Molecular Determinants of Cancer Therapy Resistance to HDAC Inhibitor-Induced Autophagy
Identifieur interne : 000571 ( Pmc/Checkpoint ); précédent : 000570; suivant : 000572Molecular Determinants of Cancer Therapy Resistance to HDAC Inhibitor-Induced Autophagy
Auteurs : Maria Mrakovcic [Allemagne] ; Leopold F. FröhlichSource :
- Cancers [ 2072-6694 ] ; 2019.
Abstract
Histone deacetylation inhibitors (HDACi) offer high potential for future cancer therapy as they can re-establish the expression of epigenetically silenced cell death programs. HDACi-induced autophagy offers the possibility to counteract the frequently present apoptosis-resistance as well as stress conditions of cancer cells. Opposed to the function of apoptosis and necrosis however, autophagy activated in cancer cells can engage in a tumor-suppressive or tumor-promoting manner depending on mostly unclarified factors. As a physiological adaption to apoptosis resistance in early phases of tumorigenesis, autophagy seems to resume a tumorsuppressive role that confines tumor necrosis and inflammation or even induces cell death in malignant cells. During later stages of tumor development, chemotherapeutic drug-induced autophagy seems to be reprogrammed by the cancer cell to prevent its elimination and support tumor progression. Consistently, HDACi-mediated activation of autophagy seems to exert a protective function that prevents the induction of apoptotic or necrotic cell death in cancer cells. Thus, resistance to HDACi-induced cell death is often encountered in various types of cancer as well. The current review highlights the different mechanisms of HDACi-elicited autophagy and corresponding possible molecular determinants of therapeutic resistance in cancer.
Url:
DOI: 10.3390/cancers12010109
PubMed: 31906235
PubMed Central: 7016854
Affiliations:
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Molecular Determinants of Cancer Therapy Resistance to HDAC Inhibitor-Induced Autophagy</title><author><name sortKey="Mrakovcic, Maria" sort="Mrakovcic, Maria" uniqKey="Mrakovcic M" first="Maria" last="Mrakovcic">Maria Mrakovcic</name><affiliation><nlm:aff id="af1-cancers-12-00109">Department of Cranio-Maxillofacial Surgery, University of Münster, 48149 Münster, Germany;<email>leopold.froehlich@ukmuenster.de</email></nlm:aff></affiliation><affiliation wicri:level="3"><nlm:aff id="af2-cancers-12-00109">Department of Medical Microbiology, University of Münster, 48149 Münster, Germany</nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Medical Microbiology, University of Münster, 48149 Münster</wicri:regionArea><placeName><region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region><region type="district" nuts="2">District de Münster</region><settlement type="city">Münster</settlement></placeName></affiliation></author><author><name sortKey="Frohlich, Leopold F" sort="Frohlich, Leopold F" uniqKey="Frohlich L" first="Leopold F." last="Fröhlich">Leopold F. Fröhlich</name><affiliation><nlm:aff id="af1-cancers-12-00109">Department of Cranio-Maxillofacial Surgery, University of Münster, 48149 Münster, Germany;<email>leopold.froehlich@ukmuenster.de</email></nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">31906235</idno><idno type="pmc">7016854</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7016854</idno><idno type="RBID">PMC:7016854</idno><idno type="doi">10.3390/cancers12010109</idno><date when="2019">2019</date><idno type="wicri:Area/Pmc/Corpus">000911</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000911</idno><idno type="wicri:Area/Pmc/Curation">000911</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">000911</idno><idno type="wicri:Area/Pmc/Checkpoint">000571</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Checkpoint">000571</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Molecular Determinants of Cancer Therapy Resistance to HDAC Inhibitor-Induced Autophagy</title><author><name sortKey="Mrakovcic, Maria" sort="Mrakovcic, Maria" uniqKey="Mrakovcic M" first="Maria" last="Mrakovcic">Maria Mrakovcic</name><affiliation><nlm:aff id="af1-cancers-12-00109">Department of Cranio-Maxillofacial Surgery, University of Münster, 48149 Münster, Germany;<email>leopold.froehlich@ukmuenster.de</email></nlm:aff></affiliation><affiliation wicri:level="3"><nlm:aff id="af2-cancers-12-00109">Department of Medical Microbiology, University of Münster, 48149 Münster, Germany</nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Medical Microbiology, University of Münster, 48149 Münster</wicri:regionArea><placeName><region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region><region type="district" nuts="2">District de Münster</region><settlement type="city">Münster</settlement></placeName></affiliation></author><author><name sortKey="Frohlich, Leopold F" sort="Frohlich, Leopold F" uniqKey="Frohlich L" first="Leopold F." last="Fröhlich">Leopold F. Fröhlich</name><affiliation><nlm:aff id="af1-cancers-12-00109">Department of Cranio-Maxillofacial Surgery, University of Münster, 48149 Münster, Germany;<email>leopold.froehlich@ukmuenster.de</email></nlm:aff></affiliation></author></analytic><series><title level="j">Cancers</title><idno type="eISSN">2072-6694</idno><imprint><date when="2019">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Histone deacetylation inhibitors (HDACi) offer high potential for future cancer therapy as they can re-establish the expression of epigenetically silenced cell death programs. HDACi-induced autophagy offers the possibility to counteract the frequently present apoptosis-resistance as well as stress conditions of cancer cells. Opposed to the function of apoptosis and necrosis however, autophagy activated in cancer cells can engage in a tumor-suppressive or tumor-promoting manner depending on mostly unclarified factors. As a physiological adaption to apoptosis resistance in early phases of tumorigenesis, autophagy seems to resume a tumorsuppressive role that confines tumor necrosis and inflammation or even induces cell death in malignant cells. During later stages of tumor development, chemotherapeutic drug-induced autophagy seems to be reprogrammed by the cancer cell to prevent its elimination and support tumor progression. Consistently, HDACi-mediated activation of autophagy seems to exert a protective function that prevents the induction of apoptotic or necrotic cell death in cancer cells. Thus, resistance to HDACi-induced cell death is often encountered in various types of cancer as well. 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<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">31906235</article-id><article-id pub-id-type="pmc">7016854</article-id><article-id pub-id-type="doi">10.3390/cancers12010109</article-id><article-id pub-id-type="publisher-id">cancers-12-00109</article-id><article-categories><subj-group subj-group-type="heading"><subject>Review</subject></subj-group></article-categories><title-group><article-title>Molecular Determinants of Cancer Therapy Resistance to HDAC Inhibitor-Induced Autophagy</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Mrakovcic</surname><given-names>Maria</given-names></name><xref ref-type="aff" rid="af1-cancers-12-00109">1</xref><xref ref-type="aff" rid="af2-cancers-12-00109">2</xref><xref rid="c1-cancers-12-00109" ref-type="corresp">*</xref></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="true">https://orcid.org/0000-0001-7408-2166</contrib-id><name><surname>Fröhlich</surname><given-names>Leopold F.</given-names></name><xref ref-type="aff" rid="af1-cancers-12-00109">1</xref></contrib></contrib-group><aff id="af1-cancers-12-00109"><label>1</label>Department of Cranio-Maxillofacial Surgery, University of Münster, 48149 Münster, Germany;<email>leopold.froehlich@ukmuenster.de</email></aff><aff id="af2-cancers-12-00109"><label>2</label>Department of Medical Microbiology, University of Münster, 48149 Münster, Germany</aff><author-notes><corresp id="c1-cancers-12-00109"><label>*</label>Correspondence: <email>maria.mrakovcic@web.de</email>; Tel.: +49-251-83-55369</corresp></author-notes><pub-date pub-type="epub"><day>31</day><month>12</month><year>2019</year></pub-date><pub-date pub-type="collection"><month>1</month><year>2020</year></pub-date><volume>12</volume><issue>1</issue><elocation-id>109</elocation-id><history><date date-type="received"><day>22</day><month>11</month><year>2019</year></date><date date-type="accepted"><day>20</day><month>12</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>Histone deacetylation inhibitors (HDACi) offer high potential for future cancer therapy as they can re-establish the expression of epigenetically silenced cell death programs. HDACi-induced autophagy offers the possibility to counteract the frequently present apoptosis-resistance as well as stress conditions of cancer cells. Opposed to the function of apoptosis and necrosis however, autophagy activated in cancer cells can engage in a tumor-suppressive or tumor-promoting manner depending on mostly unclarified factors. As a physiological adaption to apoptosis resistance in early phases of tumorigenesis, autophagy seems to resume a tumorsuppressive role that confines tumor necrosis and inflammation or even induces cell death in malignant cells. During later stages of tumor development, chemotherapeutic drug-induced autophagy seems to be reprogrammed by the cancer cell to prevent its elimination and support tumor progression. Consistently, HDACi-mediated activation of autophagy seems to exert a protective function that prevents the induction of apoptotic or necrotic cell death in cancer cells. Thus, resistance to HDACi-induced cell death is often encountered in various types of cancer as well. The current review highlights the different mechanisms of HDACi-elicited autophagy and corresponding possible molecular determinants of therapeutic resistance in cancer. </p></abstract><kwd-group><kwd>histone deacetylase inhibitor</kwd><kwd>HDACi</kwd><kwd>drug resistance</kwd><kwd>autophagy</kwd><kwd>cell death</kwd><kwd>cancer</kwd><kwd>tumor</kwd><kwd>chemotherapy</kwd><kwd>radiotherapy</kwd></kwd-group></article-meta></front><floats-group><fig id="cancers-12-00109-f001" orientation="portrait" position="float"><label>Figure 1</label><caption><p>Overview about major effector mechanisms of histone deacetylase (HDAC) inhibitor (HDACi) in cancer cells. Important individually affected molecules (blue font) of the different categories of HDACi- activated anti-tumor pathways (grey boxes) are displayed. HDACi interfere with the deacetylation of histone and non-histone protein deacetylation of many tumor tuppressor genes and oncogenes (among other regulatory proteins) in cancer cells; this posttranslational modification renders them active and thereby induces the different effector mechanisms eventually causing cell death. ↑ upregulation or activation; ↓ downregulation or inhibition; HAT, histone acetyl transferase(s); ROS, rewactive oxygen species; TRX, thioredoxin; TBP2, TRX-binding protein 2; p53, tumor suppressor protein p53; VHL, von Hippel Lindau factor; HIF1α, hypoxia-inducible factor 1α; VEGF, vascular endothelial growth factor; bFGF, basic fibroblast growth factor; mTOR, mammalian target of rapamycin; NF-κB, nuclear factor lappa B; p21, cyclin-dependent kinase inhibitor 1 (p21<sup>CIP/WAF1</sup>); HDAC6, histon deacetylase 6, <italic>c-MYC</italic>, cellular homolog of the oncogene (<italic>v-myc</italic>) of avian myelocytomatosis virus strain 29; <italic>c-SRC</italic>, cellular SRC kinase oncogene; ER, endoplasmatic reticulum; Ku70, Lupus Ku autoantigen protein p70; Ku 86, Lupus Ku autoantigen protein p86; RAD51 (BRCC5); DNA repair protein RAD51 homolog; BRCA1/2, BRCA1/2, DNA repair associated (prev. breast cancer suceptibility protein ½).</p></caption><graphic xlink:href="cancers-12-00109-g001"></graphic></fig><fig id="cancers-12-00109-f002" orientation="portrait" position="float"><label>Figure 2</label><caption><p>Different mechanisms of histone deacetylase (HDAC) inhibitor-induced autophagy (grey boxes) and presumed molecular determinants that cause resistance (red font). As many cancer cells already block many pathways leading to apoptosis (black arrow), which cannot be reversed by HDACi treatment, the additional occurrence of resistance to autophagy or the additional use of autophagy inhibitors (red arrow) eventually facilitates cancer cell survival. BECN1, BECLIN-1; Mutp53, mutant p53; MDM2, mouse double minute 2; HSP90, heat shock protein 90; TRX, thioredoxin; MDR1, multiple drug resistance-1.</p></caption><graphic xlink:href="cancers-12-00109-g002"></graphic></fig><table-wrap id="cancers-12-00109-t001" orientation="portrait" position="float"><object-id pub-id-type="pii">cancers-12-00109-t001_Table 1</object-id><label>Table 1</label><caption><p>Mechanisms of HDACi-induced autophagy and potential mechanisms of resistance.</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">Autophagic Regulation</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">HDACi</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Cancer Cell Type</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Ref.</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Mechanisms of Resistance</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Ref.</th></tr></thead><tbody><tr><td rowspan="9" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">mTOR Inhibition</td><td align="center" valign="middle" rowspan="1" colspan="1">SAHA</td><td align="center" valign="middle" rowspan="1" colspan="1">ESS-1</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B49-cancers-12-00109" ref-type="bibr">49</xref>,<xref rid="B153-cancers-12-00109" ref-type="bibr">153</xref>]</td><td rowspan="9" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">Constitutive PI3K-AKT signaling<break></break>-AKToverexpression<break></break>-PI3K mutations<break></break>-Loss of PTEN, ARHI, LKB-1<break></break>-other upstream factors<break></break>Beclin-1 deficiency<break></break>Bcl-2 overexpression</td><td align="center" valign="middle" rowspan="1" colspan="1"></td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">SAHA</td><td align="center" valign="middle" rowspan="1" colspan="1">Glioblastoma </td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B136-cancers-12-00109" ref-type="bibr">136</xref>]</td><td align="center" valign="middle" rowspan="1" colspan="1"></td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Butyrate, SAHA</td><td align="center" valign="middle" rowspan="1" colspan="1">HelaS3 </td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B135-cancers-12-00109" ref-type="bibr">135</xref>,<xref rid="B154-cancers-12-00109" ref-type="bibr">154</xref>] </td><td align="center" valign="middle" rowspan="1" colspan="1"></td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">SAHA, OSU-HAD, C42</td><td align="center" valign="middle" rowspan="1" colspan="1">HCC, Hep3B, HepG2 </td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B139-cancers-12-00109" ref-type="bibr">139</xref>]</td><td rowspan="2" align="center" valign="middle" colspan="1">[<xref rid="B155-cancers-12-00109" ref-type="bibr">155</xref>,<xref rid="B156-cancers-12-00109" ref-type="bibr">156</xref>,<xref rid="B157-cancers-12-00109" ref-type="bibr">157</xref>,<xref rid="B158-cancers-12-00109" ref-type="bibr">158</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">SAHA</td><td align="center" valign="middle" rowspan="1" colspan="1">Jurkat T-cells </td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B137-cancers-12-00109" ref-type="bibr">137</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">SAHA</td><td align="center" valign="middle" rowspan="1" colspan="1">Gliobastoma SC</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B138-cancers-12-00109" ref-type="bibr">138</xref>] </td><td align="center" valign="middle" rowspan="1" colspan="1"></td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Apicidin</td><td align="center" valign="middle" rowspan="1" colspan="1">Salivary MEC</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B134-cancers-12-00109" ref-type="bibr">134</xref>,<xref rid="B159-cancers-12-00109" ref-type="bibr">159</xref>]</td><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">[<xref rid="B160-cancers-12-00109" ref-type="bibr">160</xref>,<xref rid="B161-cancers-12-00109" ref-type="bibr">161</xref>,<xref rid="B162-cancers-12-00109" ref-type="bibr">162</xref>,<xref rid="B163-cancers-12-00109" ref-type="bibr">163</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">* MGCD0103</td><td align="center" valign="middle" rowspan="1" colspan="1">Primary CLL </td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B151-cancers-12-00109" ref-type="bibr">151</xref>,<xref rid="B152-cancers-12-00109" ref-type="bibr">152</xref>] </td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">* SAHA, TSA, VPA, MS-275, JQ2</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">DS-AMKL cells</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B64-cancers-12-00109" ref-type="bibr">64</xref>]</td></tr><tr><td rowspan="6" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">ROS Accumulation</td><td align="center" valign="middle" rowspan="1" colspan="1">SAHA</td><td align="center" valign="middle" rowspan="1" colspan="1">Jurkat T-cells</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B137-cancers-12-00109" ref-type="bibr">137</xref>]</td><td rowspan="6" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">Increased levels of ROS scavengers/antioxidant enzymes (TRX)</td><td rowspan="6" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">[<xref rid="B164-cancers-12-00109" ref-type="bibr">164</xref>,<xref rid="B165-cancers-12-00109" ref-type="bibr">165</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">SAHA</td><td align="center" valign="middle" rowspan="1" colspan="1">CMLL </td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B58-cancers-12-00109" ref-type="bibr">58</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">FK228</td><td align="center" valign="middle" rowspan="1" colspan="1">Gastric carcinoma </td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B165-cancers-12-00109" ref-type="bibr">165</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">M-275</td><td align="center" valign="middle" rowspan="1" colspan="1">HCT116</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B166-cancers-12-00109" ref-type="bibr">166</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">VPA, SAHA</td><td align="center" valign="middle" rowspan="1" colspan="1">AML (Kasumi-1)</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B62-cancers-12-00109" ref-type="bibr">62</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">VPA, TSA</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">PaCa44, Panc1</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B130-cancers-12-00109" ref-type="bibr">130</xref>]</td></tr><tr><td rowspan="5" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">p53 Acetylation & Deficiency</td><td align="center" valign="middle" rowspan="1" colspan="1">Sirtinol</td><td align="center" valign="middle" rowspan="1" colspan="1">MCF-7</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B131-cancers-12-00109" ref-type="bibr">131</xref>]</td><td rowspan="5" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">Overexpression/GOF<break></break>of mutant p53 <break></break>Decreased degradation of p53 (MDM2, HSP90)</td><td rowspan="5" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">[<xref rid="B167-cancers-12-00109" ref-type="bibr">167</xref>,<xref rid="B168-cancers-12-00109" ref-type="bibr">168</xref>,<xref rid="B169-cancers-12-00109" ref-type="bibr">169</xref>,<xref rid="B170-cancers-12-00109" ref-type="bibr">170</xref>,<xref rid="B171-cancers-12-00109" ref-type="bibr">171</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">MHY2256</td><td align="center" valign="middle" rowspan="1" colspan="1">MCF-7 </td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B132-cancers-12-00109" ref-type="bibr">132</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">MHY2256</td><td align="center" valign="middle" rowspan="1" colspan="1">Endometrial </td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B133-cancers-12-00109" ref-type="bibr">133</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">SAHA</td><td align="center" valign="middle" rowspan="1" colspan="1">ESS-1</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B49-cancers-12-00109" ref-type="bibr">49</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">VPA, TSA</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">PaCa44, Panc1</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B130-cancers-12-00109" ref-type="bibr">130</xref>]</td></tr><tr><td rowspan="4" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">p21 Upregulation </td><td align="center" valign="middle" rowspan="1" colspan="1">SAHA, H40</td><td align="center" valign="middle" rowspan="1" colspan="1">PC-3M, HL-60</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B142-cancers-12-00109" ref-type="bibr">142</xref>]</td><td rowspan="4" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">Deregulated phosphorylation by Akt1 <break></break>Deregulation by p53 <break></break>(p53R2; cytoplasmic p21)</td><td rowspan="4" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">[<xref rid="B172-cancers-12-00109" ref-type="bibr">172</xref>,<xref rid="B173-cancers-12-00109" ref-type="bibr">173</xref>,<xref rid="B174-cancers-12-00109" ref-type="bibr">174</xref>,<xref rid="B175-cancers-12-00109" ref-type="bibr">175</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">MRJF4</td><td align="center" valign="middle" rowspan="1" colspan="1">PC3</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B128-cancers-12-00109" ref-type="bibr">128</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Apicidin</td><td align="center" valign="middle" rowspan="1" colspan="1">Salivary MEC </td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B134-cancers-12-00109" ref-type="bibr">134</xref>,<xref rid="B159-cancers-12-00109" ref-type="bibr">159</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">VPA, TSA</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">PaCa44, Panc1</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B130-cancers-12-00109" ref-type="bibr">130</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">NF-κB Hyper-acetylation</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">SAHA, MS-275</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">PC3</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B141-cancers-12-00109" ref-type="bibr">141</xref>]</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">(Constitutive) NF-κB upregulation</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B176-cancers-12-00109" ref-type="bibr">176</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">FOXO1 Transcription</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">LBH589</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">HepG2, HCT116</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B145-cancers-12-00109" ref-type="bibr">145</xref>]</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">MDR1 upregulation<break></break>Anti-oxidative enzyme upregulation </td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B177-cancers-12-00109" ref-type="bibr">177</xref>,<xref rid="B178-cancers-12-00109" ref-type="bibr">178</xref>,<xref rid="B179-cancers-12-00109" ref-type="bibr">179</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">DAPK Upregulation</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">SAHA, TSA, LBH589, JQ2</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">HCT116</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B147-cancers-12-00109" ref-type="bibr">147</xref>]</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">DAPK hypermethylation & ubiquitination</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B180-cancers-12-00109" ref-type="bibr">180</xref>,<xref rid="B181-cancers-12-00109" ref-type="bibr">181</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">NRF2 upregulation</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">SAHA, TSA</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Huh-7, MGC-803</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B146-cancers-12-00109" ref-type="bibr">146</xref>]</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Aberrant NRF2 <break></break>expression</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B182-cancers-12-00109" ref-type="bibr">182</xref>,<xref rid="B183-cancers-12-00109" ref-type="bibr">183</xref>,<xref rid="B184-cancers-12-00109" ref-type="bibr">184</xref>]</td></tr></tbody></table><table-wrap-foot><fn><p>* Suppression of autophagy due to mTOR activation; HDACi, histone deacetylase inhibitor; SAHA, suberoylanilide hydroxamic acid; VPA, valproic acid; TSA, trichostatin A; MGCD0103, mocetinostat; MS-275, etinostat; FK228, romidepsin; LBH589, panobinostat; SC, stem cells; MEC, Mucoepidermoid carcinoma; CLL, chronic lymphocytic leukemia;; DS-AMKL, down syndrome associated acute myeloid leukemia; AML, acute myeloid leukemia; MDM2, mouse double minute 2; TRX, thioredoxin; HSP90, heat shock protein 90.</p></fn></table-wrap-foot></table-wrap></floats-group></pmc><affiliations><list><country><li>Allemagne</li></country><region><li>District de Münster</li><li>Rhénanie-du-Nord-Westphalie</li></region><settlement><li>Münster</li></settlement></list><tree><noCountry><name sortKey="Frohlich, Leopold F" sort="Frohlich, Leopold F" uniqKey="Frohlich L" first="Leopold F." last="Fröhlich">Leopold F. Fröhlich</name></noCountry><country name="Allemagne"><region name="Rhénanie-du-Nord-Westphalie"><name sortKey="Mrakovcic, Maria" sort="Mrakovcic, Maria" uniqKey="Mrakovcic M" first="Maria" last="Mrakovcic">Maria Mrakovcic</name></region></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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