Dynamic protein coronas revealed as a modulator of silver nanoparticle sulphidation in vitro

Nature Communications

Volumn 7, Issue , 2016, Pages

  MiclǍuş, Teodora ^a   Beer, Christiane ^a   Chevallier, Jacques ^a   Scavenius, Carsten ^a   Bochenkov, Vladimir E ^a,b   Enghild, Jan J ^a   Sutherland, Duncan S ^a  

^a AARHUS UNIVERSITY   (Denmark)

^b MOSCOW STATE UNIVERSITY   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

POVIDONE; PROTEIN CORONA; SILVER NANOPARTICLE; ION; METAL NANOPARTICLE; PROTEIN; SILVER; SILVER DERIVATIVE; SILVER SULFIDE;

BIOTRANSFORMATION; CATION; CONCENTRATION (COMPOSITION); CORONA; PROTEIN; SAFETY; SERUM; SILVER; SULFIDE; TOXICITY TEST;

ANIMAL CELL; ARTICLE; CELL CULTURE; CYTOKINE RELEASE; DRUG TRANSFORMATION; IN VITRO STUDY; IN VIVO STUDY; MACROPHAGE; NONHUMAN; ADSORPTION; CELL CULTURE TECHNIQUE; CHEMISTRY; METABOLISM; PARTICLE SIZE;

ADSORPTION; CELL CULTURE TECHNIQUES; IONS; METAL NANOPARTICLES; PARTICLE SIZE; PROTEIN CORONA; PROTEINS; SILVER; SILVER COMPOUNDS;

EID: 84973659193     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms11770     Document Type: Article

References (69)

1. Monopoli, M. P., Aberg, C., Salvati, A. & Dawson, K. A. Biomolecular coronas provide the biological identity of nanosized materials. Nat. Nanotechnol 7, 779-786 (2012).
2. Walczyk, D., Baldelli Bombelli, F., Monopoli, M. P., Lynch, I. & Dawson, K. A. What the cell ''sees'' in bionanoscience. J. Am. Chem. Soc. 132, 5761-5768 (2010).
3. Tenzer, S. et al. Rapid formation of plasma protein corona critically affects nanoparticle pathophysiology. Nat. Nanotechnol 8, 772-781 (2013).
4. Walkey, C. D. et al. Protein corona fingerprinting predicts the cellular interaction of gold and silver nanoparticles. ACS Nano 8, 2439-2455 (2014).
5. Albanese, A. et al. Secreted biomolecules alter the biological identity and cellular interactions of nanoparticles. ACS Nano 8, 5515-5526 (2014).
6. Walkey, C. D., Olsen, J. B., Guo, H., Emili, A. & Chan, W. C. W. Nanoparticle size and surface chemistry determine serum protein adsorption and macrophage uptake. J. Am. Chem. Soc. 134, 2139-2147 (2012).
7. Pelaz, B. et al. Interfacing engineered nanoparticles with biological systems: anticipating adverse nano-bio interactions. Small 9, 1573-1584 (2013).
8. Docter, D. et al. The nanoparticles biomolecule corona: lessons learned - challenge accepted? Chem. Soc. Rev. 44, 6094-6121 (2015).
9. Del Pino, P. et al. Protein corona formation around nanoparticles - from the past to the future. Mater. Horiz 1, 301-313 (2014).
10. Casals, E., Pfaller, T., Duschl, A., Oostingh, G. J. & Puntes, V. Time evolution of the nanoparticle protein corona. ACS Nano 4, 3623-3632 (2010).
11. Röcker, C., Pötzl, M., Zhang, F., Parak, W. J. & Nienhaus, G. U. A quantitative fluorescence study of protein monolayer formation on colloidal nanoparticles. Nat. Nanotechnol 4, 577-580 (2009).
12. Milani, S., Baldelli Bombelli, F., Pitek, A. S., Dawson, K. A. & Rädler, J. Reversible versus irreversible binding of transferrin to polystyrene nanoparticles: soft and hard corona. ACS Nano 6, 2533-2541 (2012).
13. Monopoli, M. P. et al. Physical-chemical aspects of protein corona: relevance to in vitro and in vivo biological impacts of nanomaterials. J. Am. Chem. Soc. 133, 2525-2534 (2011).
14. 2-NPs spots histidine rich glycoprotein as a major player able to hamper nanoparticle capture by macrophages. Nanoscale 7, 17710-17728 (2015).
15. Lundqvist, M. et al. Nanoparticle size and surface properties determine the protein corona with possible implications for biological impacts. Proc. Natl Acad. Sci. USA 105, 14265-14270 (2008).
16. Eigenheer, R. et al. Silver nanoparticle protein corona composition compared across engineered particle properties and environmentally relevant reaction conditions. Environ. Sci. Nano 1, 238-247 (2014).
17. Nel, A. E. et al. Understanding the biophysicochemical interactions at the nano-bio interface. Nat. Mater. 8, 543-557 (2009).
18. Tenzer, S. et al. Nanoparticle size is a critical physic-chemical determinant of the human blood plasma corona: a comprehensive quantitative proteomic analysis. ACS Nano 5, 7155-7167 (2011).
19. Deng, Z. J. et al. Differential plasma protein binding to metal oxide nanoparticles. Nanotechnology 20, 455101-455109 (2009).
20. Walkey, C. D. & Chan,W. C.W. Understanding and controlling the interaction of nanomaterials with proteins in physiological environment. Chem. Soc. Rev. 41, 2780-2799 (2012).
21. Lesniak, A. et al. Effects of the presence or absence of a protein corona on silica nanoparticle uptake and impact on cells. ACS Nano 6, 5845-5857 (2012).
22. Liu, R., Jiang, W., Walkey, C. D., Chan, W. C. W. & Cohen, Y. Prediction of nanoparticles-cell association based on corona proteins and physicochemical properties. Nanoscale 7, 9664-9675 (2015).
23. Setyawati, M. I., Tay, C. Y., Docter, D., Stauber, R. H. & Leond, D. T. Understanding and exploiting nanoparticles' intimacy with the blood vessel and blood. Chem. Soc. Rev. 44, 8174-8199 (2015).
24. MiclǍus?, T., Bochenkov, V. E., Ogaki, R., Howard, K. A. & Sutherland, D. S. Spatial mapping and quantification of soft and hard protein coronas at silver nanocubes. Nano Lett. 14, 2086-2093 (2014).
25. Beer, C., Foldbjerg, R., Hayashi, Y., Sutherland, D. S. & Autrup, H. Toxicity of silver nanoparticles - nanoparticle or silver ion? Toxicol. Lett. 208, 286-292 (2012).
26. Foldbjerg, R. et al. Silver nanoparticles - wolves in sheep's clothing? Toxicol. Res 4, 563-575 (2015).
27. Gliga, A. R., Skoglund, S., Wallinder, I. O., Fadeel, B. & Karlsson, H. L. Size-dependent cytotoxicity of silver nanoparticles in human lung cells: the role of cellular uptake, agglomeration and Ag release. Part. Fibre. Toxicol 11, 11-27 (2014).
28. Johnston, H. J. et al. A review of the in vivo and in vitro toxicity of silver and gold particulates: particle attributes and biological mechanism responsible for the observed toxicity. Crit. Rev. Toxicol. 40, 328-346 (2010).
29. Henglein, A. Colloidal silver nanoparticles: photochemical preparation and interaction with O2, CCl4, and some metal ions. Chem. Mater. 10, 444-450 (1998).
30. Lok, C.-N. et al. Silver nanoparticles: partial oxidation and antibacterial activities. J. Biol. Inorg. Chem. 12, 527-534 (2007).
31. Sotiriou, G. A., Meyer, A., Knijnenburg, J. T. N., Panke, S. & Pratsinis, S. E. Quantifying the origin of released Ag+ ions from nanosilver. Langmuir 28, 15929-15936 (2012).
32. Liu, J. & Hurt, R. H. Ion release kinetics and particle persistence in aqueous nano-silver colloids. Environ. Sci. Technol. 44, 2169-2175 (2010).
33. Ma, R. et al. Size-controlled dissolution of organic-coated silver nanoparticles. Environ. Sci. Technol. 46, 752-759 (2012).
34. Liu, J., Pennell, K. G. & Hurt, R. H. Kinetics and mechanism of nanosilver oxysulfidation. Environ. Sci. Technol. 45, 7345-7353 (2011).
35. Reinsch, B. C. et al. Sulfidation of silver nanoparticles decreases Escherichia coli growth inhibition. Environ. Sci. Technol. 46, 6992-7000 (2012).
36. Levard, C. et al. Sulfidation of silver nanoparticles: natural antidote to their toxicity. Environ. Sci. Technol. 47, 13440-13448 (2013).
37. Devi, G. P. et al. Sulfidation of silver nanoparticles reduces its toxicity in zebrafish. Aquat. Toxicol. 158, 149-156 (2015).
38. Starnes, D. L. et al. Impact of sulfidation on the bioavailability and toxicity of silver nanoparticles to Caenorhabditis elegans. Environ. Pollut. 196, 239-246 (2015).
39. Kim, B., Park, C.-S., Murayama, S. & Hochella, Jr. M. F. Discovery and characterization of silver sulfide nanoparticles in final sewage sludge products. Environ. Sci. Technol. 44, 7509-7514 (2010).
40. Kent, R. D., Oser, J. G. & Vikesland, P. J. Controlled evaluation of silver nanoparticle sulfidation in full-scale wastewater treatment plant. Environ. Sci. Technol. 48, 8564-8572 (2014).
41. Thalmann, B., Voegelin, A., Sinnet, B., Morgenroth, E. & Kaegi, R. Sulfidation kinetics of silver nanoparticles reacted with metal sulfides. Environ. Sci. Technol. 48, 4885-4892 (2014).
42. Yu, S.-J., Yin, Y.-G., Chao, J.-B., Shen, M.-H. & Liu, J.-F. Highly dynamic PVP-coated silver nanoparticles in aquatic environments: chemical and morphology change induced by oxidation of Ag0 and reduction of Ag+. Environ. Sci. Technol. 48, 403-411 (2014).
43. Liu, J., Sonshine, D. A., Shervani, S. & Hurt, R. H. Controlled release of biologically active silver from nanosilver surfaces. ACS Nano 4, 6903-6913 (2010).
44. Gondikas, A. P. et al. Cysteine-induced modifications of zero-valent silver nanomaterials: implications for particles surface chemistry, aggregation, dissolution, and silver speciation. Environ. Sci. Technol. 46, 7037-7045 (2012).
45. Jiang, X. et al. Fast intracellular dissolution and persistent cellular uptake of silver nanoparticles in CHO-K1 cells: implication for cytotoxicity. Nanotoxicology 9, 181-189 (2015).
46. Wang, L. et al. Use of synchrotron radiation-analytical techniques to reveal chemical origin of silver-nanoparticle cytotoxicity. ACS Nano 9, 6532-6547 (2015).
47. Chen, S. et al. Sulfidation of silver nanowires inside human alveolar epithelial cells: a potential detoxification mechanism. Nanoscale 5, 9839-9847 (2013).
48. Chen, S. et al. High-resolution analytical electron microscopy reveals cell culture media-induced changes to the chemistry of silver nanowires. Environ. Sci. Technol. 47, 13813-13821 (2013).
49. Choi, O. et al. Role of sulfide and ligand strength in controlling nanosilver toxicity. Water. Res 43, 1879-1886 (2009).
50. Bianchini, A. et al. Evaluation of the effect of reactive sulfide on the acute toxicity of silver (I) to Daphnia magna. Part 2: toxicity results. Environ. Toxicol. Chem. 21, 1294-1300 (2002).
51. Mann, R. M., Ernste, M. J., Bell, R. A., Kramer, J. R. & Wood, C. M. Evaluation of the protective effects of reactive sulfide on the acute toxicity of silver to rainbow trout (Oncorhynchus Mykiss). Enviro. Toxicol. Chem 23, 1204-1210 (2004).
52. Selected Powder Diffraction Data for Metals & Alloys Data Book. 1st edn. vol. 1JCPDS International Center for Diffraction Data, 1982).
53. Cia, X., Zeng, J., Zhang, Q., Moran, C. H. & Xia, Y. Recent developments in shape-controlled synthesis of silver nanocrystals. J. Phys. Chem. C 116, 21647-21656 (2012).
54. Wang, Y., Zheng, Y., Huang, C. Z. & Xia, Y. Synthesis of Ag nanocubes 18-32 nm in edge length: the effects of polyol on reduction kinetics, size control and reproducibility. J. Am. Chem. Soc. 135, 1941-1951 (2013).
55. Elechiguerra, J. L. et al. Corrosion at the nanoscale: the case of silver nanowires and nanoparticles. Chem. Mater. 17, 6042-6052 (2005).
56. El-Khairy, L., Ueland, P. M., Refsum, H., Graham, I. M. & Vollset, S. E. Plasma total cysteine as a risk factor for vascular disease. Circulation 103, 2544-2549 (2001).
57. Salemi, G. et al. Blood levels of homocysteine, cysteine, glutathione, folic acid, and vitamin B12 in the acute phase of atherothrombosis stroke. Neural. Sci 30, 361-364 (2009).
58. Levard, C., Hotze, E. M., Lowry, G. V. & Brown, Jr. G. E. Environmental transformations of silver nanoparticles: Impact on stability and toxicity. Environ. Sci. Technol. 46, 6900-6914 (2012).
59. Bopst, M., Haas, C., Car, B. & Engster, H. P. The combined inactivation of tumor necrosis factor and interleukin-6 prevents induction of the major acute phase proteins by endotoxin. Eur. J. Immunol. 28, 4130-4137 (1998).
60. Martinez-Gutierrez, F. et al. Antibacterial activity, inflammatory response, coagulation and cytotoxicity effects of silver nanoparticles. Nanomed. Nanotechnol 8, 328-336 (2012).
61. Park, M.V.D.Z. et al. The effect of particle size on the cytotoxicity, inflammation, developmental toxicity and genotoxicity of silver nanoparticles. Biomaterials 32, 9810-9817 (2011).
62. Driscoll, K. E. TNFa and MIP-2 production: role in particle-induced inflammation and regulation by oxidative stress. Toxicol. Lett. 112-113, 177-184 (2000).
63. Zhang, Q., Li, W., Wen, L.-P., Chen, J. & Xia, Y. Facile synthesis of Ag nanocubes of 30 to 70 nm in edge length with CF3COOAg as a precursor. Chem. Eur. J 16, 10234-10239 (2010).
64. Wiley, B., Sun, Y., Mayers, B. & Xia, Y. Shape-controlled synthesis of metal nanoparticles: the case of silver. Chem. Eur. J 11, 454-463 (2005).
65. Foldbjerg, R., Dang, D. A. & Autrup, H. Cytotoxicity and genotoxicity of silver nanoparticles in the human lung cancer cell line, A549. Arch. Toxicol. 85, 743-750 (2011).
66. Reidy, B., Haase, A., Luch, A., Dawson, K. A. & Lynch, I. Mechanism of silver nanoparticle release, transformation and toxicity: a critical review of current knowledge and recommendations for future studies and applications. Materials 6, 2295-2350 (2013).
67. Helmlinger, J. et al. Silver nanoparticles with different size and shape: equal cytotoxicity, but different antibacterial effects. RSC Adv 6, 18490-18501 (2016).
68. Foldbjerg, R. et al. Global gene expression profiling of human lung epithelial cells after exposure to nanosilver. Toxicol. Sci. 130, 145-157 (2012).
69. Jiang, X. et al. Multi-platform genotoxicity analysis of silver nanoparticles in the model cell line CHO-K1. Toxicol. Lett. 222, 55-63 (2013).