Patient-derived organoids model treatment response of metastatic gastrointestinal cancers
Cancer organoids are miniature, three-dimensional cell culture models that can be made from primary patient tumors and studied in the laboratory. Vlachogiannis et al. asked whether such “tumor-in-a-dish” approaches can be used to predict drug responses in the clinic. They generated a live organoid b...
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| Published in | Science (American Association for the Advancement of Science) Vol. 359; no. 6378; pp. 920 - 926 |
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| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
The American Association for the Advancement of Science
23.02.2018
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| Subjects | |
| Online Access | Get full text |
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| Abstract | Cancer organoids are miniature, three-dimensional cell culture models that can be made from primary patient tumors and studied in the laboratory. Vlachogiannis
et al.
asked whether such “tumor-in-a-dish” approaches can be used to predict drug responses in the clinic. They generated a live organoid biobank from patients with metastatic gastrointestinal cancer who had previously been enrolled in phase I or II clinical trials. This allowed the authors to compare organoid drug responses with how the patient actually responded in the clinic. Encouragingly, the organoids had similar molecular profiles to those of the patient tumor, reinforcing their value as a platform for drug screening and development.
Science
, this issue p.
920
Organoids can recapitulate patient responses in the clinic, with potential for drug screening and personalized medicine.
Patient-derived organoids (PDOs) have recently emerged as robust preclinical models; however, their potential to predict clinical outcomes in patients has remained unclear. We report on a living biobank of PDOs from metastatic, heavily pretreated colorectal and gastroesophageal cancer patients recruited in phase 1/2 clinical trials. Phenotypic and genotypic profiling of PDOs showed a high degree of similarity to the original patient tumors. Molecular profiling of tumor organoids was matched to drug-screening results, suggesting that PDOs could complement existing approaches in defining cancer vulnerabilities and improving treatment responses. We compared responses to anticancer agents ex vivo in organoids and PDO-based orthotopic mouse tumor xenograft models with the responses of the patients in clinical trials. Our data suggest that PDOs can recapitulate patient responses in the clinic and could be implemented in personalized medicine programs. |
|---|---|
| AbstractList | Patient-derived organoids (PDOs) have recently emerged as robust pre-clinical models, however, their potential to predict patient clinical outcomes remain unclear. We report a living biobank of PDOs from metastatic, heavily-pretreated colorectal and gastroesophageal cancer patients recruited in phase I/II clinical trials. Phenotypic and genotypic profiling of PDOs showed a high-degree of similarity to the original patient tumor. Molecular profiling of tumor organoids was matched to drug screening results, suggesting PDOs could complement existing approaches in defining cancer vulnerabilities and improving treatment responses. We compared
ex vivo
organoid responses to anticancer agents, and PDO-based orthotopic mouse tumor xenograft models to the response of the patient in clinical trials. Our data suggest that PDOs can recapitulate patient responses in the clinic, and have the potential to be implemented in personalized medicine programs. Cancer organoids to model therapy responseCancer organoids are miniature, three-dimensional cell culture models that can be made from primary patient tumors and studied in the laboratory. Vlachogiannis et al. asked whether such “tumor-in-a-dish” approaches can be used to predict drug responses in the clinic. They generated a live organoid biobank from patients with metastatic gastrointestinal cancer who had previously been enrolled in phase I or II clinical trials. This allowed the authors to compare organoid drug responses with how the patient actually responded in the clinic. Encouragingly, the organoids had similar molecular profiles to those of the patient tumor, reinforcing their value as a platform for drug screening and development.Science, this issue p. 920Patient-derived organoids (PDOs) have recently emerged as robust preclinical models; however, their potential to predict clinical outcomes in patients has remained unclear. We report on a living biobank of PDOs from metastatic, heavily pretreated colorectal and gastroesophageal cancer patients recruited in phase 1/2 clinical trials. Phenotypic and genotypic profiling of PDOs showed a high degree of similarity to the original patient tumors. Molecular profiling of tumor organoids was matched to drug-screening results, suggesting that PDOs could complement existing approaches in defining cancer vulnerabilities and improving treatment responses. We compared responses to anticancer agents ex vivo in organoids and PDO-based orthotopic mouse tumor xenograft models with the responses of the patients in clinical trials. Our data suggest that PDOs can recapitulate patient responses in the clinic and could be implemented in personalized medicine programs. Patient-derived organoids (PDOs) have recently emerged as robust preclinical models; however, their potential to predict clinical outcomes in patients has remained unclear. We report on a living biobank of PDOs from metastatic, heavily pretreated colorectal and gastroesophageal cancer patients recruited in phase 1/2 clinical trials. Phenotypic and genotypic profiling of PDOs showed a high degree of similarity to the original patient tumors. Molecular profiling of tumor organoids was matched to drug-screening results, suggesting that PDOs could complement existing approaches in defining cancer vulnerabilities and improving treatment responses. We compared responses to anticancer agents ex vivo in organoids and PDO-based orthotopic mouse tumor xenograft models with the responses of the patients in clinical trials. Our data suggest that PDOs can recapitulate patient responses in the clinic and could be implemented in personalized medicine programs.Patient-derived organoids (PDOs) have recently emerged as robust preclinical models; however, their potential to predict clinical outcomes in patients has remained unclear. We report on a living biobank of PDOs from metastatic, heavily pretreated colorectal and gastroesophageal cancer patients recruited in phase 1/2 clinical trials. Phenotypic and genotypic profiling of PDOs showed a high degree of similarity to the original patient tumors. Molecular profiling of tumor organoids was matched to drug-screening results, suggesting that PDOs could complement existing approaches in defining cancer vulnerabilities and improving treatment responses. We compared responses to anticancer agents ex vivo in organoids and PDO-based orthotopic mouse tumor xenograft models with the responses of the patients in clinical trials. Our data suggest that PDOs can recapitulate patient responses in the clinic and could be implemented in personalized medicine programs. Cancer organoids are miniature, three-dimensional cell culture models that can be made from primary patient tumors and studied in the laboratory. Vlachogiannis et al. asked whether such “tumor-in-a-dish” approaches can be used to predict drug responses in the clinic. They generated a live organoid biobank from patients with metastatic gastrointestinal cancer who had previously been enrolled in phase I or II clinical trials. This allowed the authors to compare organoid drug responses with how the patient actually responded in the clinic. Encouragingly, the organoids had similar molecular profiles to those of the patient tumor, reinforcing their value as a platform for drug screening and development. Science , this issue p. 920 Organoids can recapitulate patient responses in the clinic, with potential for drug screening and personalized medicine. Patient-derived organoids (PDOs) have recently emerged as robust preclinical models; however, their potential to predict clinical outcomes in patients has remained unclear. We report on a living biobank of PDOs from metastatic, heavily pretreated colorectal and gastroesophageal cancer patients recruited in phase 1/2 clinical trials. Phenotypic and genotypic profiling of PDOs showed a high degree of similarity to the original patient tumors. Molecular profiling of tumor organoids was matched to drug-screening results, suggesting that PDOs could complement existing approaches in defining cancer vulnerabilities and improving treatment responses. We compared responses to anticancer agents ex vivo in organoids and PDO-based orthotopic mouse tumor xenograft models with the responses of the patients in clinical trials. Our data suggest that PDOs can recapitulate patient responses in the clinic and could be implemented in personalized medicine programs. Patient-derived organoids (PDOs) have recently emerged as robust preclinical models; however, their potential to predict clinical outcomes in patients has remained unclear. We report on a living biobank of PDOs from metastatic, heavily pretreated colorectal and gastroesophageal cancer patients recruited in phase 1/2 clinical trials. Phenotypic and genotypic profiling of PDOs showed a high degree of similarity to the original patient tumors. Molecular profiling of tumor organoids was matched to drug-screening results, suggesting that PDOs could complement existing approaches in defining cancer vulnerabilities and improving treatment responses. We compared responses to anticancer agents ex vivo in organoids and PDO-based orthotopic mouse tumor xenograft models with the responses of the patients in clinical trials. Our data suggest that PDOs can recapitulate patient responses in the clinic and could be implemented in personalized medicine programs. |
| Author | Starling, Naureen Darvish-Damavandi, Mahnaz Begum, Ruwaida Sadanandam, Anguraj Khan, Khurum Lote, Hazel Fassan, Matteo Huntingford, Ian Valeri, Nicola Fotiadis, Nicos Burke, Rosemary Vlachogiannis, Georgios Moorcraft, Sing Yu Bali, Maria Cunningham, David Koh, Dow-Mu Hedayat, Somaieh Workman, Paul Tunariu, Nina Dowsett, Mitchell Lampis, Andrea Sottoriva, Andrea de Bono, Johann Braconi, Chiara Jamin, Yann Spiteri, Inmaculada Chau, Ian Smyth, Elizabeth C. Eccles, Suzanne Rata, Mihaela Vatsiou, Alexandra Collins, David Clarke, Paul A. Hahne, Jens C. Watkins, David Sansom, Owen J. Robinson, Simon P. Ragulan, Chanthirika Eltahir, Zakaria Fernández-Mateos, Javier Rao, Sheela Eason, Katherine Hulkki-Wilson, Sanna |
| AuthorAffiliation | 2 Centre for Evolution and Cancer, The Institute of Cancer Research, London, United Kingdom 4 Department of Medicine, The Royal Marsden NHS Trust, London, United Kingdom 6 Department of Radiology, The Royal Marsden NHS Trust, London, United Kingdom 1 Division of Molecular Pathology, The Institute of Cancer Research, London, United Kingdom 9 Department of Medicine, Surgical Pathology and Cytopathology Unit, University of Padua, Padua, Italy 8 Division of Clinical Studies, The Institute of Cancer Research, London, United Kingdom 5 Cancer Research UK Cancer Therapeutics Unit, The Institute of Cancer Research, London, United Kingdom 7 Ralph Lauren Centre for Breast Cancer Research, Royal Marsden Hospital NHS Trust, London, United Kingdom 3 Cancer Research UK Cancer Imaging Centre, Division of Radiotherapy and Imaging, The Institute of Cancer Research and Royal Marsden Hospital, London, United Kingdom 10 Beatson Institute for Cancer Research, Glasgow, United Kingdom |
| AuthorAffiliation_xml | – name: 4 Department of Medicine, The Royal Marsden NHS Trust, London, United Kingdom – name: 7 Ralph Lauren Centre for Breast Cancer Research, Royal Marsden Hospital NHS Trust, London, United Kingdom – name: 6 Department of Radiology, The Royal Marsden NHS Trust, London, United Kingdom – name: 9 Department of Medicine, Surgical Pathology and Cytopathology Unit, University of Padua, Padua, Italy – name: 1 Division of Molecular Pathology, The Institute of Cancer Research, London, United Kingdom – name: 3 Cancer Research UK Cancer Imaging Centre, Division of Radiotherapy and Imaging, The Institute of Cancer Research and Royal Marsden Hospital, London, United Kingdom – name: 5 Cancer Research UK Cancer Therapeutics Unit, The Institute of Cancer Research, London, United Kingdom – name: 8 Division of Clinical Studies, The Institute of Cancer Research, London, United Kingdom – name: 2 Centre for Evolution and Cancer, The Institute of Cancer Research, London, United Kingdom – name: 10 Beatson Institute for Cancer Research, Glasgow, United Kingdom |
| Author_xml | – sequence: 1 givenname: Georgios orcidid: 0000-0003-3114-8772 surname: Vlachogiannis fullname: Vlachogiannis, Georgios organization: Division of Molecular Pathology, The Institute of Cancer Research, London, UK – sequence: 2 givenname: Somaieh orcidid: 0000-0002-3547-9184 surname: Hedayat fullname: Hedayat, Somaieh organization: Division of Molecular Pathology, The Institute of Cancer Research, London, UK – sequence: 3 givenname: Alexandra surname: Vatsiou fullname: Vatsiou, Alexandra organization: Centre for Evolution and Cancer, The Institute of Cancer Research, London, UK – sequence: 4 givenname: Yann orcidid: 0000-0003-0350-3757 surname: Jamin fullname: Jamin, Yann organization: Cancer Research UK Cancer Imaging Centre, Division of Radiotherapy and Imaging, The Institute of Cancer Research and Royal Marsden Hospital, London, UK – sequence: 5 givenname: Javier orcidid: 0000-0002-4949-4131 surname: Fernández-Mateos fullname: Fernández-Mateos, Javier organization: Division of Molecular Pathology, The Institute of Cancer Research, London, UK., Centre for Evolution and Cancer, The Institute of Cancer Research, London, UK – sequence: 6 givenname: Khurum surname: Khan fullname: Khan, Khurum organization: Division of Molecular Pathology, The Institute of Cancer Research, London, UK., Department of Medicine, The Royal Marsden NHS Trust, London, UK – sequence: 7 givenname: Andrea orcidid: 0000-0002-0665-9100 surname: Lampis fullname: Lampis, Andrea organization: Division of Molecular Pathology, The Institute of Cancer Research, London, UK – sequence: 8 givenname: Katherine orcidid: 0000-0001-6903-9067 surname: Eason fullname: Eason, Katherine organization: Division of Molecular Pathology, The Institute of Cancer Research, London, UK – sequence: 9 givenname: Ian orcidid: 0000-0002-5164-9278 surname: Huntingford fullname: Huntingford, Ian organization: Division of Molecular Pathology, The Institute of Cancer Research, London, UK – sequence: 10 givenname: 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Trust, London, UK – sequence: 24 givenname: Mahnaz orcidid: 0000-0003-0226-2621 surname: Darvish-Damavandi fullname: Darvish-Damavandi, Mahnaz organization: Division of Molecular Pathology, The Institute of Cancer Research, London, UK – sequence: 25 givenname: Hazel orcidid: 0000-0003-1172-0372 surname: Lote fullname: Lote, Hazel organization: Division of Molecular Pathology, The Institute of Cancer Research, London, UK., Department of Medicine, The Royal Marsden NHS Trust, London, UK – sequence: 26 givenname: Zakaria surname: Eltahir fullname: Eltahir, Zakaria organization: Division of Molecular Pathology, The Institute of Cancer Research, London, UK – sequence: 27 givenname: Elizabeth C. surname: Smyth fullname: Smyth, Elizabeth C. organization: Department of Medicine, The Royal Marsden NHS Trust, London, UK – sequence: 28 givenname: Ruwaida surname: Begum fullname: Begum, Ruwaida organization: Department of Medicine, The Royal Marsden NHS Trust, London, UK – sequence: 29 givenname: Paul A. orcidid: 0000-0001-9342-1290 surname: Clarke fullname: Clarke, Paul A. organization: Cancer Research UK Cancer Therapeutics Unit, The Institute of Cancer Research, London, UK – sequence: 30 givenname: Jens C. surname: Hahne fullname: Hahne, Jens C. organization: Division of Molecular Pathology, The Institute of Cancer Research, London, UK – sequence: 31 givenname: Mitchell surname: Dowsett fullname: Dowsett, Mitchell organization: Ralph Lauren Centre for Breast Cancer Research, Royal Marsden Hospital NHS Trust, London, UK – sequence: 32 givenname: Johann surname: de Bono fullname: de Bono, Johann organization: Division of Clinical Studies, The Institute of Cancer Research, London, UK – sequence: 33 givenname: Paul orcidid: 0000-0003-1659-3034 surname: Workman fullname: Workman, Paul organization: Cancer Research UK Cancer Therapeutics Unit, The Institute of Cancer Research, London, UK – sequence: 34 givenname: Anguraj orcidid: 0000-0001-8485-5150 surname: Sadanandam fullname: 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NHS Trust, London, UK., Cancer Research UK Cancer Therapeutics Unit, The Institute of Cancer Research, London, UK – sequence: 40 givenname: Andrea orcidid: 0000-0001-6709-9533 surname: Sottoriva fullname: Sottoriva, Andrea organization: Centre for Evolution and Cancer, The Institute of Cancer Research, London, UK – sequence: 41 givenname: Simon P. orcidid: 0000-0003-4101-7274 surname: Robinson fullname: Robinson, Simon P. organization: Cancer Research UK Cancer Imaging Centre, Division of Radiotherapy and Imaging, The Institute of Cancer Research and Royal Marsden Hospital, London, UK – sequence: 42 givenname: David surname: Cunningham fullname: Cunningham, David organization: Department of Medicine, The Royal Marsden NHS Trust, London, UK – sequence: 43 givenname: Nicola orcidid: 0000-0002-5426-5683 surname: Valeri fullname: Valeri, Nicola organization: Division of Molecular Pathology, The Institute of Cancer Research, London, UK., Department of Medicine, The Royal Marsden NHS Trust, London, UK |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/29472484$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | Copyright © 2018 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Copyright © 2018 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works |
| Copyright_xml | – notice: Copyright © 2018 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. – notice: Copyright © 2018 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works |
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| DOI | 10.1126/science.aao2774 |
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| References | e_1_3_3_17_2 e_1_3_3_16_2 e_1_3_3_19_2 e_1_3_3_18_2 e_1_3_3_13_2 e_1_3_3_12_2 e_1_3_3_15_2 e_1_3_3_34_2 e_1_3_3_14_2 e_1_3_3_35_2 e_1_3_3_32_2 e_1_3_3_33_2 e_1_3_3_11_2 e_1_3_3_30_2 e_1_3_3_10_2 e_1_3_3_31_2 e_1_3_3_6_2 e_1_3_3_5_2 e_1_3_3_8_2 e_1_3_3_7_2 e_1_3_3_28_2 e_1_3_3_9_2 e_1_3_3_27_2 e_1_3_3_29_2 e_1_3_3_24_2 e_1_3_3_23_2 e_1_3_3_26_2 e_1_3_3_25_2 e_1_3_3_2_2 e_1_3_3_20_2 e_1_3_3_4_2 e_1_3_3_22_2 e_1_3_3_3_2 e_1_3_3_21_2 29535134 - Cancer Discov. 2018 May;8(5):524. doi: 10.1158/2159-8290.CD-NB2018-029. 29535457 - Nat Rev Gastroenterol Hepatol. 2018 Apr;15(4):189. doi: 10.1038/nrgastro.2018.25. 29784911 - Nat Cell Biol. 2018 Jun;20(6):634. doi: 10.1038/s41556-018-0116-1. |
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| Snippet | Cancer organoids are miniature, three-dimensional cell culture models that can be made from primary patient tumors and studied in the laboratory. Vlachogiannis... Patient-derived organoids (PDOs) have recently emerged as robust preclinical models; however, their potential to predict clinical outcomes in patients has... Cancer organoids to model therapy responseCancer organoids are miniature, three-dimensional cell culture models that can be made from primary patient tumors... Patient-derived organoids (PDOs) have recently emerged as robust pre-clinical models, however, their potential to predict patient clinical outcomes remain... |
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| SubjectTerms | Animal models Animals Anticancer properties Antineoplastic Agents - pharmacology Antineoplastic Agents - therapeutic use Antitumor agents Cancer Cell culture Clinical trials Drug Resistance, Neoplasm Drug screening Feedback (Response) Gastrointestinal Neoplasms - drug therapy Gastrointestinal Neoplasms - pathology Genomics Humans Mathematical models Medical research Metastases Metastasis Mice Neoplasm Metastasis Organoids Organoids - drug effects Organoids - metabolism Patients Phenylurea Compounds - pharmacology Phenylurea Compounds - therapeutic use Precision medicine Precision Medicine - methods Pyridines - pharmacology Pyridines - therapeutic use Screening Three dimensional models Tumors Xenograft Model Antitumor Assays Xenografts Xenotransplantation |
| Title | Patient-derived organoids model treatment response of metastatic gastrointestinal cancers |
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