Assessment of cultured fish hepatocytes for studying cellular uptake and (eco)toxicity of nanoparticles
Tessa M. Scown A F , Rhys M. Goodhead A F , Blair D. Johnston A , Julian Moger B , Mohammed Baalousha C , Jamie R. Lead C , Ronny van Aerle A , Taisen Iguchi D and Charles R. Tyler A EA Ecotoxicology and Aquatic Biology Research Group, Hatherly Laboratories, University of Exeter, Prince of Wales Road, Exeter, EX4 4PS, UK.
B Biomedical Physics Group, School of Physics, University of Exeter, Stocker Road, Exeter, EX4 4QL, UK.
C School of Geography, Earth, and Environmental Sciences, University of Birmingham, Edgbaston, Birmingham, B15 2TT, UK.
D Okazaki Institute for Integrative Bioscience, National Institute for Basic Biology, 5-1 Higashiyama, Myodaiji, Okazaki, Aichi 444-8787, Japan.
E Corresponding author. Email: c.r.tyler@exeter.ac.uk
F Co-first authors. Email: t.m.scown@exeter.ac.uk; r.m.goodhead@exeter.ac.uk
Environmental Chemistry 7(1) 36-49 https://doi.org/10.1071/EN09125
Submitted: 2 October 2009 Accepted: 22 December 2009 Published: 22 February 2010
Environmental context. The production and application of engineered nanoparticles is rapidly increasing, and development of suitable models for screening nanoparticles for possible toxic effects is essential to protect aquatic organisms and support the sustainable development of the nanotechnology industry. Here, the suitability of isolated rainbow trout hepatocytes was assessed for high through-put toxicity screening of nanoparticles and for studying uptake of nanoparticles into cells.
Abstract. Relatively little is known regarding the fate and possible toxic effects of engineered nanoparticles (ENPs) in the aquatic environment. We assessed the suitability of isolated trout hepatocytes for high throughput toxicity screening of ENPs, exposing them to a variety of metal and metal oxide nanoparticles and their bulk counterparts. We found no effects of the ENPs on cell viability, or on lipid peroxidation, with the exception of exposure to ZnO nanoparticles, or on glutathione-S-transferase (GST) levels, for exposure concentrations up to 500 μg mL–1. All ENPs, however, were internalised in the cultured hepatocytes, as shown by coherent anti-Stokes Raman scattering (CARS) as an imaging technique. Our findings suggest that fish hepatocyte cultures are suitable for studies investigating the cellular uptake of ENPs, but they do not appear to be sensitive to ENP exposure and thus not a good in vitro model for nanoparticle toxicity screening.
Additional keywords: coherent anti-Stokes Raman scattering, in vitro, metal oxides, rainbow trout, silver.
Acknowledgements
This work was supported by the Natural Environment Research Council [NER/S/A/2005/13319 NE/D004942/1, NE/C002369/1 and the UK Environment Agency to C.R.T. and R.v.A.]. The NERC Facility FENAC (Birmingham, UK) is acknowledged for help with nanoparticle characterisation. We thank Chris Pook for help with the GST assay, Dr Anke Lange and Dr Lisa Bickley for help with the hepatocyte isolations. All investigations were performed in accordance with the Animals (Scientific Procedures) Act, 1986 (UK).
[1]
[2]
R. J. Aitken ,
M. Q. Chaudhry ,
A. B. A. Boxall ,
H. Hull ,
Manufacture and use of nanomaterials: current status in the UK and global trends.
Occup. Med. 2006
, 56, 300.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
[3]
[4]
I. Beck-Speier ,
N. Dayal ,
E. Karg ,
K. L. Maier ,
G. Schumann ,
H. Schulz ,
M. Semmler ,
S. Takenaka ,
et al. Oxidative stress and lipid mediators induced in alveolar macrophages by ultrafine particles.
Free Radic. Biol. Med. 2005
, 38, 1080.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[5]
J.-R. Gurr ,
A. S. S. Wang ,
C.-H. Chen ,
K.-Y. Jan ,
Ultrafine titanium dioxide particles in the absence of photoactivation can induce oxidative damage to human bronchial epithelial cells.
Toxicology 2005
, 213, 66.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[6]
C. M. Sayes ,
R. Wahi ,
P. A. Kurian ,
Y. P. Liu ,
J. L. West ,
K. D. Ausman ,
D. B. Warheit ,
V. L. Colvin ,
Correlating nanoscale titania structure with toxicity: a cytotoxicity and inflammatory response study with human dermal fibroblasts and human lung epithelial cells.
Toxicol. Sci. 2006
, 92, 174.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[7]
M. Geiser ,
B. Rothen-Rutishauser ,
N. Kapp ,
S. Schurch ,
W. Kreyling ,
H. Schulz ,
M. Semmler ,
V. Im Hoff ,
J. Heyder ,
P. Gehr ,
Ultrafine particles cross cellular membranes by nonphagocytic mechanisms in lungs and cultured cells.
Environ. Health Perspect. 2005
, 113, 1555.
| PubMed |
[8]
Z. Pan ,
W. Lee ,
L. Slutsky ,
R. A. Clark ,
N. Pernodet ,
M. H. Rafailovich ,
Adverse effects of titanium dioxide nanoparticles on human dermal fibroblasts and how to protect cells.
Small 2009
, 5, 511.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[9]
S. Lu ,
R. Duffin ,
C. Poland ,
P. Daly ,
F. Murphy ,
E. Drost ,
W. MacNee ,
V. Stone ,
K. Donaldson ,
Efficacy of simple short-term in vitro assays for predicting the potential of metal oxide nanoparticles to cause pulmonary inflammation.
Environ. Health Perspect. 2009
, 117, 241.
|
CAS |
PubMed |
[10]
L. Bickley ,
A. Lange ,
M. Winter ,
C. Tyler ,
Fish hepatocyte cultures as an alternative to in vivo tests for screening oestrogen receptor active chemicals.
Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2007
, 146, S72.
| Crossref | GoogleScholarGoogle Scholar |
[11]
M. Strmac ,
T. Braunbeck ,
Cytological and biochemical effects of a mixture of 20 pollutants on isolated rainbow trout (Oncorhynchus mykiss) hepatocytes.
Ecotoxicol. Environ. Saf. 2002
, 53, 293.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[12]
R. F. Domingos ,
N. Tufenkji ,
K. J. Wilkinson ,
Aggregation of titanium dioxide nanoparticles: role of a fulvic acid.
Environ. Sci. Technol. 2009
, 43, 1282.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[13]
K. F. Soto ,
A. Carrasco ,
T. G. Powell ,
K. M. Garza ,
L. E. Murr ,
Comparative in vitro cytotoxicity of some manufactureed nanoparticulate materials characterized by transmission electron microscopy.
J. Nanopart. Res. 2005
, 7, 145.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
[14]
A. Petri-Fink ,
B. Steitz ,
A. Finka ,
J. Salaklang ,
H. Hofmann ,
Effect of cell media on polymer coated superparamagnetic iron oxide nanoparticles (SPIONs): colloidal stability, cytotoxicity, and cellular uptake studies.
Eur. J. Pharm. Biopharm. 2008
, 68, 129.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[15]
Q.-L. Fan ,
K.-G. Neoh ,
E.-T. Kang ,
B. Shuter ,
S.-C. Wang ,
Solvent-free atom transfer radical polymerization for the preparation of poly(poly(ethyleneglycol) monomethacrylate)-grafted Fe3O4 nanoparticles: synthesis, characterization and cellular uptake.
Biomaterials 2007
, 28, 5426.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[16]
J. Cheng ,
C. M. Chan ,
L. M. Veca ,
W. L. Poon ,
P. K. Chan ,
L. Qu ,
Y.-P. Sun ,
S. H. Cheng ,
Acute and long-term effects after single loading of functionalized multi-walled carbon nanotubes into zebrafish (Danio rerio).
Toxicol. Appl. Pharmacol. 2009
, 235, 216.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[17]
K. J. Lee ,
P. D. Nallathamby ,
L. M. Browning ,
C. J. Osgood ,
X.-H. Xu ,
In vivo imaging of transport and biocompatibility of single silver nanoparticles in early development of zebrafish embryos.
ACS Nano 2007
, 1, 133.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[18]
J.-Y. Roh ,
S. J. Sim ,
J. Yi ,
K. Park ,
K. H. Chung ,
D.-Y. Ryu ,
J. Choi ,
Ecotoxicity of silver nanoparticles on the soil nematode Caenohabditis elegans using functional ecotoxicogenomics.
Environ. Sci. Technol. 2009
, 43, 3933.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[19]
J. Moger ,
B. D. Johnston ,
C. R. Tyler ,
Imaging metal oxide nanoparticles in biological structures with CARS microscopy.
Opt. Express 2008
, 16, 3408.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[20]
C. Risso-de Faverney ,
A. Devaux ,
M. Lafaurie ,
J. P. Girard ,
R. Rahmani ,
Toxic effects of wasteaters collected at upstream and downstream sites of a purification station in cultures of rainbow trout hepatocytes.
Arch. Environ. Contam. Toxicol. 2001
, 41, 129.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[21]
B. V. Derjaguin ,
L. D. Landau ,
Theory of the stability of strongly charged lyophobic sols and of the adhesion of strongly charged particles in solutions of electrolytes.
Acta Phys. Chim URSS 1941
, 14, 633.
[22]
[23]
G. Flouriot ,
G. Monod ,
Y. Valotaire ,
A. Devaux ,
J.-P. Cravedi ,
Xenobiotic metabolizing enzyme activities in aggregate culture of rainbow trout hepatocytes.
Mar. Environ. Res. 1995
, 39, 293.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
[24]
J.-P. Cravedi ,
A. Paris ,
G. Monad ,
A. Devaux ,
G. Flouriot ,
Y. Valotaire ,
Maintenance of cytochrome P450 content and phase I and phase II enzyme activities in trout hepatocytes cultured as pheroidal aggregates.
Comp. Biochem. Physiol. Part Toxicol. Pharmacol. 1996
, 113, 241.
[25]
A. Simon ,
B. Gouget ,
M. Mayne ,
N. Herlin ,
C. Reynaud ,
J. Degrouard ,
M. Carriere ,
In vitro investigation of TiO2, Al2O3, Au nanoparticles and mutli-walled carbon nanotubes cyto- and genotoxicity on lung, kidney cells and hepatocytes.
Toxicol. Lett. 2007
, 172, S36.
| Crossref | GoogleScholarGoogle Scholar |
[26]
S. M. Hussain ,
K. L. Hess ,
J. M. Gearhart ,
K. T. Geiss ,
J. J. Schlager ,
In vitro toxicity of nanoparticles in BRL 3A rat liver cells.
Toxicol. In Vitro 2005
, 19, 975.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[27]
F. Gagné ,
D. Maysinger ,
C. André ,
C. Blaise ,
Cytotoxicity of aged cadmium-telluride quantum dots to rainbow trout hepatocytes.
Nanotoxicology 2008
, 2, 113.
| Crossref | GoogleScholarGoogle Scholar |
[28]
J. G. Teeguarden ,
P. M. Hinderliter ,
G. Orr ,
B. D. Thrall ,
J. G. Pounds ,
Particokinetics in vitro: dosimetry considerations for in vitro nanoparticle toxicity assessments.
Toxicol. Sci. 2006
, 95, 300.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[29]
L. K. Limbach ,
Y.-C. Li ,
R. N. Grass ,
T. J. Brunner ,
M. A. Hintermann ,
M. Muller ,
D. Gunther ,
W. J. Stark ,
Oxide nanoparticle uptake in human lung fibroblasts: effects of particle size, agglomeration and diffusion at low concentrations.
Environ. Sci. Technol. 2005
, 39, 9370.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[30]
H. A. Jeng ,
J. Swanson ,
Toxicity of metal oxide nanoparticles in mammalian cells.
J. Environ. Sci. Health Part A Tox. Hazard. Subst. Environ. Eng. 2006
, 41, 2699.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
[31]
H. Yang ,
C. Liu ,
D. Yang ,
H. Zhang ,
Z. Zhuge Xi ,
Comparative study of cytotoxicity, oxidative stress and genotoxicity induced by four typical nanomaterials: the role of particle size, shape and composition.
J. Appl. Toxicol. 2009
, 29, 69.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[32]
S. J. Kemp ,
A. J. Thorley ,
J. Gorelik ,
M. J. Seckl ,
M. J. O’Hare ,
A. Arcaro ,
Y. Korchev ,
P. Goldstraw ,
T. D. Tetley ,
Immortalization of human alveolar epithelial cells to investigate nanoparticle uptake.
Am. J. Respir. Cell Mol. Biol. 2008
, 39, 591.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[33]
R. D. Handy ,
T. B. Henry ,
T. M. Scown ,
B. D. Johnston ,
C. R. Tyler ,
Manufactured nanoparticles: their uptake and effects on fish – a mechanistic analysis.
Ecotoxicology 2008
, 17, 396.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[34]
L. G. Rodriguez ,
S. J. Lockett ,
G. R. Holtom ,
Coherent anti-Stokes Raman scattering microscopy: a biological review.
Cytometry A 2006
, 69A, 779.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
[35]
T. M. Scown ,
R. van Aerle ,
B. D. Johnston ,
S. Cumberland ,
J. R. Lead ,
R. Owen ,
C. R. Tyler ,
High doses of intravenously administered titanium dioxide nanoparticles accumulate in the kidneys of rainbow trout but with no observable impairment of renal function.
Toxicol. Sci. 2009
, 109, 372.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[36]
V. Sharma ,
R. K. Shukla ,
N. Saxena ,
D. Parmar ,
M. Das ,
A. Dhawan ,
DNA damaging potential of zinc oxide nanoparticles in human epidermal cells.
Toxicol. Lett. 2009
, 185, 211.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[37]
X. Zhu ,
J. Wang ,
X. Zhang ,
Y. Chang ,
Y. Chen ,
The impact of ZnO nanoparticle aggregates on the embryonic development of zebrafish (Danio rerio).
Nanotechnology 2009
, 20, 195103.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[38]
E. Navarro ,
F. Piccapietra ,
B. Wagner ,
F. Marconi ,
R. Kaegi ,
N. Odzak ,
L. Sigg ,
R. Behra ,
Toxicity of silver nanoparticles to Chlamydomonas reinhardtii.
Environ. Sci. Technol. 2008
, 42, 8959.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[39]
N. M. Franklin ,
N. J. Rogers ,
S. C. Apte ,
G. E. Batley ,
G. E. Gadd ,
P. S. Casey ,
Comparative toxicity of nanoparticulate ZnO, bulk ZnO, and ZnCl2 to a freshwater microalga (Pseudokirchneriella subcapitata): the importance of particle solubility.
Environ. Sci. Technol. 2007
, 41, 8484.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[40]
M. F. Rahman ,
J. Wang ,
T. A. Patterson ,
U. T. Saini ,
B. L. Robinson ,
G. D. Newport ,
R. C. Murdock ,
J. J. Schlager ,
S. M. Hussain ,
S. F. Ali ,
Expression of genes related to oxidative stress in the mouse brain after exposure to silver-25 nanoparticles.
Toxicol. Lett. 2009
, 187, 15.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[41]
W. F. Vevers ,
A. N. Jha ,
Genotoxic and cytotoxic potential of titanium dioxide (TiO2) nanoparticles on fish cells in vitro.
Ecotoxicology 2008
, 17, 410.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[42]
E. J. Park ,
J. Yi ,
Y. H. Chung ,
D.-Y. Ryu ,
J. Choi ,
K. Park ,
Oxidative stress and apoptosis induced by titanium dioxide nanoparticles in cultured BEAS-2B cells.
Toxicol. Lett. 2008
, 180, 222.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[43]
S. Arora ,
J. Jain ,
J. M. Rajwade ,
K. M. Paknikar ,
Cellular responses induced by silver nanoparticles: in vitro studies.
Toxicol. Lett. 2008
, 179, 93.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[44]
C. Carlson ,
A. M. Schrand ,
L. K. Braydich-Stolle ,
K. L. Hess ,
R. L. Jones ,
J. J. Schlager ,
S. M. Hussain ,
Unique cellular interaction of silver nanoparticles: size-dependent generation of reactive oxygen species.
J. Phys. Chem. B 2008
, 112, 13608.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[45]
Y.-H. Hsin ,
C.-F. Chen ,
S. Huang ,
T.-S. Shih ,
P.-S. Lai ,
P. J. Chueh ,
The apoptotic effect of nanosilver is mediated by a ROS- and JNK-dependent mechanism involving the mitochondrial pathway in NIH3T3 cells.
Toxicol. Lett. 2008
, 179, 130.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[46]
E.-J. Park ,
J. Choi ,
Y.-K. Park ,
K. Park ,
Oxidative stress induced by cerium oxide nanoparticles in cultured BEAS-2B cells.
Toxicology 2008
, 245, 90.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[47]
J. F. Reeves ,
S. J. Davies ,
N. J. F. Dodd ,
A. N. Jha ,
Hydroxyl radicals (OH) are associated with titanium dioxide (TiO2) nanoparticle-induced cytotoxicity and oxidative DNA damage in fish cells.
Mutat. Res. 2008
, 640, 113.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[48]
D. A. Symonds ,
I. Merchenthaler ,
J. A. Flaws ,
Methoxychlor and estradiol induce oxidative stress DNA damage in the mouse ovarian surface epithelium.
Toxicol. Sci. 2008
, 105, 182.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[49]
P. Hoarau ,
G. Garello ,
M. Gnassia-Barelli ,
M. Romeo ,
J.-P. Girard ,
Purification and partial characterization of seven glutathione-S-transferase isoforms from the clam Ruditapes decussatus.
Eur. J. Biochem. 2002
, 269, 4359.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[50]
A. Meister ,
Glutathione metabolism and its selective modification.
J. Biol. Chem. 1988
, 263, 17205.
|
CAS |
PubMed |
[51]
A. Jemec ,
D. Drobne ,
M. Remškar ,
K. Sepčić ,
T. Tišler ,
Effects of ingested nano-sized titanium dioxide on terrestrial isopods (Porcellio scaber).
Environ. Toxicol. Chem. 2008
, 27, 1904.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[52]
D. Drobne ,
A. Jemec ,
Z. Pipan Tkalec ,
In vivo screening to determine hazards of nanoparticles: Nanosized TiO2.
Environ. Pollut. 2009
, 157, 1157.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[53]
S. Pandey ,
S. Parvez ,
R. A. Ansari ,
M. Ali ,
M. Kaur ,
F. Hayat ,
F. Ahmad ,
S. Raisuddin ,
Effects of exposure to multiple trace metals on biochemical, histological and ultrastructural features of gills of a freshwater fish, Channa punctata Bloch.
Chem. Biol. Interact. 2008
, 174, 183.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[54]
P. A. Walker ,
N. R. Bury ,
C. Hogstrand ,
Influence of culture conditions on metal-induced responses in a cultured rainbow trout gill epithelium.
Environ. Sci. Technol. 2007
, 41, 6505.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[55]
E. M. Mager ,
H. Wintz ,
C. D. Vulpe ,
K. V. Brix ,
M. Grosell ,
Toxicogenomics of water chemistry influence on chronic lead exposure to the fathead minnow (Pimephales promelas).
Aquat. Toxicol. 2008
, 87, 200.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[56]
M. Perez-Lopez ,
M. C. Novoa-Valinas ,
M. J. Melgar-Riol ,
Glutathione S-transferase cytosolic isoforms as biomarkers of polychlorinated biphenyl (Arochlor-1254) experimental contamination in rainbow trout.
Toxicol. Lett. 2002
, 136, 97.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[57]
M. Pérez-López ,
P. Rouimi ,
L. Debrauwer ,
J. P. Cravedi ,
Glutathione-S-transferase subunits pattern in rainbow trout isolated hepatocytes.
Mar. Environ. Res. 1998
, 46, 385.
| Crossref |
[58]
J. E. Klaunig ,
Establishment of fish hepatocyte cultures for use in in-vitro carcinogenicity studies.
Natl. Cancer Inst. Monogr. 1984
, 65, 163.
|
CAS |
PubMed |
[59]
C. R. Gioda ,
L. A. Lissner ,
A. Pretto ,
J. B. T. da Rocha ,
M. R. C. Schetinger ,
J. R. Neto ,
V. M. Morsch ,
V. L. Loro ,
Exposure to sublethal concentrations of Zn(II) and Cu(II) changes biochemical parameters in Leporinus obtusidens
Chemosphere 2007
, 69, 170.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[60]
O. Fırat ,
H. Y. Çogun ,
S. Aslanyavrusu ,
F. Kargin ,
Antioxidant responses and metal accumulation in tissues of Nile tilapia Oreochromis niloticus under Zn, Cd and Zn plus Cd exposures.
J. Appl. Toxicol. 2009
, 29, 295.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[61]
G. Atli ,
O. Alptekin ,
S. Tukel ,
M. Canli ,
Response of catalase activity to Ag+, Cd2+, Cr6+, Cu2+ and Zn2+ in five tissues of freshwater fish Oreochromis niloticus
Comp. Biochem. Physiol. Part Toxicol. Pharmacol. 2006
, 143, 218.
| Crossref | GoogleScholarGoogle Scholar |
[62]
M. K. Yeo ,
M. Kang ,
Effects of nanometre sized silver materials on biological toxicity during zebrafish embryogenesis.
Bull. Korean Chem. Soc. 2008
, 29, 1179.
|
CAS |
[63]
L. K. Bickley ,
A. Lange ,
M. J. Winter ,
C. R. Tyler ,
Evaluation of a carp primary hepatocyte culture system for screening chemicals for oestrogenic activity.
Aquat. Toxicol. 2009
, 94, 195.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[64]
S. M. Baksi ,
J. M. Frazier ,
Review: isolated fish hepatocytes – model systems for toxicology research.
Aquat. Toxicol. 1990
, 16, 229.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
[65]
J. H. Hanks ,
R. E. Wallace ,
Relation of oxygen and temperature in the preservation of tissues by refrigeration.
Proc. Soc. Exp. Biol. Med. 1949
, 71, 196.
|
CAS |
PubMed |
[66]
S. J. Stohs ,
D. Bagchi ,
Oxidative mechanisms in the toxicity of metal ions.
Free Radic. Biol. Med. 1995
, 18, 321.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[67]
N. Ercal ,
H. Gurer-Orhan ,
N. Aykin-Burns ,
Toxic metals and oxidative stress. Part I: Mechanisms involved in metal-induced oxidative damage.
Curr. Top. Med. Chem. 2001
, 1, 529.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[68]
E. Conner ,
R. Margulies ,
M. Liu ,
S. W. Smilen ,
R. F. Porges ,
C. Kwon ,
Vaginal delivery and serum markers of ischemia/reperfusion injury.
Int. J. Gynaecol. Obstet. 2006
, 94, 96.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[69]
Z. Bouraoui ,
M. Banni ,
J. Ghedira ,
C. Clerandeau ,
H. Guerbej ,
J. F. Narbonne ,
H. Boussetta ,
Acute effects of cadmium on liver phase I and phase II enzymes and metallothionein accumulation on sea bream Sparus aurata
Fish Physiol. Biochem. 2008
, 34, 201.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[70]
L. Canesi ,
A. Viarengo ,
C. Leonzio ,
M. Filippelli ,
G. Gallo ,
Heavy metals and glutathione metabolism in mussel tissues.
Aquat. Toxicol. 1999
, 46, 67.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
[71]
C. M. Wood ,
C. Hogstrand ,
F. Galvez ,
R. S. Munger ,
The physiology of waterborne silver toxicity in freshwater rainbow trout (Oncorhynchus mykiss) 1. The effects of ionic Ag+.
Aquat. Toxicol. 1996
, 35, 93.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
[72]
A. E. Porter ,
M. Gass ,
K. Muller ,
J. N. Skepper ,
P. Midgley ,
M. Welland ,
Visualizing the uptake of C-60 to the cytoplasm and nucleaus of human monocyte-derived macrophage cells using energy-filtered transmission electron microscopy and electron tomography.
Environ. Sci. Technol. 2007
, 41, 3012.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
