Interaction of polyacrylic acid coated and non-coated iron oxide nanoparticles with human neutrophils.

Iron oxide nanoparticles (ION), with different coatings and sizes, have attracted extensive interest in the last years to be applied in drug delivery, cancer therapy and as contrast agents in imagiologic techniques such as magnetic resonance imaging. However, the safety of these nanoparticles is still not completely established, particularly to host defense systems that are usually recruited for their clearance from the body. In this paper, given the importance of neutrophils in the immune response of the organism to nanoparticles, the effect of polyacrylic acid (PAA)-coated and non-coated ION on human neutrophils was evaluated in vitro, namely their capacity to activate the oxidative burst and to modify their lifespan. The obtained results showed that the studied PAA-coated and non-coated ION triggered neutrophils' oxidative burst in a NADPH oxidase dependent manner, and that PAA-coated ION increased - while non-coated ION prevented - apoptotic signaling and apoptosis. These effects may have important clinical implications in biomedical applications of ION.

[1]  P. Gaehtgens,et al.  Bcl-Xl– and Bax-–Mediated Regulation of Apoptosis of Human Neutrophils Via Caspase-3 , 1999 .

[2]  M. Grandsaigne,et al.  Critical role of mitochondria, but not caspases, during glucocorticosteroid-induced human eosinophil apoptosis. , 2002, American journal of respiratory cell and molecular biology.

[3]  G. Dai,et al.  Superparamagnetic iron oxide does not affect the viability and function of adipose-derived stem cells, and superparamagnetic iron oxide-enhanced magnetic resonance imaging identifies viable cells. , 2009, Magnetic resonance imaging.

[4]  Zhuang Liu,et al.  Ferroferric oxide nanoparticles induce prosurvival autophagy in human blood cells by modulating the Beclin 1/Bcl-2/VPS34 complex , 2014, International journal of nanomedicine.

[5]  Lorenzo Galluzzi,et al.  Mitochondrial membrane permeabilization in cell death. , 2007, Physiological reviews.

[6]  E. M. Reyes-Reyes,et al.  Environmental toxicity, oxidative stress and apoptosis: ménage à trois. , 2009, Mutation research.

[7]  L. Olsen,et al.  On the mechanism of oscillations in neutrophils. , 2010, Biophysical chemistry.

[8]  E. Fernandes,et al.  Nickel induces apoptosis in human neutrophils , 2013, BioMetals.

[9]  Baoan Chen,et al.  Influence of synthetic superparamagnetic iron oxide on dendritic cells , 2011, International journal of nanomedicine.

[10]  Jeremy N Skepper,et al.  Effect of ultrasmall superparamagnetic iron oxide nanoparticles (Ferumoxtran-10) on human monocyte-macrophages in vitro. , 2007, Biomaterials.

[11]  J. Gearhart,et al.  In vitro toxicity of nanoparticles in BRL 3A rat liver cells. , 2005, Toxicology in vitro : an international journal published in association with BIBRA.

[12]  S. Maiti,et al.  Magnetite (Fe3O4) nanocrystals affect the expression of genes involved in the TGF-beta signalling pathway. , 2011, Molecular bioSystems.

[13]  G. Goya,et al.  The influence of colloidal parameters on the specific power absorption of PAA-coated magnetite nanoparticles , 2011, Nanoscale research letters.

[14]  V. Cabuil,et al.  Preparation and properties of monodisperse magnetic fluids , 1995 .

[15]  D. Girard,et al.  Activation of human neutrophils by titanium dioxide (TiO2) nanoparticles. , 2010, Toxicology in vitro : an international journal published in association with BIBRA.

[16]  Z. Sládek,et al.  Neutrophil apoptosis during experimentally induced Staphylococcus aureus mastitis. , 2005, Veterinary research.

[17]  Hong Yang,et al.  Phosphorylation of p53 on Key Serines Is Dispensable for Transcriptional Activation and Apoptosis*♦ , 2004, Journal of Biological Chemistry.

[18]  E. Fernandes,et al.  Nickel induces oxidative burst, NF-κB activation and interleukin-8 production in human neutrophils , 2010, JBIC Journal of Biological Inorganic Chemistry.

[19]  E. Fernandes,et al.  Isolation and activation of human neutrophils in vitro. The importance of the anticoagulant used during blood collection. , 2008, Clinical biochemistry.

[20]  Vincent Castranova,et al.  Iron oxide nanoparticles induce human microvascular endothelial cell permeability through reactive oxygen species production and microtubule remodeling , 2009, Particle and Fibre Toxicology.

[21]  E. Fernandes,et al.  Optimization of experimental settings for the analysis of human neutrophils oxidative burst in vitro. , 2009, Talanta.

[22]  B. Wang,et al.  Endothelial dysfunction and inflammation induced by iron oxide nanoparticle exposure: Risk factors for early atherosclerosis. , 2011, Toxicology letters.

[23]  Seddik Hammad,et al.  Gebel-criteria for risk assessment in nanotoxicology , 2014, EXCLI journal.

[24]  E. Fernandes,et al.  Optical probes for detection and quantification of neutrophils' oxidative burst. A review. , 2009, Analytica chimica acta.

[25]  L. Jonas,et al.  Delay of neutrophil apoptosis by the neuropeptide substance P: involvement of caspase cascade , 2001, Peptides.

[26]  Sungho Jin,et al.  Magnetic nanoparticles for theragnostics. , 2009, Advanced drug delivery reviews.

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

[28]  K. Dassler,et al.  Studying the effect of particle size and coating type on the blood kinetics of superparamagnetic iron oxide nanoparticles , 2012, International journal of nanomedicine.

[29]  Abhalaxmi Singh,et al.  Transferrin-conjugated curcumin-loaded superparamagnetic iron oxide nanoparticles induce augmented cellular uptake and apoptosis in K562 cells. , 2012, Acta biomaterialia.

[30]  Xianglin Shi,et al.  Intracellular signal transduction of cells in response to carcinogenic metals. , 2002, Critical reviews in oncology/hematology.

[31]  S. Orrenius,et al.  Involvement of caspases in neutrophil apoptosis: regulation by reactive oxygen species. , 1998, Blood.

[32]  J. Marshall,et al.  The IL-1β-Converting Enzyme (Caspase-1) Inhibits Apoptosis of Inflammatory Neutrophils Through Activation of IL-1β , 1998, The Journal of Immunology.

[33]  K. Landfester,et al.  The effect of carboxydextran-coated superparamagnetic iron oxide nanoparticles on c-Jun N-terminal kinase-mediated apoptosis in human macrophages. , 2010, Biomaterials.

[34]  C. Marcinkiewicz,et al.  alpha(9)beta(1) integrin engagement inhibits neutrophil spontaneous apoptosis: involvement of Bcl-2 family members. , 2010, Biochimica et biophysica acta.

[35]  Tak Yee Aw,et al.  Reactive oxygen species, cellular redox systems, and apoptosis. , 2010, Free radical biology & medicine.

[36]  K. Sakaguchi,et al.  DNA damage activates p53 through a phosphorylation-acetylation cascade. , 1998, Genes & development.

[37]  A. Dinda,et al.  Concentration-dependent toxicity of iron oxide nanoparticles mediated by increased oxidative stress , 2010, International journal of nanomedicine.

[38]  V. Rasche,et al.  Lysosomal degradation of the carboxydextran shell of coated superparamagnetic iron oxide nanoparticles and the fate of professional phagocytes. , 2010, Biomaterials.

[39]  Diana Anderson,et al.  Zinc oxide nanoparticles induce oxidative DNA damage and ROS-triggered mitochondria mediated apoptosis in human liver cells (HepG2) , 2012, Apoptosis.

[40]  V. Ridger,et al.  Caspase-1-Deficient Mice Have Delayed Neutrophil Apoptosis and a Prolonged Inflammatory Response to Lipopolysaccharide-Induced Acute Lung Injury1 , 2002, The Journal of Immunology.

[41]  M. Nakamoto,et al.  Rapamycin induces p53-independent apoptosis through the mitochondrial pathway in non-small cell lung cancer cells. , 2012, Oncology reports.

[42]  M. Pibiri,et al.  Increased ROS generation and p53 activation in α-lipoic acid-induced apoptosis of hepatoma cells , 2006, Apoptosis.

[43]  E. Fernandes,et al.  Acetaminophen prevents oxidative burst and delays apoptosis in human neutrophils. , 2013, Toxicology letters.

[44]  K. Murase,et al.  Inflammatory imaging with ultrasmall superparamagnetic iron oxide. , 2011, Magnetic resonance imaging.

[45]  Li‐jun Wu,et al.  Reactive oxygen species mediate oridonin-induced HepG2 apoptosis through p53, MAPK, and mitochondrial signaling pathways. , 2008, Journal of pharmacological sciences.

[46]  H. Karlsson,et al.  Copper oxide nanoparticles are highly toxic: a comparison between metal oxide nanoparticles and carbon nanotubes. , 2008, Chemical research in toxicology.

[47]  F. Gao,et al.  Magnetic nanoparticle of Fe3O4 and 5-bromotetrandrin interact synergistically to induce apoptosis by daunorubicin in leukemia cells , 2009, International journal of nanomedicine.

[48]  Jie Wu,et al.  Investigation on mechanism of growth arrest induced by iron oxide nanoparticles in PC12 cells. , 2011, Journal of nanoscience and nanotechnology.

[49]  Yin-Kai Chen,et al.  The promotion of human mesenchymal stem cell proliferation by superparamagnetic iron oxide nanoparticles. , 2009, Biomaterials.

[50]  Yongmin Chang,et al.  The effect of static magnetic fields on the aggregation and cytotoxicity of magnetic nanoparticles. , 2011, Biomaterials.

[51]  Q. Lu,et al.  Fe3O4 nanoparticles with daunorubicin induce apoptosis through caspase 8-PARP pathway and inhibit K562 leukemia cell-induced tumor growth in vivo. , 2011, Nanomedicine : nanotechnology, biology, and medicine.

[52]  William G. Cheadle,et al.  Endotoxin Inhibits Apoptosis but Induces Primary Necrosis in Neutrophils , 2005, Inflammation.

[53]  Jaebeom Lee,et al.  Subtle cytotoxicity and genotoxicity differences in superparamagnetic iron oxide nanoparticles coated with various functional groups , 2011, International journal of nanomedicine.

[54]  Jie Wu,et al.  Neurotoxic potential of iron oxide nanoparticles in the rat brain striatum and hippocampus. , 2013, Neurotoxicology.