Amino Acid Deprivation-Induced Autophagy Requires Upregulation of DIRAS3 through Reduction of E2F1 and E2F4 Transcriptional Repression
Identifieur interne : 000A97 ( Main/Exploration ); précédent : 000A96; suivant : 000A98Amino Acid Deprivation-Induced Autophagy Requires Upregulation of DIRAS3 through Reduction of E2F1 and E2F4 Transcriptional Repression
Auteurs : Margie N. Sutton ; Gilbert Y. Huang ; Jinhua Zhou [République populaire de Chine] ; Weiqun Mao ; Robert Langley ; Zhen Lu ; Robert C. BastSource :
- Cancers [ 2072-6694 ] ; 2019.
Abstract
Failure to cure ovarian cancer relates to the persistence of dormant, drug-resistant cancer cells following surgery and chemotherapy. “Second look” surgery can detect small, poorly vascularized nodules of persistent ovarian cancer in ~50% of patients, where >80% are undergoing autophagy and express DIRAS3. Autophagy is one mechanism by which dormant cancer cells survive in nutrient poor environments. DIRAS3 is a tumor suppressor gene downregulated in >60% of primary ovarian cancers by genetic, epigenetic, transcriptional and post-transcriptional mechanisms, that upon re-expression can induce autophagy and dormancy in a xenograft model of ovarian cancer. We examined the expression of DIRAS3 and autophagy in ovarian cancer cells following nutrient deprivation and the mechanism by which they are upregulated. We have found that DIRAS3 mediates autophagy induced by amino acid starvation, where nutrient sensing by mTOR plays a central role. Withdrawal of amino acids downregulates mTOR, decreases binding of E2F1/4 to the DIRAS3 promoter, upregulates DIRAS3 and induces autophagy. By contrast, acute amino acid deprivation did not affect epigenetic regulation of DIRAS3 or expression of miRNAs that regulate DIRAS3. Under nutrient poor conditions DIRAS3 can be transcriptionally upregulated, inducing autophagy that could sustain dormant ovarian cancer cells.
Url:
DOI: 10.3390/cancers11050603
PubMed: 31052266
PubMed Central: 6562629
Affiliations:
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Amino Acid Deprivation-Induced Autophagy Requires Upregulation of DIRAS3 through Reduction of E2F1 and E2F4 Transcriptional Repression</title><author><name sortKey="Sutton, Margie N" sort="Sutton, Margie N" uniqKey="Sutton M" first="Margie N." last="Sutton">Margie N. Sutton</name><affiliation><nlm:aff id="af1-cancers-11-00603">Department of Experimental Therapeutics, The University of Texas M.D. Anderson Cancer Center, Houston, TX 77030, USA;<email>mnsutton@mdanderson.org</email> (M.N.S.);<email>gilbert.y.huang@gmail.com</email> (G.Y.H.);<email>jsjhzh@126.com</email> (J.Z.);<email>Wmao@mdanderson.org</email> (W.M.)</nlm:aff></affiliation></author><author><name sortKey="Huang, Gilbert Y" sort="Huang, Gilbert Y" uniqKey="Huang G" first="Gilbert Y." last="Huang">Gilbert Y. Huang</name><affiliation><nlm:aff id="af1-cancers-11-00603">Department of Experimental Therapeutics, The University of Texas M.D. Anderson Cancer Center, Houston, TX 77030, USA;<email>mnsutton@mdanderson.org</email> (M.N.S.);<email>gilbert.y.huang@gmail.com</email> (G.Y.H.);<email>jsjhzh@126.com</email> (J.Z.);<email>Wmao@mdanderson.org</email> (W.M.)</nlm:aff></affiliation></author><author><name sortKey="Zhou, Jinhua" sort="Zhou, Jinhua" uniqKey="Zhou J" first="Jinhua" last="Zhou">Jinhua Zhou</name><affiliation><nlm:aff id="af1-cancers-11-00603">Department of Experimental Therapeutics, The University of Texas M.D. Anderson Cancer Center, Houston, TX 77030, USA;<email>mnsutton@mdanderson.org</email> (M.N.S.);<email>gilbert.y.huang@gmail.com</email> (G.Y.H.);<email>jsjhzh@126.com</email> (J.Z.);<email>Wmao@mdanderson.org</email> (W.M.)</nlm:aff></affiliation><affiliation wicri:level="1"><nlm:aff id="af2-cancers-11-00603">Department of Obstetrics and Gynecology, The First Affiliated Hospital of Soochow University, Suzhou 215006, China</nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Obstetrics and Gynecology, The First Affiliated Hospital of Soochow University, Suzhou 215006</wicri:regionArea><wicri:noRegion>Suzhou 215006</wicri:noRegion></affiliation></author><author><name sortKey="Mao, Weiqun" sort="Mao, Weiqun" uniqKey="Mao W" first="Weiqun" last="Mao">Weiqun Mao</name><affiliation><nlm:aff id="af1-cancers-11-00603">Department of Experimental Therapeutics, The University of Texas M.D. Anderson Cancer Center, Houston, TX 77030, USA;<email>mnsutton@mdanderson.org</email> (M.N.S.);<email>gilbert.y.huang@gmail.com</email> (G.Y.H.);<email>jsjhzh@126.com</email> (J.Z.);<email>Wmao@mdanderson.org</email> (W.M.)</nlm:aff></affiliation></author><author><name sortKey="Langley, Robert" sort="Langley, Robert" uniqKey="Langley R" first="Robert" last="Langley">Robert Langley</name><affiliation><nlm:aff id="af3-cancers-11-00603">Office of Translational Research, The University of Texas M.D. Anderson Cancer Center, Houston, TX 77030, USA;<email>rlangley@mdanderson.org</email></nlm:aff></affiliation></author><author><name sortKey="Lu, Zhen" sort="Lu, Zhen" uniqKey="Lu Z" first="Zhen" last="Lu">Zhen Lu</name><affiliation><nlm:aff id="af1-cancers-11-00603">Department of Experimental Therapeutics, The University of Texas M.D. Anderson Cancer Center, Houston, TX 77030, USA;<email>mnsutton@mdanderson.org</email> (M.N.S.);<email>gilbert.y.huang@gmail.com</email> (G.Y.H.);<email>jsjhzh@126.com</email> (J.Z.);<email>Wmao@mdanderson.org</email> (W.M.)</nlm:aff></affiliation></author><author><name sortKey="Bast, Robert C" sort="Bast, Robert C" uniqKey="Bast R" first="Robert C." last="Bast">Robert C. Bast</name><affiliation><nlm:aff id="af1-cancers-11-00603">Department of Experimental Therapeutics, The University of Texas M.D. Anderson Cancer Center, Houston, TX 77030, USA;<email>mnsutton@mdanderson.org</email> (M.N.S.);<email>gilbert.y.huang@gmail.com</email> (G.Y.H.);<email>jsjhzh@126.com</email> (J.Z.);<email>Wmao@mdanderson.org</email> (W.M.)</nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">31052266</idno><idno type="pmc">6562629</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6562629</idno><idno type="RBID">PMC:6562629</idno><idno type="doi">10.3390/cancers11050603</idno><date when="2019">2019</date><idno type="wicri:Area/Pmc/Corpus">000450</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000450</idno><idno type="wicri:Area/Pmc/Curation">000450</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">000450</idno><idno type="wicri:Area/Pmc/Checkpoint">000A23</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Checkpoint">000A23</idno><idno type="wicri:Area/Ncbi/Merge">000587</idno><idno type="wicri:Area/Ncbi/Curation">000587</idno><idno type="wicri:Area/Ncbi/Checkpoint">000587</idno><idno type="wicri:Area/Main/Merge">000A97</idno><idno type="wicri:Area/Main/Curation">000A97</idno><idno type="wicri:Area/Main/Exploration">000A97</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Amino Acid Deprivation-Induced Autophagy Requires Upregulation of DIRAS3 through Reduction of E2F1 and E2F4 Transcriptional Repression</title><author><name sortKey="Sutton, Margie N" sort="Sutton, Margie N" uniqKey="Sutton M" first="Margie N." last="Sutton">Margie N. Sutton</name><affiliation><nlm:aff id="af1-cancers-11-00603">Department of Experimental Therapeutics, The University of Texas M.D. Anderson Cancer Center, Houston, TX 77030, USA;<email>mnsutton@mdanderson.org</email> (M.N.S.);<email>gilbert.y.huang@gmail.com</email> (G.Y.H.);<email>jsjhzh@126.com</email> (J.Z.);<email>Wmao@mdanderson.org</email> (W.M.)</nlm:aff></affiliation></author><author><name sortKey="Huang, Gilbert Y" sort="Huang, Gilbert Y" uniqKey="Huang G" first="Gilbert Y." last="Huang">Gilbert Y. Huang</name><affiliation><nlm:aff id="af1-cancers-11-00603">Department of Experimental Therapeutics, The University of Texas M.D. Anderson Cancer Center, Houston, TX 77030, USA;<email>mnsutton@mdanderson.org</email> (M.N.S.);<email>gilbert.y.huang@gmail.com</email> (G.Y.H.);<email>jsjhzh@126.com</email> (J.Z.);<email>Wmao@mdanderson.org</email> (W.M.)</nlm:aff></affiliation></author><author><name sortKey="Zhou, Jinhua" sort="Zhou, Jinhua" uniqKey="Zhou J" first="Jinhua" last="Zhou">Jinhua Zhou</name><affiliation><nlm:aff id="af1-cancers-11-00603">Department of Experimental Therapeutics, The University of Texas M.D. Anderson Cancer Center, Houston, TX 77030, USA;<email>mnsutton@mdanderson.org</email> (M.N.S.);<email>gilbert.y.huang@gmail.com</email> (G.Y.H.);<email>jsjhzh@126.com</email> (J.Z.);<email>Wmao@mdanderson.org</email> (W.M.)</nlm:aff></affiliation><affiliation wicri:level="1"><nlm:aff id="af2-cancers-11-00603">Department of Obstetrics and Gynecology, The First Affiliated Hospital of Soochow University, Suzhou 215006, China</nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Obstetrics and Gynecology, The First Affiliated Hospital of Soochow University, Suzhou 215006</wicri:regionArea><wicri:noRegion>Suzhou 215006</wicri:noRegion></affiliation></author><author><name sortKey="Mao, Weiqun" sort="Mao, Weiqun" uniqKey="Mao W" first="Weiqun" last="Mao">Weiqun Mao</name><affiliation><nlm:aff id="af1-cancers-11-00603">Department of Experimental Therapeutics, The University of Texas M.D. Anderson Cancer Center, Houston, TX 77030, USA;<email>mnsutton@mdanderson.org</email> (M.N.S.);<email>gilbert.y.huang@gmail.com</email> (G.Y.H.);<email>jsjhzh@126.com</email> (J.Z.);<email>Wmao@mdanderson.org</email> (W.M.)</nlm:aff></affiliation></author><author><name sortKey="Langley, Robert" sort="Langley, Robert" uniqKey="Langley R" first="Robert" last="Langley">Robert Langley</name><affiliation><nlm:aff id="af3-cancers-11-00603">Office of Translational Research, The University of Texas M.D. Anderson Cancer Center, Houston, TX 77030, USA;<email>rlangley@mdanderson.org</email></nlm:aff></affiliation></author><author><name sortKey="Lu, Zhen" sort="Lu, Zhen" uniqKey="Lu Z" first="Zhen" last="Lu">Zhen Lu</name><affiliation><nlm:aff id="af1-cancers-11-00603">Department of Experimental Therapeutics, The University of Texas M.D. Anderson Cancer Center, Houston, TX 77030, USA;<email>mnsutton@mdanderson.org</email> (M.N.S.);<email>gilbert.y.huang@gmail.com</email> (G.Y.H.);<email>jsjhzh@126.com</email> (J.Z.);<email>Wmao@mdanderson.org</email> (W.M.)</nlm:aff></affiliation></author><author><name sortKey="Bast, Robert C" sort="Bast, Robert C" uniqKey="Bast R" first="Robert C." last="Bast">Robert C. Bast</name><affiliation><nlm:aff id="af1-cancers-11-00603">Department of Experimental Therapeutics, The University of Texas M.D. Anderson Cancer Center, Houston, TX 77030, USA;<email>mnsutton@mdanderson.org</email> (M.N.S.);<email>gilbert.y.huang@gmail.com</email> (G.Y.H.);<email>jsjhzh@126.com</email> (J.Z.);<email>Wmao@mdanderson.org</email> (W.M.)</nlm:aff></affiliation></author></analytic><series><title level="j">Cancers</title><idno type="eISSN">2072-6694</idno><imprint><date when="2019">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Failure to cure ovarian cancer relates to the persistence of dormant, drug-resistant cancer cells following surgery and chemotherapy. “Second look” surgery can detect small, poorly vascularized nodules of persistent ovarian cancer in ~50% of patients, where >80% are undergoing autophagy and express DIRAS3. Autophagy is one mechanism by which dormant cancer cells survive in nutrient poor environments. DIRAS3 is a tumor suppressor gene downregulated in >60% of primary ovarian cancers by genetic, epigenetic, transcriptional and post-transcriptional mechanisms, that upon re-expression can induce autophagy and dormancy in a xenograft model of ovarian cancer. We examined the expression of DIRAS3 and autophagy in ovarian cancer cells following nutrient deprivation and the mechanism by which they are upregulated. We have found that DIRAS3 mediates autophagy induced by amino acid starvation, where nutrient sensing by mTOR plays a central role. Withdrawal of amino acids downregulates mTOR, decreases binding of E2F1/4 to the DIRAS3 promoter, upregulates DIRAS3 and induces autophagy. By contrast, acute amino acid deprivation did not affect epigenetic regulation of DIRAS3 or expression of miRNAs that regulate DIRAS3. Under nutrient poor conditions DIRAS3 can be transcriptionally upregulated, inducing autophagy that could sustain dormant ovarian cancer cells.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Siegel, R L" uniqKey="Siegel R">R.L. Siegel</name></author><author><name sortKey="Miller, K D" uniqKey="Miller K">K.D. Miller</name></author><author><name sortKey="Jemal, A" uniqKey="Jemal A">A. Jemal</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Lu, Z" uniqKey="Lu Z">Z. Lu</name></author><author><name sortKey="Baquero, M T" uniqKey="Baquero M">M.T. Baquero</name></author><author><name sortKey="Yang, H" uniqKey="Yang H">H. Yang</name></author><author><name sortKey="Yang, M" uniqKey="Yang M">M. Yang</name></author><author><name sortKey="Reger, A S" uniqKey="Reger A">A.S. Reger</name></author><author><name sortKey="Kim, C" uniqKey="Kim C">C. 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Issa</name></author></analytic></biblStruct></listBibl></div1></back></TEI><affiliations><list><country><li>République populaire de Chine</li></country></list><tree><noCountry><name sortKey="Bast, Robert C" sort="Bast, Robert C" uniqKey="Bast R" first="Robert C." last="Bast">Robert C. Bast</name><name sortKey="Huang, Gilbert Y" sort="Huang, Gilbert Y" uniqKey="Huang G" first="Gilbert Y." last="Huang">Gilbert Y. Huang</name><name sortKey="Langley, Robert" sort="Langley, Robert" uniqKey="Langley R" first="Robert" last="Langley">Robert Langley</name><name sortKey="Lu, Zhen" sort="Lu, Zhen" uniqKey="Lu Z" first="Zhen" last="Lu">Zhen Lu</name><name sortKey="Mao, Weiqun" sort="Mao, Weiqun" uniqKey="Mao W" first="Weiqun" last="Mao">Weiqun Mao</name><name sortKey="Sutton, Margie N" sort="Sutton, Margie N" uniqKey="Sutton M" first="Margie N." last="Sutton">Margie N. Sutton</name></noCountry><country name="République populaire de Chine"><noRegion><name sortKey="Zhou, Jinhua" sort="Zhou, Jinhua" uniqKey="Zhou J" first="Jinhua" last="Zhou">Jinhua Zhou</name></noRegion></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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