández, E. Demir, R. Marcos, and C. Cortés. 2020. “Interactions of Graphene Oxide and Graphene Nanoplatelets with the in Vitro Caco-2/HT29 Model of Intestinal Barrier.” Scientific Reports 10 (1): 2793. https://doi.org/10.1038/s41598-020-59755-0
   PubMed Web of Science ®Google Scholar
• Domenech, J., A. Rodríguez-Garraus, A. L. de Cerain, A. Azqueta, and J. Catalán. 2022. “Genotoxicity of Graphene-Based Materials.” Nanomaterials 12 (11): 1795. https://doi.org/10.3390/nano12111795
   Web of Science ®Google Scholar
• Fadeel, B., C. Bussy, S. Merino, E. Vázquez, E. Flahaut, F. Mouchet, L. Evariste, et al. 2018. “Safety Assessment of Graphene-Based Materials: Focus on Human Health and the Environment.” ACS Nano American Chemical Society 12 (11): 10582–10620. https://doi.org/10.1021/acsnano.8b04758
   PubMed Web of Science ®Google Scholar
• Fenech, M. 2020. “Cytokinesis-Block Micronucleus Cytome Assay Evolution into a More Comprehensive Method to Measure Chromosomal Instability.” Genes 11 (10): 1–13. https://doi.org/10.3390/genes11101203
   Web of Science ®Google Scholar
• Ferrari, A. C., and D. M. Basko. 2013. “Raman Spectroscopy as a Versatile Tool for Studying the Properties of Graphene.” Nature Nanotechnology 8 (4): 235–246. https://doi.org/10.1038/nnano.2013.46
   PubMed Web of Science ®Google Scholar
• Franz, P., A. Bürkle, P. Wick, and C. Hirsch. 2020. “Exploring Flow Cytometry-Based Micronucleus Scoring for Reliable Nanomaterial Genotoxicity Assessment.” Chemical Research in Toxicology 33 (10): 2538–2549. https://doi.org/10.1021/acs.chemrestox.0c00071
   PubMed Web of Science ®Google Scholar
• Galindo, B., S. G. Alcolea, J. Gómez, A. Navas, A. O. Murguialday, M. P. Fernandez, R. C. Puelles, et al. 2014. “Effect of the Number of Layers of Graphene on the Electrical Properties of TPU Polymers.” IOP Conference Series Materials Science and Engineering 64: 012008. https://doi.org/10.1088/1757-899X/64/1/012008
   Google Scholar
• García-Rodríguez, A., L. Kazantseva, L. Vila, L. Rubio, A. Velázquez, M. J. Ramírez, R. Marcos, et al. 2019. “Micronuclei Detection by Flow Cytometry as a High-Throughput Approach for the Genotoxicity Testing of Nanomaterials.” Nanomaterials 9 (12): 1677. https://doi.org/10.3390/nano9121677
   Web of Science ®Google Scholar
• Geim, A. K., and K. S. Novoselov. 2007. “The Rise of Graphene.” Nature Materials 6 (3): 183–191. https://doi.org/10.1038/nmat1849
   PubMed Web of Science ®Google Scholar
• Gómez, J., E. Villaro, A. Navas, and I. Recio. 2017. “Testing the Influence of the Temperature, RH and Filler Type and Content on the Universal Power Law for New Reduced Graphene Oxide TPU Composites.” Materials Research Express 4 (10): 105020–105020. https://doi.org/10.1088/2053-1591/aa8e11
   Web of Science ®Google Scholar
• Guo, F., M. Creighton, Y. Chen, R. Hurt, and I. Külaots. 2014. “Porous Structures in Stacked, Crumpled and Pillared Graphene-Based 3D Materials.” Carbon 66: 476–484. https://doi.org/10.1016/j.carbon.2013.09.024
   PubMed Web of Science ®Google Scholar
• Guo, Z., S. Chakraborty, F. A. Monikh, D.-D. Varsou, A. J. Chetwynd, A. Afantitis, I. Lynch, et al. 2021. “Surface Functionalization of Graphene‐Based Materials: Biological Behavior, Toxicology, and Safe‐by‐Design Aspects.” Advanced Biology 5 (9): e2100637. https://doi.org/10.1002/adbi.202100637
   PubMedGoogle Scholar
• Hashemi, E., O. Akhavan, M. Shamsara, R. Rahighi, A. Esfandiar, and A. R. Tayefeh. 2014. “Cyto and Genotoxicities of Graphene Oxide and Reduced Graphene Oxide Sheets on Spermatozoa.” RSC Advances 4 (52): 27213–27223. https://doi.org/10.1039/c4ra01047g
   Web of Science ®Google Scholar
• Hinzmann, M., S. Jaworski, M. Kutwin, J. Jagiełło, R. Koziński, M. Wierzbicki, M. Grodzik, et al. 2014. “Nanoparticles Containing Allotropes of Carbon Have Genotoxic Effects on Glioblastoma Multiforme Cells.” International Journal of Nanomedicine 9 (1): 2409–2417. https://doi.org/10.2147/IJN.S62497
   PubMedGoogle Scholar
• Huang, X., Z. Yin, S. Wu, X. Qi, Q. He, Q. Zhang, Q. Yan, et al. 2011. “Graphene-Based Materials: Synthesis, Characterization, Properties, and Applications.” Small 7 (14): 1876–1902. https://doi.org/10.1002/smll.201002009
   PubMed Web of Science ®Google Scholar
• Kohl, Y., E. Rundén-Pran, E. Mariussen, M. Hesler, N. El Yamani, E. M. Longhin, M. Dusinska, et al. 2020. “Genotoxicity of Nanomaterials: Advanced in Vitro Models and High Throughput Methods for Human Hazard Assessment—A Review.” Nanomaterials 10 (10): 1911. https://doi.org/10.3390/nano10101911
   Web of Science ®Google Scholar
• Li, R., L. M. Guiney, C. H. Chang, N. D. Mansukhani, Z. Ji, X. Wang, Y.-P. Liao, et al. 2018. “Surface Oxidation of Graphene Oxide Determines Membrane Damage, Lipid Peroxidation, and Cytotoxicity in Macrophages in a Pulmonary Toxicity Model.” ACS Nano 12 (2): 1390–1402. https://doi.org/10.1021/acsnano.7b07737
   PubMed Web of Science ®Google Scholar
• Magne, T. M., T. de Oliveira Vieira, L. M. R. Alencar, F. F. M. Junior, S. Gemini-Piperni, S. V. Carneiro, L. M. U. D. Fechine, et al. 2022. “Graphene and Its Derivatives: understanding the Main Chemical and Medicinal Chemistry Roles for Biomedical Applications.” Journal of Nanostructure in Chemistry 12 (5): 693–727. https://doi.org/10.1007/s40097-021-00444-3
   PubMed Web of Science ®Google Scholar
• Mahmoudi, T., Y. Wang, and Y. B. Hahn. 2018. “Graphene and Its Derivatives for Solar Cells Application.” Nano Energy 47: 51–65. https://doi.org/10.1016/j.nanoen.2018.02.047
   Web of Science ®Google Scholar
• Majeed, W., S. Bourdo, D. M. Petibone, V. Saini, K. B. Vang, Z. A. Nima, K. M. Alghazali, et al. 2017. “The Role of Surface Chemistry in the Cytotoxicity Profile of Graphene.” Journal of Applied Toxicology 37 (4): 462–470. https://doi.org/10.1002/jat.3379
   PubMed Web of Science ®Google Scholar
• Mittal, S., V. Kumar, N. Dhiman, L. K. S. Chauhan, R. Pasricha, and A. K. Pandey. 2016. “Physico-Chemical Properties Based Differential Toxicity of Graphene Oxide/Reduced Graphene Oxide in Human Lung Cells Mediated through Oxidative Stress.” Scientific Reports 6 (1): 39548–39548. https://doi.org/10.1038/srep39548
   PubMedGoogle Scholar
• Mukherjee, S. P., N. Lozano, M. Kucki, A. E. Del Rio-Castillo, L. Newman, E. Vázquez, K. Kostarelos, et al. 2016. “Detection of Endotoxin Contamination of Graphene Based Materials Using the TNF-α Expression Test and Guidelines for Endotoxin-Free Graphene Oxide Production.” PLOS One 11 (11): e0166816-e0166816. https://doi.org/10.1371/journal.pone.0166816
   Web of Science ®Google Scholar
• OECD. 2023. Test No. 487: In Vitro Mammalian Cell Micronucleus Test. https://www.oecd-ilibrary.org/docserver/9789264264861-en.pdf?expires=1696319862&id=id&accname=guest&checksum=35B99E0BF45E0F053ADE2A260CD274D5
   Google Scholar
• Ou, L., X. Lv, Z. Wu, W. Xia, Y. Huang, L. Chen, W. Sun, et al. 2021. “Oxygen Content-Related DNA Damage of Graphene Oxide on Human Retinal Pigment Epithelium Cells.” Journal of Materials Science Materials in Medicine 32 (2): 20. https://doi.org/10.1007/s10856-021-06491-0
   PubMed Web of Science ®Google Scholar
• Park, M. V. D. Z., E. A. J. Bleeker, W. Brand, F. R. Cassee, M. van Elk, I. Gosens, W. H. de Jong, et al. 2017. “Considerations for Safe Innovation: The Case of Graphene.” ACS Nano 11 (10): 9574–9593. https://doi.org/10.1021/acsnano.7b04120
   PubMed Web of Science ®Google Scholar
• Pei, S., and H. M. Cheng. 2012. “The Reduction of Graphene Oxide.” Carbon 50 (9): 3210–3228. https://doi.org/10.1016/j.carbon.2011.11.010
   Web of Science ®Google Scholar
• Pelin, M., L. Fusco, V. León, C. Martín, A. Criado, S. Sosa, E. Vázquez, et al. 2017. “Differential Cytotoxic Effects of Graphene and Graphene Oxide on Skin Keratinocytes.” Scientific Reports 7 (1): 40572. https://doi.org/10.1038/srep40572
   PubMedGoogle Scholar
• Pelin, M., C. Passerino, A. Rodríguez-Garraus, M. Carlin, S. Sosa, S. Suhonen, G. Vales, et al. 2023. “Role of Chemical Reduction and Formulation of Graphene Oxide on Its Cytotoxicity towards Human Epithelial Bronchial Cells.” Nanomaterials 13 (15): 2189. https://doi.org/10.3390/nano13152189
   Web of Science ®Google Scholar
• Pelin, M., S. Sosa, M. Prato, and A. Tubaro. 2018. “Occupational Exposure to Graphene Based Nanomaterials: Risk Assessment.” Nanoscale Royal Society of Chemistry 10 (34): 15894–15903. in https://doi.org/10.1039/c8nr04950e
   Google Scholar
• Promega. 2023. CytoTox-ONE™ Homogeneous Membrane Integrity Assay Instructions for Use of Products G7890, G7891 and G7892.
   Google Scholar
• Ray, S. C. 2015. “Application and Uses of Graphene Oxide and Reduced Graphene Oxide.” In Applications of Graphene and Graphene-Oxide Based Nanomaterials, edited by Sekhar Chandra Ray, 39–55. Amsterdam: Elsevier.
   Google Scholar
• Razaq, A., F. Bibi, X. Zheng, R. Papadakis, S. H. M. Jafri, and H. Li. 2022. “Review on Graphene-, Graphene Oxide-, Reduced Graphene Oxide-Based Flexible Composites: From Fabrication to Applications.” Materials 15 (3): 1012. https://doi.org/10.3390/ma15031012
   PubMed Web of Science ®Google Scholar
• Reina, G., J. M. González-Domínguez, A. Criado, E. Vázquez, A. Bianco, and M. Prato. 2017. “Promises, Facts and Challenges for Graphene in Biomedical Applications.” Chemical Society Reviews 46 (15): 4400–4416. https://doi.org/10.1039/c7cs00363c
   PubMed Web of Science ®Google Scholar
• Rodriguez-Garraus, A., A. Azqueta, F. Laborda, A. C. Gimenez-Ingalaturre, A. Ezquerra, L. Lostao, A. Lopez de Cerain, et al. 2022. “In Vitro Genotoxicity Evaluation of an Antiseptic Formulation Containing Kaolin and Silver Nanoparticles.” Nanomaterials 12 (6): 914. https://doi.org/10.3390/nano12060914
   Web of Science ®Google Scholar
• Ruijter, N., L. G. Soeteman-Hernández, M. Carrière, M. Boyles, P. McLean, J. Catalán, A. Katsumiti, et al. 2023. “The State of the Art and Challenges of in Vitro Methods for Human Hazard Assessment of Nanomaterials in the Context of Safe-by-Design.” Nanomaterials 13 (3): 472. https://doi.org/10.3390/nano13030472
   Web of Science ®Google Scholar
• Sargent, L. M., A. F. Hubbs, S.-H. Young, M. L. Kashon, C. Z. Dinu, J. L. Salisbury, S. A. Benkovic, et al. 2012. “Single-Walled Carbon Nanotube-Induced Mitotic Disruption.” Mutation Research 745 (1–2): 28–37. https://doi.org/10.1016/j.mrgentox.2011.11.017
   PubMed Web of Science ®Google Scholar
• Tarelho, J. P. G., M. P. Soares dos Santos, J. A. F. Ferreira, A. Ramos, S. Kopyl, S. O. Kim, S. Hong, et al. 2018. “Graphene-Based Materials and Structures for Energy Harvesting with Fluids – A Review.” Materials Today 21 (10): 1019–1041. https://doi.org/10.1016/j.mattod.2018.06.004
   Web of Science ®Google Scholar
• Vales, G., S. Suhonen, K. M. Siivola, K. M. Savolainen, J. Catalán, and H. Norppa. 2020. “Size, Surface Functionalization, and Genotoxicity of Gold Nanoparticles in Vitro.” Nanomaterials 10 (2): 271. https://doi.org/10.3390/nano10020271
   Web of Science ®Google Scholar
• Wick, P., A. E. Louw-Gaume, M. Kucki, H. F. Krug, K. Kostarelos, B. Fadeel, K. A. Dawson, et al. 2014. “Classification Framework for Graphene-Based Materials.” Angewandte Chemie 53 (30): 7714–7718. https://doi.org/10.1002/anie.201403335
   Google Scholar
• Zhang, W., L. Yan, M. Li, R. Zhao, X. Yang, T. Ji, Z. Gu, et al. 2015. “Deciphering the Underlying Mechanisms of Oxidation-State Dependent Cytotoxicity of Graphene Oxide on Mammalian Cells.” Toxicology Letters 237 (2): 61–71. https://doi.org/10.1016/j.toxlet.2015.05.021
   PubMed Web of Science ®Google Scholar