Artemisinin compounds sensitize cancer cells to ferroptosis by regulating iron homeostasis
The antimalarial drug artemisinin and its derivatives have been explored as potential anticancer agents, but their underlying mechanisms are controversial. In this study, we found that artemisinin compounds can sensitize cancer cells to ferroptosis, a new form of programmed cell death driven by iron...
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Veröffentlicht in: | Cell death and differentiation 2020-01, Vol.27 (1), p.242-254 |
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description | The antimalarial drug artemisinin and its derivatives have been explored as potential anticancer agents, but their underlying mechanisms are controversial. In this study, we found that artemisinin compounds can sensitize cancer cells to ferroptosis, a new form of programmed cell death driven by iron-dependent lipid peroxidation. Mechanistically, dihydroartemisinin (DAT) can induce lysosomal degradation of ferritin in an autophagy-independent manner, increasing the cellular free iron level and causing cells to become more sensitive to ferroptosis. Further, by associating with cellular free iron and thus stimulating the binding of iron-regulatory proteins (IRPs) with mRNA molecules containing iron-responsive element (IRE) sequences, DAT impinges on IRP/IRE-controlled iron homeostasis to further increase cellular free iron. Importantly, in both in vitro and a mouse xenograft model in which ferroptosis was triggered in cancer cells by the inducible knockout of GPX4, we found that DAT can augment GPX4 inhibition-induced ferroptosis in a cohort of cancer cells that are otherwise highly resistant to ferroptosis. Collectively, artemisinin compounds can sensitize cells to ferroptosis by regulating cellular iron homeostasis. Our findings can be exploited clinically to enhance the effect of future ferroptosis-inducing cancer therapies. |
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In this study, we found that artemisinin compounds can sensitize cancer cells to ferroptosis, a new form of programmed cell death driven by iron-dependent lipid peroxidation. Mechanistically, dihydroartemisinin (DAT) can induce lysosomal degradation of ferritin in an autophagy-independent manner, increasing the cellular free iron level and causing cells to become more sensitive to ferroptosis. Further, by associating with cellular free iron and thus stimulating the binding of iron-regulatory proteins (IRPs) with mRNA molecules containing iron-responsive element (IRE) sequences, DAT impinges on IRP/IRE-controlled iron homeostasis to further increase cellular free iron. Importantly, in both in vitro and a mouse xenograft model in which ferroptosis was triggered in cancer cells by the inducible knockout of GPX4, we found that DAT can augment GPX4 inhibition-induced ferroptosis in a cohort of cancer cells that are otherwise highly resistant to ferroptosis. Collectively, artemisinin compounds can sensitize cells to ferroptosis by regulating cellular iron homeostasis. Our findings can be exploited clinically to enhance the effect of future ferroptosis-inducing cancer therapies.</description><identifier>ISSN: 1350-9047</identifier><identifier>EISSN: 1476-5403</identifier><identifier>DOI: 10.1038/s41418-019-0352-3</identifier><identifier>PMID: 31114026</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>13/1 ; 13/106 ; 13/31 ; 13/51 ; 14/19 ; 631/67 ; 631/80 ; 631/80/39 ; 64/60 ; Animals ; Antineoplastic Agents - pharmacology ; Antineoplastic Agents - therapeutic use ; Apoptosis ; Artemisinin ; Artemisinins - chemistry ; Artemisinins - pharmacology ; Artemisinins - therapeutic use ; Autophagy - drug effects ; Biochemistry ; Biomedical and Life Sciences ; Cancer ; Cell Biology ; Cell Cycle Analysis ; Cell Line, Tumor ; Female ; Ferroptosis ; Ferroptosis - drug effects ; Homeostasis ; Humans ; Iron - metabolism ; Iron-Regulatory Proteins - metabolism ; Life Sciences ; Lysosomes - metabolism ; Mice, Nude ; Neoplasms - metabolism ; Response Elements ; Stem Cells ; Xenografts</subject><ispartof>Cell death and differentiation, 2020-01, Vol.27 (1), p.242-254</ispartof><rights>ADMC Associazione Differenziamento e Morte Cellulare 2019</rights><rights>ADMC Associazione Differenziamento e Morte Cellulare 2019.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c536t-6effd4103bed9b7019afe3b000159d9afc4da415d666129237d5e0475e0f92ee3</citedby><cites>FETCH-LOGICAL-c536t-6effd4103bed9b7019afe3b000159d9afc4da415d666129237d5e0475e0f92ee3</cites><orcidid>0000-0001-6206-1958</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7205875/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7205875/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,727,780,784,885,27923,27924,41487,42556,51318,53790,53792</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31114026$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Chen, Guo-Qing</creatorcontrib><creatorcontrib>Benthani, Fahad A.</creatorcontrib><creatorcontrib>Wu, Jiao</creatorcontrib><creatorcontrib>Liang, Deguang</creatorcontrib><creatorcontrib>Bian, Zhao-Xiang</creatorcontrib><creatorcontrib>Jiang, Xuejun</creatorcontrib><title>Artemisinin compounds sensitize cancer cells to ferroptosis by regulating iron homeostasis</title><title>Cell death and differentiation</title><addtitle>Cell Death Differ</addtitle><addtitle>Cell Death Differ</addtitle><description>The antimalarial drug artemisinin and its derivatives have been explored as potential anticancer agents, but their underlying mechanisms are controversial. In this study, we found that artemisinin compounds can sensitize cancer cells to ferroptosis, a new form of programmed cell death driven by iron-dependent lipid peroxidation. Mechanistically, dihydroartemisinin (DAT) can induce lysosomal degradation of ferritin in an autophagy-independent manner, increasing the cellular free iron level and causing cells to become more sensitive to ferroptosis. Further, by associating with cellular free iron and thus stimulating the binding of iron-regulatory proteins (IRPs) with mRNA molecules containing iron-responsive element (IRE) sequences, DAT impinges on IRP/IRE-controlled iron homeostasis to further increase cellular free iron. Importantly, in both in vitro and a mouse xenograft model in which ferroptosis was triggered in cancer cells by the inducible knockout of GPX4, we found that DAT can augment GPX4 inhibition-induced ferroptosis in a cohort of cancer cells that are otherwise highly resistant to ferroptosis. Collectively, artemisinin compounds can sensitize cells to ferroptosis by regulating cellular iron homeostasis. Our findings can be exploited clinically to enhance the effect of future ferroptosis-inducing cancer therapies.</description><subject>13/1</subject><subject>13/106</subject><subject>13/31</subject><subject>13/51</subject><subject>14/19</subject><subject>631/67</subject><subject>631/80</subject><subject>631/80/39</subject><subject>64/60</subject><subject>Animals</subject><subject>Antineoplastic Agents - pharmacology</subject><subject>Antineoplastic Agents - therapeutic use</subject><subject>Apoptosis</subject><subject>Artemisinin</subject><subject>Artemisinins - chemistry</subject><subject>Artemisinins - pharmacology</subject><subject>Artemisinins - therapeutic use</subject><subject>Autophagy - drug effects</subject><subject>Biochemistry</subject><subject>Biomedical and Life Sciences</subject><subject>Cancer</subject><subject>Cell Biology</subject><subject>Cell Cycle Analysis</subject><subject>Cell Line, Tumor</subject><subject>Female</subject><subject>Ferroptosis</subject><subject>Ferroptosis - drug effects</subject><subject>Homeostasis</subject><subject>Humans</subject><subject>Iron - metabolism</subject><subject>Iron-Regulatory Proteins - metabolism</subject><subject>Life Sciences</subject><subject>Lysosomes - metabolism</subject><subject>Mice, Nude</subject><subject>Neoplasms - metabolism</subject><subject>Response Elements</subject><subject>Stem Cells</subject><subject>Xenografts</subject><issn>1350-9047</issn><issn>1476-5403</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><recordid>eNp1kUtr3TAQhUVpaR7tD-imCLrJxqnesjeBENKmEOim3XQjZHt8o2BLN5IcSH995nLT9AHd6MEcnZlPh5B3nJ1yJtuPRXHF24bxrmFSi0a-IIdcWdNoxeRLPEvNmo4pe0COSrlljBnbmdfkQHLOFRPmkPw4zxWWUEIMkQ5p2aY1joUWiCXU8BPo4OMAmQ4wz4XWRCfIOW1rKqHQ_oFm2KyzryFuaMgp0pu0QCrVY_kNeTX5ucDbp_2YfP90-e3iqrn--vnLxfl1M2hpamNgmkaFPD2MXW8Rxk8gexyW627Ey6BGr7gejTFcdELaUQMy4TJ1AkAek7O973btFxgHiDX72W1zWHx-cMkH93clhhu3SffOCqZbq9Hg5Mkgp7sVSnX4ITtgHyGtxQkhBbMtdkfph3-kt2nNEfEciqyUreIcVXyvGnIqJcP0PAxnbpec2yfnENbtknMS37z_k-L5xa-oUCD2goKluIH8u_X_XR8BmqKmCQ</recordid><startdate>20200101</startdate><enddate>20200101</enddate><creator>Chen, Guo-Qing</creator><creator>Benthani, Fahad A.</creator><creator>Wu, Jiao</creator><creator>Liang, Deguang</creator><creator>Bian, Zhao-Xiang</creator><creator>Jiang, Xuejun</creator><general>Nature Publishing Group UK</general><general>Nature Publishing Group</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7QP</scope><scope>7QR</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>8AO</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>P64</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-6206-1958</orcidid></search><sort><creationdate>20200101</creationdate><title>Artemisinin compounds sensitize cancer cells to ferroptosis by regulating iron homeostasis</title><author>Chen, Guo-Qing ; Benthani, Fahad A. ; Wu, Jiao ; Liang, Deguang ; Bian, Zhao-Xiang ; Jiang, Xuejun</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c536t-6effd4103bed9b7019afe3b000159d9afc4da415d666129237d5e0475e0f92ee3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>13/1</topic><topic>13/106</topic><topic>13/31</topic><topic>13/51</topic><topic>14/19</topic><topic>631/67</topic><topic>631/80</topic><topic>631/80/39</topic><topic>64/60</topic><topic>Animals</topic><topic>Antineoplastic Agents - pharmacology</topic><topic>Antineoplastic Agents - therapeutic use</topic><topic>Apoptosis</topic><topic>Artemisinin</topic><topic>Artemisinins - chemistry</topic><topic>Artemisinins - pharmacology</topic><topic>Artemisinins - therapeutic use</topic><topic>Autophagy - drug effects</topic><topic>Biochemistry</topic><topic>Biomedical and Life Sciences</topic><topic>Cancer</topic><topic>Cell Biology</topic><topic>Cell Cycle Analysis</topic><topic>Cell Line, Tumor</topic><topic>Female</topic><topic>Ferroptosis</topic><topic>Ferroptosis - drug effects</topic><topic>Homeostasis</topic><topic>Humans</topic><topic>Iron - metabolism</topic><topic>Iron-Regulatory Proteins - metabolism</topic><topic>Life Sciences</topic><topic>Lysosomes - metabolism</topic><topic>Mice, Nude</topic><topic>Neoplasms - metabolism</topic><topic>Response Elements</topic><topic>Stem Cells</topic><topic>Xenografts</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Chen, Guo-Qing</creatorcontrib><creatorcontrib>Benthani, Fahad A.</creatorcontrib><creatorcontrib>Wu, Jiao</creatorcontrib><creatorcontrib>Liang, Deguang</creatorcontrib><creatorcontrib>Bian, Zhao-Xiang</creatorcontrib><creatorcontrib>Jiang, Xuejun</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Immunology Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Biology Database (Alumni Edition)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Cell death and differentiation</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Chen, Guo-Qing</au><au>Benthani, Fahad A.</au><au>Wu, Jiao</au><au>Liang, Deguang</au><au>Bian, Zhao-Xiang</au><au>Jiang, Xuejun</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Artemisinin compounds sensitize cancer cells to ferroptosis by regulating iron homeostasis</atitle><jtitle>Cell death and differentiation</jtitle><stitle>Cell Death Differ</stitle><addtitle>Cell Death Differ</addtitle><date>2020-01-01</date><risdate>2020</risdate><volume>27</volume><issue>1</issue><spage>242</spage><epage>254</epage><pages>242-254</pages><issn>1350-9047</issn><eissn>1476-5403</eissn><abstract>The antimalarial drug artemisinin and its derivatives have been explored as potential anticancer agents, but their underlying mechanisms are controversial. In this study, we found that artemisinin compounds can sensitize cancer cells to ferroptosis, a new form of programmed cell death driven by iron-dependent lipid peroxidation. Mechanistically, dihydroartemisinin (DAT) can induce lysosomal degradation of ferritin in an autophagy-independent manner, increasing the cellular free iron level and causing cells to become more sensitive to ferroptosis. Further, by associating with cellular free iron and thus stimulating the binding of iron-regulatory proteins (IRPs) with mRNA molecules containing iron-responsive element (IRE) sequences, DAT impinges on IRP/IRE-controlled iron homeostasis to further increase cellular free iron. Importantly, in both in vitro and a mouse xenograft model in which ferroptosis was triggered in cancer cells by the inducible knockout of GPX4, we found that DAT can augment GPX4 inhibition-induced ferroptosis in a cohort of cancer cells that are otherwise highly resistant to ferroptosis. Collectively, artemisinin compounds can sensitize cells to ferroptosis by regulating cellular iron homeostasis. Our findings can be exploited clinically to enhance the effect of future ferroptosis-inducing cancer therapies.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>31114026</pmid><doi>10.1038/s41418-019-0352-3</doi><tpages>13</tpages><orcidid>https://orcid.org/0000-0001-6206-1958</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | 13/1 13/106 13/31 13/51 14/19 631/67 631/80 631/80/39 64/60 Animals Antineoplastic Agents - pharmacology Antineoplastic Agents - therapeutic use Apoptosis Artemisinin Artemisinins - chemistry Artemisinins - pharmacology Artemisinins - therapeutic use Autophagy - drug effects Biochemistry Biomedical and Life Sciences Cancer Cell Biology Cell Cycle Analysis Cell Line, Tumor Female Ferroptosis Ferroptosis - drug effects Homeostasis Humans Iron - metabolism Iron-Regulatory Proteins - metabolism Life Sciences Lysosomes - metabolism Mice, Nude Neoplasms - metabolism Response Elements Stem Cells Xenografts |
title | Artemisinin compounds sensitize cancer cells to ferroptosis by regulating iron homeostasis |
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