Importance of agglomeration state and exposure conditions for uptake and pro-inflammatory responses to amorphous silica nanoparticles in bronchial epithelial cells

Abstract Amorphous silica nanoparticles (SiNPs, 30 and 50 nm) and rhodamine-coated SiNPs (50 nm) were examined for their ability to induce pro-inflammatory responses and cytotoxicity in BEAS-2B cells under different experimental conditions. The SiNPs formed micrometre-sized agglomerates in the absence of bovine serum albumin (BSA) in the culture medium, whereas with BSA (0.1%) they were much less agglomerated. All the SiNPs induced IL-6 and IL-8 responses, as measured by ELISA and real-time PCR. The responses were more marked without BSA and higher for the rhodamine SiNPs than the plain ones. Rhodamine SiNPs were not taken up by cells during a 3-h exposure, even though cytokine mRNAs were up-regulated. In conclusion, agglomerated SiNPs induced more potent cytokine responses than the non-agglomerated ones; either due to the agglomeration state per se or more conceivably to a change in surface reactivity against cellular targets due to BSA. Furthermore, cytokine expression was up-regulated independently of SiNP uptake.

[1]  Bengt Fadeel,et al.  Better safe than sorry: Understanding the toxicological properties of inorganic nanoparticles manufactured for biomedical applications. , 2010, Advanced drug delivery reviews.

[2]  L. Murr,et al.  Cytotoxic Responses and Potential Respiratory Health Effects of Carbon and Carbonaceous Nanoparticulates in the Paso del Norte Airshed Environment , 2008, International journal of environmental research and public health.

[3]  M. Lag,et al.  Particles from wood smoke and traffic induce differential pro-inflammatory response patterns in co-cultures. , 2008, Toxicology and applied pharmacology.

[4]  K. O'Reilly,et al.  Crystalline and amorphous silica differentially regulate the cyclooxygenase-prostaglandin pathway in pulmonary fibroblasts: implications for pulmonary fibrosis. , 2005, American journal of physiology. Lung cellular and molecular physiology.

[5]  E. Antignac,et al.  Safety assessment of personal care products/cosmetics and their ingredients. , 2010, Toxicology and applied pharmacology.

[6]  Chung-Yuan Mou,et al.  The effect of surface charge on the uptake and biological function of mesoporous silica nanoparticles in 3T3-L1 cells and human mesenchymal stem cells. , 2007, Biomaterials.

[7]  R. Hamilton,et al.  A comparison of dispersing media for various engineered carbon nanoparticles , 2007, Particle and Fibre Toxicology.

[8]  A. C. Hunter,et al.  Nanomedicine: current status and future prospects , 2005, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[9]  Benoit Nemery,et al.  Assay conditions can influence the outcome of cytotoxicity tests of nanomaterials: better assay characterization is needed to compare studies. , 2010, Toxicology in vitro : an international journal published in association with BIBRA.

[10]  Conrad Coester,et al.  Particle and Fibre Toxicology BioMed Central Methodology , 2008 .

[11]  P. Whitefield,et al.  Quantification of F(2)-isoprostane isomers in cultured human lung epithelial cells after silica oxide and metal oxide nanoparticle treatment by liquid chromatography/tandem mass spectrometry. , 2010, Talanta.

[12]  J. Bacri,et al.  Intracellular uptake of anionic superparamagnetic nanoparticles as a function of their surface coating. , 2003, Biomaterials.

[13]  T Myran,et al.  Mineral and/or metal content as critical determinants of particle-induced release of IL-6 and IL-8 from A549 cells. , 2000, Journal of toxicology and environmental health. Part A.

[14]  Saber M Hussain,et al.  Characterization of nanomaterial dispersion in solution prior to in vitro exposure using dynamic light scattering technique. , 2008, Toxicological sciences : an official journal of the Society of Toxicology.

[15]  Kenneth A. Dawson,et al.  Protein–Nanoparticle Interactions , 2008, Nano-Enabled Medical Applications.

[16]  Eun-Jung Park,et al.  Oxidative stress and pro-inflammatory responses induced by silica nanoparticles in vivo and in vitro. , 2009, Toxicology letters.

[17]  Giulio Caracciolo,et al.  Surface adsorption of protein corona controls the cell internalization mechanism of DC-Chol-DOPE/DNA lipoplexes in serum. , 2010, Biochimica et biophysica acta.

[18]  Shigeru Deguchi,et al.  Stabilization of C60 nanoparticles by protein adsorption and its implications for toxicity studies. , 2007, Chemical research in toxicology.

[19]  Jiao Sun,et al.  Endothelial cells dysfunction induced by silica nanoparticles through oxidative stress via JNK/P53 and NF-kappaB pathways. , 2010, Biomaterials.

[20]  T. Hirano,et al.  IL-6 signal transduction and its physiological roles: the signal orchestration model. , 2003, Reviews of physiology, biochemistry and pharmacology.

[21]  Albert Duschl,et al.  Dispersion medium modulates oxidative stress response of human lung epithelial cells upon exposure to carbon nanomaterial samples. , 2009, Toxicology and applied pharmacology.

[22]  K. Landfester,et al.  Uptake of functionalized, fluorescent-labeled polymeric particles in different cell lines and stem cells. , 2006, Biomaterials.

[23]  Laetitia Gonzalez,et al.  Synthesis and characterization of stable monodisperse silica nanoparticle sols for in vitro cytotoxicity testing. , 2010, Langmuir : the ACS journal of surfaces and colloids.

[24]  Sara Linse,et al.  The nanoparticle-protein complex as a biological entity; a complex fluids and surface science challenge for the 21st century. , 2007, Advances in colloid and interface science.

[25]  James L. McGrath,et al.  The influence of protein adsorption on nanoparticle association with cultured endothelial cells. , 2009, Biomaterials.

[26]  Jinhee Choi,et al.  Oxidative stress of silica nanoparticles in human bronchial epithelial cell, Beas-2B. , 2009, Toxicology in vitro : an international journal published in association with BIBRA.

[27]  G Chambers,et al.  Single walled carbon nanotubes induce indirect cytotoxicity by medium depletion in A549 lung cells. , 2008, Toxicology letters.

[28]  Laetitia Gonzalez,et al.  Nominal and effective dosimetry of silica nanoparticles in cytotoxicity assays. , 2008, Toxicological sciences : an official journal of the Society of Toxicology.

[29]  T. Schiestel,et al.  A nonviral DNA delivery system based on surface modified silica-nanoparticles can efficiently transfect cells in vitro. , 2000, Bioconjugate chemistry.

[30]  Feng Gao,et al.  Oxidative stress contributes to silica nanoparticle-induced cytotoxicity in human embryonic kidney cells. , 2009, Toxicology in vitro : an international journal published in association with BIBRA.

[31]  Nicklas Raun Jacobsen,et al.  Lung inflammation and genotoxicity following pulmonary exposure to nanoparticles in ApoE-/- mice , 2009, Particle and Fibre Toxicology.

[32]  Joel G Pounds,et al.  Particokinetics in vitro: dosimetry considerations for in vitro nanoparticle toxicity assessments. , 2007, Toxicological sciences : an official journal of the Society of Toxicology.

[33]  T. Guilarte,et al.  Silica-Based Nanoparticle Uptake and Cellular Response by Primary Microglia , 2009, Environmental health perspectives.

[34]  Laetitia Gonzalez,et al.  Size-dependent cytotoxicity of monodisperse silica nanoparticles in human endothelial cells. , 2009, Small.

[35]  J. Veranth,et al.  Inflammatory cytokines and cell death in BEAS-2B lung cells treated with soil dust, lipopolysaccharide, and surface-modified particles. , 2004, Toxicological sciences : an official journal of the Society of Toxicology.

[36]  Yi Zhang,et al.  The effect of multiwalled carbon nanotube agglomeration on their accumulation in and damage to organs in mice , 2009 .

[37]  Moonjung Choi,et al.  Cellular uptake, cytotoxicity, and innate immune response of silica-titania hollow nanoparticles based on size and surface functionality. , 2010, ACS nano.

[38]  Flemming R Cassee,et al.  Impact of agglomeration state of nano- and submicron sized gold particles on pulmonary inflammation , 2010, Particle and Fibre Toxicology.

[39]  Minbo Lan,et al.  Nano-SiO2 induces apoptosis via activation of p53 and Bax mediated by oxidative stress in human hepatic cell line. , 2010, Toxicology in vitro : an international journal published in association with BIBRA.

[40]  R. Hamel,et al.  Carbon black and titanium dioxide nanoparticles induce pro-inflammatory responses in bronchial epithelial cells: Need for multiparametric evaluation due to adsorption artifacts , 2009, Inhalation toxicology.

[41]  Parag Aggarwal,et al.  Nanoparticle interaction with plasma proteins as it relates to particle biodistribution, biocompatibility and therapeutic efficacy. , 2009, Advanced drug delivery reviews.

[42]  Vincent Castranova,et al.  Pulmonary Inflammation After Intraperitoneal Administration of Ultrafine Titanium Dioxide (TiO2) At Rest or in Lungs Primed with Lipopolysaccharide , 2010, Journal of toxicology and environmental health. Part A.

[43]  K. Chung,et al.  Cytokines in chronic obstructive pulmonary disease , 2001, European Respiratory Journal.

[44]  Iqbal Ahmad,et al.  Nanotoxicity of pure silica mediated through oxidant generation rather than glutathione depletion in human lung epithelial cells. , 2010, Toxicology.

[45]  Kenneth A. Dawson,et al.  Nanoparticle size and surface properties determine the protein corona with possible implications for biological impacts , 2008, Proceedings of the National Academy of Sciences.

[46]  A Tossavainen,et al.  Preparation of nanoparticle dispersions for in-vitro toxicity testing , 2009, Human & experimental toxicology.

[47]  Wei Wang,et al.  Toxicity of amorphous silica nanoparticles in mouse keratinocytes , 2009 .

[48]  John Meurig Thomas.  Principles and practice of heterogeneous catalysis , 1996 .

[49]  M. Lag,et al.  Cytokine and chemokine expression patterns in lung epithelial cells exposed to components characteristic of particulate air pollution. , 2009, Toxicology.

[50]  Aldert H Piersma,et al.  In vitro developmental toxicity test detects inhibition of stem cell differentiation by silica nanoparticles. , 2009, Toxicology and applied pharmacology.

[51]  Yinfa Ma,et al.  Study of uptake and loss of silica nanoparticles in living human lung epithelial cells at single cell level , 2009, Analytical and bioanalytical chemistry.