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Article

Platinum–Iron Nanoparticles for Oxygen-Enhanced Sonodynamic Tumor Cell Suppression

by
Qianya Dong
and
Zhenqi Jiang
*
School of Medical Technology, Beijing Institute of Technology, Beijing 100081, China
*
Author to whom correspondence should be addressed.
Inorganics 2024, 12(12), 331; https://doi.org/10.3390/inorganics12120331
Submission received: 2 December 2024 / Revised: 14 December 2024 / Accepted: 17 December 2024 / Published: 18 December 2024
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Abstract

:
A type of nanoparticle has been developed to simultaneously alleviate tumor hypoxia and enhance the effectiveness of sonodynamic therapy aimed at improving cancer treatment outcomes. Small-sized iron–platinum nanoparticles were prepared using a thermal reduction method, and their particle size and crystal structure were characterized. The ability of these nanoparticles to decompose hydrogen peroxide to produce oxygen and generate singlet oxygen under ultrasound irradiation was further tested. The effect of iron–platinum nanoparticles on inhibition of the proliferation of MCF-7 tumor cells under hypoxic conditions was also evaluated. The prepared iron–platinum nanoparticles effectively decomposed hydrogen peroxide to produce oxygen, reversing the hypoxic environment of tumors. Additionally, they generated singlet oxygen under ultrasound irradiation, which killed tumor cells and inhibited their proliferation. This study successfully developed small-sized iron–platinum nanoparticles that can alleviate tumor hypoxia by decomposing excess hydrogen peroxide in tumor cells to produce oxygen. Under ultrasound irradiation, these nanoparticles generate singlet oxygen, inhibiting tumor growth. The nanoparticles demonstrated good safety and are potentially valuable in enhancing oxygen-enhanced sonodynamic cancer therapy.

1. Introduction

Various non-invasive treatment methods have been developed for cancer treatment, including photothermal therapy (PTT), photodynamic therapy (PDT), and sonodynamic therapy (SDT) [1,2,3,4,5]. As one of the main categories of phototherapy, PDT can effectively destroy cancer cells without damaging normal tissue by generating reactive oxygen species (ROS) in the target area [6,7,8,9]. However, due to the characteristics of photosensitizers and light, PDT has some limitations, such as poor penetration depth. In contrast, SDT, as an emerging cancer treatment method, has many advantages. For example, SDT has a high penetration depth and can treat deep-seated tumors without the need for an endoscope [10,11,12]. Additionally, the equipment used for SDT is simple and relatively inexpensive, which is an added advantage. Therefore, these factors have led to widespread attention on SDT as a treatment modality [13,14,15].
SDT is an innovative cancer treatment method that utilizes sonosensitizers to generate reactive oxygen species under ultrasound irradiation, selectively destroying tumor cells [16,17]. This technology offers high selectivity and moderate side effects, making it particularly suitable for tumors that cannot be surgically removed or are resistant to traditional radiotherapy and chemotherapy [18,19]. Sonodynamic therapy not only shows significant efficacy in superficial tumors such as skin cancer, oral cancer, and esophageal cancer, but also demonstrates potential in studies on deep-seated tumors like brain tumors, lung cancer, and pancreatic cancer. In recent years, with continuous advancements in sonosensitizers and ultrasound technology, the efficacy and safety of SDT have been further enhanced [20,21]. Many studies indicate that combining sonodynamic therapy with traditional treatments like surgery, chemotherapy, and radiotherapy can significantly improve therapeutic outcomes, reduce recurrence rates, and lower the risk of metastasis [22,23].
Current research indicates that hypoxia within tumors significantly impedes the effectiveness of sonodynamic therapy (SDT), and various nanomaterials have been developed to overcome these obstacles [24,25,26]. For instance, hybrid nanoparticles are capable of delivering oxygen and altering the tumor’s hypoxic environment to enhance the efficacy of SDT [27,28,29]. Compared to these oxygen-supplying hybrid nanoparticles, enzymes have been introduced to facilitate the production of oxygen in tumors, including both natural enzymes and nanozymes [30,31,32]. In recent years, nanozymes have been extensively studied in the biomedical field. Apart from natural enzymes, nanozymes have garnered attention and research because they not only mimic the oxygen-generating function of natural enzymes (for instance, platinum nanoparticles and ferroferric oxide nanoparticles have been found to exhibit peroxidase-like properties), but they also offer advantages such as easy preparation, high stability, ease of surface modification, adjustable enzymatic activity, and low production costs [33,34,35]. In reported literature, nanozymes are typically co-loaded with photosensitizers in nanocarriers [3,36,37,38]. Although this drug-loading strategy can effectively enhance the therapeutic effect of SDT, it still has some drawbacks, such as low loading capacity of nanozymes, early release or premature deactivation during circulation, and catalyst poisoning during the catalytic process [39,40]. In contrast, a few nanozymes have been developed that can simultaneously improve the hypoxic tumor environment and increase the therapeutic effect of SDT.
In this article, we designed and synthesized iron–platinum (FePt) nanoparticles. First, we synthesized FePt nanoparticles approximately 3.22 nanometers in size via a thermal reduction method and determined their structure using X-ray diffraction. We evaluated the ability of these FePt nanoparticles to decompose hydrogen peroxide to produce oxygen and to produce singlet oxygen under ultrasonic conditions. Furthermore, we co-incubated the FePt nanoparticles with cells to observe their biotoxicity and their effectiveness in killing tumor cells under ultrasound. The results showed that the synthesized FePt nanoparticles not only reversed tumor hypoxia by producing oxygen through the decomposition of hydrogen peroxide, but also inhibited the growth of tumor cells by generating singlet oxygen under ultrasound.

2. Results and Discussion

2.1. Synthesis and Characterization of Iron–Platinum Nanoparticles

We synthesized iron–platinum nanoparticles using an improved thermal reduction method. After vacuum drying, the synthesized iron–platinum nanoparticles could effectively disperse in water to form a solution, which is beneficial for subsequent testing and evaluation of the antitumor effect. We first observed the synthesized iron–platinum nanoparticles under a transmission electron microscope. As shown in Figure 1a, the synthesized iron–platinum nanoparticles are round, with a particle size of approximately 3.22 nanometers. This indicates the successful synthesis of nanoparticles through the thermal reduction method. Subsequently, the crystal structure of the particles was characterized by X-ray diffraction (XRD). The XRD spectrum (Figure 1b) shows peaks at 40.9°, 46.6°, and 71.3°, corresponding to the (111), (200), and (220) crystal planes of iron–platinum nanoparticles (PDF#29-0717). These results indicate that we successfully synthesized iron–platinum nanoparticles, which could be used in subsequent tests. Furthermore, we tested the colloidal properties of FePt dispersed in PBS solution. The results of the particle size distribution analysis (Figure 1c) indicated that the synthesized nanoparticles could disperse uniformly in the aqueous solution without agglomeration, and their surfaces exhibited a negative charge, which also confirmed their ability to disperse evenly in the solution. Additionally, no significant aggregation was observed in the dispersion during a ten-day stability test (Figure 1d).

2.2. Evaluation of the Oxygen Generating Capability of Iron–Platinum Nanoparticles in Hydrogen Peroxide Decomposition

We first evaluated the peroxidase-like characteristics of iron–platinum nanoparticles. The results in Figure 2 show the oxygen generation of iron–platinum nanoparticles and the control group in hydrogen peroxide solution (200 µM, the concentration of hydrogen peroxide in the tumor microenvironment) over 10 min. In the initial 2 min, iron–platinum nanoparticles generated 3.2 ppm of oxygen in the hydrogen peroxide solution. Subsequently, the oxygen generation of iron–platinum nanoparticles in the hydrogen peroxide solution showed an approximately linear increase over time, producing about 8.1 ppm of oxygen from the 1st to the 10th minute. In addition, we adjusted the concentration of hydrogen peroxide in the solution to 100 and 400 µM to react with 50 µg/mL of nanoparticles. The results showed that the change in dissolved oxygen concentration in water was not significantly different from that at 200 µM, indicating that the rate of this reaction is not dependent on the concentration of hydrogen peroxide. In contrast, diluted hydrogen peroxide in PBS solution did not generate oxygen during the same time. These results indicate that iron–platinum nanoparticles generate oxygen immediately upon addition to the hydrogen peroxide solution. Our study found that the synthesized iron–platinum nanoparticles simulate peroxidase activity, effectively decomposing hydrogen peroxide and generating oxygen, which suggests they may also catalyze the generation of oxygen in the tumor microenvironment, potentially alleviating tumor hypoxia.

2.3. Evaluation of Singlet Oxygen Generation by Iron–Platinum Nanoparticles Under Sonodynamic Therapy

To study the therapeutic effect of iron–platinum nanoparticles in sonodynamic therapy (SDT), we used a singlet oxygen sensor green (SOSG) probe to measure the generation of singlet oxygen in vitro. The experiment was conducted in both normoxic and hypoxic conditions to assess the performance of iron–platinum nanoparticles at different oxygen concentrations. The experimental results shown in Figure 3 indicate that in the absence of hydrogen peroxide in the solution, under ultrasound irradiation, iron–platinum nanoparticles generated singlet oxygen effectively in a normoxic environment, while producing negligible amounts in a hypoxic environment. This suggests that the sonodynamic effect of iron–platinum nanoparticles relies significantly on the oxygen concentration, making it challenging to generate singlet oxygen in hypoxic tumor environments and subsequently kill tumor cells effectively. When hydrogen peroxide is added to the solution, the production of singlet oxygen in a normoxic environment significantly increases, suggesting that iron–platinum nanoparticles can decompose hydrogen peroxide to produce oxygen, which is then converted into singlet oxygen under ultrasound, enhancing singlet oxygen generation. Furthermore, in a hypoxic environment, the production of singlet oxygen also increases with prolonged irradiation time, indicating that iron–platinum nanoparticles can effectively decompose hydrogen peroxide to produce oxygen and convert it into singlet oxygen under ultrasound, achieving an oxygen-enhanced sonodynamic effect. These findings suggest that iron–platinum nanoparticles can generate oxygen by decomposing hydrogen peroxide and produce singlet oxygen under ultrasound irradiation in both normoxic and hypoxic environments, potentially enhancing the treatment effect of SDT in tumor cells. In additional, we also tested the increase temperature under US. The results showed that after five minutes of ultrasound, the temperature in the ultrasound group only increased by 1.2 °C, and in the material group with 50 μg/mL it only increased by 1.4 °C. Such an increase in temperature is insufficient to cause cell death.

2.4. Evaluation of Tumor Cell Growth Inhibition by Iron–Platinum Nanoparticles

Encouraged by the aforementioned results, we proceeded to evaluate the anticancer effects of iron–platinum nanoparticles. Before studying their antitumor effects as SDT oxygen-enhanced sonosensitizers, we first assessed their dark toxicity on MCF-7 cells to determine the safe dosage range. As shown in Figure 4a, cell viability in all test groups exceeded 90%, indicating no significant cytotoxicity at concentrations of 0, 1, 3, 5, 10, and 20 μg/mL.
Subsequently, we tested the SDT effects of iron–platinum nanoparticles under normoxic and hypoxic conditions. Figure 4b shows that under ultrasound irradiation in a normoxic environment, MCF-7 cell viability decreased with increasing dosage, although ultrasound alone did not show an effective killing effect. At a dosage concentration of 20 μg/mL, the cell viability of iron–platinum nanoparticles was 24.6% (compared to the pure ultrasound group, p < 0.01). These results suggest that under ultrasound irradiation in a normoxic environment, iron–platinum nanoparticles exhibit cytotoxicity to MCF-7 cells. Further, in a hypoxic environment, as also shown in Figure 4b, cell viability decreased sharply with increasing concentrations of iron–platinum nanoparticles, reaching 37.2% at a dosage of 20 μg/mL (compared to the pure ultrasound group, p < 0.01). These findings indicate that iron–platinum nanoparticles may generate oxygen in a hypoxic intracellular environment, thereby enhancing the therapeutic effect of SDT, although cell survival rates were slightly higher than those in the normoxic group. This suggests that as nanozymes, iron–platinum nanoparticles can decompose hydrogen peroxide to produce oxygen within cells, further resulting in the production of singlet oxygen under ultrasound irradiation to achieve tumor cell inhibition.
Sonodynamic therapy for tumors is expected to become a standard treatment method, offering patients more therapeutic options and hope. However, the hypoxic environment of tumors often limits the effectiveness of sonodynamic therapy and has become a key obstacle to its further development. In previous studies, many methods have been developed to overcome the challenges posed by hypoxia. For example, carrying oxygen within nanocarriers [41,42,43] and using catalase to decompose hydrogen peroxide to generate oxygen [44,45,46,47]. However, these approaches often face issues such as increased complexity of nanocarriers, premature oxygen release, and lack of synergy between catalase and sonosensitizers. Compared to the aforementioned solutions, the nanoparticles proposed in this study combine hydrogen peroxide decomposition with sonosensitizers, avoiding the problem of premature oxygen leakage associated with oxygen-carrying methods and addressing the lack of synergy between catalase and sonosensitizers.

3. Materials and Methods

3.1. Instruments and Materials

The human breast cancer cell line MCF-7 was sourced from the Cell Bank of the Chinese Academy of Sciences. The cell viability assay kits were purchased from MedChemExpress (MCE) in Monmouth Junction, NJ, USA, and the DMEM high-glucose complete culture medium was obtained from Shanghai Zhongqiao Xinzhuo Biotechnology Co., Ltd. (Shanghai, China). Platinum(II) acetylacetonate, iron(III) acetylacetonate, 1,2-hexadecanediol, oleic acid, dioctyl ether, chloroform, and ethanol were all purchased from Shanghai Titan Scientific Co., Ltd. (Shanghai, China).

3.2. Main Instruments

High-resolution transmission electron microscopy images were captured and observed using a JEOL2100 (JEOL, Akishima, Japan). The size of FePt nanoparticles was measured by a Nano measurer. The crystal structure characteristics of the samples were determined by an X-ray powder diffractometer (XRD, D8 Discover, Bruker AXS, Karlsruhe, Germany). The DLS and zeta potential were measured at room temperature using a particle analyzer (Nano-ZS, Malvern, UK).

3.3. Synthesis of Iron–Platinum Nanoparticles

Iron–platinum nanoparticles were synthesized via a thermal reduction method. Specifically, 290 mg of platinum(II) acetylacetonate, 353 mg of iron(III) acetylacetonate, 774 mg of 1,2-hexadecanediol, 4 mL of oleic acid, 4 mL of oleylamine, and 4 mL of dioctyl ether were mixed in a three-neck flask. The mixture was then heated to 100 °C under a gentle nitrogen flow (heating rate approximately 15 °C/min). After 20 min, the reaction system was heated to 240 °C at a rate of 15 °C/min and maintained for 1 h, then cooled to room temperature. The resulting product was washed 3 times with chloroform and ethanol, then dried in a vacuum drying oven for further testing and use. The dried iron–platinum nanoparticles were re-dispersed using PBS solution. The solution was kept in 4 °C before used.

3.4. Measurement of Dissolved Oxygen Generation by Decomposition of Hydrogen Peroxide with Iron–Platinum Nanoparticles

PBS was treated with nitrogen for 20 min to remove dissolved oxygen. In oxygen-free PBS, 200 µM (100 and 400 µM for other tests) of hydrogen peroxide was incubated with 50 µg/mL iron–platinum nanoparticles at 37 °C, and the dissolved oxygen concentration was measured every two minutes using an oxygen meter (Xylem, Washington, DC, USA) for a total duration of 10 min.

3.5. Singlet Oxygen Generation Test for Iron–Platinum Nanoparticles

Under normoxic conditions, the measurement of singlet oxygen generation involved preparing iron–platinum nanoparticle suspensions at an equal ligand dose (50 μg/mL) in phosphate-buffered saline (PBS). A stock solution of SOSG (5 µL, 5 mM) was added to every 2 mL suspension (final concentration 12.5 µM), and the mixture was exposed to ultrasound (1 MHz, 1 W/cm2, 50% duty cycle) for 0, 1, 2, 3, 4, and 5 min. Fluorescence was measured with a fluorometer at different time points.
Under hypoxic conditions, iron–platinum nanoparticle suspensions at an equal ligand dose (50 μg/mL) were prepared in PBS. To each 2 mL suspension, SOSG stock solution and H2O2 were added, achieving final SOSG and H2O2 concentrations of 12.5 µM and 100 µM, respectively. Control samples were prepared by adding SOSG stock solution to the suspension without H2O2. The mixture was deoxygenated by bubbling with nitrogen for 20 min. Subsequently, the mixture was irradiated with ultrasound (1 MHz, 1 W/cm2, 50% duty cycle) for 0, 1, 2, 3, 4, and 5 min, and fluorescence was measured at different time points.

3.6. Cytotoxicity Test for Iron–Platinum Nanoparticles

Dark cytotoxicity was studied without ultrasonic irradiation. MCF-7 cells were seeded at 10,000 cells per well in a 96-well plate and incubated for 24 h. Iron–platinum nanoparticles at ligand doses of 0, 1, 3, 5, 10, and 20 μg/mL were then added. After 24 h of further incubation, cell viability was measured using a CCK-8 kit.

3.7. Sonodynamic Therapy Efficacy Test for Iron–Platinum Nanoparticles

To determine the cytotoxicity of iron–platinum nanoparticles under ultrasonic irradiation in normoxic conditions, cells were seeded at 5000 cells per well in a 96-well plate and incubated for 24 h. For hypoxic conditions, cells were similarly seeded and incubated for 24 h, then transferred to an anaerobic chamber (95% N2 and 5% CO2) for 6 h.
Iron–platinum nanoparticles at ligand doses of 0, 1, 3, 5, 10, and 20 μg/mL were added to the cells. Following 6 h of incubation, the cells were exposed to ultrasound (1 MHz, 1 W/cm2, 50% duty cycle) for 5 min. Cells were further incubated for 18 h, and cell viability was measured using a CCK-8 kit.

3.8. Ultrasound Thermal Effect Test

PBS and PBS containing 50 µg/mL FePt nanoparticles were irradiated with ultrasound (1 W/cm2, 1 MHz, 50% duty cycle) for ten minutes. The solution temperatures before and after irradiation were measured using an infrared thermometer, and the temperature difference was calculated.

3.9. Statistical Methods

Quantitative data are expressed as mean ± STD. A paired t-test was used for comparisons between two groups, with p < 0.05 indicating statistical significance.

4. Conclusions

In this manuscript, we synthesized iron–platinum alloy nanoparticles using a thermal reduction method. We assessed their particle size using transmission electron microscopy and confirmed their crystalline structure via XRD. Additionally, we evaluated the ability of these iron–platinum nanoparticles to decompose hydrogen peroxide to release oxygen. These nanoparticles effectively decompose hydrogen peroxide, alleviating hypoxic conditions. Further sonodynamic tests showed that the iron–platinum nanoparticles could convert oxygen into singlet oxygen under ultrasound irradiation, potentially inhibiting tumor cells. In tumor cell models, ultrasound irradiation significantly inhibited tumor cells under both normoxic and hypoxic conditions, achieving the goal of enhanced sonodynamic oxygen-mediated tumor killing. This was also demonstrated in vitro, confirming the potential of the synthesized iron–platinum nanoparticles for tumor sonodynamic therapy. In this study, ultrasmall iron–platinum nanoparticles capable of effectively decomposing hydrogen peroxide to produce oxygen and kill tumor cells under ultrasound irradiation, thus inhibiting tumor cell proliferation, were successfully prepared. These nanoparticles have considerable potential and prospects for application in tumor oxygen-enhanced sonodynamic therapy. Further research is needed to investigate the in vivo stability, tumor targeting, and metabolism of the nanoparticles. Only with in-depth exploration of these related studies can these nanoparticles be expected to be further utilized for efficient tumor treatment.

Author Contributions

Methodology, Q.D.; Writing—original draft, Q.D.; Writing—review & editing, Z.J.; Project administration, Z.J. All authors have read and agreed to the published version of the manuscript.

Funding

This work was developed with financial support from Young Elite Scientists Sponsorship Program by BATSA (BYESS2023244) and Beijing Institute of Technology Research Fund Program for Young Scholars.

Data Availability Statement

The original contributions presented in this study are included in the article and further inquiries can be directed to the corresponding author.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Characterization of iron–platinum nanoparticles: (a) transmission electron microscopy results and particle size distribution analysis; (b) X-ray diffraction test results; (c) DLS test result; (d) stability of FePt in PBS for 10 days at 4 °C (n = 3).
Figure 1. Characterization of iron–platinum nanoparticles: (a) transmission electron microscopy results and particle size distribution analysis; (b) X-ray diffraction test results; (c) DLS test result; (d) stability of FePt in PBS for 10 days at 4 °C (n = 3).
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Figure 2. Oxygen generation capability of Iron–platinum nanoparticles in decomposing hydrogen peroxide (n = 3).
Figure 2. Oxygen generation capability of Iron–platinum nanoparticles in decomposing hydrogen peroxide (n = 3).
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Figure 3. The 1O2 fluorescence signal of FePt nanoparticles under (a) normoxic environment and (b) hypoxic environment under US (1 MHz) at 1 W/cm2 (n = 3).
Figure 3. The 1O2 fluorescence signal of FePt nanoparticles under (a) normoxic environment and (b) hypoxic environment under US (1 MHz) at 1 W/cm2 (n = 3).
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Figure 4. (a) Cell viability of FePt nanoparticles at a series of concentration. (n = 3); (b) the cell viability of FePt nanoparticles at a series of concentrations under normoxic and hypoxic environments under US (1 MHz) for 5 min at 1 W/cm2 (n = 3, **, p < 0.01).
Figure 4. (a) Cell viability of FePt nanoparticles at a series of concentration. (n = 3); (b) the cell viability of FePt nanoparticles at a series of concentrations under normoxic and hypoxic environments under US (1 MHz) for 5 min at 1 W/cm2 (n = 3, **, p < 0.01).
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Dong, Q.; Jiang, Z. Platinum–Iron Nanoparticles for Oxygen-Enhanced Sonodynamic Tumor Cell Suppression. Inorganics 2024, 12, 331. https://doi.org/10.3390/inorganics12120331

AMA Style

Dong Q, Jiang Z. Platinum–Iron Nanoparticles for Oxygen-Enhanced Sonodynamic Tumor Cell Suppression. Inorganics. 2024; 12(12):331. https://doi.org/10.3390/inorganics12120331

Chicago/Turabian Style

Dong, Qianya, and Zhenqi Jiang. 2024. "Platinum–Iron Nanoparticles for Oxygen-Enhanced Sonodynamic Tumor Cell Suppression" Inorganics 12, no. 12: 331. https://doi.org/10.3390/inorganics12120331

APA Style

Dong, Q., & Jiang, Z. (2024). Platinum–Iron Nanoparticles for Oxygen-Enhanced Sonodynamic Tumor Cell Suppression. Inorganics, 12(12), 331. https://doi.org/10.3390/inorganics12120331

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