Chemical Mechanisms of Nanoparticle Radiosensitization and Radioprotection: A Review of Structure-Function Relationships Influencing Reactive Oxygen Species
Abstract
:1. Introduction
2. Nanoparticle Localization, ROS Transport and Cellular Damage
3. Mechanisms of Nanoparticle ROS Enhancement
4. Types of ROS and Analysis Methods
4.1. Raman Spectroscopy
4.2. Fluorescent Dyes
4.3. Electron Spin Resonance
5. Dependence on Metal Content
6. Dependence on Size
7. Dependence on Shape, Structure and Stability
8. Dependence on Surface Functionalization
9. Summary
Funding
Conflicts of Interest
References
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Assay | Specificity |
---|---|
2′,7′-dichlorofluorescein diacetate (DCFDA) | Non-specific for most ROS or nitrogen species [88,89] |
7-hydroxycoumarin | Hydroxyl radical from hydrogen peroxide [89] |
Dihydrorhodamine (DHR) | Superoxide radical, peroxynitrite anion and hydroxyl radical [90,91] |
3′-(p-aminophenyl) fluorescein (APF) | Hydroxyl radical, hypochlorite or peroxynitrite anion [88,89] |
Dihydroethidium (DHE) | Superoxide radical and hydroxyl radical [89,91] |
Singlet oxygen sensor green | Singlet oxygen [92] |
MitoSOX | Superoxide radical [91] |
Authors | Type of Nanoparticle and Size | Measurement Method | Radiation Dose | Key Observations |
---|---|---|---|---|
Abdul Rashid et al. [101] | Gold nanospheres, superparamagnetic iron oxide NPs, platinum nanodiamonds and bismuth oxide nanorods Size: 1.9 nm, 15 nm, 42 nm, 70 nm respectively | DCFDA with HCT 116 cell line | 4 Gy from a 150 MeV proton beam | In order of sensitization enhancer ratio; SPIONs < AuNPs < PtNDs < BiNRs. This was reflected in ROS generation and suggested to be the main variable between different NPs |
Adams et al. [102] | Gallium oxyhydroxide in an anisotropic and “orzo” shape Size: 53 nm and 49 nm respectively | DCFDA in vitro with PC12 cell line | Up to 10 Gy from a 6 MeV LINAC | Generation of ROS was related to the stability and structure of NPs. The less stable the NP, the greater ROS generation due to an increased number of metal ions and chemical interactions |
Bouras et al. [103] | Superparamagnetic iron oxide conjugated with cetuximab Size: 10 nm core | DCFDA in vitro with U87MG cell line | 10 Gy from a 320 keV X-ray source | Cetuximab coated iron NPs had higher internalization and ROS generation compared to non-coated NPs |
Chen et al. [33] | Hafnium-doped hydroxyapatite nanocrystal Size: 100 nm | DCFDA in vitro with A549 cell line | 5 Gy from a 662 keV gamma source | Radiolysis enhancement due to physical mechanisms. Suggested hafnium ions near intracellular organelles to promote ROS generation |
Chen et al. [93] | Ceria coated with neogambogic acid Size: 3–5 nm before coating | DCFDA in vitro with MCF-7 cell line | 6 Gy from a 6 MeV LINAC | Ceria NPs promoted autophagy of tumour cells, while also contributing to radioprotection by inhibiting ROS due to Cs4+ |
Choi et al. [104] | Pegylated gold NPs Size: 20 nm | Dihydrorhodamine in vitro with MDA-MB-231 cell line and in vivo in a murine model | 2–10 Gy from 320 kV X-ray source | Gold NPs functionalized with dihydrorhodamine was used to analyse ROS on the surface of the NP. |
Colon et al. [105] | Cerium oxide NPs Size: Possibly 3–5 nm or 10–50 nm aggregates | DCFDA in vitro with CRL-1541 cell line | 20 Gy from a 160 keV X-ray source | Increased radioprotection by scavenging and regulating ROS by the increased ratio of Ce4+ and upregulation of superoxide dismutase 2 |
Fang et al. [65] | Peptide templated gold nanoclusters Size: 3 nm | DCFDA in vitro with MCF-7 cell line | 4 Gy from a 160 keV X-ray source | Increased ROS generation and radiosensitization when NPs were targeted to mitochondria |
Gilles et al. [74] | Uncoated gold NPs Size: 32.4 nm | 7-hydroxycoumarin in solution | 15 Gy from a 17.5 keV X-ray source | Physical mechanisms do not govern radiosensitization. Physico-chemical mechanisms and the interfacial water around NPs is important for ROS production and radiosensitization |
Higgins et al. [106] | Titania NPs loaded with gold Size: 6.5 nm and 21.6 nm | Methylene Blue degradation in solution | 35 Gy/min from a 225 kV X-ray source | NPs displayed radiosensitization by radical generation. Smaller NPs have increased surface area and more catalytic sites for chemical interactions |
Jeynes et al. [3] | Gold NPs conjugated with fetal bovine serum or TAT peptide Size: 60 nm and 80 nm respectively | DMSO in vitro with RT112 cell line | 5 Gy from a 250 kVp X-ray source and 5 Gy from a 3 MeV proton source | During X-ray irradiation with NPs, DMSO scavenged ROS. This was not seen with a proton experiment |
Jiang et al. [107] | Copper oxide NPs Size: 5.4 nm | DCFDA with MCF-7 cell line | 6 MV X-ray source | Copper oxide NPs contributed to ROS generation and autophagy |
Khalil et al. [97] | Citrate-coated gold NPs Size: 9 nm, 21 nm and 30 nm | DMSO and 2-amino-2-hydroxymethyl-1-3-propanediol in water | 11–89 Gy with a 1.5 keV cathode source | H2O2 was crucial in production of hydroxyl radicals, mediated by gold NPs. Radical scavengers confirmed higher ROS production with smaller gold core |
Klein et al. [108] | Silicon coated with amino-silane Size: 1 nm | DCFDA in vitro with MCF-7 and 3T3 cell lines | 3 Gy from a 120 keV X-ray source | NPs enhanced mitochondrial membrane depolarization, provoking oxidative stress |
Klein et al. [78] | Superparamagnetic iron oxide NPs uncoated and coated with citric or malic acid Size: 9–20 nm uncoated, 7–17 nm with citric acid coat and 6–16 nm for malic acid coat | DCFDA in vitro with MCF-7, Caco-2 and 3T3 cell lines | 1 Gy or 3 Gy from a 120 keV X-ray source | Internalization of the NPs into the mitochondria provoked oxidative stress under irradiation |
Liu et al. [4] | Gold NPs with different coatings Size: 13 nm gold | DCFDA in vitro with A431 cell line | 10 Gy from a 6 MeV LINAC | NPs released nitrite ions upon irradiation to increase ROS generation due to nanoparticle coating |
Lu et al. [109] | La2O3, CeO2, CeO2-Gd, Nd2O3, Nd2O3-Si, Gd2O3 Size: <100 nm for all | DCFDA with U-87 MG and Mo59K cell lines | 3 Gy from 250 keV source | Cell lines responded differently to NPs incubation and irradiation. Gd and Ce based NPs generated ROS |
Ma et al. [110] | Gold nanospheres, nanospikes and nanorods Size: 53.2 nm nanospheres, 54.0 nm nanospikes and 50.2 nm nanorods | DCFDA in vitro with KB cell line | 4 Gy from a 6 MeV LINAC | Shape affected internalization. Unclear if increases in ROS generation were shape dependent or due to difference in internalization. Spheres were the most effective |
Ma et al. [111] | FePt NPs in nanosheets Size: 3.05 nm particles and 500 nm nanosheet | DCFDA with H1975 cell line | 4 Gy from a 204 kV photon beam | The nanosheet inhibited cell proliferation and increased ROS generation. Once in the cytoplasm, FePt NPs were internalized in the mitochondria and lysosome |
Misawa et al. [75] | Citrate-coated gold Size: 5–250 nm | 3′-(p-aminophenyl) fluorescein and dihydroethidium respectively and in solution | Up to 10 Gy from a 100 keV X-ray source | ROS generation was proportional with the inverse of the diameter of the nanoparticle |
Morita et al. [112] | Polyacrylic acid-modified titanium dioxide with H2O2 Size: 124 nm | 3′-(p-aminophenyl) fluorescein in solution | Up to 18 Gy from an 80 keV X-ray source | H2O2 bound to surface and gradually released from nanoparticle surface, adding ROS |
Nakayama et al. [113] | Titanium peroxide with coating of polyacrylic acid Size: 50–70 nm | 3′-(p-aminophenyl) fluorescein, DCFDA and dihydroethidium. Measured in solution and in vitro with MIA PaCa-2 cell line | Up to 30 Gy from a 150 keV X-ray source | Nanoparticle coating peroxidised into H2O2, catalysing ROS generation |
Nicol et al. [114] | Gold NPs functionalized with peptides Size: 28.7 nm before peptides and 45.9 nm after | DCFDA in vitro with MDA-MB-231 and MCF-7 cell lines | 2 Gy from a 160 keV X-ray source | Nanoparticle coating inhibited SOD-2 expression and promotes cellular uptake, leaving cells susceptible to increased levels of ROS |
Seo et al. [115] | Gadolinium oxide and gadolinium-chelate NPs Size: 40–45 nm | Dihydrorhodamine in vitro with CT26 cell line | Up to 15 Gy from a 45 MeV proton source | Gd ions from Gd-Gd de-excitation promoted ROS generation for radiosensitization |
Shao et al. [72] | Hollow mesoporous silica NPs with sodium percarbonate in the cavity and coated with polyacrylic acid Size: 290 nm with 80 nm core | DCFDA in vitro with ZR-75-30 cell line | Unknown dose from a 60 keV X-ray source | NPs transported sodium percarbonate to the cancer microenvironment, increasing oxygen and generation of ROS |
Taggart et al. [96] | Aurovist™ gold nanoparticles. Size: 1.9 nm | Nonyl-Acridine Orange in vitro with MDA-MB-231 and DU145 cell lines | 2 Gy with a 225 kV X-ray generator | Gold NPs and irradiation increased levels of ROS, leading to reduced mitochondrial membrane polarization |
Vasilieva et al. [116] | Nanodiamonds conjugated with neocuproine Size: 6 nm | DCFDA in vitro with HepG2 cell line | 3 Gy from a 137Cs gamma source | NPs scavenged ROS but mechanisms are not well known |
Wu et al. [117] | Silver coated with polyvinylpyrroliodone Size: 15.38 nm | DCFDA in vitro and MitoSOX (mitochondrial probe) with U251 cell line | No irradiation source used for ROS generation | Silver NPs increased inhibition of protective autophagy and ROS generation was increased |
Yong et al. [118] | Gadolinium-containing polyoxometalates-conjugated chitosan Size: 30 nm | DCFDA in solution and in vitro with BEL-7402 cell line | 2 Gy from an unknown X-ray source | NPs reduced glutathione levels by redox reaction. Reduction of antioxidants lead to increased levels of ROS and oxidative stress |
Youkhana et al. [119] | Anatase titanium oxide coated with aminopropyl trimethoxysilane Size: 30 nm | DCFDA in vitro with HaCaT and DU145 cell lines | 15 Gy and 14 Gy from a 6 MeV LINAC | ROS generation was dependent on the nanoparticle concentration |
Yu et al. [120] | Selenium NPs coated with PEG Size: 500 nm | DCFDA in solution | 8 Gy from an unknown X-ray source | ROS generation using DCFDA was time dependent, decreasing intensity after 40 min. NPs contributed to ROS generation and degraded in cells |
Zhou et al. [121] | Bismuth heteropolytungstate (BiP5W30) nanocluster Size: 1.5 nm | Terephthalic acid in solution. ELISA kit with human hydroxyl radical capture antibody in HeLa cell line. DCFDA was also used. | 50 kV with unknown X-ray source | Nanocluster promoted radiosensitization through physical and physico-chemical mechanisms. Depletion of glutathione by redox reactions, further promoting oxidative stress |
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Howard, D.; Sebastian, S.; Le, Q.V.-C.; Thierry, B.; Kempson, I. Chemical Mechanisms of Nanoparticle Radiosensitization and Radioprotection: A Review of Structure-Function Relationships Influencing Reactive Oxygen Species. Int. J. Mol. Sci. 2020, 21, 579. https://doi.org/10.3390/ijms21020579
Howard D, Sebastian S, Le QV-C, Thierry B, Kempson I. Chemical Mechanisms of Nanoparticle Radiosensitization and Radioprotection: A Review of Structure-Function Relationships Influencing Reactive Oxygen Species. International Journal of Molecular Sciences. 2020; 21(2):579. https://doi.org/10.3390/ijms21020579
Chicago/Turabian StyleHoward, Douglas, Sonia Sebastian, Quy Van-Chanh Le, Benjamin Thierry, and Ivan Kempson. 2020. "Chemical Mechanisms of Nanoparticle Radiosensitization and Radioprotection: A Review of Structure-Function Relationships Influencing Reactive Oxygen Species" International Journal of Molecular Sciences 21, no. 2: 579. https://doi.org/10.3390/ijms21020579