Effects of the presence or absence of a protein corona on silica nanoparticle uptake and impact on cells.

Nanoparticles enter cells through active processes, thanks to their capability of interacting with the cellular machinery. The protein layer (corona) that forms on their surface once nanoparticles are in contact with biological fluids, such as the cell serum, mediates the interactions with cells in situ. As a consequence of this, here we show that the same nanomaterial can lead to very different biological outcomes, when exposed to cells in the presence or absence of a preformed corona. In particular, silica nanoparticles exposed to cells in the absence of serum have a stronger adhesion to the cell membrane and higher internalization efficiency, in comparison to what is observed in medium containing serum, when a preformed corona is present on their surface. The different exposure conditions not only affect the uptake levels but also result in differences in the intracellular nanoparticle location and impact on cells. Interestingly, we also show that after only one hour of exposure, a corona of very different nature forms on the nanoparticles exposed to cells in the absence of serum. Evidence suggests that these different outcomes can all be connected to the different adhesion and surface properties in the two conditions.

[1]  Jun-Sung Kim,et al.  Cellular uptake of magnetic nanoparticle is mediated through energy-dependent endocytosis in A549 cells , 2006, Journal of veterinary science.

[2]  Chad A Mirkin,et al.  Scavenger receptors mediate cellular uptake of polyvalent oligonucleotide-functionalized gold nanoparticles. , 2010, Bioconjugate chemistry.

[3]  Kenneth A. Dawson,et al.  Role of cell cycle on the cellular uptake and dilution of nanoparticles in a cell population. , 2011, Nature nanotechnology.

[4]  Jim E Riviere,et al.  An index for characterization of nanomaterials in biological systems. , 2010, Nature nanotechnology.

[5]  Satyajit Mayor,et al.  Pathways of clathrin-independent endocytosis , 2007, Nature Reviews Molecular Cell Biology.

[6]  Katharina Landfester,et al.  Differential uptake of functionalized polystyrene nanoparticles by human macrophages and a monocytic cell line. , 2011, ACS nano.

[7]  I. Zuhorn,et al.  Size-dependent internalization of particles via the pathways of clathrin- and caveolae-mediated endocytosis. , 2004, The Biochemical journal.

[8]  L. Kobzik,et al.  Lung macrophage uptake of unopsonized environmental particulates. Role of scavenger-type receptors. , 1995, Journal of immunology.

[9]  Min Huang,et al.  Uptake of FITC-Chitosan Nanoparticles by A549 Cells , 2002, Pharmaceutical Research.

[10]  Feng Zhang,et al.  Quantitative analysis of the protein corona on FePt nanoparticles formed by transferrin binding , 2010, Journal of The Royal Society Interface.

[11]  Kemin Wang,et al.  Uptake of silica-coated nanoparticles by HeLa cells. , 2005, Journal of nanoscience and nanotechnology.

[12]  H. McMahon,et al.  Mechanisms of endocytosis. , 2009, Annual review of biochemistry.

[13]  Sanjay Mathur,et al.  Microsomal Glutathione Transferase 1 Protects Against Toxicity Induced by Silica Nanoparticles but Not by Zinc Oxide Nanoparticles , 2012, ACS nano.

[14]  K. Dawson,et al.  Effects of Transport Inhibitors on the Cellular Uptake of Carboxylated Polystyrene Nanoparticles in Different Cell Lines , 2011, PloS one.

[15]  Kenneth A. Dawson,et al.  Nanobiotechnology: Nanoparticle coronas take shape , 2011 .

[16]  V. Rotello,et al.  Stability, toxicity and differential cellular uptake of protein passivated-Fe3O4 nanoparticles , 2009 .

[17]  K. Dawson,et al.  Experimental and theoretical comparison of intracellular import of polymeric nanoparticles and small molecules: toward models of uptake kinetics. , 2011, Nanomedicine : nanotechnology, biology, and medicine.

[18]  R. Zhou,et al.  Binding of blood proteins to carbon nanotubes reduces cytotoxicity , 2011, Proceedings of the National Academy of Sciences.

[19]  Albert Duschl,et al.  Time evolution of the nanoparticle protein corona. , 2010, ACS nano.

[20]  Iseult Lynch,et al.  Serum heat inactivation affects protein corona composition and nanoparticle uptake. , 2010, Biomaterials.

[21]  A. Shevchenko,et al.  Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. , 1996, Analytical chemistry.

[22]  Wolfgang J Parak,et al.  A quantitative fluorescence study of protein monolayer formation on colloidal nanoparticles. , 2009, Nature nanotechnology.

[23]  Sara Linse,et al.  Understanding the nanoparticle–protein corona using methods to quantify exchange rates and affinities of proteins for nanoparticles , 2007, Proceedings of the National Academy of Sciences.

[24]  Alison Elder,et al.  Correlating physico-chemical with toxicological properties of nanoparticles: the present and the future. , 2010, ACS nano.

[25]  P. Netti,et al.  Effect of serum proteins on polystyrene nanoparticle uptake and intracellular trafficking in endothelial cells , 2011 .

[26]  S. K. Sundaram,et al.  Adsorbed proteins influence the biological activity and molecular targeting of nanomaterials. , 2007, Toxicological sciences : an official journal of the Society of Toxicology.

[27]  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.

[28]  Stephanie E. A. Gratton,et al.  The effect of particle design on cellular internalization pathways , 2008, Proceedings of the National Academy of Sciences.

[29]  Jin-Ho Choy,et al.  Toxicological effects of inorganic nanoparticles on human lung cancer A549 cells. , 2009, Journal of inorganic biochemistry.

[30]  Monty Liong,et al.  Mesoporous Silica Nanoparticles for Cancer Therapy: Energy-Dependent Cellular Uptake and Delivery of Paclitaxel to Cancer Cells , 2007, Nanobiotechnology : the journal at the intersection of nanotechnology, molecular biology, and biomedical sciences.

[31]  Qing Huang,et al.  Effects of serum proteins on intracellular uptake and cytotoxicity of carbon nanoparticles , 2009 .

[32]  Iseult Lynch,et al.  Protein-nanoparticle interactions: What does the cell see? , 2009, Nature nanotechnology.

[33]  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.

[34]  Sandra L. Schmid,et al.  Regulated portals of entry into the cell , 2003, Nature.

[35]  T. Xia,et al.  Understanding biophysicochemical interactions at the nano-bio interface. , 2009, Nature materials.

[36]  Kohei Tahara,et al.  Improved cellular uptake of chitosan-modified PLGA nanospheres by A549 cells. , 2009, International journal of pharmaceutics.

[37]  Warren C W Chan,et al.  Nanoparticle-mediated cellular response is size-dependent. , 2008, Nature nanotechnology.

[38]  Iseult Lynch,et al.  What the cell "sees" in bionanoscience. , 2010, Journal of the American Chemical Society.

[39]  Kirsten Sandvig,et al.  Endocytosis and intracellular transport of nanoparticles: Present knowledge and need for future studies , 2011 .

[40]  Ki Chul Park,et al.  Effect of dispersants of multi-walled carbon nanotubes on cellular uptake and biological responses , 2011, International journal of nanomedicine.

[41]  C. Fan,et al.  Protein corona-mediated mitigation of cytotoxicity of graphene oxide. , 2011, ACS nano.

[42]  Sara Linse,et al.  Detailed identification of plasma proteins adsorbed on copolymer nanoparticles. , 2007, Angewandte Chemie.

[43]  R. Hamilton,et al.  MARCO Mediates Silica Uptake and Toxicity in Alveolar Macrophages from C57BL/6 Mice* , 2006, Journal of Biological Chemistry.

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

[45]  G. Oberdörster,et al.  Safety assessment for nanotechnology and nanomedicine: concepts of nanotoxicology , 2010, Journal of internal medicine.

[46]  Iseult Lynch,et al.  Physical-chemical aspects of protein corona: relevance to in vitro and in vivo biological impacts of nanoparticles. , 2011, Journal of the American Chemical Society.

[47]  K. Dawson,et al.  Time and space resolved uptake study of silica nanoparticles by human cells. , 2011, Molecular bioSystems.

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