Specific uptake and genotoxicity induced by polystyrene nanobeads with distinct surface chemistry on human lung epithelial cells and macrophages

PLoS ONE

Volumn 10, Issue 4, 2015, Pages

  Paget, Vincent ^a   Dekali, Samir ^a,b   Kortulewski, Thierry ^c   Grall, Romain ^c   Gamez, Christelle ^a   Blazy, Kelly ^a   Aguerre Chariol, Olivier ^a   Chevillard, Sylvie ^c   Braun, Anne ^a   Rat, Patrice ^b   Lacroix, Ghislaine ^a  

^a INSTITUT NATIONAL DE L ENVIRONNEMENT INDUSTRIEL ET DES RISQUES INERIS   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c INSTITUT DE RADIOBIOLOGIE CELLULAIRE ET MOLÉCULAIRE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTATHIONE; NANOBEAD; POLYSTYRENE; REACTIVE OXYGEN METABOLITE; H2AFX PROTEIN, HUMAN; HISTONE; NANOPARTICLE; OXAZINE DERIVATIVE; POLYSTYRENE DERIVATIVE; RESAZURIN; XANTHENE DERIVATIVE;

ARTICLE; CELL INTERACTION; CELL LINE; CELL TRANSPORT; CONTROLLED STUDY; CYTOPLASM; CYTOTOXICITY TEST; DOUBLE STRANDED DNA BREAK; GENOTOXICITY; HUMAN; HUMAN CELL; LUNG ALVEOLUS EPITHELIUM; MACROPHAGE; PARTICLE SIZE; PROTEIN DEPLETION; SURFACE PROPERTY; AGONISTS; AMINATION; CELL SURVIVAL; CHEMISTRY; CYTOLOGY; DNA DAMAGE; DRUG EFFECTS; EPITHELIUM CELL; GENETICS; METABOLISM; ULTRASTRUCTURE;

AMINATION; CELL LINE; CELL SURVIVAL; DNA BREAKS, DOUBLE-STRANDED; DNA DAMAGE; EPITHELIAL CELLS; GLUTATHIONE; HISTONES; HUMANS; MACROPHAGES; NANOPARTICLES; OXAZINES; PARTICLE SIZE; POLYSTYRENES; REACTIVE OXYGEN SPECIES; SURFACE PROPERTIES; XANTHENES;

EID: 84929501365     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0123297     Document Type: Article

References (64)

1. Gwinn MR, Vallyathan V. Nanoparticles: health effects - pros and cons. Environ Health Perspect 2006; 114: 1818-1825. PMID: 17185269
2. ISO (2008) Nanotechnologies - Terminology and definitions for nano-objects - Nanoparticle, nanofibre and nanoplate. ISO/TS 27687:2008.
3. Tetley TD. Health effects of nanomaterials. Biochem Soc Trans 2007; 35: 527-531. PMID: 17511644
4. Oberdorster G, Oberdorster E, Oberdorster J. Nanotoxicology: an emerging discipline evolving from studies of ultrafine particles. Environ Health Perspect 2005; 113: 823-839. PMID: 16002369
5. Zhao F, Zhao Y, Liu Y, Chang X, Chen C, Zhao Y. Cellular uptake, intracellular trafficking, and cytotoxicity of nanomaterials. Small 2011; 7: 1322-1337. doi: 10.1002/smll.201100001 PMID: 21520409
6. Zhu MT, Feng WY, Wang Y, Wang B, Wang M, Ouyang H, et al. Particokinetics and extrapulmonary translocation of intratracheally instilled ferric oxide nanoparticles in rats and the potential health risk assessment. Toxicol Sci 2009; 107: 342-351. doi: 10.1093/toxsci/kfn245 PMID: 19023088
7. Geiser M, Kreyling WG. Deposition and biokinetics of inhaled nanoparticles. Part Fibre Toxicol 2010; 7: 2. doi: 10.1186/1743-8977-7-2 PMID: 20205860
8. Klein SG, Hennen J, Serchi T, Blomeke B, Gutleb AC. Potential of coculture in vitro models to study inflammatory and sensitizing effects of particles on the lung. Toxicol In Vitro 2011; 25: 1516-1534. doi: 10.1016/j.tiv.2011.09.006 PMID: 21963807
9. Warheit DB, Reed KL, Sayes CM. A role for nanoparticle surface reactivity in facilitating pulmonary toxicity and development of a base set of hazard assays as a component of nanoparticle risk management. Inhal Toxicol 2009; 21 Suppl 1: 61-67. doi: 10.1080/08958370902942640 PMID: 19558235
10. Mukhopadhyay A, Grabinski C, Afrooz AR, Saleh NB, Hussain S. Effect of gold nanosphere surface chemistry on protein adsorption and cell uptake in vitro. Appl Biochem Biotechnol 2012; 167: 327-337. doi: 10.1007/s12010-012-9666-z PMID: 22547299
11. Lunov O, Syrovets T, Loos C, Beil J, Delacher M, Tron K, et al. Differential uptake of functionalized polystyrene nanoparticles by human macrophages and a monocytic cell line. ACS Nano 2011; 5: 1657-1669. doi: 10.1021/nn2000756 PMID: 21344890
12. Frohlich E, Samberger C, Kueznik T, Absenger M, Roblegg E, Zimmer A, et al. Cytotoxicity of nanoparticles independent from oxidative stress. J Toxicol Sci 2009; 34: 363-375. PMID: 19652459
13. Nel A, Xia T, Madler L, Li N. Toxic potential of materials at the nanolevel. Science 2006; 311: 622-627. PMID: 16456071
14. Shukla RK, Sharma V, Pandey AK, Singh S, Sultana S, Dhawan A. ROS-mediated genotoxicity induced by titanium dioxide nanoparticles in human epidermal cells. Toxicol In Vitro 2011; 25: 231-241. doi: 10.1016/j.tiv.2010.11.008 PMID: 21092754
15. Thubagere A, Reinhard BM. Nanoparticle-induced apoptosis propagates through hydrogen-peroxide-mediated bystander killing: insights from a human intestinal epithelium in vitro model. ACS Nano 2010; 4: 3611-3622. doi: 10.1021/nn100389a PMID: 20560658
16. Karlsson HL. The comet assay in nanotoxicology research. Anal Bioanal Chem 2010; 398: 651-666. doi: 10.1007/s00216-010-3977-0 PMID: 20640410
17. Singh N, Manshian B, Jenkins GJ, Griffiths SM, Williams PM, Maffeis TG, et al. NanoGenotoxicology: the DNA damaging potential of engineered nanomaterials. Biomaterials 2009; 30: 3891-3914. doi: 10.1016/j.biomaterials.2009.04.009 PMID: 19427031
18. Ahamed M, Karns M, Goodson M, Rowe J, Hussain SM, Schlager JJ, et al. DNA damage response to different surface chemistry of silver nanoparticles in mammalian cells. Toxicol Appl Pharmacol 2008; 233: 404-410. doi: 10.1016/j.taap.2008.09.015 PMID: 18930072
19. Lewis DJ, Bruce C, Bohic S, Cloetens P, Hammond SP, Arbon D, et al. Intracellular synchrotron nanoimaging and DNA damage/genotoxicity screening of novel lanthanide-coated nanovectors. Nanomedicine (Lond) 2010; 5: 1547-1557. doi: 10.2217/nnm.10.96 PMID: 20879836
20. Xie H, Mason MM, Wise JP Sr. Genotoxicity of metal nanoparticles. Rev Environ Health 2010; 26: 251-268.
21. Mah LJ, El-Osta A, Karagiannis TC. gammaH2AX: a sensitive molecular marker of DNA damage and repair. Leukemia 2010; 24: 679-686. doi: 10.1038/leu.2010.6 PMID: 20130602
22. Matthews JB, Green TR, Stone MH, Wroblewski BM, Fisher J, Ingham E. Comparison of the response of three human monocytic cell lines to challenge with polyethylene particles of known size and dose. Journal of Materials Science Materials in Medicine 2001; 12: 249-258. PMID: 15348309
23. Wottrich R, Diabate S, Krug HF. Biological effects of ultrafine model particles in human macrophages and epithelial cells in mono- and co-culture. International Journal of Hygiene and Environmental Health 2004; 207: 353-361. PMID: 15471099
24. Lanone S, Rogerieux F, Geys J, Dupont A, Maillot-Marechal E, Boczkowski J, et al. Comparative toxicity of 24 manufactured nanoparticles in human alveolar epithelial and macrophage cell lines. Part Fibre Toxicol 2009; 6: 14. doi: 10.1186/1743-8977-6-14 PMID: 19405955
25. Geys J, Coenegrachts L, Vercammen J, Engelborghs Y, Nemmar A, Nemery B, et al. In vitro study of the pulmonary translocation of nanoparticles: a preliminary study. Toxicol Lett 2006; 160: 218-226. PMID: 16137845
26. Geys J, Nemery B, Hoet PH. Optimisation of culture conditions to develop an in vitro pulmonary permeability model. Toxicol In Vitro 2007; 21: 1215-1219. PMID: 17629671
27. Lehmann AD, Daum N, Bur M, Lehr CM, Gehr P, Rothen-Rutishauser BM. An in vitro triple cell co-culture model with primary cells mimicking the human alveolar epithelial barrier. European Journal of Pharmaceutics & Biopharmaceutics 2011; 77: 398-406.
28. Stentebjerg-Andersen A, Notlevsen IV, Brodin B, Nielsen CU. Calu-3 cells grown under AIC and LCC conditions: implications for dipeptide uptake and transepithelial transport of substances. European Journal of Pharmaceutics & Biopharmaceutics 2011; 78: 19-26.
29. Paur HR, Cassee FR, Teeguardenc J, Fissand H, Diabatee S, Aufderheidef M, et al. In-vitro cell exposure studies for the assessment of nanoparticle toxicity in the lung-A dialog between aerosol science and biology. Journal of Aerosol Science 2011; 42: 668-692.
30. Kamencic H, Lyon A, Paterson PG, Juurlink BH. Monochlorobimane fluorometric method to measure tissue glutathione. Anal Biochem 2000; 286: 35-37. PMID: 11038270
31. Redon CE, Nakamura AJ, Martin OA, Parekh PR, Weyemi US, Bonner WM. Recent developments in the use of gamma-H2AX as a quantitative DNA double-strand break biomarker. Aging (Albany NY) 2011; 3: 168-174. PMID: 21325706
32. Tsamou M, Jennen DG, Claessen SM, Magkoufopoulou C, Kleinjans JC, van Delft JH. Performance of in vitro gammaH2AX assay in HepG2 cells to predict in vivo genotoxicity. Mutagenesis 2012; 27: 645-652. doi: 10.1093/mutage/ges030 PMID: 22914676
33. Ruenraroengsak P, Novak P, Berhanu D, Thorley AJ, Valsami-Jones E, Gorelik J, et al. Respiratory epithelial cytotoxicity and membrane damage (holes) caused by amine-modified nanoparticles. Nanotoxicology 2012; 6: 94-108. doi: 10.3109/17435390.2011.558643 PMID: 21352086
34. Wang XZ, Yang Y, Li RF, McGuinnes C, Adamson J, Megson IL, et al. Principal Component and Causal Analysis of Structural and Acute in vitro Toxicity Data for Nanoparticles. Nanotoxicology 2014; 8: 465-476. doi: 10.3109/17435390.2013.796534 PMID: 23586395
35. Dekali S, Divetain A, Kortulewski T, Vanbaelinghem J, Gamez C, Rogerieux F, et al. Cell cooperation and role of the P2X7 receptor in pulmonary inflammation induced by nanoparticles. Nanotoxicology 2013; 7: 1302-1314. doi: 10.3109/17435390.2012.735269 PMID: 23020093
36. Holder AL, Goth-Goldstein R, Lucas D, Koshland CP. Particle-Induced Artifacts in the MTT and LDH Viability Assays. Chem Res Toxicol 2010; 25: 1885-1892.
37. Kroll A, Pillukat MH, Hahn D, Schnekenburger J. Interference of engineered nanoparticles with in vitro toxicity assays. Arch Toxicol 2012; 86: 1123-1136. doi: 10.1007/s00204-012-0837-z PMID: 22407301
38. Stone V, Johnston H, Schins RP. Development of in vitro systems for nanotoxicology: methodological considerations. Crit Rev Toxicol 2009; 39: 613-626. doi: 10.1080/10408440903120975 PMID: 19650720
39. Zaqout MS, Sumizawa T, Igisu H, Wilson D, Myojo T, Ueno S. Binding of titanium dioxide nanoparticles to lactate dehydrogenase. Environ Health Prev Med 2012; 17: 341-345. doi: 10.1007/s12199-011-0245-7 PMID: 21993949
40. Ong KJ, MacCormack TJ, Clark RJ, Ede JD, Ortega VA, Felix LC, et al. Widespread nanoparticleassay interference: implications for nanotoxicity testing. PLoS One 2014; 9: e90650. doi: 10.1371/journal.pone.0090650 PMID: 24618833
41. Kawata K, Osawa M, Okabe S. In vitro toxicity of silver nanoparticles at noncytotoxic doses to HepG2 human hepatoma cells. Environ Sci Technol 2009; 43: 6046-6051. PMID: 19731716
42. Frohlich E, Bonstingl G, Hofler A, Meindl C, Leitinger G, Pieber TR, et al. Comparison of two in vitro systems to assess cellular effects of nanoparticles-containing aerosols. Toxicol In Vitro 2012; 27: 409-417. doi: 10.1016/j.tiv.2012.08.008 PMID: 22906573
43. Frohlich E, Meindl C, Roblegg E, Griesbacher A, Pieber TR. Cytotoxity of nanoparticles is influenced by size, proliferation and embryonic origin of the cells used for testing. Nanotoxicology 2012; 6: 424-439. doi: 10.3109/17435390.2011.586478 PMID: 21627401
44. Kim JA, Aberg C, de Carcer G, Malumbres M, Salvati A, Dawson KA. Low dose of amino-modified nanoparticles induces cell cycle arrest. ACS Nano 2013; 7: 7483-7494. doi: 10.1021/nn403126e PMID: 23941353
45. Wang F, Bexiga MG, Anguissola S, Boya P, Simpson JC, Salvati A, et al. Time resolved study of cell death mechanisms induced by amine-modified polystyrene nanoparticles. Nanoscale 2013; 5: 10868-10876. doi: 10.1039/c3nr03249c PMID: 24108393
46. Anguissola S, Garry D, Salvati A, O'Brien PJ, Dawson KA. High Content Analysis Provides Mechanistic Insights on the Pathways of Toxicity Induced by Amine-Modified Polystyrene Nanoparticles. PLoS One 2014; 9: e108025. doi: 10.1371/journal.pone.0108025 PMID: 25238162
47. Xia T, Kovochich M, Brant J, Hotze M, Sempf J, Oberley T, et al. Comparison of the abilities of ambient and manufactured nanoparticles to induce cellular toxicity according to an oxidative stress paradigm. Nano Lett 2006; 6: 1794-1807. PMID: 16895376
48. Bhattacharjee S, de Haan LH, Evers NM, Jiang X, Marcelis AT, Zuilhof H, et al. Role of surface charge and oxidative stress in cytotoxicity of organic monolayer-coated silicon nanoparticles towards macrophage NR8383 cells. Part Fibre Toxicol 2010; 7: 25. doi: 10.1186/1743-8977-7-25 PMID: 20831820
49. Bhabra G, Sood A, Fisher B, Cartwright L, Saunders M, Evans WH, et al. Nanoparticles can cause DNA damage across a cellular barrier. Nat Nanotechnol 2009; 4: 876-883. doi: 10.1038/nnano.2009.313 PMID: 19893513
50. McCarthy J, Gong X, Nahirney D, Duszyk M, Radomski M. Polystyrene nanoparticles activate ion transport in human airway epithelial cells. Int J Nanomedicine 2011; 6: 1343-1356. doi: 10.2147/IJN.S21145 PMID: 21760729
51. Lunov O, Syrovets T, Loos C, Nienhaus GU, Mailander V, Landfester K, et al. Amino-functionalized polystyrene nanoparticles activate the NLRP3 inflammasome in human macrophages. ACS Nano 2011; 5: 9648-9657. doi: 10.1021/nn203596e PMID: 22111911
52. Zucker RM, Massaro EJ, Sanders KM, Degn LL, Boyes WK. Detection of TiO2 nanoparticles in cells by flow cytometry. Cytometry A 2010; 77: 677-685. doi: 10.1002/cyto.a.20927 PMID: 20564539
53. Park EJ, Yi J, Chung KH, Ryu DY, Choi J, Park K. Oxidative stress and apoptosis induced by titanium dioxide nanoparticles in cultured BEAS-2B cells. Toxicol Lett 2008; 180: 222-229. doi: 10.1016/j.toxlet.2008.06.869 PMID: 18662754
54. Donaldson K, Poland CA, Schins RP. Possible genotoxic mechanisms of nanoparticles: criteria for improved test strategies. Nanotoxicology 2010; 4: 414-420. doi: 10.3109/17435390.2010.482751 PMID: 20925449
55. Donaldson K, Poland CA. Inhaled nanoparticles and lung cancer-what we can learn from conventional particle toxicology. Swiss Med Wkly 2012; 142: w13547. doi: 10.4414/smw.2012.13547 PMID: 22714122
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: 5421-5426. PMID: 10951200
57. Perrot S, Dutertre-Catella H, Martin C, Rat P, Warnet JM. Resazurin metabolism assay is a new sensitive alternative test in isolated pig cornea. Toxicol Sci 2003; 72: 122-129. PMID: 12604841
58. Perrot S, Dutertre-Catella H, Martin C, Warnet JM, Rat P. A new nondestructive cytometric assay based on resazurin metabolism and an organ culture model for the assessment of corneal viability. Cytometry A 2003; 55: 7-14. PMID: 12938183
59. Paget V, Sergent JA, Grall R, Altmeyer-Morel S, Girard HA, Petit T, et al. Carboxylated nanodiamonds are neither cytotoxic nor genotoxic on liver, kidney, intestine and lung human cell lines. Nanotoxicology 2014; 8 Suppl 1: 46-56. doi: 10.3109/17435390.2013.855828 PMID: 24266793
60. Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods 2012; 9: 671-675. PMID: 22930834
61. Carpenter AE, Jones TR, Lamprecht MR, Clarke C, Kang IH, Friman O, et al. CellProfiler: image analysis software for identifying and quantifying cell phenotypes. Genome Biol 2006; 7: R100. PMID: 17076895
62. Osseni RA, Debbasch C, Christen MO, Rat P, Warnet JM. Tacrine-induced Reactive Oxygen Species in a Human Liver Cell Line: The Role of Anethole Dithiolethione as a Scavenger. Toxicol In Vitro 1999; 13: 683-688. PMID: 20654534
63. Debbasch C, Pisella PJ, De Saint Jean M, Rat P, Warnet JM, Baudouin C. Mitochondrial activity and glutathione injury in apoptosis induced by unpreserved and preserved beta-blockers on Chang conjunctival cells. Invest Ophthalmol Vis Sci 2001; 42: 2525-2533. PMID: 11581193
64. Team RDC. R: A language and environment for statistical computing. 2005.