Gefitinib-mediated apoptosis is enhanced via inhibition of autophagy by chloroquine diphosphate in cutaneous squamous cell carcinoma cells
Identifieur interne : 000744 ( Pmc/Checkpoint ); précédent : 000743; suivant : 000745Gefitinib-mediated apoptosis is enhanced via inhibition of autophagy by chloroquine diphosphate in cutaneous squamous cell carcinoma cells
Auteurs : Jianyu Wang [République populaire de Chine] ; Chaopeng Wang [République populaire de Chine] ; Xia Hu [République populaire de Chine] ; Chang Yu [République populaire de Chine] ; Liang Zhou [République populaire de Chine] ; Zhenhua Ding [République populaire de Chine] ; Meijuan Zhou [République populaire de Chine]Source :
- Oncology Letters [ 1792-1074 ] ; 2019.
Abstract
The development of cutaneous squamous cell carcinoma (cSCC) is associated with activation of the epidermal growth factor receptor (EGFR). EGFR-targeting presents a promising strategy for improving therapeutic efficacy. However, recent studies have suggested that tumours overexpressing EGFR depend on autophagy for survival and exhibit resistance to EGFR-targeting drugs. Chloroquine diphosphate (CQ), an autophagy inhibitor that may enhance the cytocidal effect of gefitinib against cSCC, was used in the present study. Cytotoxicity assays were performed to determine the half-maximal inhibitory concentration values of gefitinib and CQ in A431 cells. Drug interaction was analysed using CompuSyn software, which also determined combination index and dose reduction index values. Apoptosis and autophagy of A431 cells were investigated via flow cytometry, western blotting analyses, acridine orange/ethidium bromide staining and monodansylcadaverine staining. Suppression of autophagy by CQ, which was demonstrated by an alteration in microtubule associated protein 1 light chain 3-B in CQ pre-treated A431 cells, significantly enhanced cell apoptosis, which suggested that gefitinib-induced autophagy is cytoprotective. Thus, CQ was demonstrated to exhibit a synergistic apoptotic effect when used in combination with gefitinib during cSCC therapy. Further
Url:
DOI: 10.3892/ol.2019.10308
PubMed: 31289508
PubMed Central: 6540344
Affiliations:
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<series><title level="j">Oncology Letters</title>
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<front><div type="abstract" xml:lang="en"><p>The development of cutaneous squamous cell carcinoma (cSCC) is associated with activation of the epidermal growth factor receptor (EGFR). EGFR-targeting presents a promising strategy for improving therapeutic efficacy. However, recent studies have suggested that tumours overexpressing EGFR depend on autophagy for survival and exhibit resistance to EGFR-targeting drugs. Chloroquine diphosphate (CQ), an autophagy inhibitor that may enhance the cytocidal effect of gefitinib against cSCC, was used in the present study. Cytotoxicity assays were performed to determine the half-maximal inhibitory concentration values of gefitinib and CQ in A431 cells. Drug interaction was analysed using CompuSyn software, which also determined combination index and dose reduction index values. Apoptosis and autophagy of A431 cells were investigated via flow cytometry, western blotting analyses, acridine orange/ethidium bromide staining and monodansylcadaverine staining. Suppression of autophagy by CQ, which was demonstrated by an alteration in microtubule associated protein 1 light chain 3-B in CQ pre-treated A431 cells, significantly enhanced cell apoptosis, which suggested that gefitinib-induced autophagy is cytoprotective. Thus, CQ was demonstrated to exhibit a synergistic apoptotic effect when used in combination with gefitinib during cSCC therapy. Further <italic>in vivo</italic>
investigations are required to confirm the results of the present study.</p>
</div>
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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">Oncol Lett</journal-id>
<journal-id journal-id-type="iso-abbrev">Oncol Lett</journal-id>
<journal-id journal-id-type="publisher-id">OL</journal-id>
<journal-title-group><journal-title>Oncology Letters</journal-title>
</journal-title-group>
<issn pub-type="ppub">1792-1074</issn>
<issn pub-type="epub">1792-1082</issn>
<publisher><publisher-name>D.A. Spandidos</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">31289508</article-id>
<article-id pub-id-type="pmc">6540344</article-id>
<article-id pub-id-type="doi">10.3892/ol.2019.10308</article-id>
<article-id pub-id-type="publisher-id">OL-0-0-10308</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Articles</subject>
</subj-group>
</article-categories>
<title-group><article-title>Gefitinib-mediated apoptosis is enhanced via inhibition of autophagy by chloroquine diphosphate in cutaneous squamous cell carcinoma cells</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Wang</surname>
<given-names>Jianyu</given-names>
</name>
<xref ref-type="aff" rid="af1-ol-0-0-10308"></xref>
<xref rid="fn1-ol-0-0-10308" ref-type="author-notes">*</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Wang</surname>
<given-names>Chaopeng</given-names>
</name>
<xref ref-type="aff" rid="af1-ol-0-0-10308"></xref>
<xref rid="fn1-ol-0-0-10308" ref-type="author-notes">*</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Hu</surname>
<given-names>Xia</given-names>
</name>
<xref ref-type="aff" rid="af1-ol-0-0-10308"></xref>
<xref rid="fn1-ol-0-0-10308" ref-type="author-notes">*</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Yu</surname>
<given-names>Chang</given-names>
</name>
<xref ref-type="aff" rid="af1-ol-0-0-10308"></xref>
</contrib>
<contrib contrib-type="author"><name><surname>Zhou</surname>
<given-names>Liang</given-names>
</name>
<xref ref-type="aff" rid="af1-ol-0-0-10308"></xref>
</contrib>
<contrib contrib-type="author"><name><surname>Ding</surname>
<given-names>Zhenhua</given-names>
</name>
<xref ref-type="aff" rid="af1-ol-0-0-10308"></xref>
</contrib>
<contrib contrib-type="author"><name><surname>Zhou</surname>
<given-names>Meijuan</given-names>
</name>
<xref ref-type="aff" rid="af1-ol-0-0-10308"></xref>
<xref rid="c1-ol-0-0-10308" ref-type="corresp"></xref>
</contrib>
</contrib-group>
<aff id="af1-ol-0-0-10308">Department of Radiation Medicine, School of Public Health, Southern Medical University, Guangzhou, Guangdong 510515, P.R. China</aff>
<author-notes><corresp id="c1-ol-0-0-10308"><italic>Correspondence to</italic>
: Professor Meijuan Zhou, Department of Radiation Medicine, School of Public Health, Southern Medical University, 1023 Shatai South Road, Guangzhou, Guangdong 510515, P.R. China, E-mail: <email>lkzmj@smu.edu.cn</email>
</corresp>
<fn id="fn1-ol-0-0-10308"><label>*</label>
<p>Contributed equally</p>
</fn>
</author-notes>
<pub-date pub-type="ppub"><month>7</month>
<year>2019</year>
</pub-date>
<pub-date pub-type="epub"><day>03</day>
<month>5</month>
<year>2019</year>
</pub-date>
<pub-date pub-type="pmc-release"><day>03</day>
<month>5</month>
<year>2019</year>
</pub-date>
<pmc-comment> PMC Release delay is 0 months and 0 days and was based on the . </pmc-comment>
<volume>18</volume>
<issue>1</issue>
<fpage>368</fpage>
<lpage>374</lpage>
<history><date date-type="received"><day>23</day>
<month>4</month>
<year>2018</year>
</date>
<date date-type="accepted"><day>21</day>
<month>3</month>
<year>2019</year>
</date>
</history>
<permissions><copyright-statement>Copyright: © Wang et al.</copyright-statement>
<copyright-year>2019</copyright-year>
<license license-type="open-access"><license-p>This is an open access article distributed under the terms of the <ext-link ext-link-type="uri" xlink:href="https://creativecommons.org/licenses/by-nc-nd/4.0/">Creative Commons Attribution-NonCommercial-NoDerivs License</ext-link>
, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made.</license-p>
</license>
</permissions>
<abstract><p>The development of cutaneous squamous cell carcinoma (cSCC) is associated with activation of the epidermal growth factor receptor (EGFR). EGFR-targeting presents a promising strategy for improving therapeutic efficacy. However, recent studies have suggested that tumours overexpressing EGFR depend on autophagy for survival and exhibit resistance to EGFR-targeting drugs. Chloroquine diphosphate (CQ), an autophagy inhibitor that may enhance the cytocidal effect of gefitinib against cSCC, was used in the present study. Cytotoxicity assays were performed to determine the half-maximal inhibitory concentration values of gefitinib and CQ in A431 cells. Drug interaction was analysed using CompuSyn software, which also determined combination index and dose reduction index values. Apoptosis and autophagy of A431 cells were investigated via flow cytometry, western blotting analyses, acridine orange/ethidium bromide staining and monodansylcadaverine staining. Suppression of autophagy by CQ, which was demonstrated by an alteration in microtubule associated protein 1 light chain 3-B in CQ pre-treated A431 cells, significantly enhanced cell apoptosis, which suggested that gefitinib-induced autophagy is cytoprotective. Thus, CQ was demonstrated to exhibit a synergistic apoptotic effect when used in combination with gefitinib during cSCC therapy. Further <italic>in vivo</italic>
investigations are required to confirm the results of the present study.</p>
</abstract>
<kwd-group><kwd>cutaneous squamous cell carcinoma</kwd>
<kwd>autophagy</kwd>
<kwd>apoptosis</kwd>
<kwd>gefitinib</kwd>
<kwd>chloroquine diphosphate</kwd>
<kwd>synergism</kwd>
</kwd-group>
</article-meta>
</front>
<floats-group><fig id="f1-ol-0-0-10308" orientation="portrait" position="float"><label>Figure 1.</label>
<caption><p>Cytotoxicity of gefitinib and chloroquine diphosphate. Cellular cytotoxicity in A431 cells treated with either (A) gefitinib or (B) chloroquine diphosphate in A431 cells was investigated via Cell Counting Kit-8 assays. Data are presented as the means ± standard deviation (n=3).</p>
</caption>
<graphic xlink:href="ol-18-01-0368-g00"></graphic>
</fig>
<fig id="f2-ol-0-0-10308" orientation="portrait" position="float"><label>Figure 2.</label>
<caption><p>CompuSyn analysis of cytotoxicity data was used to determine synergy, additivity and antagonism between Ge and CQ in A431 cells. (A) Dose-effect plots of Ge, CQ and Ge + CQ. (B) CI plots presenting CI values of <1 indicated synergism between Ge and CQ. (C) Isobolograms revealing effective doses required for inhibition at 50% (Fa 0.5), 75% (Fa 0.75) and 90% (Fa 0.9) for each individual drug. Synergism is demonstrated by the dose pair plotted as a point (symbol) below their respective Fa isobole or line. (D) DRI of Ge and CQ drug combinations are presented, and >1 DRI value indicated favourable drug combinations. (E) Data obtained via CompuSyn analysis. All data are representative of three independent experimental repeats. CI, combination index; DRI, dose reduction index; Ge, gefitinib; CQ, chloroquine diphosphate; Fa, fraction affected.</p>
</caption>
<graphic xlink:href="ol-18-01-0368-g01"></graphic>
</fig>
<fig id="f3-ol-0-0-10308" orientation="portrait" position="float"><label>Figure 3.</label>
<caption><p>Ge and CQ induce apoptosis via the caspase-dependent apoptosis pathway. (A) A431 cells were stained with acridine orange/ethidium bromide to determine levels of apoptosis and then observed under a fluorescence microscope. Magnification, ×10. Scale bar, 500 µm. (B) Following treatment with 20 µM Ge and 188 µM CQ for 12 h, levels of apoptosis were analysed in A431 cells. (C) Statistical analysis of apoptosis levels in A431 cells in untreated, single drug treatment and combination treatment groups. Data are expressed as the mean ± standard deviation (n=3). ***P<0.001 vs. control group. ΦΦΦP<0.001 vs. Ge treatment group. ###P<0.001 vs. CQ treatment group. (D) Protein expression levels of caspase-3, cleaved caspase-3, PARP and cleaved PARP. CQ, chloroquine diphosphate; Ge, gefitinib; PARP, poly-(ADP-ribose) polymerase; PI, propidium iodide; FITC, fluorescein isothiocyanate.</p>
</caption>
<graphic xlink:href="ol-18-01-0368-g02"></graphic>
</fig>
<fig id="f4-ol-0-0-10308" orientation="portrait" position="float"><label>Figure 4.</label>
<caption><p>Ge induces autophagy and CQ blocks autophagy in A431 cells. (A) A431 cells were treated with increasing concentrations of Ge for 12 h in the presence or absence of pre-treatment with CQ for 1 h. Expression levels of LC3-II were detected via western blotting. (B) A431 cells were treated with Ge for 3, 6, 9 or 12 h in the presence or absence of pre-treatment with CQ for 1 h. Expression levels of LC3-II were detected via western blotting. (C) A431 cells observed under a fluorescence microscope were stained with monodansylcadaverine to identify the formation of autophagic vacuoles. Magnification, ×20. Scale bar, 500 µm. CQ, chloroquine diphosphate; Ge, gefitinib; LC3-II, microtubule associated protein 1 light chain 3β.</p>
</caption>
<graphic xlink:href="ol-18-01-0368-g03"></graphic>
</fig>
</floats-group>
</pmc>
<affiliations><list><country><li>République populaire de Chine</li>
</country>
</list>
<tree><country name="République populaire de Chine"><noRegion><name sortKey="Wang, Jianyu" sort="Wang, Jianyu" uniqKey="Wang J" first="Jianyu" last="Wang">Jianyu Wang</name>
</noRegion>
<name sortKey="Ding, Zhenhua" sort="Ding, Zhenhua" uniqKey="Ding Z" first="Zhenhua" last="Ding">Zhenhua Ding</name>
<name sortKey="Hu, Xia" sort="Hu, Xia" uniqKey="Hu X" first="Xia" last="Hu">Xia Hu</name>
<name sortKey="Wang, Chaopeng" sort="Wang, Chaopeng" uniqKey="Wang C" first="Chaopeng" last="Wang">Chaopeng Wang</name>
<name sortKey="Yu, Chang" sort="Yu, Chang" uniqKey="Yu C" first="Chang" last="Yu">Chang Yu</name>
<name sortKey="Zhou, Liang" sort="Zhou, Liang" uniqKey="Zhou L" first="Liang" last="Zhou">Liang Zhou</name>
<name sortKey="Zhou, Meijuan" sort="Zhou, Meijuan" uniqKey="Zhou M" first="Meijuan" last="Zhou">Meijuan Zhou</name>
</country>
</tree>
</affiliations>
</record>
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