The role of iron redox state in the genotoxicity of ultrafine superparamagnetic iron oxide nanoparticles

Biomaterials

Volumn 33, Issue 1, 2012, Pages 163-170

  Singh, Neenu ^a   Jenkins, Gareth J S ^a   Nelson, Bryant C ^b   Marquis, Bryce J ^b   Maffeis, Thierry G G ^a   Brown, Andy P ^c   Williams, Paul M ^a   Wright, Chris J ^a   Doak, Shareen H ^a  

^a SWANSEA UNIVERSITY   (United Kingdom)

^b NATIONAL INSTITUTE OF STANDARDS AND TECHNOLOGY   (United States)

^c UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

Biocompatibility; Genotoxicity; Iron oxide nanoparticles; Metal ion release; Oxidation

Indexed keywords

BIOMEDICAL APPLICATIONS; CELLULAR UPTAKE; DNA DAMAGES; GENOTOXICITIES; HUMAN EXPOSURES; IRON OXIDE NANOPARTICLES; METAL ION RELEASE; OXIDATIVE DNA DAMAGE; PHYSICO-CHEMICALS; POTENTIAL MECHANISM; REDOX STATE; SUPERPARAMAGNETIC IRON OXIDE NANOPARTICLES; TARGETED DRUG DELIVERY; ULTRAFINE;

BIOCOMPATIBILITY; DRUG DELIVERY; IRON; MAGNETIC FLUIDS; MEDICAL APPLICATIONS; MEDICAL NANOTECHNOLOGY; METAL IONS; NANOPARTICLES; OXIDATION; SUPERPARAMAGNETISM; SURFACE CHEMISTRY;

IRON OXIDES;

SUPERPARAMAGNETIC IRON OXIDE NANOPARTICLE;

ARTICLE; BIOCOMPATIBILITY; CONTROLLED STUDY; DNA DAMAGE; GENOTOXICITY; HUMAN; HUMAN CELL; NANOFABRICATION; NANOMEDICINE; OXIDATION REDUCTION STATE; PRIORITY JOURNAL;

CELL LINE; DNA DAMAGE; FERRIC COMPOUNDS; GAS CHROMATOGRAPHY-MASS SPECTROMETRY; HUMANS; MAGNETITE NANOPARTICLES; MICROSCOPY, ELECTRON, TRANSMISSION; OXIDATION-REDUCTION; PHOTOELECTRON SPECTROSCOPY;

EID: 82855172067     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2011.09.087     Document Type: Article

References (48)

1. Bulte J.W., Douglas T., Witwer B., Zhang S.C., Strable E., Lewis B.K., et al. Magnetodendrimers allow endosomal magnetic labeling and in vivo tracking of stem cells. Nat Biotechnol 2001, 19(12):1141-1147.
2. Bulte J.W., Kraitchman D.L. Iron oxide MR contrast agents for molecular and cellular imaging. NMR Biomed 2004, 17(7):484-499.
3. Gupta A.K., Gupta M. Synthesis and surface engineering of iron oxide nanoparticles for biomedical applications. Biomaterials 2005, 26(18):3995-4021.
4. Pamme N., Wilhelm C. Continuous sorting of magnetic cells via on-chip free-flow magnetophoresis. Lab Chip 2006, 6(8):974-980.
5. Weinstein J.S., Varallyay C.G., Dosa E., Gahramanov S., Hamilton B., Rooney W.D., et al. Superparamagnetic iron oxide nanoparticles: diagnostic magnetic resonance imaging and potential therapeutic applications in neurooncology and central nervous system inflammatory pathologies, a review. J Cereb Blood Flow Metab 2010, 30(1):15-35.
6. Soenen S.J., De Cuyper M. Assessing iron oxide nanoparticle toxicity in vitro: current status and future prospects. Nanomedicine (Lond) 2010, 5(8):1261-1275.
7. Veiseh O., Gunn J.W., Zhang M. Design and fabrication of magnetic nanoparticles for targeted drug delivery and imaging. Adv Drug Deliv Rev 2010, 62(3):284-304.
8. Song M.M., Song W.J., Bi H., Wang J., Wu W.L., Sun J., et al. Cytotoxicity and cellular uptake of iron nanowires. Biomaterials 2010, 31(7):1509-1517.
9. Apopa P.L., Qian Y., Shao R., Guo N.L., Schwegler-Berry D., Pacurari M., et al. Iron oxide nanoparticles induce human microvascular endothelial cell permeability through reactive oxygen species production and microtubule remodeling. Part Fibre Toxicol 2009, 6:1.
10. Auffan M., Decome L., Rose J., Orsiere T., De Meo M., Briois V., et al. In vitro interactions between DMSA-coated maghemite nanoparticles and human fibroblasts: a physicochemical and cyto-genotoxical study. Environ Sci Technol 2006, 40(14):4367-4373.
11. Berry C.C., Charles S., Wells S., Dalby M.J., Curtis A.S. The influence of transferrin stabilised magnetic nanoparticles on human dermal fibroblasts in culture. Int J Pharm 2004, 269(1):211-225.
12. Pisanic T.R., Blackwell J.D., Shubayev V.I., Finones R.R., Jin S. Nanotoxicity of iron oxide nanoparticle internalization in growing neurons. Biomaterials 2007, 28(16):2572-2581.
13. Hamm B., Staks T., Taupitz M., Maibauer R., Speidel A., Huppertz A., et al. Contrast-enhanced MR imaging of liver and spleen: first experience in humans with a new superparamagnetic iron oxide. J Magn Reson Imaging 1994, 4(5):659-668.
14. Dias A.M., Hussain A., Marcos A.S., Roque A.C. A biotechnological perspective on the application of iron oxide magnetic colloids modified with polysaccharides. Biotechnol Adv 2011, 29(1):142-155.
15. Laurent S., Forge D., Port M., Roch A., Robic C., Vander Elst L., et al. Magnetic iron oxide nanoparticles: synthesis, stabilization, vectorization, physicochemical characterizations, and biological applications. Chem Rev 2008, 108(6):2064-2110.
16. 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(9):1726-1732.
17. Karlsson H.L., Gustafsson J., Cronholm P., Moller L. Size-dependent toxicity of metal oxide particles-a comparison between nano- and micrometer size. Toxicol Lett 2009, 188(2):112-118.
18. Hanini A., Schmitt A., Kacem K., Chau F., Ammar S., Gavard J. Evaluation of iron oxide nanoparticle biocompatibility. Int J Nanomedicine 2011, 6:787-794.
19. 4 nanoparticles with six different mammalian cell lines. J Nanoparticle Res 2010, 13(1):199-212.
20. Muller K., Skepper J.N., Posfai M., Trivedi R., Howarth S., Corot C., et al. Effect of ultrasmall superparamagnetic iron oxide nanoparticles (Ferumoxtran-10) on human monocyte-macrophages in vitro. Biomaterials 2007, 28(9):1629-1642.
21. Dizdaroglu M., Laval J., Boiteux S. Substrate specificity of the Escherichia coli endonuclease III: excision of thymine- and cytosine-derived lesions in DNA produced by radiation-generated free radicals. Biochemistry 1993, 32(45):12105-12111.
22. Reddy P., Jaruga P., O'Connor T., Rodriguez H., Dizdaroglu M. Overexpression and rapid purification of Escherichia coli formamidopyrimidine-DNA glycosylase. Protein Expr Purif 2004, 34(1):126-133.
23. Griffiths S.M., Singh N., Jenkins G.J., Williams P.M., Orbaek A.W., Barron A.R., et al. Dextran coated ultrafine superparamagnetic iron oxide nanoparticles: compatibility with common fluorometric and colorimetric dyes. Anal Chem 2011, 83(10):3778-3785.
24. Hondow N., Harrington J., Brydson R., Doak S.H., Singh N., Manshian B., et al. STEM mode in the SEM: a practical tool for nanotoxicology. Nanotoxicology 2011, 5(2):215-227.
25. Doak S.H., Griffiths S.M., Manshian B., Singh N., Williams P.M., Brown A.P., et al. Confounding experimental considerations in nanogenotoxicology. Mutagenesis 2009, 24(4):285-293.
26. Lunov O., Syrovets T., Buchele B., Jiang X., Rocker C., Tron K., et al. The effect of carboxydextran-coated superparamagnetic iron oxide nanoparticles on c-Jun N-terminal kinase-mediated apoptosis in human macrophages. Biomaterials 2010, 31(19):5063-5071.
27. Fellows M.D., O'Donovan M.R., Lorge E., Kirkland D. Comparison of different methods for an accurate assessment of cytotoxicity in the in vitro micronucleus test. II: practical aspects with toxic agents. Mutat Res 2008, 655(1-2):4-21.
28. Ellard S., Mohammed Y., Dogra S., Wolfel C., Doehmer J., Parry J.M. The use of genetically engineered V79 Chinese hamster cultures expressing rat liver CYP1A1, 1A2 and 2B1 cDNAs in micronucleus assays. Mutagenesis 1991, 6(6):461-470.
29. Jaruga P., Kirkali G., Dizdaroglu M. Measurement of formamidopyrimidines in DNA. Free Radic Biol Med 2008, 45(12):1601-1609.
30. Riemer J., Hoepken H.H., Czerwinska H., Robinson S.R., Dringen R. Colorimetric ferrozine-based assay for the quantitation of iron in cultured cells. Anal Biochem 2004, 331(2):370-375.
31. Arbab A.S., Wilson L.B., Ashari P., Jordan E.K., Lewis B.K., Frank J.A. A model of lysosomal metabolism of dextran coated superparamagnetic iron oxide (SPIO) nanoparticles: implications for cellular magnetic resonance imaging. NMR Biomed 2005, 18(6):383-389.
32. Soenen S.J., Himmelreich U., Nuytten N., Pisanic T.R., Ferrari A., De Cuyper M. Intracellular nanoparticle coating stability determines nanoparticle diagnostics efficacy and cell functionality. Small 2010, 6(19):2136-2145.
33. Clogston J.D., Patri A.K. Zeta potential measurement. Methods Mol Biol 2011, 697:63-70.
34. Boyer C., Whittaker M.R., Bulmus V., Liu J., Davis T.P. The design and utility of polymer-stabilized iron oxide nanoparticles for nanomedicine applications. NPG Asia Mater 2010, 2:23-30.
35. Corchero J.L., Villaverde A. Biomedical applications of distally controlled magnetic nanoparticles. Trends Biotechnol 2009, 27(8):468-476.
36. Lynch I., Cedervall T., Lundqvist M., Cabaleiro-Lago C., Linse S., Dawson K.A. The nanoparticle-protein complex as a biological entity; a complex fluids and surface science challenge for the 21st century. Adv Colloid Interface Sci 2007, 134-135:167-174.
37. Singh N., Jenkins G.J., Asadi R., Doak S.H. Potential toxicity of superparamagnetic iron oxide nanoparticles (SPION). Nano Rev 2010, 10.3402/nano.v1i0.5358.
38. Wilhelm C., Billotey C., Roger J., Pons J.N., Bacri J.C., Gazeau F. Intracellular uptake of anionic superparamagnetic nanoparticles as a function of their surface coating. Biomaterials 2003, 24(6):1001-1011.
39. Xing X., He X., Peng J., Wang K., Tan W. Uptake of silica-coated nanoparticles by HeLa cells. J Nanosci Nanotechnol 2005, 5(10):1688-1693.
40. Mahmoudi M., Simchi A., Imani M., Shokrgozar M.A., Milani A.S., Hafeli U.O., et al. A new approach for the in vitro identification of the cytotoxicity of superparamagnetic iron oxide nanoparticles. Colloids Surf B Biointerfaces 2010, 75(1):300-309.
41. Petersen E., Nelson B. Mechanisms and measurements of nanomaterial-induced oxidative damage to DNA. Anal Bioanal Chem 2010, 398(2):613-650.
42. Wang L., Zhang J., Zheng Y., Yang J., Zhang Q., Zhu X. Bioeffects of CdTe quantum dots on human umbilical vein endothelial cells. J Nanosci Nanotechnol 2010, 10(12):8591-8596.
43. Shukla R.K., Sharma V., Pandey A.K., Singh S., Sultana S., Dhawan A. ROS-mediated genotoxicity induced by titanium dioxide nanoparticles in human epidermal cells. Toxicol in Vitro 2011, 25(1):231-241.
44. Karlsson H.L., Holgersson A., Moller L. Mechanisms related to the genotoxicity of particles in the subway and from other sources. Chem Res Toxicol 2008, 21(3):726-731.
45. Kruszewski M., Iwanenko T. Labile iron pool correlates with iron content in the nucleus and the formation of oxidative DNA damage in mouse lymphoma L5178Y cell lines. Acta Biochim Pol 2003, 50(1):211-215.
46. Petrat F., de Groot H., Rauen U. Subcellular distribution of chelatable iron: a laser scanning microscopic study in isolated hepatocytes and liver endothelial cells. Biochem J 2001, 356(Pt 1):61-69.
47. Gackowski D., Kruszewski M., Bartlomiejczyk T., Jawien A., Ciecierski M., Olinski R. The level of 8-oxo-7,8-dihydro-2'-deoxyguanosine is positively correlated with the size of the labile iron pool in human lymphocytes. J Biol Inorg Chem 2002, 7(4-5):548-550.
48. Chourpa I., Douziech-Eyrolles L., Ngaboni-Okassa L., Fouquenet J.F., Cohen-Jonathan S., Souce M., et al. Molecular composition of iron oxide nanoparticles, precursors for magnetic drug targeting, as characterized by confocal Raman microspectroscopy. Analyst 2005, 130(10):1395-1403.