Comparative cytotoxicity of nanosilver in human liver HepG2 and colon Caco2 cells in culture

Journal of Applied Toxicology

Volumn 34, Issue 11, 2014, Pages 1155-1166

  Sahu, Saura C ^a   Zheng, Jiwen ^b   Graham, Lesley ^b   Chen, Lynn ^c   Ihrie, John ^a   Yourick, Jeffrey J ^a   Sprando, Robert L ^a  

^a CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

^b CENTER FOR DEVICES AND RADIOLOGICAL HEALTH   (United States)

^c UNIVERSITY OF MARYLAND   (United States)

Author keywords

Caco2 cells; Cytotoxicity; HepG2 cells; Mitochondrial injury; Nanoparticles; Nanosilver; Oxidative stress; Silver nanoparticles

Indexed keywords

DICHLOROFLUORESCEIN; DOUBLE STRANDED DNA; SILVER NANOPARTICLE; METAL NANOPARTICLE; SILVER;

ARTICLE; CACO-2 CELL LINE; CELL CULTURE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOTOXICITY; DNA DAMAGE; HEP-G2 CELL LINE; HUMAN; HUMAN CELL; IN VITRO STUDY; LIMIT OF DETECTION; LIMIT OF QUANTITATION; MASS SPECTROMETRY; MITOCHONDRIAL MEMBRANE POTENTIAL; OXIDATIVE STRESS; PHOTON CORRELATION SPECTROSCOPY; RESAZURIN ASSAY; TRANSMISSION ELECTRON MICROSCOPY; CACO 2 CELL LINE; COMPARATIVE STUDY; DOSE RESPONSE; DRUG EFFECTS; HEPG2 CELL LINE; MITOCHONDRION;

CACO-2 CELLS; DNA DAMAGE; DOSE-RESPONSE RELATIONSHIP, DRUG; HEP G2 CELLS; HUMANS; METAL NANOPARTICLES; MICROSCOPY, ELECTRON, TRANSMISSION; MITOCHONDRIA; OXIDATIVE STRESS; SILVER;

EID: 84907868660     PISSN: 0260437X     EISSN: 10991263     Source Type: Journal    
DOI: 10.1002/jat.2994     Document Type: Article

References (86)

1. AshaRani PV, Mun GLK, Hande MP, Valiyaveettil . 2009. Cytotoxicity and genotoxicity of silver nanoparticles in human cells. ACS Nano 3: 279-290.
2. st century: Bringing the vision to life. Toxicol. Sci. 107: 324-330.
3. Avalos A, Haza AI, Mateo D, Morales P. 2013. Cytotoxicity and ROS production of manufactured silver nanoparticles of different sizes in hepatoma and leukemia cells. J. Appl. Toxicol. 2014; 34: 413-423.
4. Bajt ML, Knight TR, Lemasters JJ, Jaeschke H. 2004. Acetaminophen-induced oxidant stress and cell injury in cultured mouse hepatocyets: Protection by N-acetyl cysteine. Toxicol. Sci. 80: 343-349.
5. Baracca A, Sgarbi G, Solaini G, Lenaz G. 2003. Rhodamine 123 as a probe of mitochondrial membrane potential: Evaluation of proton flux through F(0) during ATP synthesis. Biochim. Biophys. Acta 1606: 137-146.
6. +3-containing (Hematite) particles for their toxicological properties in human lung cells In Vitro. Toxicol. Sci. 126: 173-182.
7. Birringer M, Lington D, Vertuani S, Manfredini S, Schartau D, Glei M, Ristow M, 2010. Proapoptotic effects of long-chain vitamin E metabolites in HepG2 cells are mediated by oxidative stress. Free Rad. Biol. Med. 49: 1315-1322.
8. Bohmert L, Niemann B, Thunemann AF, Lampen A. 2012. Cytotoxicity of peptide-coated silver nanoparticles on the human intestinal cell line Caco2. Arch. Toxicol. 86: 1107-115.
9. Brandon EFA, Bosch TM, Deenen MJ, Levink R, van der Wal E, van Meerveld JBM, Bijl M, Beijnen JH, Schellen JHM, Meijerman I. 2006. Validation of in vitro cell models used in drug metabolism and transport studies: genotypning of cytochrome P450 and drug transporter polymorphism in the human hepatoma (HepG2), ovarian carcinoma (IGROV-1) and colon carcinoma (Caco2, LS180) cell lines. Toxicol. Appl. Pharmacol. 211: 1-10.
10. Buerki-Thurnherr T, Xiao L, Diener L, Arslan O, Hirsch C, Maeder-Althaus X, Grieder K, Wampfler B, Mathur S, Wick P, Krug HF. 2013. In vitro mechanistic study towards a better understanding of ZnO nanoparticle toxicity. Nanotoxicology 7: 402-426.
11. st century: A view from the chemical industry. Toxicol. Sci. 112: 297-302.
12. Carlson C, Husssain SM, Schrand AM, Hess K, Jones RL, Schlager JJ. 2008. Unique cellular interaction of silver nanoparticles: Size-dependent generation of reactive oxygen species. J. Phys. Chem. B 112: 13608-13619
13. Chantret I, Barbat A, Dussaulx E, Brattain MG, Zweibaum A. 1988. Epithelial polarity, villin expression and enterocytic differentiation of cultured human colon carcinoma cells: A survey of twenty cell lines. Cancer Res. 48: 1936-1942.
14. Chopra M, Dharmarajan AM, Meiss G, Schrenk D. 2009. Inhibition of UV-C Light-Induced Apoptosis in Liver Cells by 2, 3, 7, 8-Tetrachlorodibenzo-p-Dioxin. Toxicol. Sci. 111: 49-63.
15. Chopra DP, Dombkowski AA, Stemmer PM, Parker GC. 2010. Intestinal epithelial cells in vitro. Stem Cells Dev. 19: 131-142.
16. Dashti N, Wolfbaurer G, Koren E, Knowles B, Alanpovic P. 1984. Catabolism of human low density lipoproteins by human hepatoma cell line HepG2. Biochim. Biophys. Acta 794: 373-384.
17. Delhalle S, Duvoix A, Schnekenburger M, Dicato M, Dietrich M. 2003. An introduction to the molecular mechanisms of apoptosis. Ann. N.Y. Acad. Sci. 1010: 1-9.
18. De Lima R, Seabra AB, Durán N. 2012. Silver nanoparticles: a brief review of cytotoxicity and genotoxicity of chemically and biogenically synthesized nanoparticles. J. Appl. Toxicol. 32: 867-879.
19. Dierickx PJ. 1987. Inhibition of glutathione-dependent uridine uptake in cultured human hepatoma cells. Med. Sci. Res. 15: 1349-1350.
20. Dudas J, Mansuroglu T, Moriconi F, Haller F, Wilting J, Lorf T, Fuzes L, Ramadori G. 2008. Altered regulation of Prox1-gene-expression in liver tumors. BMC Cancer 8: 92-106.
21. Dziendzikowska K, Gromadzka-Ostrowska J, Lankoff A, Oczkowski M, Krawczyńska A, Chwastowska J, Sadowska-Bratek M, Chajduk E, Wojewódzka M, Dušinská M, Kruszewski M. 2012. Time-dependent biodistribution and excretion of silver nanoparticles in male Wistar rats. J. Appl. Toxicol. 32: 920-928
22. Fang J, Beland FA. 2009. Long-term exposure to Zidovudine delays cell cycle progression, induces apoptosis and decreases telomerase activity in human hepatocytes. Toxicol. Sci. 111: 120-130.
23. Gaiser BK, Hirn S, Kermanizadeh A, Kanase N, Fytianos K, Wenk A, Haberl N, Brunelli A, Kreyling WG, Stone V. 2013. Effects of silver nanoparticles on the liver and hepatocytes in vitro. Toxicol. Sci. 131: 537-547.
24. Gerloff K, Albrecht C, Boots AW, Forster I, Schins RPF. 2009. Cytotoxicity and oxidative DNA damage by nanoparticles in human intestinal Caco2 cells. Nanotoxicology 3: 355-364.
25. Gerloff K, Pereira D, Faria N, Boots AW, Kolling J, Forster I, Albrecht C, Powell JJ, Schins RPF. 2013. Influence of simulated gastrointestinal conditions on particle-induced cytotoxicity and interleukin-8 regulation in differentiated and undifferentiated Caco2 cells. Nanotoxicology 7: 353-366.
26. Grub S, Persohn E, Trommer WE, Wolf A. 2000. Induction of apoptosis by the o-hydroxyethyl-d(ser)8-cyclosporine A derivative SDZ IMM 125 in rat hepatocytes. J. Pharmacol. Exp. Ther. 293: 24-32.
27. Haase A, Rott S, Mantion A, Graf P, Plendl J, Thunemann A, Meier W, Taubert A, Luch A, Reiser G. 2012. Effects of silver nanoparticles on primary mixed neural cell cultures: Uptake, oxidative stress and acute calcium responses. Toxicol. Sci. 126: 457-468
28. Hail N, Lotan R. 2000. Mitochondrial Permeability Transition Is a Central Coordinating Event in N-(4-Hydroxyphenyl)retinamide-induced Apoptosis. Cancer Epidemiol. Biomarkers Prev. 9: 1293-1301.
29. Halliwell B, Whiteman M. 2004. Measuring reactive species and oxidative damage in vivo and in cell culture: how should you do it and what do the results mean? Br. J. Pharmacol. 142: 231-255.
30. Hamid R, Rotshteyn Y, Rabadi L, Parikh R, Bullock P. 2004. Comparision of alamar blue and MTT assays for high through-put screening. Toxicol. In Vitro 18: 703-710.
31. Harris, AJ, Dial SL, Casciano DA. 2004. Comparision of basal gene expression profiles and effects of hepatocarcinogens on gene expression in cultured primary human hepatocytes and HepG2 cells. Mut. Res. 549: 79-99.
32. Hartung T, Daston G. 2009. Are in vitro tests suitable for regulatory use? Toxicol. Sci. 111: 23-27.
33. Horev-Azaria L, Kirkpatrick CJ, Korenstein R, Marche PN, Maimon O, Ponti J, Romano R, Rossi F, Golla-Schindler U, Sommer D, Uboldi C, Unger RE, Villiers C. 2011. Predictive toxicology of cobalt nanoparticles and ions: Comparative in vitro study of different cellular models using methods of knowledge discovery from data. Toxicol. Sci. 122: 489-501
34. Hussain SM, Hess KL, Gearhardt JH, Geiss KT, Schlager JJ. 2005. In vitro toxicity of nanoparticles in BRL 3A rat liver cells. Toxicol. In Vitro 19: 975-983.
35. Jain J, Arora S, Rajwade JM, Omray P, Khandelwal S, Paknikar KM. 2009. Silver Nanoparticles in Therapeutics: Development of an Antimicrobial Gel Formulation for Topical Use. Mol. Pharmaceutics 6, 1388-1401.
36. Jennen DG, Magkoufopoulou C, Ketelslegers HB, van Herwijnen MH, Kleinjans JC, van Delft JH. 2010. Comparison of HepG2 and HepaRG by whole genome gene expression analysis for the purpose of chemical hazard identification. Toxicol. Sci. 115: 66-79.
37. Johnson LV, Walsh ML, Chen LB. 1980. Localization of mitochondria in living cells with rhodamine 123. Proc. Natl. Acad. Sci. U. S. A. 77: 990-994.
38. Kao Y, Chen Y, Cheng T, Chiung YM, Liu P. 2012. Zinc oxide nanoparticles interfere with zinc ion homeostasis to cause cytotoxicity. Toxicol. Sci. 125: 462-472.
39. Kiang TKL, Teng XW, Stoyan Karagiozov S, Surendradoss J, Chang TKH, Abbott FS. 2010. Role of oxidative metabolism in the effect of valproic acid on markers of cell viability, necrosis, and oxidative stress in sandwich-cultured rat hepatocytes. Toxicol. Sci. 118: 501-509.
40. Kim S, Ryu D. 2012. Silver nanoparticle-induced oxidative stress, genotoxicity and apoptosis in cultured cells and animal tissues. J. Appl. Toxicol. 33: 78-89.
41. Kim JS, Kuk E, Yu KN, Park SJ, Lee HJ, Kim SH, Park YH, Hwang CY. 2007. Antimicrobial effects of silver nanoparticles. Nanomedicine 3: 95-101.
42. Knowles BB, Howe CC, Aden DP. 1980. Human hepatocellular carcinoma cell line secrete the major plasma proteins and hepatitis B surface antigen. Science 209: 479-499.
43. Lee HC, Wei YH. 2007. Oxidative stress, mitochondrial DNA mutation and apoptosis in aging. Exp. Biol. Med. 232: 592-606.
44. Lemasters JJ, Nieminen AI, Qian T, Elmore SP, Nishimura Y, Cascio W, Bradham C, Brenner DA. 1998. The mitochondrial permeability transition in cell death: Acommon mechanism in necrosis, apoptosis and autophagy. Biochim. Biophys. Acta 66: 177-196.
45. Lok CN, Ho CM, Chen R, Sun H, Tam PK, Chiu JF, Che CM. 2006. Proteomic analysis of the mode of antibacterial action of silver nanoparticles. J. Proteome Res. 5: 916-924.
46. Marselos M, Storm S, Michalopoulos G. 1987. Effect of Phenobarbital and 3-methylcholanthrene on aldehyde dehydrogenase activity in HepG2 cells and normal hepatocytes. Chem. Biol. Interact. 62: 75-88.
47. st century in a regulatory context: Another Ames test? or a new edition of 'the red book"? Toxicol. Sci. 108: 19-21.
48. Merrill CL, Ni H, Yoon LW, Tirmenstein MA, Narayanan P, Benavides GR, Easton M, Creech D, Hu C, McFarland D, Hahn L, Thomas HC, Morgan KT. 2002. Etomoxir-induced oxidative stress in HepG2 cells detected by differential gene expression is confirmed biochemically. Toxicol. Sci. 68: 93-101.
49. Morones JR, Elechiguerra JL, Camacho A, Holt K, Kouri JB, Ramírez JT, Yacaman MJ. 2005. The bactericidal effect of silver nanoparticles. Nanotechnology 16: 2346-235.
50. Nakatsu Y, Kotake Y, Ohta S. 2007. Concentration dependence of the mechanisms of tributyltin-induced apoptosis. Toxicol. Sci. 97: 438-447.
51. Nam S, Kim SW, An Y. 2012. No evidence of the genotoxic potential of gold, silver, zinc oxide and titanium dioxide nanoparticles in the SOS chromotest. J. Appl. Toxicol. 33: 1061-1069.
52. O'Brien J, Wilson I, Orton T, Pognan F. 2000. Invesigation of the Alamar Blue (resazurine) fluorescent dye for the assessment of mammalian cell cytotoxicity. Eur. J. Biochem. 267: 5421-5426.
53. O'Brien PJ, Irwin W, Diaz D, Howard-Cofield E, Krejsa CM, Slaughter MR, Gao B, Kaludercic N, Angeline A, Bernardi P. 2006. High concordance of drug-induced human hepatotoxicity with in vitro cytotoxicity measured in a novel cell-based model using high content screening. Arch. Toxicol. 80: 580-604.
54. Pascarelli NA, Moretti E, Terzuoli G, Lamboglia A, Renieri T, Fioravanti A, Collodel G. 2013. Effects of gold and silver nanoparticles in cultured human osteoarthritic chondrocytes. J. Appl. Toxicol. 33: 1506-1513.
55. Piao MJ, Kang KA, Lee IK, Kim HS, Choi YJ, Hyun JW. 2011. Silver nanoparticles induce oxidative cell damage in human liver cells through inhibition of reduced glutathione and induction of mitochondria-involved apoptosis. Toxicol. Lett. 201: 92-100.
56. 20 aggregates. J. Appl. Toxicol. 2014; 34: 404-412.
57. Powers CM, Badireddy AR, Ryde IT, Seidler FJ, Slotkins TA. 2011. Silver nanoparticles compromise neurodevelopment in PC12 cells: Critical contributions of silver ion, particle size, coating and composition. Environ. Health Perspect. 119: 37-44.
58. Rage R, Mitchen J, Wilding G. 1990. DNA fluorometric assay in 96-well tissue culture plates using Hoechst 33258 after cell lysis by freezing in distilled water. Anal. Biochem. 191: 31-34.
59. Rat P, Korwin-Zmijowska C, Warnet JM, Adolphe M. 1994. New in vitro fluorimetric microtitration assays for toxicological screening. Cell Biol. Toxicol. 10: 329-337.
60. Ripcke J, Zarse K, Ristow M, Birringer M. 2009. Small-molecule targeting of the mitochondrial compartment with an endogenously cleaved reversible tag. Chembiochem 10: 1689-1696.
61. Roe AL, Snawder JE, Benson RW, Roberts DW, Casciano DA. 1993. HepG2 cells: an in vitro model for P45-dependent metabolism of acetaminophen. Biochem. Biophys. Res. Commun. 190: 15-19.
62. Sahu SC, Gaines DW, Williams KM, Raybourne RB. 2007. A synthetic polypeptide based on human E-cadherin inhibits invasion of human intestinal and liver cell lines by Listeria Monocytogenes. J. Med. Microbiol. 56: 1011-1016.
63. Sahu SC, Garthoff LH, Robl MG, Chirtel SJ, Ruggles DI, Flynn TJ, Sobotka TJ. 2008. Rat liver clone-9 cells in culture as a model for evaluating hepatotoxic potential of food-related products: Hepatotoxicity of deoxynivalenol. J. Appl. Toxicol. 28: 765-772.
64. Sahu SC, O'Donnell M, Wiesenfeld P. 2010. Comparative hepatotoxicity of deoxynivalenol in rat, mouse and human liver cells in culture. J. Appl. Tox. 30: 566-573.
65. Sahu SC, Amankwa-Sakyi M, O'Donnell MW, Sprando RL. 2012. Effects of usnic acid exposure on human hepatoblastoma HepG2 cells in culture. J. Appl. Toxicol. 32: 722-730
66. Said T, Dutot M, Martin C, Beaudeux J, Boucher C, Enee E, Boudouin C, Warnet J, Rat P. 2007. Cytoprotective effect against UV-induced DNA damage and oxidative stress: Role of new biological UV filter. Eur. J. Pharm. Sci. 30: 203-210.
67. Sassa S, Sugita O, Galbraith R, Kappa A. 1987. Drug metabolism by the human hepatoma cell, HepG2. Biochem. Biophys. Res. Commun. 143: 52-57.
68. Schoonen WG, de Roos JA, Westerink WM, Debiton E. 2005a. Cytotoxic effects of 110 reference compounds on HepG2 cells and for 60 compounds on HeLa, ECC-1 and CHO cells. II mechanistic assays on NAD(P)H, ATP and DNA contents. Toxicol. In Vitro 19: 491-503.
69. Schoonen WG, Westerink WM, de Roos JA, Debiton E. 2005b. Cytotoxic effects of 100 reference compounds on Hep G2 and HeLa cells and of 60 compounds on ECC-1 and CHO cells. I mechanistic assays on ROS, glutathione depletion and calcein uptake. Toxicol. In Vitro 19: 505-516.
70. Shao J, White CC, Dabrowski MJ, Kavanagh TJ, Eckert ML, Gallagher EP. 2008. The role of mitochondrial and oxidative injury in BDE 47 toxicity to human fetal liver hematopoietic stem cells. Toxicol. Sci. 101: 81-90.
71. Shimoda R, Achanzar WE, Qu W, Nagamine T, Takagi H, Mori M, Waalkes MP. 2003. Metallothionein Is a Potential Negative Regulator of Apoptosis. Toxicol. Sci. 73: 294-300.
72. Slaughter MR, Bugelski PJ, O'Brien PJ. 1999. Evaluation of alamar blue reduction for the in vitro assay of hepatocytes toxicity. Toxicol. In Vitro 13: 567-569.
73. Sondi I, Salopek-Sondi B. 2004. Silver nanoparticles as antimicrobial agents: A case study on E. Coli as a model for Gram-negative bacteria. J. Colloid Interface Sci. 275: 177-182
74. Song W, Zhang J, Guo J, Zhang J, Ding F, Li L, Sun Z. 2010. Role of the dissolved zinc ion and reactive oxygen species in cytotoxicity of ZnO nanoparticles. Toxicol. Lett. 199: 389-397.
75. Stacey NH, Klaassen CD. 1981. Inhibition of lipid peroxidation without prevention of cellular injury in isolated rat hepatocytes. Toxicol. Appl. Pharmacol. 58: 8-18.
76. Tong V, Teng XW, Chang TKH, Abbott FS. 2005. Valproic acid II: Effects on oxidative stress, mitochondrial membrane potential, and cytotoxicity in glutathione-depleted rat hepatocytes. Toxicol. Sci. 86: 436-443.
77. Uranga RM, Giusto NM, Salvador GA. 2009. Iron-induced oxidative injury differentially regulates PI3K/Akt/GSK3β pathway in synaptic endings from adult and aged rats. Toxicol. Sci. 111: 331-344.
78. Van Dartel DAM, Pennings JLA, de la Fonteyne LJJ, Brauers KJJ, Claessen S, van Delft JH, Kleinjans JCS, Piersma AH. 2011. Evaluation of developmental toxicant identification using gene expression profiling in embryonic stem cell differentiation cultures. Toxicol. Sci. 119: 126-134.
79. 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.
80. Xia T, Kovochich M, Liong M, Zink JI, Nel AE. 2008. Cationic polystyrene nanosphere toxicity depends on cell-specific endocytic and mitochondrial injury pathways. ACS Nano 2: 85-96.
81. Xu JJ, Henstock PV, Dunn MC, Smith AR, Chabot JR, de Gaarf D. 2008. Cellular imaging predictions of clinical drug-induced liver injury. Toxicol. Sci. 105: 97-105.
82. Xue Y, Zhang S, Huang Y, Zhang T, Liu X, Hu Y, Zhang Z, Tang M. 2012. Acute toxic effects and gender-related biokinetics of silver nanoparticles following an intravenous injection in mice. J. Appl. Toxicol. 32: 890-899.
83. Yamashita S, Furubayashi T, Kataoka M, Sakane T, Sezaki H, Tokuda H. 2000. Optimized conditions for prediction of intestinal drug permeability using Caco-2 cells. Eur. J. Pharm. Sci. 10: 195-204.
84. Zhang L, Mu X, Fu J, Zhou Z. 2007. In vitro cytotoxicity assay with selected chemicals using human cells to predict target-organ toxicity of liver and kidney. Toxicol. In Vitro 21: 734-740.
85. Zimmermann SK, Zarse TJ, Schulz K, Siems L, Muller-Kuhrt M, Birringer S, Ristow M. 2008. A cell-based high-throughput assay system reveals modulation of oxidative and non-oxidative glucose metabolism due to commonly used organic solvents. Horm. Metab. Res. 40: 29-37.
86. Zorov DB, Juhaszova M, Sollott SJ. 2006. Mitochondrial ROS-induced ROS release: An update and review. Biochim. Biophys. Acta 1757: 509-517.