Patient-Derived Ovarian Cancer Organoids Mimic Clinical Response and Exhibit Heterogeneous Inter- and Intrapatient Drug Responses
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Abstract
Abstract Purpose There remains an unmet need for preclinical models to enable personalized therapy for ovarian cancer (OC) patients. Recently, patient-derived organoid (PDO) cultures of patients with OC have been established that faithfully represent the histopathological features and genomic landscape of the patient tumor. In this study, we evaluate the capacity of OC PDOs to predict clinical drug response and functional consequences of tumor heterogeneity. Experimental design 36 genomically characterized PDOs from 23 patients with known clinical histories were exposed to chemotherapeutics and targeted drugs. Results OC PDOs maintained genomic features of the original tumor lesion and recapitulated patient response to neoadjuvant carboplatin and paclitaxel combination treatment, according to distinct clinical outcomes (histopathological, biochemical and radiological). PDOs displayed inter-as well as intrapatient drug response heterogeneity, which could in part be explained by genetic aberrations. All PDOs were resistant to PARP-inhibitors, in accordance with homologous recombination pathway fidelity and genome-wide mutation context. KRAS, BRAF and NRAS mutation status predicted response to BRAF-inhibitor vemurafenib and pan-HER-inhibitor afatinib, and explained differential response among four PDOs derived from distinct tumor locations of an individual patient. Importantly, PDO drug screening identified sensitivity to at least one drug for the majority of patients (88%). Conclusions OC PDOs are a valuable preclinical model system that can provide insights in drug response for individual patients with OC, complementary to genetic testing. Generating PDOs of multiple tumor locations can improve clinical decision making and increase our knowledge on genetic and drug response heterogeneity.
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These ovarian tumoroid models show great promise for conducting ex vivo drug assays to predict therapeutic response in the women from which they were established.
“These models show great promise for conducting ex vivo drug assays to predict therapeutic response in the women from which they were established (De Witte et al., 2020; Maenhoudt et al., 2020; Nanki et al., 2020; Gorski et al., 2021).”
From Three-dimensional modelling of ovarian cancer: from cell lines to organoids for discovery and personalized medicine (2022) · cites this paper as De Witte et al., 2020
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- Authors
- de Witte, C. J., Espejo Valle-Inclan, J., Hami, N., Lõhmussaar, K., Kopper, O., Vreuls, C. P. H., Jonges, G. N., van Diest, P., Nguyen, L., Clevers, H., Kloosterman, W. P., Cuppen, E., Snippert, H. J. G., Zweemer, R. P., Witteveen, P. O., & Stelloo, E.
- Affiliations
- Utrecht University (NL)
- Royal Netherlands Academy of Arts and Sciences (NL)
- Corresponding author
- Stelloo, Ellen
- ORCID
- Venue
- Cell Reports
- Publisher
- Elsevier BV
- Published
- 2020-06
- Volume
- 31
- Issue
- 11
- Pages
- 107762
- ISSN
- 2211-1247 (ISSN-L)
- OpenAlex
- W3036048749
- Cited by
- 303
- References
- 53
- Citations by year
- 2026: 42 · 2025: 59 · 2024: 50 · 2023: 50 · 2022: 54 · 2021: 41 · 2020: 7
- FWCI
- 33.46
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Cell Reports (publishedVersion, cc-by-nc-nd)
- medRxiv (acceptedVersion, cc-by-nd)
- PubMed (publishedVersion)
- KNAW Research Portal (The Royal Netherlands Academy of Arts and Sciences) (publishedVersion, other-oa)
- Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Utrecht University Repository (Utrecht University) (submittedVersion, other-oa)
- Funders
- KWF Kankerbestrijding (RUG-2017-11352, UU2015-7743)
- Leids Universitair Medisch Centrum
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Ovarian cancer diagnosis and treatment
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › BRCA gene mutations in cancer
- Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
- Keywords
- ovarian cancer, patient-derived organoids, drug response prediction, tumor heterogeneity, interpatient heterogeneity, intrapatient heterogeneity, carboplatin, paclitaxel, neoadjuvant chemotherapy, targeted therapy, preclinical models, personalized treatment, drug screening
- MeSH terms
- Carcinoma, Ovarian Epithelial, Antineoplastic Agents, Drug Screening Assays, Antitumor, Pharmaceutical Preparations, Female, Humans, Organoids, Ovarian Neoplasms, Paclitaxel, Drug Resistance, Neoplasm, Precision Medicine
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