Biological Functions and Molecular Mechanisms of Antibiotic Tigecycline in the Treatment of Cancers
Identifieur interne : 000A19 ( Pmc/Curation ); précédent : 000A18; suivant : 000A20Biological Functions and Molecular Mechanisms of Antibiotic Tigecycline in the Treatment of Cancers
Auteurs : Zhen Dong [République populaire de Chine] ; Muhammad Nadeem Abbas [République populaire de Chine] ; Saima Kausar [République populaire de Chine] ; Jie Yang [République populaire de Chine] ; Lin Li [République populaire de Chine] ; Li Tan [République populaire de Chine] ; Hongjuan Cui [République populaire de Chine]Source :
- International Journal of Molecular Sciences [ 1422-0067 ] ; 2019.
Abstract
As an FDA-approved drug, glycylcycline tigecycline has been used to treat complicated microbial infections. However, recent studies in multiple hematologic and malignant solid tumors reveal that tigecycline treatment induces cell cycle arrest, apoptosis, autophagy and oxidative stress. In addition, tigecycline also inhibits mitochondrial oxidative phosphorylation, cell proliferation, migration, invasion and angiogenesis. Importantly, combinations of tigecycline with chemotherapeutic or targeted drugs such as venetoclax, doxorubicin, vincristine, paclitaxel, cisplatin, and imatinib, have shown to be promising strategies for cancer treatment. Mechanism of action studies reveal that tigecycline leads to the inhibition of mitochondrial translation possibly through interacting with mitochondrial ribosome. Meanwhile, this drug also interferes with several other cell pathways/targets including MYC, HIFs, PI3K/AKT or AMPK-mediated mTOR, cytoplasmic p21 CIP1/Waf1, and Wnt/β-catenin signaling. These evidences indicate that antibiotic tigecycline is a promising drug for cancer treatment alone or in combination with other anticancer drugs. This review summarizes the biological function of tigecycline in the treatment of tumors and comprehensively discusses its mode of action.
Url:
DOI: 10.3390/ijms20143577
PubMed: 31336613
PubMed Central: 6678986
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<country xml:lang="fr">République populaire de Chine</country>
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</affiliation>
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<author><name sortKey="Tan, Li" sort="Tan, Li" uniqKey="Tan L" first="Li" last="Tan">Li Tan</name>
<affiliation wicri:level="1"><nlm:aff id="af1-ijms-20-03577">State Key Laboratory of Silkworm Genome Biology, Institute of Sericulture and Systems Biology, Southwest University, Beibei, Chongqing 400716, China</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>State Key Laboratory of Silkworm Genome Biology, Institute of Sericulture and Systems Biology, Southwest University, Beibei, Chongqing 400716</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="af2-ijms-20-03577">Cancer Center, Medical Research Institute, Southwest University, Beibei, Chongqing 400716, China</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>Cancer Center, Medical Research Institute, Southwest University, Beibei, Chongqing 400716</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="af3-ijms-20-03577">Engineering Research Center for Cancer Biomedical and Translational Medicine, Southwest University, Beibei, Chongqing 400716, China</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>Engineering Research Center for Cancer Biomedical and Translational Medicine, Southwest University, Beibei, Chongqing 400716</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="af4-ijms-20-03577">Chongqing Engineering and Technology Research Center for Silk Biomaterials and Regenerative Medicine, Southwest University, Beibei, Chongqing 400716, China</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>Chongqing Engineering and Technology Research Center for Silk Biomaterials and Regenerative Medicine, Southwest University, Beibei, Chongqing 400716</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Cui, Hongjuan" sort="Cui, Hongjuan" uniqKey="Cui H" first="Hongjuan" last="Cui">Hongjuan Cui</name>
<affiliation wicri:level="1"><nlm:aff id="af1-ijms-20-03577">State Key Laboratory of Silkworm Genome Biology, Institute of Sericulture and Systems Biology, Southwest University, Beibei, Chongqing 400716, China</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>State Key Laboratory of Silkworm Genome Biology, Institute of Sericulture and Systems Biology, Southwest University, Beibei, Chongqing 400716</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="af2-ijms-20-03577">Cancer Center, Medical Research Institute, Southwest University, Beibei, Chongqing 400716, China</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>Cancer Center, Medical Research Institute, Southwest University, Beibei, Chongqing 400716</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="af3-ijms-20-03577">Engineering Research Center for Cancer Biomedical and Translational Medicine, Southwest University, Beibei, Chongqing 400716, China</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>Engineering Research Center for Cancer Biomedical and Translational Medicine, Southwest University, Beibei, Chongqing 400716</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="af4-ijms-20-03577">Chongqing Engineering and Technology Research Center for Silk Biomaterials and Regenerative Medicine, Southwest University, Beibei, Chongqing 400716, China</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>Chongqing Engineering and Technology Research Center for Silk Biomaterials and Regenerative Medicine, Southwest University, Beibei, Chongqing 400716</wicri:regionArea>
</affiliation>
</author>
</analytic>
<series><title level="j">International Journal of Molecular Sciences</title>
<idno type="eISSN">1422-0067</idno>
<imprint><date when="2019">2019</date>
</imprint>
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<front><div type="abstract" xml:lang="en"><p>As an FDA-approved drug, glycylcycline tigecycline has been used to treat complicated microbial infections. However, recent studies in multiple hematologic and malignant solid tumors reveal that tigecycline treatment induces cell cycle arrest, apoptosis, autophagy and oxidative stress. In addition, tigecycline also inhibits mitochondrial oxidative phosphorylation, cell proliferation, migration, invasion and angiogenesis. Importantly, combinations of tigecycline with chemotherapeutic or targeted drugs such as venetoclax, doxorubicin, vincristine, paclitaxel, cisplatin, and imatinib, have shown to be promising strategies for cancer treatment. Mechanism of action studies reveal that tigecycline leads to the inhibition of mitochondrial translation possibly through interacting with mitochondrial ribosome. Meanwhile, this drug also interferes with several other cell pathways/targets including MYC, HIFs, PI3K/AKT or AMPK-mediated mTOR, cytoplasmic p21 <sup>CIP1/Waf1</sup>
, and Wnt/β-catenin signaling. These evidences indicate that antibiotic tigecycline is a promising drug for cancer treatment alone or in combination with other anticancer drugs. This review summarizes the biological function of tigecycline in the treatment of tumors and comprehensively discusses its mode of action.</p>
</div>
</front>
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<pmc article-type="review-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Int J Mol Sci</journal-id>
<journal-id journal-id-type="iso-abbrev">Int J Mol Sci</journal-id>
<journal-id journal-id-type="publisher-id">ijms</journal-id>
<journal-title-group><journal-title>International Journal of Molecular Sciences</journal-title>
</journal-title-group>
<issn pub-type="epub">1422-0067</issn>
<publisher><publisher-name>MDPI</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">31336613</article-id>
<article-id pub-id-type="pmc">6678986</article-id>
<article-id pub-id-type="doi">10.3390/ijms20143577</article-id>
<article-id pub-id-type="publisher-id">ijms-20-03577</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Review</subject>
</subj-group>
</article-categories>
<title-group><article-title>Biological Functions and Molecular Mechanisms of Antibiotic Tigecycline in the Treatment of Cancers</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="true">https://orcid.org/0000-0003-3108-0245</contrib-id>
<name><surname>Dong</surname>
<given-names>Zhen</given-names>
</name>
<xref ref-type="aff" rid="af1-ijms-20-03577">1</xref>
<xref ref-type="aff" rid="af2-ijms-20-03577">2</xref>
<xref ref-type="aff" rid="af3-ijms-20-03577">3</xref>
<xref ref-type="aff" rid="af4-ijms-20-03577">4</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Abbas</surname>
<given-names>Muhammad Nadeem</given-names>
</name>
<xref ref-type="aff" rid="af1-ijms-20-03577">1</xref>
<xref ref-type="aff" rid="af2-ijms-20-03577">2</xref>
<xref ref-type="aff" rid="af3-ijms-20-03577">3</xref>
<xref ref-type="aff" rid="af4-ijms-20-03577">4</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Kausar</surname>
<given-names>Saima</given-names>
</name>
<xref ref-type="aff" rid="af1-ijms-20-03577">1</xref>
<xref ref-type="aff" rid="af2-ijms-20-03577">2</xref>
<xref ref-type="aff" rid="af3-ijms-20-03577">3</xref>
<xref ref-type="aff" rid="af4-ijms-20-03577">4</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Yang</surname>
<given-names>Jie</given-names>
</name>
<xref ref-type="aff" rid="af1-ijms-20-03577">1</xref>
<xref ref-type="aff" rid="af2-ijms-20-03577">2</xref>
<xref ref-type="aff" rid="af3-ijms-20-03577">3</xref>
<xref ref-type="aff" rid="af4-ijms-20-03577">4</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Li</surname>
<given-names>Lin</given-names>
</name>
<xref ref-type="aff" rid="af1-ijms-20-03577">1</xref>
<xref ref-type="aff" rid="af2-ijms-20-03577">2</xref>
<xref ref-type="aff" rid="af3-ijms-20-03577">3</xref>
<xref ref-type="aff" rid="af4-ijms-20-03577">4</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Tan</surname>
<given-names>Li</given-names>
</name>
<xref ref-type="aff" rid="af1-ijms-20-03577">1</xref>
<xref ref-type="aff" rid="af2-ijms-20-03577">2</xref>
<xref ref-type="aff" rid="af3-ijms-20-03577">3</xref>
<xref ref-type="aff" rid="af4-ijms-20-03577">4</xref>
</contrib>
<contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="true">https://orcid.org/0000-0003-1178-1570</contrib-id>
<name><surname>Cui</surname>
<given-names>Hongjuan</given-names>
</name>
<xref ref-type="aff" rid="af1-ijms-20-03577">1</xref>
<xref ref-type="aff" rid="af2-ijms-20-03577">2</xref>
<xref ref-type="aff" rid="af3-ijms-20-03577">3</xref>
<xref ref-type="aff" rid="af4-ijms-20-03577">4</xref>
<xref rid="c1-ijms-20-03577" ref-type="corresp">*</xref>
</contrib>
</contrib-group>
<aff id="af1-ijms-20-03577"><label>1</label>
State Key Laboratory of Silkworm Genome Biology, Institute of Sericulture and Systems Biology, Southwest University, Beibei, Chongqing 400716, China</aff>
<aff id="af2-ijms-20-03577"><label>2</label>
Cancer Center, Medical Research Institute, Southwest University, Beibei, Chongqing 400716, China</aff>
<aff id="af3-ijms-20-03577"><label>3</label>
Engineering Research Center for Cancer Biomedical and Translational Medicine, Southwest University, Beibei, Chongqing 400716, China</aff>
<aff id="af4-ijms-20-03577"><label>4</label>
Chongqing Engineering and Technology Research Center for Silk Biomaterials and Regenerative Medicine, Southwest University, Beibei, Chongqing 400716, China</aff>
<author-notes><corresp id="c1-ijms-20-03577"><label>*</label>
Correspondence: <email>hcui@swu.edu.cn</email>
; Tel.: +86-23-6825-1713; Fax: +86-23-6825-1128</corresp>
</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>20</volume>
<issue>14</issue>
<elocation-id>3577</elocation-id>
<history><date date-type="received"><day>14</day>
<month>6</month>
<year>2019</year>
</date>
<date date-type="accepted"><day>19</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>As an FDA-approved drug, glycylcycline tigecycline has been used to treat complicated microbial infections. However, recent studies in multiple hematologic and malignant solid tumors reveal that tigecycline treatment induces cell cycle arrest, apoptosis, autophagy and oxidative stress. In addition, tigecycline also inhibits mitochondrial oxidative phosphorylation, cell proliferation, migration, invasion and angiogenesis. Importantly, combinations of tigecycline with chemotherapeutic or targeted drugs such as venetoclax, doxorubicin, vincristine, paclitaxel, cisplatin, and imatinib, have shown to be promising strategies for cancer treatment. Mechanism of action studies reveal that tigecycline leads to the inhibition of mitochondrial translation possibly through interacting with mitochondrial ribosome. Meanwhile, this drug also interferes with several other cell pathways/targets including MYC, HIFs, PI3K/AKT or AMPK-mediated mTOR, cytoplasmic p21 <sup>CIP1/Waf1</sup>
, and Wnt/β-catenin signaling. These evidences indicate that antibiotic tigecycline is a promising drug for cancer treatment alone or in combination with other anticancer drugs. This review summarizes the biological function of tigecycline in the treatment of tumors and comprehensively discusses its mode of action.</p>
</abstract>
<kwd-group><kwd>antibiotics</kwd>
<kwd>tigecycline</kwd>
<kwd>cell cycle arrest</kwd>
<kwd>autophagy</kwd>
<kwd>mitochondrial translation</kwd>
<kwd>OxPhos</kwd>
</kwd-group>
</article-meta>
</front>
<floats-group><fig id="ijms-20-03577-f001" orientation="portrait" position="float"><label>Figure 1</label>
<caption><p>The biological effects of tigecycline in cancer cells. Tigecycline treatment induces decrease in OxPhos, dysfunction of mitochondria, inhibition of EMT and migration/invasion, suppression of angiogenesis, arrest of cell cycle, increase of ROS and oxidative stress/damages, promotion of intrinsic apoptois and activation of autophagy. CytoC, cytochrome C; EMT, epithelial–mesenchymal transition; ETC, electron transfer chain; mtDNA, mitochondrial DNA; ND4, NADH dehydrogenase subunit 4; OxPhos, oxidative phosphorylation; PC, pyruvate carboxylase; PDH, pyruvate dehydrogenase; ROS, reactive oxygen species.</p>
</caption>
<graphic xlink:href="ijms-20-03577-g001"></graphic>
</fig>
<fig id="ijms-20-03577-f002" orientation="portrait" position="float"><label>Figure 2</label>
<caption><p>Mode of action of tigecycline in cancer cells. 4E-BP1, eukaryotic translation initiation factor 4E-binding protein 1; AMPK, AMP-activated protein kinase; BCL9, B-cell CLL/lymphoma 9; FOXO3a, forkhead box O3; HES1, hairy and enhancer of split homolog-1; mTOR, mammalian target of rapamycin; p70S6K, ribosomal protein S6 kinase; p-rS6, ribosomal S6 protein.</p>
</caption>
<graphic xlink:href="ijms-20-03577-g002"></graphic>
</fig>
<fig id="ijms-20-03577-f003" orientation="portrait" position="float"><label>Figure 3</label>
<caption><p>The effect of tigecycline on mitochondrial translation. Elongation factor EF-Tu binds to GTP to form a complex with tRNA and amino acid. Then this complex delivers (AA)-tRNA into ribosomal A site. Tigecycline may target the mitochondrial ribosome through inhibiting the EF-Tu/(AA)-tRNA/GTP complex delivery. AA, amino acid; EF-GM, elongation factor G, mitochondrial; EF-Ts, elongation factor Ts, mitochondrial; EF-Tu, elongation factor thermo unstable; GDP, guanosine-5’-diphosphate; GTP, guanosine-5’-triphosphate; MTPs, mitochondrial translated peptides.</p>
</caption>
<graphic xlink:href="ijms-20-03577-g003"></graphic>
</fig>
<fig id="ijms-20-03577-f004" orientation="portrait" position="float"><label>Figure 4</label>
<caption><p>Tigecycline promotes susceptibility of tumors to chemotherapy and targeted therapy. ALL, acute lymphoblastic leukemia; CML, chronic myeloid leukemia.</p>
</caption>
<graphic xlink:href="ijms-20-03577-g004"></graphic>
</fig>
<fig id="ijms-20-03577-f005" orientation="portrait" position="float"><label>Figure 5</label>
<caption><p>Hypothesis on the causality of phenotypes induced by tigecycline treatment in cancer cells.</p>
</caption>
<graphic xlink:href="ijms-20-03577-g005"></graphic>
</fig>
<table-wrap id="ijms-20-03577-t001" orientation="portrait" position="float"><object-id pub-id-type="pii">ijms-20-03577-t001_Table 1</object-id>
<label>Table 1</label>
<caption><p>IC50 of tigecycline in several types of tumor cells. Please note that direct comparison of the IC50 data is not straightforward since obtained in different conditions with different methods.</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">Cancer Type</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Cell Line Name</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">IC50 (Treatment Time)</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Methods</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">References</th>
</tr>
</thead>
<tbody><tr><td rowspan="2" align="center" valign="middle" colspan="1">Melanoma</td>
<td align="center" valign="middle" rowspan="1" colspan="1">A375</td>
<td align="center" valign="middle" rowspan="1" colspan="1">7.24 μM (48 h)</td>
<td rowspan="2" align="center" valign="middle" colspan="1">MTT assay</td>
<td rowspan="2" align="center" valign="middle" colspan="1">[<xref rid="B25-ijms-20-03577" ref-type="bibr">25</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">MV3</td>
<td align="center" valign="middle" rowspan="1" colspan="1">10.9 μM (48 h)</td>
</tr>
<tr><td rowspan="4" align="center" valign="middle" colspan="1">Non-small cell lung cancer</td>
<td align="center" valign="middle" rowspan="1" colspan="1">A549</td>
<td align="center" valign="middle" rowspan="1" colspan="1">5.8 μM (14 d)</td>
<td rowspan="4" align="center" valign="middle" colspan="1">Colony formation</td>
<td rowspan="4" align="center" valign="middle" colspan="1">[<xref rid="B28-ijms-20-03577" ref-type="bibr">28</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">PC19</td>
<td align="center" valign="middle" rowspan="1" colspan="1">8.7 μM (14 d)</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">H157</td>
<td align="center" valign="middle" rowspan="1" colspan="1">6.8 μM (14 d)</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">EBC-1</td>
<td align="center" valign="middle" rowspan="1" colspan="1">5.9 μM (14 d)</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">CML</td>
<td align="center" valign="middle" rowspan="1" colspan="1">K562</td>
<td align="center" valign="middle" rowspan="1" colspan="1">51.4 μM (48 h)</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Cell Counting Kit-8 assay</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B33-ijms-20-03577" ref-type="bibr">33</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">RB1/TP53-mutant human TNBC cells</td>
<td align="center" valign="middle" rowspan="1" colspan="1">BT549; MDA-MB-436; Du4475</td>
<td align="center" valign="middle" rowspan="1" colspan="1">average IC50 = 3 μM (72 h)</td>
<td rowspan="2" align="center" valign="middle" colspan="1">MTT assay</td>
<td rowspan="2" align="center" valign="middle" colspan="1">[<xref rid="B29-ijms-20-03577" ref-type="bibr">29</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">RB1-proficient/TP53-mutant TNBC cells</td>
<td align="center" valign="middle" rowspan="1" colspan="1">HCC38; Hs578t; MDA-MB-231</td>
<td align="center" valign="middle" rowspan="1" colspan="1">average IC50 ≈ 20 μM (72 h) *</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Mouse colon cancer</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">CT26</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">33 μM (72 h)</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">CyQuant direct cell proliferation assay</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B36-ijms-20-03577" ref-type="bibr">36</xref>
]</td>
</tr>
</tbody>
</table>
<table-wrap-foot><fn><p>* This average IC50 of tigecycline in RB1-proficient/TP53-mutant TNBC cells was presumably calculated by using GraphPas Prism 6 according to the approximate inhibition rate from Figure 8D in the original article [<xref rid="B29-ijms-20-03577" ref-type="bibr">29</xref>
]. The authors only provided an information in the text that the average IC50 of tigecycline in RB1-proficient/TP53-mutant TNBC cells was more than 8 μM. CML: chronic myeloid leukemia; TNBC: triple-negative breast cancer.</p>
</fn>
</table-wrap-foot>
</table-wrap>
<table-wrap id="ijms-20-03577-t002" orientation="portrait" position="float"><object-id pub-id-type="pii">ijms-20-03577-t002_Table 2</object-id>
<label>Table 2</label>
<caption><p>Different biological phenotypes and signaling pathways or molecular mechanisms induced by tigecycline in different cancer cells.</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">Classification</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Cancer Type</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Main Biological Phenotypes</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Pathways or Molecular Mechanisms</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">References</th>
</tr>
</thead>
<tbody><tr><td rowspan="5" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">Hematologic tumors</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Myc-driven lymphomas</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Abnormally swollen mitochondria, OxPhos↓, ETC↓, intrinsic apoptosis</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Mitochondrial translation↓</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B37-ijms-20-03577" ref-type="bibr">37</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">CML</td>
<td align="center" valign="middle" rowspan="1" colspan="1">OxPhos↓, autophagy, intrinsic apoptosis</td>
<td align="center" valign="middle" rowspan="1" colspan="1">PI3K-AKT-mTOR↓, mitochondrial translation↓</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B33-ijms-20-03577" ref-type="bibr">33</xref>
,<xref rid="B35-ijms-20-03577" ref-type="bibr">35</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">ALL</td>
<td align="center" valign="middle" rowspan="1" colspan="1">OxPhos↓, oxidative damages</td>
<td align="center" valign="middle" rowspan="1" colspan="1">--</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B34-ijms-20-03577" ref-type="bibr">34</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">DLBCLs</td>
<td align="center" valign="middle" rowspan="1" colspan="1">OxPhos↓, ETC↓, ROS↑</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Mitochondrial translation↓</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B30-ijms-20-03577" ref-type="bibr">30</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">AML</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Abnormally swollen mitochondria, OxPhos↓</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Mitochondrial translation↓, EF-Tu↓, HIFs↑</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B22-ijms-20-03577" ref-type="bibr">22</xref>
,<xref rid="B38-ijms-20-03577" ref-type="bibr">38</xref>
]</td>
</tr>
<tr><td rowspan="13" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">Solid tumors</td>
<td align="center" valign="middle" rowspan="1" colspan="1">NSCLC</td>
<td align="center" valign="middle" rowspan="1" colspan="1">OxPhos↓, intrinsic apoptosis, ROS↑, MMP↓, ATP levels↓</td>
<td align="center" valign="middle" rowspan="1" colspan="1">--</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B28-ijms-20-03577" ref-type="bibr">28</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Ovarian cancer</td>
<td align="center" valign="middle" rowspan="1" colspan="1">OxPhos↓, ETC↓, ROS↑, oxidative damage, cell cycle arrest at G2/M phase, intrinsic apoptosis</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Mitochondrial translation↓, Myc↓</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B6-ijms-20-03577" ref-type="bibr">6</xref>
,<xref rid="B39-ijms-20-03577" ref-type="bibr">39</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">HCC</td>
<td align="center" valign="middle" rowspan="1" colspan="1">ATP levels↓, OxPhos↓, ROS↑, oxidative damage</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Mitochondrial translation↓</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B31-ijms-20-03577" ref-type="bibr">31</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">RB1-deficient TNBC</td>
<td align="center" valign="middle" rowspan="1" colspan="1">ATP levels↓, OxPhos↓</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Mitochondrial translation↓</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B29-ijms-20-03577" ref-type="bibr">29</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Melanoma</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Cell cycle arrest at G0/G1 phase, migration/invasion↓</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Cytoplasmic p21↓</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B25-ijms-20-03577" ref-type="bibr">25</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Glioma</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Cell cycle arrest at G0/G1 phase</td>
<td align="center" valign="middle" rowspan="1" colspan="1">miR-199b-5p-HES1-AKT↑</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B27-ijms-20-03577" ref-type="bibr">27</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Neuroblastoma</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Cell cycle arrest at G0/G1 phase</td>
<td align="center" valign="middle" rowspan="1" colspan="1">AKT-FOXO3a↓</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B26-ijms-20-03577" ref-type="bibr">26</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Oral squamous cell carcinoma</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Cell cycle arrest at G0/G1 phase</td>
<td align="center" valign="middle" rowspan="1" colspan="1">CDK4-CCNE2↓</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B24-ijms-20-03577" ref-type="bibr">24</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Multiple myeloma</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Cell cycle arrest at G0/G1 phase, autophagy</td>
<td align="center" valign="middle" rowspan="1" colspan="1">AMPK-mTOR↑</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B40-ijms-20-03577" ref-type="bibr">40</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Gastric cancer</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Autophagy</td>
<td align="center" valign="middle" rowspan="1" colspan="1">AMPK-mTOR↑</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B23-ijms-20-03577" ref-type="bibr">23</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Retinoblastoma</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Intrinsic apoptosis, oxidative damage, angiogenesis↓, ATP levels↓</td>
<td align="center" valign="middle" rowspan="1" colspan="1">--</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B41-ijms-20-03577" ref-type="bibr">41</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Cervical squamous cell carcinoma</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Intrinsic apoptosis</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Wnt/β-catenin↓</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B32-ijms-20-03577" ref-type="bibr">32</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Renal cell carcinoma</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Intrinsic apoptosis</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Mitochondrial translation↓, EF-Tu↓, PI3K/AKT-mTOR↓</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B42-ijms-20-03577" ref-type="bibr">42</xref>
]</td>
</tr>
</tbody>
</table>
<table-wrap-foot><fn><p>‘↑’ represents activation or unregulation, and ‘↓’ represents inhibition or dowregulation. ALL: acute lymphoblastic leukemia; DLBCLs: diffuse large B-cell lymphomas; AML: acute myeloid leukemia; HCC: hepatocellular carcinoma.</p>
</fn>
</table-wrap-foot>
</table-wrap>
</floats-group>
</pmc>
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