The Photocatalytic Inactivation Effect of Fe-Doped TiO<sub>2</sub> Nanocomposites on Leukemic HL60 Cells-Based Photodynamic Therapy

Huang, Kangqiang; Chen, Li; Liao, Meixiang; Xiong, Jianwen

doi:https://doi.org/10.1155/2012/367072

International Journal of Photoenergy

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Abstract Introduction Materials and Methods Results and Discussion Conclusion Acknowledgments References Copyright Related Articles

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TiO<sub>2</sub> Photocatalytic Materials

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Research Article | Open Access

Volume 2012 | Article ID 367072 | https://doi.org/10.1155/2012/367072

The Photocatalytic Inactivation Effect of Fe-Doped TiO₂ Nanocomposites on Leukemic HL60 Cells-Based Photodynamic Therapy

Kangqiang Huang,¹Li Chen,²Meixiang Liao,³and Jianwen Xiong¹

Academic Editor: Jiaguo Yu

Received07 Oct 2011

Revised06 Dec 2011

Accepted06 Dec 2011

Published19 Feb 2012

Abstract

The Fe-doped TiO₂ nanocomposites synthesized by a deposition-precipitation method were characterized by X-ray diffraction (XRD), transmission electron microscope (TEM), X-ray photoelectron spectroscopy (XPS), and UV-vis adsorption spectra and then were taken as a new “photosensitizer” for photodynamic therapy (PDT). The photocatalytic inactivation of Fe-doped TiO₂ on Leukemic HL60 cells was investigated using PDT reaction chamber based on LED light source, and the viability of HL60 cells was examined by Cell Counting Kit-8 (CCK-8) assay. The experimental results showed that the growth of leukemic HL60 cells was significantly inhibited by adding TiO₂ nanoparticles, and the inactivation efficiency could be effectively enhanced by the surface modification of TiO₂ nanoparticles with Fe doping. Furthermore, the optimized conditions were achieved at 5 wt% Fe/TiO₂ at a final concentration of 200 μg/mL, in which up to 82.5% PDT efficiency for the HL60 cells can be obtained under the irradiation of 403 nm light (the power density is 5 mW/cm²) within 60 minutes.

1. Introduction

Photodynamic therapy (PDT) is a new technique for cancer treatment. It takes advantage of the selective accumulation of photosensitizers, which accumulate in tumor tissues and produce singlet oxygen to inactivate the tumor cells through series of the photochemical reactions or photobiological reactions at a specific light wavelength within the absorption spectra of the photosensitizer, to achieve local treatment purposes [1]. In PDT, light, oxygen, and photosensitizer are combined to produce a selective therapeutic effect in the target tissue [2, 3]. Among these three agents, photosensitizer, as the energy carrier and the interaction bridge, is playing an important role in tumor treatment [1, 4]. However, tumors in human body with varying degrees of depth the application of traditional photosensitizers is restricted because of their inherent properties. Therefore, seeking for a high-performance photosensitizer and improving the existing properties of photosensitizer have become the main focus of PDT study.

Compared to other semiconductor oxides, TiO₂ has been widely used and proved to be an important potential photosensitizer because of their unique physical and biological properties [5–7], such as photostable, inexpensive, nontoxic properties, and it has high oxidative power, no secondary pollution. Moreover, with the rapidly development of nanotechnology, nanoparticles have shown a wide range of potential applications in biological and biomedical fields [8–11]. TiO₂ nanoparticles as an anticancer drug or used for energy transfer material to improve the traditional photodynamic effect have been noticed [12–15]. Nevertheless, the electron-hole pairs of TiO₂ can be formed only under ultraviolet light. Additionally, the photogenerated holes are easy to recombine with the photoinduced electrons, which greatly reduce the photocatalytic inactivation efficiency of TiO₂ nanoparticles and hinder its practical applications [16–19]. Fortunately, it has been demonstrated that the photocatalytic efficiency and the visible light absorption of TiO₂ can be effectively improved by the method of transition metal doping [20–23].

In this paper, nanoparticles of TiO₂ and Fe-doped TiO₂ were used as a photosensitizer to kill cancer cells. Up to our knowledge, there still no previous report on the study of photocatalytic inactivation effects of Fe/TiO₂ on HL60 cells. Our experimental results show that the photocatalytic inactivation efficiency on human HL60 cancer cells could be greatly enhanced by the Fe modification of TiO₂ nanoparticles, which have not only significantly improved the selective inactivation of tumor cells in vitro and accurate PDT dosimetry, but also have potential clinical applications when TiO₂ nanoparticles are used as a photosensitizer or energy transferor in photodynamic therapy.

2. Materials and Methods

2.1. Chemicals and Apparatus

HL60 cells were kindly provided by the Department of Medicine of Sun Yat-sen University in China. The TiO₂ nanoparticles, Fe/TiO₂ (2%) and Fe/TiO₂ (5%) nanocomposites, 5-aminolevulinic acid (ALA) and phosphate buffered saline (PBS) were purchased from Sigma (USA). The Cell Counting Kit-8 (CCK-8) was purchased from Dojindo (Japan). RPMI medium 1640 and foetal calf serum (FCS) were obtained from Gibco BRL (USA). All chemicals used were of the highest purity commercially available. The stock solutions of the compounds were prepared in serum-free medium immediately before using in experiments.

These apparatus, including D8 Focus X-ray diffraction (XRD) (Bruker, Germany), AXIS Ultra X-ray photoelectron spectroscopy (XPS) (Kratos, UK), U-3010 UV-visible spectrophotometer (Hitachi, Japan), JEM-2100HR transmission electron microscope (TEM, Japan), HH.CP-TW80 CO₂ incubator, DG5031 ELISA reader, XDS-1A inverted microscope, PDT reaction chamber, 96-well plates, cell count board, and so on were used in this research.

2.2. Light Source

To reach a high efficiency of PDT, An in-house built lamp with many high-power light-emitting diodes (LEDs), emitting light in the visible-light region 400–410 nm and with a peak at 403 nm, was taken as light sources in the experiments. The fluence rate at the position of the sample was 5 mW/cm² as measured with a photodiode. As shown in Figure 1, the blue LEDs can better meet the needs of PDT experiments.

2.3. Preparation of TiO₂ Nanoparticles and Fe-Doped TiO₂ Nanocomposites Solutions

The pure TiO₂ nanoparticles, 2 wt% Fe/TiO₂ and 5 wt% Fe/TiO₂ nanocomposites, were synthesized using the deposition-precipitation method. Firstly, (6 g), neopelex (DBS, 0.18 g), (32 g), definite volumes of doubly distilled water (250 mL), absolute ethyl alcohol (0.25 mL), and 98% were mixed with appropriate amount of (0 g, 0.1 g, 0.5 g resp.) to make up the reaction liquid, which then would be treated in water bath at 80°C under vigorous stirring for 2 to 3 hours at pH 8. Afterwards, the reactant was transferred from the water bath to be deposited for 24 h. The third process was the washing and filtering, and DBS were removed by washing with deionized water. BaCl₂ solution was employed to check whether exists. The formatting of BaSO₄ white sediment indicated more washing was needed. The resulting precipitates were washed again with ethyl before dehydration, drying in the dry-box for 3 h. Finally, The Fe-doped TiO₂ was obtained after calcined at 400°C for 30 min and grinded for 15 min.

The prepared nanoparticles were encapsulated in three bottles, respectively. Subsequently, they were placed in YX-280B-type pressure steam sterilizer with a high temperature and high pressure (120°C, 1.5 atm) to sterilize for 30 minutes. Finally, an appropriate amount of culture medium was added to fully dissolve the nanoparticles. All solutions were filtered through a membrane filter and stored in the dark at 4°C before taken into the experiments.

2.4. Cell Culture

Human leukemia HL60 cells were cultured in RPMI 1640 medium supplemented with 10% fetal bovine serum (FBS) in a humidified incubator with 5% CO₂ at 37°C until confluent. All experiments were performed using cells during the logarithmic growth phase. The cell concentration was measured using a cell count board and the cell density was adjusted to the required final concentration.

2.5. Cell Viability Assay

There are many ways to check the cell viability. The method of CCK-8 (Cell Counting Kit-8), which is much simpler, more sensitive, and reproducible than the traditional method of MTT [24], was used to detect the activation of cell during the experiment. CCK-8 assay based on the ability of a mitochondrial dehydrogenase enzyme from viable cells contains WST-8, which can be reduced to a highly water-soluble yellow-colored formazan dye by dehydrogenase in the presence of an electron carrier (1-methoxy PMS). The number of surviving cells is directly proportional to the level of the formazan product created. The amount of formazan dye can be reflected by the absorbance at 450 nm. Therefore, the characteristic of CCK-8 can be used directly for cell proliferation and toxicity analysis.

2.6. Experimental Design

Firstly, 96-well plates were divided into several parts according to experimental needs (including the control groups and zero groups). Three repeated wells were set under the same experimental conditions. Secondly, HL60 cells in logarithmic growth phase were seeded in 96-well plates, afterwards the prepared solutions of TiO₂, Fe/TiO₂ (2%), Fe/TiO₂ (5%) at various concentrations were added in the appropriate samples respectively, and each well was infused with an appropriate volume of cell culture medium to ensure that the final volume was 200 μL, while the zero pores contain only 200 μL of culture medium. Thirdly, light exposure was carried out immediately after 4 h incubation (The average fluence rate used was 5 mW/cm², the irradiation dose was 18 J/cm²). After that, 20 μL of solution was added to each well and incubated for other 4 hours. Finally, the OD values of the samples were detected by the ELISA reader based on dual-wavelength method (the test wavelength at 450 nm and reference wavelength at 630 nm). Three parallel tests were performed for each sample to ensure accuracy.

2.7. Statistical Analysis

Data are presented as means ± S.D. (standard deviation) from at least three independent experiments. Statistical analysis was then performed using the statistical software SPSS11.5, Values of were considered statistically significant.

3. Results and Discussion

3.1. Characterization of Fe-TiO₂ Nanocomposites

3.1.1. X-Ray Diffraction

The crystallite size is calculated by the Scherrer formula [25]: where is the crystalline size, is the X-ray wavelength (0.1541 nm), is the constant usually taken as 0.89, is the Bragg’s angle for anatase phase titania, and is the pure full width of the diffraction line at half of the maximum intensity. According to the above formula, it is estimated that the average particle sizes are 20.2 nm, 19.8 nm, 17.2 nm for pure TiO₂, 2 wt% Fe-doped TiO₂, and 5 wt% Fe-doped TiO₂, respectively. Apparently, the incorporation of Fe into TiO₂ could effectively inhibit the crystal grain growth of TiO₂, leading to smaller particle.

XRD was also used to further examine the average crystalline properties of the Fe-doped TiO₂. As shown in Figure 2, the XRD diffraction peaks of the synthesized Fe-doped samples around of , , , , , , which could be indexed to the characteristic peaks (1 0 1), (0 0 4), (2 0 0), (1 0 5), (2 1 1), and (2 0 4) of anatase TiO₂. Thus, the Fe-doped TiO₂ nanocomposites obtained by the deposition-precipitation method have primarily the anatase phase. Furthermore, it is demonstrated that the diffraction peaks of Fe-doped TiO₂ gradually shift towards smaller angle with the increase of Fe-doping concentration compared with that of pure TiO₂, indicating that the lattices of TiO₂ have been expanded by the Fe-doping, which make it possible for to diffuse into the TiO₂ lattices to replace . Additionally, there is no indication of a peak corresponding to iron oxide (Fe₂O₃) observed, further indicating that exists by replacing part of in the crystal lattices of TiO₂, which is mainly contributed to the ionic radius of (0.064 nm) to be almost equal to that of (0.068 nm).

3.1.2. TEM Studies

The morphology and size of the Fe-doped TiO₂ nanocomposites were studied with a JEM-2100HR transmission electron microscope. As can be seen in Figure 3, TiO₂ particles are spherical or square-shaped with a primary particle size of approximately 18 nm. The measurements are basically consistent with the XRD results.

3.1.3. XPS Analysis

In order to determine whether the successful implementation of the Fe doping, the surface of Fe/TiO₂ (5%) nanocomposites calcined at 400°C has been investigated using XPS analysis. As can be observed from Figure 4, the characteristic peak corresponding to is located at 710 eV, which reveals that Fe in the doped samples exists mainly in the form of [26]. The result is consistent with the results obtained by X-ray diffraction. Additionally, according to the XPS measurements, the concentration of Fe over the surface of TiO₂ is 4.68 wt%, which is basically consistent with the theoretical expectation.

3.1.4. UV-Vis Spectroscopy

The UV-visible absorption spectra of TiO₂ nanoparticles doped with different amounts of Fe in the visible light region were measured using U-3010 UV-visible spectrometer, as shown in Figure 5.

The UV-Vis absorption spectra show that the absorption edges of Fe-doped TiO₂ nanoparticles are slightly shifted to longer wavelengths “red-shift” with increasing amount of Fe, and the absorption for the doped TiO₂ in the visible light region is significantly enhanced compared with that of pure TiO₂. Additionally, as shown in Figure 5, the starting point of absorption edge of updoped TiO₂ is 393 nm while that for Fe/TiO₂ (2%) is 407 nm and Fe/TiO₂ (5%) is 425 nm, indicating that the visible light absorption of TiO₂ nanoparticles has been effectively enhanced by the surface modification with Fe.

3.2. Effects of Photoexcited TiO₂ with or without Fe Doping on Proliferation of HL60 Cells

HL60 cells in the logarithmic phase at a density of 1 × 10⁵ cells/mL were seeded into 96-well culture plates which had been divided into 4 groups, namely: the control group, the TiO₂ group, the Fe/TiO₂ (2%) group, the Fe/TiO₂ (5%) group, respectively. The final concentration of the groups with nanoparticles was 200 μg/mL. Besides, some culture media were added, respectively, so as to the total volume is 200 μL per well. The optical density values (OD values) of the samples were measured by DG5031 ELISA reader for 6 consecutive days without adding nutrients. The experimental data are presented in Figure 6.

As can be seen from Figure 6, all the HL60 cells showed a low growth rate on the first day indicating they were in the adaptation period. The growth rate for the HL60 cells increased rapidly in the logarithmic phase during the next three days. In this paper, the cells during this period were used in all experiments. On the fifth day, due to nutrient depletion, metabolite accumulation, and environmental changes, the growth rate of cells becomes more and more slow and stabilized downgradually. With the continuous depletion of nutrients and the accumulation of toxic metabolites, the number of viable cells started to decrease from the sixth day.

Figure 6 also demonstrates that the OD values of the experimental groups in the presence of nanoparticles are much lower and with a shorter growth phase than that of the control group under the same conditions. Apparently, TiO₂ nanoparticles or Fe/TiO₂ nanocomposites have a certain degree of inhibitory or toxic effects on the proliferation of HL60 cells. Moreover, the inhibition effects on HL60 cells become more and more obvious with the increasing Fe-doping concentration.

3.3. Influence of Nanoparticles Concentrations on the Relative Survival of HL60 Cells

It is required for the photosensitive antitumor drugs used in PDT not only to have high photocatalytic inactivation capability under light irradiation, but also to have no toxicity in the dark. Therefore, it is very important to investigate the self-generated toxicity of TiO₂ nanoparticles or Fe/TiO₂ nanocomposites. The toxicity of TiO₂ or Fe/TiO₂ was measured by exposing HL60 cells in the medium containing various concentrations of TiO₂ or Fe/TiO₂ (0 μg/mL, 50 μg/mL, 100 μgL/mL, 150 μg/mL, 200 μg/mL, 250 μg/mL, 500 μgL/mL, 1000 μg/mL) for 48 hours in dark, respectively. The OD values of HL60 cells at different concentrations of nanoparticles were normalized by the OD values of control group (the final concentration of nanoparticles was 0 μg/mL). The relative survival rates of HL60 cells are shown in Figure 7.

As can be seen from Figure 7, with the increasing concentration of nanoparticles solution, the viability of HL60 cells decreased gradually. At a concentration of 1000 μg/mL, the three survival rates were 77%, 73%, 65.3%, respectively. In comparison, when the concentration reduced the range of 0~250 μg/mL, the survival rates of HL60 cells were all above 90%. In this case, the TiO₂ nanoparticles and Fe/TiO₂ nanocomposites could be considered as basically nontoxic materials for cancer cells in the dark, which is in agreement with the suggestions reported in references [27, 28] that TiO₂ is nontoxic for animals.

3.4. Influence of Nanocomposites-Based PDT on the Viability of HL60 Cells

The HL60 cells were inoculated into two 96-well plates marked with A or B. The cell suspensions of A plate were exposed to light after incubating for 24 hours and then preincubated for another 24 hours in the dark. The HL60 cells in plate B were incubated for 48 hours in the incubator without light treatment. The final concentration of nanoparticles TiO₂ nanoparticles or Fe/TiO₂ nanocomposites was 200 μg/mL and each experiment was repeated three times in order to reduce the error. The OD values of experimental groups were then measured by DG5031 ELISA reader, as shown in Table 1.

These measured OD values of cells after light irradiation were normalized by the OD values of cells without light treatment. The relative survival of HL60 and PDT efficiency under different nanoparticles were calculated by the following equations: relative viability = OD_Light/OD_Dark, and PDT efficiency = 1−relative viability. The results are presented in Figure 8.

According to the measurements shown in Table 1, the OD values of HL60 cells exposed to light are significantly lower than that of the control group without light treatment, for both in the absence and in the presence of nanoparticles. Illumination causes a decline survival rate of tumor cells without TiO₂ nanocomposites which is mainly due to the near-ultraviolet light (403 nm) which itself has a certain degree of killing effect on tumor cells. PDT is designed to “selectively kill tumor cells while not harming normal cells as possible.” If light irradiation have a greater killing effect on tumor cell in the absence of photosensitive drugs, it will also inevitably lead to a greater damage to normal cells. Therefore, more attention should be paid to light elements of PDT, to minimize light damage on normal cells. Our previous experiments have demonstrated that the light density of 5 mW/cm² and the light irradiation dose of 18 J/cm² are the best inactivation parameters of tumor HL60 cells-based photodynamic therapy, which are consistent with the literature reports [29, 30]. Therefore, a more effective approach to solve the problem is to enhance the visible light absorption of TiO₂. Furthermore, the OD values of HL60 cells exposed to light with nanoparticles are significantly lower than these without nanoparticles, which is in agreement with our previous result that nanoparticles have a certain degree of inhibition/toxicity on the growth of cells.

As shown in Figure 8, the relative survival rate of HL60 cells in the presence of nanoparticles is significantly lower than that without nanoparticles. It means that PDT efficiency of HL60 cells with nanoparticles is higher than that of HL60 cells without nanoparticles. In addition, Fe/TiO₂ nanocomposites present much higher efficiency in photokilling HL60 cancer cells than TiO₂ nanoparticles. These results reveal that the modification of Fe on the surface of TiO₂ nanoparticles can greatly enhance the photocatalytic inactivation effect of TiO₂ on HL60 cells. Additionally, Fe/TiO₂ (5%) group displays a little higher inactivation efficiency compared with Fe/TiO₂ (2%) group, when 200 μg/mL Fe/TiO₂ (5%) nanocomposites were added, the inactivation efficiency of HL60 cells can up to 82.5% after a 60-minute irradiation. Although a higher concentration of Fe/TiO₂ nanocomposites or TiO₂ nanoparticles could achieve a higher-photocatalytic killing effect, but it is not preferable to use a very high concentration of photocatalyst for practical consideration as it might block the blood vessels. On the other hand, at high dopant concentrations, due to the decrease of the distance between trapping sites, the recombination rate of the photoinduced electrons and holes increases, resulting in lower photocatalytic activity. Therefore, the doping concentration of Fe should not be too high.

It has been demonstrated that the cell damage mechanism based on ligh-excited Fe/TiO₂ nanocomposites is accomplished through a series of chain reactions by means of reactive oxygen species- (ROS-) induced cell death [31–33].

The generation mechanism of reactive oxygen species (ROS) on Fe-doped TiO₂ nanocomposites under UV irradiation is displayed in Scheme 1. When illuminated by ultraviolet light, photoinduced electrons and holes could be created, which can transfer to the surface of Fe nanoparticles and reduce the dissolved O₂ to produce the superoxide anion . At the same time, the photogenerated holes on the TiO₂ surface can further react with water to generate powerful hydroxyl radicals () and other oxidative radicals (), which are capable of destroying the membrane and component of tumor cells. The recombination rate of the photoproduced electrons and holes can be effectively inhibited by the above process, so the photocatalytic activity of TiO₂ nanoparticles is significantly enhanced by the modification of Fe. Additionally, the enhanced photocatalytic activity of Fe-doped TiO₂ nanocomposites can also be explained by a new energy level produced in the bandgap of TiO₂ due to the dispersion of Fe nanoparticles, as suggested in the literature [30–37]. Regardless of complexity, it is apparent that there are several key photosensitive that have been involved which could be also explained as follows:

4. Conclusion

In this paper, the prepared Fe/TiO₂ characterized by X-ray diffraction (XRD), transmission electron microscope (TEM), X-ray photoelectron spectroscopy (XPS), and UV-Vis adsorption spectra, respectively, was successfully applied as a photosensitizer-based photodynamic therapy to kill human HL60 cancer cells in vitro. The experimental results show that the absorption of TiO₂ nanoparticles in the visible light region could be enhanced effectively by the method of Fe doping, and both pure TiO₂ and Fe/TiO₂ nanocomposites at high concentrations can have a significant inhibition/toxicity on the growth of HL60 cells. It is also found that the photocatalytic inactivation effect on HL60 cells with nanoparticles is obviously higher than that without nanoparticles under the same conditions. Furthermore, Fe/TiO₂ nanocomposites presented much higher PDT efficiency in photokilling HL60 cancer cells than TiO₂ nanoparticles. These indicate that the photocatalytic inactivation effects of TiO₂ on HL60 cells could be greatly improved by the modification of Fe on the surface of TiO₂ nanoparticles. The PDT efficiency of Fe/TiO₂ (5%) nanocomposites on HL60 cells can reach 82.5% at a concentration of 200 μg/mL after a 60-minute light treatment. The high photocatalytic inactivation effects of Fe/TiO₂ nanocomposites on human HL60 cancer cells suggests that it may be an important potential photosensitizer-based photodynamic therapy for cancer treatment [38–40].

Acknowledgments

This work has been financially supported by National Natural Science Foundation of China (61072029), Natural Science Foundation of Guangdong Province (10151063101000025), and Science and Technology Planning Project of Guangzhou city (2010Y1-C111).

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Copyright © 2012 Kangqiang Huang et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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