Predictive value of in vitro assays depends on the mechanism of toxicity of metal oxide nanoparticles

Particle and Fibre Toxicology

Volumn 10, Issue 1, 2013, Pages

  Cho, Wan Seob ^a,b   Duffin, Rodger ^a   Bradley, Mark ^a   Megson, Ian L ^c   MacNee, William ^a   Lee, Jong K ^d   Jeong, Jayoung ^d   Donaldson, Ken ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b Dong A University   (South Korea)

^c UNIVERSITY OF THE HIGHLANDS AND ISLANDS   (United Kingdom)

^d National Institute of Food and Drug Safety Evaluation   (South Korea)

Author keywords

In vitro; In vivo; Inflammation; Mechanism; Nanoparticles; Prediction; Toxicity

Indexed keywords

BLACK CARBON; CERIUM OXIDE; CHROMIC OXIDE; COBALT OXIDE; COPPER OXIDE; CYTOKINE; INTERLEUKIN 1BETA; INTERLEUKIN 8; METAL OXIDE; METAL OXIDE NANOPARTICLE; NANOPARTICLE; NITRIC OXIDE; SILICON DIOXIDE; TITANIUM DIOXIDE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; ZINC OXIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ASSAY; CHEMICAL REACTION; CONTROLLED STUDY; CYTOTOXICITY; EPITHELIUM CELL; ERYTHROCYTE; FEMALE; HUMAN; HUMAN CELL; IN VITRO CELL ASSAY; IN VITRO STUDY; IN VIVO STUDY; MACROPHAGE; MONOCYTE; NONHUMAN; PNEUMONIA; PREDICTIVE VALUE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SOLUBILITY; WISTAR RAT;

ANIMALIA; RATTUS;

ANIMALS; CELL DIFFERENTIATION; CELL LINE; CULTURE MEDIA, CONDITIONED; HUMANS; MACROPHAGES; METAL NANOPARTICLES; OXIDES; RATS;

EID: 84886228257     PISSN: None     EISSN: 17438977     Source Type: Journal    
DOI: 10.1186/1743-8977-10-55     Document Type: Article

References (38)

1. Nel AE, Madler L, Velegol D, Xia T, Hoek EM, Somasundaran P, Klaessig F, Castranova V, Thompson M. Understanding biophysicochemical interactions at the nano-bio interface. Nat Mater 2009, 8:543-557. 10.1038/nmat2442, 19525947.
2. Borm PJ, Robbins D, Haubold S, Kuhlbusch T, Fissan H, Donaldson K, Schins R, Stone V, Kreyling W, Lademann J, et al. The potential risks of nanomaterials: a review carried out for ECETOC. Part Fibre Toxicol 2006, 3:11. 10.1186/1743-8977-3-11, 1584248, 16907977.
3. Organisation for Economic Co-operation and Development Nanosafety at the OECD: the first five years 2006-2010 2011, Paris: OECD, Organisation for Economic Co-operation and Development.
4. Organisation for Economic Co-operation and Development Six years of OECD work on the safety of manufactured nanomaterials: achievements and future opportunities 2013, Paris: OECD, Organisation for Economic Co-operation and Development.
5. Donaldson K, Borm PJ, Castranova V, Gulumian M. The limits of testing particle-mediated oxidative stress in vitro in predicting diverse pathologies; relevance for testing of nanoparticles. Part Fibre Toxicol 2009, 6:13. 10.1186/1743-8977-6-13, 2685764, 19397808.
6. Alfaro-Moreno E, Nawrot TS, Vanaudenaerde BM, Hoylaerts MF, Vanoirbeek JA, Nemery B, Hoet PH. Co-cultures of multiple cell types mimic pulmonary cell communication in response to urban PM10. Eur Respir J 2008, 32:1184-1194. 10.1183/09031936.00044008, 18653652.
7. Park EK, Jung HS, Yang HI, Yoo MC, Kim C, Kim KS. Optimized THP-1 differentiation is required for the detection of responses to weak stimuli. Inflamm Res 2007, 56:45-50. 10.1007/s00011-007-6115-5, 17334670.
8. Sohaebuddin SK, Thevenot PT, Baker D, Eaton JW, Tang L. Nanomaterial cytotoxicity is composition, size, and cell type dependent. Part Fibre Toxicol 2010, 7:22. 10.1186/1743-8977-7-22, 2936333, 20727197.
9. Kroll A, Dierker C, Rommel C, Hahn D, Wohlleben W, Schulze-Isfort C, Gobbert C, Voetz M, Hardinghaus F, Schnekenburger J. Cytotoxicity screening of 23 engineered nanomaterials using a test matrix of ten cell lines and three different assays. Part Fibre Toxicol 2011, 8:9. 10.1186/1743-8977-8-9, 3059267, 21345205.
10. Sayes CM, Reed KL, Warheit DB. Assessing toxicity of fine and nanoparticles: comparing in vitro measurements to in vivo pulmonary toxicity profiles. Toxicol Sci 2007, 97:163-180. 10.1093/toxsci/kfm018, 17301066.
11. Editorial The dose makes the poison. Nat Nanotechnol 2011, 6:329. Editorial.
12. Duffin R, Tran L, Brown D, Stone V, Donaldson K. Proinflammogenic effects of low-toxicity and metal nanoparticles in vivo and in vitro: highlighting the role of particle surface area and surface reactivity. Inhal Toxicol 2007, 19:849-856. 10.1080/08958370701479323, 17687716.
13. Fubini B, Ghiazza M, Fenoglio I. Physico-chemical features of engineered nanoparticles relevant to their toxicity. Nanotoxicology 2010, 4:347-363. 10.3109/17435390.2010.509519, 20858045.
14. Oberdorster G, Maynard A, Donaldson K, Castranova V, Fitzpatrick J, Ausman K, Carter J, Karn B, Kreyling W, Lai D, et al. Principles for characterizing the potential human health effects from exposure to nanomaterials: elements of a screening strategy. Part Fibre Toxicol 2005, 2:8. 10.1186/1743-8977-2-8, 1260029, 16209704.
15. Johnston HJ, Hutchison G, Christensen FM, Peters S, Hankin S, Stone V. A review of the in vivo and in vitro toxicity of silver and gold particulates: particle attributes and biological mechanisms responsible for the observed toxicity. Crit Rev Toxicol 2010, 40:328-346. 10.3109/10408440903453074, 20128631.
16. Cho WS, Duffin R, Poland CA, Howie SE, MacNee W, Bradley M, Megson IL, Donaldson K. Metal oxide nanoparticles induce unique inflammatory footprints in the lung: important implications for nanoparticle testing. Environ Health Perspect 2010, 118:1699-1706. 10.1289/ehp.1002201, 3002189, 20729176.
17. Cho WS, Duffin R, Bradley M, Megson IL, MacNee W, Howie SEM, Donaldson K. NiO and Co3O4 nanoparticles induce lung DTH-like responses and alveolar lipoproteinosis. Eur Respir J 2012, 39:546-557. 10.1183/09031936.00047111, 21828028.
18. Cho WS, Duffin R, Poland CA, Duschl A, Oostingh GJ, Macnee W, Bradley M, Megson IL, Donaldson K. 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 2012, 6:22-35. 10.3109/17435390.2011.552810, 21332300.
19. Bian SW, Mudunkotuwa IA, Rupasinghe T, Grassian VH. Aggregation and dissolution of 4 nm ZnO nanoparticles in aqueous environments: influence of pH, ionic strength, size, and adsorption of humic acid. Langmuir 2011, 27:6059-6068. 10.1021/la200570n, 21500814.
20. Studer AM, Limbach LK, Van Duc L, Krumeich F, Athanassiou EK, Gerber LC, Moch H, Stark WJ. Nanoparticle cytotoxicity depends on intracellular solubility: comparison of stabilized copper metal and degradable copper oxide nanoparticles. Toxicol Lett 2010, 197:169-174. 10.1016/j.toxlet.2010.05.012, 20621582.
21. Yazdi AS, Guarda G, Riteau N, Drexler SK, Tardivel A, Couillin I, Tschopp J. Nanoparticles activate the NLR pyrin domain containing 3 (Nlrp3) inflammasome and cause pulmonary inflammation through release of IL-1alpha and IL-1beta. Proc Natl Acad Sci USA 2010, 107:19449-19454. 10.1073/pnas.1008155107, 2984140, 20974980.
22. Hornung V, Bauernfeind F, Halle A, Samstad EO, Kono H, Rock KL, Fitzgerald KA, Latz E. Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nat Immunol 2008, 9:847-856. 10.1038/ni.1631, 2834784, 18604214.
23. Totlandsdal AI, Refsnes M, Skomedal T, Osnes JB, Schwarze PE, Lag M. Particle-induced cytokine responses in cardiac cell cultures-the effect of particles versus soluble mediators released by particle-exposed lung cells. Toxicol Sci 2008, 106:233-241. 10.1093/toxsci/kfn162, 18700232.
24. Shaw CA, Robertson S, Miller MR, Duffin R, Tabor CM, Donaldson K, Newby DE, Hadoke PW. Diesel exhaust particulate-exposed macrophages cause marked endothelial cell activation. Am J Respir Cell Mol Biol 2010, 44:840-851.
25. Jimenez LA, Drost EM, Gilmour PS, Rahman I, Antonicelli F, Ritchie H, MacNee W, Donaldson K. PM(10)-exposed macrophages stimulate a proinflammatory response in lung epithelial cells via TNF-alpha. Am J Physiol Lung Cell Mol Physiol 2002, 282:L237-L248.
26. Cho WS, Duffin R, Thielbeer F, Bradley M, Megson IL, Macnee W, Poland CA, Tran CL, Donaldson K. Zeta potential and solubility to toxic ions as mechanisms of lung inflammation caused by metal/metal oxide nanoparticles. Toxicol Sci 2012, 126:469-477. 10.1093/toxsci/kfs006, 22240982.
27. Donaldson K, Schinwald A, Murphy F, Cho WS, Duffin R, Tran L, Poland C. The biologically effective dose in inhalation nanotoxicology. Acc Chem Res 2013, 46(3):723-732. 10.1021/ar300092y, 23003923.
28. Thielbeer F, Donaldson K, Bradley M, Johansson EM, Cho WS, Duffin R, Megson IL, Macnee W. Surface functionalization affects the zeta potential, coronal stability and membranolytic activity of polymeric nanoparticles. Nanotoxicology in press.
29. Lu S, Duffin R, Poland C, Daly P, Murphy F, Drost E, Macnee W, Stone V, Donaldson K. Efficacy of simple short-term in vitro assays for predicting the potential of metal oxide nanoparticles to cause pulmonary inflammation. Environ Health Perspect 2009, 117:241-247. 2649226, 19270794.
30. Casals E, Puntes VF. Inorganic nanoparticle biomolecular corona: formation, evolution and biological impact. Nanomedicine (Lond) 2012, 7(12):1917-1930. 10.2217/nnm.12.169, 23249335.
31. Maiorano G, Sabella S, Sorce B, Brunetti V, Malvindi MA, Cingolani R, Pompa PP. Effects of cell culture media on the dynamic formation of protein-nanoparticle complexes and influence on the cellular response. ACS Nano 2010, 4(12):7481-7491. 10.1021/nn101557e, 21082814.
32. Macickova T, Navarova J, Urbancikova M, Horakova K. Comparison of isoproterenol-induced changes in lysosomal enzyme activity in vivo and in vitro. Gen Physiol Biophys 1999, 18 Spec No:86-91.
33. Horie M, Nishio K, Fujita K, Kato H, Nakamura A, Kinugasa S, Endoh S, Miyauchi A, Yamamoto K, Murayama H, et al. Ultrafine NiO particles induce cytotoxicity in vitro by cellular uptake and subsequent Ni(II) release. Chem Res Toxicol 2009, 22:1415-1426. 10.1021/tx900171n, 19630433.
34. Ogami A, Morimoto Y, Myojo T, Oyabu T, Murakami M, Todoroki M, Nishi K, Kadoya C, Yamamoto M, Tanaka I. Pathological features of different sizes of nickel oxide following intratracheal instillation in rats. Inhal Toxicol 2009, 21:812-818. 10.1080/08958370802499022, 19225964.
35. Cozens AL, Yezzi MJ, Kunzelmann K, Ohrui T, Chin L, Eng K, Finkbeiner WE, Widdicombe JH, Gruenert DC. CFTR expression and chloride secretion in polarized immortal human bronchial epithelial cells. Am J Respir Cell Mol Biol 1994, 10(1):38-47. 10.1165/ajrcmb.10.1.7507342, 7507342.
36. Dransfield I, Buckle AM, Savill JS, McDowall A, Haslett C, Hogg N. Neutrophil apoptosis is associated with a reduction in CD16 (Fc gamma RIII) expression. J Immunol 1994, 153:1254-1263.
37. Kroll A, Pillukat MH, Hahn D, Schnekenburger J. Current in vitro methods in nanoparticle risk assessment: limitations and challenges. Eur J Pharm Biopharm 2009, 72:370-377. 10.1016/j.ejpb.2008.08.009, 18775492.
38. Monteiller C, Tran L, MacNee W, Faux S, Jones A, Miller B, Donaldson K. The pro-inflammatory effects of low-toxicity low-solubility particles, nanoparticles and fine particles, on epithelial cells in vitro: the role of surface area. Occup Environ Med 2007, 64:609-615. 10.1136/oem.2005.024802, 2092561, 17409182.