Intracellular responses to reactive oxygen and nitrogen species, and lipid peroxidation in apoptotic cells cultivated in plasma-activated medium

Furuta, Ryo; Kurake, Naoyuki; Ishikawa, Kenji; Takeda, Keigo; Hashizume, Hiroshi; Tanaka, Hiromasa; Kondo, Hiroki; Sekine, Makoto; Hori, Masaru

doi:10.1002/ppap.201700123

Cited by 24 publications

(21 citation statements)

References 50 publications

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“…Figures (a, b) show the H 2 O 2 levels in the stored PAM. Figures (c, d) Figures 3 and 4, it can be stated that H 2 O 2 mainly contributes to the death of cancer cells after the indirect cold plasma irradiation on the culture medium, as previously suggested [31,32]. [23,37].…”

Section: Measurement Of Nitrite Concentration In Pam and Pamsupporting

confidence: 72%

“…Additionally, cell death by ME-APPJ (788 MHz) utilizing a coaxial transmission line resonator (CTLR) was also confirmed [25]. As such, many studies on the mechanism by which CAP induces cancer cell death have been reported [26][27][28][29][30][31][32][33], but for the indirect treatment utilizing PAM, there is still a lack of research on physical changes in the stage before death occurs.…”

Section: Introductionmentioning

confidence: 94%

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Anticancer Effects of Plasma-Activated Medium Produced by a Microwave-Excited Atmospheric Pressure Argon Plasma Jet

Joh

Chung

et al. 2020

Oxidative Medicine and Cellular Longevity

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Cold atmospheric plasma (CAP) has been reported to have strong anticancer effects in vitro and in vivo. CAP has been known to induce apoptosis in most cancer cells by treatment to cells using direct and indirect treatment methods. There are many reports of apoptosis pathways induced by CAP, but for indirect treatment, there is still a lack of fundamental research on how CAP can cause apoptosis in cancer cells. In this study, we applied an indirect treatment method to determine how CAP can induce cancer cell death. First, plasma-activated medium (PAM) was produced by a 2.45 GHz microwave-excited atmospheric pressure plasma jet (ME-APPJ). Next, the amounts of various reactive species in the PAM were estimated using colorimetric methods. The concentration of NO2– and H2O2 in PAM cultured with cancer cells was measured, and intracellular reactive oxidative stress (ROS) changes were observed using flow cytometry. When PAM was incubated with A549 lung cancer cells, there was little change in NO2– concentration, but the concentration of H2O2 gradually decreased after 30 min. While the intracellular ROS of A549 cells was rapidly increased at 2 hours, there was no significant change in that of PAM-treated normal cells. Furthermore, PAM had a significant cytotoxic effect on A549 cells but had little effect on normal cell viability. In addition, using flow cytometry, we confirmed that apoptosis of A549 cells occurred following flow cytometry and western blot analysis. These results suggest that among various reactive species produced by PAM, hydrogen peroxide plays a key role in inducing cancer cell apoptosis.

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Section: Measurement Of Nitrite Concentration In Pam and Pamsupporting

confidence: 72%

Section: Introductionmentioning

confidence: 94%

Anticancer Effects of Plasma-Activated Medium Produced by a Microwave-Excited Atmospheric Pressure Argon Plasma Jet

Joh

Chung

et al. 2020

Oxidative Medicine and Cellular Longevity

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“…Plasmas are multi-component systems generating UV radiation, visible light, electromagnetic fields, thermal radiation, electrons and ions, and reactive oxygen species (ROS) and reactive nitrogen species (RNS) [2]. The latter play a crucial role in mediating the plasma effects in cells [3][4][5] by mediating oxidative modifications [6][7][8] to induce signaling pathways [9][10][11]. First discovered as a new tool for disinfection and wound healing [12][13][14], plasma also demonstrates cytotoxicity towards cancer cells [15][16][17].…”

Section: Introductionmentioning

confidence: 99%

Combination Treatment with Cold Physical Plasma and Pulsed Electric Fields Augments ROS Production and Cytotoxicity in Lymphoma

Wolff

Kolb

Weltmann

et al. 2020

Cancers

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New approaches in oncotherapy rely on the combination of different treatments to enhance the efficacy of established monotherapies. Pulsed electric fields (PEFs) are an established method (electrochemotherapy) for enhancing cellular drug uptake while cold physical plasma is an emerging and promising anticancer technology. This study aimed to combine both technologies to elucidate their cytotoxic potential as well as the underlying mechanisms of the effects observed. An electric field generator (0.9–1.0 kV/cm and 100-μs pulse duration) and an atmospheric pressure argon plasma jet were employed for the treatment of lymphoma cell lines as a model system. PEF but not plasma treatment induced cell membrane permeabilization. Additive cytotoxicity was observed for the metabolic activity and viability of the cells while the sequence of treatment in the combination played only a minor role. Intriguingly, a parallel combination was more effective compared to a 15-min pause between both treatment regimens. A combination effect was also found for lipid peroxidation; however, none could be observed in the cytosolic and mitochondrial reactive oxygen species (ROS) production. The supplementation with either antioxidant, a pan-caspase-inhibitor or a ferroptosis inhibitor, all partially rescued lymphoma cells from terminal cell death, which contributes to the mechanistic understanding of this combination treatment.

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“…The chemical components produced by CAPs, identified as the active agents responsible for the biological effects, have been extensively studied [ 6 , 7 ]. The reactive oxygen and nitrogen species (RONS) generated and delivered by plasma cause functional and structural damage to lipids in cell membranes [ 8 ], oxidize proteins [ 9 ], induce DNA breaks [ 10 ], and promote cell death by different mechanisms [ 11 , 12 ]. In contrast, the physical components produced by plasma such as UV photons and electromagnetic fields on their own have a negligible cellular impact [ 13 ].…”

Section: Introductionmentioning

confidence: 99%

Reduction of Human Glioblastoma Spheroids Using Cold Atmospheric Plasma: The Combined Effect of Short- and Long-Lived Reactive Species

Privat-Maldonado

Gorbanev

Dewilde

et al. 2018

Cancers

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Cold atmospheric plasma (CAP) is a promising technology against multiple types of cancer. However, the current findings on the effect of CAP on two-dimensional glioblastoma cultures do not consider the role of the tumour microenvironment. The aim of this study was to determine the ability of CAP to reduce and control glioblastoma spheroid tumours in vitro. Three-dimensional glioblastoma spheroid tumours (U87-Red, U251-Red) were consecutively treated directly and indirectly with a CAP using dry He, He + 5% H2O or He + 20% H2O. The cytotoxicity and spheroid shrinkage were monitored using live imaging. The reactive oxygen and nitrogen species produced in phosphate buffered saline (PBS) were measured by electron paramagnetic resonance (EPR) and colourimetry. Cell migration was also assessed. Our results demonstrate that consecutive CAP treatments (He + 20% H2O) substantially shrank U87-Red spheroids and to a lesser degree, U251-Red spheroids. The cytotoxic effect was due to the short- and long-lived species delivered by CAP: they inhibited spheroid growth, reduced cell migration and decreased proliferation in CAP-treated spheroids. Direct treatments were more effective than indirect treatments, suggesting the importance of CAP-generated, short-lived species for the growth inhibition and cell cytotoxicity of solid glioblastoma tumours. We concluded that CAP treatment can effectively reduce glioblastoma tumour size and restrict cell migration, thus demonstrating the potential of CAP therapies for glioblastoma.

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Intracellular responses to reactive oxygen and nitrogen species, and lipid peroxidation in apoptotic cells cultivated in plasma-activated medium

Cited by 24 publications

References 50 publications

Anticancer Effects of Plasma-Activated Medium Produced by a Microwave-Excited Atmospheric Pressure Argon Plasma Jet

Anticancer Effects of Plasma-Activated Medium Produced by a Microwave-Excited Atmospheric Pressure Argon Plasma Jet

Combination Treatment with Cold Physical Plasma and Pulsed Electric Fields Augments ROS Production and Cytotoxicity in Lymphoma

Reduction of Human Glioblastoma Spheroids Using Cold Atmospheric Plasma: The Combined Effect of Short- and Long-Lived Reactive Species

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