Carbohydrate functionalization of silver nanoparticles modulates cytotoxicity and cellular uptake

Journal of Nanobiotechnology

Peter H Seeberger¹  Andreas Luch⁵  Andrea Haase⁵  Larissa Müller²  Chian-Hui Lai³  Guillermo Orts-Gil³  David C Kennedy⁴ 

[1] Institute for Chemistry and Biochemistry, Free University Berlin, Arnimallee 22, Berlin, 14195, Germany;Division 1.1 Inorganic Trace Analysis, Federal Institute for Materials Research and Testing (BAM), Richard-Willstätter-Straße 11, Berlin, 12489, Germany;Department of Biomolecular Systems, Max Planck Institute of Colloids and Interfaces (MPIKG), Potsdam, 14476, Germany;National Research Council Canada (CNRC), 100 Sussex Drive, Ottawa, Ontario, Canada;Departments Chemical and Product Safety, German Federal Institute for Risk Assessment (BfR), Berlin, 10589, Germany

关键词: Bio-interfaces;    Nanotoxicology;    Carbohydrates;    Nanoparticles;    Silver;   

Others  :  1139284
DOI  :  10.1186/s12951-014-0059-z

 received in 2014-08-06, accepted in 2014-12-11,  发布年份 2014

【 摘 要 】

Background

Increasing use of silver nanoparticles (Ag-NPs) in various products is resulting in a greater likelihood of human exposure to these materials. Nevertheless, little is still known about the influence of carbohydrates on the toxicity and cellular uptake of nanoparticles.

Methods

Ag-NPs functionalized with three different monosaccharides and ethylene glycol were synthesized and characterised. Oxidative stress and toxicity was evaluated by protein carbonylation and MTT assay, respectively. Cellular uptake was evaluated by confocal microscopy and ICP-MS.

Results

Ag-NPs coated with galactose and mannose were considerably less toxic to neuronal-like cells and hepatocytes compared to particles functionalized by glucose, ethylene glycol or citrate. Toxicity correlated to oxidative stress but not to cellular uptake.

Conclusions

Carbohydrate coating on silver nanoparticles modulates both oxidative stress and cellular uptake, but mainly the first has an impact on toxicity. These findings provide new perspectives on modulating the bioactivity of Ag-NPs by using carbohydrates.

【 授权许可】

   
2014 Kennedy et al.; licensee BioMed Central.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

【 参考文献 】

• [1]Gao J, Gu H, Xu B: Multifunctional magnetic nanoparticles: design, synthesis, and biomedical applications. Acc Chem Res 2009, 42(8):1097-1107.
• [2]Lai C-H, Chang T-C, Chuang Y-J, Tzou D-L, Lin C-C: Stepwise orthogonal click chemistry toward fabrication of paclitaxel/galactose functionalized fluorescent nanoparticles for HepG2 cell targeting and delivery. Bioconjug Chem 2013, 24(10):1698-1709.
• [3]Reidy B, Haase A, Luch A, Dawson K, Lynch I: Mechanisms of silver nanoparticle release, transformation and toxicity: a critical review of current knowledge and recommendations for future studies and applications. Materials 2013, 6(6):2295-2350.
• [4]Sun TY, Gottschalk F, Hungerbühler K, Nowack B: Comprehensive probabilistic modelling of environmental emissions of engineered nanomaterials. Environ Pollut 2014, 185:69-76.
• [5]Pastoriza-Santos I, Liz-Marzan LM: Colloidal silver nanoplates: state of the art and future challenges. J Mater Chem 2008, 18(15):1724-1737.
• [6]Marradi M, Chiodo F, Garcia I, Penades S: Glyconanoparticles as multifunctional and multimodal carbohydrate systems. Chem Soc Rev 2013, 42(11):4728-4745.
• [7]Lai C-H, Lai N-C, Chuang Y-J, Chou F-I, Yang C-M, Lin C-C: Trivalent galactosyl-functionalized mesoporous silica nanoparticles as a target-specific delivery system for boron neutron capture therapy. Nanoscale 2013, 5(19):9412-9418.
• [8]Chiodo F, Marradi M, Calvo J, Yuste E, Penadés S: Glycosystems in nanotechnology: gold glyconanoparticles as carrier for anti-HIV prodrugs. Beilstein J Org Chem 2014, 10:1339-1346.
• [9]Zhang C, Wan X, Zheng X, Shao X, Liu Q, Zhang Q, Qian Y: Dual-functional nanoparticles targeting amyloid plaques in the brains of Alzheimer's disease mice. Biomaterials 2014, 35(1):456-465.
• [10]Farr TD, Lai C-H, Grünstein D, Orts-Gil G, Wang C-C, Boehm-Sturm P, Seeberger PH, Harms C: Imaging early endothelial inflammation following stroke by core shell silica superparamagnetic glyconanoparticles that target selectin. Nano Lett 2014, 14(4):2130-2134.
• [11]Seeberger PH, Werz DB: Synthesis and medical applications of oligosaccharides. Nature 2007, 446(7139):1046-1051.
• [12]Mammen M, Choi S-K, Whitesides GM: Polyvalent interactions in biological systems: implications for design and use of multivalent ligands and inhibitors. Angew Chem Int Ed 1998, 37(20):2754-2794.
• [13]Yin Win K, Feng S-S: Effects of particle size and surface coating on cellular uptake of polymeric nanoparticles for oral delivery of anticancer drugs. Biomaterials 2005, 26(15):2713-2722.
• [14]Chithrani BD, Chan WCW: Elucidating the mechanism of cellular uptake and removal of protein-coated gold nanoparticles of different sizes and shapes. Nano Lett 2007, 7(6):1542-1550.
• [15]Miao A-J, Schwehr KA, Xu C, Zhang S-J, Luo Z, Quigg A, Santschi PH: The algal toxicity of silver engineered nanoparticles and detoxification by exopolymeric substances. Environ Pollut 2009, 157(11):3034-3041.
• [16]Sur I, Cam D, Kahraman M, Baysal A, Culha M: Interaction of multi-functional silver nanoparticles with living cells. Nanotechnology 2010, 21(17):175104.
• [17]Johnston HJ, Hutchison G, Christensen FM, Peters S, Hankin S, Stone V: A review of the in vivo and in vitro toxicity of silver and gold particulates: particle attributes and biological mechanisms responsible for the observed toxicity. Crit Rev Toxicol 2010, 40(4):328-346.
• [18]Pillai ZS, Kamat PV: What factors control the size and shape of silver nanoparticles in the citrate ion reduction method? J Phys Chem B 2003, 108(3):945-951.
• [19]Woehrle GH, Hutchison JE, Özkâr S, Finke RG: Analysis of nanoparticle transmission electron microscopy data using a public- domain image-processing program, image. Turk J Chem 2006, 30:1-13.
• [20]Kittler S, Greulich C, Gebauer JS, Diendorf J, Treuel L, Ruiz L, Gonzalez-Calbet JM, Vallet-Regi M, Zellner R, Köller M, Epple M: The influence of proteins on the dispersability and cell-biological activity of silver nanoparticles. J Mater Chem 2010, 20:512-518.
• [21]Drescher D, Orts-Gil G, Laube G, Natte K, Veh RW, Oesterle W, Kneipp J: Toxicity of amorphous silica nanoparticles on eukaryotic cell model is determined by particle agglomeration and serum protein adsorption effects. Anal Bioanal Chem 2011, 400(5):1593-1604.
• [22]Orts-Gil G, Natte K, Drescher D, Bresch H, Mantion A, Kneipp J, Österle W: Characterisation of silica nanoparticles prior to in vitro studies: from primary particles to agglomerates. J Nanoparticle Res 2011, 13(4):1593-1604.
• [23]Lai C-H, Lin C-Y, Wu H-T, Chan H-S, Chuang Y-J, Chen C-T, Lin C-C: Galactose encapsulated multifunctional nanoparticle for HepG2 cell internalization. Adv Funct Mater 2010, 20(22):3948-3958.
• [24]Kittler S, Greulich C, Diendorf J, Köller M, Epple M: Toxicity of silver nanoparticles increases during storage because of slow dissolution under release of silver ions. Chem Mater 2010, 22(16):4548-4554.
• [25]Loza K, Diendorf J, Sengstock C, Ruiz-Gonzalez L, Gonzalez-Calbet JM, Vallet-Regi M, Koller M, Epple M: The dissolution and biological effects of silver nanoparticles in biological media. J Mater Chem B 2014, 2(12):1634-1643.
• [26]Park E-J, Yi J, Kim Y, Choi K, Park K: Silver nanoparticles induce cytotoxicity by a Trojan-horse type mechanism. Toxicol in Vitro 2010, 24(3):872-878.
• [27]Vaseem M, Tripathy N, Khang G, Hahn Y-B: Green chemistry of glucose-capped ferromagnetic hcp-nickel nanoparticles and their reduced toxicity. RSC Adv 2013, 3(25):9698-9704.
• [28]El Badawy AM, Silva RG, Morris B, Scheckel KG, Suidan MT, Tolaymat TM: Surface charge-dependent toxicity of silver nanoparticles. Environ Sci Technol 2010, 45(1):283-287.
• [29]Barondes S, Rosen S: Cell surface carbohydrate-binding proteins: role in cell recognition. Neuronal Recognit Springer US 1976, 11:331-335.
• [30]Petri-Fink A, Steitz B, Finka A, Salaklang J, Hofmann H: Effect of cell media on polymer coated superparamagnetic iron oxide nanoparticles (SPIONs): colloidal stability, cytotoxicity, and cellular uptake studies. Eur J Pharm Biopharm 2008, 68(1):129-137.
• [31]Bajaj A, Samanta B, Yan H, Jerry DJ, Rotello VM: Stability, toxicity and differential cellular uptake of protein passivated-Fe3O4nanoparticles. J Mater Chem 2009, 19(35):6328-6331.
• [32]Lesniak A, Fenaroli F, Monopoli MP, Äberg C, Dawson KA, Salvati A: Effects of the presence or absence of a protein corona on silica nanoparticle uptake and impact on cells. ACS Nano 2012, 6(7):5845-5857.
• [33]Dorota Walczyk FBB, Monopoli MP, Lynch I, Dawson KA: What the cell “sees” in bionanoscience. J Am Chem Soc 2010, 132(16):5761-5768.
• [34]Lynch I, Cedervall T, Lundqvist M, Cabaleiro-Lago C, Linse S, Dawson KA: The nanoparticle-protein complex as a biological entity; a complex fluids and surface science challenge for the 21st century. Adv Colloid Interf Sci 2007, 134–135:167-174.
• [35]Monopoli M, Walczyk D, Campbell A, Elia G, Lynch I, Baldelli Bombelli F, Dawson K: Physical-chemical aspects of protein corona: relevance to in vitro and in vivo biological impacts of nanoparticles. J Am Chem Soc 2011, 133:2525-2534.