Secondary Somatic Mutations Restoring RAD51C and RAD51D Associated with Acquired Resistance to the PARP Inhibitor Rucaparib in High-Grade Ovarian Carcinoma.
Identifieur interne : 000379 ( PubMed/Checkpoint ); précédent : 000378; suivant : 000380Secondary Somatic Mutations Restoring RAD51C and RAD51D Associated with Acquired Resistance to the PARP Inhibitor Rucaparib in High-Grade Ovarian Carcinoma.
Auteurs : Olga Kondrashova [Australie] ; Minh Nguyen [États-Unis] ; Kristy Shield-Artin [Australie] ; Anna V. Tinker [Canada] ; Nelson N H. Teng [États-Unis] ; Maria I. Harrell [États-Unis] ; Michael J. Kuiper [Australie] ; Gwo-Yaw Ho [Australie] ; Holly Barker [Australie] ; Maria Jasin [États-Unis] ; Rohit Prakash [États-Unis] ; Elizabeth M. Kass [États-Unis] ; Meghan R. Sullivan [États-Unis] ; Gregory J. Brunette [États-Unis] ; Kara A. Bernstein [États-Unis] ; Robert L. Coleman [États-Unis] ; Anne Floquet [France] ; Michael Friedlander [Australie] ; Ganessan Kichenadasse [Australie] ; David M. O'Malley [États-Unis] ; Amit Oza [Canada] ; James Sun [États-Unis] ; Liliane Robillard [États-Unis] ; Lara Maloney [États-Unis] ; David Bowtell ; Heidi Giordano [États-Unis] ; Matthew J. Wakefield [Australie] ; Scott H. Kaufmann [États-Unis] ; Andrew D. Simmons [États-Unis] ; Thomas C. Harding [États-Unis] ; Mitch Raponi [États-Unis] ; Iain A. Mcneish [Royaume-Uni] ; Elizabeth M. Swisher [États-Unis] ; Kevin K. Lin [États-Unis] ; Clare L. Scott [Australie]Source :
- Cancer discovery [ 2159-8290 ] ; 2017.
Abstract
High-grade epithelial ovarian carcinomas containing mutated BRCA1 or BRCA2 (BRCA1/2) homologous recombination (HR) genes are sensitive to platinum-based chemotherapy and PARP inhibitors (PARPi), while restoration of HR function due to secondary mutations in BRCA1/2 has been recognized as an important resistance mechanism. We sequenced core HR pathway genes in 12 pairs of pretreatment and postprogression tumor biopsy samples collected from patients in ARIEL2 Part 1, a phase II study of the PARPi rucaparib as treatment for platinum-sensitive, relapsed ovarian carcinoma. In 6 of 12 pretreatment biopsies, a truncation mutation in BRCA1, RAD51C, or RAD51D was identified. In five of six paired postprogression biopsies, one or more secondary mutations restored the open reading frame. Four distinct secondary mutations and spatial heterogeneity were observed for RAD51CIn vitro complementation assays and a patient-derived xenograft, as well as predictive molecular modeling, confirmed that resistance to rucaparib was associated with secondary mutations.Significance: Analyses of primary and secondary mutations in RAD51C and RAD51D provide evidence for these primary mutations in conferring PARPi sensitivity and secondary mutations as a mechanism of acquired PARPi resistance. PARPi resistance due to secondary mutations underpins the need for early delivery of PARPi therapy and for combination strategies. Cancer Discov; 7(9); 984-98. ©2017 AACR.See related commentary by Domchek, p. 937See related article by Quigley et al., p. 999See related article by Goodall et al., p. 1006This article is highlighted in the In This Issue feature, p. 920.
DOI: 10.1158/2159-8290.CD-17-0419
PubMed: 28588062
Affiliations:
- Australie, Canada, France, Royaume-Uni, États-Unis
- Aquitaine, Californie, Colorado, Massachusetts, Minnesota, Nouvelle-Aquitaine, Ohio, Pennsylvanie, Texas, Victoria (État), Washington (État), Écosse, État de New York
- Bordeaux, Glasgow, Melbourne
- Université de Glasgow, Université de Melbourne
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Wakefield</name><affiliation wicri:level="1"><nlm:affiliation>Walter and Eliza Hall Institute of Medical Research, Melbourne, Victoria, Australia.</nlm:affiliation><country xml:lang="fr">Australie</country><wicri:regionArea>Walter and Eliza Hall Institute of Medical Research, Melbourne, Victoria</wicri:regionArea><wicri:noRegion>Victoria</wicri:noRegion></affiliation></author><author><name sortKey="Kaufmann, Scott H" sort="Kaufmann, Scott H" uniqKey="Kaufmann S" first="Scott H" last="Kaufmann">Scott H. Kaufmann</name><affiliation wicri:level="2"><nlm:affiliation>Mayo Clinic Cancer Center, Rochester, Minnesota.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Minnesota</region></placeName><wicri:cityArea>Mayo Clinic Cancer Center, Rochester</wicri:cityArea></affiliation></author><author><name sortKey="Simmons, Andrew D" sort="Simmons, Andrew D" uniqKey="Simmons A" first="Andrew D" last="Simmons">Andrew D. Simmons</name><affiliation wicri:level="2"><nlm:affiliation>Clovis Oncology, Inc., Boulder, Colorado.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Colorado</region></placeName><wicri:cityArea>Clovis Oncology, Inc., Boulder</wicri:cityArea></affiliation></author><author><name sortKey="Harding, Thomas C" sort="Harding, Thomas C" uniqKey="Harding T" first="Thomas C" last="Harding">Thomas C. Harding</name><affiliation wicri:level="2"><nlm:affiliation>Clovis Oncology, Inc., Boulder, Colorado.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Colorado</region></placeName><wicri:cityArea>Clovis Oncology, Inc., Boulder</wicri:cityArea></affiliation></author><author><name sortKey="Raponi, Mitch" sort="Raponi, Mitch" uniqKey="Raponi M" first="Mitch" last="Raponi">Mitch Raponi</name><affiliation wicri:level="2"><nlm:affiliation>Clovis Oncology, Inc., Boulder, Colorado.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Colorado</region></placeName><wicri:cityArea>Clovis Oncology, Inc., Boulder</wicri:cityArea></affiliation></author><author><name sortKey="Mcneish, Iain A" sort="Mcneish, Iain A" uniqKey="Mcneish I" first="Iain A" last="Mcneish">Iain A. Mcneish</name><affiliation wicri:level="4"><nlm:affiliation>Institute of Cancer Sciences, University of Glasgow, Glasgow, United Kingdom.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Institute of Cancer Sciences, University of Glasgow, Glasgow</wicri:regionArea><orgName type="university">Université de Glasgow</orgName><placeName><settlement type="city">Glasgow</settlement><region type="country">Écosse</region></placeName></affiliation></author><author><name sortKey="Swisher, Elizabeth M" sort="Swisher, Elizabeth M" uniqKey="Swisher E" first="Elizabeth M" last="Swisher">Elizabeth M. Swisher</name><affiliation wicri:level="2"><nlm:affiliation>University of Washington, Seattle, Washington.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Washington (État)</region></placeName><wicri:cityArea>University of Washington, Seattle</wicri:cityArea></affiliation></author><author><name sortKey="Lin, Kevin K" sort="Lin, Kevin K" uniqKey="Lin K" first="Kevin K" last="Lin">Kevin K. Lin</name><affiliation wicri:level="2"><nlm:affiliation>Clovis Oncology, Inc., Boulder, Colorado.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Colorado</region></placeName><wicri:cityArea>Clovis Oncology, Inc., Boulder</wicri:cityArea></affiliation></author><author><name sortKey="Scott, Clare L" sort="Scott, Clare L" uniqKey="Scott C" first="Clare L" last="Scott">Clare L. Scott</name><affiliation wicri:level="1"><nlm:affiliation>Walter and Eliza Hall Institute of Medical Research, Melbourne, Victoria, Australia. scottc@wehi.edu.au.</nlm:affiliation><country xml:lang="fr">Australie</country><wicri:regionArea>Walter and Eliza Hall Institute of Medical Research, Melbourne, Victoria</wicri:regionArea><wicri:noRegion>Victoria</wicri:noRegion></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PubMed</idno><date when="2017">2017</date><idno type="RBID">pubmed:28588062</idno><idno type="pmid">28588062</idno><idno type="doi">10.1158/2159-8290.CD-17-0419</idno><idno type="wicri:Area/PubMed/Corpus">000647</idno><idno type="wicri:explorRef" wicri:stream="PubMed" wicri:step="Corpus" wicri:corpus="PubMed">000647</idno><idno type="wicri:Area/PubMed/Curation">000645</idno><idno type="wicri:explorRef" wicri:stream="PubMed" wicri:step="Curation">000645</idno><idno type="wicri:Area/PubMed/Checkpoint">000645</idno><idno type="wicri:explorRef" wicri:stream="Checkpoint" wicri:step="PubMed">000645</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en">Secondary Somatic Mutations Restoring RAD51C and RAD51D Associated with Acquired Resistance to the PARP Inhibitor Rucaparib in High-Grade Ovarian Carcinoma.</title><author><name sortKey="Kondrashova, Olga" sort="Kondrashova, Olga" uniqKey="Kondrashova O" first="Olga" last="Kondrashova">Olga Kondrashova</name><affiliation wicri:level="1"><nlm:affiliation>Walter and Eliza Hall Institute of Medical Research, Melbourne, Victoria, Australia.</nlm:affiliation><country xml:lang="fr">Australie</country><wicri:regionArea>Walter and Eliza Hall Institute of Medical Research, Melbourne, Victoria</wicri:regionArea><wicri:noRegion>Victoria</wicri:noRegion></affiliation></author><author><name sortKey="Nguyen, Minh" sort="Nguyen, Minh" uniqKey="Nguyen M" first="Minh" last="Nguyen">Minh Nguyen</name><affiliation wicri:level="2"><nlm:affiliation>Clovis Oncology, Inc., Boulder, Colorado.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Colorado</region></placeName><wicri:cityArea>Clovis Oncology, Inc., Boulder</wicri:cityArea></affiliation></author><author><name sortKey="Shield Artin, Kristy" sort="Shield Artin, Kristy" uniqKey="Shield Artin K" first="Kristy" last="Shield-Artin">Kristy Shield-Artin</name><affiliation wicri:level="1"><nlm:affiliation>Walter and Eliza Hall Institute of Medical Research, Melbourne, Victoria, Australia.</nlm:affiliation><country xml:lang="fr">Australie</country><wicri:regionArea>Walter and Eliza Hall Institute of Medical Research, Melbourne, Victoria</wicri:regionArea><wicri:noRegion>Victoria</wicri:noRegion></affiliation></author><author><name sortKey="Tinker, Anna V" sort="Tinker, Anna V" uniqKey="Tinker A" first="Anna V" last="Tinker">Anna V. Tinker</name><affiliation wicri:level="1"><nlm:affiliation>British Columbia Cancer Agency, Vancouver, British Columbia, Canada.</nlm:affiliation><country xml:lang="fr">Canada</country><wicri:regionArea>British Columbia Cancer Agency, Vancouver, British Columbia</wicri:regionArea><wicri:noRegion>British Columbia</wicri:noRegion></affiliation></author><author><name sortKey="Teng, Nelson N H" sort="Teng, Nelson N H" uniqKey="Teng N" first="Nelson N H" last="Teng">Nelson N H. Teng</name><affiliation wicri:level="2"><nlm:affiliation>Stanford University, Palo Alto, California.</nlm:affiliation><country>États-Unis</country><placeName><region type="state">Californie</region></placeName><wicri:cityArea>Stanford University, Palo Alto</wicri:cityArea></affiliation></author><author><name sortKey="Harrell, Maria I" sort="Harrell, Maria I" uniqKey="Harrell M" first="Maria I" last="Harrell">Maria I. Harrell</name><affiliation wicri:level="2"><nlm:affiliation>University of Washington, Seattle, Washington.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Washington (État)</region></placeName><wicri:cityArea>University of Washington, Seattle</wicri:cityArea></affiliation></author><author><name sortKey="Kuiper, Michael J" sort="Kuiper, Michael J" uniqKey="Kuiper M" first="Michael J" last="Kuiper">Michael J. Kuiper</name><affiliation wicri:level="4"><nlm:affiliation>Melbourne Bioinformatics, The University of Melbourne, Melbourne, Victoria, Australia.</nlm:affiliation><country xml:lang="fr">Australie</country><wicri:regionArea>Melbourne Bioinformatics, The University of Melbourne, Melbourne, Victoria</wicri:regionArea><orgName type="university">Université de Melbourne</orgName><placeName><settlement type="city">Melbourne</settlement><region type="état">Victoria (État)</region></placeName></affiliation></author><author><name sortKey="Ho, Gwo Yaw" sort="Ho, Gwo Yaw" uniqKey="Ho G" first="Gwo-Yaw" last="Ho">Gwo-Yaw Ho</name><affiliation wicri:level="1"><nlm:affiliation>Walter and Eliza Hall Institute of Medical Research, Melbourne, Victoria, Australia.</nlm:affiliation><country xml:lang="fr">Australie</country><wicri:regionArea>Walter and Eliza Hall Institute of Medical Research, Melbourne, Victoria</wicri:regionArea><wicri:noRegion>Victoria</wicri:noRegion></affiliation></author><author><name sortKey="Barker, Holly" sort="Barker, Holly" uniqKey="Barker H" first="Holly" last="Barker">Holly Barker</name><affiliation wicri:level="1"><nlm:affiliation>Walter and Eliza Hall Institute of Medical Research, Melbourne, Victoria, Australia.</nlm:affiliation><country xml:lang="fr">Australie</country><wicri:regionArea>Walter and Eliza Hall Institute of Medical Research, Melbourne, Victoria</wicri:regionArea><wicri:noRegion>Victoria</wicri:noRegion></affiliation></author><author><name sortKey="Jasin, Maria" sort="Jasin, Maria" uniqKey="Jasin M" first="Maria" last="Jasin">Maria Jasin</name><affiliation wicri:level="2"><nlm:affiliation>Developmental Biology Program, Memorial Sloan Kettering Cancer Center, New York, New York.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">État de New York</region></placeName><wicri:cityArea>Developmental Biology Program, Memorial Sloan Kettering Cancer Center, New York</wicri:cityArea></affiliation></author><author><name sortKey="Prakash, Rohit" sort="Prakash, Rohit" uniqKey="Prakash R" first="Rohit" last="Prakash">Rohit Prakash</name><affiliation wicri:level="2"><nlm:affiliation>Developmental Biology Program, Memorial Sloan Kettering Cancer Center, New York, New York.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">État de New York</region></placeName><wicri:cityArea>Developmental Biology Program, Memorial Sloan Kettering Cancer Center, New York</wicri:cityArea></affiliation></author><author><name sortKey="Kass, Elizabeth M" sort="Kass, Elizabeth M" uniqKey="Kass E" first="Elizabeth M" last="Kass">Elizabeth M. Kass</name><affiliation wicri:level="2"><nlm:affiliation>Developmental Biology Program, Memorial Sloan Kettering Cancer Center, New York, New York.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">État de New York</region></placeName><wicri:cityArea>Developmental Biology Program, Memorial Sloan Kettering Cancer Center, New York</wicri:cityArea></affiliation></author><author><name sortKey="Sullivan, Meghan R" sort="Sullivan, Meghan R" uniqKey="Sullivan M" first="Meghan R" last="Sullivan">Meghan R. Sullivan</name><affiliation wicri:level="2"><nlm:affiliation>Department of Microbiology and Molecular Genetics, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Pennsylvanie</region></placeName><wicri:cityArea>Department of Microbiology and Molecular Genetics, University of Pittsburgh School of Medicine, Pittsburgh</wicri:cityArea></affiliation></author><author><name sortKey="Brunette, Gregory J" sort="Brunette, Gregory J" uniqKey="Brunette G" first="Gregory J" last="Brunette">Gregory J. Brunette</name><affiliation wicri:level="2"><nlm:affiliation>Department of Microbiology and Molecular Genetics, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Pennsylvanie</region></placeName><wicri:cityArea>Department of Microbiology and Molecular Genetics, University of Pittsburgh School of Medicine, Pittsburgh</wicri:cityArea></affiliation></author><author><name sortKey="Bernstein, Kara A" sort="Bernstein, Kara A" uniqKey="Bernstein K" first="Kara A" last="Bernstein">Kara A. Bernstein</name><affiliation wicri:level="2"><nlm:affiliation>Department of Microbiology and Molecular Genetics, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Pennsylvanie</region></placeName><wicri:cityArea>Department of Microbiology and Molecular Genetics, University of Pittsburgh School of Medicine, Pittsburgh</wicri:cityArea></affiliation></author><author><name sortKey="Coleman, Robert L" sort="Coleman, Robert L" uniqKey="Coleman R" first="Robert L" last="Coleman">Robert L. Coleman</name><affiliation wicri:level="2"><nlm:affiliation>The University of Texas MD Anderson Cancer Center, Houston, Texas.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Texas</region></placeName><wicri:cityArea>The University of Texas MD Anderson Cancer Center, Houston</wicri:cityArea></affiliation></author><author><name sortKey="Floquet, Anne" sort="Floquet, Anne" uniqKey="Floquet A" first="Anne" last="Floquet">Anne Floquet</name><affiliation wicri:level="3"><nlm:affiliation>Institut Bergonié, Bordeaux, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Institut Bergonié, Bordeaux</wicri:regionArea><placeName><region type="region">Nouvelle-Aquitaine</region><region type="old region">Aquitaine</region><settlement type="city">Bordeaux</settlement></placeName></affiliation></author><author><name sortKey="Friedlander, Michael" sort="Friedlander, Michael" uniqKey="Friedlander M" first="Michael" last="Friedlander">Michael Friedlander</name><affiliation wicri:level="1"><nlm:affiliation>University of New South Wales and Prince of Wales Hospital, Sydney, New South Wales, Australia.</nlm:affiliation><country xml:lang="fr">Australie</country><wicri:regionArea>University of New South Wales and Prince of Wales Hospital, Sydney, New South Wales</wicri:regionArea><wicri:noRegion>New South Wales</wicri:noRegion></affiliation></author><author><name sortKey="Kichenadasse, Ganessan" sort="Kichenadasse, Ganessan" uniqKey="Kichenadasse G" first="Ganessan" last="Kichenadasse">Ganessan Kichenadasse</name><affiliation wicri:level="1"><nlm:affiliation>Flinders University, Adelaide, South Australia, Australia.</nlm:affiliation><country xml:lang="fr">Australie</country><wicri:regionArea>Flinders University, Adelaide, South Australia</wicri:regionArea><wicri:noRegion>South Australia</wicri:noRegion></affiliation></author><author><name sortKey="O Malley, David M" sort="O Malley, David M" uniqKey="O Malley D" first="David M" last="O'Malley">David M. O'Malley</name><affiliation wicri:level="2"><nlm:affiliation>The Ohio State University, James Cancer Center, Columbus, Ohio.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Ohio</region></placeName><wicri:cityArea>The Ohio State University, James Cancer Center, Columbus</wicri:cityArea></affiliation></author><author><name sortKey="Oza, Amit" sort="Oza, Amit" uniqKey="Oza A" first="Amit" last="Oza">Amit Oza</name><affiliation wicri:level="1"><nlm:affiliation>Princess Margaret Cancer Centre, University Health Network, Toronto, Ontario, Canada.</nlm:affiliation><country xml:lang="fr">Canada</country><wicri:regionArea>Princess Margaret Cancer Centre, University Health Network, Toronto, Ontario</wicri:regionArea><wicri:noRegion>Ontario</wicri:noRegion></affiliation></author><author><name sortKey="Sun, James" sort="Sun, James" uniqKey="Sun J" first="James" last="Sun">James Sun</name><affiliation wicri:level="2"><nlm:affiliation>Foundation Medicine, Inc., Cambridge, Massachusetts.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Massachusetts</region></placeName><wicri:cityArea>Foundation Medicine, Inc., Cambridge</wicri:cityArea></affiliation></author><author><name sortKey="Robillard, Liliane" sort="Robillard, Liliane" uniqKey="Robillard L" first="Liliane" last="Robillard">Liliane Robillard</name><affiliation wicri:level="2"><nlm:affiliation>Clovis Oncology, Inc., Boulder, Colorado.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Colorado</region></placeName><wicri:cityArea>Clovis Oncology, Inc., Boulder</wicri:cityArea></affiliation></author><author><name sortKey="Maloney, Lara" sort="Maloney, Lara" uniqKey="Maloney L" first="Lara" last="Maloney">Lara Maloney</name><affiliation wicri:level="2"><nlm:affiliation>Clovis Oncology, Inc., Boulder, Colorado.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Colorado</region></placeName><wicri:cityArea>Clovis Oncology, Inc., Boulder</wicri:cityArea></affiliation></author><author><name sortKey="Bowtell, David" sort="Bowtell, David" uniqKey="Bowtell D" first="David" last="Bowtell">David Bowtell</name></author><author><name sortKey="Giordano, Heidi" sort="Giordano, Heidi" uniqKey="Giordano H" first="Heidi" last="Giordano">Heidi Giordano</name><affiliation wicri:level="2"><nlm:affiliation>Clovis Oncology, Inc., Boulder, Colorado.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Colorado</region></placeName><wicri:cityArea>Clovis Oncology, Inc., Boulder</wicri:cityArea></affiliation></author><author><name sortKey="Wakefield, Matthew J" sort="Wakefield, Matthew J" uniqKey="Wakefield M" first="Matthew J" last="Wakefield">Matthew J. Wakefield</name><affiliation wicri:level="1"><nlm:affiliation>Walter and Eliza Hall Institute of Medical Research, Melbourne, Victoria, Australia.</nlm:affiliation><country xml:lang="fr">Australie</country><wicri:regionArea>Walter and Eliza Hall Institute of Medical Research, Melbourne, Victoria</wicri:regionArea><wicri:noRegion>Victoria</wicri:noRegion></affiliation></author><author><name sortKey="Kaufmann, Scott H" sort="Kaufmann, Scott H" uniqKey="Kaufmann S" first="Scott H" last="Kaufmann">Scott H. Kaufmann</name><affiliation wicri:level="2"><nlm:affiliation>Mayo Clinic Cancer Center, Rochester, Minnesota.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Minnesota</region></placeName><wicri:cityArea>Mayo Clinic Cancer Center, Rochester</wicri:cityArea></affiliation></author><author><name sortKey="Simmons, Andrew D" sort="Simmons, Andrew D" uniqKey="Simmons A" first="Andrew D" last="Simmons">Andrew D. Simmons</name><affiliation wicri:level="2"><nlm:affiliation>Clovis Oncology, Inc., Boulder, Colorado.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Colorado</region></placeName><wicri:cityArea>Clovis Oncology, Inc., Boulder</wicri:cityArea></affiliation></author><author><name sortKey="Harding, Thomas C" sort="Harding, Thomas C" uniqKey="Harding T" first="Thomas C" last="Harding">Thomas C. Harding</name><affiliation wicri:level="2"><nlm:affiliation>Clovis Oncology, Inc., Boulder, Colorado.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Colorado</region></placeName><wicri:cityArea>Clovis Oncology, Inc., Boulder</wicri:cityArea></affiliation></author><author><name sortKey="Raponi, Mitch" sort="Raponi, Mitch" uniqKey="Raponi M" first="Mitch" last="Raponi">Mitch Raponi</name><affiliation wicri:level="2"><nlm:affiliation>Clovis Oncology, Inc., Boulder, Colorado.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Colorado</region></placeName><wicri:cityArea>Clovis Oncology, Inc., Boulder</wicri:cityArea></affiliation></author><author><name sortKey="Mcneish, Iain A" sort="Mcneish, Iain A" uniqKey="Mcneish I" first="Iain A" last="Mcneish">Iain A. Mcneish</name><affiliation wicri:level="4"><nlm:affiliation>Institute of Cancer Sciences, University of Glasgow, Glasgow, United Kingdom.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Institute of Cancer Sciences, University of Glasgow, Glasgow</wicri:regionArea><orgName type="university">Université de Glasgow</orgName><placeName><settlement type="city">Glasgow</settlement><region type="country">Écosse</region></placeName></affiliation></author><author><name sortKey="Swisher, Elizabeth M" sort="Swisher, Elizabeth M" uniqKey="Swisher E" first="Elizabeth M" last="Swisher">Elizabeth M. Swisher</name><affiliation wicri:level="2"><nlm:affiliation>University of Washington, Seattle, Washington.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Washington (État)</region></placeName><wicri:cityArea>University of Washington, Seattle</wicri:cityArea></affiliation></author><author><name sortKey="Lin, Kevin K" sort="Lin, Kevin K" uniqKey="Lin K" first="Kevin K" last="Lin">Kevin K. Lin</name><affiliation wicri:level="2"><nlm:affiliation>Clovis Oncology, Inc., Boulder, Colorado.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Colorado</region></placeName><wicri:cityArea>Clovis Oncology, Inc., Boulder</wicri:cityArea></affiliation></author><author><name sortKey="Scott, Clare L" sort="Scott, Clare L" uniqKey="Scott C" first="Clare L" last="Scott">Clare L. Scott</name><affiliation wicri:level="1"><nlm:affiliation>Walter and Eliza Hall Institute of Medical Research, Melbourne, Victoria, Australia. scottc@wehi.edu.au.</nlm:affiliation><country xml:lang="fr">Australie</country><wicri:regionArea>Walter and Eliza Hall Institute of Medical Research, Melbourne, Victoria</wicri:regionArea><wicri:noRegion>Victoria</wicri:noRegion></affiliation></author></analytic><series><title level="j">Cancer discovery</title><idno type="eISSN">2159-8290</idno><imprint><date when="2017" type="published">2017</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">High-grade epithelial ovarian carcinomas containing mutated BRCA1 or BRCA2 (BRCA1/2) homologous recombination (HR) genes are sensitive to platinum-based chemotherapy and PARP inhibitors (PARPi), while restoration of HR function due to secondary mutations in BRCA1/2 has been recognized as an important resistance mechanism. We sequenced core HR pathway genes in 12 pairs of pretreatment and postprogression tumor biopsy samples collected from patients in ARIEL2 Part 1, a phase II study of the PARPi rucaparib as treatment for platinum-sensitive, relapsed ovarian carcinoma. In 6 of 12 pretreatment biopsies, a truncation mutation in BRCA1, RAD51C, or RAD51D was identified. In five of six paired postprogression biopsies, one or more secondary mutations restored the open reading frame. Four distinct secondary mutations and spatial heterogeneity were observed for RAD51CIn vitro complementation assays and a patient-derived xenograft, as well as predictive molecular modeling, confirmed that resistance to rucaparib was associated with secondary mutations.Significance: Analyses of primary and secondary mutations in RAD51C and RAD51D provide evidence for these primary mutations in conferring PARPi sensitivity and secondary mutations as a mechanism of acquired PARPi resistance. PARPi resistance due to secondary mutations underpins the need for early delivery of PARPi therapy and for combination strategies. Cancer Discov; 7(9); 984-98. ©2017 AACR.See related commentary by Domchek, p. 937See related article by Quigley et al., p. 999See related article by Goodall et al., p. 1006This article is highlighted in the In This Issue feature, p. 920.</div></front></TEI><pubmed><MedlineCitation Status="In-Process" Owner="NLM"><PMID Version="1">28588062</PMID><DateCreated><Year>2017</Year><Month>06</Month><Day>07</Day></DateCreated><DateRevised><Year>2017</Year><Month>09</Month><Day>27</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">2159-8290</ISSN><JournalIssue CitedMedium="Internet"><Volume>7</Volume><Issue>9</Issue><PubDate><Year>2017</Year><Month>Sep</Month></PubDate></JournalIssue><Title>Cancer discovery</Title><ISOAbbreviation>Cancer Discov</ISOAbbreviation></Journal><ArticleTitle>Secondary Somatic Mutations Restoring RAD51C and RAD51D Associated with Acquired Resistance to the PARP Inhibitor Rucaparib in High-Grade Ovarian Carcinoma.</ArticleTitle><Pagination><MedlinePgn>984-998</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1158/2159-8290.CD-17-0419</ELocationID><Abstract><AbstractText>High-grade epithelial ovarian carcinomas containing mutated BRCA1 or BRCA2 (BRCA1/2) homologous recombination (HR) genes are sensitive to platinum-based chemotherapy and PARP inhibitors (PARPi), while restoration of HR function due to secondary mutations in BRCA1/2 has been recognized as an important resistance mechanism. We sequenced core HR pathway genes in 12 pairs of pretreatment and postprogression tumor biopsy samples collected from patients in ARIEL2 Part 1, a phase II study of the PARPi rucaparib as treatment for platinum-sensitive, relapsed ovarian carcinoma. In 6 of 12 pretreatment biopsies, a truncation mutation in BRCA1, RAD51C, or RAD51D was identified. In five of six paired postprogression biopsies, one or more secondary mutations restored the open reading frame. Four distinct secondary mutations and spatial heterogeneity were observed for RAD51CIn vitro complementation assays and a patient-derived xenograft, as well as predictive molecular modeling, confirmed that resistance to rucaparib was associated with secondary mutations.Significance: Analyses of primary and secondary mutations in RAD51C and RAD51D provide evidence for these primary mutations in conferring PARPi sensitivity and secondary mutations as a mechanism of acquired PARPi resistance. PARPi resistance due to secondary mutations underpins the need for early delivery of PARPi therapy and for combination strategies. Cancer Discov; 7(9); 984-98. ©2017 AACR.See related commentary by Domchek, p. 937See related article by Quigley et al., p. 999See related article by Goodall et al., p. 1006This article is highlighted in the In This Issue feature, p. 920.</AbstractText><CopyrightInformation>©2017 American Association for Cancer Research.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Kondrashova</LastName><ForeName>Olga</ForeName><Initials>O</Initials><AffiliationInfo><Affiliation>Walter and Eliza Hall Institute of Medical Research, Melbourne, Victoria, Australia.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Medical Biology, The University of Melbourne, Melbourne, Victoria, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Nguyen</LastName><ForeName>Minh</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>Clovis Oncology, Inc., Boulder, Colorado.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Shield-Artin</LastName><ForeName>Kristy</ForeName><Initials>K</Initials><AffiliationInfo><Affiliation>Walter and Eliza Hall Institute of Medical Research, Melbourne, Victoria, Australia.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Medical Biology, The University of Melbourne, Melbourne, Victoria, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Tinker</LastName><ForeName>Anna V</ForeName><Initials>AV</Initials><AffiliationInfo><Affiliation>British Columbia Cancer Agency, Vancouver, British Columbia, Canada.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Teng</LastName><ForeName>Nelson N H</ForeName><Initials>NNH</Initials><AffiliationInfo><Affiliation>Stanford University, Palo Alto, California.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Harrell</LastName><ForeName>Maria I</ForeName><Initials>MI</Initials><AffiliationInfo><Affiliation>University of Washington, Seattle, Washington.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kuiper</LastName><ForeName>Michael J</ForeName><Initials>MJ</Initials><AffiliationInfo><Affiliation>Melbourne Bioinformatics, The University of Melbourne, Melbourne, Victoria, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Ho</LastName><ForeName>Gwo-Yaw</ForeName><Initials>GY</Initials><AffiliationInfo><Affiliation>Walter and Eliza Hall Institute of Medical Research, Melbourne, Victoria, Australia.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Medical Biology, The University of Melbourne, Melbourne, Victoria, Australia.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Medical Oncology, Peter MacCallum Cancer Centre, Melbourne, Victoria, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Barker</LastName><ForeName>Holly</ForeName><Initials>H</Initials><AffiliationInfo><Affiliation>Walter and Eliza Hall Institute of Medical Research, Melbourne, Victoria, Australia.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Medical Biology, The University of Melbourne, Melbourne, Victoria, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Jasin</LastName><ForeName>Maria</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>Developmental Biology Program, Memorial Sloan Kettering Cancer Center, New York, New York.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Prakash</LastName><ForeName>Rohit</ForeName><Initials>R</Initials><AffiliationInfo><Affiliation>Developmental Biology Program, Memorial Sloan Kettering Cancer Center, New York, New York.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kass</LastName><ForeName>Elizabeth M</ForeName><Initials>EM</Initials><AffiliationInfo><Affiliation>Developmental Biology Program, Memorial Sloan Kettering Cancer Center, New York, New York.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Sullivan</LastName><ForeName>Meghan R</ForeName><Initials>MR</Initials><AffiliationInfo><Affiliation>Department of Microbiology and Molecular Genetics, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Brunette</LastName><ForeName>Gregory J</ForeName><Initials>GJ</Initials><AffiliationInfo><Affiliation>Department of Microbiology and Molecular Genetics, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Bernstein</LastName><ForeName>Kara A</ForeName><Initials>KA</Initials><AffiliationInfo><Affiliation>Department of Microbiology and Molecular Genetics, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Coleman</LastName><ForeName>Robert L</ForeName><Initials>RL</Initials><AffiliationInfo><Affiliation>The University of Texas MD Anderson Cancer Center, Houston, Texas.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Floquet</LastName><ForeName>Anne</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Institut Bergonié, Bordeaux, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Friedlander</LastName><ForeName>Michael</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>University of New South Wales and Prince of Wales Hospital, Sydney, New South Wales, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kichenadasse</LastName><ForeName>Ganessan</ForeName><Initials>G</Initials><AffiliationInfo><Affiliation>Flinders University, Adelaide, South Australia, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>O'Malley</LastName><ForeName>David M</ForeName><Initials>DM</Initials><AffiliationInfo><Affiliation>The Ohio State University, James Cancer Center, Columbus, Ohio.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Oza</LastName><ForeName>Amit</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Princess Margaret Cancer Centre, University Health Network, Toronto, Ontario, Canada.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Sun</LastName><ForeName>James</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Foundation Medicine, Inc., Cambridge, Massachusetts.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Robillard</LastName><ForeName>Liliane</ForeName><Initials>L</Initials><AffiliationInfo><Affiliation>Clovis Oncology, Inc., Boulder, Colorado.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Maloney</LastName><ForeName>Lara</ForeName><Initials>L</Initials><AffiliationInfo><Affiliation>Clovis Oncology, Inc., Boulder, Colorado.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Bowtell</LastName><ForeName>David</ForeName><Initials>D</Initials></Author><Author ValidYN="Y"><LastName>Giordano</LastName><ForeName>Heidi</ForeName><Initials>H</Initials><AffiliationInfo><Affiliation>Clovis Oncology, Inc., Boulder, Colorado.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wakefield</LastName><ForeName>Matthew J</ForeName><Initials>MJ</Initials><AffiliationInfo><Affiliation>Walter and Eliza Hall Institute of Medical Research, Melbourne, Victoria, Australia.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Melbourne Bioinformatics, The University of Melbourne, Melbourne, Victoria, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kaufmann</LastName><ForeName>Scott H</ForeName><Initials>SH</Initials><AffiliationInfo><Affiliation>Mayo Clinic Cancer Center, Rochester, Minnesota.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Simmons</LastName><ForeName>Andrew D</ForeName><Initials>AD</Initials><AffiliationInfo><Affiliation>Clovis Oncology, Inc., Boulder, Colorado.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Harding</LastName><ForeName>Thomas C</ForeName><Initials>TC</Initials><AffiliationInfo><Affiliation>Clovis Oncology, Inc., Boulder, Colorado.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Raponi</LastName><ForeName>Mitch</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>Clovis Oncology, Inc., Boulder, Colorado.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>McNeish</LastName><ForeName>Iain A</ForeName><Initials>IA</Initials><AffiliationInfo><Affiliation>Institute of Cancer Sciences, University of Glasgow, Glasgow, United Kingdom.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Swisher</LastName><ForeName>Elizabeth M</ForeName><Initials>EM</Initials><AffiliationInfo><Affiliation>University of Washington, Seattle, Washington.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Lin</LastName><ForeName>Kevin K</ForeName><Initials>KK</Initials><AffiliationInfo><Affiliation>Clovis Oncology, Inc., Boulder, Colorado.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Scott</LastName><ForeName>Clare L</ForeName><Initials>CL</Initials><AffiliationInfo><Affiliation>Walter and Eliza Hall Institute of Medical Research, Melbourne, Victoria, Australia. scottc@wehi.edu.au.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Medical Biology, The University of Melbourne, Melbourne, Victoria, Australia.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Medical Oncology, Peter MacCallum Cancer Centre, Melbourne, Victoria, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><CollectiveName>AOCS Study Group</CollectiveName></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>F32 GM110978</GrantID><Acronym>GM</Acronym><Agency>NIGMS NIH HHS</Agency><Country>United States</Country></Grant><Grant><GrantID>R01 CA185660</GrantID><Acronym>CA</Acronym><Agency>NCI NIH HHS</Agency><Country>United States</Country></Grant><Grant><GrantID>R01 ES024872</GrantID><Acronym>ES</Acronym><Agency>NIEHS NIH HHS</Agency><Country>United States</Country></Grant><Grant><GrantID>P50 CA083636</GrantID><Acronym>CA</Acronym><Agency>NCI NIH HHS</Agency><Country>United States</Country></Grant><Grant><GrantID>P30 CA008748</GrantID><Acronym>CA</Acronym><Agency>NCI NIH HHS</Agency><Country>United States</Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate 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PubStatus="pubmed"><Year>2017</Year><Month>6</Month><Day>8</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2017</Year><Month>6</Month><Day>8</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2017</Year><Month>6</Month><Day>8</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>ppublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">28588062</ArticleId><ArticleId IdType="pii">2159-8290.CD-17-0419</ArticleId><ArticleId IdType="doi">10.1158/2159-8290.CD-17-0419</ArticleId><ArticleId IdType="pmc">PMC5612362</ArticleId><ArticleId IdType="mid">NIHMS904258</ArticleId></ArticleIdList></PubmedData></pubmed><affiliations><list><country><li>Australie</li><li>Canada</li><li>France</li><li>Royaume-Uni</li><li>États-Unis</li></country><region><li>Aquitaine</li><li>Californie</li><li>Colorado</li><li>Massachusetts</li><li>Minnesota</li><li>Nouvelle-Aquitaine</li><li>Ohio</li><li>Pennsylvanie</li><li>Texas</li><li>Victoria (État)</li><li>Washington (État)</li><li>Écosse</li><li>État de New York</li></region><settlement><li>Bordeaux</li><li>Glasgow</li><li>Melbourne</li></settlement><orgName><li>Université de Glasgow</li><li>Université de Melbourne</li></orgName></list><tree><noCountry><name sortKey="Bowtell, David" sort="Bowtell, David" uniqKey="Bowtell D" first="David" last="Bowtell">David Bowtell</name></noCountry><country name="Australie"><noRegion><name sortKey="Kondrashova, Olga" sort="Kondrashova, Olga" uniqKey="Kondrashova O" first="Olga" last="Kondrashova">Olga Kondrashova</name></noRegion><name sortKey="Barker, Holly" sort="Barker, Holly" uniqKey="Barker H" first="Holly" last="Barker">Holly Barker</name><name sortKey="Friedlander, Michael" sort="Friedlander, Michael" uniqKey="Friedlander M" first="Michael" last="Friedlander">Michael Friedlander</name><name sortKey="Ho, Gwo Yaw" sort="Ho, Gwo Yaw" uniqKey="Ho G" first="Gwo-Yaw" last="Ho">Gwo-Yaw Ho</name><name sortKey="Kichenadasse, Ganessan" sort="Kichenadasse, Ganessan" uniqKey="Kichenadasse G" first="Ganessan" last="Kichenadasse">Ganessan Kichenadasse</name><name sortKey="Kuiper, Michael J" sort="Kuiper, Michael J" uniqKey="Kuiper M" first="Michael J" last="Kuiper">Michael J. Kuiper</name><name sortKey="Scott, Clare L" sort="Scott, Clare L" uniqKey="Scott C" first="Clare L" last="Scott">Clare L. Scott</name><name sortKey="Shield Artin, Kristy" sort="Shield Artin, Kristy" uniqKey="Shield Artin K" first="Kristy" last="Shield-Artin">Kristy Shield-Artin</name><name sortKey="Wakefield, Matthew J" sort="Wakefield, Matthew J" uniqKey="Wakefield M" first="Matthew J" last="Wakefield">Matthew J. Wakefield</name></country><country name="États-Unis"><region name="Colorado"><name sortKey="Nguyen, Minh" sort="Nguyen, Minh" uniqKey="Nguyen M" first="Minh" last="Nguyen">Minh Nguyen</name></region><name sortKey="Bernstein, Kara A" sort="Bernstein, Kara A" uniqKey="Bernstein K" first="Kara A" last="Bernstein">Kara A. Bernstein</name><name sortKey="Brunette, Gregory J" sort="Brunette, Gregory J" uniqKey="Brunette G" first="Gregory J" last="Brunette">Gregory J. Brunette</name><name sortKey="Coleman, Robert L" sort="Coleman, Robert L" uniqKey="Coleman R" first="Robert L" last="Coleman">Robert L. Coleman</name><name sortKey="Giordano, Heidi" sort="Giordano, Heidi" uniqKey="Giordano H" first="Heidi" last="Giordano">Heidi Giordano</name><name sortKey="Harding, Thomas C" sort="Harding, Thomas C" uniqKey="Harding T" first="Thomas C" last="Harding">Thomas C. Harding</name><name sortKey="Harrell, Maria I" sort="Harrell, Maria I" uniqKey="Harrell M" first="Maria I" last="Harrell">Maria I. Harrell</name><name sortKey="Jasin, Maria" sort="Jasin, Maria" uniqKey="Jasin M" first="Maria" last="Jasin">Maria Jasin</name><name sortKey="Kass, Elizabeth M" sort="Kass, Elizabeth M" uniqKey="Kass E" first="Elizabeth M" last="Kass">Elizabeth M. Kass</name><name sortKey="Kaufmann, Scott H" sort="Kaufmann, Scott H" uniqKey="Kaufmann S" first="Scott H" last="Kaufmann">Scott H. Kaufmann</name><name sortKey="Lin, Kevin K" sort="Lin, Kevin K" uniqKey="Lin K" first="Kevin K" last="Lin">Kevin K. Lin</name><name sortKey="Maloney, Lara" sort="Maloney, Lara" uniqKey="Maloney L" first="Lara" last="Maloney">Lara Maloney</name><name sortKey="O Malley, David M" sort="O Malley, David M" uniqKey="O Malley D" first="David M" last="O'Malley">David M. O'Malley</name><name sortKey="Prakash, Rohit" sort="Prakash, Rohit" uniqKey="Prakash R" first="Rohit" last="Prakash">Rohit Prakash</name><name sortKey="Raponi, Mitch" sort="Raponi, Mitch" uniqKey="Raponi M" first="Mitch" last="Raponi">Mitch Raponi</name><name sortKey="Robillard, Liliane" sort="Robillard, Liliane" uniqKey="Robillard L" first="Liliane" last="Robillard">Liliane Robillard</name><name sortKey="Simmons, Andrew D" sort="Simmons, Andrew D" uniqKey="Simmons A" first="Andrew D" last="Simmons">Andrew D. Simmons</name><name sortKey="Sullivan, Meghan R" sort="Sullivan, Meghan R" uniqKey="Sullivan M" first="Meghan R" last="Sullivan">Meghan R. Sullivan</name><name sortKey="Sun, James" sort="Sun, James" uniqKey="Sun J" first="James" last="Sun">James Sun</name><name sortKey="Swisher, Elizabeth M" sort="Swisher, Elizabeth M" uniqKey="Swisher E" first="Elizabeth M" last="Swisher">Elizabeth M. Swisher</name><name sortKey="Teng, Nelson N H" sort="Teng, Nelson N H" uniqKey="Teng N" first="Nelson N H" last="Teng">Nelson N H. Teng</name></country><country name="Canada"><noRegion><name sortKey="Tinker, Anna V" sort="Tinker, Anna V" uniqKey="Tinker A" first="Anna V" last="Tinker">Anna V. Tinker</name></noRegion><name sortKey="Oza, Amit" sort="Oza, Amit" uniqKey="Oza A" first="Amit" last="Oza">Amit Oza</name></country><country name="France"><region name="Nouvelle-Aquitaine"><name sortKey="Floquet, Anne" sort="Floquet, Anne" uniqKey="Floquet A" first="Anne" last="Floquet">Anne Floquet</name></region></country><country name="Royaume-Uni"><region name="Écosse"><name sortKey="Mcneish, Iain A" sort="Mcneish, Iain A" uniqKey="Mcneish I" first="Iain A" last="Mcneish">Iain A. Mcneish</name></region></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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