Dihydromyricetin induced lncRNA MALAT1-TFEB-dependent autophagic cell death in cutaneous squamous cell carcinoma
Identifieur interne : 000921 ( Ncbi/Merge ); précédent : 000920; suivant : 000922Dihydromyricetin induced lncRNA MALAT1-TFEB-dependent autophagic cell death in cutaneous squamous cell carcinoma
Auteurs : Miduo Tan [République populaire de Chine] ; Bin Jiang [République populaire de Chine] ; Haihua Wang [République populaire de Chine] ; Wei Ouyang [République populaire de Chine] ; Xiang Chen [République populaire de Chine] ; Taoli Wang [République populaire de Chine] ; Dan Dong [République populaire de Chine] ; Shun Yi [République populaire de Chine] ; Jiansheng Yi [République populaire de Chine] ; Yan Huang [République populaire de Chine] ; Manling Tang [République populaire de Chine] ; Yan Xiao [République populaire de Chine] ; Zuiming Jiang [République populaire de Chine] ; Wei Zhou [République populaire de Chine]Source :
- Journal of Cancer [ 1837-9664 ] ; 2019.
Abstract
Cutaneous squamous cell carcinoma (CSCC) is the second most common skin cancer. Dihydromyricetin (DHM), a Rattan tea extract, has been shown to have antitumor activity with no obvious toxicity to normal cells in vitro and in vivo. However, its efficacy in the treatment of CSCC and the underlying antitumor mechanism has not been fully elucidated yet. In our study, DHM increased autophagic flux in the A431 cells, as evidenced by the upregulation of LC3-II and downregulation of P62/SQSTM1. Moreover, the pharmacological or genetic blocking autophagy decreased DHM-induced cell death, indicating DHM triggered autophagic cell death in A431 cells. Specifically, DHM induced TFEB(Ser142) de-phosphorylation, activated TFEB nuclear translocation and increased of TFEB reporter activity, which contributed to the expression of autophagy-related genes and subsequent initiated autophagic cell death in A431 cells. Importantly, DHM decreased lncRNA MALAT1 expression and MALAT1 overexpression abrogated the effects of DHM on TFEB-dependent autophagy both in vitro and in vivo. Taken together, DHM induces CSCC cell death via inducing excessive autophagy, which is mediated through the
Url:
DOI: 10.7150/jca.32807
PubMed: 31413743
PubMed Central: 6691703
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TFEB-dependent autophagic cell death in cutaneous squamous cell carcinoma</title>
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<front><div type="abstract" xml:lang="en"><p>Cutaneous squamous cell carcinoma (CSCC) is the second most common skin cancer. Dihydromyricetin (DHM), a Rattan tea extract, has been shown to have antitumor activity with no obvious toxicity to normal cells in vitro and in vivo. However, its efficacy in the treatment of CSCC and the underlying antitumor mechanism has not been fully elucidated yet. In our study, DHM increased autophagic flux in the A431 cells, as evidenced by the upregulation of LC3-II and downregulation of P62/SQSTM1. Moreover, the pharmacological or genetic blocking autophagy decreased DHM-induced cell death, indicating DHM triggered autophagic cell death in A431 cells. Specifically, DHM induced TFEB<sup>(Ser142)</sup>
de-phosphorylation, activated TFEB nuclear translocation and increased of TFEB reporter activity, which contributed to the expression of autophagy-related genes and subsequent initiated autophagic cell death in A431 cells. Importantly, DHM decreased lncRNA MALAT1 expression and MALAT1 overexpression abrogated the effects of DHM on TFEB-dependent autophagy both in vitro and in vivo. Taken together, DHM induces CSCC cell death via inducing excessive autophagy, which is mediated through the <italic>MALAT1</italic>
-TFEB pathway. Therefore, DHM may be beneficial for the development of chemotherapy for CSCC.</p>
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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">J Cancer</journal-id>
<journal-id journal-id-type="iso-abbrev">J Cancer</journal-id>
<journal-id journal-id-type="publisher-id">jca</journal-id>
<journal-title-group><journal-title>Journal of Cancer</journal-title>
</journal-title-group>
<issn pub-type="epub">1837-9664</issn>
<publisher><publisher-name>Ivyspring International Publisher</publisher-name>
<publisher-loc>Sydney</publisher-loc>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">31413743</article-id>
<article-id pub-id-type="pmc">6691703</article-id>
<article-id pub-id-type="doi">10.7150/jca.32807</article-id>
<article-id pub-id-type="publisher-id">jcav10p4245</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Research Paper</subject>
</subj-group>
</article-categories>
<title-group><article-title>Dihydromyricetin induced lncRNA MALAT1<italic>-</italic>
TFEB-dependent autophagic cell death in cutaneous squamous cell carcinoma</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Tan</surname>
<given-names>Miduo</given-names>
</name>
<xref ref-type="aff" rid="A1">1</xref>
<xref ref-type="author-notes" rid="FNA_star">*</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Jiang</surname>
<given-names>Bin</given-names>
</name>
<xref ref-type="aff" rid="A2">2</xref>
<xref ref-type="author-notes" rid="FNA_star">*</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Wang</surname>
<given-names>Haihua</given-names>
</name>
<xref ref-type="aff" rid="A3">3</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Ouyang</surname>
<given-names>Wei</given-names>
</name>
<xref ref-type="aff" rid="A4">4</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Chen</surname>
<given-names>Xiang</given-names>
</name>
<xref ref-type="aff" rid="A5">5</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Wang</surname>
<given-names>Taoli</given-names>
</name>
<xref ref-type="aff" rid="A6">6</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Dong</surname>
<given-names>Dan</given-names>
</name>
<xref ref-type="aff" rid="A7">7</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Yi</surname>
<given-names>Shun</given-names>
</name>
<xref ref-type="aff" rid="A8">8</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Yi</surname>
<given-names>Jiansheng</given-names>
</name>
<xref ref-type="aff" rid="A1">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Huang</surname>
<given-names>Yan</given-names>
</name>
<xref ref-type="aff" rid="A1">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Tang</surname>
<given-names>Manling</given-names>
</name>
<xref ref-type="aff" rid="A5">5</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Xiao</surname>
<given-names>Yan</given-names>
</name>
<xref ref-type="aff" rid="A9">9</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Jiang</surname>
<given-names>Zuiming</given-names>
</name>
<xref ref-type="aff" rid="A5">5</xref>
<xref ref-type="corresp" rid="FNA_envelop">✉</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Zhou</surname>
<given-names>Wei</given-names>
</name>
<xref ref-type="aff" rid="A1">1</xref>
<xref ref-type="corresp" rid="FNA_envelop">✉</xref>
</contrib>
</contrib-group>
<aff id="A1"><label>1</label>
Surgery Department of Galactophore, The Affiliated Zhuzhou Hospital of Xiangya Medical College CSU, Zhuzhou 412000, China.</aff>
<aff id="A2"><label>2</label>
Department of Plastic Surgery, The Second Hospital University of South China, Hengyang, 421001, China.</aff>
<aff id="A3"><label>3</label>
Department of Burns and Plastic Surgery, The Affiliated Zhuzhou Hospital of Xiangya Medical College CSU, Zhuzhou 412000, China.</aff>
<aff id="A4"><label>4</label>
Department of Oncology, The Affiliated Zhuzhou Hospital of Xiangya Medical College CSU, Zhuzhou 412000, China.</aff>
<aff id="A5"><label>5</label>
Clinical Laboratory Center, The Affiliated Zhuzhou Hospital of Xiangya Medical College CSU, Zhuzhou 412000, China.</aff>
<aff id="A6"><label>6</label>
Department of Pathology, The Affiliated Zhuzhou Hospital of Xiangya Medical College CSU, Zhuzhou 412000, China.</aff>
<aff id="A7"><label>7</label>
Department of Dermatology, The Second Hospital University of South China, Hengyang, 421001, China</aff>
<aff id="A8"><label>8</label>
Department of General surgery, The Affiliated Zhuzhou Hospital of Xiangya Medical College CSU, Zhuzhou 412000, China</aff>
<aff id="A9"><label>9</label>
Department of Otolaryngology, The Affiliated Zhuzhou Hospital of Xiangya Medical College CSU, Zhuzhou 412000, China</aff>
<author-notes><corresp id="FNA_envelop">✉ Corresponding authors: Wei Zhou and Zuiming Jiang. E-mail: <email>zhouweisci@sina.com</email>
(WZ) or <email>1475069651@qq.com</email>
(ZMJ)</corresp>
<fn fn-type="equal" id="FNA_star"><p><sup>*</sup>
Authors contributed equally to this work.</p>
</fn>
<fn fn-type="COI-statement"><p>Competing Interests: The authors have declared that no competing interest exists.</p>
</fn>
</author-notes>
<pub-date pub-type="collection"><year>2019</year>
</pub-date>
<pub-date pub-type="epub"><day>10</day>
<month>7</month>
<year>2019</year>
</pub-date>
<volume>10</volume>
<issue>18</issue>
<fpage>4245</fpage>
<lpage>4255</lpage>
<history><date date-type="received"><day>4</day>
<month>1</month>
<year>2019</year>
</date>
<date date-type="accepted"><day>26</day>
<month>5</month>
<year>2019</year>
</date>
</history>
<permissions><copyright-statement>© The author(s)</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 Creative Commons Attribution License (<ext-link ext-link-type="uri" xlink:href="https://creativecommons.org/licenses/by/4.0/">https://creativecommons.org/licenses/by/4.0/</ext-link>
). See <ext-link ext-link-type="uri" xlink:href="http://ivyspring.com/terms">http://ivyspring.com/terms</ext-link>
for full terms and conditions.</license-p>
</license>
</permissions>
<abstract><p>Cutaneous squamous cell carcinoma (CSCC) is the second most common skin cancer. Dihydromyricetin (DHM), a Rattan tea extract, has been shown to have antitumor activity with no obvious toxicity to normal cells in vitro and in vivo. However, its efficacy in the treatment of CSCC and the underlying antitumor mechanism has not been fully elucidated yet. In our study, DHM increased autophagic flux in the A431 cells, as evidenced by the upregulation of LC3-II and downregulation of P62/SQSTM1. Moreover, the pharmacological or genetic blocking autophagy decreased DHM-induced cell death, indicating DHM triggered autophagic cell death in A431 cells. Specifically, DHM induced TFEB<sup>(Ser142)</sup>
de-phosphorylation, activated TFEB nuclear translocation and increased of TFEB reporter activity, which contributed to the expression of autophagy-related genes and subsequent initiated autophagic cell death in A431 cells. Importantly, DHM decreased lncRNA MALAT1 expression and MALAT1 overexpression abrogated the effects of DHM on TFEB-dependent autophagy both in vitro and in vivo. Taken together, DHM induces CSCC cell death via inducing excessive autophagy, which is mediated through the <italic>MALAT1</italic>
-TFEB pathway. Therefore, DHM may be beneficial for the development of chemotherapy for CSCC.</p>
</abstract>
<kwd-group><kwd>Dihydromyricetin</kwd>
<kwd>autophagy</kwd>
<kwd>TFEB</kwd>
<kwd>MALAT1</kwd>
<kwd>Cutaneous squamous cell carcinoma</kwd>
</kwd-group>
</article-meta>
</front>
<floats-group><fig id="F1" position="float"><label>Figure 1</label>
<caption><p>DHM induces autophagic cell death in A431 cells. (A) A431 cells were treated with different concentrations of DHM for 24 h, and the expression levels of the autophagy-associated proteins LC3-I/II, and p62/SQSTM1 were then assessed by western blotting. A431 cells were pretreated with 10 µM CQ for 2 h and incubated with 100 µM DHM for another 24 h. (B) The LC3II levels were then assessed by western blotting; A431 cells were preincubated with (C-D) 3-MA (2 mM) for 2 h or <italic>ATG5</italic>
-si for 24 h and then treated with 100 µM DHM for another 24 h, then Trypan blue assay used to assess cell death. **P<0.01 versus the control group, <sup>##</sup>
P< 0.01 versus the DHM (100 µM) group (n=6).</p>
</caption>
<graphic xlink:href="jcav10p4245g001"></graphic>
</fig>
<fig id="F2" position="float"><label>Figure 2</label>
<caption><p>DHM increases TFEB activity in A431 cells. (A) A431 cells were treated with different concentrations of DHM for 24 h, and the mRNA level of TFEB were then analyzed by RT-PCR; (B) Immunofluorescence of A431 cells incubated with anti-TFEB antibody and DAPI after DHM (100 µM) treatment for 24 h; (C) A431 cells were transfected with TFEB-luciferase expression vector and incubated with different concentrations of DHM. The luciferase activity was then measured. (D) The mRNA levels of TFEB-target genes were measured using RT-PCR. (E) phosphorylation of TFEB protein was detected by western blotting; *P<0.05, **P<0.01 versus the control group (n=6).</p>
</caption>
<graphic xlink:href="jcav10p4245g002"></graphic>
</fig>
<fig id="F3" position="float"><label>Figure 3</label>
<caption><p>TFEB mediates DHM-induced autophagy. (A) The mRNA levels of <italic>TFEB</italic>
were determined in <italic>TFEB</italic>
siRNA-transfected A431 cells using RT-PCR. (B-C) A431 cells were treated with siRNA against <italic>TFEB</italic>
or control siRNA and then incubated with 100 µM DHM for another 24 h before measuring the Luciferase activity and TFEB-target genes. (D) Trypan blue assay used to assess cell death. **P <0.01 versus the control group, <sup>##</sup>
P< 0.01 versus the Control-si+ DHM (100 µM) group (n=6).</p>
</caption>
<graphic xlink:href="jcav10p4245g003"></graphic>
</fig>
<fig id="F4" position="float"><label>Figure 4</label>
<caption><p>MALAT1 is an upstream signaling molecule that activates the TFEB-dependent autophagy pathway. (A) A431 cells were treated with different doses of DHM and then examined the <italic>MALAT1</italic>
expression; The effect of <italic>MALAT1</italic>
overexpression on TFEB-depended autophagy was studied. (B) The mRNA level of TFEB was detected by RT-PCR. (C) phosphorylation of TFEB protein was detected by western blotting; (D) The TFEB Luciferase activity was then measured. (E) The levels of nuclear TFEB were analyzed by Immunofluorescence; (F) The mRNA levels of TFEB-target genes were measured using RT-PCR. (G) Trypan blue assay used to assess cell death. * P<0.05, **P<0.01, versus the control group;<sup> #</sup>
P<0.05, <sup>##</sup>
P<0.01 versus the DHM (100 µM) group (n=6).</p>
</caption>
<graphic xlink:href="jcav10p4245g004"></graphic>
</fig>
<fig id="F5" position="float"><label>Figure 5</label>
<caption><p>MALAT1 overexpression abolished anti-tumor effect of DHM <italic>in vivo</italic>
. (A) The mRNA level of MALAT1 was detected by RT-PCR. (B-C) After excision from the mice, the xenografts were photographed, and the tumor volume and weight were measured. * P<0.05, **P<0.01, versus the control group;<sup> #</sup>
P<0.05, <sup>##</sup>
P<0.01 versus the DHM group (n=10).</p>
</caption>
<graphic xlink:href="jcav10p4245g005"></graphic>
</fig>
<fig id="F6" position="float"><label>Figure 6</label>
<caption><p>MALAT1 overexpression abolished DHM-induced TFEB-depended autophagic cell death <italic>in vivo</italic>
. (A) The mRNA level of TFEB was detected by RT-PCR. (B) phosphorylation of TFEB (Ser142) protein was detected by western blotting; (C) The levels of cytoplasmic and nuclear TFEB protein were analyzed by Western blot; (D) The mRNA levels of TFEB-target genes were measured using RT-PCR. **P<0.01, versus the control group;<sup> #</sup>
P<0.05, <sup>##</sup>
P<0.01 versus the DHM group (n=10).</p>
</caption>
<graphic xlink:href="jcav10p4245g006"></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="Tan, Miduo" sort="Tan, Miduo" uniqKey="Tan M" first="Miduo" last="Tan">Miduo Tan</name>
</noRegion>
<name sortKey="Chen, Xiang" sort="Chen, Xiang" uniqKey="Chen X" first="Xiang" last="Chen">Xiang Chen</name>
<name sortKey="Dong, Dan" sort="Dong, Dan" uniqKey="Dong D" first="Dan" last="Dong">Dan Dong</name>
<name sortKey="Huang, Yan" sort="Huang, Yan" uniqKey="Huang Y" first="Yan" last="Huang">Yan Huang</name>
<name sortKey="Jiang, Bin" sort="Jiang, Bin" uniqKey="Jiang B" first="Bin" last="Jiang">Bin Jiang</name>
<name sortKey="Jiang, Zuiming" sort="Jiang, Zuiming" uniqKey="Jiang Z" first="Zuiming" last="Jiang">Zuiming Jiang</name>
<name sortKey="Ouyang, Wei" sort="Ouyang, Wei" uniqKey="Ouyang W" first="Wei" last="Ouyang">Wei Ouyang</name>
<name sortKey="Tang, Manling" sort="Tang, Manling" uniqKey="Tang M" first="Manling" last="Tang">Manling Tang</name>
<name sortKey="Wang, Haihua" sort="Wang, Haihua" uniqKey="Wang H" first="Haihua" last="Wang">Haihua Wang</name>
<name sortKey="Wang, Taoli" sort="Wang, Taoli" uniqKey="Wang T" first="Taoli" last="Wang">Taoli Wang</name>
<name sortKey="Xiao, Yan" sort="Xiao, Yan" uniqKey="Xiao Y" first="Yan" last="Xiao">Yan Xiao</name>
<name sortKey="Yi, Jiansheng" sort="Yi, Jiansheng" uniqKey="Yi J" first="Jiansheng" last="Yi">Jiansheng Yi</name>
<name sortKey="Yi, Shun" sort="Yi, Shun" uniqKey="Yi S" first="Shun" last="Yi">Shun Yi</name>
<name sortKey="Zhou, Wei" sort="Zhou, Wei" uniqKey="Zhou W" first="Wei" last="Zhou">Wei Zhou</name>
</country>
</tree>
</affiliations>
</record>
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