Evaluation of Toxicity Ranking for Metal Oxide Nanoparticles via an in Vitro Dosimetry Model

ACS Nano

Volumn 9, Issue 9, 2015, Pages 9303-9313

  Liu, Rong ^a   Liu, Haoyang Haven ^a,b   Ji, Zhaoxia ^a   Chang, Chong Hyun ^a   Xia, Tian ^a   Nel, Andre E ^a   Cohen, Yoram ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

dose response; dosimetry; nanomaterial; nanotoxicology; sedimentation

Indexed keywords

AGGLOMERATION; BIOMATERIALS; CALCULATIONS; CELL CULTURE; DOSIMETRY; FRACTAL DIMENSION; HAZARDS; METAL NANOPARTICLES; METALLIC COMPOUNDS; NANOPARTICLES; PARTICLE SIZE; PARTICLE SIZE ANALYSIS; SEDIMENTATION; SUSPENSIONS (FLUIDS); TOXICITY;

DOSE RESPONSE; DOSE-RESPONSE ANALYSIS; ENGINEERED NANOPARTICLES; METAL OXIDE NANOPARTICLES; NANOMATERIAL; NANOTOXICOLOGY; PHYSICOCHEMICAL PARAMETERS; SUSPENSION PROPERTIES;

METALS;

METAL NANOPARTICLE; OXIDE;

CHEMISTRY; DOSE RESPONSE; PARTICLE SIZE; RADIOMETRY; TOXICITY TESTING;

DOSE-RESPONSE RELATIONSHIP, DRUG; METAL NANOPARTICLES; OXIDES; PARTICLE SIZE; RADIOMETRY; TOXICITY TESTS;

EID: 84942284308     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/acsnano.5b04420     Document Type: Article

References (70)

1. Guo, Z.; Tan, L. Fundamentals and Applications of Nanomaterials, 1 st ed.; Artech House: Boston, 2009.
2. The Wilson Center. Inventory Finds Increase in Consumer Products Containing Nanoscale Materials http://www.nanotechproject.org/cpi/ (accessed on July 1, 2015).
3. Colvin, V. L. The Potential Environmental Impact of Engineered Nanomaterials Nat. Biotechnol. 2003, 21, 1166-1170 10.1038/nbt875
4. Gerber, C.; Lang, H. P. How the Doors to the Nanoworld Were Opened Nat. Nanotechnol. 2006, 1, 3-5 10.1038/nnano.2006.70
5. Scown, T. M.; Van Aerle, R.; Tyler, C. R. Review: Do Engineered Nanoparticles Pose a Significant Threat to the Aquatic Environment? Crit. Rev. Toxicol. 2010, 40, 653-670 10.3109/10408444.2010.494174
6. Nel, A.; Xia, T.; Mädler, L.; Li, N. Toxic Potential of Materials at the Nanolevel Science (Washington, DC, U. S.) 2006, 311, 622-627 10.1126/science.1114397
7. Sharifi, S.; Behzadi, S.; Laurent, S.; Laird Forrest, M.; Stroeve, P.; Mahmoudi, M. Toxicity of Nanomaterials Chem. Soc. Rev. 2012, 41, 2323-2343 10.1039/C1CS15188F
8. Jiang, W.; Kim, B. Y. S.; Rutka, J. T.; Chan, W. C. W. Nanoparticle-Mediated Cellular Response Is Size-Dependent Nat. Nanotechnol. 2008, 3, 145-150 10.1038/nnano.2008.30
9. Kahru, A.; Dubourguier, H.-C. From Ecotoxicology to Nanoecotoxicology Toxicology 2010, 269, 105-119 10.1016/j.tox.2009.08.016
10. Wang, X.; Xia, T.; Ntim, S. A.; Ji, Z.; Lin, S.; Meng, H.; Chung, C.-H.; George, S.; Zhang, H.; Wang, M. et al. Dispersal State of Multiwalled Carbon Nanotubes Elicits Profibrogenic Cellular Responses That Correlate with Fibrogenesis Biomarkers and Fibrosis in the Murine Lung ACS Nano 2011, 5, 9772-9787 10.1021/nn2033055
11. Asharani, P. V.; Lianwu, Y.; Gong, Z.; Valiyaveettil, S. Comparison of the Toxicity of Silver, Gold and Platinum Nanoparticles in Developing Zebrafish Embryos Nanotoxicology 2011, 5, 43-54 10.3109/17435390.2010.489207
12. Hardman, R. A Toxicologic Review of Quantum Dots: Toxicity Depends on Physicochemical and Environmental Factors Environ. Health Perspect. 2006, 114, 165-172 10.1289/ehp.8284
13. Zhang, H.; Ji, Z.; Xia, T.; Meng, H.; Low-Kam, C.; Liu, R.; Pokhrel, S.; Lin, S.; Wang, X.; Liao, Y.-P. et al. Use of Metal Oxide Nanoparticle Band Gap to Develop a Predictive Paradigm for Oxidative Stress and Acute Pulmonary Inflammation ACS Nano 2012, 6, 4349-4368 10.1021/nn3010087
14. Cohen, Y.; Rallo, R.; Liu, R.; Liu, H. H. In Silico Analysis of Nanomaterials Hazard and Risk Acc. Chem. Res. 2013, 46, 802-812 10.1021/ar300049e
15. De Jong, W. H.; Borm, P. J. A. Drug Delivery and Nanoparticles: Applications and Hazards Int. J. Nanomed. 2008, 3, 133-149 10.2147/IJN.S596
16. Cattaneo, A. G.; Gornati, R.; Sabbioni, E.; Chiriva-Internati, M.; Cobos, E.; Jenkins, M. R.; Bernardini, G. Nanotechnology and Human Health: Risks and Benefits J. Appl. Toxicol. 2010, 30, 730-744 10.1002/jat.1609
17. Damoiseaux, R.; George, S.; Li, M.; Pokhrel, S.; Ji, Z.; France, B.; Xia, T.; Suarez, E.; Rallo, R.; Mädler, L. et al. No Time to Lose - High Throughput Screening to Assess Nanomaterial Safety Nanoscale 2011, 3, 1345-1360 10.1039/c0nr00618a
18. Wiesner, M. R.; Lowry, G. V.; Alvarez, P.; Dionysiou, D.; Biswas, P. Assessing the Risks of Manufactured Nanomaterials Environ. Sci. Technol. 2006, 40, 4336-4345 10.1021/es062726m
19. Linkov, I.; Bates, M. E.; Canis, L. J.; Seager, T. P.; Keisler, J. M. A Decision-Directed Approach for Prioritizing Research into the Impact of Nanomaterials on the Environment and Human Health Nat. Nanotechnol. 2011, 6, 784-787 10.1038/nnano.2011.163
20. Xia, T.; Malasarn, D.; Lin, S.; Ji, Z.; Zhang, H.; Miller, R. J.; Keller, A. A.; Nisbet, R. M.; Harthorn, B. H.; Godwin, H. A. et al. Implementation of a Multidisciplinary Approach to Solve Complex Nano EHS Problems by the UC Center for the Environmental Implications of Nanotechnology Small 2013, 9, 1428-1443 10.1002/smll.201201700
21. Shaw, S. Y.; Westly, E. C.; Pittet, M. J.; Subramanian, A.; Schreiber, S. L.; Weissleder, R. Perturbational Profiling of Nanomaterial Biologic Activity Proc. Natl. Acad. Sci. U. S. A. 2008, 105, 7387-7392 10.1073/pnas.0802878105
22. Krewski, D.; Acosta, D.; Andersen, M.; Anderson, H.; Bailar, J. C.; Boekelheide, K.; Brent, R.; Charnley, G.; Cheung, V. G.; Green, S. et al. Toxicity Testing in the 21st Century: A Vision and a Strategy J. Toxicol. Environ. Health, Part B 2010, 13, 51-138 10.1080/10937404.2010.483176
23. George, S.; Pokhrel, S.; Xia, T.; Gilbert, B.; Ji, Z.; Schowalter, M.; Rosenauer, A.; Damoiseaux, R.; Bradley, K. A.; Mädler, L. et al. Use of a Rapid Cytotoxicity Screening Approach to Engineer a Safer Zinc Oxide Nanoparticle through Iron Doping ACS Nano 2010, 4, 15-29 10.1021/nn901503q
24. Lin, S.; Zhao, Y.; Xia, T.; Meng, H.; Ji, Z.; Liu, R.; George, S.; Xiong, S.; Wang, X.; Zhang, H. et al. High Content Screening in Zebrafish Speeds up Hazard Ranking of Transition Metal Oxide Nanoparticles ACS Nano 2011, 5, 7284-7295 10.1021/nn202116p
25. Wittmaack, K. In Search of the Most Relevant Parameter for Quantifying Lung Inflammatory Response to Nanoparticle Exposure: Particle Number, Surface Area, or What? Environ. Health Perspect. 2006, 115, 187-194 10.1289/ehp.9254
26. Teeguarden, J. G.; Hinderliter, P. M.; Orr, G.; Thrall, B. D.; Pounds, J. G. Particokinetics in Vitro: Dosimetry Considerations for in Vitro Nanoparticle Toxicity Assessments Toxicol. Sci. 2006, 95, 300-312 10.1093/toxsci/kfl165
27. Cho, E. C.; Zhang, Q.; Xia, Y. The Effect of Sedimentation and Diffusion on Cellular Uptake of Gold Nanoparticles Nat. Nanotechnol. 2011, 6, 385-391 10.1038/nnano.2011.58
28. Park, M. S.; Park, J.; Jeon, S. K.; Yoon, T. H. The Effects of Sedimentation and Dissolution on the Cytotoxicity of Ag Nanoparticles J. Nanosci. Nanotechnol. 2013, 13, 7264-7270 10.1166/jnn.2013.8086
29. Yoon, D.; Woo, D.; Kim, J.; Kim, M.; Kim, T.; Hwang, E.-S.; Baik, S. Agglomeration, Sedimentation, and Cellular Toxicity of Alumina Nanoparticles in Cell Culture Medium J. Nanopart. Res. 2011, 13, 2543-2551 10.1007/s11051-010-0147-4
30. Sharma, G.; Kodali, V.; Gaffrey, M.; Wang, W.; Minard, K. R.; Karin, N. J.; Teeguarden, J. G.; Thrall, B. D. Iron Oxide Nanoparticle Agglomeration Influences Dose Rates and Modulates Oxidative Stress-Mediated Dose-Response Profiles in Vitro Nanotoxicology 2014, 8, 663-675 10.3109/17435390.2013.822115
31. Pal, A. K.; Bello, D.; Cohen, J.; Demokritou, P. Implications of in Vitro Dosimetry on Toxicological Ranking of Low Aspect Ratio Engineered Nanomaterials Nanotoxicology 2015, 1-15 10.3109/17435390.2014.986670
32. Summers, M. R. B.; Brown, M. R.; Hondow, N.; Brydson, R.; Rees, P.; Brown, A. P. Statistical Prediction of Nanoparticle Delivery: From Culture Media to Cell Nanotechnology 2015, 26, 155101 10.1088/0957-4484/26/15/155101
33. Cohen, J.; Deloid, G.; Pyrgiotakis, G.; Demokritou, P. Interactions of Engineered Nanomaterials in Physiological Media and Implications for in Vitro Dosimetry Nanotoxicology 2013, 7, 417-431 10.3109/17435390.2012.666576
34. Cohen, J. M.; Teeguarden, J. G.; Demokritou, P. An Integrated Approach for the in Vitro Dosimetry of Engineered Nanomaterials Part. Fibre Toxicol. 2014, 11, 20 10.1186/1743-8977-11-20
35. Deloid, G.; Cohen, J. M.; Darrah, T.; Derk, R.; Rojanasakul, L.; Pyrgiotakis, G.; Wohlleben, W.; Demokritou, P. Estimating the Effective Density of Engineered Nanomaterials for in Vitro Dosimetry Nat. Commun. 2014, 5, 3514 10.1038/ncomms4514
36. Hinderliter, P. M.; Minard, K. R.; Orr, G.; Chrisler, W. B.; Thrall, B. D.; Pounds, J. G.; Teeguarden, J. G. ISDD: A Computational Model of Particle Sedimentation, Diffusion and Target Cell Dosimetry for in Vitro Toxicity Studies Part. Fibre Toxicol. 2010, 7, 36 10.1186/1743-8977-7-36
37. Liu, R.; Zhang, H. Y.; Ji, Z. X.; Rallo, R.; Xia, T.; Chang, C. H.; Nel, A.; Cohen, Y. Development of Structure-Activity Relationship for Metal Oxide Nanoparticles Nanoscale 2013, 5, 5644-5653 10.1039/c3nr01533e
38. Ji, Z.; Jin, X.; George, S.; Xia, T.; Meng, H.; Wang, X.; Suarez, E.; Zhang, H.; Hoek, E. M. V; Godwin, H. et al. Dispersion and Stability Optimization of TiO2 Nanoparticles in Cell Culture Media Environ. Sci. Technol. 2010, 44, 7309-7314 10.1021/es100417s
39. Zook, J. M.; Rastogi, V.; MacCuspie, R. I.; Keene, A. M.; Fagan, J. Measuring Agglomerate Size Distribution and Dependence of Localized Surface Plasmon Resonance Absorbance on Gold Nanoparticle Agglomerate Size Using Analytical Ultracentrifugation ACS Nano 2011, 5, 8070-8079 10.1021/nn202645b
40. Zook, J. M.; MacCuspie, R. I.; Locascio, L. E.; Halter, M. D.; Elliott, J. T. Stable Nanoparticle Aggregates/agglomerates of Different Sizes and the Effect of Their Size on Hemolytic Cytotoxicity Nanotoxicology 2011, 5, 517-530 10.3109/17435390.2010.536615
41. Li, X.; Logan, B. E. Collision Frequencies of Fractal Aggregates with Small Particles by Differential Sedimentation Environ. Sci. Technol. 1997, 31, 1229-1236 10.1021/es960771w
42. Johnson, C. P.; Li, X.; Logan, B. E. Settling Velocities of Fractal Aggregates Environ. Sci. Technol. 1996, 30, 1911-1918 10.1021/es950604g
43. Li, X. Y.; Logan, B. E. Permeability of Fractal Aggregates Water Res. 2001, 35, 3373-3380 10.1016/S0043-1354(01)00061-6
44. Liu, R.; Rallo, R.; George, S.; Ji, Z.; Nair, S.; Nel, A. E.; Cohen, Y. Classification NanoSAR Development for Cytotoxicity of Metal Oxide Nanoparticles Small 2011, 7, 1118-1126 10.1002/smll.201002366
45. Liu, H. H.; Surawanvijit, S.; Rallo, R.; Orkoulas, G.; Cohen, Y. Analysis of Nanoparticle Agglomeration in Aqueous Suspensions via Constant-Number Monte Carlo Simulation Environ. Sci. Technol. 2011, 45, 9284-9292 10.1021/es202134p
46. Liu, H. H.; Lanphere, J.; Walker, S.; Cohen, Y. Effect of Hydration Repulsion on Nanoparticle Agglomeration Evaluated via a Constant Number Monte - Carlo Simulation Nanotechnology 2015, 26, 45708 10.1088/0957-4484/26/4/045708
47. Hunter, R. J. Foundations of Colloid Science, 2 nd ed.; Oxford University Press: New York, 2001.
48. Sheldon, K. F. Smoke, Dust, and Haze: Fundamentals of Aerosol Dynamics, 2 nd ed.; Oxford University Press: New York, 2000.
49. Quik, J. T. K.; Lynch, I.; Van Hoecke, K.; Miermans, C. J. H.; De Schamphelaere, K. A. C.; Janssen, C. R.; Dawson, K. A.; Stuart, M. A. C.; Van De Meent, D. Effect of Natural Organic Matter on Cerium Dioxide Nanoparticles Settling in Model Fresh Water Chemosphere 2010, 81, 711-715 10.1016/j.chemosphere.2010.07.062
50. Han, X.; Corson, N.; Wade-Mercer, P.; Gelein, R.; Jiang, J.; Sahu, M.; Biswas, P.; Finkelstein, J. N.; Elder, A.; Oberdörster, G. Assessing the Relevance of in Vitro Studies in Nanotoxicology by Examining Correlations between in Vitro and in Vivo Data Toxicology 2012, 297, 1-9 10.1016/j.tox.2012.03.006
51. Ritz, C. Toward a Unified Approach to Dose-Response Modeling in Ecotoxicology Environ. Toxicol. Chem. 2010, 29, 220-229 10.1002/etc.7
52. Sampah, M. E. S.; Shen, L.; Jilek, B. L.; Siliciano, R. F. Dose-Response Curve Slope Is a Missing Dimension in the Analysis of HIV-1 Drug Resistance Proc. Natl. Acad. Sci. U. S. A. 2011, 108, 7613-7618 10.1073/pnas.1018360108
53. Walkey, C. D.; Olsen, J. B.; Song, F.; Liu, R.; Guo, H.; Olsen, W.; Cohen, Y.; Emili, A.; Chan, W. C. W. Protein Corona Fingerprinting Predicts the Cell Association of Gold Nanoparticles ACS Nano 2014, 8, 2439-2455 10.1021/nn406018q
54. Lundqvist, M.; Stigler, J.; Elia, G.; Lynch, I.; Cedervall, T.; Dawson, K. A. Nanoparticle Size and Surface Properties Determine the Protein Corona with Possible Implications for Biological Impacts Proc. Natl. Acad. Sci. U. S. A. 2008, 105, 14265-14270 10.1073/pnas.0805135105
55. Liu, R.; Rallo, R.; Bilal, M.; Cohen, Y. Quantitative Structure-Activity Relationships for Cellular Uptake of Surface-Modified Nanoparticles Comb. Chem. High Throughput Screening 2015, 18, 365-375 10.2174/1386207318666150306105525
56. Weissleder, R.; Kelly, K.; Sun, E. Y.; Shtatland, T.; Josephson, L. Cell-Specific Targeting of Nanoparticles by Multivalent Attachment of Small Molecules Nat. Biotechnol. 2005, 23, 1418-1423 10.1038/nbt1159
57. Asati, A.; Santra, S.; Kaittanis, C.; Perez, J. M. Surface-Charge-Dependent Cell Localization and Cytotoxicity of Cerium Oxide Nanoparticles ACS Nano 2010, 4, 5321-5331 10.1021/nn100816s
58. Xu, L.; Takemura, T.; Xu, M.; Hanagata, N. Toxicity of Silver Nanoparticles as Assessed by Global Gene Expression Analysis Mater. Express 2011, 1, 74-79 10.1166/mex.2011.1010
59. Mortensen, N. P.; Hurst, G. B.; Wang, W.; Foster, C. M.; Nallathamby, P. D.; Retterer, S. T. Dynamic Development of the Protein Corona on Silica Nanoparticles: Composition and Role in Toxicity Nanoscale 2013, 5, 6372-6380 10.1039/c3nr33280b
60. Liu, R.; France, B.; George, S.; Rallo, R.; Zhang, H.; Xia, T.; Nel, A.; Bradley, K.; Cohen, Y. Association Rule Mining of Cellular Responses Induced by Metal and Metal Oxide Nanoparticles Analyst 2014, 139, 943-953 10.1039/C3AN01409F
61. Rallo, R.; France, B.; Liu, R.; Nair, S.; George, S.; Damoiseaux, R.; Giralt, F.; Nel, A.; Bradley, K.; Cohen, Y. Self-Organizing Map Analysis of Toxicity-Related Cell Signaling Pathways for Metal and Metal Oxide Nanoparticles Environ. Sci. Technol. 2011, 45, 1695-1702 10.1021/es103606x
62. Lison, D.; Vietti, G.; van den Brule, S. Paracelsus in Nanotoxicology Part. Fibre Toxicol. 2014, 11, 35 10.1186/s12989-014-0035-7
63. Song, C.; Wang, P.; Makse, H. A. A Phase Diagram for Jammed Matter Nature 2008, 453, 629-632 10.1038/nature06981
64. Rogak, S. N.; Flagan, R. C. Stokes Drag on Self-Similar Clusters of Spheres J. Colloid Interface Sci. 1990, 134, 206-218 10.1016/0021-9797(90)90268-S
65. Lee, D. J.; Chen, G. W.; Liao, Y. C.; Hsieh, C. C. On the Free-Settling Test for Estimating Activated Sludge Floc Density Water Res. 1996, 30, 541-550 10.1016/0043-1354(95)00229-4
66. Veerapaneni, S.; Wiesner, M. R. Hydrodynamics of Fractal Aggregates with Radially Varying Permeability J. Colloid Interface Sci. 1996, 177, 45-57 10.1006/jcis.1996.0005
67. Woodfield, D.; Bickert, G. An Improved Permeability Model for Fractal Aggregates Settling in Creeping Flow Water Res. 2001, 35, 3801-3806 10.1016/S0043-1354(01)00128-2
68. Gmachowski, L. Transport Properties of Fractal Aggregates Calculated by Permeability Colloids Surf., A 2003, 215, 173-179 10.1016/S0927-7757(02)00440-5
69. Fröhlich, E.; Bonstingl, G.; Höfler, A.; Meindl, C.; Leitinger, G.; Pieber, T. R.; Roblegg, E. Comparison of Two in Vitro Systems to Assess Cellular Effects of Nanoparticles-Containing Aerosols Toxicol. In Vitro 2013, 27, 409-417 10.1016/j.tiv.2012.08.008
70. Nymark, P.; Jensen, K.; Suhonen, S.; Kembouche, Y.; Vippola, M.; Kleinjans, J.; Catalan, J.; Norppa, H.; van Delft, J.; Briede, J. Free Radical Scavenging and Formation by Multi-Walled Carbon Nanotubes in Cell Free Conditions and in Human Bronchial Epithelial Cells Part. Fibre Toxicol. 2014, 11, 4 10.1186/1743-8977-11-4