The DOI matches its Crossref record; 46 of the 47 references it cites were found in a registry or an index.
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.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
The source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“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]
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
NIH Image to ImageJ: 25 years of image analysis
Schneider, C. A., Rasband, W. S., & Eliceiri, K. W. (2012) · Nature Methods · doi:10.1038/nmeth.2089 · Cited by 64,638
PD-1 and PD-L1 Immune Checkpoint Blockade to Treat Breast Cancer
Hartkopf, A. D., Taran, F., Wallwiener, M., Walter, C. B., Krämer, B., Grischke, E., & Brucker, S. Y. (2016) · Breast Care · doi:10.1159/000453569 · Cited by 30,989
The Genome Analysis Toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data
McKenna, A., Hanna, M., Banks, E., Sivachenko, A., Cibulskis, K., Kernytsky, A., Garimella, K., Altshuler, D., Gabriel, S., Daly, M., et al. (2010) · Genome Research · doi:10.1101/gr.107524.110 · Cited by 27,895 · cited 3×
“REAGENT or RESOURCE SOURCE IDENTIFIER Somatic Indel Detector (GATK) McKenna et al., 2010 https://software.broadinstitute.org/gatk/ snpEff, version 4.3 Cingolani et al., 2012 http://snpeff.sourceforge.net FlowJo version 10 https://www.flowjo.com/ ImageJ version 1.50i Schneider et al., 2012 https://imagej.nih.gov/ij/”
InfluentialAdverse Renal Effects of Immune Checkpoint Inhibitors: A Narrative Review
Wanchoo, R., Karam, S., Uppal, N. N., Barta, V. S., Deray, G., Devoe, C., Launay‐Vacher, V., Jhaveri, K. D., & on behalf of Cancer and Kidney International Network Workgroup on Immune Checkpoint Inhibitors (2017) · American Journal of Nephrology · doi:10.1159/000455014 · Cited by 15,320
Cingolani, P., Platts, A., Wang, L. L., Coon, M., Nguyen, T., Wang, L., Land, S. J., Lu, X., & Ruden, D. M. (2012) · Fly · doi:10.4161/fly.19695 · Cited by 11,816
Signatures of mutational processes in human cancer
Initiative, A. P. C. G., Alexandrov, L. B., ICGC Breast Cancer Consortium, ICGC MMML-Seq Consortium, PedBrain, I., Nik-Zainal, S., Wedge, D. C., Aparicio, S. A. J. R., Behjati, S., Biankin, A. V., et al. (2013) · Nature · doi:10.1038/nature12477 · Cited by 9,660
Self-citationPD-1 Blockade in Tumors with Mismatch-Repair Deficiency
Le, D. T., Uram, J. N., Wang, H., Bartlett, B. R., Kemberling, H., Eyring, A. D., Skora, A. D., Luber, B. S., Azad, N. S., Laheru, D., et al. (2015) · New England Journal of Medicine · doi:10.1056/nejmoa1500596 · Cited by 9,377
Nivolumab versus docetaxel in advanced nonsquamous non-small-cell lung cancer
Borghaei, H., Paz-Ares, L., Horn, L., Spigel, D. R., Steins, M., Ready, N. E., Chow, L. Q., Vokes, E. E., Felip, E., Holgado, E., et al. (2015) · New England Journal of Medicine · doi:10.1056/nejmoa1507643 · Cited by 9,335 · cited 2×
“, 2012) and response to PD-1/PD-L1 blockade is restricted to approximately 20% of patients (Garon et al., 2015; Borghaei et al., 2015).”
Comprehensive molecular characterization of human colon and rectal cancer
The Cancer Genome Atlas Network (2012) · Nature · doi:10.1038/nature11252 · Cited by 8,499
Combined Nivolumab and Ipilimumab or Monotherapy in Untreated Melanoma
Larkin, J., Chiarion-Sileni, V., Gonzalez, R., Grob, J. J., Cowey, C. L., Lao, C. D., Schadendorf, D., Dummer, R., Smylie, M., Rutkowski, P., et al. (2015) · New England Journal of Medicine · doi:10.1056/nejmoa1504030 · Cited by 8,157 · cited 1×
“The use of antibodies against immune checkpoints, such as CTLA-4 and PD-1/PD-L1, has shown clear clinical benefit for patients with advanced cancer, including melanoma, nonsmall-cell lung cancer (NSCLC), and mismatch repair-deficient (dMMR) colorectal cancer (CRC) (Larkin et al., 2015; Garon et al., 2015; Borghaei et…”
Self-citation
Flagged first, then by citations
1 of the 47 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Items 401–500 of 1,000
The Organoid Platform: Promises and Challenges as Tools in the Fight against COVID-19
Geurts, M. H., van der Vaart, J., Beumer, J., & Clevers, H. C. (2021) · Stem Cell Reports · doi:10.1016/j.stemcr.2020.11.009 · Cited by 27
“That study revealed successful antigen presentation of tumor organoid cells to T cells, which subsequently became activated (Dijkstra et al., 2018).”
Self-citation3D Bioprinting of Model Tissues That Mimic the Tumor Microenvironment
Bojin, F. M., Robu, A., Bejenariu, M. I., Ordodi, V. L., Olteanu, G., Cean, A., Popescu, R., Neagu, M., Gavriliuc, O. I., Neagu, A., et al. (2021) · Micromachines · doi:10.3390/mi12050535 · Cited by 27
“The co-culture of PBMCs and epithelial tumor organoids allowed for the expansion of tumor-reactive T-cells [28].”
BackgroundZheng, R., Li, Y., Chen, D., Su, J., Han, N., Chen, H., Ning, Z., Xiao, M., Zhao, M., & Zhu, B. (2021) · Viruses · doi:10.3390/v13122384 · Cited by 26
“The main objects of this experiment were T cells, which were suspended growth cells [22].”
Yu, Y., Zhu, Y.-J., Xiao, Z., Chen, Y., Chang, X., Liu, Y., Tang, Q., & Zhang, H. (2022) · Biomarker Research · doi:10.1186/s40364-022-00421-0 · Cited by 27
Tumor Organoid and Spheroid Models for Cervical Cancer
Kutle, I., Polten, R., Hachenberg, J., Klapdor, R., Morgan, M. A., & Schambach, A. (2023) · Cancers · doi:10.3390/cancers15092518 · Cited by 28
Preclinical Models for the Study of Lung Cancer Pathogenesis and Therapy DevelopmentPreprint
Estape, A. A., Foggetti, G., Starrett, J. H., Nguyen, D. X., & Politi, K. A. (2021) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a037820 · Cited by 23
Technological advances and challenges in constructing complex gut organoid systems
Zheng, L., Zhan, Y., Wang, C., Fan, Q., Sun, D., Li, Y., & Xiong, Y. (2024) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2024.1432744 · Cited by 27
Challenges in validation of combination treatment strategies for CRC using patient-derived organoids
Benboubker, V., Ramzy, G. M., Jacobs, S., & Nowak-Sliwinska, P. M. (2024) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-024-03173-x · Cited by 29
“Several new technologies have been developed by different groups [104–108], in which PDOs are used to identify tumor-reactive T cells, assess a patient’s potential response to immune checkpoint blockade, and identify neoantigens in individual tumors, to which cell therapies could be applied.”
Yao, N., Jing, N., Lin, J., Niu, W., Yan, W., Yuan, H., Xiong, Z., Hou, Q., Qiao, X., Liu, Q., et al. (2025) · Investigational New Drugs · doi:10.1007/s10637-025-01523-w · Cited by 30
Mapping lung squamous cell carcinoma pathogenesis through in vitro and in vivo models
Gómez‐López, S., Whiteman, Z. E., & Janes, S. M. (2021) · Communications Biology · doi:10.1038/s42003-021-02470-x · Cited by 26
Scientific Validation and Clinical Application of Lung Cancer Organoids
Lee, D., Kim, Y., & Chung, C. (2021) · Cells · doi:10.3390/cells10113012 · Cited by 25
“Few studies have cultured LCOs from tissues obtained from distant LN biopsies, percutaneous needle biopsies, and EBUS biopsies [11,12,33,34,36].”
BackgroundInfluentialApplication Progress of Organoids in Colorectal Cancer
Luo, L., Ma, Y., Zheng, Y., Su, J., & Huang, G. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.815067 · Cited by 30
“Moreover, these T cells can also be used to evaluate the efficiency of killing matched tumor organoids (Dijkstra et al., 2018).”
BackgroundThree-dimensional models of the lung: past, present and future: a mini review
Sen, C., Freund, D., & Gomperts, B. N. (2022) · Biochemical Society Transactions · doi:10.1042/bst20190569 · Cited by 25
Next generation patient derived tumor organoids
Podaza, E., Kuo, H., Nguyen, J., Elemento, O., & Martín, M. L. (2022) · Translational research · doi:10.1016/j.trsl.2022.08.003 · Cited by 26
Development and characterization of patient-derived salivary gland cancer organoid cultures
Lassche, G., van Boxtel, W., Aalders, T. W., van Hooij, O., Grunsven, A. C. H. V. E., Verhaegh, G. W. C. T., van Herpen, C. M. L., & Schalken, J. A. (2022) · Oral Oncology · doi:10.1016/j.oraloncology.2022.106186 · Cited by 29
Chen, J., & Na, F. (2022) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2022.1066869 · Cited by 25
“Platforms that allow the analysis and modeling of the complexity of the microenvironment would greatly contribute to the understanding of the critical mechanism that mediates a successful antitumor immune response (Dijkstra et al., 2018; Yuki et al., 2020; Wu et al., 2022).”
BackgroundThe Patient-Derived Cancer Organoids: Promises and Challenges as Platforms for Cancer Discovery
Bae, J., Choi, Y. S., Cho, G., & Jang, S. J. (2022) · Cancers · doi:10.3390/cancers14092144 · Cited by 27
Kotsifaki, A., Maroulaki, S., & Armakolas, A. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25094832 · Cited by 29
“Investigations, such as the seminal work by Banys-Paluchowski et al. and Dijkstra et al., have established a robust link between the detection of CTCs and an elevated association between disease recurrence and metastasis [144,170].”
MethodModeling lung adenocarcinoma metastases using patient-derived organoids
Liu, Y., Lankadasari, M. B., Rosiene, J. A., Johnson, K. E., Zhou, J., Bapat, S., Chow-Tsang, L.-F., Tian, H., Mastrogiacomo, B., He, D., et al. (2024) · Cell Reports Medicine · doi:10.1016/j.xcrm.2024.101777 · Cited by 25
“48 However, given our interest in immune priming to enhance tumor cell immunogenicity, we used a PDO composed of pure tumor cells and a PBMC coculture system 51 to focus on the tumor cells exclusively and identify the most appropriate immune-priming strategy (chemotherapy or radiation).”
Li, P., Huang, M., Li, M., Li, G., Ma, Y., Zhao, Y. X., Wang, X., Zhang, Y., & Shi, C. (2025) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-025-03332-8 · Cited by 26
“Considering that PDO_3 is less sensitive to chemotherapy and targeted drugs, we constructed a co-culture model of organoids with PBMCs from autologous to test the effect of the PD-1 inhibitor pembrolizumab [32].”
Poggi, A. D., Villa, F., Fernandez, J. L. C., Costa, D., Zocchi, M. R., & Benelli, R. (2021) · Cancers · doi:10.3390/cancers13143417 · Cited by 25
Weitz, J., Tiriac, H., de Mendoza, T. H., Wascher, A. A., & Lowy, A. M. (2021) · Cancers · doi:10.3390/cancers13194991 · Cited by 27
“Organoid co-cultures enabled the study of cell–cell interactions and facilitated the testing of stromal-targeted therapeutics; however, these methods relied upon human cells that were typically not autologous or syngeneic [26,27].”
Lung Cancer Organoids: The Rough Path to Personalized Medicine
Rossi, R., Angelis, M. L. D., Xhelili, E., Sette, G., Eramo, A., Maria, R. D., Incani, U. C., Francescangeli, F., & Zeuner, A. (2022) · Cancers · doi:10.3390/cancers14153703 · Cited by 27
Genomic and Epigenomic Characterization of Tumor Organoid Models
Nam, C., Ziman, B., Sheth, M., Zhao, H., & Lin, D. (2022) · Cancers · doi:10.3390/cancers14174090 · Cited by 23
Chen, X., Sifakis, E. G., Robertson, S., Neo, S., Jun, S.-H., Tong, L., Tay, A. H. M., Lövrot, J., Hellgren, R., Margolin, S., et al. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2209856120 · Cited by 22
“Compared with the epithelial-only organoid models (15, 48), or coculture of peripheral blood cells with organoids (49), the BC WTCs preserve the primary tumor cells with their endogenous TME components (Fig.”
Xu, X., Wang, S., Zhou, J., Chen, J., Huang, Y., Kumari, R., Mao, B., Zheng, M., An, X., tu, X., et al. (2023) · PLoS ONE · doi:10.1371/journal.pone.0279821 · Cited by 26
Self-citationBioengineering Approaches for the Pancreatic Tumor Organoids Research and Application
Song, T., Kong, B., Liu, R., Luo, Y., Wang, Y., & Zhao, Y. (2023) · Advanced Healthcare Materials · doi:10.1002/adhm.202300984 · Cited by 24
Xiong, J., Dai, Y.-T., Wang, W., Zhang, H., Wang, C., Tong, Y., Cheng, S., Zhong, H., Yu, S., Jiang, L., et al. (2023) · 中国科学通报：英文版 · doi:10.1016/j.scib.2023.09.029 · Cited by 26
Wang, X., Dai, Z., Lin, X., Zou, X., Wang, R., Tasiheng, Y., Yan, Y., Ma, M., Chen, Y., Cheng, H., et al. (2024) · Cancer Letters · doi:10.1016/j.canlet.2024.216741 · Cited by 24
Rational Treatment of Metastatic Colorectal Cancer: A Reverse Tale of Men, Mice, and Culture Dishes
Avolio, M., & Trusolino, L. (2021) · Cancer Discovery · doi:10.1158/2159-8290.cd-20-1531 · Cited by 25
Dijkstra, J. J., Neikes, H. K., Rezaeifard, S., Ma, X., Voest, E. E., Tauriello, D. V. F., & Vermeulen, M. (2023) · Journal of Proteome Research · doi:10.1021/acs.jproteome.2c00551 · Cited by 23
Self-citationLi, Z., Ma, L., Gao, Z., Wang, X., Che, X., Zhang, P., Li, Y., Zhang, Q., Liu, T., Sun, Y., et al. (2024) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-024-03749-8 · Cited by 24
Building a Functional Salivary Gland for Cell-Based Therapy: More than Secretory Epithelial Acini
Barrows, C. M. L., Wu, D., Farach‐Carson, M. C., & Young, S. W. (2020) · Tissue Engineering Part A · doi:10.1089/ten.tea.2020.0184 · Cited by 23
Gendre, D. A., Ameti, E., Karenovicŝ, W., Perriraz, N., Triponez, F., & Serre‐Beinier, V. (2021) · Oncotarget · doi:10.18632/oncotarget.28134 · Cited by 24
Xie, F., Liu, Z., Wang, P., Cai, M., Li, Y., Yan, J., Lin, Q., & Luo, F. (2022) · Advanced Healthcare Materials · doi:10.1002/adhm.202102770 · Cited by 24
Engineered Microphysiological Systems for Testing Effectiveness of Cell-Based Cancer Immunotherapies
Campisi, M., Shelton, S. E., Chen, M., Kamm, R. D., Barbie, D. A., & Knelson, E. H. (2022) · Cancers · doi:10.3390/cancers14153561 · Cited by 24
Beelen, N. A., Aberle, M. R., Bruno, V., Damink, S. W. M. O., Bos, G. M. J., Rensen, S. S., & Wieten, L. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1133796 · Cited by 26
Landon‐Brace, N., Li, N. T., & McGuigan, A. P. (2023) · Advanced Healthcare Materials · doi:10.1002/adhm.202300903 · Cited by 25
Cholangiocarcinoma Disease Modelling Through Patients Derived Organoids
Amato, F., Rae, C. J., Prete, M. G., & Braconi, C. (2020) · Cells · doi:10.3390/cells9040832 · Cited by 23
Mechanoimmunology in the solid tumor microenvironment
Golo, M., Newman, P. L. H., Kempe, D., & Biro, M. (2024) · Biochemical Society Transactions · doi:10.1042/bst20231427 · Cited by 23
TIL Therapy in Lung Cancer: Current Progress and Perspectives
Hu, W., Bian, Y., & Ji, H. (2024) · Advanced Science · doi:10.1002/advs.202409356 · Cited by 25
Human Organoids and Their Application in Tumor Models, Disease Modeling, and Tissue Engineering
Song, S., Liu, Z., Wang, Y., & Gong, B. (2025) · Medicine Bulletin · doi:10.1002/mdb2.70001 · Cited by 25
Kidney organoid systems for studies of immune-mediated kidney diseases: challenges and opportunities
Stein, M. C., Braun, F., Krebs, C. F., & Bunders, M. J. (2021) · Cell and Tissue Research · doi:10.1007/s00441-021-03499-4 · Cited by 23
Greco, L., Rubbino, F., Morelli, A., Gaiani, F., Grizzi, F., de’Angelis, G. L., Malesci, A., & Laghi, L. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222111469 · Cited by 22
Fate mapping and scRNA sequencing reveal origin and diversity of lymph node stromal precursors
Lenti, E., Genovese, L., Bianchessi, S., Maurizio, A., Sain, S. B., di Lillo, A., Mattavelli, G., Harel, I., Bernassola, F., Hehlgans, T., et al. (2022) · Immunity · doi:10.1016/j.immuni.2022.03.002 · Cited by 22
Affolter, A., Kern, J., Bieback, K., Scherl, C., Rotter, N., & Lammert, A. (2022) · International Journal of Oncology · doi:10.3892/ijo.2022.5378 · Cited by 22
“The authors aim at discovering personalized determinants of response to immu‐ notherapy (117).”
BackgroundTumor Organoid Model and Its Pharmacological Applications in Tumorigenesis Prevention
Cao, X., Zheng, W., Qiang, Y., Yao, N., Zuo, F., & Qiu, S. (2022) · Current Molecular Pharmacology · doi:10.2174/1874467215666220803125822 · Cited by 23
Patrício, D., Santiago, J., Mano, J. F., & Fardilha, M. (2022) · WIREs Mechanisms of Disease · doi:10.1002/wsbm.1590 · Cited by 26
Targeting alternative splicing in cancer immunotherapy
Han, N., & Liu, Z. (2023) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2023.1232146 · Cited by 21
Luo, H., Wang, W., Mai, J., Yin, R., Cai, X., & Li, Q. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1267918 · Cited by 22
Mouse Models of Oncoimmunology in Hepatocellular Carcinoma
Bresnahan, E. R., Lindblad, K. E., de Galarreta, M. R., & Lujambio, A. (2020) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-19-2923 · Cited by 22
“other cancer types (ie, in colorectal cancer and lung cancer) (80).”
BackgroundModeling the tumor immune microenvironment for drug discovery using 3D culture
Lee, J. Y., & Chaudhuri, O. (2021) · APL Bioengineering · doi:10.1063/5.0030693 · Cited by 22
Microdissection tools to generate organoids for modeling the tumor immune microenvironment
Cordts, S. C., Yuki, K., Echeverri, M. F. H., Narasimhan, B., Kuo, C. J., & Tang, S. K. Y. (2024) · Microsystems & Nanoengineering · doi:10.1038/s41378-024-00756-8 · Cited by 21
“Prior studies have assembled organoids (or spheroids) from single tumor cells that lack stroma and cocultured them with peripheral immune populations 19 – 21 .”
Intestinal organoid coculture systems: current approaches, challenges, and future directions
Al-Qadami, G. H., Raposo, A. E., Chien, C.-C., Ma, C., Priebe, I. K., Hor, M., & Fung, K. Y. C. (2024) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00203.2024 · Cited by 24
Tseng, Y., & Boehm, J. S. (2019) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2019.02.007 · Cited by 21
Alkan, A., Hofving, T., Angenete, E., & Yrlid, U. (2021) · Biomarker Research · doi:10.1186/s40364-021-00313-9 · Cited by 22
Functional precision cancer medicine: drug sensitivity screening enabled by cell culture models
Flobak, Å., Skånland, S. S., Hovig, E. J., Taskén, K., & Russnes, H. G. (2022) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2022.08.009 · Cited by 26
Feng, B., Pan, B., Huang, J., Du, Y., Wang, X., Wu, J., Ma, R., Shen, B., Huang, G., & Feng, J. (2023) · Cancer Letters · doi:10.1016/j.canlet.2023.216224 · Cited by 21
Biomarkers and experimental models for cancer immunology investigation
Xu, H., Jia, Z., Liu, F., Li, J., Huang, Y., Jiang, Y., Pu, P., Shang, T., Tang, P., Zhou, Y., et al. (2023) · MedComm · doi:10.1002/mco2.437 · Cited by 21
“257,264 Tumor-reactive T cells with high cytotoxicity and specificity from peripheral blood can be efficiently enriched in coculture systems of autologous patient-derived organoids (PDOs) from patients with dMMR CRC and NSCLC. 257 Submerged models can also reproduce characteristic responses of…”
BackgroundYang, X., Yang, Y., Zhang, Z., & Li, M. (2023) · Langmuir · doi:10.1021/acs.langmuir.3c03046 · Cited by 21
Organoids as a tool to study homeostatic and pathological immune–epithelial interactions in the gut
Kromann, E. H., Peña‐Cearra, A., & Neves, J. F. (2024) · Clinical & Experimental Immunology · doi:10.1093/cei/uxad118 · Cited by 22
“Recent work has demonstrated how patient-derived tumour organoids are advancing treatments by selectively expanding autologous tumour-reactive T cells [88, 89] (Fig.”
BackgroundAdvancements in 3D In Vitro Models for Colorectal Cancer
Vitale, S., Calapà, F., Colonna, F., Luongo, F., Biffoni, M., Maria, R. D., & Fiori, M. E. (2024) · Advanced Science · doi:10.1002/advs.202405084 · Cited by 22
Preclinical pharmacology modeling of chimeric antigen receptor T therapies
Kumari, R., Ouyang, X., Wang, J., Xu, X., Zheng, M., An, X., & Li, Q. (2021) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2021.08.008 · Cited by 21
Tumor organoid model of colorectal cancer (Review)
Yang, C., Xiao, W., Wang, R., Hu, Y., Yi, K., Sun, X., Wang, G., & Xu, X. (2023) · Oncology Letters · doi:10.3892/ol.2023.13914 · Cited by 24
Breast cancer organoids and their applications for precision cancer immunotherapy
Guan, D., Liu, X., Shi, Q., He, B., Zheng, C., & Meng, X. (2023) · World Journal of Surgical Oncology · doi:10.1186/s12957-023-03231-2 · Cited by 20
“…to enhance clinical outcomes in BC, particularly for TNBC. Growing evidence suggests that BC is markedly heterogeneous concerning immune infiltration and the TME, and that lymphocyte infiltration into tumors is related to a better prognosis and better clinical responses to chemotherapy [82, 83].”
BackgroundPatient-derived glioblastoma organoids reflect tumor heterogeneity and treatment sensitivity
Verduin, M., Hoosemans, L., Vanmechelen, M., van Heumen, M., Piepers, J. A. F., Astuti, G., Ackermans, L. P. C. M., Schijns, O. E. M. G., Kampen, K. R., Tjan‐Heijnen, V. C. G., et al. (2023) · Neuro-Oncology Advances · doi:10.1093/noajnl/vdad152 · Cited by 20
“38 Additionally, co-culture systems of patient-derived GBM cells together with human embryonic stem-cell-derived cerebral organoids have been developed to mimic invasion and GBM–brain cell interaction.”
BackgroundMethodLeto, S. M., Grassi, E., Avolio, M., Vurchio, V., Cottino, F., Ferri, M., Zanella, E. R., Borgato, S., Corti, G., di Blasio, L., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-51909-2 · Cited by 20
“…models that preserve the overall tumor cellular contexture and architecture, including cocultures of tumoroids with autologous peripheral blood lymphocytes 62 or carcinoma-associated fi broblasts 63,64 , human air – liquid interface cohesive units 65 , and thin-slice tumor fragments 66 .”
Long-term maintenance of patient-specific characteristics in tumoroids from six cancer indications
Paul, C. D., Yankaskas, C., Thakuri, P. S., Balhouse, B. N., Salen, S., Bullock, A., Beam, S., Chatman, A., Djikeng, S., Yang, X. J., et al. (2025) · Scientific Reports · doi:10.1038/s41598-025-86979-9 · Cited by 19
“That said, murine-derived BME may itself cause reactivity of CD4 + T cells 62 , and the microenvironment in which tumoroid and immune cell co-culture assays are performed should be carefully considered.”
Madan, A., Saini, R., Dhiman, N., Juan, S., & Satapathy, M. K. (2025) · Organoids · doi:10.3390/organoids4040023 · Cited by 24
“Critical parameters such as PD-L1 expression, HLA class I presentation, interferon-gamma sensitivity, and tumor mutational burden can be interrogated under various conditions, including IFN-γ stimulation or co-culture with immune effector cells [157].”
Dominijanni, A. J., Mazzocchi, A. R., Shelkey, E., Forsythe, S. D., Devarasetty, M., & Söker, S. (2020) · Current Opinion in Biomedical Engineering · doi:10.1016/j.cobme.2020.03.005 · Cited by 20
Multimodal predictors for precision immunotherapy
Roelofsen, L. M., Kaptein, P., & Thommen, D. S. (2022) · Immuno-Oncology Technology · doi:10.1016/j.iotech.2022.100071 · Cited by 19
DeStefanis, R. A., Kratz, J. D., Olson, A. M., Sunil, A., DeZeeuw, A. K., Gillette, A. A., Sha, G. C., Johnson, K. A., Pasch, C. A., Clipson, L. J., et al. (2022) · Scientific Reports · doi:10.1038/s41598-022-08937-z · Cited by 21
Spatiotemporal T cell dynamics in a 3D bioprinted immunotherapy model
Morley, C. D., Flores, C., Drake, J., Moore, G. L., Mitchell, D. A., & Angelini, T. E. (2022) · Bioprinting · doi:10.1016/j.bprint.2022.e00231 · Cited by 21
Clinical applications of 3D normal and breast cancer organoids: A review of concepts and methods
Lewis, S. M., Callaway, M. K., & dos Santos, C. O. (2022) · Experimental Biology and Medicine · doi:10.1177/15353702221131877 · Cited by 20
Advancements in melanoma cancer metastasis models
Melo, L. M. N., Kumar, S., Riess, V., Szylo, K. J., Eisenburger, R. T., Schadendorf, D., Ubellacker, J. M., & Tasdogan, A. (2022) · Pigment Cell & Melanoma Research · doi:10.1111/pcmr.13078 · Cited by 20
“A key advantage of 3D organoids includes the ability to propagate and generate a biobank of organoids from different patients for future therapy analysis (Dijkstra et al., 2018; Jacob et al., 2020; Neal et al., 2018).”
BackgroundBourreau, C., Treps, L., Faure, S., Fradin, D., & Clere, N. (2023) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2023.108347 · Cited by 20
Intersection of nanomaterials and organoids technology in biomedicine
Shen, C., Zhang, Z., Li, X., Huang, Y.-P., Wang, Y., Zhou, H. R., Xiong, L., Wen, Y., Zou, H., & Liu, Z. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1172262 · Cited by 21
Divoux, J., Florent, R., Jacobs, M., Lequesne, J., Grellard, J., San, C., Grossi, S. M., Kerdja, K., Clarisse, B., Boudier, G., et al. (2023) · BMC Cancer · doi:10.1186/s12885-023-11362-8 · Cited by 23
Engineering Heterogeneous Tumor Models for Biomedical Applications
Wu, Z., Huang, D., Wang, J., Zhao, Y., Sun, W., & Shen, X. (2023) · Advanced Science · doi:10.1002/advs.202304160 · Cited by 19
Organoids: An Emerging Precision Medicine Model for Prostate Cancer Research
Waseem, M., & Wang, B. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25021093 · Cited by 21
“Additionally, previous studies have shown that co-culturing NSCLC or colon organoids with matched PBMC cells resulted in an increase in the CD8 + anti-tumor T cell population [94].”
BackgroundGao, C., Jiang, J., Zhao, J., Xu, Z. P., & Zhang, L. L. (2024) · Coordination Chemistry Reviews · doi:10.1016/j.ccr.2024.216109 · Cited by 23
Pappas, K., Choi, D., Sawyers, C. L., & Karthaus, W. R. (2019) · Journal of Visualized Experiments · doi:10.3791/60346 · Cited by 20
The potential application of organoids in breast cancer research and treatment
Ebrahimi, N., Esfahani, A. N., Samizade, S., Mansouri, A., Ghanaatian, M., Adelian, S., Shadman-Manesh, V., & Hamblin, M. R. (2021) · Human Genetics · doi:10.1007/s00439-021-02390-0 · Cited by 20
Chen, D., Xu, L., Xuan, M., Chu, Q., & Xue, C. (2024) · Clinical and Translational Medicine · doi:10.1002/ctm2.1802 · Cited by 20
“56 Using CRISPR-mediated mutagenesis, Coelho et al. 57 systematically explored the genetic landscapes of interferon γ (IFN-γ ) in colorectal cancer tumour organoids co-cultured with matched tumour-reactive T cells.”
BackgroundD’Amore, T., Zolfanelli, C., Lauciello, V., Ciancia, A. D., Vagliasindi, A., Smaoui, S., & Varzakas, T. H. (2025) · Microorganisms · doi:10.3390/microorganisms13061335 · Cited by 21
“Organoids derived from cancerous tissue (tumoroids) are particularly valuable for modeling tumor biology and drug responses [155–158].”
Intratumoural vaccination via checkpoint degradation-coupled antigen presentation
Han, Y., Ma, Y., Pei, M., Yin, S., Wang, J., Guo, L., Fang, Y., Guo, W., Deng, C. L., Zhao, S., et al. (2026) · Nature · doi:10.1038/s41586-025-09903-1 · Cited by 23
Phenotype transition of fibroblasts incorporated into patient‐derived oral carcinoma organoids
Chen, X., Li, R., Zhao, H., Wang, X., Shao, Z., & Shang, Z. (2021) · Oral Diseases · doi:10.1111/odi.14071 · Cited by 19
Wang, Z., Yu, Y., Wu, P., Ye, Q., Guo, Y., Zhang, X., Xi, L., Li, Q., Jin, Y., Zhou, D., et al. (2021) · Cell Death Discovery · doi:10.1038/s41420-022-01014-4 · Cited by 19
“Co-cultures of peripheral blood lymphocytes with PDOs have been used for screening immune checkpoint inhibitors [25].”
Wang, X., Chan, Y. S., Wong, K., Yoshitake, R., Sadava, D., Synold, T. W., Frankel, P. H., Twardowski, P. W., Lau, C., & Chen, S. (2023) · Cancers · doi:10.3390/cancers15030701 · Cited by 21
Head and neck cancer patient-derived tumouroid cultures: opportunities and challenges
Basnayake, B. W. M. T. J., Leo, P., Rao, S., Vasani, S. S., Kenny, L., Haass, N. K., & Punyadeera, C. (2023) · British Journal of Cancer · doi:10.1038/s41416-023-02167-4 · Cited by 23
“Additional supplements, such as antiCD28, anti-CD3, and IL-2 antibodies, have been suggested for the long-term preservation of immune cells [111, 117].”
BackgroundChan, W. S., Mo, X.-T., Ip, P. P. C., & Tse, K. Y. (2023) · Cancer Medicine · doi:10.1002/cam4.6521 · Cited by 20
“119 The enriched tumor-reactive T cells could then be used to kill the efficacy and mechanism of matched tumor organoids.”
BackgroundEstablishing mouse and human oral esophageal organoids to investigate the tumor immune response
Jiang, Y., Zhao, H., Kong, S., Zhou, D., Dong, J., Cheng, Y., Zhang, S., Wang, F., Kalra, A., Yang, N., et al. (2024) · Disease Models & Mechanisms · doi:10.1242/dmm.050319 · Cited by 19
Organoid models: the future companions of personalized drug development
Piraino, F., Costa, M., Meyer, M., Cornish, G. H., Ceroni, C., Garnier, V., Hoehnel, S., & Brandenberg, N. (2024) · Biofabrication · doi:10.1088/1758-5090/ad3e30 · Cited by 21
“To address these issues, co-culturing tumor organoids with autologous immune components such as T cell lymphocytes (T cells) became a compelling tool for understanding interactions between tumor cells and the immune system [54, 102, 103].”
Sun, Y., Maggs, L., Panda, A., Wright, S. J., Cicerchia, A. M., Jenney, A., Perricone, M. D., Mills, C. E., Cattaneo, G., Ventin, M., et al. (2025) · Cancer Immunology Research · doi:10.1158/2326-6066.cir-23-1011 · Cited by 17
Lees, E. A., Forbester, J. L., Forrest, S., Kane, L., Goulding, D., & Dougan, G. (2019) · Journal of Visualized Experiments · doi:10.3791/59478 · Cited by 19
Advancing cancer immunotherapy: a vision for the field
de Miranda, N. F. C. C., & Trajanoski, Z. (2019) · Genome Medicine · doi:10.1186/s13073-019-0662-6 · Cited by 19
Ren, J., Wang, C., Ye, M., Yuan, Q., Wang, C., & Feng, X. (2022) · Combinatorial Chemistry & High Throughput Screening · doi:10.2174/1386207325666220404125228 · Cited by 19
Du, L., Zheng, Z., Zhang, K., Sun, H., Lü, Y., Sun, M., Pang, M., Jiang, S., He, Y., Du, S., et al. (2025) · Molecular Cancer · doi:10.1186/s12943-025-02466-9 · Cited by 18
“Prior studies confirm that co-culturing tumor organoids with immune cells effectively recapitulates the tumor immune microenvironment (TIME) [63–66].”
Single-cell sequencing and organoids: applications in organ development and disease
Li, T., Yin, J., Hao, Y., Gao, W., Li, Q., Feng, Q., Tao, B., Hao, M., Liu, Y., Lin, C., et al. (2025) · Molecular Biomedicine · doi:10.1186/s43556-025-00364-6 · Cited by 20
“The maturity of organoids is often limited by the imper-fections of the culture systems [88].”
Vascularizing organoids-on-chip for perfused and personalized models
Menzani, B., Gea, P. D., Gidrol, X., & Tubbs, E. (2026) · Lab on a Chip · doi:10.1039/d5lc00890e · Cited by 20
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
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
