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Sufentanil impairs autophagic degradation and inhibits cell migration in NCI-H460 in vitro

Identifieur interne : 000376 ( Pmc/Checkpoint ); précédent : 000375; suivant : 000377

Sufentanil impairs autophagic degradation and inhibits cell migration in NCI-H460 in vitro

Auteurs : Hui Jiang [République populaire de Chine] ; Hongxian Wang [République populaire de Chine] ; Weiwei Zou [République populaire de Chine] ; Yuexia Hu [République populaire de Chine] ; Chen Chen [République populaire de Chine] ; Chunhui Wang [République populaire de Chine]

Source :

RBID : PMC:6865617

Abstract

Metastasis, which involves the spread of cancer cells to distant tissues and organs, is a major cause of cancer-associated mortality. Although the use of anesthetics and analgesics may affect cancer cell metastasis, the underlying molecular mechanism remains unclear. Autophagy is a lysosome-based dynamic intracellular catabolic process that serves a crucial role in cancer cell metastasis. In order to investigate the role of autophagy in the migration of cancer cells treated with analgesics, immunofluorescence, western blotting, wound healing assay and cell invasion assay were performed in the present study. The results from immunofluorescence and western blotting demonstrated that the opioid analgesic sufentanil stimulated LC3 induction in NCI-H460 cells. Furthermore, sufentanil increased LC3 and Beclin1 protein levels, but inhibited the fusion of autophagosomes and lysosomes. In addition, sufentanil decreased cathepsin D protein level and increased p62 protein level. The addition of chloroquine (CQ) to sufentanil did not induce a further increase in LC3-II protein levels in NCI-H460 cells, suggesting the impairment of autophagic degradation. Furthermore, treatment with trehalose stimulated the migration of sufentanil-treated cells, whereas additional treatment with CQ did not further decrease the migration of sufentanil-treated cells. In addition, sufentanil co-treatment with trehalose significantly increased the invasion of lung cancer cells, whereas, additional treatment with CQ did not further reduce the invasion of sufentanil-treated cells. These results indicated that autophagy may be involved in the inhibition of NCI-H460 cell migration by sufentanil, and that sufentanil may be considered as a favorable analgesic for patients with lung cancer.


Url:
DOI: 10.3892/ol.2019.10997
PubMed: 31788126
PubMed Central: 6865617


Affiliations:


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PMC:6865617

Le document en format XML

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<p>Metastasis, which involves the spread of cancer cells to distant tissues and organs, is a major cause of cancer-associated mortality. Although the use of anesthetics and analgesics may affect cancer cell metastasis, the underlying molecular mechanism remains unclear. Autophagy is a lysosome-based dynamic intracellular catabolic process that serves a crucial role in cancer cell metastasis. In order to investigate the role of autophagy in the migration of cancer cells treated with analgesics, immunofluorescence, western blotting, wound healing assay and cell invasion assay were performed in the present study. The results from immunofluorescence and western blotting demonstrated that the opioid analgesic sufentanil stimulated LC3 induction in NCI-H460 cells. Furthermore, sufentanil increased LC3 and Beclin1 protein levels, but inhibited the fusion of autophagosomes and lysosomes. In addition, sufentanil decreased cathepsin D protein level and increased p62 protein level. The addition of chloroquine (CQ) to sufentanil did not induce a further increase in LC3-II protein levels in NCI-H460 cells, suggesting the impairment of autophagic degradation. Furthermore, treatment with trehalose stimulated the migration of sufentanil-treated cells, whereas additional treatment with CQ did not further decrease the migration of sufentanil-treated cells. In addition, sufentanil co-treatment with trehalose significantly increased the invasion of lung cancer cells, whereas, additional treatment with CQ did not further reduce the invasion of sufentanil-treated cells. These results indicated that autophagy may be involved in the inhibition of NCI-H460 cell migration by sufentanil, and that sufentanil may be considered as a favorable analgesic for patients with lung cancer.</p>
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</TEI>
<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">31788126</article-id>
<article-id pub-id-type="pmc">6865617</article-id>
<article-id pub-id-type="doi">10.3892/ol.2019.10997</article-id>
<article-id pub-id-type="publisher-id">OL-0-0-10997</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Articles</subject>
</subj-group>
</article-categories>
<title-group>
<article-title>Sufentanil impairs autophagic degradation and inhibits cell migration in NCI-H460
<italic>in vitro</italic>
</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Jiang</surname>
<given-names>Hui</given-names>
</name>
<xref ref-type="aff" rid="af1-ol-0-0-10997"></xref>
<xref rid="fn1-ol-0-0-10997" ref-type="author-notes">*</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Wang</surname>
<given-names>Hongxian</given-names>
</name>
<xref ref-type="aff" rid="af1-ol-0-0-10997"></xref>
<xref rid="fn1-ol-0-0-10997" ref-type="author-notes">*</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Zou</surname>
<given-names>Weiwei</given-names>
</name>
<xref ref-type="aff" rid="af1-ol-0-0-10997"></xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Hu</surname>
<given-names>Yuexia</given-names>
</name>
<xref ref-type="aff" rid="af1-ol-0-0-10997"></xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Chen</surname>
<given-names>Chen</given-names>
</name>
<xref ref-type="aff" rid="af1-ol-0-0-10997"></xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Wang</surname>
<given-names>Chunhui</given-names>
</name>
<xref ref-type="aff" rid="af1-ol-0-0-10997"></xref>
<xref rid="c1-ol-0-0-10997" ref-type="corresp"></xref>
</contrib>
</contrib-group>
<aff id="af1-ol-0-0-10997">Department of Anesthesiology, The Fourth Affiliated Hospital of Anhui Medical University, Anhui, Hefei 20032, P.R. China</aff>
<author-notes>
<corresp id="c1-ol-0-0-10997">
<italic>Correspondence to</italic>
: Dr Chunhui Wang, Department of Anesthesiology, The Fourth Affiliated Hospital of Anhui Medical University, 100 Huaihai Road, Anhui, Hefei 20032, P.R. China, E-mail:
<email>wangchhaymz@163.com</email>
</corresp>
<fn id="fn1-ol-0-0-10997">
<label>*</label>
<p>Contributed equally</p>
</fn>
</author-notes>
<pub-date pub-type="ppub">
<month>12</month>
<year>2019</year>
</pub-date>
<pub-date pub-type="epub">
<day>17</day>
<month>10</month>
<year>2019</year>
</pub-date>
<pub-date pub-type="pmc-release">
<day>17</day>
<month>10</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>6</issue>
<fpage>6829</fpage>
<lpage>6835</lpage>
<history>
<date date-type="received">
<day>18</day>
<month>10</month>
<year>2018</year>
</date>
<date date-type="accepted">
<day>13</day>
<month>8</month>
<year>2019</year>
</date>
</history>
<permissions>
<copyright-statement>Copyright: © Jiang 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>Metastasis, which involves the spread of cancer cells to distant tissues and organs, is a major cause of cancer-associated mortality. Although the use of anesthetics and analgesics may affect cancer cell metastasis, the underlying molecular mechanism remains unclear. Autophagy is a lysosome-based dynamic intracellular catabolic process that serves a crucial role in cancer cell metastasis. In order to investigate the role of autophagy in the migration of cancer cells treated with analgesics, immunofluorescence, western blotting, wound healing assay and cell invasion assay were performed in the present study. The results from immunofluorescence and western blotting demonstrated that the opioid analgesic sufentanil stimulated LC3 induction in NCI-H460 cells. Furthermore, sufentanil increased LC3 and Beclin1 protein levels, but inhibited the fusion of autophagosomes and lysosomes. In addition, sufentanil decreased cathepsin D protein level and increased p62 protein level. The addition of chloroquine (CQ) to sufentanil did not induce a further increase in LC3-II protein levels in NCI-H460 cells, suggesting the impairment of autophagic degradation. Furthermore, treatment with trehalose stimulated the migration of sufentanil-treated cells, whereas additional treatment with CQ did not further decrease the migration of sufentanil-treated cells. In addition, sufentanil co-treatment with trehalose significantly increased the invasion of lung cancer cells, whereas, additional treatment with CQ did not further reduce the invasion of sufentanil-treated cells. These results indicated that autophagy may be involved in the inhibition of NCI-H460 cell migration by sufentanil, and that sufentanil may be considered as a favorable analgesic for patients with lung cancer.</p>
</abstract>
<kwd-group>
<kwd>autophagy</kwd>
<kwd>sufentanil</kwd>
<kwd>cancer cell migration</kwd>
</kwd-group>
</article-meta>
</front>
<floats-group>
<fig id="f1-ol-0-0-10997" orientation="portrait" position="float">
<label>Figure 1.</label>
<caption>
<p>Sufentanil induced autophagosomes accumulation. (A) Immunofluorescence microscopy for LC3 labeling (green). (B) Quantification of LC3 positive cells from (A). (C) Western blotting analysis of LC3, Beclin1 p62 and β-actin levels. NCI-H460 cells were treated with sufentanil (1 nM) or trehalose (100 mM) for 24 h prior to the experiments. The arrows are pointing to autophagosomes. Scale bar, 5 µm. ***P<0.001 (comparison between any two means). Sufen, sufentanil; Tre, trehalose.</p>
</caption>
<graphic xlink:href="ol-18-06-6829-g00"></graphic>
</fig>
<fig id="f2-ol-0-0-10997" orientation="portrait" position="float">
<label>Figure 2.</label>
<caption>
<p>Sufentanil blocked the fusion of autophagosomes and lysosomes. (A) Immunofluorescence microscopy for LC3 (green) and LAMP1 (red) double staining. (B) Pearson's co-localization coefficient of cells from (A) NCI-H460 cells were treated with sufentanil (1 nM) or trehalose (100 mM) for 24 h prior to the experiments. Scale bar, 5 µm. *P<0.05 (comparison between any two means). LAMP1, lysosomal-associated membrane protein 1; Sufen, sufentanil; Tre, trehalose.</p>
</caption>
<graphic xlink:href="ol-18-06-6829-g01"></graphic>
</fig>
<fig id="f3-ol-0-0-10997" orientation="portrait" position="float">
<label>Figure 3.</label>
<caption>
<p>Sufentanil impaired autophagic degradation. (A) Western blot analysis of p62, LC3, CathD and β-actin levels. NCI-H460 cells were treated with 1 nM sufentanil for 24 h. (B-D) Quantification of p62, LC3II and CathD levels compared with β-actin levels. (E) Western blot analysis of LC3 and β-actin. Cells were treated with 1 nM sufentanil with or without CQ for 24 h prior to experiments. (F) Quantification of LC3II levels compared with β-actin levels. **P<0.01 (comparison between any two means); NS, not significant. Sufen, sufentanil. CathD, cathepsin D; CQ, chloroquine.</p>
</caption>
<graphic xlink:href="ol-18-06-6829-g02"></graphic>
</fig>
<fig id="f4-ol-0-0-10997" orientation="portrait" position="float">
<label>Figure 4.</label>
<caption>
<p>Autophagy was involved in the inhibition of migration by sufentanil. (A) Sufentanil suppressed wound closure. Scratched NCI-H460 cells were treated with 1 nM sufentanil, PBS, 1 nM sufentanil + 50 µM CQ or 1 nM sufentanil + 100 mM trehalose for 24 h. Scale bar, 1 mm. (B) Wound closure quantification from (A). (C) Cell invasion images. Scale bar, 50 µm. (D) Quantification of the invaded cells per field from (C). **P<0.01 and ***P<0.001 (comparison between any two means). CQ, chloroquine; NS, not significant; Sufen, sufentanil; Tre, trehalose.</p>
</caption>
<graphic xlink:href="ol-18-06-6829-g03"></graphic>
</fig>
</floats-group>
</pmc>
<affiliations>
<list>
<country>
<li>République populaire de Chine</li>
</country>
<region>
<li>Anhui</li>
</region>
<settlement>
<li>Hefei</li>
</settlement>
</list>
<tree>
<country name="République populaire de Chine">
<region name="Anhui">
<name sortKey="Jiang, Hui" sort="Jiang, Hui" uniqKey="Jiang H" first="Hui" last="Jiang">Hui Jiang</name>
</region>
<name sortKey="Chen, Chen" sort="Chen, Chen" uniqKey="Chen C" first="Chen" last="Chen">Chen Chen</name>
<name sortKey="Hu, Yuexia" sort="Hu, Yuexia" uniqKey="Hu Y" first="Yuexia" last="Hu">Yuexia Hu</name>
<name sortKey="Wang, Chunhui" sort="Wang, Chunhui" uniqKey="Wang C" first="Chunhui" last="Wang">Chunhui Wang</name>
<name sortKey="Wang, Hongxian" sort="Wang, Hongxian" uniqKey="Wang H" first="Hongxian" last="Wang">Hongxian Wang</name>
<name sortKey="Zou, Weiwei" sort="Zou, Weiwei" uniqKey="Zou W" first="Weiwei" last="Zou">Weiwei Zou</name>
</country>
</tree>
</affiliations>
</record>

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