Dynamic monitoring of metal oxide nanoparticle toxicity by label free impedance sensing

Chemical Research in Toxicology

Volumn 25, Issue 1, 2012, Pages 140-152

  Seiffert, Joanna M ^a   Baradez, Marc Olivier ^a   Nischwitz, Volker ^a   Lekishvili, Tamara ^a   Goenaga Infante, Heidi ^a   Marshall, Damian ^a  

^a LGC   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

COPPER OXIDE; GLUTATHIONE; METAL OXIDE; NANOPARTICLE; REACTIVE OXYGEN METABOLITE; TITANIUM DIOXIDE; ZINC OXIDE;

APOPTOSIS; ARTICLE; CELL LOSS; CELL MEMBRANE; CELL STRUCTURE; CYTOTOXICITY; ELECTROCHEMICAL IMPEDANCE SPECTROSCOPY; EXPOSURE; HUMAN; HUMAN CELL; IC 50; IMAGE ANALYSIS; IMPEDANCE; SPECTROSCOPY; TOXICITY TESTING;

CELL LINE, TUMOR; CELL SURVIVAL; COPPER; ELECTRIC IMPEDANCE; GLUTATHIONE; HUMANS; METAL NANOPARTICLES; REACTIVE OXYGEN SPECIES; TITANIUM; ZINC OXIDE;

EID: 84855822969     PISSN: 0893228X     EISSN: 15205010     Source Type: Journal    
DOI: 10.1021/tx200355m     Document Type: Article

References (63)

1. Maynard, A. and Michelson, E. (2011) The Nanotechnology Consumer Products Inventory, Project on Emerging Nanotechnologies, Woodrow Wilson International Centre for Scholars, Washington, D.C., http://nanotechproject.org/44>
2. Lee, C. J., Lee, T. J., Lyu, S. C., Zhang, Y., Ruh, H., and Lee, H. (2002) Field emission from well-aligned zinc oxide nanowires grown at low temperature J. Appl. Phys. Lett. 81, 3648-3650
3. Xu, C. X., Sun, X. W., Chen, B. J., Shum, P., Li, S., and Hu, X. (2004) Nanostructural zinc oxide and its electrical and optical properties J. Appl. Phys. 95, 661-666
4. Park, B. (2007) Current and Future Applications of Nanotechnology, in Nanotechnology: Consequences for Human Health and the Environment (Hester, R. E. and Harrison, R. M., Eds.) Royal Society of Chemistry Publishing, London, U.K.
5. Kreyling, W. G., Semmler, M., Erbe, F., Mayer, P., Takenaka, S, Schulz, H., Oberdorster, G., and Ziesenis, A. (2002) Translocation of ultrafine insoluble iridium particles from lung epithelium to extrapulmonary organs is size dependent but very low J. Toxicol. Environ. Health A. 65, 1513-1530 (Pubitemid 35217498)
6. Fenart, L., Casanova, A, Dehouck, B., Duhen, C, Slupek, Cecchelli, R., and Betbeder, D. (1999) Evaluation of effect of charge and lipid coating on ability of 60-nm nanoparticles to cross an in vitro model of the blood-brain barrier J. Pharmacol. Exp. Ther. 291, 1017-1022
7. De Jong, W. H., Hagens, W. I., Krystek, P., Burger, M. C., Sips, A. J., Geertsma, R. E., and Particle (2008) size-dependent organ distribution of gold nanoparticles after intravenous administration Biomaterial 12, 1912-1919
8. Wick, P., Malek, A., Manser, P., Meili, D., Maeder-Althaus, X., Diener, L., Diener, P-A, Zisch, A, Krug, H. F., and von Mandach, U. (2010) Barrier capacity of human placenta for nanosized materials Environ. Health Perspect. 118, 432-436
9. Duffin, R., Tran, L., Brown, D., Stone, V., and Donaldson, K. (2007) Pro-inflammogenic effects of low-toxicity and metal nanoparticles in vivo and in vitro: highlighting the role of particle surface area and surface reactivity Inhal. Toxicol. 10, 849-56 (Pubitemid 47237750)
10. Montellier, C., Tran, L., MacNee, W., Faux, S., Jones, A., Miller, B., and Donaldson, K. (2007) 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. 9, 609-15 (Pubitemid 47345256)
11. Poland, C. A., Duffin, R., Kinloch, I., Maynard, A., Wallace, W. A., Seaton, A., Stone, V., Brown, S., Macnee, W., and Donaldson, K. (2008) Carbon nanotubes introduced into the abdominal cavity of mice show asbestos like pathogenicity in a pilot study Nat. Nanotechnol. 3, 423-428
12. Jiang, J., Oberdörster, G., Elder, A., Gelein, R., Pamela Mercer, P., and Biswas, P. (2008) Does nanoparticle activity depend upon size and crystal phase? Nanotoxicol. 2 (1) 33-42
13. Ayres, J. G., Borm, P., Cassee, F. R., Castranova, V., Donaldson, K., Ghio, A., Harrison, R. M., Hider, R., Kelly, F. J., Ingeborg M. Kooter, I. M., Marano, F., Maynard, R. L., Mudway, I. S., Nel, A., Sioutas, C., Smith, S., Baeza-Squiban, A., Cho, A., Duggan, S., and Froines, J. (2008) Evaluating the toxicity of airborne particulate matter and nanoparticles by measuring oxidative stress potential: a workshop report and consensus statement Inhal. Toxicol. 20 (1) 75-99 (Pubitemid 351194921)
14. Limbach, L., Li, Y., Grass, R., Brunner, T., Hinterman, M., Muller, M., Gunther, D, and Stark, W. (2005) Oxide nanoparticle uptake in human lung fibroblasts: effect on particle size, agglomeration, and diffusion at low concentrations Environ. Sci. Technol. 39 (23) 9370-9376 (Pubitemid 41741229)
15. Xia, T., Kovochich, M., Liong, M., Madler, L., Gilbert, B., Shi, H., Yeh, J. I., Zink, J. I., and Nel, A. E. (2008) Comparison of the mechanism of toxicity of zinc oxide and cerium oxide nanoparticles based on dissolution and oxidative stress properties ACS Nano 2, 2121-2134
16. Limbach, L,K, Wick, P., Manser, P., Grass, R. N., Bruinink, A., and Stark, W. J. (2007) Exposure of engineered nanoparticles to human lung epithelial cells: influence of chemical composition and catalytic activity on oxidative stress Environ. Sci. Technol. 41 (11) 4158-4163 (Pubitemid 46903235)
17. Cho, W-S, Duffin, R., Poland, C. A., Howie, S. E. M., MacNee, W., Bradley, M., Megson, I. L., and Donaldson, K. (2010) Metal oxide nanoparticles induce unique inflammatory footprints in the lung: important implications for nanoparticle testing Environ. Health Perspect. 118, 1699-1706
18. Teeguarden, J. G., Hinderliter, P. M., Orr, G., Thrall, B. D., and Pounds, J. G. (2007) Particokinetics in vitro: dosimetry considerations for in vitro nanoparticle toxicology assessments Toxicol. Sci. 95, 300-312 (Pubitemid 46152602)
19. Wörle-Knirsch, J., Pulskamp, K., and Krug, H. (2006) Oops they did it again! Carbon nanotubes hoax scientists in viability assays Nano Lett. 6 (6) 1261-1268 (Pubitemid 44013492)
20. Monteiro-Riviere, N. A., Inman, A. O., and Zhang, L. W. (2009) Limitations and relative utility of screening assays to assess engineered nanoparticle toxicity in a human cell line Toxicol. App. Pharmacol. 234 (2) 222-235
21. Alvarez, P. J., Colvin, V., Lead, J., and Stone, V. (2009) Research priorities to advance eco-responsible nanotechnology ACS Nano 3 (7) 1616-1619
22. Xing, J. Z., Zhu, L., Jackson, J. A., Gabos, S., Sun, X. J., Wang, X. B., and Xu, X. (2005) Dynamic monitoring of cytotoxicity on microelectronic sensors Chem. Res. Toxicol. 2, 154-161 (Pubitemid 40256233)
23. Huang, L., Xie, L., Boyd, J. M., and Li, X.-F. (2008) Cell-electronic sensing of particle-induced cellular responses Analyst 133, 643-648 (Pubitemid 351572820)
24. Solly, K., Wang, X., Xu, X., Strulovici, B., and Zheng, W. (2004) Application of real-time cell electronic sensing (RT-CES) technology to cell-based assays Assay Drug Dev. Technol. 2, 363-372 (Pubitemid 39276278)
25. Wegener, J., Keese, C. R., and Giaever, I. (2000) Electric cell-substrate impedance sensing (ECIS) as a noninvasive means to monitor the kinetics of cell spreading to artificial surfaces Exp. Cell Res. 259, 158-166
26. Yu, N, Atienza, J., Bernard, J., Blanc, S., Zhu, J., Wang, X, Xu, X., and Abassi, Y. (2006) Real-time monitoring of morphological changes in living cells by electronic cell sensor arrays: an approach to study G protein- coupled receptors Anal. Chem. 78 (1) 35-43 (Pubitemid 43050137)
27. Fang, Y., Frutos, A. G., and Verklereen, V. (2008) Label-free cell-based assays for GPCR screening. Combinat. Chem High Throughput Screen. 11, 357-369 (Pubitemid 351830306)
28. Wang, X., Becker, F. F., and Gascoyne, P. R. C. (2002) Membrane dielectric changes indicate induced apoptosis in HL-60 cells more sensitively than surface phosphatidylserine expression or DNA fragmentation Biochim. Biophys. Acta 1564 (2) 412-420
29. Arndt, S., Seebach, J., Psathaki, K., Galla, H.-J., and Wegener, J. (2004) Bioelectrical impedance assay to monitor changes in cell shape during apoptosis Biosensor. Bioelectronic. 19, 583-594 (Pubitemid 37542351)
30. Karlsson, H. L., Cronholm, P., Gustafsson, J., and Möller, L. (2009) Copper oxide nanoparticles are highly toxic: a comparison between metal oxide nanoparticles and carbon nanotubes Chem. Res. Toxicol. 21, 1726-1732
31. Cho, Wan-Seob, Duffin, R., Poland, C. A., Duschl, A., Oostingh, G. J., Macnee, M., Megson, I. L., and Donnaldson, K. (2011) 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 Nanotoxicol. 10.3109/17435390.2011.552810
32. Oberdörster, G., Maynard, A., Donaldson, K., Castranova, V., Fitzpatrick, J., Kevin Ausman, K., Carter, J., Karn, B., Kreyling, W., Lai, D., Olin, S., Monteiro-Riviere, N., Warheit, D., and Yang, H. (2005) Principles for characterizing the potential human health effects from exposure to nanomaterials: elements of a screening strategy Particle Fibre Toxicol. 2, 8
33. Nel, A., Xia, T., and Mädler, L. (2006) Toxic potential of materials at the Nanolevel Science 311 (5761) 622-627 (Pubitemid 43191298)
34. Kroll, A., Pillukat, M. H., Hahn, D., and Schnekenburger, J. (2009) Current in vitro methods in nanoparticle risk assessment: Limitations and challenges Eur. J. Pharm. Biopharm. 72 (2) 370-377
35. Male, K. B., Lachance, M., Hrapoviv, B., Sunahara., S., and Luong, J. H. T. (2008) Assessment of cytotoxicity of quantum dots and gold nanoparticles using cell-based impedance spectroscopy Anal. Chem. 80, 5487-5493
36. Wu, C., Shi, L., Li, Q., and Jiang, H. (2010) Probing the dynamic effect of cys-CdTe quantum dots toward cancer cells in vitro Chem. Res. Toxicol. 23, 82-88
37. Abassi, Y. A., Biao, B., Zhang, W., Ye, P., Kirstein, S. L., Gaylord, M. R., Feinstein, S. C., Wang, X., and Xu, X. (2009) Kinetic cell-based morphological screening: prediction of mechanism of compound action and off-target effects Chem Biol. 16 (7) 712-723
38. Bhaskar, L., Krishnan, V., and Thampan, R. (2007) Cytoskeletal elements and intracellular transport J. Cell. Biochem. 101 (5) 1097-1108 (Pubitemid 47253713)
39. Maeno, E., Ishizaki, Y., Toku Kanaseki, T., Akihiro Hazama, A., and Yasunobu Okada, Y. (2000) Normotonic cell shrinkage because of disordered volume regulation is an early prerequisite to apoptosis Proc. Natl. Acad. Sci. U.S.A. 97 (17) 9487-9492 (Pubitemid 30650802)
40. Jeng, H. A. and Swanson, J. (2006) Toxicity of metal oxide nanoparticles in mammalian cells J. Environ. Sci. Health, Part A 41 (12) 2699-2711
41. Stone, V. and Donaldson, K. (2006) Nanotoxicology: Signs of stress Nat. Nanotechnol. 1, 23-24
42. Stohs, S. J. and Bagchi, D. (1995) Oxidative mechanisms in the toxicity of metal ions Free Radical Biol. Med. 18 (2) 321-336
43. Bishop, G. M., Dringen, R., and Robinson, S. R. (2007) Zinc stimulates the production of toxic reactive oxygen species (ROS) and inhibits glutathione reductase in astrocytes Free Radical Biol. Med. 42, 1222-1230 (Pubitemid 46428515)
44. Singh, A, Misra, V, Thimmulappa, R. K., Lee, H, Ames, S, Hoque, M. O., Herman, J. G., Baylin, S. B., Sidransky, D, Gabrielson, E, Brock, M. V., and Biswal, S. (2006) Dysfunctional KEAP1-NRF2 interaction in non-small-cell lung cancer PLoS Med. 3 (10) e420
45. Marchan, R., Hammond, C. L., and Ballatori, N. (2008) Multidrug resistance-associated protein 1 as a major mediator of basal and apoptotic glutathione release Biochim. Biophys. Acta 1778 (10) 2413-2420
46. Ghibelli, L., Fanelli, C., Rotillo, E., Lafavia, E., Copolla, S., Colussi, C., Civitareale, P., and Ciriolo, M. R. (1998) Rescue of cells from apoptosis by inhibition of active GSH extrusion FASEB J. 12, 479-486 (Pubitemid 28146527)
47. Hammond, C. L., Marchan, R., Krance, S. M., and Ballatori, N. (2007) Glutathione export during apoptosis requires functional multidrug resistance-associated proteins J. Biol. Chem. 282 (19) 14337-14347 (Pubitemid 47100459)
48. Filomeni, G., Rotilio, G., and Ciriolo, M. R. (2002) Cell signalling and the glutathione redox system Biochem. Pharmacol. 64 (5-6) 1057-1064 (Pubitemid 35232281)
49. Ballatori, N., Krance, S. M., Marchan, R., and Hammond, C. L. (2009) Plasma membrane glutathione transporters and their roles in cell physiology and pathophysiology Mol. Aspects Med. 30 (1-2) 13-28
50. Scheffer, G. L., Pijnenborg, A. C., Smit, E. F., Müller, M., Postma, D. S., Timens, W., van der Valk, P., de Vries, E. G., and Scheper, R. J. (2002) Multidrug resistance related molecules in human and murine lung J. Clin. Pathol. 332-339 (Pubitemid 34494170)
51. Kang, H.-K., Lee, E., Pyo, H., and Lim, S.-J. (2001) Cyclooxygenase independent down-regulation of multidrug resistance associated protein-1 expression by celecoxib in human lung cancer cells Mol. Cancer. Ther. 4, 1358-1363
52. Leslie, E. M., Deeley, R. G., and Cole, S. P. C. (2001) Toxicological relevance of the multidrug resistance protein 1, MRP1 (ABCC1) and related transporters Toxicol. 167, 3-23 (Pubitemid 32830943)
53. Zaman, G. J. R., Lankelema, J., van Tellingen, O., Beijnen, J., Dekker, H., Paulusma, C., Oude Elferinkii, R. P. J., Bass, F., and Borst, P. (1995) Role of glutathione in the export of compounds from cells by the multidrug-resistance-associated protein Proc. Natl. Acad. Sci. U.S.A. 92, 7690-7694
54. Salomon, J. J. and Ehrhardt, C. (2010) Nanoparticles attenuate P-glycoprotein/MDR1 function in A549 human alveolar epithelial cells Eur. J. Pharm. Biopharm. 77 (3) 392-397
55. Meng, H., Liong, M., Xia, T., Li, Z., Ji, Z., Zink, J. I., and Nel, A. E. (2010) Engineered design of mesoporous silica nanoparticles to deliver doxorubicin and P-Glycoprotein siRNA to overcome drug resistance in a cancer cell line ACS Nano 4 (8) 4539-4550
56. Kagan, V. E., Borisenko, G. G., Serinkan, B. F., Tyurina, Y. Y., Tyurin, V. A., Jiang, J., Liu, S. X., Shvedova, A. A., Fabisiak, J. P., Uthaisang, W., and Fadeel, B. (2003) Appetizing rancidity of apoptotic cells for macrophages: oxidation, externalization, and recognition of phosphatidylserine Am. J. Physiol. Lung Cell Mol. Physiol. 285 (1) L1-17
57. Spörl, F, Wunderskirchner, M, Ullrich, O, Bömke, G, Breitenbach, U, Blatt, T, Wenck, H, Wittern, K. P., and Schrader, A. (2010) Real-time monitoring of membrane cholesterol reveals new insights into epidermal differentiation J. Invest. Dermatol. 130 (5) 1268-78
58. Peters, M. F. and Scott, C. W. (2009) Evaluating cellular impedance assays for detection of GPCR pleiotropic signalling and functional selectivity J. Biomol. Screen. 14 (3) 246-255
59. Tarantola, M., Schneider, D., Sunnick, E., Adam, H., Pierrat, S., Rosman, C., Breus, V., Sönnichsen, C., Basché, T., Wegener, J., and Janshoff, A. (2009) Cytotoxicity of metal and semiconductor nanoparticles indicated by cellular micromotility ACS Nano 3 (1) 213-22
60. Reno, F., Burattini, S., Rossi, S., Luchetti, F., Columbaro, M., Santi, S., Papa, S., and Falcieri, E. (1998) Phospholipid rearrangement of apoptotic membrane does not depend on nuclear activity Histochem. Cell Biol. 110, 467-476 (Pubitemid 28480279)
61. Drenou, B., Blancheteau, V., Burgess, D. H., Fauchet, R., Charron, D. J., and Mooney, N. A. (1999) A caspase-independent pathway of MHC class II antigen-mediated apoptosis of human B lymphocytes J. Immunol. 163, 4115-4124 (Pubitemid 29474473)
62. Tietze, F. (1969) Enzymatic method for quantitative determination of nanogram quantities of total and oxidised glutathione: application to mammalian blood and other tissues Anal. Biochem. 27, 502-522
63. Faul, F, Erdfelder, E, Buchner, A, and Lang, A. L. (2009) Statistical power analyses using G*Power 3.1: Tests for correlation and regression analyses Behavior Res. Methods 41 (4) 1149-1160