Targeting lonidamine to mitochondria mitigates lung tumorigenesis and brain metastasis
Identifieur interne : 000029 ( France/Analysis ); précédent : 000028; suivant : 000030Targeting lonidamine to mitochondria mitigates lung tumorigenesis and brain metastasis
Auteurs : Gang Cheng [États-Unis] ; Qi Zhang [États-Unis] ; Jing Pan [États-Unis] ; Yongik Lee [États-Unis] ; Olivier Ouari [France] ; Micael Hardy [France] ; Monika Zielonka [États-Unis] ; Charles R. Myers [États-Unis] ; Jacek Zielonka [États-Unis] ; Katherine Weh [États-Unis] ; Andrew C. Chang [États-Unis] ; Guoan Chen [États-Unis] ; Laura Kresty [États-Unis] ; Balaraman Kalyanaraman [États-Unis] ; Ming You [États-Unis]Source :
- Nature Communications [ 2041-1723 ] ; 2019.
Abstract
Lung cancer often has a poor prognosis, with brain metastases a major reason for mortality. We modified lonidamine (LND), an antiglycolytic drug with limited efficacy, to mitochondria-targeted mito-lonidamine (Mito-LND) which is 100-fold more potent. Mito-LND, a tumor-selective inhibitor of oxidative phosphorylation, inhibits mitochondrial bioenergetics in lung cancer cells and mitigates lung cancer cell viability, growth, progression, and metastasis of lung cancer xenografts in mice. Mito-LND blocks lung tumor development and brain metastasis by inhibiting mitochondrial bioenergetics, stimulating the formation of reactive oxygen species, oxidizing mitochondrial peroxiredoxin, inactivating AKT/mTOR/p70S6K signaling, and inducing autophagic cell death in lung cancer cells. Mito-LND causes no toxicity in mice even when administered for eight weeks at 50 times the effective cancer inhibitory dose. Collectively, these findings show that mitochondrial targeting of LND is a promising therapeutic approach for investigating the role of autophagy in mitigating lung cancer development and brain metastasis.
Url:
DOI: 10.1038/s41467-019-10042-1
PubMed: 31101821
PubMed Central: 6525201
Affiliations:
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PMC:6525201Le document en format XML
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institution-id-type="GRID">grid.30760.32</institution-id><institution>Department of Pharmacology and Toxicology,</institution><institution>Medical College of Wisconsin,</institution></institution-wrap>8701 Watertown Plank Road, Milwaukee, WI 53226 USA</nlm:aff><country xml:lang="fr">États-Unis</country><placeName><region type="state">Wisconsin</region></placeName><wicri:cityArea>8701 Watertown Plank Road, Milwaukee</wicri:cityArea></affiliation></author><author><name sortKey="Ouari, Olivier" sort="Ouari, Olivier" uniqKey="Ouari O" first="Olivier" last="Ouari">Olivier Ouari</name><affiliation wicri:level="3"><nlm:aff id="Aff5"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2112 9282</institution-id><institution-id institution-id-type="GRID">grid.4444.0</institution-id><institution>Aix Marseille Univ,</institution><institution>CNRS,</institution></institution-wrap>ICR UMR 7273, 13013 Marseille, France</nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>ICR UMR 7273, 13013 Marseille</wicri:regionArea><placeName><region type="region" nuts="2">Provence-Alpes-Côte d'Azur</region><settlement type="city">Marseille</settlement></placeName></affiliation></author><author><name sortKey="Hardy, Micael" sort="Hardy, Micael" uniqKey="Hardy M" first="Micael" last="Hardy">Micael Hardy</name><affiliation wicri:level="3"><nlm:aff id="Aff5"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2112 9282</institution-id><institution-id institution-id-type="GRID">grid.4444.0</institution-id><institution>Aix Marseille Univ,</institution><institution>CNRS,</institution></institution-wrap>ICR UMR 7273, 13013 Marseille, France</nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>ICR UMR 7273, 13013 Marseille</wicri:regionArea><placeName><region type="region" nuts="2">Provence-Alpes-Côte d'Azur</region><settlement type="city">Marseille</settlement></placeName></affiliation></author><author><name sortKey="Zielonka, Monika" sort="Zielonka, Monika" uniqKey="Zielonka M" first="Monika" last="Zielonka">Monika Zielonka</name><affiliation wicri:level="2"><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2111 8460</institution-id><institution-id institution-id-type="GRID">grid.30760.32</institution-id><institution>Department of Biophysics,</institution><institution>Medical College of Wisconsin,</institution></institution-wrap>8701 Watertown Plank Road, Milwaukee, WI 53226 USA</nlm:aff><country xml:lang="fr">États-Unis</country><placeName><region type="state">Wisconsin</region></placeName><wicri:cityArea>8701 Watertown Plank Road, Milwaukee</wicri:cityArea></affiliation><affiliation wicri:level="2"><nlm:aff id="Aff3"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2111 8460</institution-id><institution-id institution-id-type="GRID">grid.30760.32</institution-id><institution>Center for Disease Prevention Research,</institution><institution>Medical College of Wisconsin,</institution></institution-wrap>8701 Watertown Plank Road, Milwaukee, WI 53226 USA</nlm:aff><country xml:lang="fr">États-Unis</country><placeName><region type="state">Wisconsin</region></placeName><wicri:cityArea>8701 Watertown Plank Road, Milwaukee</wicri:cityArea></affiliation></author><author><name sortKey="Myers, Charles R" sort="Myers, Charles R" uniqKey="Myers C" first="Charles R." last="Myers">Charles R. Myers</name><affiliation wicri:level="2"><nlm:aff id="Aff3"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2111 8460</institution-id><institution-id institution-id-type="GRID">grid.30760.32</institution-id><institution>Center for Disease Prevention Research,</institution><institution>Medical College of Wisconsin,</institution></institution-wrap>8701 Watertown Plank Road, Milwaukee, WI 53226 USA</nlm:aff><country xml:lang="fr">États-Unis</country><placeName><region type="state">Wisconsin</region></placeName><wicri:cityArea>8701 Watertown Plank Road, Milwaukee</wicri:cityArea></affiliation><affiliation wicri:level="2"><nlm:aff id="Aff4"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2111 8460</institution-id><institution-id institution-id-type="GRID">grid.30760.32</institution-id><institution>Department of Pharmacology and Toxicology,</institution><institution>Medical College of Wisconsin,</institution></institution-wrap>8701 Watertown Plank Road, Milwaukee, WI 53226 USA</nlm:aff><country xml:lang="fr">États-Unis</country><placeName><region type="state">Wisconsin</region></placeName><wicri:cityArea>8701 Watertown Plank Road, Milwaukee</wicri:cityArea></affiliation></author><author><name sortKey="Zielonka, Jacek" sort="Zielonka, Jacek" uniqKey="Zielonka J" first="Jacek" last="Zielonka">Jacek Zielonka</name><affiliation wicri:level="2"><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2111 8460</institution-id><institution-id institution-id-type="GRID">grid.30760.32</institution-id><institution>Free Radical Research Center,</institution><institution>Medical College of Wisconsin,</institution></institution-wrap>8701 Watertown Plank Road, Milwaukee, WI 53226 USA</nlm:aff><country xml:lang="fr">États-Unis</country><placeName><region type="state">Wisconsin</region></placeName><wicri:cityArea>8701 Watertown Plank Road, Milwaukee</wicri:cityArea></affiliation><affiliation wicri:level="2"><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2111 8460</institution-id><institution-id institution-id-type="GRID">grid.30760.32</institution-id><institution>Department of Biophysics,</institution><institution>Medical College of Wisconsin,</institution></institution-wrap>8701 Watertown Plank Road, Milwaukee, WI 53226 USA</nlm:aff><country xml:lang="fr">États-Unis</country><placeName><region type="state">Wisconsin</region></placeName><wicri:cityArea>8701 Watertown Plank Road, Milwaukee</wicri:cityArea></affiliation><affiliation wicri:level="2"><nlm:aff id="Aff3"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2111 8460</institution-id><institution-id institution-id-type="GRID">grid.30760.32</institution-id><institution>Center for Disease Prevention Research,</institution><institution>Medical College of Wisconsin,</institution></institution-wrap>8701 Watertown Plank Road, Milwaukee, WI 53226 USA</nlm:aff><country xml:lang="fr">États-Unis</country><placeName><region type="state">Wisconsin</region></placeName><wicri:cityArea>8701 Watertown Plank Road, Milwaukee</wicri:cityArea></affiliation></author><author><name sortKey="Weh, Katherine" sort="Weh, Katherine" uniqKey="Weh K" first="Katherine" last="Weh">Katherine Weh</name><affiliation wicri:level="2"><nlm:aff id="Aff6"><institution-wrap><institution-id institution-id-type="ISNI">0000000086837370</institution-id><institution-id institution-id-type="GRID">grid.214458.e</institution-id><institution>Section of Thoracic Surgery, Department of Surgery, Rogel Cancer Center,</institution><institution>University of Michigan,</institution></institution-wrap>1500 East Medical Center Drive, Ann Arbor, MI 48109 USA</nlm:aff><country xml:lang="fr">États-Unis</country><placeName><region type="state">Michigan</region></placeName><wicri:cityArea>1500 East Medical Center Drive, Ann Arbor</wicri:cityArea></affiliation></author><author><name sortKey="Chang, Andrew C" sort="Chang, Andrew C" uniqKey="Chang A" first="Andrew C." last="Chang">Andrew C. Chang</name><affiliation wicri:level="2"><nlm:aff id="Aff6"><institution-wrap><institution-id institution-id-type="ISNI">0000000086837370</institution-id><institution-id institution-id-type="GRID">grid.214458.e</institution-id><institution>Section of Thoracic Surgery, Department of Surgery, Rogel Cancer Center,</institution><institution>University of Michigan,</institution></institution-wrap>1500 East Medical Center Drive, Ann Arbor, MI 48109 USA</nlm:aff><country xml:lang="fr">États-Unis</country><placeName><region type="state">Michigan</region></placeName><wicri:cityArea>1500 East Medical Center Drive, Ann Arbor</wicri:cityArea></affiliation></author><author><name sortKey="Chen, Guoan" sort="Chen, Guoan" uniqKey="Chen G" first="Guoan" last="Chen">Guoan Chen</name><affiliation wicri:level="2"><nlm:aff id="Aff6"><institution-wrap><institution-id institution-id-type="ISNI">0000000086837370</institution-id><institution-id institution-id-type="GRID">grid.214458.e</institution-id><institution>Section of Thoracic Surgery, Department of Surgery, Rogel Cancer Center,</institution><institution>University of Michigan,</institution></institution-wrap>1500 East Medical Center Drive, Ann Arbor, MI 48109 USA</nlm:aff><country xml:lang="fr">États-Unis</country><placeName><region type="state">Michigan</region></placeName><wicri:cityArea>1500 East Medical Center Drive, Ann Arbor</wicri:cityArea></affiliation></author><author><name sortKey="Kresty, Laura" sort="Kresty, Laura" uniqKey="Kresty L" first="Laura" last="Kresty">Laura Kresty</name><affiliation wicri:level="2"><nlm:aff id="Aff6"><institution-wrap><institution-id institution-id-type="ISNI">0000000086837370</institution-id><institution-id institution-id-type="GRID">grid.214458.e</institution-id><institution>Section of Thoracic Surgery, Department of Surgery, Rogel Cancer Center,</institution><institution>University of Michigan,</institution></institution-wrap>1500 East Medical Center Drive, Ann Arbor, MI 48109 USA</nlm:aff><country xml:lang="fr">États-Unis</country><placeName><region type="state">Michigan</region></placeName><wicri:cityArea>1500 East Medical Center Drive, Ann Arbor</wicri:cityArea></affiliation></author><author><name sortKey="Kalyanaraman, Balaraman" sort="Kalyanaraman, Balaraman" uniqKey="Kalyanaraman B" first="Balaraman" last="Kalyanaraman">Balaraman Kalyanaraman</name><affiliation wicri:level="2"><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2111 8460</institution-id><institution-id institution-id-type="GRID">grid.30760.32</institution-id><institution>Free Radical Research Center,</institution><institution>Medical College of Wisconsin,</institution></institution-wrap>8701 Watertown Plank Road, Milwaukee, WI 53226 USA</nlm:aff><country xml:lang="fr">États-Unis</country><placeName><region type="state">Wisconsin</region></placeName><wicri:cityArea>8701 Watertown Plank Road, Milwaukee</wicri:cityArea></affiliation><affiliation wicri:level="2"><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2111 8460</institution-id><institution-id institution-id-type="GRID">grid.30760.32</institution-id><institution>Department of Biophysics,</institution><institution>Medical College of Wisconsin,</institution></institution-wrap>8701 Watertown Plank Road, Milwaukee, WI 53226 USA</nlm:aff><country xml:lang="fr">États-Unis</country><placeName><region type="state">Wisconsin</region></placeName><wicri:cityArea>8701 Watertown Plank Road, Milwaukee</wicri:cityArea></affiliation><affiliation wicri:level="2"><nlm:aff id="Aff3"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2111 8460</institution-id><institution-id institution-id-type="GRID">grid.30760.32</institution-id><institution>Center for Disease Prevention Research,</institution><institution>Medical College of Wisconsin,</institution></institution-wrap>8701 Watertown Plank Road, Milwaukee, WI 53226 USA</nlm:aff><country xml:lang="fr">États-Unis</country><placeName><region type="state">Wisconsin</region></placeName><wicri:cityArea>8701 Watertown Plank Road, Milwaukee</wicri:cityArea></affiliation></author><author><name sortKey="You, Ming" sort="You, Ming" uniqKey="You M" first="Ming" last="You">Ming You</name><affiliation wicri:level="2"><nlm:aff id="Aff3"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2111 8460</institution-id><institution-id institution-id-type="GRID">grid.30760.32</institution-id><institution>Center for Disease Prevention Research,</institution><institution>Medical College of Wisconsin,</institution></institution-wrap>8701 Watertown Plank Road, Milwaukee, WI 53226 USA</nlm:aff><country xml:lang="fr">États-Unis</country><placeName><region type="state">Wisconsin</region></placeName><wicri:cityArea>8701 Watertown Plank Road, Milwaukee</wicri:cityArea></affiliation><affiliation wicri:level="2"><nlm:aff id="Aff4"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2111 8460</institution-id><institution-id institution-id-type="GRID">grid.30760.32</institution-id><institution>Department of Pharmacology and Toxicology,</institution><institution>Medical College of Wisconsin,</institution></institution-wrap>8701 Watertown Plank Road, Milwaukee, WI 53226 USA</nlm:aff><country xml:lang="fr">États-Unis</country><placeName><region type="state">Wisconsin</region></placeName><wicri:cityArea>8701 Watertown Plank Road, Milwaukee</wicri:cityArea></affiliation></author></analytic><series><title level="j">Nature Communications</title><idno type="eISSN">2041-1723</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 id="Par1">Lung cancer often has a poor prognosis, with brain metastases a major reason for mortality. We modified lonidamine (LND), an antiglycolytic drug with limited efficacy, to mitochondria-targeted mito-lonidamine (Mito-LND) which is 100-fold more potent. Mito-LND, a tumor-selective inhibitor of oxidative phosphorylation, inhibits mitochondrial bioenergetics in lung cancer cells and mitigates lung cancer cell viability, growth, progression, and metastasis of lung cancer xenografts in mice. Mito-LND blocks lung tumor development and brain metastasis by inhibiting mitochondrial bioenergetics, stimulating the formation of reactive oxygen species, oxidizing mitochondrial peroxiredoxin, inactivating AKT/mTOR/p70S6K signaling, and inducing autophagic cell death in lung cancer cells. Mito-LND causes no toxicity in mice even when administered for eight weeks at 50 times the effective cancer inhibitory dose. Collectively, these findings show that mitochondrial targeting of LND is a promising therapeutic approach for investigating the role of autophagy in mitigating lung cancer development and brain metastasis.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Jemal, A" uniqKey="Jemal A">A Jemal</name></author><author><name sortKey="Siegel, R" uniqKey="Siegel R">R Siegel</name></author><author><name sortKey="Xu, J" uniqKey="Xu J">J Xu</name></author><author><name sortKey="Ward, E" uniqKey="Ward E">E Ward</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Kromer, C" uniqKey="Kromer C">C Kromer</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Goldberg, Sb" uniqKey="Goldberg S">SB Goldberg</name></author><author><name sortKey="Contessa, Jn" uniqKey="Contessa J">JN Contessa</name></author><author><name sortKey="Omay, Sb" uniqKey="Omay S">SB Omay</name></author><author><name 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sortKey="Muqit, Mm" uniqKey="Muqit M">MM Muqit</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Li, Bx" uniqKey="Li B">BX Li</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Jager, S" uniqKey="Jager S">S Jager</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Lindqvist, Lm" uniqKey="Lindqvist L">LM Lindqvist</name></author><author><name sortKey="Heinlein, M" uniqKey="Heinlein M">M Heinlein</name></author><author><name sortKey="Huang, Dc" uniqKey="Huang D">DC Huang</name></author><author><name sortKey="Vaux, Dl" uniqKey="Vaux D">DL Vaux</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Irwin, S" uniqKey="Irwin S">S Irwin</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Moser, Vc" uniqKey="Moser V">VC Moser</name></author></analytic></biblStruct><biblStruct></biblStruct><biblStruct><analytic><author><name sortKey="Porporato, Pe" uniqKey="Porporato P">PE Porporato</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Ben Yoseph, O" uniqKey="Ben Yoseph O">O Ben-Yoseph</name></author><author><name sortKey="Lyons, Jc" uniqKey="Lyons J">JC Lyons</name></author><author><name sortKey="Song, Cw" uniqKey="Song C">CW Song</name></author><author><name sortKey="Ross, Bd" uniqKey="Ross B">BD Ross</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Nancolas, B" uniqKey="Nancolas B">B Nancolas</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Milane, L" uniqKey="Milane L">L Milane</name></author><author><name sortKey="Duan, Z" uniqKey="Duan Z">Z Duan</name></author><author><name sortKey="Amiji, M" uniqKey="Amiji M">M Amiji</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Zielonka, J" uniqKey="Zielonka J">J Zielonka</name></author><author><name sortKey="Kalyanaraman, B" uniqKey="Kalyanaraman B">B Kalyanaraman</name></author></analytic></biblStruct><biblStruct></biblStruct><biblStruct><analytic><author><name sortKey="Rosenfeldt, Mt" uniqKey="Rosenfeldt M">MT Rosenfeldt</name></author><author><name sortKey="Ryan, Km" uniqKey="Ryan K">KM Ryan</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Cai, J" uniqKey="Cai J">J Cai</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="White, E" uniqKey="White E">E White</name></author><author><name sortKey="Dipaola, Rs" uniqKey="Dipaola R">RS DiPaola</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Scherz Shouval, R" uniqKey="Scherz Shouval R">R Scherz-Shouval</name></author><author><name sortKey="Elazar, Z" uniqKey="Elazar Z">Z Elazar</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Wang, X" uniqKey="Wang X">X Wang</name></author><author><name sortKey="Du, Z" uniqKey="Du Z">Z Du</name></author><author><name sortKey="Li, L" uniqKey="Li L">L Li</name></author><author><name sortKey="Shi, M" uniqKey="Shi M">M Shi</name></author><author><name sortKey="Yu, Y" uniqKey="Yu Y">Y Yu</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Chandran, K" uniqKey="Chandran K">K Chandran</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Dickey, Js" uniqKey="Dickey J">JS Dickey</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Mukhopadhyay, P" uniqKey="Mukhopadhyay P">P Mukhopadhyay</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Phelps, Rm" uniqKey="Phelps R">RM Phelps</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Nguyen, Dx" uniqKey="Nguyen D">DX Nguyen</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Zielonka, J" uniqKey="Zielonka J">J Zielonka</name></author><author><name sortKey="Hardy, M" uniqKey="Hardy M">M Hardy</name></author><author><name sortKey="Kalyanaraman, B" uniqKey="Kalyanaraman B">B Kalyanaraman</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Salabei, Jk" uniqKey="Salabei J">JK Salabei</name></author><author><name sortKey="Gibb, Aa" uniqKey="Gibb A">AA Gibb</name></author><author><name sortKey="Hill, Bg" uniqKey="Hill B">BG Hill</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Frezza, C" uniqKey="Frezza C">C Frezza</name></author><author><name sortKey="Cipolat, S" uniqKey="Cipolat S">S Cipolat</name></author><author><name sortKey="Scorrano, L" uniqKey="Scorrano L">L Scorrano</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Smith, Ra" uniqKey="Smith R">RA Smith</name></author><author><name sortKey="Kelso, Gf" uniqKey="Kelso G">GF Kelso</name></author><author><name sortKey="James, Am" uniqKey="James A">AM James</name></author><author><name sortKey="Murphy, Mp" uniqKey="Murphy M">MP Murphy</name></author></analytic></biblStruct></listBibl></div1></back></TEI><affiliations><list><country><li>France</li><li>États-Unis</li></country><region><li>Michigan</li><li>Provence-Alpes-Côte d'Azur</li><li>Wisconsin</li></region><settlement><li>Marseille</li></settlement></list><tree><country name="États-Unis"><region name="Wisconsin"><name sortKey="Cheng, Gang" sort="Cheng, Gang" uniqKey="Cheng G" first="Gang" last="Cheng">Gang Cheng</name></region><name sortKey="Chang, Andrew C" sort="Chang, Andrew C" uniqKey="Chang A" first="Andrew C." last="Chang">Andrew C. Chang</name><name sortKey="Chen, Guoan" sort="Chen, Guoan" uniqKey="Chen G" first="Guoan" last="Chen">Guoan Chen</name><name sortKey="Cheng, Gang" sort="Cheng, Gang" uniqKey="Cheng G" first="Gang" last="Cheng">Gang Cheng</name><name sortKey="Cheng, Gang" sort="Cheng, Gang" uniqKey="Cheng G" first="Gang" last="Cheng">Gang Cheng</name><name sortKey="Kalyanaraman, Balaraman" sort="Kalyanaraman, Balaraman" uniqKey="Kalyanaraman B" first="Balaraman" last="Kalyanaraman">Balaraman Kalyanaraman</name><name sortKey="Kalyanaraman, Balaraman" sort="Kalyanaraman, Balaraman" uniqKey="Kalyanaraman B" first="Balaraman" last="Kalyanaraman">Balaraman Kalyanaraman</name><name sortKey="Kalyanaraman, Balaraman" sort="Kalyanaraman, Balaraman" uniqKey="Kalyanaraman B" first="Balaraman" last="Kalyanaraman">Balaraman Kalyanaraman</name><name sortKey="Kresty, Laura" sort="Kresty, Laura" uniqKey="Kresty L" first="Laura" last="Kresty">Laura Kresty</name><name sortKey="Lee, Yongik" sort="Lee, Yongik" uniqKey="Lee Y" first="Yongik" last="Lee">Yongik Lee</name><name sortKey="Myers, Charles R" sort="Myers, Charles R" uniqKey="Myers C" first="Charles R." last="Myers">Charles R. Myers</name><name sortKey="Myers, Charles R" sort="Myers, Charles R" uniqKey="Myers C" first="Charles R." last="Myers">Charles R. Myers</name><name sortKey="Pan, Jing" sort="Pan, Jing" uniqKey="Pan J" first="Jing" last="Pan">Jing Pan</name><name sortKey="Pan, Jing" sort="Pan, Jing" uniqKey="Pan J" first="Jing" last="Pan">Jing Pan</name><name sortKey="Weh, Katherine" sort="Weh, Katherine" uniqKey="Weh K" first="Katherine" last="Weh">Katherine Weh</name><name sortKey="You, Ming" sort="You, Ming" uniqKey="You M" first="Ming" last="You">Ming You</name><name sortKey="You, Ming" sort="You, Ming" uniqKey="You M" first="Ming" last="You">Ming You</name><name sortKey="Zhang, Qi" sort="Zhang, Qi" uniqKey="Zhang Q" first="Qi" last="Zhang">Qi Zhang</name><name sortKey="Zhang, Qi" sort="Zhang, Qi" uniqKey="Zhang Q" first="Qi" last="Zhang">Qi Zhang</name><name sortKey="Zielonka, Jacek" sort="Zielonka, Jacek" uniqKey="Zielonka J" first="Jacek" last="Zielonka">Jacek Zielonka</name><name sortKey="Zielonka, Jacek" sort="Zielonka, Jacek" uniqKey="Zielonka J" first="Jacek" last="Zielonka">Jacek Zielonka</name><name sortKey="Zielonka, Jacek" sort="Zielonka, Jacek" uniqKey="Zielonka J" first="Jacek" last="Zielonka">Jacek Zielonka</name><name sortKey="Zielonka, Monika" sort="Zielonka, Monika" uniqKey="Zielonka M" first="Monika" last="Zielonka">Monika Zielonka</name><name sortKey="Zielonka, Monika" sort="Zielonka, Monika" uniqKey="Zielonka M" first="Monika" last="Zielonka">Monika Zielonka</name></country><country name="France"><region name="Provence-Alpes-Côte d'Azur"><name sortKey="Ouari, Olivier" sort="Ouari, Olivier" uniqKey="Ouari O" first="Olivier" last="Ouari">Olivier Ouari</name></region><name sortKey="Hardy, Micael" sort="Hardy, Micael" uniqKey="Hardy M" first="Micael" last="Hardy">Micael Hardy</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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