Reprogramming of Amino Acid Transporters to Support Aspartate and Glutamate Dependency Sustains Endocrine Resistance in Breast Cancer
Identifieur interne : 000034 ( France/Analysis ); précédent : 000033; suivant : 000035Reprogramming of Amino Acid Transporters to Support Aspartate and Glutamate Dependency Sustains Endocrine Resistance in Breast Cancer
Auteurs : Marina Bacci [Italie] ; Nicla Lorito [Italie] ; Luigi Ippolito [Italie] ; Matteo Ramazzotti [Italie] ; Simone Luti [Italie] ; Simone Romagnoli [Italie] ; Matteo Parri [Italie] ; Francesca Bianchini [Italie] ; Federica Cappellesso [Belgique] ; Federico Virga [Belgique, Italie] ; Qiong Gao [Royaume-Uni] ; Bruno M. Sim Es [Royaume-Uni] ; Elisabetta Marangoni [France] ; Lesley-Ann Martin [Royaume-Uni] ; Giuseppina Comito [Italie] ; Manuela Ferracin [Italie] ; Elisa Giannoni [Italie] ; Massimiliano Mazzone [Belgique] ; Paola Chiarugi [Italie] ; Andrea Morandi [Italie]Source :
- Cell Reports [ 2211-1247 ] ; 2019.
Abstract
Endocrine therapy (ET) is the standard of care for estrogen receptor-positive (ER+) breast cancers. Despite its efficacy, ∼40% of women relapse with ET-resistant (ETR) disease. A global transcription analysis in ETR cells reveals a downregulation of the neutral and basic amino acid transporter SLC6A14 governed by enhanced miR-23b-3p expression, resulting in impaired amino acid metabolism. This altered amino acid metabolism in ETR cells is supported by the activation of autophagy and the enhanced import of acidic amino acids (aspartate and glutamate) mediated by the SLC1A2 transporter. The clinical significance of these findings is validated by multiple orthogonal approaches in a large cohort of ET-treated patients, in patient-derived xenografts, and in
Url:
DOI: 10.1016/j.celrep.2019.06.010
PubMed: 31269432
PubMed Central: 6616584
Affiliations:
- Belgique, France, Italie, Royaume-Uni
- Angleterre, Grand Manchester, Piémont, Île-de-France
- Manchester, Turin
- Université de Manchester
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PMC:6616584Le document en format XML
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50134</wicri:regionArea><wicri:noRegion>Florence 50134</wicri:noRegion></affiliation></author><author><name sortKey="Lorito, Nicla" sort="Lorito, Nicla" uniqKey="Lorito N" first="Nicla" last="Lorito">Nicla Lorito</name><affiliation wicri:level="1"><nlm:aff id="aff1">Department of Experimental and Clinical Biomedical Sciences, University of Florence, Florence 50134, Italy</nlm:aff><country xml:lang="fr">Italie</country><wicri:regionArea>Department of Experimental and Clinical Biomedical Sciences, University of Florence, Florence 50134</wicri:regionArea><wicri:noRegion>Florence 50134</wicri:noRegion></affiliation></author><author><name sortKey="Ippolito, Luigi" sort="Ippolito, Luigi" uniqKey="Ippolito L" first="Luigi" last="Ippolito">Luigi Ippolito</name><affiliation wicri:level="1"><nlm:aff id="aff1">Department of Experimental and Clinical Biomedical Sciences, University of Florence, Florence 50134, Italy</nlm:aff><country xml:lang="fr">Italie</country><wicri:regionArea>Department of Experimental and Clinical Biomedical Sciences, University of Florence, Florence 50134</wicri:regionArea><wicri:noRegion>Florence 50134</wicri:noRegion></affiliation></author><author><name sortKey="Ramazzotti, Matteo" sort="Ramazzotti, Matteo" uniqKey="Ramazzotti M" first="Matteo" last="Ramazzotti">Matteo Ramazzotti</name><affiliation wicri:level="1"><nlm:aff id="aff1">Department of Experimental and Clinical Biomedical Sciences, University of Florence, Florence 50134, Italy</nlm:aff><country xml:lang="fr">Italie</country><wicri:regionArea>Department of Experimental and Clinical Biomedical Sciences, University of Florence, Florence 50134</wicri:regionArea><wicri:noRegion>Florence 50134</wicri:noRegion></affiliation></author><author><name sortKey="Luti, Simone" sort="Luti, Simone" uniqKey="Luti S" first="Simone" last="Luti">Simone Luti</name><affiliation wicri:level="1"><nlm:aff id="aff1">Department of Experimental and Clinical Biomedical Sciences, University of Florence, Florence 50134, Italy</nlm:aff><country xml:lang="fr">Italie</country><wicri:regionArea>Department of Experimental and Clinical Biomedical Sciences, University of Florence, Florence 50134</wicri:regionArea><wicri:noRegion>Florence 50134</wicri:noRegion></affiliation></author><author><name sortKey="Romagnoli, Simone" sort="Romagnoli, Simone" uniqKey="Romagnoli S" first="Simone" last="Romagnoli">Simone Romagnoli</name><affiliation wicri:level="1"><nlm:aff id="aff1">Department of Experimental and Clinical Biomedical Sciences, University of Florence, Florence 50134, Italy</nlm:aff><country xml:lang="fr">Italie</country><wicri:regionArea>Department of Experimental and Clinical Biomedical Sciences, University of Florence, Florence 50134</wicri:regionArea><wicri:noRegion>Florence 50134</wicri:noRegion></affiliation></author><author><name sortKey="Parri, Matteo" sort="Parri, Matteo" uniqKey="Parri M" first="Matteo" last="Parri">Matteo Parri</name><affiliation wicri:level="1"><nlm:aff id="aff1">Department of Experimental and Clinical Biomedical Sciences, University of Florence, Florence 50134, Italy</nlm:aff><country xml:lang="fr">Italie</country><wicri:regionArea>Department of Experimental and Clinical Biomedical Sciences, University of Florence, Florence 50134</wicri:regionArea><wicri:noRegion>Florence 50134</wicri:noRegion></affiliation></author><author><name sortKey="Bianchini, Francesca" sort="Bianchini, Francesca" uniqKey="Bianchini F" first="Francesca" last="Bianchini">Francesca Bianchini</name><affiliation wicri:level="1"><nlm:aff id="aff1">Department of Experimental and Clinical Biomedical Sciences, University of Florence, Florence 50134, Italy</nlm:aff><country xml:lang="fr">Italie</country><wicri:regionArea>Department of Experimental and Clinical Biomedical Sciences, University of Florence, Florence 50134</wicri:regionArea><wicri:noRegion>Florence 50134</wicri:noRegion></affiliation></author><author><name sortKey="Cappellesso, Federica" sort="Cappellesso, Federica" 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wicri:level="1"><nlm:aff id="aff3">Molecular Biotechnology Center (MBC), Department of Molecular Biotechnology and Health Sciences, University of Turin, Turin 10126, Italy</nlm:aff><country xml:lang="fr">Italie</country><wicri:regionArea>Molecular Biotechnology Center (MBC), Department of Molecular Biotechnology and Health Sciences, University of Turin, Turin 10126</wicri:regionArea><placeName><settlement type="city">Turin</settlement><region type="région" nuts="2">Piémont</region></placeName></affiliation></author><author><name sortKey="Gao, Qiong" sort="Gao, Qiong" uniqKey="Gao Q" first="Qiong" last="Gao">Qiong Gao</name><affiliation wicri:level="1"><nlm:aff id="aff4">The Breast Cancer Now Toby Robins Research Centre, The Institute of Cancer Research, London SW3 6JB, UK</nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>The Breast Cancer Now Toby Robins Research Centre, The Institute of Cancer Research, London SW3 6JB</wicri:regionArea><wicri:noRegion>London SW3 6JB</wicri:noRegion></affiliation></author><author><name sortKey="Sim Es, Bruno M" sort="Sim Es, Bruno M" uniqKey="Sim Es B" first="Bruno M." last="Sim Es">Bruno M. Sim Es</name><affiliation wicri:level="4"><nlm:aff id="aff5">Breast Cancer Now Research Unit, Division of Cancer Sciences, Manchester Cancer Research Centre, University of Manchester, Manchester M20 4GJ, UK</nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Breast Cancer Now Research Unit, Division of Cancer Sciences, Manchester Cancer Research Centre, University of Manchester, Manchester M20 4GJ</wicri:regionArea><orgName type="university">Université de Manchester</orgName><placeName><settlement type="city">Manchester</settlement><region type="nation">Angleterre</region><region nuts="2" type="region">Grand Manchester</region></placeName></affiliation></author><author><name sortKey="Marangoni, Elisabetta" sort="Marangoni, Elisabetta" uniqKey="Marangoni E" first="Elisabetta" last="Marangoni">Elisabetta Marangoni</name><affiliation wicri:level="3"><nlm:aff id="aff6">Institut Curie, PSL Research University, Translational Research Department, Paris 75248, France</nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Institut Curie, PSL Research University, Translational Research Department, Paris 75248</wicri:regionArea><placeName><region type="region" nuts="2">Île-de-France</region></placeName></affiliation></author><author><name sortKey="Martin, Lesley Ann" sort="Martin, Lesley Ann" uniqKey="Martin L" first="Lesley-Ann" last="Martin">Lesley-Ann Martin</name><affiliation wicri:level="1"><nlm:aff id="aff4">The Breast Cancer Now Toby Robins Research Centre, The Institute of Cancer Research, London SW3 6JB, UK</nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>The Breast Cancer Now Toby Robins Research Centre, The Institute of Cancer Research, London SW3 6JB</wicri:regionArea><wicri:noRegion>London SW3 6JB</wicri:noRegion></affiliation></author><author><name sortKey="Comito, Giuseppina" sort="Comito, Giuseppina" uniqKey="Comito G" first="Giuseppina" last="Comito">Giuseppina Comito</name><affiliation wicri:level="1"><nlm:aff id="aff1">Department of Experimental and Clinical Biomedical Sciences, University of Florence, Florence 50134, Italy</nlm:aff><country xml:lang="fr">Italie</country><wicri:regionArea>Department of Experimental and Clinical Biomedical Sciences, University of Florence, Florence 50134</wicri:regionArea><wicri:noRegion>Florence 50134</wicri:noRegion></affiliation></author><author><name sortKey="Ferracin, Manuela" sort="Ferracin, Manuela" uniqKey="Ferracin M" first="Manuela" last="Ferracin">Manuela Ferracin</name><affiliation wicri:level="1"><nlm:aff id="aff7">Department of Experimental, Diagnostic, and Specialty Medicine (DIMES), University of Bologna, Bologna 40126, Italy</nlm:aff><country xml:lang="fr">Italie</country><wicri:regionArea>Department of Experimental, Diagnostic, and Specialty Medicine (DIMES), University of Bologna, Bologna 40126</wicri:regionArea><wicri:noRegion>Bologna 40126</wicri:noRegion></affiliation></author><author><name sortKey="Giannoni, Elisa" sort="Giannoni, Elisa" uniqKey="Giannoni E" first="Elisa" last="Giannoni">Elisa Giannoni</name><affiliation wicri:level="1"><nlm:aff id="aff1">Department of Experimental and Clinical Biomedical Sciences, University of Florence, Florence 50134, Italy</nlm:aff><country xml:lang="fr">Italie</country><wicri:regionArea>Department of Experimental and Clinical Biomedical Sciences, University of Florence, Florence 50134</wicri:regionArea><wicri:noRegion>Florence 50134</wicri:noRegion></affiliation></author><author><name sortKey="Mazzone, Massimiliano" sort="Mazzone, Massimiliano" uniqKey="Mazzone M" first="Massimiliano" last="Mazzone">Massimiliano Mazzone</name><affiliation wicri:level="1"><nlm:aff id="aff2">VIB Center for Cancer Biology, Department of Oncology, University of Leuven, Leuven 3000, Belgium</nlm:aff><country xml:lang="fr">Belgique</country><wicri:regionArea>VIB Center for Cancer Biology, Department of Oncology, University of Leuven, Leuven 3000</wicri:regionArea><wicri:noRegion>Leuven 3000</wicri:noRegion></affiliation></author><author><name sortKey="Chiarugi, Paola" sort="Chiarugi, Paola" uniqKey="Chiarugi P" first="Paola" last="Chiarugi">Paola Chiarugi</name><affiliation wicri:level="1"><nlm:aff id="aff1">Department of Experimental and Clinical Biomedical Sciences, University of Florence, Florence 50134, Italy</nlm:aff><country xml:lang="fr">Italie</country><wicri:regionArea>Department of Experimental and Clinical Biomedical Sciences, University of Florence, Florence 50134</wicri:regionArea><wicri:noRegion>Florence 50134</wicri:noRegion></affiliation></author><author><name sortKey="Morandi, Andrea" sort="Morandi, Andrea" uniqKey="Morandi A" first="Andrea" last="Morandi">Andrea Morandi</name><affiliation wicri:level="1"><nlm:aff id="aff1">Department of Experimental and Clinical Biomedical Sciences, University of Florence, Florence 50134, Italy</nlm:aff><country xml:lang="fr">Italie</country><wicri:regionArea>Department of Experimental and Clinical Biomedical Sciences, University of Florence, Florence 50134</wicri:regionArea><wicri:noRegion>Florence 50134</wicri:noRegion></affiliation></author></analytic><series><title level="j">Cell Reports</title><idno type="eISSN">2211-1247</idno><imprint><date when="2019">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><title>Summary</title><p>Endocrine therapy (ET) is the standard of care for estrogen receptor-positive (ER<sup>+</sup>) breast cancers. Despite its efficacy, ∼40% of women relapse with ET-resistant (ETR) disease. A global transcription analysis in ETR cells reveals a downregulation of the neutral and basic amino acid transporter SLC6A14 governed by enhanced miR-23b-3p expression, resulting in impaired amino acid metabolism. This altered amino acid metabolism in ETR cells is supported by the activation of autophagy and the enhanced import of acidic amino acids (aspartate and glutamate) mediated by the SLC1A2 transporter. The clinical significance of these findings is validated by multiple orthogonal approaches in a large cohort of ET-treated patients, in patient-derived xenografts, and in <italic>in vivo</italic> experiments. Targeting these amino acid metabolic dependencies resensitizes ETR cells to therapy and impairs the aggressive features of ETR cells, offering predictive biomarkers and potential targetable pathways to be exploited to combat or delay ETR in ER<sup>+</sup> breast cancers.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct></listBibl></div1></back></TEI><affiliations><list><country><li>Belgique</li><li>France</li><li>Italie</li><li>Royaume-Uni</li></country><region><li>Angleterre</li><li>Grand Manchester</li><li>Piémont</li><li>Île-de-France</li></region><settlement><li>Manchester</li><li>Turin</li></settlement><orgName><li>Université de Manchester</li></orgName></list><tree><country name="Italie"><noRegion><name sortKey="Bacci, Marina" sort="Bacci, Marina" uniqKey="Bacci M" first="Marina" last="Bacci">Marina Bacci</name></noRegion><name sortKey="Bianchini, Francesca" sort="Bianchini, Francesca" uniqKey="Bianchini F" first="Francesca" last="Bianchini">Francesca Bianchini</name><name sortKey="Chiarugi, Paola" sort="Chiarugi, Paola" uniqKey="Chiarugi P" first="Paola" last="Chiarugi">Paola Chiarugi</name><name sortKey="Comito, Giuseppina" sort="Comito, Giuseppina" uniqKey="Comito G" first="Giuseppina" last="Comito">Giuseppina Comito</name><name sortKey="Ferracin, Manuela" sort="Ferracin, Manuela" uniqKey="Ferracin M" first="Manuela" last="Ferracin">Manuela Ferracin</name><name sortKey="Giannoni, Elisa" sort="Giannoni, Elisa" uniqKey="Giannoni E" first="Elisa" last="Giannoni">Elisa Giannoni</name><name sortKey="Ippolito, Luigi" sort="Ippolito, Luigi" uniqKey="Ippolito L" first="Luigi" last="Ippolito">Luigi Ippolito</name><name sortKey="Lorito, Nicla" sort="Lorito, Nicla" uniqKey="Lorito N" first="Nicla" last="Lorito">Nicla Lorito</name><name sortKey="Luti, Simone" sort="Luti, Simone" uniqKey="Luti S" first="Simone" last="Luti">Simone Luti</name><name sortKey="Morandi, Andrea" sort="Morandi, Andrea" uniqKey="Morandi A" first="Andrea" last="Morandi">Andrea Morandi</name><name sortKey="Parri, Matteo" sort="Parri, Matteo" uniqKey="Parri M" first="Matteo" last="Parri">Matteo Parri</name><name sortKey="Ramazzotti, Matteo" sort="Ramazzotti, Matteo" uniqKey="Ramazzotti M" first="Matteo" last="Ramazzotti">Matteo Ramazzotti</name><name sortKey="Romagnoli, Simone" sort="Romagnoli, Simone" uniqKey="Romagnoli S" first="Simone" last="Romagnoli">Simone Romagnoli</name><name sortKey="Virga, Federico" sort="Virga, Federico" uniqKey="Virga F" first="Federico" last="Virga">Federico Virga</name></country><country name="Belgique"><noRegion><name sortKey="Cappellesso, Federica" sort="Cappellesso, Federica" uniqKey="Cappellesso F" first="Federica" last="Cappellesso">Federica Cappellesso</name></noRegion><name sortKey="Mazzone, Massimiliano" sort="Mazzone, Massimiliano" uniqKey="Mazzone M" first="Massimiliano" last="Mazzone">Massimiliano Mazzone</name><name sortKey="Virga, Federico" sort="Virga, Federico" uniqKey="Virga F" first="Federico" last="Virga">Federico Virga</name></country><country name="Royaume-Uni"><noRegion><name sortKey="Gao, Qiong" sort="Gao, Qiong" uniqKey="Gao Q" first="Qiong" last="Gao">Qiong Gao</name></noRegion><name sortKey="Martin, Lesley Ann" sort="Martin, Lesley Ann" uniqKey="Martin L" first="Lesley-Ann" last="Martin">Lesley-Ann Martin</name><name sortKey="Sim Es, Bruno M" sort="Sim Es, Bruno M" uniqKey="Sim Es B" first="Bruno M." last="Sim Es">Bruno M. Sim Es</name></country><country name="France"><region name="Île-de-France"><name sortKey="Marangoni, Elisabetta" sort="Marangoni, Elisabetta" uniqKey="Marangoni E" first="Elisabetta" last="Marangoni">Elisabetta Marangoni</name></region></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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