Size-dependent cytotoxicity of silver nanoparticles in human lung cells: The role of cellular uptake, agglomeration and Ag release

Particle and Fibre Toxicology

Volumn 11, Issue 1, 2014, Pages

  Gliga, Anda R ^a   Skoglund, Sara ^b   Odnevall Wallinder, Inger ^b   Fadeel, Bengt ^a   Karlsson, Hanna L ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b ROYAL INSTITUTE OF TECHNOLOGY   (Sweden)

Author keywords

BEAS 2B cells; Cytotoxicity; Genotoxicity; Silver nanoparticles; Silver release; Size dependent toxicity

Indexed keywords

CELL LINE; CELL SURVIVAL; COLORING AGENTS; COMET ASSAY; CULTURE MEDIA; DNA DAMAGE; ENDOCYTOSIS; EPITHELIAL CELLS; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; L-LACTATE DEHYDROGENASE; LUNG; METAL NANOPARTICLES; MICROSCOPY, ELECTRON, TRANSMISSION; OXAZINES; PARTICLE SIZE; REACTIVE OXYGEN SPECIES; SILVER; SPECTROPHOTOMETRY, ATOMIC; SPECTROPHOTOMETRY, ULTRAVIOLET; XANTHENES;

EID: 84894377473     PISSN: None     EISSN: 17438977     Source Type: Journal    
DOI: 10.1186/1743-8977-11-11     Document Type: Article

References (59)

1. Nel A, Xia T, Madler L, Li N. Toxic potential of materials at the nanolevel. Science 2006, 311(5761):622-627. 10.1126/science.1114397, 16456071.
2. Project on emerging nanotechnologies. [http://www.nanotechproject.org/cpi/].
3. Nowack B, Krug HF, Height M. 120 years of nanosilver history: implications for policy makers. Environ Sci Technol 2011, 45(4):1177-1183. 10.1021/es103316q, 21218770.
4. Ahamed M, AlSalhi MS, Siddiqui MKJ. Silver nanoparticle applications and human health. Clin Chim Acta 2010, 411(23-24):1841-1848.
5. Chen X, Schluesener HJ. Nanosilver: a nanoproduct in medical application. Toxicol Lett 2008, 176(1):1-12. 10.1016/j.toxlet.2007.10.004, 18022772.
6. Schrurs F, Lison D. Focusing the research efforts. Nat Nanotechnol 2012, 7(9):546-548. 10.1038/nnano.2012.148, 22902960.
7. Kim S, Ryu DY. Silver nanoparticle-induced oxidative stress, genotoxicity and apoptosis in cultured cells and animal tissues. J Appl Toxicol 2013, 33(2):78-89. 10.1002/jat.2792, 22936301.
8. Hackenberg S, Scherzed A, Kessler M, Hummel S, Technau A, Froelich K, Ginzkey C, Koehler C, Hagen R, Kleinsasser N. Silver nanoparticles: evaluation of DNA damage, toxicity and functional impairment in human mesenchymal stem cells. Toxicol Lett 2011, 201(1):27-33. 10.1016/j.toxlet.2010.12.001, 21145381.
9. Samberg ME, Loboa EG, Oldenburg SJ, Monteiro-Riviere NA. Silver nanoparticles do not influence stem cell differentiation but cause minimal toxicity. Nanomedicine 2012, 7(8):1197-1209. 10.2217/nnm.12.18, 3474209, 22583572.
10. Kittler S, Greulich C, Diendorf J, Koller M, Epple M. Toxicity of silver nanoparticles increases during storage because of slow dissolution under release of silver ions. Chem Mat 2010, 22(16):4548-4554.
11. Samberg ME, Orndorff PE, Monteiro-Riviere NA. Antibacterial efficacy of silver nanoparticles of different sizes, surface conditions and synthesis methods. Nanotoxicology 2011, 5(2):244-253. 10.3109/17435390.2010.525669, 21034371.
12. Beer C, Foldbjerg R, Hayashi Y, Sutherland DS, Autrup H. Toxicity of silver nanoparticles - nanoparticle or silver ion?. Toxicol Lett 2012, 208(3):286-292. 10.1016/j.toxlet.2011.11.002, 22101214.
13. Foldbjerg R, Irving ES, Hayashi Y, Sutherland DS, Thorsen K, Autrup H, Beer C. Global gene expression profiling of human lung epithelial cells after exposure to nanosilver. Toxicol Sci 2012, 130(1):145-157. 10.1093/toxsci/kfs225, 22831968.
14. Cronholm P, Karlsson HL, Hedberg J, Lowe TA, Winnberg L, Elihn K, Wallinder IO, Moller L. Intracellular uptake and toxicity of Ag and CuO nanoparticles: a comparison between nanoparticles and their corresponding metal ions. Small 2013, 9(7):970-982. 10.1002/smll.201201069, 23296910.
15. Liu W, Wu Y, Wang C, Li HC, Wang T, Liao CY, Cui L, Zhou QF, Yan B, Jiang GB. Impact of silver nanoparticles on human cells: effect of particle size. Nanotoxicology 2010, 4(3):319-330. 10.3109/17435390.2010.483745, 20795913.
16. Kim TH, Kim M, Park HS, Shin US, Gong MS, Kim HW. Size-dependent cellular toxicity of silver nanoparticles. J Biomed Mater Res A 2012, 100(4):1033-1043.
17. Khlebtsov BN, Khlebtsov NG. On the measurement of gold nanoparticle sizes by the dynamic light scattering method. Colloid J 2011, 73(1):118-127.
18. El Badawy AM, Luxton TP, Silva RG, Scheckel KG, Suidan MT, Tolaymat TM. Impact of environmental conditions (pH, ionic strength, and electrolyte type) on the surface charge and aggregation of silver nanoparticles suspensions. Environ Sci Technol 2010, 44(4):1260-1266. 10.1021/es902240k, 20099802.
19. Tomaszewska E, Soliwoda K, Kadziola K, Tkacz-Szczesna B, Celichowski G, Cichomski M, Szmaja W, Grobelny J. Detection limits of DLS and UV-vis spectroscopy in characterization of polydisperse nanoparticles colloids. J Nanomaterials 2013, 2013:10.
20. Skoglund S, Lowe TA, Hedberg J, Blomberg E, Wallinder IO, Wold S, Lundin M. Effect of laundry surfactants on surface charge and colloidal stability of silver nanoparticles. Langmuir 2013, 29(28):8882-8891. 10.1021/la4012873, 23758058.
21. Han X, Gelein R, Corson N, Wade-Mercer P, Jiang J, Biswas P, Finkelstein JN, Elder A, Oberdorster G. Validation of an LDH assay for assessing nanoparticle toxicity. Toxicology 2011, 287(1-3):99-104.
22. Holder AL, Marr LC. Toxicity of silver nanoparticles at the air-liquid interface. Biomed Res Int 2013, 328934(10):24.
23. Menon MP, Wright CE. A radiotracer probe to study metal interaction with human lactate dehydrogenase isoenzymes. J Protein Chem 1989, 8(6):757-766. 10.1007/BF01024900, 2624685.
24. Karlsson M, Kurz T, Brunk UT, Nilsson SE, Frennesson CI. What does the commonly used DCF test for oxidative stress really show?. Biochem J 2010, 428(2):183-190. 10.1042/BJ20100208, 20331437.
25. Stebounova L, Guio E, Grassian V. Silver nanoparticles in simulated biological media: a study of aggregation, sedimentation, and dissolution. J Nanoparticle Res 2011, 13(1):233-244.
26. Chernousova S, Epple M. Silver as antibacterial agent: ion, nanoparticle, and metal. Angew Chem Int Ed Engl 2013, 52(6):1636-1653. 10.1002/anie.201205923, 23255416.
27. Behra R, Sigg L, Clift MJ, Herzog F, Minghetti M, Johnston B, Petri-Fink A, Rothen-Rutishauser B. Bioavailability of silver nanoparticles and ions: from a chemical and biochemical perspective. J R Soc Interface 2013, 10(87):6.
28. Lee J, Ahn K, Kim S, Jeon K, Lee J, Yu I. Continuous 3-day exposure assessment of workplace manufacturing silver nanoparticles. J Nanoparticle Res 2012, 14(9):1-10.
29. Wang X, Ji Z, Chang CH, Zhang H, Wang M, Liao YP, Lin S, Meng H, Li R, Sun B, et al. Use of coated silver nanoparticles to understand the relationship of particle dissolution and bioavailability to cell and lung toxicological potential. Small 2013, 27(10):201301597.
30. Carlson C, Hussain SM, Schrand AM, Braydich-Stolle LK, Hess KL, Jones RL, Schlager JJ. Unique cellular interaction of silver nanoparticles: size-dependent generation of reactive oxygen species. J Phys Chem B 2008, 112(43):13608-13619. 10.1021/jp712087m, 18831567.
31. George S, Lin S, Ji Z, Thomas CR, Li L, Mecklenburg M, Meng H, Wang X, Zhang H, Xia T, et al. Surface defects on plate-shaped silver nanoparticles contribute to its hazard potential in a fish gill cell line and zebrafish embryos. ACS Nano 2012, 6(5):3745-3759. 10.1021/nn204671v, 22482460.
32. Li N, Xia T, Nel AE. The role of oxidative stress in ambient particulate matter-induced lung diseases and its implications in the toxicity of engineered nanoparticles. Free Radic Biol Med 2008, 44(9):1689-1699. 10.1016/j.freeradbiomed.2008.01.028, 2387181, 18313407.
33. Karlsson HL. The comet assay in nanotoxicology research. Anal Bioanal Chem 2010, 398(2):651-666. 10.1007/s00216-010-3977-0, 20640410.
34. Kain J, Karlsson HL, Moller L. DNA damage induced by micro- and nanoparticles-interaction with FPG influences the detection of DNA oxidation in the comet assay. Mutagenesis 2012, 27(4):491-500. 10.1093/mutage/ges010, 22447192.
35. AshaRani PV, Sethu S, Lim H, Balaji G, Valiyaveettil S, Hande MP. Differential regulation of intracellular factors mediating cell cycle, DNA repair and inflammation following exposure to silver nanoparticles in human cells. Genome Integr 2012, 3(1):2. 10.1186/2041-9414-3-2, 3305596, 22321936.
36. Kim HR, Kim MJ, Lee SY, Oh SM, Chung KH. Genotoxic effects of silver nanoparticles stimulated by oxidative stress in human normal bronchial epithelial (BEAS-2B) cells. Mutat Res 2011, 726(2):129-135. 10.1016/j.mrgentox.2011.08.008, 21945414.
37. Asharani PV, Hande MP, Valiyaveettil S. Anti-proliferative activity of silver nanoparticles. BMC Cell Biol 2009, 10(65):1471-2121.
38. Lu W, Senapati D, Wang S, Tovmachenko O, Singh AK, Yu H, Ray PC. Effect of surface coating on the toxicity of silver nanomaterials on human skin keratinocytes. Chem Phys Lett 2010, 487(1-3):92-96.
39. Verma NK, Conroy J, Lyons PE, Coleman J, O'Sullivan MP, Kornfeld H, Kelleher D, Volkov Y. Autophagy induction by silver nanowires: a new aspect in the biocompatibility assessment of nanocomposite thin films. Toxicol Appl Pharmacol 2012, 264(3):451-461. 10.1016/j.taap.2012.08.023, 22959926.
40. Yu SJ, Chao JB, Sun J, Yin YG, Liu JF, Jiang GB. Quantification of the uptake of silver nanoparticles and ions to HepG2 cells. Environ Sci Technol 2013, 47(7):3268-3274.
41. Zhang W, Yao Y, Sullivan N, Chen Y. Modeling the primary size effects of citrate-coated silver nanoparticles on their ion release kinetics. Environ Sci Technol 2011, 45(10):4422-4428. 10.1021/es104205a, 21513312.
42. Gebauer JS, Malissek M, Simon S, Knauer SK, Maskos M, Stauber RH, Peukert W, Treuel L. Impact of the nanoparticle-protein corona on colloidal stability and protein structure. Langmuir 2012, 28(25):9673-9679. 10.1021/la301104a, 22524519.
43. Monteiro-Riviere NA, Samberg ME, Oldenburg SJ, Riviere JE. Protein binding modulates the cellular uptake of silver nanoparticles into human cells: implications for in vitro to in vivo extrapolations?. Toxicol Lett 2013, 220(3):286-293. 10.1016/j.toxlet.2013.04.022, 23660336.
44. Cho EC, Zhang Q, Xia Y. The effect of sedimentation and diffusion on cellular uptake of gold nanoparticles. Nat Nanotechnol 2011, 6(6):385-391. 10.1038/nnano.2011.58, 3227810, 21516092.
45. Wang H, Wu L, Reinhard BM. Scavenger receptor mediated endocytosis of silver nanoparticles into J774A.1 macrophages is heterogeneous. ACS Nano 2012, 6(8):7122-7132. 10.1021/nn302186n, 3482345, 22799499.
46. Zhang LW, Monteiro-Riviere NA. Mechanisms of quantum dot nanoparticle cellular uptake. Toxicol Sci 2009, 110(1):138-155. 10.1093/toxsci/kfp087, 19414515.
47. Liu J, Sonshine DA, Shervani S, Hurt RH. Controlled release of biologically active silver from nanosilver surfaces. ACS Nano 2010, 4(11):6903-6913. 10.1021/nn102272n, 3004478, 20968290.
48. Liu J, Wang Z, Liu FD, Kane AB, Hurt RH. Chemical transformations of nanosilver in biological environments. ACS Nano 2012, 6(11):9887-9899. 10.1021/nn303449n, 3508364, 23046098.
49. Xiu ZM, Zhang QB, Puppala HL, Colvin VL, Alvarez PJ. Negligible particle-specific antibacterial activity of silver nanoparticles. Nano Lett 2012, 12(8):4271-4275. 10.1021/nl301934w, 22765771.
50. Yang X, Gondikas AP, Marinakos SM, Auffan M, Liu J, Hsu-Kim H, Meyer JN. Mechanism of silver nanoparticle toxicity is dependent on dissolved silver and surface coating in Caenorhabditis elegans. Environ Sci Technol 2012, 46(2):1119-1127. 10.1021/es202417t, 22148238.
51. Shi J, Karlsson HL, Johansson K, Gogvadze V, Xiao L, Li J, Burks T, Garcia-Bennett A, Uheida A, Muhammed M, et al. Microsomal glutathione transferase 1 protects against toxicity induced by silica nanoparticles but not by zinc oxide nanoparticles. ACS Nano 2012, 6(3):1925-1938. 10.1021/nn2021056, 3314313, 22303956.
52. Ruckert P, Bates SR, Fisher AB. Role of clathrin- and actin-dependent endocytotic pathways in lung phospholipid uptake. Am J Physiol Lung Cell Mol Physiol 2003, 284(6):28.
53. Skretting G, Torgersen ML, van Deurs B, Sandvig K. Endocytic mechanisms responsible for uptake of GPI-linked diphtheria toxin receptor. J Cell Sci 1999, 112(Pt 22):3899-3909.
54. Koivusalo M, Welch C, Hayashi H, Scott CC, Kim M, Alexander T, Touret N, Hahn KM, Grinstein S. Amiloride inhibits macropinocytosis by lowering submembranous pH and preventing Rac1 and Cdc42 signaling. J Cell Biol 2010, 188(4):547-563. 10.1083/jcb.200908086, 2828922, 20156964.
55. Clague MJ, Thorpe C, Jones AT. Phosphatidylinositol 3-kinase regulation of fluid phase endocytosis. FEBS Lett 1995, 367(3):272-274. 10.1016/0014-5793(95)00576-U, 7607321.
56. Chen X, Zhong Z, Xu Z, Chen L, Wang Y. 2′,7′-Dichlorodihydrofluorescein as a fluorescent probe for reactive oxygen species measurement: forty years of application and controversy. Free Radic Res 2010, 44(6):587-604. 10.3109/10715761003709802, 20370560.
57. Mah LJ, El-Osta A, Karagiannis TC. gammaH2AX: a sensitive molecular marker of DNA damage and repair. Leukemia 2010, 24(4):679-686. 10.1038/leu.2010.6, 20130602.
58. Hedberg Y, Gustafsson J, Karlsson HL, Moller L, Odnevall Wallinder I. Bioaccessibility, bioavailability and toxicity of commercially relevant iron- and chromium-based particles: in vitro studies with an inhalation perspective. Part Fibre Toxicol 2010, 7(23):1743-8977.
59. de Meringo A, Morscheidt C, Thelohan S, Tiesler H. In vitro assessment of biodurability: acellular systems. Environ Health Perspect 1994, 5:47-53.