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Personalized In Vitro and In Vivo Cancer Models to Guide Precision Medicine

Chantal Pauli, Benjamin D. Hopkins, Davide Prandi, Reid Shaw, Tarcisio Fedrizzi, Andrea Sboner, Verena Sailer, Michael Augello, Loredana Puca, Rachele Rosati, Terra J. McNary, Yelena Churakova, Cynthia Cheung, Joanna Triscott, David Pisapia, Rema Rao, Juan Miguel Mosquera, Brian Robinson, Bishoy M. Faltas, Brooke E. Emerling, Vijayakrishna K. Gadi, Brady Bernard, Olivier Elemento, Himisha Beltran, Francesca Demichelis, Christopher J. Kemp, Carla Grandori, Lewis C. Cantley and Mark A. Rubin
Chantal Pauli
1Englander Institute for Precision Medicine, Weill Cornell Medicine-New York Presbyterian Hospital, New York, New York.
2Department of Pathology and Laboratory Medicine, Weill Cornell Medicine, New York, New York.
3Institute of Pathology and Molecular Pathology, University Hospital Zurich, Zurich, Switzerland.
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Benjamin D. Hopkins
4Meyer Cancer Center, Weill Cornell Medicine, New York, New York.
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Davide Prandi
5Center for Integrative Biology, University of Trento, Trento, Italy.
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Reid Shaw
6Cure First and SEngine Precision Medicine, Seattle, Washington.
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Tarcisio Fedrizzi
5Center for Integrative Biology, University of Trento, Trento, Italy.
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Andrea Sboner
1Englander Institute for Precision Medicine, Weill Cornell Medicine-New York Presbyterian Hospital, New York, New York.
4Meyer Cancer Center, Weill Cornell Medicine, New York, New York.
7Institute for Computational Biomedicine, Weill Cornell Medicine, New York, New York.
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Verena Sailer
1Englander Institute for Precision Medicine, Weill Cornell Medicine-New York Presbyterian Hospital, New York, New York.
2Department of Pathology and Laboratory Medicine, Weill Cornell Medicine, New York, New York.
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Michael Augello
1Englander Institute for Precision Medicine, Weill Cornell Medicine-New York Presbyterian Hospital, New York, New York.
4Meyer Cancer Center, Weill Cornell Medicine, New York, New York.
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Loredana Puca
1Englander Institute for Precision Medicine, Weill Cornell Medicine-New York Presbyterian Hospital, New York, New York.
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Rachele Rosati
6Cure First and SEngine Precision Medicine, Seattle, Washington.
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Terra J. McNary
1Englander Institute for Precision Medicine, Weill Cornell Medicine-New York Presbyterian Hospital, New York, New York.
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Yelena Churakova
1Englander Institute for Precision Medicine, Weill Cornell Medicine-New York Presbyterian Hospital, New York, New York.
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Cynthia Cheung
1Englander Institute for Precision Medicine, Weill Cornell Medicine-New York Presbyterian Hospital, New York, New York.
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Joanna Triscott
1Englander Institute for Precision Medicine, Weill Cornell Medicine-New York Presbyterian Hospital, New York, New York.
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David Pisapia
1Englander Institute for Precision Medicine, Weill Cornell Medicine-New York Presbyterian Hospital, New York, New York.
2Department of Pathology and Laboratory Medicine, Weill Cornell Medicine, New York, New York.
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Rema Rao
1Englander Institute for Precision Medicine, Weill Cornell Medicine-New York Presbyterian Hospital, New York, New York.
2Department of Pathology and Laboratory Medicine, Weill Cornell Medicine, New York, New York.
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Juan Miguel Mosquera
1Englander Institute for Precision Medicine, Weill Cornell Medicine-New York Presbyterian Hospital, New York, New York.
2Department of Pathology and Laboratory Medicine, Weill Cornell Medicine, New York, New York.
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Brian Robinson
1Englander Institute for Precision Medicine, Weill Cornell Medicine-New York Presbyterian Hospital, New York, New York.
2Department of Pathology and Laboratory Medicine, Weill Cornell Medicine, New York, New York.
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Bishoy M. Faltas
1Englander Institute for Precision Medicine, Weill Cornell Medicine-New York Presbyterian Hospital, New York, New York.
8Department of Medicine, Division of Hematology and Medical Oncology, Weill Cornell Medicine, New York, New York.
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Brooke E. Emerling
4Meyer Cancer Center, Weill Cornell Medicine, New York, New York.
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Vijayakrishna K. Gadi
9Clinical Research Division, Fred Hutchinson Cancer Research Center, Seattle, Washington.
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Brady Bernard
6Cure First and SEngine Precision Medicine, Seattle, Washington.
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Olivier Elemento
1Englander Institute for Precision Medicine, Weill Cornell Medicine-New York Presbyterian Hospital, New York, New York.
4Meyer Cancer Center, Weill Cornell Medicine, New York, New York.
7Institute for Computational Biomedicine, Weill Cornell Medicine, New York, New York.
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Himisha Beltran
1Englander Institute for Precision Medicine, Weill Cornell Medicine-New York Presbyterian Hospital, New York, New York.
8Department of Medicine, Division of Hematology and Medical Oncology, Weill Cornell Medicine, New York, New York.
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Francesca Demichelis
1Englander Institute for Precision Medicine, Weill Cornell Medicine-New York Presbyterian Hospital, New York, New York.
5Center for Integrative Biology, University of Trento, Trento, Italy.
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Christopher J. Kemp
10Division of Human Biology, Fred Hutchinson Cancer Research Center, Seattle, Washington.
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Carla Grandori
6Cure First and SEngine Precision Medicine, Seattle, Washington.
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Lewis C. Cantley
4Meyer Cancer Center, Weill Cornell Medicine, New York, New York.
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Mark A. Rubin
1Englander Institute for Precision Medicine, Weill Cornell Medicine-New York Presbyterian Hospital, New York, New York.
2Department of Pathology and Laboratory Medicine, Weill Cornell Medicine, New York, New York.
4Meyer Cancer Center, Weill Cornell Medicine, New York, New York.
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  • For correspondence: rubinma@med.cornell.edu
DOI: 10.1158/2159-8290.CD-16-1154 Published May 2017
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Abstract

Precision medicine is an approach that takes into account the influence of individuals' genes, environment, and lifestyle exposures to tailor interventions. Here, we describe the development of a robust precision cancer care platform that integrates whole-exome sequencing with a living biobank that enables high-throughput drug screens on patient-derived tumor organoids. To date, 56 tumor-derived organoid cultures and 19 patient-derived xenograft (PDX) models have been established from the 769 patients enrolled in an Institutional Review Board–approved clinical trial. Because genomics alone was insufficient to identify therapeutic options for the majority of patients with advanced disease, we used high-throughput drug screening to discover effective treatment strategies. Analysis of tumor-derived cells from four cases, two uterine malignancies and two colon cancers, identified effective drugs and drug combinations that were subsequently validated using 3-D cultures and PDX models. This platform thereby promotes the discovery of novel therapeutic approaches that can be assessed in clinical trials and provides personalized therapeutic options for individual patients where standard clinical options have been exhausted.

Significance: Integration of genomic data with drug screening from personalized in vitro and in vivo cancer models guides precision cancer care and fuels next-generation research. Cancer Discov; 7(5); 462–77. ©2017 AACR.

See related commentary by Picco and Garnett, p. 456.

This article is highlighted in the In This Issue feature, p. 443

Footnotes

  • Note: Supplementary data for this article are available at Cancer Discovery Online (http://cancerdiscovery.aacrjournals.org/).

  • Received October 12, 2016.
  • Revision received January 30, 2017.
  • Accepted January 30, 2017.
  • ©2017 American Association for Cancer Research.
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Cancer Discovery: 7 (5)
May 2017
Volume 7, Issue 5
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Personalized In Vitro and In Vivo Cancer Models to Guide Precision Medicine
Chantal Pauli, Benjamin D. Hopkins, Davide Prandi, Reid Shaw, Tarcisio Fedrizzi, Andrea Sboner, Verena Sailer, Michael Augello, Loredana Puca, Rachele Rosati, Terra J. McNary, Yelena Churakova, Cynthia Cheung, Joanna Triscott, David Pisapia, Rema Rao, Juan Miguel Mosquera, Brian Robinson, Bishoy M. Faltas, Brooke E. Emerling, Vijayakrishna K. Gadi, Brady Bernard, Olivier Elemento, Himisha Beltran, Francesca Demichelis, Christopher J. Kemp, Carla Grandori, Lewis C. Cantley and Mark A. Rubin
Cancer Discov May 1 2017 (7) (5) 462-477; DOI: 10.1158/2159-8290.CD-16-1154

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Personalized In Vitro and In Vivo Cancer Models to Guide Precision Medicine
Chantal Pauli, Benjamin D. Hopkins, Davide Prandi, Reid Shaw, Tarcisio Fedrizzi, Andrea Sboner, Verena Sailer, Michael Augello, Loredana Puca, Rachele Rosati, Terra J. McNary, Yelena Churakova, Cynthia Cheung, Joanna Triscott, David Pisapia, Rema Rao, Juan Miguel Mosquera, Brian Robinson, Bishoy M. Faltas, Brooke E. Emerling, Vijayakrishna K. Gadi, Brady Bernard, Olivier Elemento, Himisha Beltran, Francesca Demichelis, Christopher J. Kemp, Carla Grandori, Lewis C. Cantley and Mark A. Rubin
Cancer Discov May 1 2017 (7) (5) 462-477; DOI: 10.1158/2159-8290.CD-16-1154
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