Tumor-derived spheroids: Relevance to cancer stem cells and clinical applications
Open accessAbstract
Recently, many types of in vitro 3-D culture systems have been developed to recapitulate the in vivo growth conditions of cancer. The cancer 3-D culture methods aim to preserve the biological characteristics of original tumors better than conventional 2-D monolayer cultures, and include tumor-derived organoids, tumor-derived spheroids, organotypic multicellular spheroids, and multicellular tumor spheroids. The 3-D culture methods differ in terms of cancer cell sources, protocols for cell handling, and the required time intervals. Tumor-derived spheroids are unique because they are purposed for the enrichment of cancer stem cells (CSCs) or cells with stem cell-related characteristics. These spheroids are grown as floating spheres and have been used as surrogate systems to evaluate the CSC-related characteristics of solid tumors in vitro. Because eradication of CSCs is likely to be of clinical importance due to their association with the malignant nature of cancer cells, such as tumorigenicity or chemoresistance, the investigation of tumor-derived spheroids may provide invaluable clues to fight against cancer. Spheroid cultures have been established from cancers including glioma, breast, colon, ovary, and prostate cancers, and their biological and biochemical characteristics have been investigated by many research groups. In addition to the investigation of CSCs, tumor-derived spheroids may prove to be instrumental for a high-throughput screening platform or for the cultivation of CSC-related tumor cells found in the circulation or body fluids.
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3D patient-derived tumor models of CRC allow maintenance and expansion of functionally relevant cell subfractions and harbor the patients' individual genetic lesions.
“3D patient-derived tumor models of CRC (i.e., organoid and spheroid cultures) allow maintenance and expansion of functionally relevant cell subfractions and harbor the patients' individual genetic lesions (Ishiguro et al., 2017;van de Wetering et al., 2015).”
From Degradation of CCNK/CDK12 is a druggable vulnerability of colorectal cancer (2021) · cites this paper as Ishiguro et al., 2017
TICs that have the capacity to self-renew and maintain long-term tumor growth are usually rare within the tumor mass but highly enriched within spheroid cultures.
“Moreover, TICs that have the capacity to self-renew and maintain long-term tumor growth are usually rare within the tumor mass but highly enriched within spheroid cultures (Dieter et al., 2011;Ishiguro et al., 2017).”
From Degradation of CCNK/CDK12 is a druggable vulnerability of colorectal cancer (2021) · cites this paper as Ishiguro et al., 2017
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Stearoyl-CoA Desaturase 1 as a Therapeutic Target for the Treatment of Cancer
Tracz‐Gaszewska, Z., & Dobrzyń, P. (2019) · Cancers · doi:10.3390/cancers11070948 · Cited by 248 · see citing works
Podoplanin in Inflammation and Cancer
Quintanilla, M., Montero-Montero, L., Renart, J., & Martín-Villar, E. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20030707 · Cited by 235 · see citing works
Weng, C.-H., Chen, L.-Y., Lin, Y., Shih, J., Lin, Y.-C., Tseng, R.-Y., Chiu, A.-C., Yeh, Y.-H., Liu, C., Lin, Y., et al. (2018) · Oncogene · doi:10.1038/s41388-018-0454-2 · Cited by 232 · see citing works
Multicellular Tumor Spheroids (MCTS) as a 3D In Vitro Evaluation Tool of Nanoparticles
Lu, H., & Stenzel, M. H. (2018) · Small · doi:10.1002/smll.201702858 · Cited by 229 · see citing works
Modeling tumor cell adaptations to hypoxia in multicellular tumor spheroids
Riffle, S., & Hegde, R. S. (2017) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-017-0570-9 · Cited by 225 · see citing works
Zhou, Z., Cong, L., & Cong, X. (2021) · Frontiers in Oncology · doi:10.3389/fonc.2021.762184 · Cited by 181 · see citing works
Hua, F., Shang, S., Yang, Y.-W., Zhang, H., Xu, T., Yu, J., Zhou, D., Cui, B., Li, K., Lv, X., et al. (2018) · Gastroenterology · doi:10.1053/j.gastro.2018.10.031 · Cited by 172 · see citing works
m6A-RNA Demethylase FTO Inhibitors Impair Self-Renewal in Glioblastoma Stem Cells
Huff, S. E., Tiwari, S. K., Gonzalez, G. M., Wang, Y., & Rana, T. M. (2021) · ACS Chemical Biology · doi:10.1021/acschembio.0c00841 · Cited by 169 · see citing works
Patient-Derived Glioma Models: From Patients to Dish to Animals
da Hora, C. C., Schweiger, M. W., Wurdinger, T. D., & Tannous, B. A. (2019) · Cells · doi:10.3390/cells8101177 · Cited by 153 · see citing works
Promising Applications of Tumor Spheroids and Organoids for Personalized Medicine
Gilazieva, Z., Ponomarev, A. S., Rutland, C. S., Rizvanov, A. A., & Solovyeva, V. V. (2020) · Cancers · doi:10.3390/cancers12102727 · Cited by 150 · see citing works
Understanding cell‐cell communication and signaling in the colorectal cancer microenvironment
AlMusawi, S., Ahmed, M., & Nateri, A. S. (2021) · Clinical and Translational Medicine · doi:10.1002/ctm2.308 · Cited by 150 · see citing works
Yi, Y., Kim, H. J., Zheng, M., Mi, P., Naito, M., Kim, B. S., Min, H. S., Hayashi, K., Perche, F., Toh, K., et al. (2019) · Journal of Controlled Release · doi:10.1016/j.jconrel.2019.01.006 · Cited by 127 · see citing works
Ki-67 regulates global gene expression and promotes sequential stages of carcinogenesis
Mrouj, K., Andrés-Sánchez, N., Dubra, G., Singh, P., Sobecki, M., Chahar, D., Alghoul, E., Aznar, A. B., Prieto, S., Pirot, N., et al. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2026507118 · Cited by 127 · see citing works
Lee, J. M., Park, D. Y., Yang, L., Kim, E. J., Ahrberg, C. D., Lee, K., & Chung, B. G. (2018) · Scientific Reports · doi:10.1038/s41598-018-35216-7 · Cited by 126 · see citing works
Management and potentialities of primary cancer cultures in preclinical and translational studies
Miserocchi, G., Mercatali, L., Liverani, C., Vita, A. D., Spadazzi, C., Pieri, F., Bongiovanni, A., Recine, F., Amadori, D., & Ibrahim, T. (2017) · Journal of Translational Medicine · doi:10.1186/s12967-017-1328-z · Cited by 123 · see citing works
Bae, H., Song, G., & Lim, W. (2020) · Pharmaceutics · doi:10.3390/pharmaceutics12060488 · Cited by 123 · see citing works
Organoids with cancer stem cell-like properties secrete exosomes and HSP90 in a 3D nanoenvironment
Eguchi, T., Sogawa, C. A., Okusha, Y., Uchibe, K., Iinuma, R., Ono, K., Nakano, K., Murakami, J., Itoh, M., Arai, K., et al. (2018) · PLoS ONE · doi:10.1371/journal.pone.0191109 · Cited by 118 · see citing works
Gheytanchi, E., Naseri, M., Karimi‐Busheri, F., Atyabi, F., Mirsharif, E. S., Bozorgmehr, M., Ghods, R., & Madjd, Z. (2021) · Cancer Cell International · doi:10.1186/s12935-021-01898-9 · Cited by 118 · see citing works
3D Bioprinting of Tumor Models for Cancer Research
Kang, Y., Datta, P., Shanmughapriya, S., & Ozbolat, I. T. (2020) · ACS Applied Bio Materials · doi:10.1021/acsabm.0c00791 · Cited by 112 · see citing works
Targeting post-translational histone modifying enzymes in glioblastoma
Kunadis, E., Lakiotaki, E., Korkolopoulou, P. A., & Piperi, C. (2020) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2020.107721 · Cited by 111 · see citing works
Advances in Stigmasterol on its anti-tumor effect and mechanism of action
Zhang, X., Wang, J., Zhu, L., Wang, X., Meng, F., Xia, L., & Zhang, H. (2022) · Frontiers in Oncology · doi:10.3389/fonc.2022.1101289 · Cited by 109 · see citing works
Natural and Synthetic Biomaterials for Engineering Multicellular Tumor Spheroids
Kamatar, A., Gunay, G., & Acar, H. (2020) · Polymers · doi:10.3390/polym12112506 · Cited by 100 · see citing works
Evolution of the Experimental Models of Cholangiocarcinoma
Massa, A., Varamo, C., Vita, F., Tavolari, S., Neia, C. P., Brandi, G., Rizzo, A., Cavalloni, G., & Aglietta, M. (2020) · Cancers · doi:10.3390/cancers12082308 · Cited by 95 · see citing works
Degradation of CCNK/CDK12 is a druggable vulnerability of colorectal cancer
Dieter, S. M., Siegl, C., Codó, P. L., Huerta, M., Ostermann-Parucha, A. L., Schulz, E., Zowada, M. K., Martin, S., Laaber, K., Nowrouzi, A., et al. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109394 · Cited by 95 · see citing works
Critical Role of Three-Dimensional Tumorsphere Size on Experimental Outcome
Singh, S. K., Abbas, S., Saxena, A. K., Tiwari, S., Sharma, L. K., & Tiwari, M. (2020) · BioTechniques · doi:10.2144/btn-2020-0081 · Cited by 91 · see citing works
Current Advances in 3D Bioprinting for Cancer Modeling and Personalized Medicine
Germain, N., Dhayer, M., Dekiouk, S., & Marchetti, P. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23073432 · Cited by 92 · see citing works
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Current approaches in identification and isolation of cancer stem cells
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Mimicking Epithelial Tissues in Three-Dimensional Cell Culture Models
Torras, N., García-Díaz, M., Fernández‐Majada, V., & Martínez, E. (2018) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2018.00197 · Cited by 84 · see citing works
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Apigenin: Molecular Mechanisms and Therapeutic Potential against Cancer Spreading
Naponelli, V., Rocchetti, M. T., & Mangieri, D. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25105569 · Cited by 84 · see citing works
From 2D to 3D and beyond: the evolution and impact of in vitro tumor models in cancer research
Rauner, G., Gupta, P. B., & Kuperwasser, C. (2025) · Nature Methods · doi:10.1038/s41592-025-02769-1 · Cited by 73 · see citing works
Namba, Y., Sogawa, C. A., Okusha, Y., Kawai, H., Itagaki, M., Ono, K., Murakami, J., Aoyama, E., Ohyama, K., Asaumi, J., et al. (2018) · Frontiers in Oncology · doi:10.3389/fonc.2018.00376 · Cited by 74 · see citing works
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 68 · see citing works
Kim, D., Kim, M., Park, H.-B., Kim, K., & Kim, D.-E. (2019) · ACS Applied Bio Materials · doi:10.1021/acsabm.9b00705 · Cited by 68 · see citing works
Activation of Estrogen Receptor Alpha by Decitabine Inhibits Osteosarcoma Growth and Metastasis
Osuna, M. Á. L., García-López, J., Ayachi, I. E., Fatima, I., Khalid, A. B., Kumpati, J., Slayden, A. V., Seagroves, T. N., Miranda‐Carboni, G. A., & Krum, S. A. (2018) · Cancer Research · doi:10.1158/0008-5472.can-18-1255 · Cited by 65 · see citing works
Tataranni, T., Agriesti, F., Pacelli, C., Ruggieri, V., Laurenzana, I., Mazzoccoli, C., Sala, G. D., Panebianco, C., Pazienza, V., Capitanio, N., et al. (2019) · Cells · doi:10.3390/cells8050478 · Cited by 65 · see citing works
New Advances in the Study of Bone Tumors: A Lesson From the 3D Environment
Cortini, M., Baldini, N., & Avnet, S. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2019.00814 · Cited by 64 · see citing works
Gradient-sized control of tumor spheroids on a single chip
Fang, G., Lu, H., Law, A. M. K., Gallego‐Ortega, D., Jin, D., & Lin, G. (2019) · Lab on a Chip · doi:10.1039/c9lc00872a · Cited by 64 · see citing works
Long, L., Hu, Y., Long, T., Lu, X., Tuo, Y., Li, Y., Wang, M., & Ke, Z. (2021) · Journal for ImmunoTherapy of Cancer · doi:10.1136/jitc-2021-003973 · Cited by 63 · see citing works
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Miyazaki, T., Chung, S., Sakai, H., Ohata, H., Obata, Y., Shiokawa, D., Mizoguchi, Y., Kubo, T., Ichikawa, H., Taniguchi, H., et al. (2021) · Cancer Science · doi:10.1111/cas.15182 · Cited by 60 · see citing works
3D Tumor Spheroid and Organoid to Model Tumor Microenvironment for Cancer Immunotherapy
Zhu, Y., Kang, E., Wilson, M., Basso, T., Chen, E., Yu, Y., & Li, Y.-R. (2022) · Organoids · doi:10.3390/organoids1020012 · Cited by 60 · see citing works
Tumor organoids: From inception to future in cancer research
Yang, L., Yang, S., Li, X., Li, B., Li, Y., Zhang, X., Ma, Y., Peng, X., Jin, H., Fan, Q., et al. (2019) · Cancer Letters · doi:10.1016/j.canlet.2019.04.005 · Cited by 60 · see citing works
RHOA in Gastric Cancer: Functional Roles and Therapeutic Potential
Nam, S., Kim, J. H., & Lee, D. H. (2019) · Frontiers in Genetics · doi:10.3389/fgene.2019.00438 · Cited by 59 · see citing works
Azadi, S., Es, H. A., Bazaz, S. R., Thiery, J. P., Asadnia, M., & Warkiani, M. E. (2019) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2019.118526 · Cited by 58 · see citing works
Cavo, M., Cave, D. D., D’Amone, E., Gigli, G., Lonardo, E., & del Mercato, L. L. (2020) · Scientific Reports · doi:10.1038/s41598-020-66908-8 · Cited by 58 · see citing works
L1CAM promotes ovarian cancer stemness and tumor initiation via FGFR1/SRC/STAT3 signaling
Giordano, M., Decio, A., Battistini, C., Baronio, M., Bianchi, F., Villa, A., Bertalot, G., Freddi, S., Lupia, M., Jodice, M. G., et al. (2021) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-021-02117-z · Cited by 57 · see citing works
Recent advances in microfluidic technology and applications for anti-cancer drug screening
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Three-Dimensional Cell Cultures as an In Vitro Tool for Prostate Cancer Modeling and Drug Discovery
Fontana, F., Raimondi, M., Marzagalli, M., Sommariva, M., Gagliano, N., & Limonta, P. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21186806 · Cited by 56 · see citing works
MTHFD1L, A Folate Cycle Enzyme, Is Involved in Progression of Colorectal Cancer
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An omentum-inspired 3d peg hydrogel for identifying ecm-drivers of drug resistant ovarian cancer
Brooks, E. A., Gencoglu, M. F., Corbett, D. C., Stevens, K. R., & Peyton, S. R. (2019) · APL Bioengineering · doi:10.1063/1.5091713 · Cited by 51 · see citing works
Expression of Oncogenic Drivers in 3D Cell Culture Depends on Nuclear ATP Synthesis by NUDT5
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Patient-derived Models Reveal Impact of the Tumor Microenvironment on Therapeutic Response
Shafi, A. A., Schiewer, M. J., de Leeuw, R., Dylgjeri, E., McCue, P. A., Shah, N., Gomella, L. G., Lallas, C. D., Trabulsi, E. J., Centenera, M. M., et al. (2018) · European Urology Oncology · doi:10.1016/j.euo.2018.04.019 · Cited by 51 · see citing works
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A 3D Spheroid Model for Glioblastoma
Guyon, J., Andrique, L., Pujol, N., Røsland, G. V., Recher, G., Bikfalvi, A., & Daubon, T. (2020) · Journal of Visualized Experiments · doi:10.3791/60998 · Cited by 50 · see citing works
CXCR4 Inhibition Counteracts Immunosuppressive Properties of Metastatic NSCLC Stem Cells
Fortunato, O., Belisario, D. C., Compagno, M., Giovinazzo, F., Bracci, C., Pastorino, U., Horenstein, A. L., Malavasi, F., Ferracini, R., Scala, S., et al. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.02168 · Cited by 50 · see citing works
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Role of the NUDT Enzymes in Breast Cancer
Wright, R. H. G., & Beato, M. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22052267 · Cited by 48 · see citing works
Non-animal models in dermatological research
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Radiation-induced DNA damage response and resistance in colorectal cancer stem-like cells
Anuja, K., Chowdhury, A. R., Saha, A., Roy, S., Rath, A. K., Kar, M., & Banerjee, B. (2019) · International Journal of Radiation Biology · doi:10.1080/09553002.2019.1580401 · Cited by 47 · see citing works
LKB1 and cancer: The dual role of metabolic regulation
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Direct interaction of β‐catenin with nuclear ESM1 supports stemness of metastatic prostate cancer
Pan, K., Lee, W.-J., Chou, C., Yang, Y., Chang, Y., Chien, M., Hsiao, M., & Hua, K. (2020) · The EMBO Journal · doi:10.15252/embj.2020105450 · Cited by 43 · see citing works
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Adaptive phenotypic modulations lead to therapy resistance in chronic myeloid leukemia cells
Baykal, S., Açıkgöz, E., Yavuz, A. S., Geyik, Ö. G., Ateş, H., Sezerman, O. U., Özsan, G. H., & Yüce, Z. (2020) · PLoS ONE · doi:10.1371/journal.pone.0229104 · Cited by 44 · see citing works
Folate can promote the methionine-dependent reprogramming of glioblastoma cells towards pluripotency
Zgheib, R., Battaglia-Hsu, S.-F., Hergalant, S., Quéré, M., Alberto, J., Chéry, C., Rouyer, P., Gauchotte, G., Guéant, J., & Namour, F. (2019) · Cell Death and Disease · doi:10.1038/s41419-019-1836-2 · Cited by 44 · see citing works
Intrinsic and Extrinsic Factors Impacting Cancer Stemness and Tumor Progression
Ponomarev, A., Gilazieva, Z., Solovyeva, V. V., Allegrucci, C., & Rizvanov, A. A. (2022) · Cancers · doi:10.3390/cancers14040970 · Cited by 44 · see citing works
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Exosomes, metastases, and the miracle of cancer stem cell markers
Wang, Z., & Zöller, M. (2019) · Cancer and Metastasis Reviews · doi:10.1007/s10555-019-09793-6 · Cited by 41 · see citing works
TRIB3 promotes lung cancer progression by activating β-catenin signaling
Zhang, X., Zhong, N., Li, X., & Chen, M. (2019) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2019.172697 · Cited by 41 · see citing works
Engineering complexity in human tissue models of cancer
Ronaldson-Bouchard, K., Baldassarri, I., Tavakol, D. N., Graney, P. L., Samaritano, M., Cimetta, E., & Vunjak‐Novakovic, G. (2022) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2022.114181 · Cited by 41 · see citing works
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The hedgehog pathway regulates cancer stem cells in serous adenocarcinoma of the ovary
Sneha, S., Nagare, R. P., Sidhanth, C., Krishnapriya, S., Garg, M., Ramachandran, B., Murhekar, K. M., Sundersingh, S., & Ganesan, T. S. (2020) · Cellular Oncology · doi:10.1007/s13402-020-00504-w · Cited by 40 · see citing works
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Modeling glioblastoma complexity with organoids for personalized treatments
Pawlowski, K. D., Duffy, J. T., Babak, M. V., & Balyasnikova, I. V. (2023) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2023.01.002 · Cited by 39 · see citing works
Overcoming drug resistance with a docetaxel and disulfiram loaded pH-sensitive nanoparticle
Swetha, K. L., Paul, M., Maravajjala, K. S., Kumbham, S., Biswas, S., & Roy, A. (2023) · Journal of Controlled Release · doi:10.1016/j.jconrel.2023.02.023 · Cited by 39 · see citing works
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KLF7: a new candidate biomarker and therapeutic target for high-grade serous ovarian cancer
Donato, M. D., Babini, G., Mozzetti, S., Buttarelli, M., Ciucci, A., Arduini, G., Rosa, M. C. D., Scambia, G., & Gallo, D. (2020) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-020-01775-9 · Cited by 39 · see citing works
Visualizing Extracellular Vesicles and Their Function in 3D Tumor Microenvironment Models
Ural, E. E., Toomajian, V., Apu, E. H., Veletić, M., Balasingham, I., Ashammakhi, N. A., Kanada, M., & Contag, C. H. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22094784 · Cited by 39 · see citing works
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A Self-Assembling Amphiphilic Peptide Dendrimer-Based Drug Delivery System for Cancer Therapy
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Organoids Provide an Important Window on Inflammation in Cancer
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- Authors
- Ishiguro, T., Ohata, H., Sato, A., Yamawaki, K., Enomoto, T., & Okamoto, K.
- Affiliations
- Niigata University (JP)
- National Cancer Center Research Institute (JP)
- Corresponding author
- Okamoto, Koji
- Venue
- Cancer Science
- Publisher
- Wiley
- Published
- 2017-03
- Volume
- 108
- Issue
- 3
- Pages
- 283-289
- ISSN
- 1347-9032 (ISSN-L)
- 1349-7006
- PMC
- PMC5378268
- OpenAlex
- W2570959155
- Cited by
- 530
- References
- 80
- Citations by year
- 2026: 35 · 2025: 59 · 2024: 67 · 2023: 69 · 2022: 64 · 2021: 65 · 2020: 70 · 2019: 55 · 2018: 33 · 2017: 11
- FWCI
- 4.85
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Cancer Science (publishedVersion, cc-by-nc)
- PubMed Central (publishedVersion, cc-by-nc)
- PubMed (publishedVersion)
- Institutional Repositories DataBase (IRDB) (submittedVersion)
- Funders
- Ministry of Education, Culture, Sports, Science and Technology
- National Cancer Center
- Japan Society for the Promotion of Science
- Japan Agency for Medical Research and Development
- Topics
- Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
- Physical Sciences › Engineering › Biomedical Engineering › 3D Printing in Biomedical Research
- Physical Sciences › Mathematics › Modeling and Simulation › Mathematical Biology Tumor Growth
- Keywords
- cancer stem cells, tumor spheroids, tumor organoids, chemoresistance, tumorigenicity, high-throughput screening, circulating tumor cells, glioma, breast cancer, colon cancer, ovarian cancer, prostate cancer
- MeSH terms
- Humans, Neoplasms, Tumor Cells, Cultured, Neoplastic Stem Cells, Spheroids, Cellular, Cell Culture 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.
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