The DOI matches its Crossref record; 39 of the 39 references it cites were found in a registry or an index.
Efficient use of patient-derived organoids as a preclinical model for gynecologic tumors
Abstract
Objective The relevance of patient-derived cancer cells has been recently increasing, particularly in terms of drug discovery and precision medicine. Whereas Matrigel-based organoid culture is a promising technique that enables infinite proliferation of cells from many types of organs in a physiological condition, its validity in gynecologic tumors remains to be established. To address this issue, we aimed at developing an efficient method for organoid culture of both ovarian and endometrial tumors.Methods We conducted 3D culture of 21 gynecologic tumors following our original and modified protocol for Matrigel bilayer organoid culture. We investigated whether propagated organoids retained various features of the original tumors by histopathological examination and targeted genome sequencing.Results We customized the protocol we previously optimized for murine normal and cancer tissues, so as to circumvent the digestion-resistant nature inherent to gynecologic tumors. Indeed, this modified protocol improved the success rate from 45 to 90%, for robust propagation of organoids from tumors with various stages and subtypes. Finally, 14 patient-derived organoids were established. The recovered organoids were enriched for cancer cells that retained many aspects of the original tumors, including histological features, mutation profiles, and intra-tumoral heterogeneity. A subset of the expanded organoids could develop xenografts in immunodeficient mice, potentially paving the way to drug screening in vivo. Drug response assay in vitro for paclitaxel and cisplatin was feasible using organoid-derived spheroids.Conclusions We showed that patient-derived organoids closely resembled the original gynecologic tumors, and thereby would serve as a promising resource for preclinical studies.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“When grown in a modified Matrigel bilayer, organoids from MOCs could reproduce behaviors of their derivative cancer, such as production of mucin and a cystic morphology (Maru et al., 2019).”
From Three-dimensional modelling of ovarian cancer: from cell lines to organoids for discovery and personalized medicine (2022) · cites this paper as Maru et al., 2019
Citations
Cites
Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche
Sato, T., Vries, R. G., Snippert, H. J., van de Wetering, M., Barker, N., Stange, D. E., van Es, J. H., Abo, A., Kujala, P., Peters, P. J., et al. (2009) · Nature · doi:10.1038/nature07935 · Cited by 7,204
Integrated genomic characterization of endometrial carcinoma
The Cancer Genome Atlas Research Network, & Levine, D. A. (2013) · Nature · doi:10.1038/nature12113 · Cited by 5,784
Prospective Derivation of a Living Organoid Biobank of Colorectal Cancer Patients
van de Wetering, M., Francies, H. E., Francis, J. M., Bounova, G., Iorio, F., Pronk, A., van Houdt, W., van Gorp, J., Taylor-Weiner, A., Kester, L., et al. (2015) · Cell · doi:10.1016/j.cell.2015.03.053 · Cited by 2,408
Organoid models of human and mouse ductal pancreatic cancer
Boj, S. F., Hwang, C.-I., Baker, L. A., Chio, I. I. C., Engle, D. D., Corbo, V., Jager, M., Ponz-Sarvise, M., Tiriac, H., Spector, M. S., et al. (2015) · Cell · doi:10.1016/j.cell.2014.12.021 · Cited by 2,150
A living biobank of breast cancer organoids captures disease heterogeneity
Sachs, N., de Ligt, J., Kopper, O., Gogola, E., Bounova, G., Weeber, F., Balgobind, A. V., Wind, K., Gracanin, A., Begthel, H., et al. (2018) · Cell · doi:10.1016/j.cell.2017.11.010 · Cited by 1,973
Organoid Cultures Derived from Patients with Advanced Prostate Cancer
Gao, D., Vela, I., Sboner, A., Iaquinta, P. J., Karthaus, W. R., Gopalan, A., Dowling, C., Wanjala, J. N., Undvall, E. A., Arora, V. K., et al. (2014) · Cell · doi:10.1016/j.cell.2014.08.016 · Cited by 1,559
Spherical Cancer Models in Tumor Biology
Weiswald, L., Bellet, D. H., & Dangles‐Marie, V. (2015) · Neoplasia · doi:10.1016/j.neo.2014.12.004 · Cited by 1,194
Modeling colorectal cancer using CRISPR-Cas9–mediated engineering of human intestinal organoids
Matano, M., Date, S., Shimokawa, M., Takano, A., Fujii, M., Ohta, Y., Watanabe, T., Kanai, T., & Sato, T. (2015) · Nature Medicine · doi:10.1038/nm.3802 · Cited by 1,135
Bertotti, A., Migliardi, G., Galimi, F., Sassi, F., Torti, D., Isella, C., Corà, D., Di Nicolantonio, F., Buscarino, M., Petti, C., et al. (2011) · Cancer Discovery · doi:10.1158/2159-8290.cd-11-0109 · Cited by 939
Tumor Evolution and Drug Response in Patient-Derived Organoid Models of Bladder Cancer
Lee, S. H., Hu, W., Matulay, J. T., Silva, M. V., Owczarek, T. B., Kim, K., Chua, C. W., Barlow, L. J., Kandoth, C., Williams, A. B., et al. (2018) · Cell · doi:10.1016/j.cell.2018.03.017 · Cited by 873
Research works printed but not linked: 1
- Lee, 2017, vol. 28(2), e14
Cited by
Sorted by citations
Items 101–162 of 162
Synergistic effect of PARP inhibitor and BRD4 inhibitor in multiple models of ovarian cancer
Huang, Y., Liu, C., Li, X., Hu, D., Xiao, R., Qin, X., Guo, E., Yang, B., Li, X., Fan, J., et al. (2023) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.17683 · Cited by 10
Chang, Y., Wu, K., Wang, K., & Ding, D. (2024) · Cell Transplantation · doi:10.1177/09636897241281869 · Cited by 13
Organoid modeling meets cancers of female reproductive tract
Li, J., Zhou, M., Xie, J. H., Chen, J., Yang, M., Ye, C., Cheng, S., Liu, M., Li, R., & Tan, R. (2024) · Cell Death Discovery · doi:10.1038/s41420-024-02186-x · Cited by 9
Female Reproductive Tract Organoids: Applications from Physiology to Pathology
Wang, X., Yang, D., & Peng, H. (2025) · Biomolecules · doi:10.3390/biom15070925 · Cited by 10
Engineering human endometrial model systems in reproductive health and disease
Wang, Y., Guo, Y., Yang, Y., Ma, X., & Qin, J. (2025) · npj Biomedical Innovations. · doi:10.1038/s44385-025-00047-5 · Cited by 10
Casas‐Arozamena, C., Cortegoso, A., Piñeiro-Pérez, R., Abalo, A., Arias, E., Sampayo, V., Vilar, A., Bouso, M., Díaz, E., Moreno‐Bueno, G., et al. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23158539 · Cited by 9
Maru, Y., Kohno, M., Suzuka, K., Odaka, A., Masuda, M., Araki, A., Itami, M., Tanaka, N., & Hippo, Y. (2024) · Human Cell · doi:10.1007/s13577-024-01048-z · Cited by 9
Zhang, M., Kiyono, T., Aoki, K., Goshima, N., Kobayashi, S., Hiranuma, K., Shiraishi, K., Saya, H., & Nakahara, T. (2021) · Cancer Science · doi:10.1111/cas.15246 · Cited by 10
Three Dimensional Models of Endocrine Organs and Target Tissues Regulated by the Endocrine System
Luca, E., Zitzmann, K., Bornstein, S. R., Kugelmeier, P., Beuschlein, F., Nölting, S., & Hantel, C. (2023) · Cancers · doi:10.3390/cancers15184601 · Cited by 10
Advances in the use of organoids in endometrial diseases
Liu, Y., Sun, Y., & Cheng, S. (2024) · International Journal of Gynecology & Obstetrics · doi:10.1002/ijgo.15422 · Cited by 8
Deciphering the “Rosetta Stone” of ovarian cancer stem cells: Opportunities and challenges
Tan, J., Zheng, B., & Zhou, S. (2025) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2025.189346 · Cited by 8
Integration of Genomic Profiling and Organoid Development in Precision Oncology
Yoon, H., & Lee, S. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms23010216 · Cited by 9
Chemoresistance in Ovarian Cancer: The Role of Malignant Ascites
Nunes, M., & Ricardo, S. A. V. (2022) · Exon Publications eBooks · doi:10.36255/exon-publications-ovarian-cancer-malignant-ascites · Cited by 8
Abady, M. M., Jeong, J., Kwon, H., Assiri, A. M., Cho, J., & Saadeldin, I. M. (2024) · Frontiers in Pharmacology · doi:10.3389/fphar.2024.1412188 · Cited by 8
Immunofluorescence staining of colorectal cancer patient-derived organoids
Regan, J. L. (2022) · Methods in cell biology · doi:10.1016/bs.mcb.2022.04.008 · Cited by 8
Bridging the gap: how patient-derived lung cancer organoids are transforming personalized medicine
Liu, C., Shi, C., Wang, S., Qi, R., Gu, W., Yu, F., Zhang, G., & Qiu, F. X. (2025) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2025.1554268 · Cited by 10
Nikeghbal, P., Zamanian, D., Burke, D., & Steinkamp, M. P. (2025) · BMC Cancer · doi:10.1186/s12885-025-14811-8 · Cited by 9
Zhang, Y., Lu, M., Han, Y., Liu, B., Zhao, R., Liu, P., & Zhao, H. (2024) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2024.104355 · Cited by 6
Preclinical research models for endometrial cancer: development and selection of animal models
Yang, X., Shi, W. K., Lun, B., Kan, M. I., Jia, M., Wu, Y., & Li, Y. (2025) · Frontiers in Oncology · doi:10.3389/fonc.2025.1512616 · Cited by 6
Engineering the Human Endometrial–Embryo Interface: Breakthroughs in 3D Uterine Models
Douglas, J. A., Higgins, J., Wimalasiri, D. H., Winship, A., & Fitzgerald, H. C. (2026) · Biomolecules · doi:10.3390/biom16030383 · Cited by 6
Derivation of pancreatic acinar cell carcinoma cell line HS ‐1 as a patient‐derived tumor organoid
Hoshi, D., Kita, E., Maru, Y., Kogashi, H., Nakamura, Y., Tatsumi, Y., Shimozato, O., Nakamura, K., Sudo, K., Tsujimoto, A., et al. (2022) · Cancer Science · doi:10.1111/cas.15656 · Cited by 6
Cunnea, P., Fotopoulou, C., Ploski, J., Trillsch, F., Mahner, S., & Kessler, M. (2021) · Cancers · doi:10.3390/cancers13133349 · Cited by 7
Identification of target cells of human papillomavirus 18 using squamocolumnar junction organoids
Toyohara, Y., Taguchi, A., Ishii, Y., Yoshimoto, D., Yamazaki, M., Matsunaga, H., Nakatani, K., Hoshi, D., Tsuchimochi, S., Kusakabe, M., et al. (2023) · Cancer Science · doi:10.1111/cas.15988 · Cited by 6
Prospects and challenges of ovarian cancer organoids in chemotherapy research (Review)
Zhang, W., Ding, Y., He, H., Chen, K., Zeng, Q., Cao, X., Xiang, Y., & Zeng, H. (2025) · Oncology Letters · doi:10.3892/ol.2025.14944 · Cited by 6
Emerging Therapeutic Strategies for HPV-Related Cancers: From Gene Editing to Precision Oncology
Çakır, M. O., Kayhan, G., Yilmaz, B., Özdoğan, M., & Ashrafi, G. H. (2025) · Current Issues in Molecular Biology · doi:10.3390/cimb47090759 · Cited by 8
Research progress on the application of organoids in gynecological tumors
Shen, Y., Wang, Y., Wang, S., Li, C., & Han, F. (2024) · Frontiers in Pharmacology · doi:10.3389/fphar.2024.1417576 · Cited by 5
Organoids and epithelial ovarian cancer ‑ a future tool for personalized treatment decisions?
Sisman, Y., Schnack, T. H., Høgdall, E. V. S., & Høgdall, C. K. (2021) · Molecular and Clinical Oncology · doi:10.3892/mco.2021.2462 · Cited by 6
Human Cardiac Organoids: Quantification and Qualification in Cardiovascular Studies
Liu, Y., Abraham, S., & Xu, H. (2024) · International Journal of Drug Discovery and Pharmacology · doi:10.53941/ijddp.2024.100017 · Cited by 2
Tomas, E. J., Davis, J., Valdés, Y. R., & Shepherd, T. G. (2026) · Cancer Biology & Therapy · doi:10.1080/15384047.2025.2611602 · Cited by 2
Bhatt, P., Sahu, P., Mohapatra, P., Singh, M. S., & Roy, A. (2026) · Biomaterials Advances · doi:10.1016/j.bioadv.2026.214828 · Cited by 2
Buckley, K. H., Beyries, K. A., Ryeom, S. W., Yoon, S. S., & Katona, B. W. (2024) · Journal of Visualized Experiments · doi:10.3791/66094 · Cited by 2
Therapeutic application of mesenchymal stem cells in endometriosis
Varela-Pombo, C., López-Viñas, B., Tustain, S. Q., Maquieira, C. G., Mateos, J., Fafián‐Labora, J., & Arufe, M. C. (2025) · Life Sciences · doi:10.1016/j.lfs.2025.123851 · Cited by 2
Gynecological malignancy organoids: A game changer for personalized medicine
Ding, Z., Chang, X., Qu, X., Hua, K., & Qiu, J. (2025) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2025.189405 · Cited by 2
Sevinyan, L., Gupta, P., Velliou, E. G., & Madhuri, T. K. (2022) · Cancers · doi:10.3390/cancers14225628 · Cited by 2
Advances in Research on Aging in Female Infertility and Pathologic Pregnancy
(2024) · Frontiers research topics · doi:10.3389/978-2-8325-4798-4 · Cited by 2
Rodríguez-Martínez, A., Torrejón-Escribano, B., Eritja, N., Dorca‐Arévalo, J., Gabaldón, C., Sévigny, J., Matías‐Guiu, X., & Martı́n-Satué, M. (2025) · PubMed · doi:10.14670/hh-18-782 · Cited by 1
Chen, Y., Xu, N. L. J., Dong, M., Liu, W., Liu, Z., Sun, G., & Jia, Y. (2026) · Frontiers in Immunology · doi:10.3389/fimmu.2026.1773734 · Cited by 2
Cheng, Y., Cheng, Y., Zhao, B. T., Ni, C., Chen, X., & Wang, J. (2026) · Gynecology and Obstetrics Clinical Medicine · doi:10.1136/gocm-2025-000351 · Cited by 1
Recent Applications of Tissue-Engineered 3D Scaffolds in Oncology: Present and Future Perspectives
Tripathi, D., Gupta, V. K., & Pandey, P. K. (2026) · Protein and Peptide Letters · doi:10.2174/0109298665391686251124053211 · Cited by 1
El‐Tayeb, M. A. (2025) · Current Microbiology · doi:10.1007/s00284-025-04306-x · Cited by 1
3D visualization of uterus and ovary: tissue clearing techniques and biomedical applications
Liu, Q., Song, Z., Liu, S., Dong, Z., Zheng, X., Leung, T. Y., & Chen, X. (2025) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2025.1610539 · Cited by 1
Zhukova, G. V., Verenikina, E. V., Protasova, T. P., Yakubova, D. Y., & Volkova, А. V. (2021) · Voprosy Onkologii · doi:10.37469/0507-3758-2021-67-4-463-473 · Cited by 1
The use of biocompatible composite scaffolds in oncology
Kit, O. I., Maksimov, A. Y., Novikova, I. A., Гончарова, А. С., Lukbanova, E. A., Sitkovskaya, A. О., Volovik, V. G., & Chapek, S. V. (2022) · Siberian Journal of Oncology · doi:10.21294/1814-4861-2022-21-1-130-136 · Cited by 2
Models of ovarian cancer to test new agents
Sodi, V. L., Craig, A. D., Peri, S., & Connolly, D. C. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-819840-7.00012-1
Leveraging technological opportunities in cancer genomics
Valle-Inclán, J. E. (2021) · Utrecht University Repository (Utrecht University) · doi:10.33540/480
Ovarian Cancer: Towards Personalizing Ovarian Cancer Treatments Using Patient-Derived Organoids
Volpari, T., Hebner, J., Aiyar, R. S., & Martin, L. A. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-820472-6.00080-3
A Meta-analysis of 2D vs. 3D Ovarian Cancer Cellular ModelsPreprint
Kerslake, R., Belay, B., Panfilov, S., Hall, M., Kyrou, I., Randeva, H. S., Hyttinen, J., Karteris, E., & Sisu, C. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.12.05.519144
A Novel ex-vivo platform for personalized treatment in metastatic ovarian cancerPreprint
Valdivia, A., Adefolaju, A., Thang, M., Cuaboy, L. A., John, C. S., Mann, B., Satterlee, A., Bae-Jump, V. L., & Hingtgen, S. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.03.14.585117
Choi, J. H., & Gong, S. P. (2024) · Journal of Animal Reproduciton and Biotechnology · doi:10.12750/jarb.39.1.19
Current and future perspectives of xenograft models of human ovarian cancer
Inoue, J., Chiyoda, T., Muramatsu, T., Hirasawa, A., Aoki, D., & Inazawa, J. (2024) · Elsevier eBooks · doi:10.1016/b978-0-12-824040-3.00014-5
Organoids research progress in gynecological cancers: a bibliometric analysis
He, B., Ma, H., Yu, H., Li, D., Zhang, L., & Wang, J. (2024) · Frontiers in Oncology · doi:10.3389/fonc.2024.1484074
Thorel, L., Dolivet, É., Morice, P., Florent, R., Divoux, J., Perréard, M., Lecouflet, L., Desmartin, G., Alagama, C. M., Giffard, F., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.01.10.631512
Singla, S., Bagga, R., Srinivasan, R., Bhatia, P., & Bhattacharyya, S. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.06.19.660648
Construction of Multicellular Tumor-on-a-Chip Models for Ovarian Cancer Research
Ye, J., Lin, H., Zhang, Z., Xu, S., Yang, F. L., ZhuanSun, X.-M., Ji, F., Zhang, Y. F., Zhu, Y., Zhang, J., et al. (2025) · Engineering · doi:10.1016/j.eng.2025.08.028 · Cited by 1
Patient-Derived Organoids: Basic and Translational Research on Uterine Cancer
Maru, Y., Tanaka, N., & Hippo, Y. (2025) · Current human cell research and applications · doi:10.1007/978-981-95-0587-6_7
Development and Application of Tumor Organoids: An Emerging Platform for Gynecological Cancers
Hu, Y., Chen, W., Zhang, X., Wu, Y., Du, F., Wang, J., He, M., & Sun, W. T. (2025) · International Journal of Women s Health · doi:10.2147/ijwh.s567162
Zhang, Q., Huang, H., Dong, H., Ma, Q., & Jin, H. (2026) · Advanced Materials Technologies · doi:10.1002/admt.202502306 · Cited by 1
Organoids as Next-Generation Models of Tumor Drug Resistance
Wang, L., Tang, Q., Zhong, L., He, M., Zhu, X., Zheng, Q., Long, L., Wang, Y., Jiang, Q., Wang, H., et al. (2026) · Cancer Biome and Targeted Therapy · doi:10.66505/cbtt.v1i1.9
Craig, O., Salazar, C., Abdirahman, S. M., Dalvi, N., Rajadevan, N., Luu, J., Vary, R., Ramm, S., Cowley, K. J., Lim, R., et al. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.04.06.716848
Organoids and AI-integrated models in ovarian cancer research: the future of personalized therapy
Nikam, A., Bhutia, G. T., & Sarkar, S. (2026) · Frontiers in Oncology · doi:10.3389/fonc.2026.1903061
Singla, S., Bagga, R., Srinivasan, R., Bhatia, P., & Bhattacharyya, S. (2026) · Organoids · doi:10.3390/organoids5030031
Organoids: Current Applications and Future Directions
Leng, Y., Wang, Y., Cao, C., Deng, F., Lian, W., Chen, X., Lin, M., Zeng, Z., Mo, D., Li, S., et al. (2026) · MedComm · doi:10.1002/mco2.70965
Metadata
- Authors
- Maru, Y., Tanaka, N., Itami, M., & Hippo, Y.
- Affiliations
- Chiba Cancer Center Research Institute (JP)
- Chiba Cancer Center (JP)
- Corresponding author
- Hippo, Yoshitaka
- Venue
- Gynecologic Oncology
- Publisher
- Elsevier BV
- Published
- 2019-07
- Volume
- 154
- Issue
- 1
- Pages
- 189-198
- ISSN
- 0090-8258 (ISSN-L)
- OpenAlex
- W2946001968
- Cited by
- 162
- References
- 39
- Citations by year
- 2026: 12 · 2025: 23 · 2024: 28 · 2023: 21 · 2022: 25 · 2021: 31 · 2020: 17 · 2019: 5
- FWCI
- 8.14
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Gynecologic Oncology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Japan Society for the Promotion of Science
- Topics
- Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
- Physical Sciences › Engineering › Biomedical Engineering › 3D Printing in Biomedical Research
- Health Sciences › Medicine › Oncology › Ovarian cancer diagnosis and treatment
- Keywords
- patient-derived organoids, gynecologic cancer, ovarian cancer, endometrial cancer, tumor heterogeneity, paclitaxel, cisplatin, drug screening, 3D cell culture
- MeSH terms
- Animals, Drug Screening Assays, Antitumor, Female, Humans, Mice, Inbred BALB C, Mice, Nude, Neoplasm Staging, Organoids, Ovarian Neoplasms, Endometrial Neoplasms, Tissue Culture Techniques, Mice
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review