Regulating autophagy facilitated therapeutic efficacy of the sonic Hedgehog pathway inhibition on lung adenocarcinoma through GLI2 suppression and ROS production.
Identifieur interne : 000040 ( PubMed/Curation ); précédent : 000039; suivant : 000041Regulating 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.
DOI: 10.1038/s41419-019-1840-6
PubMed: 31427566
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Hospital, Fudan University, 170 Xinsong Road, Shanghai, 201199, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Minhang Hospital, Fudan University, 170 Xinsong Road, Shanghai, 201199</wicri:regionArea></affiliation></author><author><name sortKey="Wang, Shaofei" sort="Wang, Shaofei" uniqKey="Wang S" first="Shaofei" last="Wang">Shaofei Wang</name><affiliation wicri:level="1"><nlm:affiliation>Minhang Hospital, Fudan University, 170 Xinsong Road, Shanghai, 201199, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Minhang Hospital, Fudan University, 170 Xinsong Road, Shanghai, 201199</wicri:regionArea></affiliation></author><author><name sortKey="Chen, Wei" sort="Chen, Wei" uniqKey="Chen W" first="Wei" last="Chen">Wei Chen</name><affiliation wicri:level="1"><nlm:affiliation>Minhang Hospital, Fudan University, 170 Xinsong Road, Shanghai, 201199, China.</nlm:affiliation><country 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Xinsong Road, Shanghai, 201199</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:affiliation>Minhang Hospital, Fudan University, 170 Xinsong Road, Shanghai, 201199, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Minhang Hospital, Fudan University, 170 Xinsong Road, Shanghai, 201199</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:affiliation>Minhang Hospital, Fudan University, 170 Xinsong Road, Shanghai, 201199, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Minhang Hospital, Fudan University, 170 Xinsong Road, Shanghai, 201199</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:affiliation>Department of Microbiological and Biochemical Pharmacy and The Key Laboratory of Smart Drug Delivery, Ministry of Education, School of Pharmacy, Fudan University, Shanghai, 201203, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Microbiological and Biochemical Pharmacy and The Key Laboratory of Smart Drug Delivery, Ministry of Education, School of Pharmacy, Fudan University, Shanghai, 201203</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:affiliation>Department of Microbiological and Biochemical Pharmacy and The Key Laboratory of Smart Drug Delivery, Ministry of Education, School of Pharmacy, Fudan University, Shanghai, 201203, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Microbiological and Biochemical Pharmacy and The Key Laboratory of Smart Drug Delivery, Ministry of Education, School of Pharmacy, Fudan University, Shanghai, 201203</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:affiliation>The Fourth Hospital of Harbin Medical University, Harbin, 150028, P. R. China. sunxl@ems.hrbmu.edu.cn.</nlm:affiliation><country wicri:rule="url">République populaire de Chine</country></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:affiliation>The Fourth Hospital of Harbin Medical University, Harbin, 150028, P. R. China. shenbz@ems.hrbmu.edu.cn.</nlm:affiliation><country wicri:rule="url">République populaire de Chine</country></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:affiliation>Minhang Hospital, Fudan University, 170 Xinsong Road, Shanghai, 201199, China. dianwenju@fudan.edu.cn.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Minhang Hospital, Fudan University, 170 Xinsong Road, Shanghai, 201199</wicri:regionArea></affiliation></author></analytic><series><title level="j">Cell death & disease</title><idno type="eISSN">2041-4889</idno><imprint><date when="2019" type="published">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">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.</div></front></TEI><pubmed><MedlineCitation Status="In-Process" Owner="NLM"><PMID Version="1">31427566</PMID><DateRevised><Year>2020</Year><Month>03</Month><Day>13</Day></DateRevised><Article PubModel="Electronic"><Journal><ISSN IssnType="Electronic">2041-4889</ISSN><JournalIssue CitedMedium="Internet"><Volume>10</Volume><Issue>9</Issue><PubDate><Year>2019</Year><Month>08</Month><Day>19</Day></PubDate></JournalIssue><Title>Cell death & disease</Title><ISOAbbreviation>Cell Death Dis</ISOAbbreviation></Journal><ArticleTitle>Regulating autophagy facilitated therapeutic efficacy of the sonic Hedgehog pathway inhibition on lung adenocarcinoma through GLI2 suppression and ROS production.</ArticleTitle><Pagination><MedlinePgn>626</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1038/s41419-019-1840-6</ELocationID><Abstract><AbstractText>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.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Fan</LastName><ForeName>Jiajun</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Minhang Hospital, Fudan University, 170 Xinsong Road, Shanghai, 201199, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Microbiological and Biochemical Pharmacy and The Key Laboratory of Smart Drug Delivery, Ministry of Education, School of Pharmacy, Fudan University, Shanghai, 201203, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zhang</LastName><ForeName>Xuyao</ForeName><Initials>X</Initials><Identifier Source="ORCID">0000-0003-1654-5550</Identifier><AffiliationInfo><Affiliation>Minhang Hospital, Fudan University, 170 Xinsong Road, Shanghai, 201199, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Microbiological and Biochemical Pharmacy and The Key Laboratory of Smart Drug Delivery, Ministry of Education, School of Pharmacy, Fudan University, Shanghai, 201203, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wang</LastName><ForeName>Shaofei</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>Minhang Hospital, Fudan University, 170 Xinsong Road, Shanghai, 201199, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Microbiological and Biochemical Pharmacy and The Key Laboratory of Smart Drug Delivery, Ministry of Education, School of Pharmacy, Fudan University, Shanghai, 201203, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Chen</LastName><ForeName>Wei</ForeName><Initials>W</Initials><AffiliationInfo><Affiliation>Minhang Hospital, Fudan University, 170 Xinsong Road, Shanghai, 201199, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Microbiological and Biochemical Pharmacy and The Key Laboratory of Smart Drug Delivery, Ministry of Education, School of Pharmacy, Fudan University, Shanghai, 201203, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Li</LastName><ForeName>Yubin</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>Minhang Hospital, Fudan University, 170 Xinsong Road, Shanghai, 201199, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Microbiological and Biochemical Pharmacy and The Key Laboratory of Smart Drug Delivery, Ministry of Education, School of Pharmacy, Fudan University, Shanghai, 201203, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zeng</LastName><ForeName>Xian</ForeName><Initials>X</Initials><AffiliationInfo><Affiliation>Minhang Hospital, Fudan University, 170 Xinsong Road, Shanghai, 201199, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Microbiological and Biochemical Pharmacy and The Key Laboratory of Smart Drug Delivery, Ministry of Education, School of Pharmacy, Fudan University, Shanghai, 201203, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wang</LastName><ForeName>Yichen</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>Minhang Hospital, Fudan University, 170 Xinsong Road, Shanghai, 201199, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Microbiological and Biochemical Pharmacy and The Key Laboratory of Smart Drug Delivery, Ministry of Education, School of Pharmacy, Fudan University, Shanghai, 201203, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Luan</LastName><ForeName>Jingyun</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Minhang Hospital, Fudan University, 170 Xinsong Road, Shanghai, 201199, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Microbiological and Biochemical Pharmacy and The Key Laboratory of Smart Drug Delivery, Ministry of Education, School of Pharmacy, Fudan University, Shanghai, 201203, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Li</LastName><ForeName>Li</ForeName><Initials>L</Initials><AffiliationInfo><Affiliation>Department of Microbiological and Biochemical Pharmacy and The Key Laboratory of Smart Drug Delivery, Ministry of Education, School of Pharmacy, Fudan University, Shanghai, 201203, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wang</LastName><ForeName>Ziyu</ForeName><Initials>Z</Initials><AffiliationInfo><Affiliation>Department of Microbiological and Biochemical Pharmacy and The Key Laboratory of Smart Drug Delivery, Ministry of Education, School of Pharmacy, Fudan University, Shanghai, 201203, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Sun</LastName><ForeName>Xilin</ForeName><Initials>X</Initials><AffiliationInfo><Affiliation>The Fourth Hospital of Harbin Medical University, Harbin, 150028, P. R. China. sunxl@ems.hrbmu.edu.cn.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Shen</LastName><ForeName>Baozhong</ForeName><Initials>B</Initials><AffiliationInfo><Affiliation>The Fourth Hospital of Harbin Medical University, Harbin, 150028, P. R. China. shenbz@ems.hrbmu.edu.cn.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Ju</LastName><ForeName>Dianwen</ForeName><Initials>D</Initials><AffiliationInfo><Affiliation>Minhang Hospital, Fudan University, 170 Xinsong Road, Shanghai, 201199, China. dianwenju@fudan.edu.cn.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Microbiological and Biochemical Pharmacy and The Key Laboratory of Smart Drug Delivery, Ministry of Education, School of Pharmacy, Fudan University, Shanghai, 201203, China. dianwenju@fudan.edu.cn.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2019</Year><Month>08</Month><Day>19</Day></ArticleDate></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>Cell Death Dis</MedlineTA><NlmUniqueID>101524092</NlmUniqueID></MedlineJournalInfo><CitationSubset>IM</CitationSubset></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2018</Year><Month>07</Month><Day>20</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2019</Year><Month>06</Month><Day>26</Day></PubMedPubDate><PubMedPubDate PubStatus="revised"><Year>2019</Year><Month>06</Month><Day>12</Day></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2019</Year><Month>8</Month><Day>21</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2019</Year><Month>8</Month><Day>21</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate 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