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Keywords: We synthesised a new type of photochromic tungsten oxide nanoparticles, analysed their photocatalytic activity
Tungsten oxide and carried out a thorough analysis of their effect on prokaryotic and eukaryotic organisms. Ultrasmall hydrated
Nanoparticles tungsten oxide nanoparticles were prepared by means of hydrothermal treatment of tungstic acid in the presence
Phototoxicity of polyvinylpyrrolidone as a template, stabiliser and growth regulator. Tungstic acid was synthesised through an
Apoptosis
ion-exchange method using sodium tungstate solution and a strongly acidic cation exchange resin.
UV irradiation
Upon illumination, photochromic nanoparticles of WO3 were shown to increase greatly their toxicity against
both bacterial (both gram-positive and gram-negative – P. aeruginosa, E. coli and S. aureus) and mammalian cells
(primary mouse embryonic fibroblasts); under the same conditions, fungi (C. albicans) were less sensitive to the
action of tungsten oxide nanoparticles. UV irradiation of primary mouse fibroblasts in the presence of WO3
nanoparticles demonstrated a time- and dose-dependent toxic effect, the latter leading to a significant decrease
in dehydrogenase activity and an increase in the number of dead cells. WO3 nanoparticles were photo-
catalytically active under both UV light and even diffused daylight filtered through a window glass, leading to
indigo carmine organic dye discolouration.
The obtained experimental data not only show good prospects for biomedical applications of tungsten tri-
oxide, but also demonstrate the need for clear control of biosafety when it is used in various household materials
and appliances.
1. Introduction tance levels depending on changing needs [1]. One of the most pro-
mising materials for photochromic films or coatings is nanocrystalline
The modern technological paradigm requires research and devel- tungsten oxide, an n-type wide-bandgap semiconductor with a chemical
opment into new materials with specific physical and chemical prop- type of chromism [2,3]. The electro-, photo- and chemochromic prop-
erties. Recently, much attention has been paid to the development of erties of tungsten oxide (WO3) are widely used in electronic displays,
various types of stimuli-responsive materials, which are able to change optical modulators, windows with adjustable light transmission, rear-
their characteristics in response to external factors. For instance, in the view mirrors in cars, etc. [4–7]. Under light irradiation, exposure to
context of energy-saving, smart photo- or electrochromic materials chemical reagents or the application of an electric field, stoichiometric
have been developed which are able to control the throughput of visible WO3 (faintly yellowish) undergoes a number of serial transformations,
light and solar radiation into buildings by having different transmit- reversibly forming brightly coloured products [8]:
⁎
Corresponding author.
E-mail address: van@igic.ras.ru (V.K. Ivanov).
https://doi.org/10.1016/j.jphotobiol.2017.11.021
Received 15 August 2017; Received in revised form 14 November 2017; Accepted 15 November 2017
Available online 20 November 2017
1011-1344/ © 2017 Elsevier B.V. All rights reserved.
A.L. Popov et al. Journal of Photochemistry & Photobiology, B: Biology 178 (2018) 395–403
Fig. 1. Schematic diagram of the interaction mechanisms between light and WO3 nanoparticles in semiconductor (A) and plasmonic (B) states. Photocatalysis, autophotoreduction and
plasmonic heating are demonstrated.
In addition to the above-mentioned applications, tungsten oxide is contact with living cells, these ROS can cause oxidative stress, resulting
one of the most thoroughly studied photocatalysts [9–15] for organic in cell death. Another specific tungsten oxide feature is that it possesses
dye degradation. WO3 nanoparticles of different morphologies, ob- photoactivity at a wide range of wavelengths. The most widely explored
tained by the hydrothermal-microwave method, have been shown to TiO2-photocatalysts are effective under UV light only, while WO3-based
possess photocatalytic properties with respect to the discolouration of ones can change their bandgap upon irradiation, and thus tungsten
rhodamine B, indigo carmine and tetracycline hydrochloride under trioxide could be an effective visible light photocatalyst, wherein the
UV–vis irradiation [11]. WO3 nanoparticles obtained by surfactant-as- absorbed efficiency of sunlight can be enhanced enormously.
sisted sonication have provided a high rate of rhodamine B and indigo The autophotoreduction of tungsten oxide is accompanied by for-
carmine degradation under xenon lamp irradiation [12]. Multi-phase mation of free charge carriers, so photochromic colouration of tungsten
WO3 samples possess improved photocatalytic activity, (as demon- oxide occurs due to the local surface plasmon resonance (LSPR) arising
strated by the bleaching of rhodamine B), that can be attributed to a from appreciable free carrier concentrations [17,18]. It is well known
decrease in the electron-hole recombination rate, owing to the forma- that the interaction of plasmonic particles and light (HxWO3 → HxWO3⁎
tion of interphase junctions [13]. The efficient degradation of methy- photoexcitation) leads not only to redox processes on their surface (left
lene blue dye by tungsten oxide nanoplates, synthesised using a hy- part of Fig. 1, B), but also to the partial conversion of electromagnetic
drothermal or microwave-hydrothermal method, has been shown under energy into heat (right part of Fig. 1, B). The volumetric generation of
UV light irradiation [14]. The photocatalytic activity of WO3 nano- heat within the plasmonic nanoparticle Q(r, t) is affected by the in-
particles (obtained by annealing (NH4)xWO3 − y at 500 °C in air) and tensity of light, the particle's internal electromagnetic field distribution,
nanorods (prepared using a hydrothermal method using Na2WO4, HCl, and the thermal and electrical conductivity of the particle's material
(COOH)2 and NaHSO4 precursors at 200 °C) has been confirmed by the [18]:
decomposition of methyl orange in an aqueous solution under UV light
1 4πnk
σE (̃ r , t ) ∙E ̃ (r, t ); σ =
∗
irradiation [15]. Q (r , t ) =
2 λi μc
The common mechanism for organic dye degradation by photo-
active semiconductor (photocatalyst) is represented in the left part of where Ẽ(r, t) and Ẽ∗(r, t) are the generated electric field and its complex
Fig. 1, A: conjugate within the nanoparticles; σ – electrical conductivity at optical
When a photocatalyst absorbs light that has an energy that exceeds frequencies; λi – incident light wavelength; μ – relative magnetic per-
the semiconductor's bandgap, an electron of the valence band is pro- meability of the nanoparticle, and n and k – the real and imaginary
moted to the conduction band, thus creating an electron (e−)/hole (h+) parts of the refraction index of the nanoparticle, respectively. Plas-
pair. Due to the semiconductor's photoexcitation (WO3 → WO3⁎) and monic nanoparticles of non-stoichiometric tungsten oxide have been
the generation of electron/hole pairs, oxidation-reduction reactions used for photothermal cancer treatment upon IR irradiation [18–23].
take place at the surface: electrons reduce and holes oxidise the mole- Thus, volumetric heating of WO3 nanoparticles upon irradiation can
cules of the surrounding substrate (Sub). Upon contact between the dye bring an additional contribution to cytotoxicity, and thus should be
and the photoexcited nanoparticle, direct redox decomposition of the taken into account.
dye molecule occurs (Sub = Dye). More often, the first stage of pho- For this paper, we synthesised a new type of photochromic tungsten
tocatalysis is the redox transformation of water and/or oxygen oxide nanoparticles, analysed their photocatalytic activity and carried
(Sub = H2O, O2), forming the reactive oxygen species (ROS), which out a thorough analysis of their effect on prokaryotic and eukaryotic
then destroy other substances, (the indirect redox decomposition of the organisms. WO3 nanoparticles possess both dark and light cytotoxicity,
dye molecule). Obviously, the photocatalytic activity of the material which significantly distinguishes them from common photocatalysts,
can affect not only the decomposition of organic dyes, but also the and opens up new possibilities for their practical use.
biological components of living cells.
The mechanism of tungsten oxide photo-induced chromism (au-
tophotoreduction) is represented in the right part of Fig. 1, A. The ex- 2. Materials and Methods
cited electrons cause the reduction of tungsten (6 +) to (5 +) ions,
leading to the formation of coloured, non-stoichiometric, hydrated 2.1. Tungsten Oxide Nanoparticles
tungsten oxide (HxWO3, 0 < x < 1); the holes oxidise substrate (for
example, water [16]), forming ROS, such as hydroxyl radicals. Upon Ultrasmall tungsten oxide nanoparticles were synthesised by means
of hydrothermal treatment of tungstic acid in the presence of
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A.L. Popov et al. Journal of Photochemistry & Photobiology, B: Biology 178 (2018) 395–403
polyvinylpyrrolidone (PVP K-30, average mol. wt. 40,000) as a tem- Microorganisms were cultured in a slant meat-peptone agar medium
plate, stabiliser and growth regulator. Tungstic acid was prepared at 37°C for 24 h. Then they were suspended in a physiological isotonic
through an ion-exchange method using sodium tungstate (Na2WO4) solution (0.85% NaCl) and adjusted to the McFarland turbidity stan-
solution and a strongly acidic cation exchange resin (Amberlite® dard no.4 (1.2 × 109 CFU/ml). Obtained suspensions were diluted, by
IR120). Briefly, ion exchange resin (in a hydrogen form) was swollen in saline, to the required concentrations and further used to determine the
water and loaded into a glass column of 200 ml volume. Then, 100 ml antimicrobial properties of WO3 nanoparticles.
of 0.05 M sodium tungstate solution was passed through the column,
dropwise, 4 g of PVP was added to the obtained eluent, and the solution 2.3.2. Bacterial Viability Assays
was transferred to a flask and stirred for 4 h under reflux. During Two antimicrobial susceptibility tests were used: disc diffusion and
heating, the clear sol of tungsten trioxide was formed, as evidenced by dilution assay. The agar overlay assay was carried out as described
the appearance of a UV absorption band at 325 nm and a Tyndall cone. elsewhere [24,25]; it was shown that this technique is not suitable for
Transmission electron microscopy (TEM) and selected area electron nanoparticle toxicity study, due to their low diffusion capacity in agar.
diffraction (SAED) measurements were performed using a Leo912 AB The suspension dilution assay was carried out as described elsewhere
Omega analytical transmission electron microscope operating at an [26,27]; this technique proved to be adequate for the evaluation of
accelerating voltage of 100 kV. Energy dispersive X-ray (EDX) spectra bactericidal activity of the WO3 nanoparticles.
were recorded using a Carl Zeiss NVision 40 scanning electron micro- Briefly, the experiments were carried out in 1.5 ml Eppendorf tubes;
scope equipped with an Oxford Instruments X-Max detector (80 mm2) 0.1 ml of WO3 nanoparticle sols of different concentrations (test group),
at an accelerating voltage of 20 kV. or 0.1 ml of distilled water (control), were added to 0.9 ml of a sus-
For the toxicological experiments, the obtained sol was diluted with pension of microorganisms having a total titer of about 105 CFU/ml. All
water to produce 0.1–25.0 mg/ml colloid solutions. the experiments were carried out in two parallel sets, under light and
dark conditions.
2.2. Photocatalytic Activity Measurements The number of viable microorganisms was measured both in the
control samples, and in the test tubes after incubation with nano-
2.2.1. Dye particles in the dark and under UV irradiation for various intervals of
Indigo carmine was purchased from Sigma-Aldrich (Aldrich, time. Bacterial suspensions incubated under the same conditions, but
#57000) and used as received, without further purification. without nanoparticles, were used as a control. To determine the titer of
microorganisms, 0.1 ml of bacterial suspension was sampled, then im-
2.2.2. Photocatalytic Activity Test mediately diluted using the method of serial tenfold dilutions, and then
The photocatalytic activity of the obtained nanoparticles was eval- 10 μl aliquots were plated on nutrient agar. Cells were cultivated at
uated in the reaction of photodecomposition of indigo carmine in an 37°С for 24 h and the number of cell colonies on agar plates was
aqueous solution under UV irradiation, without a detailed study of the counted. The number of grown colonies was extrapolated to 1 ml of
reaction intermediates. The source of ultraviolet radiation was a ver- suspension and measured in CFU/ml.
tically installed DELUX T8 36 W G13 UV lamp (analogue of Philips TUV
G15 T8) with a maximum emission at 253.7 nm. The reaction con- 2.3.3. UV Irradiation
tainers were 1 × 1 cm cuvettes (standard quartz cells for spectro- Test tubes were exposed to ultraviolet irradiation through UV-A
photometer), located around an UV lamp at a distance of 10 cm. (λmax = 340 nm) Wood's lamp (Philips, 15 W). Samples were placed at
Cuvettes were filled with 0.25 mM of indigo carmine aqueous solution a distance of 30 cm from the lamp for 30 or 60 min; the control samples
and colourless tungsten oxide sols with various concentrations in the were kept under similar conditions, at room temperature and in the
range of 0–0.18 mM. The temperature of the environment was held at dark. Control tubes not containing nanoparticles were kept under both
25 ± 0.5 °C. The concentration of the dye in the cuvettes was de- light and dark conditions.
termined every 4–16 min, and then the cuvettes were shaken and im-
mediately returned back to their location near the lamp. The con- 2.4. Mammalian Cells Toxicity Study
centration change of the dye was determined using an Agilent
Technologies Cary 5000 UV–Vis spectrophotometer at the adsorption 2.4.1. Cell Culture
maximum of the dye λ = 600–620 nm. The removal of indigo carmine The culture of primary mouse embryonic fibroblasts was obtained
(%) was calculated according to the equation: from embryos of SHK white mice on day 13 of pregnancy, according to
the previously published protocol [28]. The cells were cultured in
C0 − Ct ∗
Dye removal (%) = 100 DMEM/F12 (1:1) medium, with the addition of 10% fetal calf serum
C0
and 100 U/ml penicillin/streptomycin, under 5% СО2 at 37°С. All ex-
where C0 and Ct are the initial concentration of indigo carmine and the periments were conducted using cultures taken from passages 1–2.
concentration of indigo carmine at a given irradiation duration (t), re-
spectively. A similar series of experiments was performed using natural 2.4.2. UV Irradiation
scattered illumination. For this, the cuvettes were exposed on a win- Primary mouse embryonic fibroblasts of the experimental group
dowsill and illuminated by diffused summer sunlight at noon (average were irradiated for 10, 15 or 20 mins with the UV light (pulsed UV lamp
European latitude), which passed through two conventional 3 mm si- with a continuous spectrum of radiation in the range of 200–700 nm
licate glasses. Melitta Alpha 05, 50 W cm− 2); the cells in the control group were not
irradiated. In the next step, cells were grown for an additional 24 h in
2.3. Bacterial Toxicity Study the CO2-incubator at 37 °C, under a humidified atmosphere of 5% CO2
(v/v), and were subsequently sampled for morphology determination,
2.3.1. Cell Cultures live/dead viability or MTT assay.
Four reference strains from the Ukrainian collection of micro-
organisms (UCM, Zabolotny Institute of Microbiology and Virology, 2.4.3. MTT Assay
National Academy of Sciences of Ukraine) were tested: Staphylococcus Determination of activity of mitochondrial and cytoplasmic dehy-
aureus UCM B-904 (ATCC 25923), Escherichia coli UCM B-906 (ATCC drogenases in living cells was performed using the MTT assay, which is
25922), Pseudomonas aeruginosa UCM B-907 (ATCC 27853) and based on the reduction of a colourless tetrazolium salt (3-[4,5-di-
Candida albicans UCM Y-2681 (ATCC 10231). methylthiazol-2-yl]-2,5-diphenyltetrazolium bromide, MTT). After an
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A.L. Popov et al. Journal of Photochemistry & Photobiology, B: Biology 178 (2018) 395–403
interval of 24 h after UV irradiation, a standard MTT assay was per- small WO3 nanoparticles demonstrated a very high rate of photo-
formed. chromic colouration, which takes place especially easily in an aqueous
medium. Our preliminary data indicate that the bandgap of thus syn-
2.4.4. Live/Dead Viability Assay thesised tungsten oxide was size-dependent. The optical bandgap cal-
To evaluate the cytotoxic effects of WO3 nanoparticles in combi- culated using the absorbance spectra (Fig. 1, C) was Eg ≈ 3.2 eV, while
nation with UV light irradiation, a Live/Dead Viability Kit (Invitrogen, for the bulk material Eg0 = 2.6 eV [29].
Life Technologies) was used. Cells attached to the 12-well plates were
processed according to the manufacturer's protocol and visualised and 3.2. Photocatalytic Activity
photographed 25 min after adding the kit, using an Axiovert 200
fluorescence-light microscope (Carl Zeiss, Germany), and recorded Indigo carmine (C16H8N2Na2O8S2) dye is prone to photodegradation
using a Canon A620 digital camera (Canon, USA). A green signal (SYTO under illumination, and is often used in connection with the photo-
9, λ = 485/498 nm) characterised the live cells and a red signal (pro- catalytic activity of nanoparticles tests [30–33], including tungsten
pidium iodide, λ = 535/617 nm) characterised the dead cells. For each oxide nanoparticles [11,12,32,33]. Our data indicate that the synthe-
cell group, four fields in each well were examined. sised WO3 sols did possess photocatalytic activity in the processes of
To evaluate the cytotoxic effect of the WO3 nanoparticles in com- indigo carmine discolouration under illumination (Fig. 3). According to
bination with UV irradiation, primary mouse embryonic fibroblasts UV–vis measurements, no absorption bands intrinsic to WO3 nano-
were incubated for 24 h in the cell growth medium, supplemented with particles in the range of 600–800 nm were observed until complete
different concentrations of WO3 nanoparticles. Next, the medium was indigo carmine discolouration (Fig. 1S).
changed for a fresh one without the WO3 nanoparticles, and the cell Indigo carmine is light-sensitive dye and can be easily decomposed
cultures were irradiated for 10, 15 and 20 min. After 24 h, the cultures under intense UV irradiation (Fig. 3, A, curve “0”). Photocatalytically
were sampled for the morphological study, the live/dead viability and active tungsten oxide nanoparticles drastically accelerated the rate of
MTT assay. dye decomposition in a concentration-dependent manner (Fig. 3, A,
curves “1”–“5”). Moreover, the photocatalytic activity of WO3 nano-
3. Results and Discussion particles remains at nearly the same high level (Fig. 3, A, curves “1”-
“5”) even upon illumination with diffused daylight filtered through a
3.1. Tungsten Oxide Nanoparticles common window, which contained only a small fraction of UV com-
ponent and could not directly destroy the dye molecules (Fig. 3, B,
Highly photochromic, ultra-small, WO3 nanoparticles were synthe- curve “0”). This fact should be taken into account by the users of “smart
sised using the protocol proposed, based on the hydrothermal treatment windows” containing tungsten oxide nanoparticles. In turn, according
of tungstic acid in the presence of polyvinylpyrrolidone (Fig. 2). Ultra- to our observations, WO3 sols illuminated by UV/yellow-filtered light
Fig. 2. A – TEM image and SAED pattern; B – EDX spectrum of WO3 nanoparticles. C, D – absorbance of WO3 sols upon exposure to direct sunlight; the spectra were taken in the dark
every 2 min. C – UV–Vis-NIR spectra, D – dynamics of the relative change of the optical density of the UV–Vis-NIR bands of WO3 sol when exposed in the dark.
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A.L. Popov et al. Journal of Photochemistry & Photobiology, B: Biology 178 (2018) 395–403
Fig. 4. Antibacterial activity of WO3 nanoparticles to various bacterial strains and yeasts
after 30 min of exposure without UV irradiation.
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A.L. Popov et al. Journal of Photochemistry & Photobiology, B: Biology 178 (2018) 395–403
Table 1 least two major mechanisms that can be involved in the antimicrobial
WO3 nanoparticles' effect on the viability of microorganisms. effect of nanoparticles, namely direct action and/or indirect interaction
[43]. In different microorganisms, nanoparticles are piled up differently
Initial concentration The time of incubation – 60 min The fold of
inhibition in the vicinity of a bacterial cell. In most cases, the nanoparticles are
Without NP 0.5 mg/ml WO3 located directly on the membrane; under stress conditions, C. albicans
NP forms exopolysaccharide capsules, which prevent contact between the
particles and the cell. In this case, the direct damaging action of the
P. aeruginosa 9.0 × 105 1.8 × 106 9.5 × 105 1.89
P. aeruginosa + 60 min UV 1.2 × 106 3.6 × 105 3.33 particles on the cell membrane is absent. In turn, an indirect me-
(340 nm) chanism, involving the nanoparticle-mediated formation of ROS (Fig. 1)
The fold of inhibition 1.5 2.64 in the microenvironment, with subsequent damaging of the cell mem-
E. coli 2.0 × 105 1.6 × 105 1.2 × 105 1.33 brane, makes probably only a small contribution to the bactericidal
E. coli + 60 min UV 1.6 × 105 3.5 × 104 4.57
action of photoactive WO3 nanoparticles.
(340 nm)
The fold of inhibition 1.0 3.43 The observed differences in the number of viable microorganisms
S. aureus 5.7 × 104 6.6 × 104 6.2 × 104 1.06 may depend on their structure and physiology: for example, the sensi-
S. aureus + 60 min UV 6.3 × 104 1.7 × 102 370.59 tivity of microorganisms to the phototoxic effect of WO3 nanoparticles
(340 nm)
(gram-positive > gram-negative > eukaryotes) correlates with the
The fold of inhibition 1.04 364.71
cell wall structure of the investigated microorganisms.
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A.L. Popov et al. Journal of Photochemistry & Photobiology, B: Biology 178 (2018) 395–403
Fig. 7. Morphology and viability analysis of primary mouse embryonic fibroblasts upon UV irradiation in the presence of different concentrations of WO3 nanoparticles (DIC-Syto 9/PI).
Scalebar: 20 μm.
and the highest WO3 nanoparticle concentration (25 mg/ml). At a nanoparticles. Additionally, it should be noted that WO3 nanoparticles
concentration of 10 and 5 mg/ml, WO3 nanoparticles, upon 10 and inhibited the growth and proliferation of primary mouse fibroblasts in a
15 min' UV irradiation, also significantly reduced the viability of the dose-dependent manner, even without exposure to UV radiation
cells, increasing the number of dead cells (Fig. 7). It is also worth noting (Fig. 8). The mechanism of the WO3 nanoparticles cytostatic effect can
that UV irradiation of the cells in the presence of WO3 nanoparticles led be explained by the direct interaction of nanoparticles with phosphate
to the detachment of cells from the substrate and their scalding, which groups in the DNA molecule, which subsequently led to the disruption
was most likely due to structural disturbances in the focal contacts of of its structure and the replication process as a whole. There was also
cells and the cytoskeleton, as a result of active ROS generation by WO3 indirect evidence of the ability of WO3 nanoparticles to inhibit enzyme
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