Regulating autophagy facilitated therapeutic efficacy of the sonic Hedgehog pathway inhibition on lung adenocarcinoma through GLI2 suppression and ROS production
Identifieur interne : 000476 ( Main/Curation ); précédent : 000475; suivant : 000477Regulating autophagy facilitated therapeutic efficacy of the sonic Hedgehog pathway inhibition on lung adenocarcinoma through GLI2 suppression and ROS production
Auteurs : Jiajun Fan [République populaire de Chine] ; Xuyao Zhang [République populaire de Chine] ; Shaofei Wang [République populaire de Chine] ; Wei Chen [République populaire de Chine] ; Yubin Li [République populaire de Chine] ; Xian Zeng [République populaire de Chine] ; Yichen Wang [République populaire de Chine] ; Jingyun Luan [République populaire de Chine] ; Li Li [République populaire de Chine] ; Ziyu Wang [République populaire de Chine] ; Xilin Sun [République populaire de Chine] ; Baozhong Shen [République populaire de Chine] ; Dianwen Ju [République populaire de Chine]Source :
- Cell Death & Disease [ 2041-4889 ] ; 2019.
Abstract
Lung adenocarcinoma (LUAD), which comprises over 50% of all cases of non-small-cell lung cancer, has a poor prognosis and requires novel therapeutic approaches. The sonic Hedgehog (Shh) pathway, which plays a crucial role in differentiation, proliferation, and survival of cancer cells, is likely to be activated in LUADs, suggesting the Shh pathway as a potential therapeutic target for LUAD treatment. In this study, we reported that vismodegib, an inhibitor of the Shh pathway, only elicited minor antitumor efficacy in A549 and NCI-H1975 LUAD cells as well as in the xenograft tumors, with overexpressed GLI2 and increased autophagic activity. The aberrant autophagy in LUAD cells was further confirmed by the three main stages of autophagic flux, including the formation of autophagosomes, the fusion of autophagosomes with lysosomes, and degradation of autophagosomes in lysosomes. Furthermore, inhibition of autophagy by siRNA against ATG5 or ATG7 rescued the sensitivity of A549 and NCI-H1975 LUAD cells to vismodegib in vitro. Meanwhile, administration of the pharmaceutical inhibitor of autophagy, chloroquine, contributed to the enhanced anti-LUAD efficacy of vismodegib in vivo, probably through overproduction of ROS, acceleration of apoptosis, and suppression of GLI2 in LUAD tissues. In summary, our research revealed that downregulating autophagy facilitated the anti-LUAD efficacy of the Shh pathway suppression, thus highlighting a potential approach for LUAD therapy via simultaneously targeting the Shh signaling and autophagy pathway.
Url:
DOI: 10.1038/s41419-019-1840-6
PubMed: 31427566
PubMed Central: 6700102
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PMC:6700102Le document en format XML
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<institution>Department of Microbiological and Biochemical Pharmacy and The Key Laboratory of Smart Drug Delivery, Ministry of Education, School of Pharmacy,</institution>
<institution>Fudan University,</institution>
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Shanghai, 201203 China</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>Shanghai</wicri:regionArea>
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<author><name sortKey="Chen, Wei" sort="Chen, Wei" uniqKey="Chen W" first="Wei" last="Chen">Wei Chen</name>
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<institution>Minhang Hospital,</institution>
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170 Xinsong Road, Shanghai, 201199 China</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
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<wicri:noRegion>Shanghai</wicri:noRegion>
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<institution>Department of Microbiological and Biochemical Pharmacy and The Key Laboratory of Smart Drug Delivery, Ministry of Education, School of Pharmacy,</institution>
<institution>Fudan University,</institution>
</institution-wrap>
Shanghai, 201203 China</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>Shanghai</wicri:regionArea>
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<author><name sortKey="Li, Yubin" sort="Li, Yubin" uniqKey="Li Y" first="Yubin" last="Li">Yubin Li</name>
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<institution>Fudan University,</institution>
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170 Xinsong Road, Shanghai, 201199 China</nlm:aff>
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<wicri:noRegion>Shanghai</wicri:noRegion>
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</institution-wrap>
Shanghai, 201203 China</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>Shanghai</wicri:regionArea>
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</author>
<author><name sortKey="Zeng, Xian" sort="Zeng, Xian" uniqKey="Zeng X" first="Xian" last="Zeng">Xian Zeng</name>
<affiliation wicri:level="1"><nlm:aff id="Aff1"><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>Minhang Hospital,</institution>
<institution>Fudan University,</institution>
</institution-wrap>
170 Xinsong Road, Shanghai, 201199 China</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>170 Xinsong Road, Shanghai</wicri:regionArea>
<wicri:noRegion>Shanghai</wicri:noRegion>
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<institution-id institution-id-type="GRID">grid.8547.e</institution-id>
<institution>Department of Microbiological and Biochemical Pharmacy and The Key Laboratory of Smart Drug Delivery, Ministry of Education, School of Pharmacy,</institution>
<institution>Fudan University,</institution>
</institution-wrap>
Shanghai, 201203 China</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>Shanghai</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Wang, Yichen" sort="Wang, Yichen" uniqKey="Wang Y" first="Yichen" last="Wang">Yichen Wang</name>
<affiliation wicri:level="1"><nlm:aff id="Aff1"><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>Minhang Hospital,</institution>
<institution>Fudan University,</institution>
</institution-wrap>
170 Xinsong Road, Shanghai, 201199 China</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>170 Xinsong Road, Shanghai</wicri:regionArea>
<wicri:noRegion>Shanghai</wicri:noRegion>
</affiliation>
<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 Microbiological and Biochemical Pharmacy and The Key Laboratory of Smart Drug Delivery, Ministry of Education, School of Pharmacy,</institution>
<institution>Fudan University,</institution>
</institution-wrap>
Shanghai, 201203 China</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>Shanghai</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Luan, Jingyun" sort="Luan, Jingyun" uniqKey="Luan J" first="Jingyun" last="Luan">Jingyun Luan</name>
<affiliation wicri:level="1"><nlm:aff id="Aff1"><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>Minhang Hospital,</institution>
<institution>Fudan University,</institution>
</institution-wrap>
170 Xinsong Road, Shanghai, 201199 China</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>170 Xinsong Road, Shanghai</wicri:regionArea>
<wicri:noRegion>Shanghai</wicri:noRegion>
</affiliation>
<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 Microbiological and Biochemical Pharmacy and The Key Laboratory of Smart Drug Delivery, Ministry of Education, School of Pharmacy,</institution>
<institution>Fudan University,</institution>
</institution-wrap>
Shanghai, 201203 China</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>Shanghai</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Li, Li" sort="Li, Li" uniqKey="Li L" first="Li" last="Li">Li Li</name>
<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 Microbiological and Biochemical Pharmacy and The Key Laboratory of Smart Drug Delivery, Ministry of Education, School of Pharmacy,</institution>
<institution>Fudan University,</institution>
</institution-wrap>
Shanghai, 201203 China</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>Shanghai</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Wang, Ziyu" sort="Wang, Ziyu" uniqKey="Wang Z" first="Ziyu" last="Wang">Ziyu Wang</name>
<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 Microbiological and Biochemical Pharmacy and The Key Laboratory of Smart Drug Delivery, Ministry of Education, School of Pharmacy,</institution>
<institution>Fudan University,</institution>
</institution-wrap>
Shanghai, 201203 China</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>Shanghai</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Sun, Xilin" sort="Sun, Xilin" uniqKey="Sun X" first="Xilin" last="Sun">Xilin Sun</name>
<affiliation wicri:level="1"><nlm:aff id="Aff3"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2204 9268</institution-id>
<institution-id institution-id-type="GRID">grid.410736.7</institution-id>
<institution>The Fourth Hospital of Harbin Medical University,</institution>
</institution-wrap>
Harbin, 150028 P. R. China</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>Harbin</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Shen, Baozhong" sort="Shen, Baozhong" uniqKey="Shen B" first="Baozhong" last="Shen">Baozhong Shen</name>
<affiliation wicri:level="1"><nlm:aff id="Aff3"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2204 9268</institution-id>
<institution-id institution-id-type="GRID">grid.410736.7</institution-id>
<institution>The Fourth Hospital of Harbin Medical University,</institution>
</institution-wrap>
Harbin, 150028 P. R. China</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>Harbin</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Ju, Dianwen" sort="Ju, Dianwen" uniqKey="Ju D" first="Dianwen" last="Ju">Dianwen Ju</name>
<affiliation wicri:level="1"><nlm:aff id="Aff1"><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>Minhang Hospital,</institution>
<institution>Fudan University,</institution>
</institution-wrap>
170 Xinsong Road, Shanghai, 201199 China</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>170 Xinsong Road, Shanghai</wicri:regionArea>
<wicri:noRegion>Shanghai</wicri:noRegion>
</affiliation>
<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 Microbiological and Biochemical Pharmacy and The Key Laboratory of Smart Drug Delivery, Ministry of Education, School of Pharmacy,</institution>
<institution>Fudan University,</institution>
</institution-wrap>
Shanghai, 201203 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="2019">2019</date>
</imprint>
</series>
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<front><div type="abstract" xml:lang="en"><p id="Par1">Lung adenocarcinoma (LUAD), which comprises over 50% of all cases of non-small-cell lung cancer, has a poor prognosis and requires novel therapeutic approaches. The sonic Hedgehog (Shh) pathway, which plays a crucial role in differentiation, proliferation, and survival of cancer cells, is likely to be activated in LUADs, suggesting the Shh pathway as a potential therapeutic target for LUAD treatment. In this study, we reported that vismodegib, an inhibitor of the Shh pathway, only elicited minor antitumor efficacy in A549 and NCI-H1975 LUAD cells as well as in the xenograft tumors, with overexpressed GLI2 and increased autophagic activity. The aberrant autophagy in LUAD cells was further confirmed by the three main stages of autophagic flux, including the formation of autophagosomes, the fusion of autophagosomes with lysosomes, and degradation of autophagosomes in lysosomes. Furthermore, inhibition of autophagy by siRNA against ATG5 or ATG7 rescued the sensitivity of A549 and NCI-H1975 LUAD cells to vismodegib in vitro. Meanwhile, administration of the pharmaceutical inhibitor of autophagy, chloroquine, contributed to the enhanced anti-LUAD efficacy of vismodegib in vivo, probably through overproduction of ROS, acceleration of apoptosis, and suppression of GLI2 in LUAD tissues. In summary, our research revealed that downregulating autophagy facilitated the anti-LUAD efficacy of the Shh pathway suppression, thus highlighting a potential approach for LUAD therapy via simultaneously targeting the Shh signaling and autophagy pathway.</p>
</div>
</front>
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