Toxicity of transition metal oxide nanoparticles: Recent insights from in vitro studies

Materials

Volumn 3, Issue 10, 2010, Pages 4842-4859

  Huang, Yue Wern ^a   Wu, Chi Heng ^a   Aronstam, Robert S ^a  

^a MISSOURI UNIVERSITY OF SCIENCE AND TECHNOLOGY   (United States)

Author keywords

Calcium homeostasis; Metal oxide; Nanoparticle; Oxidative stress; Signal transduction; Toxicity

Indexed keywords

CALCIUM HOMEOSTASIS; METAL OXIDES; NANOPARTICLE TOXICITY; PHYSICOCHEMICAL PROPERTY; SEMI-CONDUCTING PROPERTY; SURFACE CATALYTIC ACTIVITY; TRANSITION METAL OXIDE NANOPARTICLES; TRANSITION-METAL OXIDES;

CALCIUM; GENE EXPRESSION; NANOPARTICLES; NANOSTRUCTURED MATERIALS; OXIDATIVE STRESS; PHYSIOLOGY; SIGNAL TRANSDUCTION;

TOXICITY;

EID: 79959342430     PISSN: None     EISSN: 19961944     Source Type: Journal    
DOI: 10.3390/ma3104842     Document Type: Review

References (89)

1. National Nanotechnology Coordination Center. National Nanotechnology Initiative. Available online: http://www.nano.gov/html/facts/home_facts.html. (accessed on 22 October 2006)
2. Jiang, J.; Oberdorster, G.; Elder, A.; Gelein, R.; Mercer, P.; Biswas, P. Does nanoparticle activity depend upon size and crystal phase? Nanotoxicology 2008, 2, 33-42
3. Fubini, B.; Hubbard, A. Reactive oxygen species (ROS) and reactive nitrogen species (RNS) generation by silica in inflammation and fibrosis. Free Radic Biol. Med. 2003, 34, 1507-1516
4. Mossman, B.T.; Churg, A. Mechanisms in the pathogenesis of asbestosis and silicosis. Am. J. Respir. Crit. Care Med. 1998, 157, 1666-1680
5. Schins, R.P. Mechanisms of genotoxicity of particles and fibers. Inhal. Toxicol. 2002, 14, 57-78
6. Knaapen, A.M.; Borm, P.J.; Albrecht, C.; Schins, R.P. Inhaled particles and lung cancer. Part A: Mechanisms. Int. J. Cancer. 2004, 109, 799-809
7. van Maanen, J.M.; Borm, P.J.; Knaapen, A.; van Herwijnen, M.; Schilderman, P.A.; Smith, K.R.; Aust, A.E.; Tomatis, M.; Fubini, B. In vitro effects of coal fly ashes: hydroxyl radical generation, iron release, and DNA damage and toxicity in rat lung epithelial cells. Inhalation Toxicol. 1999, 11, 1123-1141
8. Driscoll, K.E.; Deyo, L.C.; Carter, J.M.; Howard, B.W.; Hassenbein, D.G.; Bertram, T.A. Effects of particle exposure and particle-elicited inflammatory cells on mutation in rat alveolar epithelial cells. Carcinogenesis 1997, 18, 423-430
9. Zhong, B.Z.; Whong, W.Z.; Ong, T.M. Detection of mineral-dust-induced DNA damage in two mammalian cell lines using the alkaline single cell gel/comet assay. Mutat. Res. 1997, 393, 181-187
10. Leanderson, P.; Tagesson, C. Hydrogen peroxide release and hydroxyl radical formation in mixtures containing mineral fibres and human neutrophils. Br. J. Ind. Med. 1992, 49, 745-759
11. Borm, P.J.; Schins, R.P.; Albrecht, C. Inhaled particles and lung cancer, part B: Paradigms and risk assessment. Int. J. Cancer 2004, 110, 3-14
12. Xia, T.; Kovochich, M.; Brant, J.; Hotze, M.; Sempf, J.; Oberley, T.; Sioutas, C.; Yeh, J.I.; Wiesner, M.R.; Nel, A.E. 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
13. Noronha, F.B.; Schmal, M.; Nicot, C.; Moraweck, B.; Frety, R. Characterization of graphite-supported palladium-cobalt catalysts by temperature-programmed reduction and magnetic measurements. J. Catal. 1997, 168, 42-50
14. Roy, S.; Das, D.; Chakravorty, D.; Agrawal, D.C. Magnetic-properties of glass-metal nanocomposites prepared by the sol-gel route and hot-pressing. J. Appl. Phys. 1993, 74, 4746-4749
15. Prinz, G.A. Magnetoelectronics. Science 1999, 283, 330-330
16. Vassiliou, J.K.; Mehrotra, V.; Russell, M.W.; Giannelis, E.P.; Mcmichael, R.D.; Shull, R.D.; Ziolo, R.F. Magnetic and optical-properties of gamma-Fe2O3 nanocrystals. J. Appl. Phys. 1993, 73, 5109-5116
17. Airapetyan, S.S.; Balayan, G.G.; Khachatryan, A.G. Synthesis and some characteristics of magnetic matrices for fixation of biologically active substances. Russ. J. Appl. Chem. 2001, 74, 519-521
18. Kobe, S.; Drazic, G.; McGuiness, P.J.; Strazisar, J. The influence of the magnetic field on the crystallisation form of calcium carbonate and the testing of a magnetic water-treatment device. J. Magn. Mag. Mater. 2001, 236, 71-76
19. Gruttner, C.; Teller, J. Preparation and characterization of magnetic nanoparticles for in-vivo applications. In Scientific and Clinical Applications of Magnetic Carriers; Hafeli, U., Schutt, W., Teller, J., Zborowski, M., Eds; Plenum Publishing Corporation: New York, NY, USA, 1997; p
20. Howard, M.A., III; Dacey, R.G.; Grady, M.S.; Ritter, R.C.; Gillies, G.T. Magnetically guided stereotaxis. In Advanced Neurosurgical Navigation; Alexander, E., III, Maciunas, R.J., Eds; Thieme Medical Publishers: New York, NY, USA, 1999; pp. 549-563
21. Howard, M.A., III; Grady, M.S.; Ritter, R.C.; Gillies, G.T.; Broaddus, W.C.; Dacey, R.G. Magnetic neurosurgery. In Stereotactic and Functional Neurosurgery; Lozano, Gildenberg & Tasker, Ed; Karger Pulbisher: Basel, Switzerland, 1996; pp. 102-107
22. Grady, M.S.; Howard, M.A.; Dacey, R.G.; Blume, W.; Lawson, M.; Werp, P.; Ritter, R.C. Experimental study of the magnetic stereotaxis system for catheter manipulation within the brain. J. Neurosurg. 2000, 93, 282-288
23. Wellman, B.J.; Howard, M.A., III; Dacey, R.G.; Grady, M.S.; Ritter, R.C.; Gillies, G.T. Magnetically guided interventional medicine. In Proceedings of the Biomedical Optics. Surgical-Assist Systems, San Jose, CA, USA, January 25-28, 1998; pp. 15-25
24. Zhu, B.L.; Xie, C.S.; Zeng, D.W.; Song, W.L.; Wang, A.H. Investigation of gas sensitivity of Sb-doped ZnO nanoparticles. Mater. Chem. Phys. 2005, 89, 148-153
25. Ramakrishna, G.G. Effect of particle size on the reactivityof quantum size ZnO nanoparticles and charge-transfer dynamics with adsorbed catechols. Langmuir 2003, 19, 3006-3012
26. Huang, G.G.; Wang, C.T.; Tang, H.T.; Huang, Y.S.; Yang, J. ZnO nanoparticle-modified infrared internal relfection elements for selective detection of volatile organic compounds. Anal. Chem. 2006, 78, 2397-2404
27. Ding, Y.; Wang, Z.L. Structure analysis of nanowires and nanobelts by transmission electron microscopy. J. Phys. Chem. 2004, 108, 12280-12291
28. Comini, E.; Faglia, G.; Sberveglieri, G.; Pan, Z.; Wang, Z.L. Stable and highly sensitive gas sensors based on semiconducting oxide nanobelts. Appl. Phys. Lett. 2002, 81, 1869-1871
29. Bai, X.D.; Gao, P.X.; Wang, Z.L.; Wang, E.G. Dual-mode mechanical resonance of individual ZnO nanobelts. Appl. Phys. Lett. 2003, 28, 4806-4808
30. Bae, S.Y.; Seo, H.W. Vertically aligned sulfur-doped ZnO nanowires synthesized via chemical vapor deposition. J. Phys. Chem. 2004, 108, 5206-5210.
31. Kumar, S.A.; Chen, S.M. Nanostructured Zinc Oxide Particles in Chemically Modified Electrodes for Biosensor Applications. Anal. Lett. 2008, 41, 141-158
32. Xia, T.; Kovochich, M.; Liong, M.; Madler, L.; Gilbert, B.; Shi, H.; Yeh, J.I.; Zink, J.I.; Nel, A.E. Comparison of the mechanism of toxicity of zinc oxide and cerium oxide nanoparticles based on dissolution and oxidative stress properties. ACS Nano 2008, 2, 2121-2134
33. Lai, J.C.; Lai, M.B.; Jandhyam, S.; Dukhande, V.V.; Bhushan, A.; Daniels, C.K.; Leung, S.W. Exposure to titanium dioxide and other metallic oxide nanoparticles induces cytotoxicity on human neural cells and fibroblasts. Int. J. Nanomed. 2008, 3, 533-545
34. Lin, W.; Stayton, I.; Huang, Y.W.; Zhou, X.D.; Ma, Y. Cytotoxicity and cell membrane depolarization induced by aluminum oxide nanoparticles in human lung epithelial cells A549. Toxico. Environ. Chem. 2008, 90, 983-996
35. Lin, W.; Xu, Y.; Huang, C.C.; Ma, Y.; Shannon, K.B.; Chen, D.R.; Huang, Y.W. Toxicity of nano- and micro-sized ZnO particles in human lung epithelial cells. J. Nanopart. Res. 2009, 11, 25-39
36. Kang, S.G.; Brown, A.L.; Chung, J.H. Oxygen tension regulates the stability of insulin receptor substrate-1 (IRS-1) through caspase-mediated cleavage. J. Biol. Chem. 2007, 282, 6090-6097
37. Lin, W.; Huang, Y.W.; Zhou, X.D.; Ma, Y. In vitro toxicity of silica nanoparticles in human lung cancer cells. Toxico. Appl. Pharmacol. 2006, 217, 252-259
38. Lin, W.; Huang, Y.W.; Zhou, X.D.; Ma, Y. Toxicity of cerium oxide nanoparticles in human lung cancer cells. Int. J. Toxicol. 2006, 25, 451-457
39. Fahmy, B.; Cormier, S.A. Copper oxide nanoparticles induce oxidative stress and cytotoxicity in airway epithelial cells. Toxicol. in vitro 2009, 23, 1365-1371
40. 2 nanoparticles: Studies on a human monoblastoid cell line. Toxicol. in vitro 2008, 22, 1689-1696
41. Komatsu, T.; Tabata, M.; Kubo-Irie, M.; Shimizu, T.; Suzuki, K.; Nihei, Y.; Takeda, K. The effects of nanoparticles on mouse testis Leydig cells in vitro. Toxicol. in vitro 2008, 22, 1825-1831
42. Ivankovic, S.; Music, S.; Gotic, M.; Ljubesic, N. Cytotoxicity of nanosize V2O5 particles to selected fibroblast and tumor cells. Toxicol. in vitro 2006, 20, 286-294
43. Huang, C.C.; Aronstam, R.S.; Chen, D.R.; Huang, Y.W. Oxidative stress, calcium homeostasis, and altered gene expression in human lung epithelial cells exposed to ZnO nanoparticles. Toxicol. in vitro 2010, 24, 45-55
44. Sarkar, S.; Sharma, C.; Yog, R.; Periakaruppan, A.; Jejelowo, O.; Thomas, R.; Barrera, E.V.; Rice-Ficht, A.C.; Wilson, B.L.; Ramesh, G.T. Analysis of stress responsive genes induced by single-walled carbon nanotubes in BJ Foreskin cells. J. Nanosci. Nanotechnol. 2007, 7, 584-592
45. Braydich-Stolle, L.K.; Speshock, J.L.; Castle, A.; Smith, M.; Murdock, R.C.; Hussain, S.M. Nanosized aluminum altered immune function. ACS Nano 2010, 4, 3661-3670
46. Donaldson, K.; Borm, P.J.; 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
47. Limbach, L.K.; Li, Y.; Grass, R.N.; Brunner, T.J.; Hintermann, M.A.; Muller, M.; Gunther, D.; Stark, W.J. Oxide nanoparticle uptake in human lung fibroblasts: Effects of particle size, agglomeration, and diffusion at low concentrations. Environ. Sci. Technol. 2005, 39, 9370-9376
48. Nakase, I.; Niwa, M.; Takeuchi, T.; Sonomura, K.; Kawabata, N.; Koike, Y.; Takehashi, M.; Tanaka, S.; Ueda, K.; Simpson, J.C.; Jones, A.T.; Sugiura, Y.; Futaki, S. Cellular uptake of arginine-rich peptides: roles for macropinocytosis and actin rearrangement. Mol. Ther. 2004, 10, 1011-1022
49. Wadia, J.S.; Dowdy, S.F. Transmembrane delivery of protein and peptide drugs by TAT-mediated transduction in the treatment of cancer. Adv. Drug Deliv. Rev. 2005, 57, 579-596
50. Tyagi, M.; Rusnati, M.; Presta, M.; Giacca, M. Internalization of HIV-1 tat requires cell surface heparan sulfate proteoglycans. J. Biol. Chem. 2001, 276, 3254-3261
51. Bahattacharjee, S.; Haan, L.H.J.; Evers, N.M.; Jiang, X.; Marcelis, A.T.M.; Zuihof, H.; Rietjens, I.M.C.M.; Alink, G.M. 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
52. Kam, N.W.; Dai, H. Carbon nanotubes as intracellular protein transporters: Generality and biological functionality. J. Am. Chem. Soc. 2005, 127, 6021-6026
53. Xu, Y.; Liu, B.R.; Lee, H.J.; Shannon, K.B.; Winiarz, J.G.; Wang, T.C.; Chiang, H.J.; Huang, Y.W. Nona-arginine facilitates delivery of quantum dots into cells via multiple pathways. J. Biomed. Biotechnol. 2010, in press
54. Liu, B.R.; Li, J.F.; Lu, S.W.; Lee, H.J.; Shannon, K.B.; Huang, Y.W.; Aronstam, R.S. Cellular internalization of quantum dots noncovalently conjugated with arginine-rich intracellular delivery peptides. J. Nanosci. Nanotechnol. 2010, 10, 6534-6543
55. Ruan, G.; Agrawal, A.; Marcus, A.I.; Nie, S. Imaging and tracking of Tat peptide-conjugated quantum dots in living Cells: New Insights into nanoparticle uptake, intracellular transport, and vesicle shedding. J. Am. Chem. Soc. 2007, 129, 14759-14766
56. Krpetic, Z.; Porta, F.; Caneva, E.; Dal Santo, V.; Scari, G. Phagocytosis of biocompatible gold nanoparticles. Langmuir 2010, 26, 14799-14805
57. Jin, C.Y.; Zhu, B.S.; Wang, X.F.; Lu, Q.H. Cytotoxicity of titanium dioxide nanoparticles in mouse fibroblast cells. Chem. Res. Toxicol. 2008, 21, 1871-1877
58. Karlsson, H.L.; Cronholm, P.; Gustafsson, J.; Moller, L. Copper oxide nanoparticles are highly toxic: A comparison between metal oxide nanoparticles and carbon nanotubes. Chem. Res. Toxicol. 2008, 21, 1726-1732
59. Hu, X.; Cook, S.; Wang, P.; Hwang, H.M. In vitro evaluation of cytotoxicity of engineered metal oxide nanoparticles. Sci. Total. Environ. 2009, 407, 3070-3072
60. 2 to yeast Saccharomyces cerevisiae. Toxicol. in vitro 2009, 23, 1116-1122
61. Limbach, L.K.; Wick, P.; Manser, P.; Grass, R.N.; Stark, W.J. Exposure of engineered nanoparticles to human lung epithelial cells: Influence of chemical composition and catalytic activity on oxidative stress. Eviron. Sci. Technol. 2007, 41, 4158-4163. Materials 2010, 3 4858
62. Horie, M.; Nishio, K.; Fujita, K.; Endoh, S.; Miyauchi, A.; Saito, Y.; Iwahashi, H.; Yamamoto, K.; Murayama, H.; Nakano, H.; Nanashima, N.; Niki, E.; Yoshida, Y. Protein adsorption of ultrafine metal oxide and its influence on cytotoxicity toward cultured cells. Chem. Res. Toxicol. 2009, 22, 543-553
63. George, S.; Pokhrel, S.; Xia, T.; Gilbert, B.; Ji, Z.; Schowalter, M.; Rosenauer, A.; Damoiseaux, R.; Bradley, K.A.; Madler, L.; Nel, A.E. Use of a rapid cytotoxicity screening approach to engineer a safer zinc oxide nanoparticle through iron doping. ACS Nano 2010, 4, 15-29
64. Chan, K.; Kan, Y.W. Nrf2 is essential for protection against acute pulmonary injury in mice. Proc. Natl. Acad. Sci. USA 1999, 96, 12731-12736
65. Hayes, J.D.; Chanas, S.A.; Henderson, C.J.; McMahon, M.; Sun, C.; Moffat, G.J.; Wolf, C.R.; Yamamoto, M. The Nrf2 transcription factor contributes both to the basal expression of glutathione S-transferases in mouse liver and to their induction by the chemopreventive synthetic antioxidants, butylated hydroxyanisole and ethoxyquin. Biochem. Soc. Trans. 2000, 28, 33-41
66. Itoh, K.; Chiba, T.; Takahashi, S.; Ishii, T.; Igarashi, K.; Katoh, Y.; Oyake, T.; Hayashi, N.; Satoh, K.; Hatayama, I.; Yamamoto, M.; Nabeshima, Y. An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochem. Biophys. Res. Commun. 1997, 236, 313-322
67. Eom, H.J.; Choi, J. Oxidative stress of CeO2 nanoparticles via p38-Nrf-2 signaling pathway in human bronchial epithelial cell, Beas-2B. Toxicol. Lett. 2009, 187, 77-83
68. Aoki, Y.; Sato, H.; Nishimura, N.; Takahashi, S.; Itoh, K.; Yamamoto, M. Accelerated DNA adduct formation in the lung of the Nrf2 knockout mouse exposed to diesel exhaust. Toxicol. Appl. Pharmacol. 2001, 173, 154-160
69. Simmons, T.W.; Jamall, I.S. Relative importance of intracellular glutathione peroxidase and catalase in vivo for prevention of peroxidation to the heart. Cardiovasc. Res. 1989, 23, 774-779
70. Wang, S.; Kotamraju, S.; Konorev, E.; Kalivendi, S.; Joseph, J.; Kalyanaraman, B. Activation of nuclear factor-kappaB during doxorubicin-induced apoptosis in endothelial cells and myocytes is pro-apoptotic: The role of hydrogen peroxide. Biochem. J. 2002, 367, 729-740
71. Bhattacharya, K.; Davoren, M.; Boertz, J.; Schins, R.P.; Hoffmann, E.; Dopp, E. Titanium dioxide nanoparticles induce oxidative stress and DNA-adduct formation but not DNA-breakage in human lung cells. Part. Fibre. Toxicol. 2009, 6, 17
72. 2. Hum. Exp. Toxicol. 2009, 28, 339-352
73. Rahman, Q.; Lohani, M.; Dopp, E.; Pemsel, H.; Jonas, L.; Weiss, D.G.; Schiffmann, D. Evidence that ultrafine titanium dioxide induces micronuclei and apoptosis in Syrian hamster embryo fibroblasts. Environ. Health Perspect 2002, 110, 797-800
74. Jeng, H.A.; Swanson, J. Toxicity of metal oxide nanoparticles in mammalian cells. J. Environ. Sci. Health, Part A: Toxic/ Hazardous Subst. Environ. Eng. 2006, 41, 2699-2711
75. Stone, V.; Tuinman, M.; Vamvakopoulos, J.E.; Shaw, J.; Brown, D.; Petterson, S.; Faux, S.P.; Borm, P.; MacNee, W.; Michaelangeli, F.; Donaldson, K. Increased calcium influx in a monocytic cell line on exposure to ultrafine carbon black. Eur. Respir. J. 2000, 15, 297-303
76. Moller, W.; Brown, D.M.; Kreyling, W.G.; Stone, V. Ultrafine particles cause cytoskeletal dysfunctions in macrophages: Role of intracellular calcium. Part. Fibre. Toxicol. 2005, 2, 7
77. Aronstam, R.S.; Patil, P. Receptors on autonomic neurons and neuroeffector cells: Muscarinic receptors. In Encyclopedia of Neuroscience. Adelman, G., Smith, B., Eds.; Elsevier Press: Amstersam, The Netherlands, 2008
78. Smyth, J.T.; Dehaven, W.I.; Bird, G.S.; Putney, J.W., Jr. Ca2+-store-dependent and -independent reversal of Stim1 localization and function. J. Cell Sci. 2008, 121, 762-772
79. Putney, J.W., Jr. Recent breakthroughs in the molecular mechanism of capacitative calcium entry (with thoughts on how we got here). Cell Calcium 2007, 42, 103-110
80. 2: Role of the specific surface area and of surface methylation of the particles. Toxicol. Appl. Pharmacol. 2007, 222, 141-151
81. 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
82. Wu, W.; Samet, J.M.; Peden, D.B.; Bromberg, P.A. Phosphorylation of p65 is required for zinc oxide nanoparticle-induced interleukin 8 expression in human bronchial epithelial cells. Environ. Health Perspect 2010, 118, 982-987
83. Karthikeyan, B.; Kalishwaralal, K.; Sheikpranbabu, S.; Deepak, V.; Haribalaganesh, R.; Gurunathan, S. Gold nanoparticles downregulate VEGF-and IL-1beta-induced cell proliferation through Src kinase in retinal pigment epithelial cells. Exp. Eye Res. 2010, 91, 769-778
84. Kahn, E.; Baarine, M.; Pelloux, S.; Riedinger, J.M.; Frouin, F.; Tourneur, Y.; Lizard, G. Iron nanoparticles increase 7-ketocholesterol-induced cell death, inflammation, and oxidation on murine cardiac HL1-NB cells. Int. J. Nanomed. 2010, 5, 185-195
85. Liu, X.; Sun, J. Endothelial cells dysfunction induced by silica nanoparticles through oxidative stress via JNK/P53 and NF-kappaB pathways. Biomaterials. 2010, 31, 8198-8209
86. 2) nanoparticles. Toxicol. in vitro 2010, 24, 1002-1008
87. Park, E.J.; Kim, H.; Kim, Y.; Yi, J.; Choi, K.; Park, K. Inflammatory responses may be induced by a single intratracheal instillation of iron nanoparticles in mice. Toxicology 2010, 275, 65-71
88. Cho, W.S.; Cho, M.; Kim, S.R.; Choi, M.; Lee, J.Y.; Han, B.S.; Park, S.N.; Yu, M.K.; Jon, S.; Jeong, J. Pulmonary toxicity and kinetic study of Cy5.5-conjugated superparamagnetic iron oxide nanoparticles by optical imaging. Toxicol. Appl. Pharmacol. 2009, 239, 106-115
89. Nygaard, U.C.; Hansen, J.S.; Samuelsen, M.; Alberg, T.; Marioara, C.D.; Lovik, M. Single-walled and multi-walled carbon nanotubes promote allergic immune responses in mice. Toxicol. Sci. 2009, 109, 113-123.