ID1 confers cancer cell chemoresistance through STAT3/ATF6-mediated induction of autophagy
Identifieur interne : 000127 ( Pmc/Checkpoint ); précédent : 000126; suivant : 000128ID1 confers cancer cell chemoresistance through STAT3/ATF6-mediated induction of autophagy
Auteurs : Jiao Meng [République populaire de Chine] ; Kaiyi Liu [République populaire de Chine] ; Yang Shao [République populaire de Chine] ; Xu Feng [République populaire de Chine] ; Zhaodong Ji [République populaire de Chine] ; Bin Chang [République populaire de Chine] ; Yan Wang [République populaire de Chine] ; Ling Xu [République populaire de Chine] ; Gong Yang [République populaire de Chine]Source :
- Cell Death & Disease [ 2041-4889 ] ; 2020.
Abstract
Chemoresistance is one of the major reasons leading to ovarian cancer high mortality and poor survival. Studies have shown that the alteration of cellular autophagy is associated with cancer cell chemoresistance. Here, we investigated whether the ovarian cancer chemoresistance is associated with the autophagy induced by the inhibitor of DNA binding 1 (ID1). By using gene overexpression or silencing, luciferase assay and human specimens, we show that ID1 induces high autophagy and confers cancer cell chemoresistance. The mechanistic study demonstrates that ID1 first activates the NF-κB signaling through facilitating the nuclear translocation of NF-κB p65, which strengthens the expression and secretion of IL-6 from cancer cells to subsequently activate the signal transducer and activator of transcription 3 (STAT3) through the protein phosphorylation at Y705. We further identified that STAT3 functions to promote the transcription of the activating transcription factor 6 (ATF6), which induces endoplasmic reticulum stress to promote cellular autophagy, granting cancer cell resistance to both cisplatin and paclitaxel treatment. Moreover, we found a significant correlation between the expression of ID1 and ATF6 in 1104 high grade serous ovarian cancer tissues, and that patients with the high expression of ID1 or ATF6 were resistant to platinum treatment and had the poor overall survival and progression-free survival. Thus, we have uncovered a mechanism in which ID1 confers cancer cell chemoresistance largely through the STAT3/ATF6-induced autophagy. The involved molecules, including ID1, STAT3, and ATF6, may have a potential to be targeted in combination with chemotherapeutic agents to improve ovarian cancer survival.
Url:
DOI: 10.1038/s41419-020-2327-1
PubMed: 32080166
PubMed Central: 7033197
Affiliations:
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<institution>Cancer Institute,</institution>
<institution>Fudan University Shanghai Cancer Center,</institution>
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Shanghai, 200032 China</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>Shanghai</wicri:regionArea>
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<affiliation wicri:level="1"><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 0125 2443</institution-id>
<institution-id institution-id-type="GRID">grid.8547.e</institution-id>
<institution>Department of Oncology, Shanghai Medical College,</institution>
<institution>Fudan University,</institution>
</institution-wrap>
Shanghai, 200032 China</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>Shanghai</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="Aff7"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 0125 2443</institution-id>
<institution-id institution-id-type="GRID">grid.8547.e</institution-id>
<institution>Central Laboratory, Shanghai Fifth People’s Hospital,</institution>
<institution>Fudan University,</institution>
</institution-wrap>
Shanghai, 200140 China</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>Shanghai</wicri:regionArea>
</affiliation>
</author>
</analytic>
<series><title level="j">Cell Death & Disease</title>
<idno type="eISSN">2041-4889</idno>
<imprint><date when="2020">2020</date>
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<front><div type="abstract" xml:lang="en"><p id="Par1">Chemoresistance is one of the major reasons leading to ovarian cancer high mortality and poor survival. Studies have shown that the alteration of cellular autophagy is associated with cancer cell chemoresistance. Here, we investigated whether the ovarian cancer chemoresistance is associated with the autophagy induced by the inhibitor of DNA binding 1 (ID1). By using gene overexpression or silencing, luciferase assay and human specimens, we show that ID1 induces high autophagy and confers cancer cell chemoresistance. The mechanistic study demonstrates that ID1 first activates the NF-κB signaling through facilitating the nuclear translocation of NF-κB p65, which strengthens the expression and secretion of IL-6 from cancer cells to subsequently activate the signal transducer and activator of transcription 3 (STAT3) through the protein phosphorylation at Y705. We further identified that STAT3 functions to promote the transcription of the activating transcription factor 6 (ATF6), which induces endoplasmic reticulum stress to promote cellular autophagy, granting cancer cell resistance to both cisplatin and paclitaxel treatment. Moreover, we found a significant correlation between the expression of ID1 and ATF6 in 1104 high grade serous ovarian cancer tissues, and that patients with the high expression of ID1 or ATF6 were resistant to platinum treatment and had the poor overall survival and progression-free survival. Thus, we have uncovered a mechanism in which ID1 confers cancer cell chemoresistance largely through the STAT3/ATF6-induced autophagy. The involved molecules, including ID1, STAT3, and ATF6, may have a potential to be targeted in combination with chemotherapeutic agents to improve ovarian cancer survival.</p>
</div>
</front>
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<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Cell Death Dis</journal-id>
<journal-id journal-id-type="iso-abbrev">Cell Death Dis</journal-id>
<journal-title-group><journal-title>Cell Death & Disease</journal-title>
</journal-title-group>
<issn pub-type="epub">2041-4889</issn>
<publisher><publisher-name>Nature Publishing Group UK</publisher-name>
<publisher-loc>London</publisher-loc>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">32080166</article-id>
<article-id pub-id-type="pmc">7033197</article-id>
<article-id pub-id-type="publisher-id">2327</article-id>
<article-id pub-id-type="doi">10.1038/s41419-020-2327-1</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Article</subject>
</subj-group>
</article-categories>
<title-group><article-title>ID1 confers cancer cell chemoresistance through STAT3/ATF6-mediated induction of autophagy</article-title>
</title-group>
<contrib-group><contrib contrib-type="author" equal-contrib="yes"><name><surname>Meng</surname>
<given-names>Jiao</given-names>
</name>
<xref ref-type="aff" rid="Aff1">1</xref>
<xref ref-type="aff" rid="Aff2">2</xref>
</contrib>
<contrib contrib-type="author" equal-contrib="yes"><name><surname>Liu</surname>
<given-names>Kaiyi</given-names>
</name>
<xref ref-type="aff" rid="Aff2">2</xref>
<xref ref-type="aff" rid="Aff3">3</xref>
</contrib>
<contrib contrib-type="author" equal-contrib="yes"><name><surname>Shao</surname>
<given-names>Yang</given-names>
</name>
<xref ref-type="aff" rid="Aff1">1</xref>
<xref ref-type="aff" rid="Aff2">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Feng</surname>
<given-names>Xu</given-names>
</name>
<xref ref-type="aff" rid="Aff1">1</xref>
<xref ref-type="aff" rid="Aff2">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Ji</surname>
<given-names>Zhaodong</given-names>
</name>
<xref ref-type="aff" rid="Aff1">1</xref>
<xref ref-type="aff" rid="Aff2">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Chang</surname>
<given-names>Bin</given-names>
</name>
<xref ref-type="aff" rid="Aff2">2</xref>
<xref ref-type="aff" rid="Aff4">4</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Wang</surname>
<given-names>Yan</given-names>
</name>
<address><email>wangxyyan@sina.com</email>
</address>
<xref ref-type="aff" rid="Aff2">2</xref>
<xref ref-type="aff" rid="Aff5">5</xref>
</contrib>
<contrib contrib-type="author" corresp="yes"><name><surname>Xu</surname>
<given-names>Ling</given-names>
</name>
<address><email>edelweiss76@163.com</email>
</address>
<xref ref-type="aff" rid="Aff6">6</xref>
</contrib>
<contrib contrib-type="author" corresp="yes"><name><surname>Yang</surname>
<given-names>Gong</given-names>
</name>
<address><email>yanggong@fudan.edu.cn</email>
</address>
<xref ref-type="aff" rid="Aff1">1</xref>
<xref ref-type="aff" rid="Aff2">2</xref>
<xref ref-type="aff" rid="Aff7">7</xref>
</contrib>
<aff id="Aff1"><label>1</label>
<institution-wrap><institution-id institution-id-type="ISNI">0000 0004 1808 0942</institution-id>
<institution-id institution-id-type="GRID">grid.452404.3</institution-id>
<institution>Cancer Institute,</institution>
<institution>Fudan University Shanghai Cancer Center,</institution>
</institution-wrap>
Shanghai, 200032 China</aff>
<aff id="Aff2"><label>2</label>
<institution-wrap><institution-id institution-id-type="ISNI">0000 0001 0125 2443</institution-id>
<institution-id institution-id-type="GRID">grid.8547.e</institution-id>
<institution>Department of Oncology, Shanghai Medical College,</institution>
<institution>Fudan University,</institution>
</institution-wrap>
Shanghai, 200032 China</aff>
<aff id="Aff3"><label>3</label>
<institution-wrap><institution-id institution-id-type="ISNI">0000 0001 0125 2443</institution-id>
<institution-id institution-id-type="GRID">grid.8547.e</institution-id>
<institution>Institute of Pediatrics, Children’s Hospital,</institution>
<institution>Fudan University,</institution>
</institution-wrap>
Shanghai, 201102 China</aff>
<aff id="Aff4"><label>4</label>
<institution-wrap><institution-id institution-id-type="ISNI">0000 0004 1808 0942</institution-id>
<institution-id institution-id-type="GRID">grid.452404.3</institution-id>
<institution>Department of Pathology,</institution>
<institution>Fudan University Shanghai Cancer Center,</institution>
</institution-wrap>
Shanghai, 200032 China</aff>
<aff id="Aff5"><label>5</label>
<institution-wrap><institution-id institution-id-type="ISNI">0000 0004 1808 0942</institution-id>
<institution-id institution-id-type="GRID">grid.452404.3</institution-id>
<institution>Department of Radiation Oncology,</institution>
<institution>Fudan University Shanghai Cancer Center,</institution>
</institution-wrap>
Shanghai, 200032 China</aff>
<aff id="Aff6"><label>6</label>
<institution-wrap><institution-id institution-id-type="ISNI">0000 0001 0125 2443</institution-id>
<institution-id institution-id-type="GRID">grid.8547.e</institution-id>
<institution>Department of Obstetrics and Gynecology, Minhang Hospital,</institution>
<institution>Fudan University,</institution>
</institution-wrap>
Shanghai, 201199 China</aff>
<aff id="Aff7"><label>7</label>
<institution-wrap><institution-id institution-id-type="ISNI">0000 0001 0125 2443</institution-id>
<institution-id institution-id-type="GRID">grid.8547.e</institution-id>
<institution>Central Laboratory, Shanghai Fifth People’s Hospital,</institution>
<institution>Fudan University,</institution>
</institution-wrap>
Shanghai, 200140 China</aff>
</contrib-group>
<pub-date pub-type="epub"><day>20</day>
<month>2</month>
<year>2020</year>
</pub-date>
<pub-date pub-type="pmc-release"><day>20</day>
<month>2</month>
<year>2020</year>
</pub-date>
<pub-date pub-type="collection"><month>2</month>
<year>2020</year>
</pub-date>
<volume>11</volume>
<issue>2</issue>
<elocation-id>137</elocation-id>
<history><date date-type="received"><day>28</day>
<month>5</month>
<year>2019</year>
</date>
<date date-type="rev-recd"><day>1</day>
<month>2</month>
<year>2020</year>
</date>
<date date-type="accepted"><day>4</day>
<month>2</month>
<year>2020</year>
</date>
</history>
<permissions><copyright-statement>© The Author(s) 2020</copyright-statement>
<license license-type="OpenAccess"><license-p><bold>Open Access</bold>
This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit <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 id="Abs1"><p id="Par1">Chemoresistance is one of the major reasons leading to ovarian cancer high mortality and poor survival. Studies have shown that the alteration of cellular autophagy is associated with cancer cell chemoresistance. Here, we investigated whether the ovarian cancer chemoresistance is associated with the autophagy induced by the inhibitor of DNA binding 1 (ID1). By using gene overexpression or silencing, luciferase assay and human specimens, we show that ID1 induces high autophagy and confers cancer cell chemoresistance. The mechanistic study demonstrates that ID1 first activates the NF-κB signaling through facilitating the nuclear translocation of NF-κB p65, which strengthens the expression and secretion of IL-6 from cancer cells to subsequently activate the signal transducer and activator of transcription 3 (STAT3) through the protein phosphorylation at Y705. We further identified that STAT3 functions to promote the transcription of the activating transcription factor 6 (ATF6), which induces endoplasmic reticulum stress to promote cellular autophagy, granting cancer cell resistance to both cisplatin and paclitaxel treatment. Moreover, we found a significant correlation between the expression of ID1 and ATF6 in 1104 high grade serous ovarian cancer tissues, and that patients with the high expression of ID1 or ATF6 were resistant to platinum treatment and had the poor overall survival and progression-free survival. Thus, we have uncovered a mechanism in which ID1 confers cancer cell chemoresistance largely through the STAT3/ATF6-induced autophagy. The involved molecules, including ID1, STAT3, and ATF6, may have a potential to be targeted in combination with chemotherapeutic agents to improve ovarian cancer survival.</p>
</abstract>
<kwd-group kwd-group-type="npg-subject"><title>Subject terms</title>
<kwd>Autophagy</kwd>
<kwd>Cancer therapy</kwd>
</kwd-group>
<funding-group><award-group><funding-source><institution-wrap><institution-id institution-id-type="FundRef">https://doi.org/10.13039/501100001809</institution-id>
<institution>National Natural Science Foundation of China (National Science Foundation of China)</institution>
</institution-wrap>
</funding-source>
<award-id>81572553</award-id>
<award-id>81772789</award-id>
<award-id>81372797</award-id>
<award-id>81502049</award-id>
<principal-award-recipient><name><surname>Wang</surname>
<given-names>Yan</given-names>
</name>
<name><surname>Yang</surname>
<given-names>Gong</given-names>
</name>
</principal-award-recipient>
</award-group>
</funding-group>
<funding-group><award-group><funding-source><institution>National Key R&D Program of China (2016YFC1303100)</institution>
</funding-source>
</award-group>
</funding-group>
<custom-meta-group><custom-meta><meta-name>issue-copyright-statement</meta-name>
<meta-value>© The Author(s) 2020</meta-value>
</custom-meta>
</custom-meta-group>
</article-meta>
</front>
</pmc>
<affiliations><list><country><li>République populaire de Chine</li>
</country>
</list>
<tree><country name="République populaire de Chine"><noRegion><name sortKey="Meng, Jiao" sort="Meng, Jiao" uniqKey="Meng J" first="Jiao" last="Meng">Jiao Meng</name>
</noRegion>
<name sortKey="Chang, Bin" sort="Chang, Bin" uniqKey="Chang B" first="Bin" last="Chang">Bin Chang</name>
<name sortKey="Chang, Bin" sort="Chang, Bin" uniqKey="Chang B" first="Bin" last="Chang">Bin Chang</name>
<name sortKey="Feng, Xu" sort="Feng, Xu" uniqKey="Feng X" first="Xu" last="Feng">Xu Feng</name>
<name sortKey="Feng, Xu" sort="Feng, Xu" uniqKey="Feng X" first="Xu" last="Feng">Xu Feng</name>
<name sortKey="Ji, Zhaodong" sort="Ji, Zhaodong" uniqKey="Ji Z" first="Zhaodong" last="Ji">Zhaodong Ji</name>
<name sortKey="Ji, Zhaodong" sort="Ji, Zhaodong" uniqKey="Ji Z" first="Zhaodong" last="Ji">Zhaodong Ji</name>
<name sortKey="Liu, Kaiyi" sort="Liu, Kaiyi" uniqKey="Liu K" first="Kaiyi" last="Liu">Kaiyi Liu</name>
<name sortKey="Liu, Kaiyi" sort="Liu, Kaiyi" uniqKey="Liu K" first="Kaiyi" last="Liu">Kaiyi Liu</name>
<name sortKey="Meng, Jiao" sort="Meng, Jiao" uniqKey="Meng J" first="Jiao" last="Meng">Jiao Meng</name>
<name sortKey="Shao, Yang" sort="Shao, Yang" uniqKey="Shao Y" first="Yang" last="Shao">Yang Shao</name>
<name sortKey="Shao, Yang" sort="Shao, Yang" uniqKey="Shao Y" first="Yang" last="Shao">Yang Shao</name>
<name sortKey="Wang, Yan" sort="Wang, Yan" uniqKey="Wang Y" first="Yan" last="Wang">Yan Wang</name>
<name sortKey="Wang, Yan" sort="Wang, Yan" uniqKey="Wang Y" first="Yan" last="Wang">Yan Wang</name>
<name sortKey="Xu, Ling" sort="Xu, Ling" uniqKey="Xu L" first="Ling" last="Xu">Ling Xu</name>
<name sortKey="Yang, Gong" sort="Yang, Gong" uniqKey="Yang G" first="Gong" last="Yang">Gong Yang</name>
<name sortKey="Yang, Gong" sort="Yang, Gong" uniqKey="Yang G" first="Gong" last="Yang">Gong Yang</name>
<name sortKey="Yang, Gong" sort="Yang, Gong" uniqKey="Yang G" first="Gong" last="Yang">Gong Yang</name>
</country>
</tree>
</affiliations>
</record>
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