Comprehensive in vitro toxicity testing of a panel of representative oxide nanomaterials: First steps towards an intelligent testing strategy

PLoS ONE

Volumn 10, Issue 5, 2015, Pages

  Farcal, Lucian ^a   Andón, Fernando Torres ^a   Di Cristo, Luisana ^b   Rotoli, Bianca Maria ^b   Bussolati, Ovidio ^b   Bergamaschi, Enrico ^b   Mech, Agnieszka ^c   Hartmann, Nanna B ^c,d   Rasmussen, Kirsten ^c   Riego Sintes, Juan ^c   Ponti, Jessica ^c   Kinsner Ovaskainen, Agnieszka ^c   Rossi, François ^c   Oomen, Agnes ^e   Bos, Peter ^e   Chen, Rui ^f   Bai, Ru ^f   Chen, Chunying ^f   Rocks, Louise ^g   Fulton, Norma ^h   Ross, Bryony ^h,i   Hutchison, Gary ^h   Tran, Lang ⁱ   Mues, Sarah ^j   Ossig, Rainer ^j   Schnekenburger, Jürgen ^j   Campagnolo, Luisa ^k   Vecchione, Lucia ^k   Pietroiusti, Antonio ^k   Fadeel, Bengt ^a   more..

^a KAROLINSKA INSTITUTE   (Sweden)

^b UNIVERSITY OF PARMA   (Italy)

^c JOINT RESEARCH CENTRE   (Italy)

^d TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^e NATIONAL INSTITUTE FOR PUBLIC HEALTH AND THE ENVIRONMENT   (Netherlands)

^f NATIONAL CENTER FOR NANOSCIENCE AND TECHNOLOGY   (China)

^g UNIVERSITY COLLEGE DUBLIN   (Ireland)

^h EDINBURGH NAPIER UNIVERSITY   (United Kingdom)

ⁱ INSTITUTE OF OCCUPATIONAL MEDICINE   (United Kingdom)

^j UNIVERSITY OF MÜNSTER   (Germany)

^k UNIVERSITY OF ROME TOR VERGATA   (Italy)

more..

Author keywords

[No Author keywords available]

Indexed keywords

NANOMATERIAL; SILICON DIOXIDE; TITANIUM DIOXIDE; ZINC OXIDE; OXIDE; TITANIUM;

ARTICLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOKINE RELEASE; CYTOTOXICITY; EMBRYOTOXICITY; GENITAL SYSTEM; HUMAN; HUMAN CELL; HUMAN TISSUE; HYDROPHILICITY; HYDROPHOBICITY; IMMUNE SYSTEM; IN VITRO STUDY; MACROPHAGE; MALE; OXIDATIVE STRESS; PHYSICAL CHEMISTRY; RESPIRATORY SYSTEM; RISK ASSESSMENT; TOXICITY TESTING; ANIMAL; CELL CULTURE TECHNIQUE; CHEMISTRY; DRUG EFFECTS; EMBRYONIC STEM CELL; EPITHELIUM CELL; IC50; LEYDIG CELL; MOUSE; SERTOLI CELL;

ANIMALS; CELL CULTURE TECHNIQUES; EMBRYONIC STEM CELLS; EPITHELIAL CELLS; HUMANS; IN VITRO TECHNIQUES; INHIBITORY CONCENTRATION 50; LEYDIG CELLS; MACROPHAGES; MALE; MICE; NANOSTRUCTURES; OXIDES; SERTOLI CELLS; SILICON DIOXIDE; TITANIUM; TOXICITY TESTS; ZINC OXIDE;

EID: 84930653106     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0127174     Document Type: Article

References (58)

1. Nel AE, Madler L, Velegol D, Xia T, Hoek EM, Somasundaran P, et al. Understanding biophysicochemical interactions at the nano-bio interface. Nat Mater 2009, 8(7):543-557. doi: 10.1038/nmat2442 PMID: 19525947
2. Manke A, Wang L, Rojanasakul Y: Mechanisms of nanoparticle-induced oxidative stress and toxicity. Biomed Res Int 2013, 2013:942916. doi: 10.1155/2013/942916 PMID: 24027766
3. Aschberger K, Micheletti C, Sokull-Kluttgen B, Christensen FM: Analysis of currently available data for characterising the risk of engineered nanomaterials to the environment and human health-lessons learned from four case studies. Environ Int 2011, 37(6):1143-1156. doi: 10.1016/j.envint.2011.02.005 PMID: 21397332
4. Johnston HJ, Hutchison GR, Christensen FM, Peters S, Hankin S, Stone V: Identification of the mechanisms that drive the toxicity of TiO(2) particulates: the contribution of physicochemical characteristics. Part Fibre Toxicol 2009, 6:33. doi: 10.1186/1743-8977-6-33 PMID: 20017923
5. Karlsson HL, Toprak MS, Fadeel B: Toxicity of Metal and Metal Oxide Nanoparticles. In: Handbook on the Toxicology of Metals. Fourth edn.: Academic Press; 2014: 75-112.
6. Stone V, Pozzi-Mucelli S, Tran L, Aschberger K, Sabella S, Vogel U, et al: ITS-NANO - Prioritising nanosafety research to develop a stakeholder driven intelligent testing strategy. Part Fibre Toxicol 2014, 11(1):9.
7. Vermeire T, Aldenberg T, Buist H, Escher S, Mangelsdorf I, Paune E, et al. OSIRIS, a quest for proof of principle for integrated testing strategies of chemicals for four human health endpoints. Regul Toxicol Pharmacol 2013, 67(2):136-145. doi: 10.1016/j.yrtph.2013.01.007 PMID: 23385135
8. Oberdorster G: Safety assessment for nanotechnology and nanomedicine: concepts of nanotoxicology. J Intern Med 2010, 267(1):89-105. doi: 10.1111/j.1365-2796.2009.02187.x PMID: 20059646
9. Guidance manual for the testing of manufactured nanomaterials: OECD's Sponsorship Programme; First revision. In: ENV/JM/MONO(2009)20/REV. OECD; 2009.
10. Hartung T, Sabbioni E: Alternative in vitro assays in nanomaterial toxicology. Wiley Interdiscip Rev Nanomed Nanobiotechnol 2011.
11. Kroll A, Dierker C, Rommel C, Hahn D, Wohlleben W, Schulze-Isfort C, et al. Cytotoxicity screening of 23 engineered nanomaterials using a test matrix of ten cell lines and three different assays. Part Fibre Toxicol 2011, 8:9. doi: 10.1186/1743-8977-8-9 PMID: 21345205
12. Hirsch C, Roesslein M, Krug HF, Wick P: Nanomaterial cell interactions: are current in vitro tests reliable? Nanomedicine (Lond) 2011, 6(5):837-847.
13. Fadeel B, Savolainen K: Broaden the discussion. Nat Nanotechnol 2013, 8(2):71. doi: 10.1038/nnano.2013.2 PMID: 23380922
14. Savolainen K, Backman U, Brouwer D, Fadeel B, Fernandes T, Kuhlbusch T, et al. Nanosafety in Europe 2015-2025: Towards Safe and Sustainable Nanomaterials and Nanotechnology Innovations. Helsinki: Finnish Institute of Occupational Health; 2013. doi: 10.3389/fphar.2015.00055 PMID: 25852557
15. Compendium of Projects in the European NanoSafety Cluster; 2014.
16. Krug HF, Wick P: Nanotoxicology: an interdisciplinary challenge. Angew Chem Int Ed Engl 2011, 50 (6):1260-1278. doi: 10.1002/anie.201001037 PMID: 21290492
17. EC-JRC Nanomaterials Repository. Available: http://ihcp.jrc.ec.europa.eu/our-activities/nanotechnology/nanomaterials-repository.
18. Roebben G, Rasmussen K, Kestens V, Linsinger TPJ, Rauscher H, Emons H, Stamm H: Reference materials and representative test materials: the nanotechnology case. J Nanoparticle Research 2013, 15.
19. Xia T, Hamilton RF, Bonner JC, Crandall ED, Elder A, Fazlollahi F, et al. Interlaboratory evaluation of in vitro cytotoxicity and inflammatory responses to engineered nanomaterials: the NIEHS Nano GO Consortium. Environ Health Perspect 2013, 121(6):683-690. doi: 10.1289/ehp.1306561 PMID: 23649538
20. Nel AE: Implementation of alternative test strategies for the safety assessment of engineered nanomaterials. J Intern Med 2013.
21. Rasmussen K, Mech A, Mast J, De Temmerman P-J, Waegeneers N, Van Steen F, et al. Synthetic Amorphous Silicon Dioxide (NM-200, NM-201, NM-202, NM-203, NM-204): Characterisation and Physico-Chemical Properties. JRC Repository: NM-series of Representative Manufactured Nanomaterials. In: JRC Scientific and Policy Reports. 2013, ISBN 978-92-79-32323-2, EUR 26046 EN.
22. Rasmussen K, Mast J, De Temmerman P-J, Verleysen E, Waegeneers N, Van Steen F, Pizzolon JC, et al: Titanium Dioxide, NM-100, NM-101, NM-102, NM-103, NM-104, NM-105: Characterisation and Physico-Chemical Properties. In: JRC Science and Policy Reports. 2014, ISBN 978-92-79-38188-1, EUR 26637 EN.
23. Singh C, Friedrichs S, Levin M, Birkedal R, Jensen KA, Pojana G, et al: Zinc Oxide (NM-110, NM-111, NM-112, NM-113) Characterisation and Test Item Preparation. JRC Repository: NM-series of Representative Manufactured Nanomaterials. In: JRC Scientific and Technical Reports. 2011, ISBN 978-92-79-22215-3, EUR 25066 EN.
24. Neun BW, Dobrovolskaia MA: Detection and quantitative evaluation of endotoxin contamination in nanoparticle formulations by LAL-based assays. Methods Mol Biol 2011, 697:121-130. doi: 10.1007/978-1-60327-198-1-12 PMID: 21116960
25. Smulders S, Kaiser JP, Zuin S, Van Landuyt KL, Golanski L, Vanoirbeek J, et al. Contamination of nanoparticles by endotoxin: evaluation of different test methods. Part Fibre Toxicol 2012, 9:41. doi: 10.1186/1743-8977-9-41 PMID: 23140310
26. Pietroiusti A, Massimiani M, Fenoglio I, Colonna M, Valentini F, Palleschi G, et al: Low doses of pristine and oxidized single-wall carbon nanotubes affect mammalian embryonic development. ACS Nano 2011, 5(6):4624-4633. doi: 10.1021/nn200372g PMID: 21615177
27. OECD Testing Programme. Available: http://www.oecd.org/science/nanosafety/sponsorshipprogrammeforthetestingofmanufacturednanomaterials.htm.
28. EU NANOGENOTOX Joint Action. Available: http://www.nanogenotox.eu/index.php?option=com-content&view=article&id=136&Itemid=158.
29. FP-7 NANoREG - A common European approach to the regulatory testing of Manufactured Nanomaterials. Available: http://nanoreg.eu/.
30. Hole P, Sillence K, Hannell C, Maguire CM, Roesslein M, Suarez G, et al: Interlaboratory comparison of size measurements on nanoparticles using nanoparticle tracking analysis (NTA). J Nanopart Res 2013, 15:2101. PMID: 24348090
31. Han X, Gelein R, Corson N, Wade-Mercer P, Jiang J, Biswas P, et al: Validation of an LDH assay for assessing nanoparticle toxicity. Toxicology 2011, 287(1-3):99-104. doi: 10.1016/j.tox.2011.06.009 PMID: 21708217
32. Monteiro-Riviere NA, Inman AO, Zhang LW: Limitations and relative utility of screening assays to assess engineered nanoparticle toxicity in a human cell line. Toxicol Appl Pharmacol 2009, 234(2):222-235. doi: 10.1016/j.taap.2008.09.030 PMID: 18983864
33. Guadagnini R, Halamoda Kenzaoui B, Cartwright L, Pojana G, Magdolenova Z, Bilanicova D, et al: Toxicity screenings of nanomaterials: challenges due to interference with assay processes and components of classic in vitro tests. Nanotoxicology 2013, Jul 27.
34. Cho WS, Duffin R, Bradley M, Megson IL, MacNee W, Lee JK, et al: Predictive value of in vitro assays depends on the mechanism of toxicity of metal oxide nanoparticles. Part Fibre Toxicol 2013, 10(1):55. doi: 10.1186/1743-8977-10-55 PMID: 24156363
35. Genschow E, Spielmann H, Scholz G, Pohl I, Seiler A, Clemann N, et al: Validation of the embryonic stem cell test in the international ECVAM validation study on three in vitro embryotoxicity tests. Altern Lab Anim 2004, 32(3):209-244. PMID: 15588166
36. Park MV, Annema W, Salvati A, Lesniak A, Elsaesser A, Barnes C, et al: In vitro developmental toxicity test detects inhibition of stem cell differentiation by silica nanoparticles. Toxicol Appl Pharmacol 2009, 240(1):108-116. doi: 10.1016/j.taap.2009.07.019 PMID: 19631676
37. Schrurs F, Lison D: Focusing the research efforts. Nat Nanotechnol 2012, 7(9):546-548. doi: 10.1038/nnano.2012.148 PMID: 22902960
38. Kroll A, Pillukat MH, Hahn D, Schnekenburger J: Interference of engineered nanoparticles with in vitro toxicity assays. Archives of toxicology 2012, 86(7):1123-1136. doi: 10.1007/s00204-012-0837-z PMID: 22407301
39. Lesniak A, Fenaroli F, Monopoli MP, Aberg C, Dawson KA, Salvati A: Effects of the presence or absence of a protein corona on silica nanoparticle uptake and impact on cells. ACS Nano 2012, 6 (7):5845-5857. doi: 10.1021/nn300223w PMID: 22721453
40. Lesniak A, Salvati A, Santos-Martinez MJ, Radomski MW, Dawson KA, Aberg C: Nanoparticle adhesion to the cell membrane and its effect on nanoparticle uptake efficiency. Journal of the American Chemical Society 2013, 135(4):1438-1444. doi: 10.1021/ja309812z PMID: 23301582
41. Love SA, Maurer-Jones MA, Thompson JW, Lin YS, Haynes CL: Assessing nanoparticle toxicity. Annu Rev Anal Chem (Palo Alto Calif) 2012, 5:181-205. doi: 10.1146/annurev-anchem-062011-143134 PMID: 22524221
42. Zhang J, Song W, Guo J, Sun Z, Li L, Ding F, Gao M: Cytotoxicity of different sized TiO2 nanoparticles in mouse macrophages. Toxicol Ind Health 2013, 29(6):523-533. doi: 10.1177/0748233712442708 PMID: 22508397
43. Olmedo DG, Tasat DR, Evelson P, Guglielmotti MB, Cabrini RL: Biological response of tissues with macrophagic activity to titanium dioxide. J Biomed Mater Res A 2008, 84(4):1087-1093. PMID: 17685404
44. Buerki-Thurnherr T, Xiao L, Diener L, Arslan O, Hirsch C, Maeder-Althaus X, et al: In vitro mechanistic study towards a better understanding of ZnO nanoparticle toxicity. Nanotoxicology 2013, 7(4):402-416. doi: 10.3109/17435390.2012.666575 PMID: 22394310
45. Rasmussen JW, Martinez E, Louka P, Wingett DG: Zinc oxide nanoparticles for selective destruction of tumor cells and potential for drug delivery applications. Expert Opin Drug Deliv 2010, 7(9):1063-1077. doi: 10.1517/17425247.2010.502560 PMID: 20716019
46. Tuomela S, Autio R, Buerki-Thurnherr T, Arslan O, Kunzmann A, Andersson-Willman B, et al: Gene expression profiling of immune-competent human cells exposed to engineered zinc oxide or titanium dioxide nanoparticles. PLoS One 2013, 8(7):e68415. doi: 10.1371/journal.pone.0068415 PMID: 23894303
47. Yin H, Casey PS, McCall MJ, Fenech M: Effects of surface chemistry on cytotoxicity, genotoxicity, and the generation of reactive oxygen species induced by ZnO nanoparticles. Langmuir 2010, 26 (19):15399-15408. doi: 10.1021/la101033n PMID: 20809599
48. Napierska D, Thomassen LC, Lison D, Martens JA, Hoet PH: The nanosilica hazard: another variable entity. Part Fibre Toxicol 2010, 7(1):39. doi: 10.1186/1743-8977-7-39 PMID: 21126379
49. Shi J, Karlsson HL, Johansson K, Gogvadze V, Xiao L, Li J, et al: Microsomal glutathione transferase 1 protects against toxicity induced by silica nanoparticles but not by zinc oxide nanoparticles. ACS Nano 2012, 6(3):1925-1938. doi: 10.1021/nn2021056 PMID: 22303956
50. Cohen JM, Teeguarden JG, Demokritou P: An integrated approach for the in vitro dosimetry of engineered nanomaterials. Part Fibre Toxicol 2014, 11:20. doi: 10.1186/1743-8977-11-20 PMID: 24885440
51. Winkler DA, Mombelli E, Pietroiusti A, Tran L, Worth A, Fadeel B, McCall MJ: Applying quantitative structure-activity relationship approaches to nanotoxicology: current status and future potential. Toxicology 2013, 313(1):15-23. doi: 10.1016/j.tox.2012.11.005 PMID: 23165187
52. NANOGENOTOX - Final protocol for producing suitable manufactured nanomaterial exposure media (Standard Operation Procedure); 2011.
53. US Pharmacopeia: Chapter 161 - Transfusion and Infusion Assemblies and Similar Medical Devices; 2011.
54. FP7-NANOMMUNE Quality Handbook - Comprehensive asseeement of hazardous effects of engineered nanomaterials on the immune system. Standard procedures for nanoparticles testing; 2011.
55. Mather JP: Establishment and characterization of two distinct mouse testicular epithelial cell lines. Biol Reprod 1980, 23(1):243-252. PMID: 6774781
56. O'Brien J, Wilson I, Orton T, Pognan F: Investigation of the Alamar Blue (resazurin) fluorescent dye for the assessment of mammalian cell cytotoxicity. Eur J Biochem 2000, 267(17):5421-5426. PMID: 10951200
57. Repetto G, del Peso A, Zurita JL: Neutral red uptake assay for the estimation of cell viability/cytotoxicity. Nat Protoc 2008, 3(7):1125-1131. doi: 10.1038/nprot.2008.75 PMID: 18600217
58. Scholz G, Pohl I, Genschow E, Klemm M, Spielmann H: Embryotoxicity screening using embryonic stem cells in vitro: correlation to in vivo teratogenicity. Cells, tissues, organs 1999, 165(3-4):203-211. PMID: 10592392