Toxicological Research

Korean Society of Toxicology & Korea Environmental Mutagen Society (한국독성학회)
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Evaluation of the skin sensitization potential of metal oxide nanoparticles using the ARE-Nrf2 Luciferase KeratinoSensTM assay

  • Kim, Sung-Hyun (Division of Toxicological Research, National Institute of Food and Drug Safety Evaluation, Ministry of Food and Drug Safety) ;
  • Lee, DongHan (Division of Toxicological Research, National Institute of Food and Drug Safety Evaluation, Ministry of Food and Drug Safety) ;
  • Lee, JinHee (Division of Toxicological Research, National Institute of Food and Drug Safety Evaluation, Ministry of Food and Drug Safety) ;
  • Yang, Jun-Young (Division of Toxicological Research, National Institute of Food and Drug Safety Evaluation, Ministry of Food and Drug Safety) ;
  • Seok, JiHyun (Division of Toxicological Research, National Institute of Food and Drug Safety Evaluation, Ministry of Food and Drug Safety) ;
  • Jung, Kikyung (Division of Toxicological Research, National Institute of Food and Drug Safety Evaluation, Ministry of Food and Drug Safety) ;
  • Lee, JongKwon (Division of Toxicological Research, National Institute of Food and Drug Safety Evaluation, Ministry of Food and Drug Safety)
  • Received : 2020.06.15
  • Accepted : 2020.10.08
  • Published : 2021.04.15
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Abstract

Numerous studies have reported the potential of chemicals for inducing skin sensitization; however, few studies have examined skin sensitization induced by nanomaterials. This study aimed to evaluate skin sensitization induced by metal oxide nanoparticles (NPs) using the ARE-Nrf2 Luciferase KeratinoSensTM assay. Seven different metal oxide NPs, including copper oxide, cobalt oxide, nickel oxide, titanium oxide, cerium oxide, iron oxide, and zinc oxide, were assessed on KeratinoSensTM cells. We selected an appropriate vehicle among three vehicles (DMSO, DW, and culture medium) by assessing the hydrodynamic size at vehicle selection process. Seven metal oxide NPs were analyzed, and their physicochemical properties, including hydrodynamic size, polydispersity, and zeta potential, were determined in the selected vehicle. Thereafter, we assessed the sensitization potential of the NPs using the ARE-Nrf2 Luciferase KeratinoSensTM assay. Copper oxide NPs induced a positive response, whereas cobalt oxide, nickel oxide, titanium oxide, cerium oxide, iron oxide, and zinc oxide NPs induced no response. These results suggest that the ARE-Nrf2 Luciferase KeratinoSensTM assay may be useful for evaluating the potential for skin sensitization induced by metal oxide NPs.

Keywords

Acknowledgement

This study was supported by grants from the Ministry of Food and Drug Safety in 2018-2019 (18181MFDS361). We would like to thank Editage (http://www.editage.co.kr) for English language editing.

References

  1. Han BI, Yi JS, Seo SJ, Kim TS, Ahn I, Ko K, Kim JH, Bae S, Lee JK (2019) Evaluation of skin sensitization potential of chemicals by local lymph node assay using 5-bromo-2-deoxyuridine with flow cytometry. Regul Toxicol Pharmacol 107:104401. https://doi.org/10.1016/j.yrtph.2019.05.026
  2. Park EJ, Park K (2009) Oxidative stress and pro-inflammatory responses induced by silica nanoparticles in vivo and in vitro. Toxicol Lett 184:18-25. https://doi.org/10.1016/j.toxlet.2008.10.012
  3. Cho WS, Duffin R, Bradley M, Megson IL, MacNee W, Lee JK, Jeong J, Donaldson K (2013) Predictive value of in vitro assays depends on the mechanism of toxicity of metal oxide nanoparticles. Part Fibre Toxicol 10:55. https://doi.org/10.1186/1743-8977-10-55
  4. Nel AE, Madler L, Velegol D, Xia T, Hoek EM, Somasundaran P, Klaessig F, Castranova V, Thompson M (2009) Understanding biophysicochemical interactions at the nano-bio interface. Nat Mater 8:543-557. https://doi.org/10.1038/nmat2442
  5. Warheit DB, Laurence BR, Reed KL, Roach DH, Reynolds GA, Webb TR (2004) Comparative pulmonary toxicity assessment of single-wall carbon nanotubes in rats. Toxicol Sci 77:117-125. https://doi.org/10.1093/toxsci/kfg228
  6. Jiang J, Oberdorster G, Biswas P (2009) Characterization of size, surface charge, and agglomeration state of nanoparticle dispersions for toxicological studies. J Nanopart Res 11:77-89. https://doi.org/10.1007/s11051-008-9446-4
  7. Mahmoudi M, Laurent S, Shokrgozar MA, Hosseinkhani M (2011) Toxicity evaluations of superparamagnetic iron oxide nanoparticles: cell "vision" versus physicochemical properties of nanoparticles. ACS Nano 5:7263-7276. https://doi.org/10.1021/nn2021088
  8. Gate L, Disdier C, Cosnier F, Gagnaire F, Devoy J, Saba W, Brun E, Chalansonnet M, Mabondzo A (2017) Biopersistence and translocation to extrapulmonary organs of titanium dioxide nanoparticles after subacute inhalation exposure to aerosol in adult and elderly rats. Toxicol Lett 265:61-69. https://doi.org/10.1016/j.toxlet.2016.11.009
  9. OECD (2018) Test No. 442D: In vitro skin sensitisation: ARE-Nrf2 luciferase test method. OECD guidelines for the testing of chemicals, Section 4. OECD Publishing, Paris. https://doi.org/10.1787/9789264229822-en
  10. OECD (2014) The adverse outcome pathway for skin sensitisation initiated by covalent binding to proteins. OECD series on testing and assessment, No. 168. OECD Publishing, Paris. https://doi.org/10.1787/9789264221444-en
  11. Park YH, Jeong SH, Yi SM, Choi BH, Kim YR, Kim IK, Kim MK, Son SW (2011) Analysis for the potential of polystyrene and TiO2 nanoparticles to induce skin irritation, phototoxicity, and sensitisation. Toxicol Vitro 25:1863-1869. https://doi.org/10.1016/j.tiv.2011.05.022
  12. Yoshioka Y, Kuroda E, Hirai T, Tsutsumi Y, Ishii KJ (2017) Allergic responses induced by the immunomodulatory effects of nanomaterials upon skin exposure. Front Immunol 8:169. https://doi.org/10.3389/fimmu.2017.00169
  13. Dwivedi PD, Tripathi A, Ansari KM, Shanker R, Das M (2011) Impact of nanoparticles on the immune system. J Biomed Nanotechnol 7:193-194. https://doi.org/10.1166/jbn.2011.1264
  14. Dykman LA, Khlebtsov NG (2017) Immunological properties of gold nanoparticles. Chem Sci 8:1719-1735. https://doi.org/10.1039/c6sc03631g
  15. Bihari P, Vippola M, Schultes S, Praetner M, Khandoga AG, Reichel CA, Coester C, Tuomi T, Rehberg M, Krombach F (2008) Optimized dispersion of nanoparticles for biological in vitro and in vivo studies. Part Fibre Toxicol 5:14. https://doi.org/10.1186/1743-8977-5-14
  16. Jeong J, Kim SH, Lee S, Lee DK, Han Y, Jeon S, Cho WS (2018) Differential contribution of constituent Metal ions to the cytotoxic effects of fast-dissolving metal-oxide nanoparticles. Front Pharmacol 9:15. https://doi.org/10.3389/fphar.2018.00015
  17. Natsch A, Ryan CA, Foertsch L, Emter R, Jaworska J, Gerberick F, Kern P (2013) A dataset on 145 chemicals tested in alternative assays for skin sensitization undergoing prevalidation. J Appl Toxicol 33:1337-1352. https://doi.org/10.1002/jat.2868
  18. EURL-ECVAM (2014) Recommendation on the KeratinoSens™ assay for skin sensitisation testing. https://ec.europa.eu/jrc/en/publication/eur-scientific-and-technical-research-reports/eurl-ecvam-recommendation-keratinosenstm-assay-skin-sensitisation-testing. Accessed 22 Oct 2020
  19. Emter R, Ellis G, Natsch A (2010) Performance of a novel keratinocyte-based reporter cell line to screen skin sensitizers in vitro. Toxicol Appl Pharmacol 245:281-290. https://doi.org/10.1016/j.taap.2010.03.009
  20. Andreas N, Caroline B, Leslie F, Frank G, Kimberly N, Allison H, Heather I, Robert L, Stefan O, Hendrik R, Andreas S, Roger E (2011) The intra-and inter-laboratory reproducibility and predictivity of the KeratinoSens assay to predict skin sensitizers in vitro: results of a ring-study in five laboratories. Toxicol Vitro 25:733-744. https://doi.org/10.1016/j.tiv.2010.12.014
  21. Andres E, Sa-Rocha VM, Barrichello C, Haupt T, Ellis G, Natsch A (2013) The sensitivity of the KeratinoSens™ assay to evaluate plant extracts: a pilot study. Toxicol Vitro 27:1220-1225. https://doi.org/10.1016/j.tiv.2013.02.008
  22. Settivari RS, Gehen SC, Amado RA, Visconti NR, Boverhof DR, Carney EW (2015) Application of the KeratinoSens™ assay for assessing the skin sensitization potential of agrochemical active ingredients and formulations. Regul Toxicol Pharmacol 72:350-360. https://doi.org/10.1016/j.yrtph.2015.05.006
  23. OECD (2017) Test No. 318: Dispersion stability of nanomaterials in simulated environmental media. OECD guidelines for the testing of chemicals, section 3. OECD Publishing, Paris. https://doi.org/10.1787/9789264284142-en
  24. Osaka T, Nakanishi T, Shanmugam S, Takahama S, Zhang H (2009) Effect of surface charge of magnetite nanoparticles on their internalization into breast cancer and umbilical vein endothelial cells. Colloids Surf B 71:325-330. https://doi.org/10.1016/j.colsurfb.2009.03.004
  25. Jeon S, Clavadetscher J, Lee DK, Chankeshwara SV, Bradley M, Cho WS (2018) Surface charge-dependent cellular uptake of polystyrene nanoparticles. Nanomaterials 8:1028. https://doi.org/10.3390/nano8121028
  26. Jang YS, Lee EY, Park YH, Jeong SH, Lee SG, Kim YR, Kim MK, Son SW (2012) The potential for skin irritation, phototoxicity, and sensitisation of ZnO nanoparticles. Mol Cell Toxicol 8:171-177. https://doi.org/10.1007/s13273-012-0021-9
  27. Hartwig A, Commission MAK (2002) Iron oxides (inhalable fraction) [MAK Value Documentation, 2011]. MAK-Collect Occup Health Saf Annu Thresholds Classif Workplace 1:1804-1869. https://doi.org/10.1002/3527600418.mb0209fste5116
  28. OECD DOSSIER ON CERIUM OXIDE (2015) Series on the safety of manufactured nanomaterials No. 45. http://www.oecd.org/officialdocuments/publicdisplaydocumentpdf/?cote=env/jm/mono(2015)8&doclanguage=en. Accessed 22 Oct 2020
  29. Wang M, Lai X, Shao L, Li L (2018) Evaluation of immunoresponses and cytotoxicity from skin exposure to metallic nanoparticles. Int J Nanomed 13:4445. https://doi.org/10.2147/IJN.S170745
  30. Filon FL, Mauro M, Adami G, Bovenzi M, Crosera M (2015) Nanoparticles skin absorption: new aspects for a safety profile evaluation. Regul Toxicol Pharmacol 72:310-322. https://doi.org/10.1016/j.yrtph.2015.05.005
  31. Fukuyama T, Ueda H, Hayashi K, Tajima Y, Shuto Y, Kosaka T, Harada T (2008) Sensitizing potential of chromated copper arsenate in local lymph node assays differs with the solvent used. J Immunotoxicol 5:99-106. https://doi.org/10.1080/15476910802085715
  32. Cho WS, Duffin R, Poland CA, Duschl A, Oostingh GJ, MacNee W, Bradley M, Megson IL, Donaldson K (2012) Differential pro-inflammatory effects of Metal oxide nanoparticles and their soluble ions in vitro and in vivo; zinc and copper nanoparticles, but not their ions, recruit eosinophils to the lungs. Nanotoxicology 6:22-35. https://doi.org/10.3109/17435390.2011.552810
  33. Jeong J, Lee S, Kim SH, Han Y, Lee DK, Yang JY, Jeong J, Roh C, Huh YS, Cho WS (2016) Evaluation of the dose metric for acute lung inflammogenicity of fast-dissolving metal oxide nanoparticles. Nanotoxicology 10:1448-1457. https://doi.org/10.1080/17435390.2016.1229518
  34. Cohen D, Soroka Y, Ma'or Z, Oron M, Portugal-Cohen M, Bregegere FM, Milner Y (2013) Evaluation of topically applied copper (II) oxide nanoparticle cytotoxicity in human skin organ culture. Toxicol In Vitro 27:292-298. https://doi.org/10.1016/j.tiv.2012.08.026