In vitro toxicity of amorphous silica nanoparticles in human colon carcinoma cells

Nanotoxicology

Volumn 7, Issue 3, 2012, Pages 274-293

  Gehrke, Helge ^a   Frühmesser, Anne ^b   Pelka, Joanna ^a   Esselen, Melanie ^b   Hecht, Lena L ^b   Blank, Holger ^b   Schuchmann, Heike P ^b   Gerthsen, Dagmar ^b   Marquardt, Clarissa ^b   Diabaté, Silvia ^b   Weiss, Carsten ^b   Marko, Doris ^a  

^a UNIVERSITY OF VIENNA   (Austria)

^b KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

Author keywords

Cellular uptake; Cytotoxicity; Glutathione; Particle agglomeration; Proliferation

Indexed keywords

DNA; GLUTATHIONE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; NANOPARTICLE; REACTIVE OXYGEN METABOLITE; SILICON DIOXIDE; TRANSCRIPTION FACTOR NRF2;

ARTICLE; CARCINOMA CELL; CELL PROLIFERATION; COLON CARCINOMA; CONTROLLED STUDY; CYTOTOXICITY; FETAL CALF SERUM; HUMAN; HUMAN CELL; IN VITRO STUDY; PARTICLE SIZE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

EID: 84876015373     PISSN: 17435390     EISSN: 17435404     Source Type: Journal    
DOI: 10.3109/17435390.2011.652207     Document Type: Article

References (76)

1. Abdelmohsen K, Gerber PA, von Montfort C, Sies H, Klotz LO. 2003. Epidermal growth factor receptor is a common mediator of quinone- induced signaling leading to phosphorylation of connexin-43: role of glutathione and tyrosine phosphatases. J Biol Chem 278 (40):38360-38367.
2. Araujo JA, Barajas B, Kleinman M, Wang X, Bennet BJ, Gong KW, et al. 2008. Ambient particulate pollutans in the ultrafine range promote early atherosclerosis and systemic oxidative stress. Circ Res 102:589- 596.
3. Arts JH, Muijser H, Duistermaat E, Junker K, Kuper CF. 2007. Five-day inhalation toxicity study of three types of synthetic amorphous silicas in Wistar rats and post-exposure evaluations for up to 3 months. Food Chem Toxicol 45(10):1856-1867.
4. Ashwood P, Thompson RPH, Powell JJ. 2007. Fine particles that adsorb lipopolysaccharide via bridging calcium cations may mimic bacterial pathogenicity towards cells. Exp Biol Med 232(1):107-117.
5. Barnes CA, Elsaesser A, Arkusz J, Smok A, Palus J, Lesniak A, et al. 2008. Reproducible Comet Assay of amorphous silica nanoparticles detects no genotoxicity. Nano Lett 8:3069-3074.
6. Bharali DJ, Klejbor I, Stachowiak EK, Dutta P, Roy I, Kaur N, et al. 2005. Organically modified silica nanoparticles: a nonviral vector for in vivo gene delivery and expression in the brain. Proc Natl Acad Sci USA 102(32):11539-11544.
7. Bockmann J, Lahl H, Eckert T, Unterhalt B. 2000. Titanium blood levels of dialysis patients compared to healthy volunteers. Pharmazie 55:468.
8. Boiteux S, Gajewski E, Laval J, Dizdaroglu M. 1992. Substrate specificity of the Escherichia coli FPG protein (formamidopyrimidine- DNA glycosylase): excision of purine lesions in DNA produced by ionizing radiation or photosensitization. Biochemistry 31:106-110
9. Boraschi D, Lucarelli M, Gatti AM, Savarino G, Quattroni P, Martinelli L, et al. 2004. Innate defence functions of macrophages can be biased by nano-sized ceramic and metallic particles. Eur Cytokine Netw 15(4):339-346.
10. Borm PJA, Robbins D, Haubold S, Kuhlbusch T, Fissan H, Donaldson K, et al. 2006. The potential risks of nanomaterials: a review carried out for ECETOC. Part Fibre Toxicol 3:11.
11. Brunauer S, Emmett PH, Teller E. 1938. Adsorption of Gases in Multimolecular Layers. J Am Chem Soc 60(2):309-319.
12. Chang J-S, Chang KLB, Hwang D-F, Kong Z-L. 2007. In vitro cytotoxicity of silica nanoparticles at high concentrations strongly depends on metabolic activity type of the cell line. Environ Sci Technol 41:2064-2068.
13. Chaudhry Q, Scotter M, Blackburn J, Ross B, Boxall A, Castle L, et al. 2008. Applications and implications of nanotechnologies for the food sector. Food Addit Contam 25:241-258.
14. Chen M, von Mikecz A. 2005. Formation of nucleoplasmic protein aggregates impairs nuclear function in response to SiO2 nanoparticles. Exp Cell Res 305(1):51-62.
15. Churg A, Gilks B, Dai J. 1999. Induction of fibrogenic mediators by fine and ultrafine titanium dioxide in rat tracheal explants. Am J Physiol 277(5 Pt 1):L975-L982.
16. Conner SD, Schmid SL. 2003. Regulated portals of entry into the cell. Nature 422(6927):37-44.
17. Dekkers S, Krystek P, Peters RJB, Lankveld DPK, Bokkers BGH, van Hoeven-Arentzen PH, et al. 2011. Presence and risks of nanosilica in food products. Nanotoxicology 5(3):393-405.
18. Desai MP, Labhasetwar V, Amidon GL, Levy RJ. 1996. Gastrointestinal uptake of biodegradable microparticles: effect of particle size. Pharm Res 13(12):1838-1845.
19. Dinkova-Kostova AT, Baird L2011. The cytoprotective role of the Keap1-Nrf2 pathway. Arch Toxicol 85(4):241-272.
20. Donaldson K, Tran L, Jimenez LA, Duffin R, Newby DE, Mills N, et al.2005. Combustion-derived nanoparticles: a review of their toxicology following inhalation exposure. Part Fibre Toxicol 2:10
21. Dordick JS, Vertegel AA, Siegel RW. 2004. Silica nanoparticle size influences the structure and enzymatic activity of adsorbed lysozyme. Langmuir 20(16):6800-6807.
22. Elder A, Yang H, Gwiazda R, Teng X, Thurston S, He H, Oberdörster G. 2007. Testing Nanomaterials of Unknown Toxicity: An Example Based on Platinum Nanoparticles of Different Shapes. Advanced Materials 19(20):3124-3129.
23. Forman HJ, Zhang H, Rinna A. 2009. Glutathione: overview of its protective roles, measurement, and biosynthesis. Mol Aspects Med 30(1-2):1-12.
24. Gehrke H, Pelka J, Hartinger CG, Blank H, Bleimund F, Schneider R, et al. 2011. Platinum nanoparticles and their cellular uptake and DNA platination at non-cytotoxic concentrations. Arch Toxicol 85(7):799-812.
25. Gerloff K, Albrecht C, Boots AW, Förster I, Shins RPF. 2009. Cytotoxicity and oxidative DNA damage by nanoparticles in human intestinal Caco-2 cells. Nanotox 3:335-364.
26. Haselsberger K, Peterson DC, Thomas D, Darling JL. 1996. Assay of anticancer drugs in tissue culture: comparison of a tetrazoliumbased assay and a protein binding dye assay in short-term cultures derived from human malignant glioma. Anticancer Drugs 7(3):331-338
27. Herrlich P, Karin M, Weiss C. 2008. Supreme EnLIGHTenment: damage recognition and signaling in the mammalian UV response. Mol Cell 29(3):279-290.
28. Hillyer JF, Albrecht RM. 2001. Gastrointestinal persorption and tissue distribution of differently sized colloidal gold nanoparticles. J Pharm Sci 90(12):1927-1936.
29. Hirsch LR, Stafford RJ, Bankson JA, Sershen SR, Rivera B, Price RE, et al. 2003. Nanoshell-mediated near-infrared thermal therapy of tumors under magnetic resonance guidance. Proc Natl Acad Sci USA 100: 13549-13554.
30. Houghton P, Fang R, Techatanawat I, Steventon G, Hylands PJ, Lee CC. 2007. The sulphorhodamine (SRB) assay and other approaches to testing plant extracts and derived compounds for activities related to reputed anticancer activity. Methods 42(4):377-387.
31. Huang H-C, Nguyen T, Pickett CB. 2002. Phosphorylation of Nrf2 at Ser-40 by Protein Kinase C Regulates Antioxidant Response Element-mediated Transcription. J Biol Chem 277(45):42769-42774.
32. Jaiswal M, LaRusso NF, Burgart LJ, Gores GJ. 2000. Inflammatory cytokines induce DNA damage and inhibit DNA repair in cholangiocarcinoma cells by a nitric oxide-dependent mechanism. Cancer Res 60(1):184-190.
33. Jani PU, McCarthy DE, Florence AT. 1994. Titanium dioxide (rutile) particles uptake from the rat GI tract and translocation to systemic organs after oral administration. J Pharm 105:157-168.
34. Jin Y, Kannan S, Wu M, Zhao JX. 2007. Toxicity of luminescent silica nanoparticles to living cells. Chem Res Toxicol 20:1126-1133.
35. Jonsson BH, Lundqvist M, Sethson I. 2004. Protein adsorption onto silica nanoparticles: Conformational changes depend on the particles' curvature and the protein stability. Langmuir 20(24):10639-10647.
36. Kane RS, Stroock AD. 2007. Nanobiotechnology: protein-nanomaterial interactions. Biotechnol Prog 23(2):316-319.
37. Karlsson HL. 2010. The comet assay in nanotoxicology research. Anal Bioanal Chem 398(2):651-666.
38. Kern M, Tjaden Z, Ngiewih Y, Puppel N, Will F, Dietrich H, et al. 2005. Inhibitors of the epidermal growth factor receptor in apple juice extract. Mol Nutr Food Res 49:317-328.
39. Kuroda E, Ishii Ken J, Uematsu S, Ohata K, Coban C, Akira S, et al. 2011. Silica crystals and aluminum salts regulate the production of prostaglandin in macrophages via NALP3 Inflammasome-Independent Mechanisms. Immunity 34(4):514-526.
40. Kwak MK, Manandhar S, Cho JM, Kim JA, Kensler TW. 2007. Induction of Nrf2-regulated genes by 3H-1, 2-dithiole-3-thione through the ERK signaling pathway in murine keratinocytes. Eur J Pharm 577(1-3):17-27.
41. Limbach LK, Wick P, Manser P, Grass RN, Bruinink A, Stark WJ. 2007. Exposure of engineered nanoparticles to human lung epithelial cells: Influence of chemical composition and catalytic activity on oxidative stress. Environ Sci Technol 41(11):4158-4163.
42. Lin W, Huang Y, Zhou X-D, Ma Y. 2006. In vitro toxicity of silica nanoparticles in human lung cancer cells. Toxicol Appl Pharmacol 217:252-259.
43. Lomer MC, Thompson RP, Powell JJ. 2002. Fine and ultrafine particles of the diet: influence on the mucosal immune response and association with Crohn's disease. Proc Nutr Soc 61:123-130.
44. Monopoli MP, Walczyk D, Campbell A, Elia G, Lynch I, Bombelli FB, et al. 2011. Physical-chemical aspects of protein corona: relevance to in vitro and in vivo biological impacts of nanoparticles. J Am Chem Soc 133(8):2525-2534.
45. Nedel F, Soki FN, Conde MCM, Zeitlin BD, Tarquinio SBC, Nör JE, et al. 2011. Comparative analysis of two colorimetric assays in dental pulp cell density. Int Endod J 44(1):59-64.
46. Nel A, Xia T, Madler L, Li N. 2006. Toxic potential of materials at the nanolevel. Science 311(5761):622-627.
47. Oberdörster G, Oberdörster E, Oberdörster J. 2005. Nanotoxicology: an emerging discipline evolving from studies of ultrafine particles. Environ Health Perspect 113:823-839.
48. Park E-J, Park K. 2009. Oxidative stress and pro-inflammatory response induced ny silica nanoparticles in vivo and in vitro. Toxicol Lett 184:18-25.
49. Pearson G, Robinson F, Gibson TB, Xu B-E, Karandikar M, Berman K, et al. 2001. Mitogen-activated protein(MAP) kinase pathways: regulation and physiological functions. Endocr Rev 22:153-183.
50. Pelka J, Gehrke H, Esselen M, Türk M, Crone M, Bräse S, et al. 2009. Cellular uptake of platinum nanoparticles in human colon carcinoma cells and their impact on cellular redox systems and dna integrity. Chem Res Toxicol 22:649-659.
51. Perry CC, Roach P, Farrar D. 2006. Surface tailoring for controlled protein adsorption: effect of topography at the nanometer scale and chemistry. J Am Chem Soc 128(12):3939-3945.
52. Peters K, Unger RE, Kirkpatrick CJ, Gatti AM, Monari E. 2004. Effects of nano-scaled particles on endothelial cell function in vitro: studies on viability, proliferation and inflammation. J Mater Sci Mater Med 15(4):321-325.
53. Powell JJ, Faria N, Thomas-McKay E, Pele LC. 2010. Origin and fate of dietary nanoparticles and microparticles in the gastrointestinal tract. J Autoimmun 34(3):J226-J233.
54. Schins RPF, Knaapen AM. 2007. Genotoxicity of poorly soluble particles. Inhal Toxicol 19(S1):189-198.
55. Singh N, Manshian B, Jenkins GJS, Griffiths SM, Williams PM, Maffeis TGG, et al. 2009. NanoGenotoxicology: the DNA damaging potential of engineered nanomaterials. Biomaterials 30(23-24):3891-3914.
56. Skehan P, Storeng R, Scudiero D, Monks A, McMahon J, Vistica D, et al. 1990. New colorimetric assay for anticancer-drug screening. J Natl Cancer Inst 82:1107-1112.
57. Stark WJ. 2011. Nanopartikel in biologischen Systemen. Angew Chem 123(6):1276-1293.
58. Stöber W, Fink A, Bohn E. 1968. Controlled growth of. monodisperse silica spheres in micron size range. J Colloid Interface Sci 26(1): 62-69.
59. Stone V, Shaw J, Brown DM, MacNee W, Faux SP, Donaldson K. 1998. The role of oxidative stress in the prolonged inhibitory effect of ultrafine carbon black on epithelial cell function. Toxicol in Vitro 12 (6):649-659.
60. Sun Z, Huang Z, Zhang DD. 2009. Phosphorylation of Nrf2 at multiple sites by MAP kinases has a limited contribution in modulating the Nrf2-dependent antioxidant response. PLoS ONE 4(8):e6588.
61. Sydlik U, Bierhals K, Soufi M, Abel J, Schins RPF, Unfried K. 2006. Ultrafine carbon particles induce apoptosis and proliferation in rat lung epithelial cells via specific signaling pathways both using EGF-R. Am J Physiol Lung Cell Mol Physiol 291(4):L725-L733.
62. Tal TL, Bromberg PA, Kim Y, Samet JM. 2008. Epidermal growth factor receptor activation by diesel particles is mediated by tyrosine phosphatase inhibition. Toxicol Appl Pharmacol 233(3):382-388.
63. Tice RR, Agurell E, Anderson D, Burlinson B, Hartmann A, Kobayashi H, et al. 2000. Single cell gel/comet assay: guidelines for in vitro and in vivo genetic toxicology testing. Environ Mol Mutagen 35:206-221.
64. Tietze F. 1969. Enzymic method for quantitative determination of nanogram amounts of total an oxidized glutathion: application to mammalian blood and other tissues. Anal Biochem 27:502-522.
65. Ulrich GD. 1971. Theory of Particle formation and growth in oxide synthesis flames. Combustion Sci Technol 4(2):47-57.
66. Unfried K, Albrecht C, Klotz LO, Von Mikecz A, Grether-Beck S, Schins RPF. 2007. Cellular responses to nanoparticles: Target structures and mechanisms. Nanotoxicology 1(1):52-71.
67. Unfried K, Sydlik U, Bierhals K, Weissenberg A, Abel J. 2008. Carbon nanoparticle-induced lung epithelial cell proliferation is mediated by receptor-dependent Akt activation. Am J Physiol Lung Cell Mol Physiol 294(2):L358-L367.
68. Valinluck V, Sowers LC. 2007. Inflammation-mediated cytosine damage: a mechanistic link between inflammation and the epigenetic alterations in human cancers. Cancer Res 67(12):5583-5586.
69. Venkatesan N, Yoshimitsu J, Ito Y, Shibata N, Takada K. 2005. Liquid filled nanoparticles as a drug delivery tool for protein therapeutics. Biomaterials 26:7154-7163.
70. Wang F, Gao F, Lan M, Yuan H, Huang Y, Liu J. 2009. Oxidative stress contributes to silica nanoparticle-induced cytotoxicity in human embryonic kidney cells. Toxicol In Vitro 23:808-815.
71. Wang JJ, Sanderson BJS, Wang H. 2007. Cytotoxicity and genotoxicity of ultrafine crystalline SiO2 particulate in cultured human lymphoblastoid cells. Environ Mol Mutagen 48(2):151-157.
72. Weissenberg A, Sydlik U, Peuschel H, Schroeder P, Schneider M, Schins RPF, et al. 2010. Reactive oxygen species as mediators of membrane-dependent signaling induced by ultrafine particles. Free Radic Biol Med 49(4):597-605.
73. Wojewódzka M, Buraczewska I, Kruszewski M. 2002. A modified neutral comet assay: elimination of lysis at high temperature and validation of the assay with anti-single-stranded DNA antibody. Mutat Res 2518:9-20.
74. Xia T, Kovochich M, Liong M, Madler L, Gilbert B, Shi HB, et al. 2008. Comparison of the Mechanism of Toxicity of Zinc Oxide and Cerium Oxide Nanoparticles Based on Dissolution and Oxidative Stress Properties. ACS Nano 2(10):2121-2134.
75. Zhang D, Neumann O, Wang H, Yuwono VM, Barhoumi A, Perham M, et al. 2009. Gold nanoparticles can induce the formation of protein-based aggrgegates at phsiological pH. Nano Lett 9:666-671.
76. Zipper LM, Mulcahy RT 2003. Erk activation is required for Nrf2 nuclear localization during pyrrolidine dithiocarbamate induction of glutamate cysteine ligase modulatory gene expression in HepG2 cells. Toxicol Sci 73(1):124-134.