Cytotoxicity and mitochondrial damage caused by silica nanoparticles

Toxicology in Vitro

Volumn 25, Issue 8, 2011, Pages 1619-1629

  Sun, Lei ^a   Li, Yang ^a   Liu, Xiaomei ^a   Jin, Minghua ^a   Zhang, Long ^a   Du, Zhongjun ^a   Guo, Caixia ^b   Huang, Peili ^b   Sun, Zhiwei ^a,b  

^a JILIN UNIVERSITY   (China)

^b CAPITAL MEDICAL UNIVERSITY   (China)

Author keywords

Cytotoxicity; Mitochondrial damage; Reactive oxygen species; Silica nanoparticle

Indexed keywords

NANOPARTICLE; REACTIVE OXYGEN METABOLITE; SILICON DIOXIDE;

APOPTOSIS; ARTICLE; CARCINOMA CELL; CELL ORGANELLE; CELL STRESS; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOPLASM; CYTOTOXICITY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DISPERSION; HUMAN; HUMAN CELL; INTRACELLULAR TRANSPORT; LIVER CELL CARCINOMA; MITOCHONDRIAL MEMBRANE; OXIDATIVE STRESS;

APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; CASPASE 3; CELL LINE, TUMOR; CYTOCHROMES C; HUMANS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICROSCOPY, ELECTRON, TRANSMISSION; MITOCHONDRIA; NANOPARTICLES; OXIDATIVE STRESS; PROTO-ONCOGENE PROTEINS C-BCL-2; REACTIVE OXYGEN SPECIES; SILICON DIOXIDE;

EID: 82655181893     PISSN: 08872333     EISSN: 18793177     Source Type: Journal    
DOI: 10.1016/j.tiv.2011.06.012     Document Type: Article

References (65)

1. Ahamed M., Posgai R., Gorey T.J., Nielsen M., Hussain S.M., Rowe J.J. Silver nanoparticles induced heat shock protein 70, oxidative stress and apoptosis in Drosophila melanogaster. Toxicol. Appl. Pharmacol. 2009, 242:263-269.
2. AshaRani P.V., Low Kah Mun G., Hande M.P., Valiyaveettil S. Cytotoxicity and genotoxicity of silver nanoparticles in human cells. ACS Nano 2009, 3:279-290.
3. Bayir H.R.S., Kagan V. Bench-to-bedside review: mitochondrial injury, oxidative stress and apoptosis - there is nothing more practical than a good theory. Critical Care 2008, 12:206.
4. Boya P., Andreau K., Poncet D., Zamzami N., Perfettini J.L., Metivier D., Ojcius D.M., Jaattela M., Kroemer G. Lysosomal membrane permeabilization induces cell death in a mitochondrion-dependent fashion. J. Exp. Med. 2003, 197:1323-1334.
5. Cartiera M.S., Johnson K.M., Rajendran V., Caplan M.J., Saltzman W.M. The uptake and intracellular fate of PLGA nanoparticles in epithelial cells. Biomaterials 2009, 30:2790-2798.
6. Cash T.P., Pan Y., Simon M.C. Reactive oxygen species and cellular oxygen sensing. Free Radic. Biol. Med. 2007, 43:1219-1225.
7. Cedervall T., Lynch I., Foy M., Berggard T., Donnelly S.C., Cagney G., Linse S., Dawson K.A. Detailed identification of plasma proteins adsorbed on copolymer nanoparticles. Angew Chem. Int. Ed. Engl. 2007, 46:5754-5756.
8. Chandra J., Samali A., Orrenius S. Triggering and modulation of apoptosis by oxidative stress. Free Radic. Biol. Med. 2000, 29:323-333.
9. Chang J.S., Chang K.L., Hwang D.F., Kong Z.L. In vitro cytotoxicitiy of silica nanoparticles at high concentrations strongly depends on the metabolic activity type of the cell line. Environ. Sci. Technol. 2007, 41:2064-2068.
10. Chithrani D.B., Dunne M., Stewart J., Allen C., Jaffray D.A. Cellular uptake and transport of gold nanoparticles incorporated in a liposomal carrier. Nanomed. Nanotechnol. Biol. Med. 2009, 6:161-169.
11. Choi J., Zheng Q., Katz H.R.S.E., Guilarte T.R. Silica-based nanoparticle uptake and cellular response by primary microglia. Environ. Health Perspect. 2010, 118:589-595.
12. Dutta D., Sundaram S.K., Teeguarden J.G., Riley B.J., Fifield L.S., Jacobs J.M., Addleman S.R., Kaysen G.A., Moudgil B.M., Weber T.J. Adsorbed proteins influence the biological activity and molecular targeting of nanomaterials. Toxicol. Sci. 2007, 100:303-315.
13. Eguchi Y., Shimizu S., Tsujimoto Y. Intracellular ATP levels determine cell death fate by apoptosis or necrosis. Cancer Res. 1997, 57:1835-1840.
14. Faklaris O., Joshi V., Irinopoulou T., Tauc P., Sennour M., Girard H.R.S., Gesset C., Arnault J.-C., Thorel A., Boudou J.-P., Curmi P.A., Treussart F. Photoluminescent diamond nanoparticles for cell labeling: study of the uptake mechanism in mammalian cells. ACS Nano 2009, 3:3955-3962.
15. Foucaud L., Wilson M.R., Brown D.M., Stone V. Measurement of reactive species production by nanoparticles prepared in biologically relevant media. Toxicol. Lett. 2007, 174:1-9.
16. Geiser M., Rothen-Rutishauser B., Kapp N., Schurch S., Kreyling W., Schulz H.R.S., Semmler M., Im Hof V., Heyder J., Gehr P. Ultrafine particles cross cellular membranes by nonphagocytic mechanisms in lungs and in cultured cells. Environ. Health Perspect. 2005, 113:1555-1560.
17. Hsin Y.-H.R.S., Chen C.-F., Huang S., Shih T.-S., Lai P.-S., Chueh P.J. The apoptotic effect of nanosilver is mediated by a ROS- and JNK-dependent mechanism involving the mitochondrial pathway in NIH3T3 cells. Toxicol. Lett. 2008, 179:130-139.
18. Huang X., Teng X., Chen D., Tang F., He J. The effect of the shape of mesoporous silica nanoparticles on cellular uptake and cell function. Biomaterials 2010, 31:438-448.
19. Jeong S.Y., Seol D.W. The role of mitochondria in apoptosis. BMB Rep. 2008, 41:11-22.
20. Jezek P., Hlavata L. Mitochondria in homeostasis of reactive oxygen species in cell, tissues, and organism. Int. J. Biochem. Cell Biol. 2005, 37:2478-2503.
21. Kim J.S., Yoon T.J., Yu K.N., Noh M.S., Woo M., Kim B.G., Lee K.H.R.S., Sohn B.H.R.S., Park S.B., Lee J.K., Cho M.H.R.S. Cellular uptake of magnetic nanoparticle is mediated through energy-dependent endocytosis in A549 cells. J. Vet. Sci. 2006, 7:321-326.
22. Kowaltowski A.J., de Souza-Pinto N.C., Castilho R.F., Vercesi A.E. Mitochondria and reactive oxygen species. Free Radic. Biol. Med. 2009, 47:333-343.
23. Kroemer G., Galluzzi L., Brenner C. Mitochondrial membrane permeabilization in cell death. Physiol. Rev. 2007, 87:99-163.
24. Kumar R., Roy I., Ohulchanskky T.Y., Vathy L.A., Bergey E.J., Sajjad M., Prasad P.N. In vivo biodistribution and clearance studies using multimodal organically modified silica nanoparticles. ACS Nano 2010, 4:699-708.
25. Li N., Sioutas C., Cho A., Schmitz D., Misra C., Sempf J., Wang M., Oberley T., Froines J., Nel A. Ultrafine particulate pollutants induce oxidative stress and mitochondrial damage. Environ. Health Perspect. 2003, 111:455-460.
26. Limbach L.K., Wick P., Manser P., Grass R.N., Bruinink A., Stark W.J. Exposure of engineered nanoparticles to human lung epithelial cells: influence of chemical composition and catalytic activity on oxidative stress. Environ. Sci. Technol. 2007, 41:4158-4163.
27. 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.
28. Lu C.W., Hung Y., Hsiao J.K., Yao M., Chung T.H.R.S., Lin Y.S., Wu S.H.R.S., Hsu S.C., Liu H.R.S.M., Mou C.Y., Yang C.S., Huang D.M., Chen Y.C. Bifunctional magnetic silica nanoparticles for highly efficient human stem cell labeling. Nano. Lett. 2007, 7:149-154.
29. Markovic Z., Todorovic-Markovic B., Kleut D., Nikolic N., Vranjes-Djuric S., Misirkic M., Vucicevic L., Janjetovic K., Isakovic A., Harhaji L., Babic-Stojic B., Dramicanin M., Trajkovic V. The mechanism of cell-damaging reactive oxygen generation by colloidal fullerenes. Biomaterials 2007, 28:5437-5448.
30. Maynard A.D., Aitken R.J., Butz T., Colvin V., Donaldson K., Oberdorster G., Philbert M.A., Ryan J., Seaton A., Stone V., Tinkle S.S., Tran L., Walker N.J., Warheit D.B. Safe handling of nanotechnology. Nature 2006, 444:267-269.
31. Meng H.R.S., Xia T., George S., Nel A.E. A predictive toxicological paradigm for the safety assessment of nanomaterials. ACS Nano 2009, 3:1620-1627.
32. Miura N., Shinohara Y. Cytotoxic effect and apoptosis induction by silver nanoparticles in HeLa cells. Biochem. Biophys. Res. Commun. 2009, 390:733-737.
33. Murdock R.C., Braydich-Stolle L., Schrand A.M., Schlager J.J., Hussain S.M. Characterization of nanomaterial dispersion in solution prior to in vitro exposure using dynamic light scattering technique. Toxicol. Sci. 2008, 101:239-253.
34. Nakamura M., Shono M., Ishimura K. Synthesis, characterization, and biological applications of multifluorescent silica nanoparticles. Anal. Chem. 2007, 79:6507-6514.
35. Nam H.R.S.Y., Kwon S.M., Chung H.R.S., Lee S.-Y., Kwon S.-H.R.S., Jeon H.R.S., Kim Y., Park J.H.R.S., Kim J., Her S., Oh Y.-K., Kwon I.C., Kim K., Jeong S.Y. Cellular uptake mechanism and intracellular fate of hydrophobically modified glycol chitosan nanoparticles. J. Controlled Release 2009, 135:259-267.
36. Nan A., Bai X., Son S.J., Lee S.B., Ghandehari H.R.S. Cellular uptake and cytotoxicity of silica nanotubes. Nano Lett. 2008, 8:2150-2154.
37. Napierska D., Thomassen L.C., Rabolli V., Lison D., Gonzalez L., Kirsch-Volders M., Martens J.A., Hoet P.H.R.S. Size-dependent cytotoxicity of monodisperse silica nanoparticles in human endothelial cells. Small 2009, 5:846-853.
38. Nel A., Xia T., Madler L., Li N. Toxic potential of materials at the nanolevel. Science 2006, 311:622-627.
39. Nishimori H.R.S., Kondoh M., Isoda K., Tsunoda S.-i., Tsutsumi Y., Yagi K. Histological analysis of 70-nm silica particles-induced chronic toxicity in mice. Eur. J. Pharm. Biopharm. 2009, 72:626-629.
40. Nishimori H.R.S., Kondoh M., Isoda K., Tsunoda S.-i., Tsutsumi Y., Yagi K. Silica nanoparticles as hepatotoxicants. Eur. J. Pharm. Biopharm. 2009, 72:496-501.
41. Oberdörster G., Oberdörster E., Oberdörster J. Nanotoxicology: an emerging discipline evolving from studies of ultrafine particles. Environ. Health Perspect. 2005, 113:823-839.
42. Ow H.R.S., Larson D.R., Srivastava M., Baird B.A., Webb W.W., Wiesner U. Bright and stable core-shell fluorescent silica nanoparticles. Nano Lett. 2005, 5:113-117.
43. Pan Y., Leifert A., Ruau D., Neuss S., Bornemann J., Schmid G., Brandau W., Simon U., Jahnen-Dechent W. Gold nanoparticles of diameter 1.4nm trigger necrosis by oxidative stress and mitochondrial damage. Small 2009, 5:2067-2076.
44. Park E.-J., Park K. Oxidative stress and pro-inflammatory responses induced by silica nanoparticles in vivo and in vitro. Toxicol. Lett. 2009, 184:18-25.
45. Park E.-J., Yi J., Chung K.-H.R.S., Ryu D.-Y., Choi J., Park K. Oxidative stress and apoptosis induced by titanium dioxide nanoparticles in cultured BEAS-2B cells. Toxicol. Lett. 2008, 180:222-229.
46. Patil S., Sandberg A., Heckert E., Self W., Seal S. Protein adsorption and cellular uptake of cerium oxide nanoparticles as a function of zeta potential. Biomaterials 2007, 28:4600-4607.
47. So S.J., Jang I.S., Han C.S. Effect of micro/nano silica particle feeding for mice. J. Nanosci. Nanotechnol. 2008, 8:5367-5371.
48. Stöber W., Fink A., Bohn E. Controlled growth of monodisperse silica spheres in the micron size range. J. Colloid Interf. Sci. 1968, 26:62-69.
49. Tantra R., Tompkins J., Quincey P. Characterisation of the de-agglomeration effects of bovine serum albumin on nanoparticles in aqueous suspension. Colloids Surf., B 2010, 75:275-281.
50. Taylor U., Klein S., Petersen S., Kues W., Barcikowski S., Rath D. Nonendosomal cellular uptake of ligand-free, positively charged gold nanoparticles. Cytometry Part A 2010, 77A:439-446.
51. Tsujimoto Y. Apoptosis and necrosis: intracellular ATP level as a determinant for cell death modes. Cell Death Differ. 1997, 4:429-434.
52. Unfried K., Albrecht C., Klotz L.-O., Von Mikecz A., Grether-Beck S., Schins R.P.F. Cellular responses to nanoparticles: target structures and mechanisms. Nanotoxicology 2007, 1:52-71.
53. Vallhov H.R.S., Gabrielsson S., Strømme M., Scheynius A., Garcia-Bennett A.E. Mesoporous silica particles induce size dependent effects on human dendritic cells. Nano Lett. 2007, 7:3576-3582.
54. Wang C., Youle R.J. The role of mitochondria in apoptosis. Annu. Rev. Genet. 2009, 43:95-118.
55. Wang F., Gao F., Lan M., Yuan H.R.S., Huang Y., Liu J. Oxidative stress contributes to silica nanoparticle-induced cytotoxicity in human embryonic kidney cells. Toxicol. In Vitro 2009, 23:808-815.
56. 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.
57. Xia T., Kovochich M., Liong M., Zink J.I., Nel A.E. Cationic polystyrene nanosphere toxicity depends on cell-specific endocytic and mitochondrial injury pathways. ACS Nano. 2007, 2:85-96.
58. Xie G., Sun J., Zhong G., Shi L., Zhang D. Biodistribution and toxicity of intravenously administered silica nanoparticles in mice. Arch. Toxicol. 2009, 84:183-190.
59. Yan J., Estévez M.C., Smith J.E., Wang K., He X., Wang L., Tan W. Dye-doped nanoparticles for bioanalysis. Nano. Today 2007, 2:44-50.
60. Ye Y., Liu J., Chen M., Sun L., Lan M. In vitro toxicity of silica nanoparticles in myocardial cells. Environ. Toxicol. Pharmacol. 2009, 29:131-137.
61. Ye Y., Liu J., Xu J., Sun L., Chen M., Lan M. Nano-SiO2 induces apoptosis via activation of p53 and Bax mediated by oxidative stress in human hepatic cell line. Toxicol. In Vitro 2010, 24:751-758.
62. Yen H.R.S.J., Hsu S.H.R.S., Tsai C.L. Cytotoxicity and immunological response of gold and silver nanoparticles of different sizes. Small 2009, 5:1553-1561.
63. Yu K., Grabinski C., Schrand A., Murdock R., Wang W., Gu B., Schlager J., Hussain S. Toxicity of amorphous silica nanoparticles in mouse keratinocytes. J. Nanopart. Res. 2009, 11:15-24.
64. Zhang L.W., Monteiro-Riviere N.A. Mechanisms of quantum dot nanoparticle cellular uptake. Toxicol. Sci. 2009, 110:138-155.
65. Zhu Y., Li W., Li Q., Li Y., Li Y., Zhang X., Huang Q. Effects of serum proteins on intracellular uptake and cytotoxicity of carbon nanoparticles. Carbon 2009, 47:1351-1358.