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3D model for CAR‐mediated cytotoxicity using patient‐derived colorectal cancer organoids
Open accessAbstract
Immunotherapy using chimeric antigen receptor (CAR)-engineered lymphocytes has shown impressive results in leukemia. However, for solid tumors such as colorectal cancer (CRC), new preclinical models are needed that allow to test CAR-mediated cytotoxicity in a tissue-like environment. Here, we developed a platform to study CAR cell cytotoxicity against 3-dimensional (3D) patient-derived colon organoids. Luciferase-based measurement served as a quantitative read-out for target cell viability. Additionally, we set up a confocal live imaging protocol to monitor effector cell recruitment and cytolytic activity at a single organoid level. As proof of principle, we demonstrated efficient targeting in diverse organoid models using CAR-engineered NK-92 cells directed toward a ubiquitous epithelial antigen (EPCAM). Tumor antigen-specific cytotoxicity was studied with CAR-NK-92 cells targeting organoids expressing EGFRvIII, a neoantigen found in several cancers. Finally, we tested a novel CAR strategy targeting FRIZZLED receptors that show increased expression in a subgroup of CRC tumors. Here, comparative killing assays with normal organoids failed to show tumor-specific activity. Taken together, we report a sensitive in vitro platform to evaluate CAR efficacy and tumor specificity in a personalized manner.
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“Non-tumor cells from adjacent normal tissue in biopsies or surgically resected samples can be used to develop control healthy organoids to confirm the tumor-specific efficacy of the tested drugs155.”
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Cites
Cancer incidence and mortality worldwide: Sources, methods and major patterns in GLOBOCAN 2012
Ferlay, J., Soerjomataram, I., Dikshit, R., Eser, S., Mathers, C., Rebelo, M., Parkin, D. M., Forman, D., & Bray, F. (2015) · International Journal of Cancer · doi:10.1002/ijc.29210 · Cited by 28,766
PD-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
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
Type, Density, and Location of Immune Cells Within Human Colorectal Tumors Predict Clinical Outcome
Galon, J., Costes, A., Sanchez-Cabo, F., Kirilovsky, A., Mlecnik, B., Lagorce-Pagès, C., Tosolini, M., Camus, M., Berger, A., Wind, P., et al. (2006) · Science · doi:10.1126/science.1129139 · Cited by 6,516
Improved vectors and genome-wide libraries for CRISPR screening
Sanjana, N. E., Shalem, O., & Zhang, F. (2014) · Nature Methods · doi:10.1038/nmeth.3047 · Cited by 5,239
Charoentong, P., Finotello, F., Angelova, M., Mayer, C., Efremova, M., Rieder, D., Hackl, H., & Trajanoski, Z. (2017) · Cell Reports · doi:10.1016/j.celrep.2016.12.019 · Cited by 5,041
Sato, T., Stange, D. E., Ferrante, M., Vries, R. G. J., van Es, J. H., van den Brink, S., van Houdt, W. J., Pronk, A., van Gorp, J., Siersema, P. D., et al. (2011) · Gastroenterology · doi:10.1053/j.gastro.2011.07.050 · Cited by 3,753
Organoid Models and Applications in Biomedical Research
Xinaris, C., Brizi, V., & Remuzzi, G. (2015) · The Nephron journals/Nephron journals · doi:10.1159/000433566 · Cited by 3,519
Chimeric Antigen Receptor Therapy
June, C. H., & Sadelain, M. (2018) · New England Journal of Medicine · doi:10.1056/nejmra1706169 · Cited by 2,411
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
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Zhao, Z., Chen, X., Dowbaj, A. M., Sljukic, A., Bratlie, K., Lin, L., Fong, E. L. S., Balachander, G. M., Chen, Z., Soragni, A., et al. (2022) · Nature Reviews Methods Primers · doi:10.1038/s43586-022-00174-y · Cited by 1,082
NK cell-based cancer immunotherapy: from basic biology to clinical development
Liu, S., Galat, V., Galat4, Y., Lee, Y. K. A., Wainwright, D., & Wu, J. (2021) · Journal of Hematology & Oncology · doi:10.1186/s13045-020-01014-w · Cited by 689
Organoid and Spheroid Tumor Models: Techniques and Applications
Gunti, S., Hoke, A. T. K., Vu, K., & London, N. R. (2021) · Cancers · doi:10.3390/cancers13040874 · Cited by 525
Next-generation cancer organoids
LeSavage, B. L., Suhar, R. A., Broguière, N., Lütolf, M. P., & Heilshorn, S. C. (2021) · Nature Materials · doi:10.1038/s41563-021-01057-5 · Cited by 479
Organoid Models of Tumor Immunology
Yuki, K., Cheng, N., Nakano, M., & Kuo, C. J. (2020) · Trends in Immunology · doi:10.1016/j.it.2020.06.010 · Cited by 418
Organoids in immunological research
Bar-Ephraim, Y. E., Kretzschmar, K., & Clevers, H. (2020) · Nature Reviews Immunology · doi:10.1038/s41577-019-0248-y · Cited by 361
Immunotherapy for Ovarian Cancer: Adjuvant, Combination, and Neoadjuvant
Yang, C. Q., Xia, B.-R., Zhang, Z.-C., Zhang, Y., Lou, G., & Jin, W. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.577869 · Cited by 358
Tumor organoids: Opportunities and challenges to guide precision medicine
Veninga, V., & Voest, E. E. (2021) · Cancer Cell · doi:10.1016/j.ccell.2021.07.020 · Cited by 339
AI-powered therapeutic target discovery
Pun, F. W., Ozerov, I. V., & Zhavoronkov, A. (2023) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2023.06.010 · Cited by 341
CAR-T Cells Hit the Tumor Microenvironment: Strategies to Overcome Tumor Escape
Rodríguez-García, A., Palazón, A., Noguera-Ortega, E., Powell, D. J., & Guedan, S. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.01109 · Cited by 326
Cancer organoids 2.0: modelling the complexity of the tumour immune microenvironment
Polak, R., Zhang, E., & Kuo, C. J. (2024) · Nature reviews. Cancer · doi:10.1038/s41568-024-00706-6 · Cited by 347
Modeling neoplastic disease with spheroids and organoids
Zanoni, M., Cortesi, M., Zamagni, A., Arienti, C., Pignatta, S., & Tesei, A. (2020) · Journal of Hematology & Oncology · doi:10.1186/s13045-020-00931-0 · Cited by 280
Uncovering the mode of action of engineered T cells in patient cancer organoids
Dekkers, J. F., Alieva, M., Cleven, A., Keramati, F., Wezenaar, A. K. L., van Vliet, E. J., Puschhof, J., Brázda, P., Johanna, I., Meringa, A. D., et al. (2022) · Nature Biotechnology · doi:10.1038/s41587-022-01397-w · Cited by 241
Jacob, F., Ming, G., & Song, H. (2020) · Nature Protocols · doi:10.1038/s41596-020-0402-9 · Cited by 219
Burger, M. C., Zhang, C., Harter, P. N., Romanski, A., Straßheimer, F., Senft, C., Tonn, T., Steinbach, J. P., & Wels, W. S. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.02683 · Cited by 211
Self-citationDeveloping Organoids from Ovarian Cancer as Experimental and Preclinical Models
Maenhoudt, N., Defraye, C., Boretto, M., Jan, Z., Heremans, R., Boeckx, B., Hermans, F., Arijs, I., Cox, B., Van Nieuwenhuysen, E., et al. (2020) · Stem Cell Reports · doi:10.1016/j.stemcr.2020.03.004 · Cited by 186
Applications of organoids for cancer biology and precision medicine
Lo, Y.-H., Karlsson, K., & Kuo, C. J. (2020) · Nature Cancer · doi:10.1038/s43018-020-0102-y · Cited by 182
Magré, L., Verstegen, M. M. A., Buschow, S. I., van der Laan, L. J. W., Peppelenbosch, M. P., & Desai, J. (2023) · Journal for ImmunoTherapy of Cancer · doi:10.1136/jitc-2022-006290 · Cited by 201
Human organoids: New strategies and methods for analyzing human development and disease
Corsini, N. S., & Knoblich, J. A. (2022) · Cell · doi:10.1016/j.cell.2022.06.051 · Cited by 176
Somatic cell-derived organoids as prototypes of human epithelial tissues and diseases
Fujii, M., & Sato, T. (2020) · Nature Materials · doi:10.1038/s41563-020-0754-0 · Cited by 176
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Qu, J., Kalyani, F. S., Liu, L., Cheng, T., & Chen, L. (2021) · 癌症:英文版 · doi:10.1002/cac2.12224 · Cited by 173
Expansion of T memory stem cells with superior anti-tumor immunity by Urolithin A-induced mitophagy
Denk, D., Petrocelli, V., Conche, C., Drachsler, M. W., Ziegler, P. K., Braun, A., Kress, A., Nicolas, A. M., Mohs, K., Becker, C., et al. (2022) · Immunity · doi:10.1016/j.immuni.2022.09.014 · Cited by 153
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Gut organoids: mini-tissues in culture to study intestinal physiology and disease
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Organoids in gastrointestinal diseases: From experimental models to clinical translation
Günther, C., Winner, B., Neurath, M. F., & Stappenbeck, T. S. (2022) · Gut · doi:10.1136/gutjnl-2021-326560 · Cited by 145
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Grönholm, M., Feodoroff, M., Antignani, G., Martins, B., Hamdan, F., & Cerullo, V. (2021) · Cancer Research · doi:10.1158/0008-5472.can-20-4026 · Cited by 146
Organoid based personalized medicine: from bench to bedside
Li, Y., Tang, P., Cai, S., Peng, J., & Hua, G. (2020) · Cell Regeneration · doi:10.1186/s13619-020-00059-z · Cited by 149
Patient-derived organoid (PDO) platforms to facilitate clinical decision making
Liu, L., Yu, L., Li, Z., Li, W., & Huang, W. (2021) · Journal of Translational Medicine · doi:10.1186/s12967-020-02677-2 · Cited by 145
Harane, S. E., Zidi, B., Harane, N. E., Krause, K., Matthes, T., & Preynat‐Seauve, O. (2023) · Cells · doi:10.3390/cells12071001 · Cited by 135
Cancer research using organoid technology
Kretzschmar, K. (2021) · Journal of Molecular Medicine · doi:10.1007/s00109-020-01990-z · Cited by 120
Farin, H. F., Mosa, M. H., Ndreshkjana, B., Grebbin, B. M., Ritter, B., Menche, C., Kennel, K. B., Ziegler, P. K., Szabó, L., Bollrath, J., et al. (2023) · Cancer Discovery · doi:10.1158/2159-8290.cd-23-0050 · Cited by 120
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Maulana, T. I., Teufel, C., Cipriano, M., Roosz, J., Lazarevski, L., van den Hil, F. E., Scheller, L., Orlova, V. V., Koch, A., Hudecek, M., et al. (2024) · Cell stem cell · doi:10.1016/j.stem.2024.04.018 · Cited by 125
Functional precision oncology using patient-derived assays: bridging genotype and phenotype
van Renterghem, A. W. J., van de Haar, J., & Voest, E. E. (2023) · Nature Reviews Clinical Oncology · doi:10.1038/s41571-023-00745-2 · Cited by 121
Seidlitz, T., Koo, B., & Stange, D. E. (2020) · Cell Death and Differentiation · doi:10.1038/s41418-020-00662-2 · Cited by 112
Cancer organoid co-culture model system: Novel approach to guide precision medicine
Yuan, J., Li, X., & Yu, S. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2022.1061388 · Cited by 114
Xiang, D., He, A., Zhou, R., Wang, Y., Xiao, X., Gong, T., Kang, W., Lin, X., Wang, X., Consortium11, P.-B. D., et al. (2024) · Theranostics · doi:10.7150/thno.96027 · Cited by 108
Glioblastoma Organoids: Pre-Clinical Applications and Challenges in the Context of Immunotherapy
Klein, E., Hau, A., Oudin, A., Golebiewska, A., & Niclou, S. P. (2020) · Frontiers in Oncology · doi:10.3389/fonc.2020.604121 · Cited by 102
Tumor organoid-immune co-culture models: exploring a new perspective of tumor immunity
Wang, J., Tao, X., Zhu, J., Dai, Z., Du, Y., Xie, Y., Chu, X., Fu, G., & Lei, Z. (2025) · Cell Death Discovery · doi:10.1038/s41420-025-02407-x · Cited by 101
The Use of Stem Cell-Derived Organoids in Disease Modeling: An Update
Azar, J. H., Bahmad, H. F., Daher, D., Moubarak, M. M., Hadadeh, O., Monzer, A., Bitar, S. A., Jamal, M., Al‐Sayegh, M., & Abou-Kheir, W. G. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22147667 · Cited by 106
3D cancer models: One step closer to in vitro human studies
Manduca, N., Maccafeo, E., Maria, R. D., Sistigu, A., & Musella, M. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1175503 · Cited by 103
The next wave of cellular immunotherapies in pancreatic cancer
Yeo, D., Giardina, C., Saxena, P., & Rasko, J. E. J. (2022) · Molecular Therapy — Oncolytics · doi:10.1016/j.omto.2022.01.010 · Cited by 95
Zhang, S., Iyer, S., Ran, H., Dolgalev, I., Gu, S. S., Wei, W., Foster, C., Loomis, C. A., Olvera, N., Dao, F., et al. (2020) · Cancer Discovery · doi:10.1158/2159-8290.cd-20-0455 · Cited by 89
Harter, M. F., Recaldin, T., Gérard, R., Avignon, B., Bollen, Y., Esposito, C., Guja-Jarosz, K., Kromer, K., Filip, A. M., Aubert, J., et al. (2023) · Nature Biomedical Engineering · doi:10.1038/s41551-023-01156-5 · Cited by 93
Organoid Models for Precision Cancer Immunotherapy
Sun, C., Lan, H., Fang, X., Yang, X., & Jin, K. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.770465 · Cited by 90
Zhu, J., Ji, L., Chen, Y., Li, H., Huang, M., Dai, Z., Wang, J., Xiang, D., Fu, G., Lei, Z., et al. (2023) · Cell Death Discovery · doi:10.1038/s41420-023-01354-9 · Cited by 92
Immunocompetent cancer-on-chip models to assess immuno-oncology therapy
Maulana, T. I., Kromidas, E., Wallstabe, L., Cipriano, M., Alb, M., Zaupa, C., Hudecek, M., Fogal, B., & Loskill, P. (2021) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2021.03.015 · Cited by 86
Surmounting the obstacles that impede effective CAR T cell trafficking to solid tumors
Donnadieu, E., Dupré, L., Pinho, L. G., & Cotta-de-Almeida, V. (2020) · Journal of Leukocyte Biology · doi:10.1002/jlb.1mr0520-746r · Cited by 85
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Vilgelm, A. E., Bergdorf, K. N., Wolf, M. M., Bharti, V., Shattuck-Brandt, R. L., Blevins, A., Jones, C. Y., Phifer, C. J., Lee, M. A., Lowe, C. L., et al. (2020) · iScience · doi:10.1016/j.isci.2020.101408 · Cited by 78
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Fitzgerald, A. A., Li, E., & Weiner, L. M. (2020) · Cancers · doi:10.3390/cancers13010056 · Cited by 85
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Mu, P., Zhou, S., Lv, T., Xia, F., Shen, L., Wan, J., Wang, Y., Zhang, H., Cai, S., Peng, J., et al. (2023) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-023-02653-w · Cited by 87
Bridging live-cell imaging and next-generation cancer treatment
Alieva, M., Wezenaar, A. K. L., Wehrens, E. J., & Rios, A. C. (2023) · Nature reviews. Cancer · doi:10.1038/s41568-023-00610-5 · Cited by 84
Applications of human organoids in the personalized treatment for digestive diseases
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Addressing Patient Specificity in the Engineering of Tumor Models
Bray, L. J., Hutmacher, D. W., & Bock, N. (2019) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2019.00217 · Cited by 79
Ronteix, G., Jain, S., Angély, C., Cazaux, M., Khazen, R., Bousso, P., & Baroud, C. N. (2022) · Nature Communications · doi:10.1038/s41467-022-30575-2 · Cited by 71
Engineering microphysiological immune system responses on chips
Miller, C. P., Shin, W., Ahn, E. H., Kim, H. J., & Kim, D.-H. (2020) · Trends in biotechnology · doi:10.1016/j.tibtech.2020.01.003 · Cited by 74
Directing CAR T cells towards the tumor vasculature for the treatment of solid tumors
Akbari, P., Katsarou, A., Daghighian, R., van Mil, L. W. H. G., Huijbers, E. J. M., Griffioen, A. W., & B, J. R. V. B. (2022) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2022.188701 · Cited by 72
Advances in colon cancer research: in vitro and animal models
Lannagan, T. R. M., Jackstadt, R., Leedham, S. J., & Sansom, O. J. (2021) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2020.12.003 · Cited by 74
Pozzi, S., Scomparin, A., Dangoor, S. I., Ajamil, D. R., Ofek, P., Neufeld, L., Krivitsky, A., Vaskovich‐Koubi, D., Kleiner, R., Dey, P., et al. (2021) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2021.04.001 · Cited by 75
Patient‐derived cancer organoids for drug screening: Basic technology and clinical application
Ren, X., Chen, W., Yang, Q., Li, X., & Xu, L. (2022) · Journal of Gastroenterology and Hepatology · doi:10.1111/jgh.15930 · Cited by 73
Organoids and Colorectal Cancer
Barbáchano, A., Fernández‐Barral, A., Bustamante‐Madrid, P., Prieto, I., Rodríguez-Salas, N., Larriba, M. J., & Múñoz, A. (2021) · Cancers · doi:10.3390/cancers13112657 · Cited by 74
Three-dimensional colon cancer organoids model the response to CEA-CD3 T-cell engagers
Teijeira, Á., Miguéliz, I., Garasa, S., Karanikas, V., Luri‐Rey, C., Cirella, A., Olivera, I., Cañamero, M., Álvarez, M., Ochoa, M. C., et al. (2022) · Theranostics · doi:10.7150/thno.63359 · Cited by 67
Preclinical Evaluation of CAR T Cell Function: In Vitro and In Vivo Models
Si, X., Xiao, L., Brown, C. E., & Wang, D. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23063154 · Cited by 70
Jeong, S. Y., & Kang, M. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241914609 · Cited by 74
Organoid models of glioblastoma: advances, applications and challenges.
Zhang, C., Jin, M.-Z., Zhao, J., Chen, J., & Jin, W. (2020) · PubMed Central · Cited by 66
Self-citationWang, W., Yuan, T., Ma, L., Zhu, Y., Bao, J., Zhao, X., Zhao, Y., Zong, Y., Zhang, Y., Yang, S., et al. (2022) · Advanced Science · doi:10.1002/advs.202105810 · Cited by 63
CAR T Cell Locomotion in Solid Tumor Microenvironment
Nguyen, D., Ogando‐Rivas, E., Liu, R., Wang, T., Rubin, J. A., Jin, L., Tao, H., Sawyer, W. W., Méndez‐Gómez, H. R., Cascio, M., et al. (2022) · Cells · doi:10.3390/cells11121974 · Cited by 65
Organoid models of the tumor microenvironment and their applications
Xia, T., Du, W., Chen, X., & Zhang, Y.-N. (2021) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.16578 · Cited by 63
Time to evolve: predicting engineered T cell-associated toxicity with next-generation models
Donnadieu, E., Luu, M., Alb, M., Anliker, B., Arcangeli, S., Bonini, C., Angelis, B. D., Choudhary, R., Espie, D., Galy, A. H. M., et al. (2022) · Journal for ImmunoTherapy of Cancer · doi:10.1136/jitc-2021-003486 · Cited by 66
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Pfohl, U., Pflaume, A., Regenbrecht, M., Finkler, S., Adelmann, Q. G., Reinhard, C., Regenbrecht, C. R. A., & Wedeken, L. (2021) · Cells · doi:10.3390/cells10040928 · Cited by 68
Grunewald, L., Lam, T., Andersch, L., Klaus, A., Schwiebert, S., Winkler, A., Gauert, A., Hagemann, A. I. H., Astrahantseff, K., Klironomos, F., et al. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.689697 · Cited by 60
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Fang, Z., Li, P., Du, F., Shang, L., & Li, L. (2023) · Experimental Hematology and Oncology · doi:10.1186/s40164-023-00433-y · Cited by 68
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Zhang, Y., Zhou, W., Yang, J., Yang, J., & Wang, W. (2023) · Experimental Hematology and Oncology · doi:10.1186/s40164-023-00431-0 · Cited by 58
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Franchi-Mendes, T., Eduardo, R., Domenici, G., & Brito, C. (2021) · Cancers · doi:10.3390/cancers13184610 · Cited by 59
Vornholz, L., Isay, S. E., Kurgyis, Z., Strobl, D. C., Loll, P., Mosa, M. H., Luecken, M. D., Sterr, M., Lickert, H., Winter, C., et al. (2023) · Science Advances · doi:10.1126/sciadv.add8564 · Cited by 60
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Kim, S., van de Wetering, M., Clevers, H. C., & Sanders, K. (2025) · Trends in cancer · doi:10.1016/j.trecan.2025.03.005 · Cited by 62
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Ma, X., Wang, Q. L., Li, G., Li, H., Xu, S., & Pang, D. (2023) · Genes & Diseases · doi:10.1016/j.gendis.2023.02.052 · Cited by 62
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Li, T., Niu, M., Zhang, W., Qin, S., Zhou, J., & Yi, M. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1361194 · Cited by 61
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Metadata
- Authors
- Schnalzger, T. E., de Groot, M. H., Zhang, C., Mosa, M. H., Michels, B. E., Röder, J., Darvishi, T., Wels, W. S., & Farin, H. F.
- Affiliations
- University of Konstanz (DE)
- German Cancer Research Center (DE)
- Goethe University Frankfurt (DE)
- Corresponding author
- Farin, Henner F
- ORCID
- Venue
- The EMBO Journal
- Published
- 2019-04-29
- Volume
- 38
- Issue
- 12
- ISSN
- 0261-4189 (ISSN-L)
- 1460-2075
- PMC
- PMC6576164
- OpenAlex
- W2942656692
- Cited by
- 354
- References
- 57
- Citations by year
- 2026: 45 · 2025: 60 · 2024: 62 · 2023: 63 · 2022: 47 · 2021: 41 · 2020: 29 · 2019: 7
- FWCI
- 12.96
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- The EMBO Journal (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Frankfurt Cancer Institute (III L 5 ‐ 519/03/03.001 ‐ (0015))
- German Cancer Consortium
- Topics
- Health Sciences › Medicine › Oncology › CAR-T cell therapy research
- Life Sciences › Immunology and Microbiology › Immunology › Immune Cell Function and Interaction
- Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
- Keywords
- chimeric antigen receptor, colorectal cancer, 3D organoids, EpCAM, EGFRvIII, Frizzled receptors, tumor antigen specificity, luciferase reporter
- MeSH terms
- Receptors, Chimeric Antigen, Cells, Cultured, Cytotoxicity, Immunologic, Humans, Models, Biological, Organoids, Receptors, Antigen, T-Cell, Colorectal Neoplasms, Genetic Therapy, Immunotherapy, Adoptive, Tissue Culture Techniques, Tissue Scaffolds, HEK293 Cells, Primary Cell Culture
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