Neoplastic cell response to tiopronin-coated gold nanoparticles

Nanomedicine: Nanotechnology, Biology, and Medicine

Volumn 9, Issue 2, 2013, Pages 264-273

  Cui, Lei ^a   Zahedi, Payam ^a   Saraceno, Justin ^a   Bristow, Robert ^a,b   Jaffray, David ^a,b   Allen, Christine ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b PRINCESS MARGARET HOSPITAL   (Canada)

Author keywords

Cancer; Cellular accumulation; Cytotoxicity; Gold nanoparticles; Reactive oxygen species

Indexed keywords

24 HOURS; ANTICANCER ACTIVITIES; BIOLOGICAL RESPONSE; CANCER; CANCER CELL LINES; CELL ACCUMULATION; CELL LINES; CELLULAR ACCUMULATION; ENDOSOMES; EXPOSURE-TIME; GLUTATHIONES; GOLD NANOPARTICLES; HELA CELL; IN-VITRO; NEOPLASTIC CELLS; REACTIVE OXYGEN SPECIES; ROS GENERATIONS; SURVIVING FRACTIONS; TIOPRONIN;

CELL CULTURE; CYTOTOXICITY; DISEASES; METAL NANOPARTICLES; OXYGEN;

GOLD;

ACETYLCYSTEINE; ANTIOXIDANT; CYSTEINE; GLUTATHIONE; GOLD NANOPARTICLE; REACTIVE OXYGEN METABOLITE; TIOPRONIN;

ANTINEOPLASTIC ACTIVITY; ARTICLE; ATOMIC EMISSION SPECTROMETRY; BIOCOMPATIBILITY; CANCER CELL; CANCER CELL CULTURE; CELL VACUOLE; CELLULAR DISTRIBUTION; CLONOGENESIS; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG DELIVERY SYSTEM; DRUG EFFICACY; DRUG EXPOSURE; DRUG MECHANISM; DRUG RESPONSE; ENDOSOME; FEMALE; HUMAN; HUMAN TISSUE; IN VITRO STUDY; INCUBATION TIME; LYSOSOME; OXIDATIVE STRESS; PROTON NUCLEAR MAGNETIC RESONANCE; TRANSMISSION ELECTRON MICROSCOPY;

ANIMALS; ANTIOXIDANTS; CELL LINE, TUMOR; CELL SURVIVAL; GLUTATHIONE; GOLD; HUMANS; MICE; NANOPARTICLES; NEOPLASMS; REACTIVE OXYGEN SPECIES; TIOPRONIN;

EID: 84873730090     PISSN: 15499634     EISSN: 15499642     Source Type: Journal    
DOI: 10.1016/j.nano.2012.05.016     Document Type: Article

References (50)

1. Shi J.J., Votruba A.R., Farokhzad O.C., Langer R. Nanotechnology in drug delivery and tissue engineering: from discovery to applications. Nano Lett 2010, 10:3223-3230.
2. Sperling R.A., Rivera gil P., Zhang F., Zanella M., Parak W.J. Biological applications of gold nanoparticles. Chem Soc Rev 2008, 37:1896-1908.
3. Huang X.H., Jain P.K., El-Sayed I.H., El-Sayed M.A. Gold nanoparticles: interesting optical properties and recent applications in cancer diagnostic and therapy. Nanomedicine (Lond.) 2007, 2:681-693.
4. Hainfeld J.F., Dilmanian F.A., Slatkin D.N., Smilowitz H.M. Radiotherapy enhancement with gold nanoparticles. J Pharm Pharmacol 2008, 60:977-985.
5. Jain P.K., Lee K.S., El-Sayed I.H., El-Sayed M.A. Calculated absorption and scattering properties of gold nanoparticles of different size, shape, and composition: applications in biological imaging and biomedicine. J Phys Chem B 2006, 110:7238-7248.
6. Zhang G., Yang Z., Lu W., Zhang R., Huang Q., Tian M., et al. Influence of anchoring ligands and particle size on the colloidal stability and in vivo biodistribution of polyethylene glycol-coated gold nanoparticles in tumor-xenografted mice. Biomaterials 2009, 30:1928-1936.
7. Hainfeld J.F., Slatkin D.N., Smilowitz H.M. The use of gold nanoparticles to enhance radiotherapy in mice. Phys Med Biol 2004, 49:N309-N315.
8. Chithrani B.D., Ghazani A.A., Chan W.C.W. Determining the size and shape dependence of gold nanoparticle uptake into mammalian cells. Nano Lett 2006, 6:662-668.
9. Mironava T., Hadjiargyrou M., Simon M., Jurukovski V., Rafailovich M.H. Gold nanoparticles cellular toxicity and recovery: effect of size, concentration and exposure time. Nanotoxicology 2010, 4:120-137.
10. Malugin A., Ghandehari H. Cellular uptake and toxicity of gold nanoparticles in prostate cancer cells: a comparative study of rods and spheres. J Appl Toxicol 2010, 30:212-217.
11. Li S.D., Huang L. Pharmacokinetics and biodistribution of nanoparticles. Mol Pharm 2008, 5:496-504.
12. Goodman T.T., Chen J.Y., Matveev K., Pun S.H. Spatio-temporal modeling of nanoparticle delivery to multicellular tumor spheroids. Biotechnol Bioeng 2008, 101:388-399.
13. Gupta A.K., Gupta M. Synthesis and surface engineering of iron oxide nanoparticles for biomedical applications. Biomaterials 2005, 26:3995-4021.
14. Otsuka H., Nagasaki Y., Kataoka K. PEGylated nanoparticles for biological and pharmaceutical applications. Adv Drug Deliv Rev 2003, 55:403-419.
15. Johnston H.J., Hutchison G., Christensen F.M., Peters S., Hankin S., Stone V. A review of the in vivo and in vitro toxicity of silver and gold particulates: particle attributes and biological mechanisms responsible for the observed toxicity. Crit Rev Toxicol 2010, 40:328-346.
16. Templeton A.C., Chen S.W., Gross S.M., Murray R.W. Water-soluble, isolable gold clusters protected by tiopronin and coenzyme A monolayers. Langmuir 1999, 15:66-76.
17. Rodriguez J.A., Dvorak J., Jirsak T., Liu G., Hrbek J., Aray Y., et al. Coverage effects and the nature of the metal-sulfur bond in S/Au(111): high-resolution photoemission and density-functional studies. J Am Chem Soc 2003, 125:276-285.
18. Templeton A.C., Cliffel D.E., Murray R.W. Redox and fluorophore functioanalization of water-soluble, tiopronin-protected gold clusters. J Am Chem Soc 1999, 121:7081-7089.
19. de la Fuente J.M., Berry C.C. Tat peptide as an efficient molecule to translocate gold nanoparticles into the cell nucleus. Bioconjug Chem 2005, 16:1176-1180.
20. Cai X., Chen H.H., Wang C.L., Chen S.T., Lai S.F., Chien C.C., et al. Imaging the cellular uptake of tiopronin-modified gold nanoparticles. Anal Bioanal Chem 2011, 401:809-816.
21. De Souza R., Zahedi P., Moriyama E.H., Allen C.J., Wilson B.C., Piquette-Miller M. Continuous docetaxel chemotherapy improves therapeutic efficacy in murine models of ovarian cancer. Mol Cancer Ther 2010, 9:1820-1830.
22. Franken N.A., Rodermond H.M., Stap J., Haveman J., van Bree C. Clonogenic assay of cells in vitro. Nat Protoc 2006, 1:2315-2319.
23. Wang H., Joseph J.A. Quantifying cellular oxidative stress by dichlorofluorescein assay using microplate reader. Free Radic Biol Med 1999, 27:612-616.
24. Lévy R., Shaheen U., Cesbron Y., Sée V. Gold nanoparticles delivery in mammalian live cells: a critical review. Nano Rev 2010, 1:1-18.
25. Hussain I., Graham S., Wang Z., Tan B., Sherrington D.C., Rannard S.P., et al. Size-controlled synthesis of near-monodisperse gold nanoparticles in the 1-4 nm range using polymeric stabilizers. J Am Chem Soc 2005, 127:16398-16399.
26. Daniel M.C., Astruc D. Gold nanoparticles: assembly, supramolecular chemistry, quantum-size-related properties, and applications toward biology, catalysis, and nanotechnology. Chem Rev 2004, 104:293-346.
27. Haiss W., Thanh N.T., Aveyard J., Fernig D.G. Determination of size and concentration of gold nanoparticles from UV-vis spectra. Anal Chem 2007, 79:4215-4221.
28. Albanese A., Chan W.C. Effect of gold nanoparticle aggregation on cell uptake and toxicity. ACS Nano 2011, 5:5478-5489.
29. Chithrani B.D., Chan W.C.W. Elucidating the mechanism of cellular uptake and removal of protein-coated gold nanoparticles of different sizes and shapes. Nano Lett 2007, 7:1542-1550.
30. Roa W., Zhang X., Guo L., Shaw A., Hu X., Xiong Y., et al. Gold nanoparticle sensitize radiotherapy of prostate cancer cells by regulation of the cell cycle. Nanotechnology 2009, 20:375101.
31. Kim J.A., Aberg C., Salvati A., Dawson K.A. Role of cell cycle on the cellular uptake and dilution of nanoparticles in a cell population. Nat Nanotechnol 2012, 7:62-68.
32. Summers H. Bionanoscience: nanoparticles in the life of a cell. Nat Nanotechnol 2012, 7:9-10.
33. 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.
34. Nel A., Xia T., Madler L., Li N. Toxic potential of materials at the nanolevel. Science 2006, 311:622-627.
35. Lin W., Huang Y.W., Zhou X.D., Ma Y. In vitro toxicity of silica nanoparticles in human lung cancer cells. Toxicol Appl Pharmacol 2006, 217:252-259.
36. Carlson C., Hussain S.M., Schrand A.M., Braydich-Stolle L.K., Hess K.L., Jones R.L., et al. Unique cellular interaction of silver nanoparticles: size-dependent generation of reactive oxygen species. J Phys Chem B 2008, 112:13608-13619.
37. Xia T., Kovochich M., Brant J., Hotze M., Sempf J., Oberley T., et al. 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.
38. Pan Y., Leifert A., Ruau D., Neuss S., Bornemann J., Schmid G., et al. Gold nanoparticles of diameter 1.4 nm trigger necrosis by oxidative stress and mitochondrial damage. Small 2009, 5:2067-2076.
39. Alkilany A.M., Murphy C.J. Toxicity and cellular uptake of gold nanoparticles: what we have learned so far?. J Nanopart Res 2010, 12:2313-2333.
40. LeBel C.P., Ischiropoulos H., Bondy S.C. Evaluation of the probe 2',7'-dichlorofluorescein as an indicator of reactive oxygen species formation and oxidative stress. Chem Res Toxicol 1992, 5:227-231.
41. Martin K.R., Barrett J.C. Reactive oxygen species as double-edged swords in cellular processes: low-dose cell signaling versus high-dose toxicity. Hum Exp Toxicol 2002, 21:71-75.
42. Schafer F.Q., Buettner G.R. Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radic Biol Med 2001, 30:1191-1212.
43. Parmentier C., Wellman M., Leroy P., Nicolas A. Measurement of glutathione redox status and related enzyme activities in cultured cells by liquid chromatography. Biologie prospective 1997, 389-394. John Libbey CIC, Paris. M.M. Galteau, P. Delwoide, G. Siest, J. Henny (Eds.).
44. Zhao Y., Gu X., Ma H., He X., Liu M., Ding Y. Association of glutathione level and cytotoxicity of gold nanoparticles in lung cancer cells. J Phys Chem 2011, 115:12797-12802.
45. Burkitt M.J., Wardman P. Cytochrome c is a potent catalyst of dichlorofluorescein oxidation: implications for the role of reactive oxygen species in apoptosis. Biochem Biophys Res Commun 2001, 282:329-333.
46. Hirsch T., Marchetti P., Susin S.A., Dallaporta B., Zamzami N., Marzo I., et al. The apoptosis-necrosis paradox. Apoptogenic proteases activated after mitochondrial permeability transition determine the mode of cell death. Oncogene 1997, 15:1573-1581.
47. Kerksick C., Willoughby D. The antioxidant role of glutathione and N-acetyl-cysteine supplements and exercise-induced oxidative stress. J Int Soc Sports Nutr 2005, 2:38-44.
48. Gao W., Xu K., Ji L., Tang B. Effect of gold nanoparticles on glutathione depletion-induced hydrogen peroxide generation and apoptosis in HL7702 cells. Toxicol Lett 2011, 205:86-95.
49. Hussain S.M., Hess K.L., Gearhart J.M., Geiss K.T., Schlager J.J. In vitro toxicity of nanoparticles in BRL 3A rat liver cells. Toxicol in Vitro 2005, 19:975-983.
50. Radu M., Munteanu M.C., Petrache S., Serban A.I., Dinu D., Hermenean A., et al. Depletion of intracellular glutathione and increased lipid peroxidation mediate cytotoxicity of hematite nanoparticles in MRC-5 cells. Acta Biochim Pol 2010, 57:355-360.