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Research Articles

Organoid Profiling Identifies Common Responders to Chemotherapy in Pancreatic Cancer

Hervé Tiriac, Pascal Belleau, Dannielle D. Engle, Dennis Plenker, Astrid Deschênes, Tim D. D. Somerville, Fieke E. M. Froeling, Richard A. Burkhart, Robert E. Denroche, Gun-Ho Jang, Koji Miyabayashi, C. Megan Young, Hardik Patel, Michelle Ma, Joseph F. LaComb, Randze Lerie D. Palmaira, Ammar A. Javed, Jasmine C. Huynh, Molly Johnson, Kanika Arora, Nicolas Robine, Minita Shah, Rashesh Sanghvi, Austin B. Goetz, Cinthya Y. Lowder, Laura Martello, Else Driehuis, Nicolas LeComte, Gokce Askan, Christine A. Iacobuzio-Donahue, Hans Clevers, Laura D. Wood, Ralph H. Hruban, Elizabeth Thompson, Andrew J. Aguirre, Brian M. Wolpin, Aaron Sasson, Joseph Kim, Maoxin Wu, Juan Carlos Bucobo, Peter Allen, Divyesh V. Sejpal, William Nealon, James D. Sullivan, Jordan M. Winter, Phyllis A. Gimotty, Jean L. Grem, Dominick J. DiMaio, Jonathan M. Buscaglia, Paul M. Grandgenett, Jonathan R. Brody, Michael A. Hollingsworth, Grainne M. O'Kane, Faiyaz Notta, Edward Kim, James M. Crawford, Craig Devoe, Allyson Ocean, Christopher L. Wolfgang, Kenneth H. Yu, Ellen Li, Christopher R. Vakoc, Benjamin Hubert, Sandra E. Fischer, Julie M. Wilson, Richard Moffitt, Jennifer Knox, Alexander Krasnitz, Steven Gallinger and David A. Tuveson
Hervé Tiriac
1Cold Spring Harbor Laboratory, Cold Spring Harbor, New York.
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Pascal Belleau
1Cold Spring Harbor Laboratory, Cold Spring Harbor, New York.
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Dannielle D. Engle
1Cold Spring Harbor Laboratory, Cold Spring Harbor, New York.
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  • ORCID record for Dannielle D. Engle
Dennis Plenker
1Cold Spring Harbor Laboratory, Cold Spring Harbor, New York.
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Astrid Deschênes
1Cold Spring Harbor Laboratory, Cold Spring Harbor, New York.
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Tim D. D. Somerville
1Cold Spring Harbor Laboratory, Cold Spring Harbor, New York.
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Fieke E. M. Froeling
1Cold Spring Harbor Laboratory, Cold Spring Harbor, New York.
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Richard A. Burkhart
2Johns Hopkins University, Division of Hepatobiliary and Pancreatic Surgery, Baltimore, Maryland.
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Robert E. Denroche
3PanCuRx Translational Research Initiative, Ontario Institute for Cancer Research, Toronto, Ontario, Canada.
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Gun-Ho Jang
3PanCuRx Translational Research Initiative, Ontario Institute for Cancer Research, Toronto, Ontario, Canada.
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Koji Miyabayashi
1Cold Spring Harbor Laboratory, Cold Spring Harbor, New York.
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C. Megan Young
1Cold Spring Harbor Laboratory, Cold Spring Harbor, New York.
4Swiss Federal Institute of Technology Lausanne (EPFL), School of Life Sciences, Swiss Institute for Experimental Cancer Research (ISREC), Laboratory of Tumor Heterogeneity and Stemness in Cancer, Lausanne, Switzerland.
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Hardik Patel
1Cold Spring Harbor Laboratory, Cold Spring Harbor, New York.
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Michelle Ma
1Cold Spring Harbor Laboratory, Cold Spring Harbor, New York.
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Joseph F. LaComb
5Department of Medicine, Stony Brook University, Stony Brook, New York.
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Randze Lerie D. Palmaira
6Memorial Sloan Kettering Cancer Center, New York, New York.
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Ammar A. Javed
2Johns Hopkins University, Division of Hepatobiliary and Pancreatic Surgery, Baltimore, Maryland.
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Jasmine C. Huynh
7University of California, Davis, Comprehensive Cancer Center, Division of Hematology and Oncology, Sacramento, California.
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Molly Johnson
8New York Genome Center, New York, New York.
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Kanika Arora
8New York Genome Center, New York, New York.
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Nicolas Robine
8New York Genome Center, New York, New York.
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Minita Shah
8New York Genome Center, New York, New York.
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Rashesh Sanghvi
8New York Genome Center, New York, New York.
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Austin B. Goetz
9Department of Surgery, Thomas Jefferson University, Philadelphia, Pennsylvania.
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Cinthya Y. Lowder
9Department of Surgery, Thomas Jefferson University, Philadelphia, Pennsylvania.
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Laura Martello
10SUNY Downstate Medical Center, Department of Medicine, New York, New York.
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Else Driehuis
11Hubrecht Institute, Royal Netherlands Academy of Arts and Sciences (KNAW), Utrecht, the Netherlands.
12University Medical Center (UMC), Utrecht, the Netherlands.
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Nicolas LeComte
6Memorial Sloan Kettering Cancer Center, New York, New York.
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Gokce Askan
6Memorial Sloan Kettering Cancer Center, New York, New York.
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Christine A. Iacobuzio-Donahue
6Memorial Sloan Kettering Cancer Center, New York, New York.
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Hans Clevers
11Hubrecht Institute, Royal Netherlands Academy of Arts and Sciences (KNAW), Utrecht, the Netherlands.
12University Medical Center (UMC), Utrecht, the Netherlands.
13Princess Maxime Center (PMC), Utrecht, the Netherlands.
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Laura D. Wood
14Department of Pathology, Johns Hopkins University, Baltimore, Maryland.
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Ralph H. Hruban
14Department of Pathology, Johns Hopkins University, Baltimore, Maryland.
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Elizabeth Thompson
14Department of Pathology, Johns Hopkins University, Baltimore, Maryland.
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Andrew J. Aguirre
15Dana-Farber Cancer Institute, Broad Institute, Boston, Massachusetts.
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Brian M. Wolpin
15Dana-Farber Cancer Institute, Broad Institute, Boston, Massachusetts.
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Aaron Sasson
16Department of Surgery, Stony Brook University, Stony Brook, New York.
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Joseph Kim
16Department of Surgery, Stony Brook University, Stony Brook, New York.
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Maoxin Wu
17Department of Pathology, Stony Brook University, Stony Brook, New York.
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Juan Carlos Bucobo
5Department of Medicine, Stony Brook University, Stony Brook, New York.
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Peter Allen
6Memorial Sloan Kettering Cancer Center, New York, New York.
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Divyesh V. Sejpal
18Donald and Barbara Zucker School of Medicine at Hofstra/Northwell, Division of Gastroenterology, Hempstead, New York.
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William Nealon
19Department of Surgery, Donald and Barbara Zucker School of Medicine at Hofstra/Northwell, Hempstead, New York.
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James D. Sullivan
19Department of Surgery, Donald and Barbara Zucker School of Medicine at Hofstra/Northwell, Hempstead, New York.
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Jordan M. Winter
9Department of Surgery, Thomas Jefferson University, Philadelphia, Pennsylvania.
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Phyllis A. Gimotty
20Department of Biostatistics, Epidemiology and Informatics, University of Pennsylvania, Philadelphia, Pennsylvania.
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Jean L. Grem
21Department of Medicine, University of Nebraska Medical Center, Omaha, Nebraska.
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Dominick J. DiMaio
22Department of Pathology and Microbiology, University of Nebraska Medical Center, Omaha, Nebraska.
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Jonathan M. Buscaglia
5Department of Medicine, Stony Brook University, Stony Brook, New York.
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Paul M. Grandgenett
23University of Nebraska Medical Center, Eppley Institute for Research in Cancer and Allied Diseases, Fred & Pamela Buffet Cancer Center, Omaha, Nebraska.
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Jonathan R. Brody
9Department of Surgery, Thomas Jefferson University, Philadelphia, Pennsylvania.
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Michael A. Hollingsworth
23University of Nebraska Medical Center, Eppley Institute for Research in Cancer and Allied Diseases, Fred & Pamela Buffet Cancer Center, Omaha, Nebraska.
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Grainne M. O'Kane
24Wallace McCain Centre for Pancreatic Cancer, Department of Medical Oncology, Princess Margaret Cancer Centre, University Health Network, University of Toronto, Toronto, Ontario, Canada.
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Faiyaz Notta
3PanCuRx Translational Research Initiative, Ontario Institute for Cancer Research, Toronto, Ontario, Canada.
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Edward Kim
7University of California, Davis, Comprehensive Cancer Center, Division of Hematology and Oncology, Sacramento, California.
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James M. Crawford
25Department of Pathology and Laboratory Medicine, Donald and Barbara Zucker School of Medicine at Hofstra/Northwell, Hempstead, New York.
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Craig Devoe
26Division of Medical Oncology, Donald and Barbara Zucker School of Medicine at Hofstra/Northwell, Hempstead, New York.
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Allyson Ocean
27Weill Cornell Medical College, New York, New York.
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Christopher L. Wolfgang
2Johns Hopkins University, Division of Hepatobiliary and Pancreatic Surgery, Baltimore, Maryland.
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Kenneth H. Yu
6Memorial Sloan Kettering Cancer Center, New York, New York.
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Ellen Li
5Department of Medicine, Stony Brook University, Stony Brook, New York.
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Christopher R. Vakoc
1Cold Spring Harbor Laboratory, Cold Spring Harbor, New York.
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Benjamin Hubert
8New York Genome Center, New York, New York.
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Sandra E. Fischer
28Department of Pathology, University Health Network, University of Toronto, Toronto, Ontario, Canada.
29Department of Laboratory Medicine and Pathobiology, University of Toronto, Toronto, Ontario, Canada.
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Julie M. Wilson
3PanCuRx Translational Research Initiative, Ontario Institute for Cancer Research, Toronto, Ontario, Canada.
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Richard Moffitt
16Department of Surgery, Stony Brook University, Stony Brook, New York.
30Department of Biomedical Informatics, Stony Brook University, Stony Brook, New York.
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Jennifer Knox
24Wallace McCain Centre for Pancreatic Cancer, Department of Medical Oncology, Princess Margaret Cancer Centre, University Health Network, University of Toronto, Toronto, Ontario, Canada.
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Alexander Krasnitz
1Cold Spring Harbor Laboratory, Cold Spring Harbor, New York.
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Steven Gallinger
3PanCuRx Translational Research Initiative, Ontario Institute for Cancer Research, Toronto, Ontario, Canada.
24Wallace McCain Centre for Pancreatic Cancer, Department of Medical Oncology, Princess Margaret Cancer Centre, University Health Network, University of Toronto, Toronto, Ontario, Canada.
31Lunenfeld-Tanenbaum Research Institute, Mount Sinai Hospital, Toronto, Ontario, Canada.
32Hepatobiliary/Pancreatic Surgical Oncology Program, University Health Network, Toronto, Ontario, Canada.
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  • For correspondence: dtuveson@cshl.edu steven.gallinger@uhn.ca
David A. Tuveson
1Cold Spring Harbor Laboratory, Cold Spring Harbor, New York.
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  • For correspondence: dtuveson@cshl.edu steven.gallinger@uhn.ca
DOI: 10.1158/2159-8290.CD-18-0349 Published September 2018
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Abstract

Pancreatic cancer is the most lethal common solid malignancy. Systemic therapies are often ineffective, and predictive biomarkers to guide treatment are urgently needed. We generated a pancreatic cancer patient–derived organoid (PDO) library that recapitulates the mutational spectrum and transcriptional subtypes of primary pancreatic cancer. New driver oncogenes were nominated and transcriptomic analyses revealed unique clusters. PDOs exhibited heterogeneous responses to standard-of-care chemotherapeutics and investigational agents. In a case study manner, we found that PDO therapeutic profiles paralleled patient outcomes and that PDOs enabled longitudinal assessment of chemosensitivity and evaluation of synchronous metastases. We derived organoid-based gene expression signatures of chemosensitivity that predicted improved responses for many patients to chemotherapy in both the adjuvant and advanced disease settings. Finally, we nominated alternative treatment strategies for chemorefractory PDOs using targeted agent therapeutic profiling. We propose that combined molecular and therapeutic profiling of PDOs may predict clinical response and enable prospective therapeutic selection.

Significance: New approaches to prioritize treatment strategies are urgently needed to improve survival and quality of life for patients with pancreatic cancer. Combined genomic, transcriptomic, and therapeutic profiling of PDOs can identify molecular and functional subtypes of pancreatic cancer, predict therapeutic responses, and facilitate precision medicine for patients with pancreatic cancer. Cancer Discov; 8(9); 1112–29. ©2018 AACR.

See related commentary by Collisson, p. 1062.

This article is highlighted in the In This Issue feature, p. 1047

Footnotes

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

  • Received March 30, 2018.
  • Revision received May 3, 2018.
  • Accepted May 25, 2018.
  • Published first May 31, 2018.
  • ©2018 American Association for Cancer Research.
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Cancer Discovery: 8 (9)
September 2018
Volume 8, Issue 9
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Organoid Profiling Identifies Common Responders to Chemotherapy in Pancreatic Cancer
Hervé Tiriac, Pascal Belleau, Dannielle D. Engle, Dennis Plenker, Astrid Deschênes, Tim D. D. Somerville, Fieke E. M. Froeling, Richard A. Burkhart, Robert E. Denroche, Gun-Ho Jang, Koji Miyabayashi, C. Megan Young, Hardik Patel, Michelle Ma, Joseph F. LaComb, Randze Lerie D. Palmaira, Ammar A. Javed, Jasmine C. Huynh, Molly Johnson, Kanika Arora, Nicolas Robine, Minita Shah, Rashesh Sanghvi, Austin B. Goetz, Cinthya Y. Lowder, Laura Martello, Else Driehuis, Nicolas LeComte, Gokce Askan, Christine A. Iacobuzio-Donahue, Hans Clevers, Laura D. Wood, Ralph H. Hruban, Elizabeth Thompson, Andrew J. Aguirre, Brian M. Wolpin, Aaron Sasson, Joseph Kim, Maoxin Wu, Juan Carlos Bucobo, Peter Allen, Divyesh V. Sejpal, William Nealon, James D. Sullivan, Jordan M. Winter, Phyllis A. Gimotty, Jean L. Grem, Dominick J. DiMaio, Jonathan M. Buscaglia, Paul M. Grandgenett, Jonathan R. Brody, Michael A. Hollingsworth, Grainne M. O'Kane, Faiyaz Notta, Edward Kim, James M. Crawford, Craig Devoe, Allyson Ocean, Christopher L. Wolfgang, Kenneth H. Yu, Ellen Li, Christopher R. Vakoc, Benjamin Hubert, Sandra E. Fischer, Julie M. Wilson, Richard Moffitt, Jennifer Knox, Alexander Krasnitz, Steven Gallinger and David A. Tuveson
Cancer Discov September 1 2018 (8) (9) 1112-1129; DOI: 10.1158/2159-8290.CD-18-0349

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Organoid Profiling Identifies Common Responders to Chemotherapy in Pancreatic Cancer
Hervé Tiriac, Pascal Belleau, Dannielle D. Engle, Dennis Plenker, Astrid Deschênes, Tim D. D. Somerville, Fieke E. M. Froeling, Richard A. Burkhart, Robert E. Denroche, Gun-Ho Jang, Koji Miyabayashi, C. Megan Young, Hardik Patel, Michelle Ma, Joseph F. LaComb, Randze Lerie D. Palmaira, Ammar A. Javed, Jasmine C. Huynh, Molly Johnson, Kanika Arora, Nicolas Robine, Minita Shah, Rashesh Sanghvi, Austin B. Goetz, Cinthya Y. Lowder, Laura Martello, Else Driehuis, Nicolas LeComte, Gokce Askan, Christine A. Iacobuzio-Donahue, Hans Clevers, Laura D. Wood, Ralph H. Hruban, Elizabeth Thompson, Andrew J. Aguirre, Brian M. Wolpin, Aaron Sasson, Joseph Kim, Maoxin Wu, Juan Carlos Bucobo, Peter Allen, Divyesh V. Sejpal, William Nealon, James D. Sullivan, Jordan M. Winter, Phyllis A. Gimotty, Jean L. Grem, Dominick J. DiMaio, Jonathan M. Buscaglia, Paul M. Grandgenett, Jonathan R. Brody, Michael A. Hollingsworth, Grainne M. O'Kane, Faiyaz Notta, Edward Kim, James M. Crawford, Craig Devoe, Allyson Ocean, Christopher L. Wolfgang, Kenneth H. Yu, Ellen Li, Christopher R. Vakoc, Benjamin Hubert, Sandra E. Fischer, Julie M. Wilson, Richard Moffitt, Jennifer Knox, Alexander Krasnitz, Steven Gallinger and David A. Tuveson
Cancer Discov September 1 2018 (8) (9) 1112-1129; DOI: 10.1158/2159-8290.CD-18-0349
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