Abstract
Engineered nanoparticles, in particular metal oxide nanoparticles, with their unique and novel properties, enable a plethora of new applications in various fields of research. These new properties have raised concerns about potential adverse effects for the environment and human health and are nowadays very controversial. A reliable, cost- and time-effective, rapid and mechanistic-based testing strategy is needed to replace current conventional phenomenological assessments. Today’s in vitro technology, providing human-based advanced cellular models representing different organ barriers such as skin, lung, placenta, or liver, may cover this need. The aim of this article is to present the current changes in (nano) toxicology strategies, the extent to which in vitro models have achieved general acceptance, and how the relevance of these models can further be improved using examples of selected metal oxide nanoparticles.
Similar content being viewed by others
References
J.W. Rasmussen, E. Martinez, P. Louka, D.G. Wingett, Expert Opin. Drug Deliv. 7, 1063 (2010).
A.K. Gupta, M. Gupta, Biomaterials 26, 3995 (2005).
T. Hartung, C. Rovida, Nature 460, 1080 (2009).
G.P. Rossini, T. Hartung, ALTEX 29, 359 (2012).
Committee on Toxicity Testing and Assessment of Environmental Agents, National Research Council, Toxicity Testing for the 21st Century: A Vision and a Strategy (The National Academies Press, Washington, DC, 2007).
A. Astashkina, D.W. Grainger, Adv. Drug Deliv. Rev. 69–70, 1 (2014).
T. Hartung, Nature 460, 208 (2009).
V.V. Mody, R. Siwale, A. Singh, H.R. Mody, J. Pharm. Bioallied Sci. 2, 282 (2010).
Future Markets Inc., The Global Market for Metal Oxide Nanoparticles to 2020 (Research and Markets, Dublin, 2013).
J.A. Rodriguez, M. Fernandez-Garcia, Synthesis, Properties, and Applications of Oxide Nanomaterials (Wiley, Hoboken 2007), p. 718.
M. Niederberger, G. Garnweitner, J. Buha, J. Polleux, J. Ba, N. Pinna, J. Sol-Gel Sci. Technol. 40, 259 (2006).
M. Niederberger, Acc. Chem. Res. 40, 793 (2007).
A.H. Lu, E.L. Salabas, F. Schuth, Angew. Chem. Int. Ed. Engl. 46, 1222 (2007).
S. Sun, H. Zeng, J. Am. Chem. Soc. 124, 8204 (2002).
V.K. LaMer, R.H. Dinegar, J. Am. Chem. Soc. 72, 4847 (1950).
M. Mahmoudi, H. Hofmann, B. Rothen-Rutishauser, A. Petri-Fink, Chem. Rev. 112, 2323 (2012).
A.J. Carterson, K. Höner zu Bentrup, C.M. Ott, M.S. Clarke, D.L. Pierson, C.R. Vanderburg, K.L. Buchanan, C.A. Nickerson, M.J. Schurr, Infect. Immun. 73, 1129 (2005).
E.L. Roggen, N.K. Soni, G.R. Verheyen, Toxicol. In Vitro 20, 1249 (2006).
G. Gstraunthaler, T. Hartung, in Cell Culture Models of Biological Barriers: In-Vitro Test Systems for Drug Absorption and Delivery, C.M. Lehr, Ed. (Taylor and Francis, New York, 2002), vol. 7, pp. 112–120.
F.P. Gruber, T. Hartung, ALTEX 21 (Suppl. 1), 3 (2004).
P.R. Wheather, H.G. Burkitt, V.G. Daniels, Functional Histology (Churchill Livingstone, Edinburgh, 1979), p. 348.
B.W. Barry, Eur. J. Pharm. Sci. 14, 101 (2001).
M. Loden, H. Breitner, H. Gonzalez, D.W. Edstrom, U. Akerstrom, J. Austad, I. Buraczewska-Norin, M. Matsson, H.C. Wulf, Br. J. Dermatol. 165, 255 (2011).
V. Sharma, R.K. Shukla, N. Saxena, D. Parmar, M. Das, A. Dhawan, Toxicol. Lett. 185, 211 (2009).
P. Boukamp, R.T. Petrussevska, D. Breitkreutz, J. Hornung, A. Markham, N.E. Fusenig, J. Cell Biol. 106, 761 (1988).
C. Zanette, M. Pelin, M. Crosera, G. Adami, M. Bovenzi, F.F. Larese, C. Florio, Toxicol. In Vitro 25, 1053 (2011).
C. Xue, J. Wu, F. Lan, W. Liu, X. Yang, F. Zeng, H. Xu, J. Nanosci. Nanotechnol. 10, 8500 (2010).
X. Yang, J. Liu, H. He, L. Zhou, C. Gong, X. Wang, L. Yang, J. Yuan, H. Huang, L. He, B. Zhang, Z. Zhuang, Part. Fibre Toxicol. 7, 1 (2010).
R. Osborne, M.A. Perkins, Toxicol. in Vitro 5, 563 (1991).
Z. Kmiec, Adv. Anat. Embryol. Cell Biol. 161, III (2001).
M.J. Coon, X.X. Ding, S.J. Pernecky, A.D. Vaz, FASEB J. 6, 669 (1992).
A. Bhushan, N. Senutovitch, S.S. Bale, W.J. McCarty, M. Hegde, R. Jindal, I. Golberg, O. Berk Usta, M.L. Yarmush, L. Vernetti, A. Gough, A. Bakan, T. Shun, R. Biasio, D. Lansing Taylor, Stem Cell Res. Ther. 4 (Suppl. 1), S16 (2013).
R. Kostadinova, F. Boess, D. Applegate, L. Suter, T. Wieser, T. Singer, B. Naughton, A. Roth, Toxicol. Appl. Pharmacol. 268, 1 (2013).
A. Kermanizadeh, G. Pojana, B.K. Gaiser, R. Birkedal, D. Bilanicova, H. Wallin, K.A. Jensen, B. Sellergren, G.R. Hutchison, A. Marcomini, V. Stone, Nanotoxicology 7, 301 (2013).
M.I. Hermanns, J. Kasper, P. Dubruel, C. Pohl, C. Uboldi, V. Vermeersch S. Fuchs, R.E. Unger, C.J. Kirkpatrick, J. R. Soc. Interface 7 (Suppl. 1), S41 (2010).
B. Rothen-Rutishauser, F. Blank, C. Muhlfeld, P. Gehr, Expert Opin. Drug Metab. Toxicol. 4, 1075 (2008).
E. Alfaro-Moreno, T.S. Nawrot, B.M. Vanaudenaerde, M.F. Hoylaerts, J.A. Vanoirbeek, B. Nemery, P.H. Hoet, Eur. Respir. J. 32, 1184 (2008).
A.D. Lehmann, F. Blank, O. Baum, P. Gehr, B.M. Rothen-Rutishauser, Part. Fibre Toxicol. 6, 26 (2009).
L. Muller, M. Riediker, P. Wick, M. Mohr, P. Gehr, B. Rothen-Rutishauser, J. R. Soc. Interface 7 (Suppl. 1), S27 (2010).
D. Huh, G.A. Hamilton, D.E. Ingber, Trends Cell Biol. 21, 745 (2011).
D. Huh, B.D. Matthews, A. Mammoto, M. Monotoya-Zavala, H.Y. Hsin, D.E. Ingber, Science 328, 1662 (2010).
D. Huh, D.C. Leslie, B.D. Matthews J.P. Fraser, S. Jurek, G.A. Hamilton K.S. Thorneloe, M.A. McAlexander, D.E. Ingber, Sci. Transl. Med. 4, 159ra147 (2012).
T. Buerki-Thurnherr, L. Xiao, L. Diener, O. Arslan, C. Hirsch, X. Maeder-Althaus, K. Grieder, B. Wampfler, S. Mathur, P. Wick, H.F. Krug, Nanotoxicology 7, 402 (2013).
S. Tuomela, R. Autio, T. Buerki-Thurnherr, O. Arslan, A. Kunzmann, B. Andersson-Willman, P. Wick, S. Mathur, A. Scheynius, H.F. Krug, B. Fadeel, R. Lahesmaa, PLoS One 8, e68415 (2013).
T. Xia, Y. Zhao, T. Sager, S. George, S. Pokhrel, N. Li, D. Schoenfeld, H. Meng, S. Lin, X. Wang, M. Wang, Z. Ji, J.I. Zink, L. Madler, V. Castranova, A.E. Nel, ACS Nano 2, 2121 (2008).
G.A. Orr, W.B. Chrisler, K.J. Cassens, R. Tan, B.J. Tarasevich, L.M. Markillie, R.C. Zangar, B.D. Thrall, Nanotoxicology 5, 296 (2010).
J.W. Park, T.B. Henry, S. Ard, F.M. Menn, R.N. Compton, G.S. Salyer, Nanotoxicology 5, 168 (2010).
A.C. Enders, T.N. Blankenship, Adv. Drug Deliv. Rev. 38, 3 (1999).
B.P. Lanphear, C.V. Vorhees, D.C. Bellinger, PLoS Med. 2, e61 (2005).
P. Latzin, M. Roosli, A. Huss, C.E. Kuehni, U. Frey, Eur. Respir. J. 33, 594 (2009).
V. Menezes, A. Malek, J.A. Keelan, Curr. Pharm. Biotechnol. 12, 731 (2011).
T. Buerki-Thurnherr, U. von Mandach, P. Wick, Swiss Med. Wkly. 142, w13559 (2012).
H. Schneider, M. Panigel, J. Dancis, Am. J. Obstet. Gynecol. 114, 822 (1972).
M. Panigel, M. Pascaud, J.L. Brun, J. Physiol. Paris 59, 277 (1967).
M. Saunders, Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol. 1, 671 (2009).
G. Bhabra, A. Sood, B. Fisher, L. Cartwright, M. Saunders, W.H. Evans, A. Surprenant, G. Lopez-Castejon, S. Mann, S.A. Davis, L.A. Hails, E. Ingham, P. Verkade, J. Lane, K. Heesom, R. Newson, C.P. Case, Nat. Nanotechnol. 4, 876 (2009).
M.C. Parry, G. Bhabra, A. Sood, F. Machado, L. Cartwright, M. Saunders, E. Ingham, R. Newson, A.W. Blom, C.P. Case, Biomaterials 31, 4477 (2010).
V. Zaga, G. Estrada-Guiterrez, J. Beltran-Montoya, R. Maida-Claros, R. Lopez-Vancell, F. Vadillo-Ortega, Biol. Reprod. 71, 1296 (2004).
C. Prouillac, S. Lecoeur, Drug Metab. Dispos. 38, 1623 (2010).
E.K. Sackmann, A.L. Fulton, D.J. Beebe, Nature 507, 181 (2014).
J.M. Kelm, V. Lorber, J.G. Snedeker, D. Schmidt, A. Broggini-Tenzer, M. Weisstanner, B. Odermatt, A. Mol, G. Zund, S.P. Hoerstrup, J. Biotechnol. 148, 46 (2010).
F. Tian, D. Razansky, G.G. Estrada, M. Semmler-Behnke, A. Beyerle, W. Kreyling, V. Ntziachristos, T. Stoeger, Inhal. Toxicol. 21 (Suppl. 1), 92 (2009).
K. Yamashita, Y. Yoshioka, K. Higashisaka, Y. Morishita, T. Yoshida, M. Fujimura, H. Kayamuro, H. Nabeshi, T. Yamashita, K. Nagano, Y. Abe, H. Kamada, Y. Kawai, T. Mayumi, T. Yoshikawa, N. Itoh, S. Tsunoda, Y. Tsutsumi, Inflammation 33, 276 (2010).
M. Chu, Q. Wu, H. Yang, R. Yuan, S. Hou, Y. Yang, Y. Zou, S. Xu, K. Xu, A. Ji, L. Sheng, Small 6, 670 (2010).
A. Pietroiusti, M. Massimiani, I. Fenoglio, M. Colonna, F. Valentini, G. Palleschi, A. Camaioni, A. Magrini, G. Siracusa, A. Bergamaschi, A. Sgambato, L. Campagnolo, ACS Nano 5, 4624 (2011).
A. Pietroiusti, L. Campagnolo, B. Fadeel, Small 9, 1557 (2012).
M.J. Clift, P. Gehr, B. Rothen-Rutishauser, Arch. Toxicol. (2010).
M. Mahmoudi, M.A. Sahraian, M.A. Shokrgozar, S. Laurent, ACS Chem. Neurosci. 2 (3), 118 (2011).
Acknowledgements
This work was financially supported by the Swiss National Foundation (Grants No. 320030, 138365, 150737, NRP 64 program, grant no 4064–131232), the Research fund of the Swiss Lung Association, Berne, the Adolphe Merkle Foundation, and the European Union Seventh Framework Program (FP 7) under grant agreement 309329 (Nanosolutions).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Wick, P., Grafmueller, S., Petri-Fink, A. et al. Advanced human in vitro models to assess metal oxide nanoparticle-cell interactions. MRS Bulletin 39, 984–989 (2014). https://doi.org/10.1557/mrs.2014.219
Published:
Issue Date:
DOI: https://doi.org/10.1557/mrs.2014.219