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Generation of Tumor-Reactive T Cells by Co-culture of Peripheral Blood Lymphocytes and Tumor Organoids
Open accessAbstract
Cancer immunotherapies have shown substantial clinical activity for a subset of patients with epithelial cancers. Still, technological platforms to study cancer T-cell interactions for individual patients and understand determinants of responsiveness are presently lacking. Here, we establish and validate a platform to induce and analyze tumor-specific T cell responses to epithelial cancers in a personalized manner. We demonstrate that co-cultures of autologous tumor organoids and peripheral blood lymphocytes can be used to enrich tumor-reactive T cells from peripheral blood of patients with mismatch repair-deficient colorectal cancer and non-small-cell lung cancer. Furthermore, we demonstrate that these T cells can be used to assess the efficiency of killing of matched tumor organoids. This platform provides an unbiased strategy for the isolation of tumor-reactive T cells and provides a means by which to assess the sensitivity of tumor cells to T cell-mediated attack at the level of the individual patient.
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“In addition, ex vivo coculture systems utilizing human peripheral blood mononuclear cells or tumor-infiltrating lymphocytes cocultured with patient-derived organoids provide valuable platforms to interrogate human-specific immune responses to phage-delivered antigens or immunotherapies [111–113]”
From Phage therapy in oncology: opportunities for cancer prevention and treatment (2026) · cites this paper as [112]
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“Additionally, PDO cocultures could potentially be applied to generate a large number of effector T cells for adoptive cell transplantation [56,57].”
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“utilized the co-culture of PDOs from MMR deficient CRC and NSCLC, with success rates of 60% and demonstrated histological similarities between the PDOs and primary tissues [130].”
Küçükköse, E., Wensink, G. E., Roelse, C. M., van Schelven, S. J., Raats, D., Boj, S. F., Koopman, M., Laoukili, J., Roodhart, J. M. L., & Kranenburg, O. (2021) · Cancers · doi:10.3390/cancers13215434 · Cited by 5
Vaccines as Priming Tools for T Cell Therapy for Epithelial Cancers
Kandalaft, L. E., & Harari, A. (2021) · Cancers · doi:10.3390/cancers13225819 · Cited by 6
“There are a few variations of this approach; for example, stimulation of lymphocytes may be done by autologous tumor cell lines or tumor organoids [98].”
BackgroundRollins, Z. A., Huang, J., Tagkopoulos, I., Faller, R., & George, S. C. (2022) · Computational and Structural Biotechnology Journal · doi:10.1016/j.csbj.2022.06.048 · Cited by 5
“However, identification of partner TCRs remains challenging, despite the fact that tumor-specific T cells can be found in the peripheral blood (11,12).”
BackgroundLi, X., Zheng, A., Liu, J., Shi, M., Liao, B., Xie, S., Yan, R., Gan, Y., Zuo, X., Gong, M., et al. (2023) · Antiviral Research · doi:10.1016/j.antiviral.2023.105608 · Cited by 5
The third dimension of tumor microenvironment—The importance of tumor stroma in 3D cancer models
Plavá, J., Čeháková, M., Kuniaková, M., Trnkova, L., Cihova, M., Boháč, M., & Danišovič, Ľ. (2023) · Experimental Biology and Medicine · doi:10.1177/15353702231198050 · Cited by 8
An Exploration of Organoid Technology: Present Advancements, Applications, and Obstacles
Mishra, I., Gupta, K., Mishra, R., Chaudhary, K., & Sharma, V. (2023) · Current Pharmaceutical Biotechnology · doi:10.2174/0113892010273024230925075231 · Cited by 5
Goto, A., Moriya, Y., Nakayama, M., Iwasaki, S., & Yamamoto, S. (2024) · Drug Metabolism and Pharmacokinetics · doi:10.1016/j.dmpk.2024.101003 · Cited by 5
Xiu, Z., Yang, Q., Xie, F., Han, F., He, W., & Liao, W. (2024) · Journal of Tissue Engineering · doi:10.1177/20417314241255470 · Cited by 5
“64 Moreover, it allows for the prediction of immunotherapy sensitivity at different stages of treatment.”
BackgroundPatient-Derived Organoids: Promises, Hurdles and Potential Clinical Applications
Hedayat, S., & Valeri, N. (2020) · Clinical Oncology · doi:10.1016/j.clon.2019.12.009 · Cited by 5
A ‘smart’ aptamer-functionalized continuous label-free cell catch–transport–release system
Zhang, B., Wang, C., Du, Y., Paxton, R. J., & He, X. (2021) · Journal of Materials Chemistry B · doi:10.1039/d1tb00739d · Cited by 5
D’Angelo, A., Shibata, K., Tokunaga, M., Furutani-Seiki, M., & Bagby, S. (2022) · Biochemistry and Biophysics Reports · doi:10.1016/j.bbrep.2022.101365 · Cited by 6
Perspective on human papillomavirus infection treatment by vaginal microbiota
Zhong, L., Zheng, J., Lin, L., Cong, Q., & Qiao, L. (2023) · Interdisciplinary medicine · doi:10.1002/inmd.20220020 · Cited by 5
Bioinformatic Approaches to Validation and Functional Analysis of 3D Lung Cancer Models
Li, P. J., Roose, J. P., Jablons, D. M., & Kratz, J. R. (2021) · Cancers · doi:10.3390/cancers13040701 · Cited by 5
Podaza, E., Capuano, J. A., Assaad, M. A., Kuo, H., Markowitz, G. J., Irizarry, A., Ravichandran, H., Ackermann, S. E., Kane, T., Manohar, J., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.07.05.546622 · Cited by 5
Randall‐Demllo, S., Al-Qadami, G. H., Raposo, A. E., Ma, C., Priebe, I. K., Hor, M., Singh, R., & Fung, K. Y. C. (2024) · Cancers · doi:10.3390/cancers16213664 · Cited by 5
“In one study, a two-week co-culture of autologous T lymphocytes with IFN-γ -stimulated tumour organoids enabled the identification of patients whose organoids stimulated cytotoxic T lymphocytes, i.e., separation into responders and non-responders based on MHC-I status and cytolytic efficiency [63].”
BackgroundInfluentialLan, H., Zhu, J., Hou, H., Zhang, C., Huo, X., Zhang, Y., Yang, F., Zhou, N., & Zhang, X. (2025) · Cell Communication and Signaling · doi:10.1186/s12964-025-02146-7 · Cited by 4
“The reliability of obtaining tumor-infiltrating lymphocytes (TILs) by culturing reactive T cells with peripheral blood mononuclear cells (PBMCs) and from established PDXs has been previously demonstrated [36].”
Dimari, G., Hu, Y., Frenzel, A., Fuchs, A., Wurm, A. A., & Fischer‐Friedrich, E. (2025) · iScience · doi:10.1016/j.isci.2025.113023 · Cited by 4
“78 Following previously established approaches, 79,80 we grew tumor clusters from MDA-MB-231 in Matrigel, both in control and MET-inducing conditions for 10 days followed by a 3-day co-culture with PBMCs.”
Upadhyay, V., Das, S., Nehru, A., Swetha, U. S., Vatsa, P. P., Chamoli, A., & Mandoli, A. (2025) · 3 Biotech · doi:10.1007/s13205-025-04472-6 · Cited by 4
“Most organoids consist predominantly of epithelial cells and lack immune, stromal, and vascular components, limiting their ability to model the tumor microenvironment (TME) and immune–tumor dynamics (Dijkstra et al. 2018) (Neal et al. 2018).”
Qin, Z., Zhang, H., Li, Y., Yang, J., Liu, H., Guan, Z., Hou, Q., Du, H., Li, X., Lin, X., et al. (2025) · Communications Biology · doi:10.1038/s42003-025-09188-0 · Cited by 5
Patient-derived organoids in non-small cell lung cancer: advances in drug sensitivity testing
Tang, W., & Tian, X. (2026) · Frontiers in Pharmacology · doi:10.3389/fphar.2025.1639268 · Cited by 4
Li, R., Wu, Y., Zheng, Z., Zhou, F., Xu, K., & Su, J. (2026) · MedComm · doi:10.1002/mco2.70575 · Cited by 4
“TME, which is facilitated by coculture models incorporating stromal and immune cells [ 58, 59 ].”
Ito, K., Iida, K., Hirano, T., Leong, M. M., Morii, K., Menju, T., Date, H., Ozasa, H., Yoshida, H., Hirai, T., et al. (2026) · Nature Communications · doi:10.1038/s41467-026-69680-x · Cited by 4
“Several studies have introduced strategies to enrich TR-Ts from peripheral blood using autologous or arti fi cial antigen-presenting cells 65 – 69 .”
Ni, D., Xing, J., Niu, G., Qiu, J., Wei, G., Chen, G., Zhou, Q., & Yin, X. (2026) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2026.1757516 · Cited by 4
Wang, X., Zhu, C., Sun, Y., Xie, X., Wang, M., Jin, Y., Gu, Y., Qian, L., Shi, L., Xu, J., et al. (2026) · Journal for ImmunoTherapy of Cancer · doi:10.1136/jitc-2025-013656 · Cited by 4
PRECISE-seq reveals disease-relevant TCR repertoires with phenotypic plasticity
Liu, S., Liang, G., Yang, Y., Shi, Y., Dong, L., Zhao, Y., Mei, B., Wang, J., Lin, F., Li, Y., et al. (2026) · The Journal of Experimental Medicine · doi:10.1084/jem.20251779 · Cited by 4
“…approaches for identifying disease-associated TCRs rely on either pMHC multimer staining (Ma et al., 2021; Newell et al., 2013) or in vitro functional screening of TCR clonotypes (Arnaud et al., 2022; Chandran et al., 2022; Dijkstra et al., 2018; Lowery et al., 2022; Rosenberg and Restifo, 2015).”
Review on Advanced Cancer Modeling for a Cancer Study
Cho, Y. (2022) · Current Issues in Molecular Biology · doi:10.3390/cimb44110362 · Cited by 4
“Dijkstra et al. (2018) generated the co-culture of tumor-reactive T cells with tumor organoids.”
BackgroundBioengineered in vitro three-dimensional tumor models in endocrine cancers
Skardal, A., Sivakumar, H., Rodríguez, M., Popova, L. V., & Dedhia, P. H. (2024) · Endocrine Related Cancer · doi:10.1530/erc-23-0344 · Cited by 4
Ren, X., Guo, T., Xu, M., Huang, Y., Liao, X., Qi, L., & Cheng, S. (2024) · Advanced Healthcare Materials · doi:10.1002/adhm.202401223 · Cited by 4
Li, X., Wang, Z., Liu, Y., Zhang, J., Zhang, L., Li, Y., An, X., Yang, Y., Yu, R., Zhao, M., et al. (2025) · Genes & Diseases · doi:10.1016/j.gendis.2025.101680 · Cited by 4
“113 This platform facilitates the isolation of tumor-reactive T cells and the assessment of cancer cell susceptibility to T cell attacks.”
Desai, M. K., Parmar, N. B., Shah, I. T., Parekh, P. S., Patel, R., & Chorawala, M. R. (2025) · Developmental Dynamics · doi:10.1002/dvdy.70042 · Cited by 4
“102,103 Intravital microscopy allows for the visualization of cells inside an entire organ.”
Construction of Lymphoma Organoids and Applications in Tumor Microenvironment Research
Zhu, M., Li, T., Han, S., Zhao, D., Chen, X., Wong, V., Wang, H., & Liu, Y. (2025) · European Journal Of Haematology · doi:10.1111/ejh.14448 · Cited by 4
“Dijkstra et al. [78] demonstrated this by co-culturing dissociated colorectal cancer organoids with peripheral blood mononuclear cells (PBMCs) from the same patient, leading to the detection of tumor-specific T cells after 2 weeks.”
Organoid Technology and Clinical Applications in Digestive System Cancer
Zhao, X., Jiang, Y., Liu, C., Hou, M., Wang, H., & Fu, J. (2021) · Engineering · doi:10.1016/j.eng.2021.04.017 · Cited by 4
Blood Divider for Simple, Surface Tension‐Based Isolation of Peripheral Blood Mononuclear Cells
Kim, B., Seo, I., Seo, G. M., Kim, W., Shin, E., & Choi, S. (2021) · Advanced Materials Technologies · doi:10.1002/admt.202100691 · Cited by 4
Patient-derived tumor models in cancer research: Evaluation of the oncostatic effects of melatonin
Martínez-Ruiz, L., López‐Rodríguez, A., Florido, J., Rodríguez-Santana, C., Ferrer, J. M. R., Acuña-Castroviejo, D., & Escames, G. (2023) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2023.115581 · Cited by 4
“1) [1,54 – 56], thus creating models that maintain aspects of the tumor structure and heterogeneity [3,57 – 59].”
Nam, Y., Cha, E., Kwak, S. M., Seo, S. J., Rim, J. H., & Jin, Y. (2024) · Journal of Microbiology and Biotechnology · doi:10.4014/jmb.2405.05036 · Cited by 4
Metadata
- Authors
- Dijkstra, K. K., Cattaneo, C. M., Weeber, F., Chalabi, M., van de Haar, J., Fanchi, L. F., Slagter, M., van der Velden, D. L., Kaing, S., Kelderman, S., van Rooij, N., van Leerdam, M. E., Depla, A., Smit, E. F., Hartemink, K. J., de Groot, R., Wolkers, M. C., Sachs, N., Snaebjornsson, P., Monkhorst, K., Haanen, J., Clevers, H., Schumacher, T. N., & Voest, E. E.
- Affiliations
- The Netherlands Cancer Institute (NL)
- Slotervaartziekenhuis (NL)
- Sanquin (NL)
- University Medical Center Utrecht (NL)
- Corresponding author
- Voest, Emile E.
- ORCID
- Dijkstra, Krijn K.
- Cattaneo, Chiara M.
- Weeber, Fleur
- Chalabi, Myriam
- van de Haar, Joris
- Fanchi, Lorenzo F.
- Slagter, Maarten
- van Rooij, Nienke
- van Leerdam, Monique E.
- Smit, Egbert F.
- Hartemink, Koen J.
- de Groot, Rosa
- Wolkers, Monika C.
- Sachs, Norman
- Monkhorst, Kim
- Haanen, John
- Clevers, Hans
- Schumacher, Ton N.
- Voest, Emile E.
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2018-09
- Volume
- 174
- Issue
- 6
- Pages
- 1586-1598.e12
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC6558289
- OpenAlex
- W2885650843
- Cited by
- 1,135
- References
- 47
- Citations by year
- 2026: 172 · 2025: 175 · 2024: 143 · 2023: 154 · 2022: 144 · 2021: 168 · 2020: 106 · 2019: 62 · 2018: 10
- FWCI
- 37.19
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- Amsterdam UMC (VU Amsterdam) - Institutional Repository (publishedVersion)
- PubMed Central (acceptedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Utrecht University Repository (Utrecht University) (submittedVersion, other-oa)
- Pure Amsterdam UMC (submittedVersion)
- KNAW Research Portal (The Royal Netherlands Academy of Arts and Sciences) (submittedVersion)
- Utrecht University Repository (Utrecht University) (submittedVersion)
- Funders
- NWO Gravitation Program (NWO (2012-2022)
- KWF (HUBR2014-7006)
- KWF Queen Wilhelmina (NKI 2013-6122)
- ERC AdG SENSIT
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
- Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Keywords
- tumor-reactive T cells, tumor organoids, peripheral blood lymphocytes, co-culture, personalized cancer immunotherapy, non-small cell lung cancer, epithelial cancers, T cell-mediated killing
- MeSH terms
- Aged, Carcinoma, Non-Small-Cell Lung, Female, Humans, Interferon-gamma, Leukocytes, Mononuclear, Lung Neoplasms, Lymphocyte Activation, Male, Middle Aged, T-Lymphocytes, Tumor Cells, Cultured, Colorectal Neoplasms, Coculture Techniques, Cell Culture Techniques, In Vitro Techniques
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