Autophagy and Its Relationship to Epithelial to Mesenchymal Transition: When Autophagy Inhibition for Cancer Therapy Turns Counterproductive
Identifieur interne : 000867 ( Pmc/Curation ); précédent : 000866; suivant : 000868Autophagy and Its Relationship to Epithelial to Mesenchymal Transition: When Autophagy Inhibition for Cancer Therapy Turns Counterproductive
Auteurs : Guadalupe Rojas-Sanchez ; Israel Cotzomi-Ortega ; Nidia G. Pazos-Salazar ; Julio Reyes-Leyva ; Paola Maycotte [Mexique]Source :
- Biology [ 2079-7737 ] ; 2019.
Abstract
The manipulation of autophagy for cancer therapy has gained recent interest in clinical settings. Although inhibition of autophagy is currently being used in clinical trials for the treatment of several malignancies, autophagy has been shown to have diverse implications for normal cell homeostasis, cancer cell survival, and signaling to cells in the tumor microenvironment. Among these implications and of relevance for cancer therapy, the autophagic process is known to be involved in the regulation of protein secretion, in tumor cell immunogenicity, and in the regulation of epithelial-to-mesenchymal transition (EMT), a critical step in the process of cancer cell invasion. In this work, we have reviewed recent evidence linking autophagy to the regulation of EMT in cancer and normal epithelial cells, and have discussed important implications for the manipulation of autophagy during cancer therapy.
Url:
DOI: 10.3390/biology8040071
PubMed: 31554173
PubMed Central: 6956138
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<author><name sortKey="Rojas Sanchez, Guadalupe" sort="Rojas Sanchez, Guadalupe" uniqKey="Rojas Sanchez G" first="Guadalupe" last="Rojas-Sanchez">Guadalupe Rojas-Sanchez</name>
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<affiliation><nlm:aff id="af2-biology-08-00071">Centro de Investigación Biomédica de Oriente (CIBIOR), Instituto Mexicano del Seguro Social (IMSS), Km 4.5 Carretera Atlixco-Metepec HGZ5, Puebla 74360, Mexico;<email>julio.reyes@imss.gob.mx</email>
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<author><name sortKey="Cotzomi Ortega, Israel" sort="Cotzomi Ortega, Israel" uniqKey="Cotzomi Ortega I" first="Israel" last="Cotzomi-Ortega">Israel Cotzomi-Ortega</name>
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(G.R.-S.);<email>israelcotzomi@gmail.com</email>
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<author><name sortKey="Cotzomi Ortega, Israel" sort="Cotzomi Ortega, Israel" uniqKey="Cotzomi Ortega I" first="Israel" last="Cotzomi-Ortega">Israel Cotzomi-Ortega</name>
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(G.R.-S.);<email>israelcotzomi@gmail.com</email>
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<author><name sortKey="Pazos Salazar, Nidia G" sort="Pazos Salazar, Nidia G" uniqKey="Pazos Salazar N" first="Nidia G." last="Pazos-Salazar">Nidia G. Pazos-Salazar</name>
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(G.R.-S.);<email>israelcotzomi@gmail.com</email>
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<author><name sortKey="Reyes Leyva, Julio" sort="Reyes Leyva, Julio" uniqKey="Reyes Leyva J" first="Julio" last="Reyes-Leyva">Julio Reyes-Leyva</name>
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<front><div type="abstract" xml:lang="en"><p>The manipulation of autophagy for cancer therapy has gained recent interest in clinical settings. Although inhibition of autophagy is currently being used in clinical trials for the treatment of several malignancies, autophagy has been shown to have diverse implications for normal cell homeostasis, cancer cell survival, and signaling to cells in the tumor microenvironment. Among these implications and of relevance for cancer therapy, the autophagic process is known to be involved in the regulation of protein secretion, in tumor cell immunogenicity, and in the regulation of epithelial-to-mesenchymal transition (EMT), a critical step in the process of cancer cell invasion. In this work, we have reviewed recent evidence linking autophagy to the regulation of EMT in cancer and normal epithelial cells, and have discussed important implications for the manipulation of autophagy during cancer therapy.</p>
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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">Biology (Basel)</journal-id>
<journal-id journal-id-type="iso-abbrev">Biology (Basel)</journal-id>
<journal-id journal-id-type="publisher-id">biology</journal-id>
<journal-title-group><journal-title>Biology</journal-title>
</journal-title-group>
<issn pub-type="epub">2079-7737</issn>
<publisher><publisher-name>MDPI</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">31554173</article-id>
<article-id pub-id-type="pmc">6956138</article-id>
<article-id pub-id-type="doi">10.3390/biology8040071</article-id>
<article-id pub-id-type="publisher-id">biology-08-00071</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Review</subject>
</subj-group>
</article-categories>
<title-group><article-title>Autophagy and Its Relationship to Epithelial to Mesenchymal Transition: When Autophagy Inhibition for Cancer Therapy Turns Counterproductive</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Rojas-Sanchez</surname>
<given-names>Guadalupe</given-names>
</name>
<xref ref-type="aff" rid="af1-biology-08-00071">1</xref>
<xref ref-type="aff" rid="af2-biology-08-00071">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Cotzomi-Ortega</surname>
<given-names>Israel</given-names>
</name>
<xref ref-type="aff" rid="af1-biology-08-00071">1</xref>
<xref ref-type="aff" rid="af2-biology-08-00071">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Pazos-Salazar</surname>
<given-names>Nidia G.</given-names>
</name>
<xref ref-type="aff" rid="af1-biology-08-00071">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Reyes-Leyva</surname>
<given-names>Julio</given-names>
</name>
<xref ref-type="aff" rid="af2-biology-08-00071">2</xref>
</contrib>
<contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="true">https://orcid.org/0000-0003-4059-0554</contrib-id>
<name><surname>Maycotte</surname>
<given-names>Paola</given-names>
</name>
<xref ref-type="aff" rid="af3-biology-08-00071">3</xref>
<xref rid="c1-biology-08-00071" ref-type="corresp">*</xref>
</contrib>
</contrib-group>
<aff id="af1-biology-08-00071"><label>1</label>
Facultad de Ciencias Químicas, Benemérita Universidad Autónoma de Puebla, Ciudad Universitaria, Puebla 72570, Mexico;<email>grs.pharm@gmail.com</email>
(G.R.-S.);<email>israelcotzomi@gmail.com</email>
(I.C.-O.);<email>nidianaye@hotmail.com</email>
(N.G.P.-S.)</aff>
<aff id="af2-biology-08-00071"><label>2</label>
Centro de Investigación Biomédica de Oriente (CIBIOR), Instituto Mexicano del Seguro Social (IMSS), Km 4.5 Carretera Atlixco-Metepec HGZ5, Puebla 74360, Mexico;<email>julio.reyes@imss.gob.mx</email>
</aff>
<aff id="af3-biology-08-00071"><label>3</label>
Consejo Nacional de Ciencia y Tecnología (CONACYT)—CIBIOR, IMSS, Puebla 74360, Mexico</aff>
<author-notes><corresp id="c1-biology-08-00071"><label>*</label>
Correspondence: <email>pmaycottego@conacyt.mx</email>
</corresp>
</author-notes>
<pub-date pub-type="epub"><day>24</day>
<month>9</month>
<year>2019</year>
</pub-date>
<pub-date pub-type="collection"><month>12</month>
<year>2019</year>
</pub-date>
<volume>8</volume>
<issue>4</issue>
<elocation-id>71</elocation-id>
<history><date date-type="received"><day>30</day>
<month>8</month>
<year>2019</year>
</date>
<date date-type="accepted"><day>20</day>
<month>9</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>The manipulation of autophagy for cancer therapy has gained recent interest in clinical settings. Although inhibition of autophagy is currently being used in clinical trials for the treatment of several malignancies, autophagy has been shown to have diverse implications for normal cell homeostasis, cancer cell survival, and signaling to cells in the tumor microenvironment. Among these implications and of relevance for cancer therapy, the autophagic process is known to be involved in the regulation of protein secretion, in tumor cell immunogenicity, and in the regulation of epithelial-to-mesenchymal transition (EMT), a critical step in the process of cancer cell invasion. In this work, we have reviewed recent evidence linking autophagy to the regulation of EMT in cancer and normal epithelial cells, and have discussed important implications for the manipulation of autophagy during cancer therapy.</p>
</abstract>
<kwd-group><kwd>autophagy</kwd>
<kwd>cancer</kwd>
<kwd>cancer therapy</kwd>
<kwd>EMT</kwd>
</kwd-group>
</article-meta>
</front>
<floats-group><fig id="biology-08-00071-f001" orientation="portrait" position="float"><label>Figure 1</label>
<caption><p>The autophagic pathway and its regulation. Two major regulators of autophagy are the mammalian target of rapamycin complex 1 (mTORC1) and AMP-activated protein kinase (AMPK). In amino-acid-rich conditions, mTORC1 negatively modulates autophagy. Under nutrient deprivation or low energy levels (sensed by AMPK), mTORC1 is inhibited and autophagy is induced. Growth factor withdrawal and hypoxia are also known triggers of autophagy. Pharmacological inhibitors of the different steps of the autophagic pathway have been described. It is of clinical relevance, since they are FDA approved drugs, that chloroquine and hydroxychloroquine are the only drugs currently used in clinical trials to inhibit autophagy in solid tumors.</p>
</caption>
<graphic xlink:href="biology-08-00071-g001"></graphic>
</fig>
<fig id="biology-08-00071-f002" orientation="portrait" position="float"><label>Figure 2</label>
<caption><p>The role of autophagy in cancer. Autophagy functions as a tumor-suppressing process in normal cells by removing damaged proteins and organelles, maintaining low reactive oxygen species (ROS) levels by mitochondria elimination and decreasing DNA damage and genome instability. Autophagy also degrades p62, the accumulation of which is known to induce pro-tumorigenic signaling and induce inflammation. Once transformation has occurred, autophagy can also maintain cellular senescence to avoid the proliferation of transformed cells. On the other hand, once a tumor is established, tumor cells use autophagy as a survival mechanism to survive metabolic stress and hypoxia, to maintain tumor-related inflammation, to maintain cancer stem cell (CSC) survival, and to survive to cancer therapy. Additionally, during the invasion process, autophagy has been shown to be necessary for metalloprotease secretion, for degradation of the extracellular matrix, and for survival to anoikis in circulating tumor cells (CTCs). Evidence suggests that autophagy could also have a dual role in the regulation of EMT, and that inhibition of autophagy might be beneficial for some patients, since it would eliminate autophagy-dependent tumor cells and avoid invasion.</p>
</caption>
<graphic xlink:href="biology-08-00071-g002"></graphic>
</fig>
<fig id="biology-08-00071-f003" orientation="portrait" position="float"><label>Figure 3</label>
<caption><p>Cytokine signaling in the tumor microenvironment. Tumor cells can control the tumor microenvironment by secreting cytokines and chemokines, which recruit and define the type of immune cells in the tumor, as well as inducing the formation of cancer associated fibroblasts (CAFs). Cytokine secretion can also influence malignancy in neighboring tumor cells by the induction of EMT and by inducing the formation of circulating tumor cells (CTCs) and metastasis. In advanced stages of cancer, a complex communication network among tumor cells, immune cells, and the other cells in the tumor microenvironment defines immune evasion, and induces proliferation and malignancy. In the figure, cytokines, chemokines, and growth factors that promote epithelial to mesenchymal transition (EMT) and malignancy are marked in red. Anti-tumorigenic immune cells are marked in blue and immune cells associated with tumor promotion are marked in red. Cancer cells are marked in purple and CSC in black.</p>
</caption>
<graphic xlink:href="biology-08-00071-g003"></graphic>
</fig>
<table-wrap id="biology-08-00071-t001" orientation="portrait" position="float"><object-id pub-id-type="pii">biology-08-00071-t001_Table 1</object-id>
<label>Table 1</label>
<caption><p>Beneficial and undesirable effects of the inhibition of autophagy in the treatment of cancer. Despite extensive evidence showing the potential for autophagy inhibition during cancer therapy, other studies suggest that inhibition of autophagy could have undesirable effects during cancer therapy. Atg, autophagy-related; MMTV-PyMT, mouse mammary tumor virus promoter/enhancer-polyomavirus middle T-antigen; MEFs, mouse embryonic fibroblasts; KO, knockout; CRC, colorectal cancer; CSCs, cancer stem cells; HCC, hepatocellular carcinoma; EMT, epithelial-to-mesenchymal transition.</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">Beneficial Effects of Autophagy Inhibition</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Cancer-Related Feature</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Counter-Productive Effects of Autophagy Inhibition</th>
</tr>
</thead>
<tbody><tr><td align="center" valign="middle" rowspan="1" colspan="1">RAS-transformed cancer cells [<xref rid="B36-biology-08-00071" ref-type="bibr">36</xref>
,<xref rid="B37-biology-08-00071" ref-type="bibr">37</xref>
]</td>
<td rowspan="6" align="center" valign="middle" colspan="1">Proliferation/<break></break>
cancer Progression</td>
<td align="center" valign="middle" rowspan="1" colspan="1"></td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1"><italic>K-ras<sup>G12D</sup>
</italic>
or <italic>Braf<sup>V600E</sup>
;atg5/7<sup>flox/flox</sup>
</italic>
mouse lung cancer models [<xref rid="B24-biology-08-00071" ref-type="bibr">24</xref>
,<xref rid="B25-biology-08-00071" ref-type="bibr">25</xref>
,<xref rid="B38-biology-08-00071" ref-type="bibr">38</xref>
]</td>
<td align="center" valign="middle" rowspan="1" colspan="1">MEFs with Atg gene KO; epidermal squamous cell carcinoma mouse xenografts [<xref rid="B39-biology-08-00071" ref-type="bibr">39</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">MMTV-PyMT mice with FIP200<sup>−/−</sup>
in mammary epithelial cells [<xref rid="B40-biology-08-00071" ref-type="bibr">40</xref>
]</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Dying autophagy-deficient cell lines induced proliferation of resistant cells in response to targeted therapy [<xref rid="B41-biology-08-00071" ref-type="bibr">41</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">KRAS mutant pancreatic cancer [<xref rid="B42-biology-08-00071" ref-type="bibr">42</xref>
]</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Mice with autophagy inhibition together with p53<sup>−/−</sup>
had increased pancreatic ductal adenocarcinoma frequency [<xref rid="B23-biology-08-00071" ref-type="bibr">23</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">BRAF<sup>V600E</sup>
central nervous system tumors [<xref rid="B43-biology-08-00071" ref-type="bibr">43</xref>
] </td>
<td align="center" valign="middle" rowspan="1" colspan="1"></td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Triple negative breast cancer cell lines [<xref rid="B44-biology-08-00071" ref-type="bibr">44</xref>
]</td>
<td align="center" valign="middle" rowspan="1" colspan="1"></td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">RACK1-induced autophagy in CRC cells [<xref rid="B45-biology-08-00071" ref-type="bibr">45</xref>
]</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"></td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"></td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">RAS transformed cancer cells [<xref rid="B37-biology-08-00071" ref-type="bibr">37</xref>
]</td>
<td rowspan="10" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">Migration/<break></break>
invasion/<break></break>
EMT or metastasis establishment</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Gastric cancer cell lines and mouse xenografts [<xref rid="B46-biology-08-00071" ref-type="bibr">46</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">HCC cell lines and xenografts [<xref rid="B47-biology-08-00071" ref-type="bibr">47</xref>
]</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Loss of ULK1 to suppress autophagy in the MDA-MB-231 breast cancer cell line during hypoxia [<xref rid="B48-biology-08-00071" ref-type="bibr">48</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Starvation- [<xref rid="B49-biology-08-00071" ref-type="bibr">49</xref>
,<xref rid="B50-biology-08-00071" ref-type="bibr">50</xref>
], TGF-β2- [<xref rid="B51-biology-08-00071" ref-type="bibr">51</xref>
], or DRAM1-<break></break>
induced [<xref rid="B52-biology-08-00071" ref-type="bibr">52</xref>
] autophagy in hepatic carcinoma cell lines</td>
<td align="center" valign="middle" rowspan="1" colspan="1">RAS-mutated cancer cells [<xref rid="B53-biology-08-00071" ref-type="bibr">53</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">TGFβ1- or rapamycin-induced autophagy in non-small cell lung cancer cells [<xref rid="B54-biology-08-00071" ref-type="bibr">54</xref>
]</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Glioblastoma cell lines [<xref rid="B55-biology-08-00071" ref-type="bibr">55</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Rapamycin-induced autophagy in CRC cell lines [<xref rid="B56-biology-08-00071" ref-type="bibr">56</xref>
]</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Ovarian cancer cell lines [<xref rid="B57-biology-08-00071" ref-type="bibr">57</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Cisplatin-induced autophagy in nasopharyngeal carcinoma cells [<xref rid="B58-biology-08-00071" ref-type="bibr">58</xref>
]</td>
<td align="center" valign="middle" rowspan="1" colspan="1">DEDD-induced autophagy in breast cancer cell lines [<xref rid="B59-biology-08-00071" ref-type="bibr">59</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1"></td>
<td align="center" valign="middle" rowspan="1" colspan="1">MEFs with <italic>Atg</italic>
gene KO; epidermal squamous cell carcinoma mouse xenografts [<xref rid="B39-biology-08-00071" ref-type="bibr">39</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1"></td>
<td align="center" valign="middle" rowspan="1" colspan="1">MDA-MB-231 breast cancer cell line [<xref rid="B60-biology-08-00071" ref-type="bibr">60</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1"></td>
<td align="center" valign="middle" rowspan="1" colspan="1">H1299 lung or HeLa cervical cancer cell lines [<xref rid="B61-biology-08-00071" ref-type="bibr">61</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"></td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Liver-specific autophagy-deficiency or TGFβ−treated immortalized hepatocytes [<xref rid="B62-biology-08-00071" ref-type="bibr">62</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">MMTV-PyMT mice with <italic>FIP200</italic>
<sup>−/−</sup>
conditional KO in mammary epithelial cells [<xref rid="B40-biology-08-00071" ref-type="bibr">40</xref>
]</td>
<td rowspan="2" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">Immunoediting</td>
<td align="center" valign="middle" rowspan="1" colspan="1">Gastric cancer cell lines [<xref rid="B35-biology-08-00071" ref-type="bibr">35</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>K-ras<sup>G12D</sup>
;Atg5<sup>flox/flox</sup>
</italic>
mouse lung cancer model [<xref rid="B24-biology-08-00071" ref-type="bibr">24</xref>
] </td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Colorectal or osteosarcoma cancer cell lines treated with immunogenic chemotherapy [<xref rid="B34-biology-08-00071" ref-type="bibr">34</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Ovarian cancer spheroids [<xref rid="B63-biology-08-00071" ref-type="bibr">63</xref>
]</td>
<td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">Tumor-initiating cells/CSCs</td>
<td align="center" valign="middle" rowspan="1" colspan="1"></td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Breast cancer stem cells [<xref rid="B32-biology-08-00071" ref-type="bibr">32</xref>
,<xref rid="B64-biology-08-00071" ref-type="bibr">64</xref>
,<xref rid="B65-biology-08-00071" ref-type="bibr">65</xref>
]</td>
<td align="center" valign="middle" rowspan="1" colspan="1"></td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Hepatic cancer stem cells [<xref rid="B66-biology-08-00071" ref-type="bibr">66</xref>
]</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"></td>
</tr>
</tbody>
</table>
</table-wrap>
</floats-group>
</pmc>
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