Sheet-type titania, but not P25, induced paraptosis accompanying apoptosis in murine alveolar macrophage cells
Introduction
Manufactured nanomaterials (MNs) are man-made materials produced on a nanoscale, and their market size is expected to reach a $1 trillion by 2015 because of the surprising growth in the nanotechnology industry (Nel et al., 2006). Thus, their prevalence in the environment and the potential risk to human health is a growing concern (Oberdörster et al., 2005, Nohynek and Dufour, 2012, Elsaesser and Howard, 2012, Koivisto et al., 2012). Titanium dioxide nanoparticles (hereafter, titania) are widely used in various products, including paper, plastics, cosmetics, photocatalysts, and paints due to their excellent brightness, their ability to filter ultraviolet (UV) light, superior biocompatibility, and safety (Yin et al., 2013, Earle, 1942, Chen et al., 2013, Skocaj et al., 2011). In contrast, many researchers have reported the hazardous effects of titania in vivo and in vitro (Trouiller et al., 2009, Gui et al., 2013, Zhao et al., 2013, Gao et al., 2012). Hence, the safety of titania is still controversial. In addition, the toxicity of nanoparticles is expected to be dependent on their physicochemical properties. Thus, the toxicity of modified nanoparticles should be investigated independently with raw materials (Hamzeh and Sunahara, 2013, Bolis et al., 2012, Nagy et al., 2012, Nel et al., 2009).
Cellular uptake of nanoparticles and the subsequent biological responses depend on the interactions between unique properties, such as the size, shape, surface chemistry, and crystal structure of the nanoparticles and the specific properties of the biological system used in the experiments. Therefore, we must simultaneously consider both properties for a more accurate understanding of nanoparticle toxicity (Verma and Stellacci, 2010, Akatsuka et al., 2009). In addition, many researchers reported that nanoparticles induce autophagy along with apoptosis (Park et al., 2014a, Zhao et al., 2013, Hussain and Garantziotis, 2013, Hussain et al., 2012, Afeseh Ngwaq et al., 2011). Both types of cell death represent programmed cell death with paraptosis based on morphological features and proteins involved in these pathways (Sperandio et al., 2000, Wang et al., 2012b, Yoon et al., 2010). In our previous study, non-coated iron oxide nanoparticles (FeNPs, rod-type) induced autophagic cell death in RAW264.7 cells, a murine macrophage cell line, whereas they induced paraptosis-like cell death in MH-S cells, a mouse alveolar macrophage cell line (Park et al., 2014a, Park et al., 2014b). Phospholipid-coated FeNPs (sphere-type) did not increase the protein levels of autophagic cell death in MH-S cells despite observed autophagic morphological changes. Herein, we investigated both inherent gene profiles of MH-S cells and the physicochemical properties of sheet-type titania (TNS). Then, we compared the toxicity of TNS and P25, a benchmark control for titania, in MH-S cells, and further explored the molecular response following TNS exposure.
Section snippets
Preparation of TNS
Titania (average primary particle size, 50 nm) and cesium carbonate were obtained from SukgyungAT (Ansan, Korea) and Sigma–Aldrich (St. Louis, MO, USA), respectively. Starting materials were calcined at high temperature to prepare powder of CsxTi2 − x/4□x/4O4, and 1 M HCl solution was added to produce protonic oxide HxTi2 − x/4□x/4O4·yH2O (□, vacancy; x = 0.7, Gao et al., 2008). Then, 2.51 mM tetrabutylammonium hydroxide was added to produce a colloidal suspension of single Ti0.91O2 nanosheet. The
Characterization of TNS
The X-ray diffraction pattern reveals that TNS has a lepidocrocite-type structure with lattice spacing of 0.89 nm, which corresponds to the (1 0 1) reflection peak of anatase TiO2 (data not shown). TNS also had a two-dimensional architecture (Fig. 1A) with a thickness of ∼2 nm, an average lateral size of 390.7 ± 292.8 nm, and an average area of 0.141 ± 0.053 μm2 (data not shown). In addition, TNS (stock concentration: 2331 mg/L) was well dispersed in the vehicle control and was thereby applied to the
Discussion
The respiratory system is a major exposure route to MNs, and alveolar macrophages are one of the primary responders to MNs entering the body. In addition, certain biological events, such as the penetration of nanoparticles into cell membranes and the phagocytosis of antigens, can be induced through a charge-matching mechanism between the cells and the target. Thus, membrane receptors play a key role in mediating the uptake of nanoparticles (Verma and Stellacci, 2010, Akatsuka et al., 2009,
Conflict of interest
The authors declare no conflict of interest.
Transparency document
Acknowledgements
We would like to thank Bengt Fadeel from the Karolinska Institute for helpful discussions. This work was supported by the Basic Science Research Program through the National Research Foundation of Korea funded by the Ministry of Education, Science and Technology (NRF-2011-35B-E00011). This work was also partly supported by the National Platform Technology Programs of the Korean Ministry of Knowledge Economy (grant 10034751).
References (78)
- et al.
Oxidative stress in ALS: key role in motor neuron injury and therapeutic target
Free Radic. Biol. Med.
(2010) - et al.
Hydrophilic/hydrophobic features of TiO2 nanoparticles as a function of crystal phase, surface area and coating, in relation to their potential toxicity in peripheral nervous system
Colloid Interface Sci.
(2012) - et al.
Silica nanoparticles and silver-doped silica nanoparticles induce endoplasmatic reticulum stress response and alter cytochrome P4501A activity
Chemosphere
(2012) - et al.
Toxicology of nanoparticles
Adv. Drug Deliv. Rev.
(2012) - et al.
PVP-coated silver nanoparticles and silver ions induce reactive oxygen species, apoptosis and necrosis in THP-1 monocytes
Toxicol. Lett.
(2009) - et al.
Ovarian dysfunction and gene-expressed characteristics of female mice caused by long-term exposure to titanium dioxide nanoparticles
J. Hazard. Mater.
(2012) - et al.
In vitro cytotoxicity and genotoxicity studies of titanium dioxide (TiO2) nanoparticles in Chinese hamster lung fibroblast cells
Toxicol. In Vitro
(2013) Autophagy and cytokines
Cytokine
(2011)- et al.
Novel derivatives of spirohydantoin induce growth inhibition of followed by apoposis in leukemia cells
Biochem. Pharmacol.
(2009) - et al.
Interaction between U-937 human macrophages and poly(propyleneimine) dendrimers
J. Control Release
(2007)
Interleukin-6 inhibits apoptosis of malignant plasma cells
Cell. Immunol.
Effects of DMSA-coated Fe3O4 magnetic nanoparticles on global gene expression of mouse macrophage RAW264. 7 cells
Toxicol. Lett.
Apoptosis and cell cycle disturbances induced by coumarin and 7-hydroxycoumarin on human lung carcinoma cell lines
Lung Cancer
Antiproliferative effects of some novel synthetic solanidine analogs on HL-60 human leukemia cells in vitro
Steroids
Silver nanoparticles induce cytotoxicity by a Trojan-horse type mechanism
Toxicol. In Vitro
Lysosomes and lysosomal cathepsins in cell death
Biochim. Biophys. Acta
A visual detection of hydrogen peroxide on the basis of Fenton reaction with gold nanoparticles
Anal. Chim. Acta
Rapid synthesis of hexagon-shaped gold nanoplates by microwave assistant method
Mater. Lett.
Necroptosis: an emerging form of programmed cell death
Crit. Rev. Oncol. Hematol.
Superoxide anion and proteasomal dysfunction contribute to curcumin-induced paraptosis malignant breast cancer cells
Free Radic. Biol. Med.
Endoplasmic reticulum stress signaling is involved in silver nanoparticles-induced apoptosis
Int. J. Biochem. Cell Biol.
Peroxynitrite target the epidermal growth factor receptor, Raf-1, and MEK independently to activate MAPK
J. Biol. Chem.
Manganese nanoparticle activates mitochondrial dependent apoptotic signaling and autophagy in dopaminergic neuronal cells
Toxicol. Appl. Pharmacol.
Construction of highly ordered lamellar nanostructures through langmuir-Blodgett deposition of molecularly thin titania nanosheets tens of micrometers wide and their excellent dielectric properties
ACS Nano
The effect of nanoparticle size, shape, and surface chemistry on biological systems
Ann. Rev. Biomed. Eng.
Programmed cell death: molecular mechanisms and implications for safety assessment of nanomaterials
Acc. Chem. Res.
Autophagy contributes to inflammation in patients with TNFR-associated periodic syndrome (TRAPS)
Ann. Rheum. Dis.
Mitochondrial nitric oxide in the signaling of cell integrated responses
Am. J. Physiol. Cell Physiol.
Characterization and preliminary toxicity assay of nano-titanium dioxide additive in sugar-coated chewing gum
Small
Necroptosis: biochemical, physiological and pathological aspects
Pathol. Oncol. Res.
The electrical conductivity of titanium dioxide
Phys. Rev.
Organelle-specific initiation of cell death pathways
Nat. Cell Biol.
Superoxide dismutases: role in redox signaling, vascular function, and diseases
Antioxid. Redox Signal.
Raman scattering properties of a protonic titanate HxTi2 − x/4x/4O4·H2O (vacancy; x = 0.7) with lepidocrocite-type layered structure
J. Phys. Chemistry B
Intragastric exposure to titanium dioxide nanoparticles induced nephrotoxicity in mice, assessed by physiological and gene expression modifications
Part Fibre Toxicol.
Autophagy and IL-1 family cytokines
Front Immunol.
Surface engineering of macrophages with nanoparticles to generate a cell-nanoparticle hybrid vehicle for hypoxia-targeted druy delivery
Int. J. Nanomedicine
Cerium dioxide nanoparticles induce apoptosis and autophagy in human peripheral blood monocytes
ACS Nano
Interplay between apoptotic and autophagy pathways after exposure to cerium dioxide nanoparticles in human monocytes
Autophagy
Cited by (11)
Amorphous silica nanoparticle-induced pulmonary inflammatory response depends on particle size and is sex-specific in rats
2020, Toxicology and Applied PharmacologyCitation Excerpt :The samples were put in Gamble's solution (a simulated lung fluid) to investigate their properties within the lung environment (Marques et al., 2011). The morphology and particle size distribution, and surface charge were analyzed using transmission electron microscopy (TEM: JEM-3000F, JEOL, Japan, 200 kV) and a zeta-potential and particle size analyzer (ELSZ-1000, Photal Otsuka Electronics, Japan), respectively (Park et al., 2011; Park et al., 2014). Five-week-old Sprague-Dawley rats (46 males and 46 females) were purchased from Orient Bio-company (Seoungnam, Korea).
Mitochondrial toxicity of nanomaterials
2020, Science of the Total EnvironmentCitation Excerpt :Ag-NPs inhibit activity of liver mitochondrial complexes II, IV and ATP synthase in Sprague-Dawley male rats (Teodoro et al., 2016). The effects of these MNMs on mitochondrial respiration ultimately result in decreased ATP production and mitochondrial dysfunction (Park et al., 2014a; Tan et al., 2016; Sharma et al., 2017). MNMs have been shown to affect mitochondrial dynamics.
Peroxiredoxin 6 suppresses Muc5ac overproduction in LPS-induced airway inflammation through H<inf>2</inf>O<inf>2</inf>-EGFR-MAPK signaling pathway
2017, Respiratory Physiology and NeurobiologyCitation Excerpt :All above findings supported that LPS-induced goblet cell metaplasia in mice airways was related to Prdx6-mediated ROS-dependent EGFR pathway in vivo. Our previous study, as well as others, reported that MAPK and EGFR phosphorylation may contribute to cell inflammation in an ROS-dependent manner (Casalino-Matsuda et al., 2006; Park et al., 2014; Yang et al., 2011a). In our present study, trachea epithelia with antioxidant treatment of Tempol presented higher Prdx6 and lower ROS levels, which might mediate more LPS-induced Muc5ac mRNA and protein expression.
Interaction of Food-Grade Nanotitania with Human and Mammalian Cell Lines Derived from GI Tract, Liver, Kidney, Lung, Brain, and Heart
2021, Nanotechnology in the Life Sciences