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Impact of ROS Generated by Chemical, Physical, and Plasma Techniques on Cancer Attenuation

Identifieur interne : 000892 ( Pmc/Curation ); précédent : 000891; suivant : 000893

Impact of ROS Generated by Chemical, Physical, and Plasma Techniques on Cancer Attenuation

Auteurs : Sarmistha Mitra [Corée du Sud] ; Linh Nhat Nguyen [Corée du Sud] ; Mahmuda Akter [Corée du Sud] ; Gyungsoon Park [Corée du Sud] ; Eun Ha Choi [Corée du Sud] ; Nagendra Kumar Kaushik [Corée du Sud]

Source :

RBID : PMC:6678366

Abstract

For the last few decades, while significant improvements have been achieved in cancer therapy, this family of diseases is still considered one of the deadliest threats to human health. Thus, there is an urgent need to find novel strategies in order to tackle this vital medical issue. One of the most pivotal causes of cancer initiation is the presence of reactive oxygen species (ROS) inside the body. Interestingly, on the other hand, high doses of ROS possess the capability to damage malignant cells. Moreover, several important intracellular mechanisms occur during the production of ROS. For these reasons, inducing ROS inside the biological system by utilizing external physical or chemical methods is a promising approach to inhibit the growth of cancer cells. Beside conventional technologies, cold atmospheric plasmas are now receiving much attention as an emerging therapeutic tool for cancer treatment due to their unique biophysical behavior, including the ability to generate considerable amounts of ROS. This review summarizes the important mechanisms of ROS generated by chemical, physical, and plasma approaches. We also emphasize the biological effects and cancer inhibition capabilities of ROS.


Url:
DOI: 10.3390/cancers11071030
PubMed: 31336648
PubMed Central: 6678366

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PMC:6678366

Le document en format XML

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<name sortKey="Kaushik, Nagendra Kumar" sort="Kaushik, Nagendra Kumar" uniqKey="Kaushik N" first="Nagendra Kumar" last="Kaushik">Nagendra Kumar Kaushik</name>
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<p>For the last few decades, while significant improvements have been achieved in cancer therapy, this family of diseases is still considered one of the deadliest threats to human health. Thus, there is an urgent need to find novel strategies in order to tackle this vital medical issue. One of the most pivotal causes of cancer initiation is the presence of reactive oxygen species (ROS) inside the body. Interestingly, on the other hand, high doses of ROS possess the capability to damage malignant cells. Moreover, several important intracellular mechanisms occur during the production of ROS. For these reasons, inducing ROS inside the biological system by utilizing external physical or chemical methods is a promising approach to inhibit the growth of cancer cells. Beside conventional technologies, cold atmospheric plasmas are now receiving much attention as an emerging therapeutic tool for cancer treatment due to their unique biophysical behavior, including the ability to generate considerable amounts of ROS. This review summarizes the important mechanisms of ROS generated by chemical, physical, and plasma approaches. We also emphasize the biological effects and cancer inhibition capabilities of ROS.</p>
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</TEI>
<pmc article-type="review-article">
<pmc-dir>properties open_access</pmc-dir>
<front>
<journal-meta>
<journal-id journal-id-type="nlm-ta">Cancers (Basel)</journal-id>
<journal-id journal-id-type="iso-abbrev">Cancers (Basel)</journal-id>
<journal-id journal-id-type="publisher-id">cancers</journal-id>
<journal-title-group>
<journal-title>Cancers</journal-title>
</journal-title-group>
<issn pub-type="epub">2072-6694</issn>
<publisher>
<publisher-name>MDPI</publisher-name>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="pmid">31336648</article-id>
<article-id pub-id-type="pmc">6678366</article-id>
<article-id pub-id-type="doi">10.3390/cancers11071030</article-id>
<article-id pub-id-type="publisher-id">cancers-11-01030</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Review</subject>
</subj-group>
</article-categories>
<title-group>
<article-title>Impact of ROS Generated by Chemical, Physical, and Plasma Techniques on Cancer Attenuation</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Mitra</surname>
<given-names>Sarmistha</given-names>
</name>
<xref ref-type="aff" rid="af1-cancers-11-01030">1</xref>
<xref ref-type="aff" rid="af2-cancers-11-01030">2</xref>
<xref ref-type="author-notes" rid="fn1-cancers-11-01030"></xref>
</contrib>
<contrib contrib-type="author">
<contrib-id contrib-id-type="orcid" authenticated="true">https://orcid.org/0000-0003-1967-3857</contrib-id>
<name>
<surname>Nguyen</surname>
<given-names>Linh Nhat</given-names>
</name>
<xref ref-type="aff" rid="af1-cancers-11-01030">1</xref>
<xref ref-type="aff" rid="af3-cancers-11-01030">3</xref>
<xref ref-type="author-notes" rid="fn1-cancers-11-01030"></xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Akter</surname>
<given-names>Mahmuda</given-names>
</name>
<xref ref-type="aff" rid="af1-cancers-11-01030">1</xref>
<xref ref-type="aff" rid="af2-cancers-11-01030">2</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Park</surname>
<given-names>Gyungsoon</given-names>
</name>
<xref ref-type="aff" rid="af1-cancers-11-01030">1</xref>
<xref ref-type="aff" rid="af2-cancers-11-01030">2</xref>
<xref ref-type="aff" rid="af3-cancers-11-01030">3</xref>
</contrib>
<contrib contrib-type="author">
<contrib-id contrib-id-type="orcid" authenticated="true">https://orcid.org/0000-0001-5385-1878</contrib-id>
<name>
<surname>Choi</surname>
<given-names>Eun Ha</given-names>
</name>
<xref ref-type="aff" rid="af1-cancers-11-01030">1</xref>
<xref ref-type="aff" rid="af2-cancers-11-01030">2</xref>
<xref ref-type="aff" rid="af3-cancers-11-01030">3</xref>
<xref rid="c1-cancers-11-01030" ref-type="corresp">*</xref>
</contrib>
<contrib contrib-type="author">
<contrib-id contrib-id-type="orcid" authenticated="true">https://orcid.org/0000-0002-4965-5046</contrib-id>
<name>
<surname>Kaushik</surname>
<given-names>Nagendra Kumar</given-names>
</name>
<xref ref-type="aff" rid="af1-cancers-11-01030">1</xref>
<xref ref-type="aff" rid="af2-cancers-11-01030">2</xref>
<xref ref-type="aff" rid="af3-cancers-11-01030">3</xref>
<xref rid="c1-cancers-11-01030" ref-type="corresp">*</xref>
</contrib>
</contrib-group>
<aff id="af1-cancers-11-01030">
<label>1</label>
Applied Plasma Medicine Center, Plasma Bioscience Research Center, Seoul 01897, Korea</aff>
<aff id="af2-cancers-11-01030">
<label>2</label>
Department of Plasma Bio-display, Kwangwoon University, Seoul 01897, Korea</aff>
<aff id="af3-cancers-11-01030">
<label>3</label>
Department of Electrical and Biological Physics, Kwangwoon University, Seoul 01897, Korea</aff>
<author-notes>
<corresp id="c1-cancers-11-01030">
<label>*</label>
Correspondence:
<email>kaushik.nagendra@kw.ac.kr</email>
(N.K.K.);
<email>ehchoi@kw.ac.kr</email>
(E.H.C.); Tel.: +82-2-940-8618 (N.K.K.)</corresp>
<fn id="fn1-cancers-11-01030">
<label></label>
<p>These authors have contributed equally.</p>
</fn>
</author-notes>
<pub-date pub-type="epub">
<day>22</day>
<month>7</month>
<year>2019</year>
</pub-date>
<pub-date pub-type="collection">
<month>7</month>
<year>2019</year>
</pub-date>
<volume>11</volume>
<issue>7</issue>
<elocation-id>1030</elocation-id>
<history>
<date date-type="received">
<day>14</day>
<month>6</month>
<year>2019</year>
</date>
<date date-type="accepted">
<day>17</day>
<month>7</month>
<year>2019</year>
</date>
</history>
<permissions>
<copyright-statement>© 2019 by the authors.</copyright-statement>
<copyright-year>2019</copyright-year>
<license license-type="open-access">
<license-p>Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (
<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">http://creativecommons.org/licenses/by/4.0/</ext-link>
).</license-p>
</license>
</permissions>
<abstract>
<p>For the last few decades, while significant improvements have been achieved in cancer therapy, this family of diseases is still considered one of the deadliest threats to human health. Thus, there is an urgent need to find novel strategies in order to tackle this vital medical issue. One of the most pivotal causes of cancer initiation is the presence of reactive oxygen species (ROS) inside the body. Interestingly, on the other hand, high doses of ROS possess the capability to damage malignant cells. Moreover, several important intracellular mechanisms occur during the production of ROS. For these reasons, inducing ROS inside the biological system by utilizing external physical or chemical methods is a promising approach to inhibit the growth of cancer cells. Beside conventional technologies, cold atmospheric plasmas are now receiving much attention as an emerging therapeutic tool for cancer treatment due to their unique biophysical behavior, including the ability to generate considerable amounts of ROS. This review summarizes the important mechanisms of ROS generated by chemical, physical, and plasma approaches. We also emphasize the biological effects and cancer inhibition capabilities of ROS.</p>
</abstract>
<kwd-group>
<kwd>reactive oxygen species</kwd>
<kwd>reactive nitrogen species</kwd>
<kwd>free radicals</kwd>
<kwd>cancers</kwd>
</kwd-group>
</article-meta>
</front>
<floats-group>
<fig id="cancers-11-01030-f001" orientation="portrait" position="float">
<label>Figure 1</label>
<caption>
<p>Schematic of primary reactive oxygen species (ROS) production mechanism.</p>
</caption>
<graphic xlink:href="cancers-11-01030-g001"></graphic>
</fig>
<fig id="cancers-11-01030-f002" orientation="portrait" position="float">
<label>Figure 2</label>
<caption>
<p>Some major intracellular (mitochondria, peroxisome, endoplasmic reticulum (ER) stress, nicotinamide adenine dinucleotide phosphate hydrogen (NADPH) oxidase, metabolizing enzymes) and extracellular (Radiations, Xenobiotics) sources of reactive oxygen species (ROS) generation [
<xref rid="B81-cancers-11-01030" ref-type="bibr">81</xref>
].</p>
</caption>
<graphic xlink:href="cancers-11-01030-g002"></graphic>
</fig>
<fig id="cancers-11-01030-f003" orientation="portrait" position="float">
<label>Figure 3</label>
<caption>
<p>Role of reactive oxygen species (ROS) in cancer inhibition by four different mechanisms and the different pathways involved in those mechanisms.</p>
</caption>
<graphic xlink:href="cancers-11-01030-g003"></graphic>
</fig>
<fig id="cancers-11-01030-f004" orientation="portrait" position="float">
<label>Figure 4</label>
<caption>
<p>Molecular mechanism of soft-jet plasma-induced cancer cell apoptosis via the mitochondrial intrinsic pathway and extracellular signal-regulated kinase/mitogen-activated protein kinase (ERK/MAPK) activation [
<xref rid="B250-cancers-11-01030" ref-type="bibr">250</xref>
].</p>
</caption>
<graphic xlink:href="cancers-11-01030-g004"></graphic>
</fig>
<table-wrap id="cancers-11-01030-t001" orientation="portrait" position="float">
<object-id pub-id-type="pii">cancers-11-01030-t001_Table 1</object-id>
<label>Table 1</label>
<caption>
<p>List of anticancer agents applied to different cancer treatment and their mechanism of action by increasing ROS production.</p>
</caption>
<table frame="hsides" rules="groups">
<thead>
<tr>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Published Year</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Anticancer Agent</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Types of Cancer</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Mechanism</th>
</tr>
</thead>
<tbody>
<tr>
<td align="center" valign="middle" rowspan="1" colspan="1">1999</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Doxorubicin</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Lung cancer [
<xref rid="B152-cancers-11-01030" ref-type="bibr">152</xref>
]</td>
<td align="center" valign="middle" rowspan="1" colspan="1">BRAF inhibition by ROS [
<xref rid="B152-cancers-11-01030" ref-type="bibr">152</xref>
,
<xref rid="B153-cancers-11-01030" ref-type="bibr">153</xref>
]</td>
</tr>
<tr>
<td align="center" valign="middle" rowspan="1" colspan="1">2018</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Actinomycin D or Decitabine</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Skin cancer [
<xref rid="B154-cancers-11-01030" ref-type="bibr">154</xref>
]</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Production of reactive species [
<xref rid="B155-cancers-11-01030" ref-type="bibr">155</xref>
]</td>
</tr>
<tr>
<td align="center" valign="middle" rowspan="1" colspan="1">2018</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Vinorelbine</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Lung cancer [
<xref rid="B156-cancers-11-01030" ref-type="bibr">156</xref>
]</td>
<td align="center" valign="middle" rowspan="1" colspan="1">ROS induced mechanism [
<xref rid="B137-cancers-11-01030" ref-type="bibr">137</xref>
]</td>
</tr>
<tr>
<td align="center" valign="middle" rowspan="1" colspan="1">2014</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Vinblastine</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Lung cancer and breast cancer [
<xref rid="B157-cancers-11-01030" ref-type="bibr">157</xref>
]</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Apoptosis induced by ROS [
<xref rid="B136-cancers-11-01030" ref-type="bibr">136</xref>
]</td>
</tr>
<tr>
<td align="center" valign="middle" rowspan="1" colspan="1">2009</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Camptothecin</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Cervical and uterus cancer [
<xref rid="B158-cancers-11-01030" ref-type="bibr">158</xref>
]</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Cell death induced by ROS</td>
</tr>
<tr>
<td align="center" valign="middle" rowspan="1" colspan="1">2006
<break></break>
2014</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Paclitaxel</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Lung cancer [
<xref rid="B159-cancers-11-01030" ref-type="bibr">159</xref>
]
<break></break>
Breast cancer [
<xref rid="B160-cancers-11-01030" ref-type="bibr">160</xref>
]</td>
<td align="center" valign="middle" rowspan="1" colspan="1">ROS-dependent activation of apoptotic cell death [
<xref rid="B161-cancers-11-01030" ref-type="bibr">161</xref>
]</td>
</tr>
<tr>
<td align="center" valign="middle" rowspan="1" colspan="1">2012</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Taxol</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Blood cancer [
<xref rid="B162-cancers-11-01030" ref-type="bibr">162</xref>
]</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Apoptosis by generation of ROS [
<xref rid="B162-cancers-11-01030" ref-type="bibr">162</xref>
]</td>
</tr>
<tr>
<td align="center" valign="middle" rowspan="1" colspan="1">2017</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Epirubicin</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Breast cancer [
<xref rid="B163-cancers-11-01030" ref-type="bibr">163</xref>
]</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Programmed death of cell by ROS [
<xref rid="B163-cancers-11-01030" ref-type="bibr">163</xref>
]</td>
</tr>
<tr>
<td align="center" valign="middle" rowspan="1" colspan="1">2012</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Resveratrol </td>
<td align="center" valign="middle" rowspan="1" colspan="1">Colon cancer [
<xref rid="B164-cancers-11-01030" ref-type="bibr">164</xref>
]</td>
<td align="center" valign="middle" rowspan="1" colspan="1">ROS production [
<xref rid="B164-cancers-11-01030" ref-type="bibr">164</xref>
]</td>
</tr>
<tr>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">2015</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Colchicine</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Colon cancer [
<xref rid="B165-cancers-11-01030" ref-type="bibr">165</xref>
]</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Increase ROS production in a dose dependent manner [
<xref rid="B165-cancers-11-01030" ref-type="bibr">165</xref>
]</td>
</tr>
</tbody>
</table>
<table-wrap-foot>
<fn>
<p>ROS: reactive oxygen species; BRAF:
<bold>serine/threonine-specific protein kinase</bold>
.</p>
</fn>
</table-wrap-foot>
</table-wrap>
<table-wrap id="cancers-11-01030-t002" orientation="portrait" position="float">
<object-id pub-id-type="pii">cancers-11-01030-t002_Table 2</object-id>
<label>Table 2</label>
<caption>
<p>List of other treatment methods used in cancer treatment via reactive oxygen species-based mechanisms.</p>
</caption>
<table frame="hsides" rules="groups">
<thead>
<tr>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Treatment Methods</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Mechanism</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Reference</th>
</tr>
</thead>
<tbody>
<tr>
<td align="center" valign="middle" rowspan="1" colspan="1">Sonodynamic therapy (SDT)</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Alter cancer microenvironment by enhancing ROS level</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[
<xref rid="B228-cancers-11-01030" ref-type="bibr">228</xref>
]</td>
</tr>
<tr>
<td align="center" valign="middle" rowspan="1" colspan="1">Tyrosin kinase inhibitor (TKI)</td>
<td align="center" valign="middle" rowspan="1" colspan="1">ROS inducing effect</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[
<xref rid="B227-cancers-11-01030" ref-type="bibr">227</xref>
]</td>
</tr>
<tr>
<td align="center" valign="middle" rowspan="1" colspan="1">Monoclonal antibody</td>
<td align="center" valign="middle" rowspan="1" colspan="1">ROS mediated apotosis</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[
<xref rid="B227-cancers-11-01030" ref-type="bibr">227</xref>
]</td>
</tr>
<tr>
<td align="center" valign="middle" rowspan="1" colspan="1">Anti-tumor immune action</td>
<td align="center" valign="middle" rowspan="1" colspan="1">By targeting tumor-associated macrophage by ROS</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[
<xref rid="B229-cancers-11-01030" ref-type="bibr">229</xref>
]</td>
</tr>
<tr>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Nanomedicine combination with anticancer drugs</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">ROS-inducing effect</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[
<xref rid="B230-cancers-11-01030" ref-type="bibr">230</xref>
]</td>
</tr>
</tbody>
</table>
</table-wrap>
<table-wrap id="cancers-11-01030-t003" orientation="portrait" position="float">
<object-id pub-id-type="pii">cancers-11-01030-t003_Table 3</object-id>
<label>Table 3</label>
<caption>
<p>List of plasma instruments and methods used in different types of cancer with their mechanisms.</p>
</caption>
<table frame="hsides" rules="groups">
<thead>
<tr>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Published Year</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Plasma Equipment</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Types of Cancer</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Mechanism</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Reference</th>
</tr>
</thead>
<tbody>
<tr>
<td align="center" valign="middle" rowspan="1" colspan="1">2017</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Plasma jet</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Pancreatic cancer</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Hydrogen peroxide</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[
<xref rid="B259-cancers-11-01030" ref-type="bibr">259</xref>
]</td>
</tr>
<tr>
<td align="center" valign="middle" rowspan="1" colspan="1">2017</td>
<td align="center" valign="middle" rowspan="1" colspan="1">DBD plasma device</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Cervical cancer</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Hydrogen peroxide</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[
<xref rid="B260-cancers-11-01030" ref-type="bibr">260</xref>
]</td>
</tr>
<tr>
<td align="center" valign="middle" rowspan="1" colspan="1">2014</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Plasma jet</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Head and neck cancer</td>
<td align="center" valign="middle" rowspan="1" colspan="1">DNA damage by ROS</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[
<xref rid="B261-cancers-11-01030" ref-type="bibr">261</xref>
]</td>
</tr>
<tr>
<td align="center" valign="middle" rowspan="1" colspan="1">2016</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Plasma generated in DI water</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Gastric cancer</td>
<td align="center" valign="middle" rowspan="1" colspan="1">ROS-induced apoptosis</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[
<xref rid="B262-cancers-11-01030" ref-type="bibr">262</xref>
]</td>
</tr>
<tr>
<td align="center" valign="middle" rowspan="1" colspan="1">2017</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Air plasma by high voltage electrode</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Triple negative breast cancer</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Hydrogen peroxide-induced apoptosis</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[
<xref rid="B256-cancers-11-01030" ref-type="bibr">256</xref>
]</td>
</tr>
<tr>
<td align="center" valign="middle" rowspan="1" colspan="1">2016</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Microplasma jet produced liquid plasma</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Triple negative breast cancer</td>
<td align="center" valign="middle" rowspan="1" colspan="1">ROS and RNS-induced apoptosis</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[
<xref rid="B263-cancers-11-01030" ref-type="bibr">263</xref>
]</td>
</tr>
<tr>
<td align="center" valign="middle" rowspan="1" colspan="1">2017</td>
<td align="center" valign="middle" rowspan="1" colspan="1">DBD plasma device</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Lung cancer</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Apoptosis induced by ROS and RNS</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[
<xref rid="B264-cancers-11-01030" ref-type="bibr">264</xref>
]</td>
</tr>
<tr>
<td align="center" valign="middle" rowspan="1" colspan="1">2015</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Water vapor with plasma jet</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Breast cancer</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Hydrogen peroxide-induced apoptosis</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[
<xref rid="B265-cancers-11-01030" ref-type="bibr">265</xref>
] </td>
</tr>
<tr>
<td align="center" valign="middle" rowspan="1" colspan="1">2017</td>
<td align="center" valign="middle" rowspan="1" colspan="1">DBD plasma</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Colon cancer</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Apoptosis and DNA damage by ROS</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[
<xref rid="B266-cancers-11-01030" ref-type="bibr">266</xref>
]</td>
</tr>
<tr>
<td align="center" valign="middle" rowspan="1" colspan="1">2013</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Jet plasma</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Brain cancer</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Plasma caused cell death</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[
<xref rid="B267-cancers-11-01030" ref-type="bibr">267</xref>
]</td>
</tr>
<tr>
<td align="center" valign="middle" rowspan="1" colspan="1">2016</td>
<td align="center" valign="middle" rowspan="1" colspan="1">DBD plasma</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Brain cancer</td>
<td align="center" valign="middle" rowspan="1" colspan="1">ROS-induced apoptosis</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[
<xref rid="B268-cancers-11-01030" ref-type="bibr">268</xref>
]</td>
</tr>
<tr>
<td align="center" valign="middle" rowspan="1" colspan="1">2012</td>
<td align="center" valign="middle" rowspan="1" colspan="1">DBD plasma</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Brain and colorectal cancer</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Apoptosis and DNA damage by ROS</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[
<xref rid="B22-cancers-11-01030" ref-type="bibr">22</xref>
]</td>
</tr>
<tr>
<td align="center" valign="middle" rowspan="1" colspan="1">2014</td>
<td align="center" valign="middle" rowspan="1" colspan="1">DBD plasma</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Thyroid cancer, Oral cancer</td>
<td align="center" valign="middle" rowspan="1" colspan="1">ROS-induced DNA damage and apotosis</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[
<xref rid="B238-cancers-11-01030" ref-type="bibr">238</xref>
]</td>
</tr>
<tr>
<td align="center" valign="middle" rowspan="1" colspan="1">2013</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Plasma-treated media</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Blood cancer</td>
<td align="center" valign="middle" rowspan="1" colspan="1">ROS-induced apoptosis</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[
<xref rid="B269-cancers-11-01030" ref-type="bibr">269</xref>
]</td>
</tr>
<tr>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">2014</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">DBD plasma</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Blood cancer</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">ROS-initiated apoptosis-related gene expression</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[
<xref rid="B270-cancers-11-01030" ref-type="bibr">270</xref>
]</td>
</tr>
</tbody>
</table>
<table-wrap-foot>
<fn>
<p>DBD: dielectric barrier discharge; DI: deionized; ROS: reactive oxygen species; RNS: reactive nitrogen species.</p>
</fn>
</table-wrap-foot>
</table-wrap>
</floats-group>
</pmc>
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