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Three-dimensional culture systems in cancer research: Focus on tumor spheroid model
Open accessAbstract
Cancer cells propagated in three-dimensional (3D) culture systems exhibit physiologically relevant cell-cell and cell-matrix interactions, gene expression and signaling pathway profiles, heterogeneity and structural complexity that reflect in vivo tumors. In recent years, development of various 3D models has improved the study of host-tumor interaction and use of high-throughput screening platforms for anti-cancer drug discovery and development. This review attempts to summarize the various 3D culture systems, with an emphasis on the most well characterized and widely applied model - multicellular tumor spheroids. This review also highlights the various techniques to generate tumor spheroids, methods to characterize them, and its applicability in cancer research.
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“This physiochemical gradient generally induces the formation of three concentric zones on a spheroid -an anoxic core in the center containing necrotic cells, a middle hypoxic zone that has a low concentration of oxygen and nutrients, and an outer zone containing highly proliferative cells [53].”
From 3D In Vitro Model (R)evolution: Unveiling Tumor–Stroma Interactions (2021) · cites this paper as [53]
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“Cancer spheroids are arguably the simplest in vitro 3D tumor models [114,115].”
From The Tumor-on-Chip: Recent Advances in the Development of Microfluidic Systems to Recapitulate the Physiology of Solid Tumors (2019) · cites this paper as [114]
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“Currently, various tumor spheroids have been fabricated by embedding cancer cells into protein‐based hydrogels such as Matrigel,[ 64 ] fibrin,[ 65 ] and collagen[ 66 ] as they incorporate specific cell‐adhesive motifs and enzymatic‐mediated matrix degradation which are beneficial to cell proliferation.”
From 3D Biomimetic Models to Reconstitute Tumor Microenvironment In Vitro: Spheroids, Organoids, and Tumor‐on‐a‐Chip (2023) · cites this paper as [66]
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“An important aspect to consider is uniformity in size and homogeneity to ensure that the results are not in fl uenced by these factors [53].”
From 3D In Vitro Model (R)evolution: Unveiling Tumor–Stroma Interactions (2021) · cites this paper as [53]
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“Tumor cell spheroids are especially useful for studying cancers that form tumor embolus, or a closely packed tumor cell cluster, as happens in in fl ammatory breast cancer [53].”
From 3D In Vitro Model (R)evolution: Unveiling Tumor–Stroma Interactions (2021) · cites this paper as [53]
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“Three-dimensional multicellular tumor spheroids have emerged as more representative in vitro models that capture essential features of tumor architecture, stromal interactions, and microenvironmental resistance mechanisms.”
From Modeling Tumor Microenvironment Complexity In Vitro: Spheroids as Physiologically Relevant Tumor Models and Strategies for Their Analysis (2025) · cites this paper as [17]
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“Spheroids exhibit spatially organized regions of proliferation, quiescence, and hypoxia, and can incorporate non-tumor cells to mimic tumor–stroma crosstalk.”
From Modeling Tumor Microenvironment Complexity In Vitro: Spheroids as Physiologically Relevant Tumor Models and Strategies for Their Analysis (2025) · cites this paper as [17]
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“By mimicking the hierarchical structure, proliferation gradients, and stromal interactions found in native tumor tissues, spheroids provide a more physiologically relevant context for evaluating anticancer agents and delivery systems [16,17].”
From Modeling Tumor Microenvironment Complexity In Vitro: Spheroids as Physiologically Relevant Tumor Models and Strategies for Their Analysis (2025) · cites this paper as [17]
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“These gradients typically emerge when spheroids exceed ~500 μm in diameter, with proliferative cells localized to the outer rim, quiescent cells residing in intermediate zones, and hypoxic or necrotic cores forming at the center due to limited diffusion [17,184,185].”
From Modeling Tumor Microenvironment Complexity In Vitro: Spheroids as Physiologically Relevant Tumor Models and Strategies for Their Analysis (2025) · cites this paper as [17]
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“Furthermore, 2D cultured cells are artificially polarized when their cytoskeleton rearranges as they are stretched on the culture plate, which in turn causes these cultured cells to express genes and proteins which are atypical [56].”
From Microfluidic modelling of the tumor microenvironment for anti-cancer drug development (2019) · cites this paper as [56]
In the citing paper
“Spheroids [98, 99] are, in general, considered similar to an early vascular stage of tumors”
In the citing paper
“Moreover, this gradient leads to the formation of concentric zones in the spheroids with a center containing an anoxic core with necrotic cells, a middle zone containing hypoxic cells, and an outer zone of highly proliferative cells, recapitulating the properties of an in vitro tumor [379].”
From Tumor microenvironment signaling and therapeutics in cancer progression (2023) · cites this paper as [379]
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Citations
Cites
Calcium's Role in Mechanotransduction during Muscle Development
Damm, T. B., & Egli, M. (2014) · Cellular Physiology and Biochemistry · doi:10.1159/000356667 · Cited by 14,552
Integrins: Versatility, modulation, and signaling in cell adhesion
Hynes, R. O. (1992) · Cell · doi:10.1016/0092-8674(92)90115-s · Cited by 9,857
Microenvironmental regulation of tumor progression and metastasis
Quail, D. F., & Joyce, J. A. (2013) · Nature Medicine · doi:10.1038/nm.3394 · Cited by 7,994
Molecular Mechanisms of Stress-Responsive Changes in Collagen and Elastin Networks in Skin
Aziz, J., Shezali, H., Radzi, Z., Yahya, N. A., Abu Kassim, N. H., Czernuszka, J., & Rahman, M. T. (2016) · Skin Pharmacology and Physiology · doi:10.1159/000447017 · Cited by 7,323
Hydrogel: Preparation, characterization, and applications: A review
Ahmed, E. M. (2015) · Journal of Advanced Research · doi:10.1016/j.jare.2013.07.006 · Cited by 5,800
Matrix Crosslinking Forces Tumor Progression by Enhancing Integrin Signaling
Levental, K. R., Yu, H., Kass, L., Lakins, J. N., Egeblad, M., Erler, J. T., Fong, S. F. T., Csiszar, K., Giaccia, A., Weninger, W., et al. (2009) · Cell · doi:10.1016/j.cell.2009.10.027 · Cited by 4,101
Tensional homeostasis and the malignant phenotype
Paszek, M. J., Zahir, N., Johnson, K. R., Lakins, J. N., Rozenberg, G. I., Gefen, A., Reinhart-King, C. A., Margulies, S. S., Dembo, M., Boettiger, D., et al. (2005) · Cancer Cell · doi:10.1016/j.ccr.2005.08.010 · Cited by 3,941
Nonlinear magic: multiphoton microscopy in the biosciences
Zipfel, W. R., Williams, R. M., & Webb, W. W. (2003) · Nature Biotechnology · doi:10.1038/nbt899 · Cited by 3,911
Microenvironmental regulation of metastasis
Joyce, J. A., & Pollard, J. W. (2009) · Nature Reviews Cancer · doi:10.1038/nrc2618 · Cited by 3,684
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
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- Chandrasekaran, 2014, Vol. 9
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Spheroids in cancer research: Recent advances and opportunities
Arora, S., Singh, S., Mittal, A. K., Desai, N., Khatri, D. K., Gugulothu, D. B., Lather, V., Pandita, D., & Vora, L. K. (2024) · Journal of Drug Delivery Science and Technology · doi:10.1016/j.jddst.2024.106033 · Cited by 76
Gutzweiler, L., Kartmann, S., Tröndle, K., Benning, L., Finkenzeller, G., Zengerle, R., Koltay, P., Stark, G. B., & Zimmermann, S. (2017) · Biofabrication · doi:10.1088/1758-5090/aa7218 · Cited by 71
Hagemann, J., JACOBI, C., Hahn, M., Schmid, V., Welz, C., Schwenk‐Zieger, S., Stauber, R. H., Baumeister, P., & Becker, S. (2017) · Anticancer Research · doi:10.21873/anticanres.11555 · Cited by 73
Facile Tumor Spheroids Formation in Large Quantity with Controllable Size and High Uniformity
Shi, W., Kwon, J., Huang, Y., Tan, J., Uhl, C. G., He, R., Zhou, C., & Liu, Y. (2018) · Scientific Reports · doi:10.1038/s41598-018-25203-3 · Cited by 69
Emerging tumor-on-chips with electrochemical biosensors
Lei, L., Ma, B., Xu, C., & Liu, H. (2022) · TrAC Trends in Analytical Chemistry · doi:10.1016/j.trac.2022.116640 · Cited by 71
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Olofsson, K., Carannante, V., Ohlin, M., Frisk, T. W., Kushiro, K., Takai, M., Lundqvist, A., Önfelt, B., & Wiklund, M. (2018) · Lab on a Chip · doi:10.1039/c8lc00537k · Cited by 68
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Redmond, J., McCarthy, H. O., Buchanan, P., Levingstone, T. J., & Dunne, N. (2021) · Materials Science and Engineering C · doi:10.1016/j.msec.2021.111944 · Cited by 71
Circulating Tumor Cell-Derived Pre-Clinical Models for Personalized Medicine
Tellez-Gabriel, M., Cochonneau, D., Cadé, M., Jubelin, C., Heymann, M., & Heymann, D. (2018) · Cancers · doi:10.3390/cancers11010019 · Cited by 68
Shah, S., & D’Souza, G. G. M. (2025) · Cells · doi:10.3390/cells14100732 · Cited by 83
“These gradients typically emerge when spheroids exceed ~500 µ m in diameter, with proliferative cells localized to the outer rim, quiescent cells residing in intermediate zones, and hypoxic or necrotic cores forming at the center due to limited diffusion [17,184,185].”
Ganguli, A., Mostafa, A., Saavedra, C., Kim, Y., Le, P., Faramarzi, V., Feathers, R. W., Berger, J., Ramos-Cruz, K. P., Adeniba, O. O., et al. (2021) · Science Advances · doi:10.1126/sciadv.abc1323 · Cited by 66
Mapping and Profiling Lipid Distribution in a 3D Model of Breast Cancer Progression
Vidavsky, N., Kunitake, J. A. M. R., Diaz-Rubio, M. E., Chiou, A. E., Loh, H.-C., Zhang, S., Mašić, A., Fischbach, C., & Estroff, L. A. (2019) · ACS Central Science · doi:10.1021/acscentsci.8b00932 · Cited by 63
Watson, P. M. D., Kavanagh, E., Allenby, G., & Vassey, M. (2017) · SLAS Discovery · doi:10.1177/2472555217691450 · Cited by 74
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Ahn, J., Kim, D., Koo, D.-J., Lim, J., Park, T., Lee, J., Ko, J., Kim, S., Kim, M., Kang, K., et al. (2022) · Acta Biomaterialia · doi:10.1016/j.actbio.2022.10.009 · Cited by 64
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Monteiro, C. F., Santos, S. C., Custódio, C. A., & Mano, J. F. (2020) · Advanced Science · doi:10.1002/advs.201902398 · Cited by 61
Tutty, M. A., Movia, D., & Prina‐Mello, A. (2022) · Drug Delivery and Translational Research · doi:10.1007/s13346-022-01147-0 · Cited by 67
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Khan, M. S., Hwang, J., Lee, K., Choi, Y., Seo, Y., Jeon, H., Hong, J. W., & Choi, J. H. (2019) · Cancers · doi:10.3390/cancers11101464 · Cited by 60
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Sano, E., Mori, C., Nashimoto, Y., Yokokawa, R., Kotera, H., & Torisawa, Y. (2018) · Biomicrofluidics · doi:10.1063/1.5027183 · Cited by 62
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Castro, F., Pereira, C. L., Macedo, M. H., Almeida, A., Silveira, M. J., Dias, S., Cardoso, A. P., Oliveira, M. J., & Sarmento, B. F. C. C. (2021) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2021.06.001 · Cited by 62
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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 57
Kim, T. Y., Kofron, C. M., King, M. E., Markes, A. R., Okundaye, A. O., Qu, Z., Mende, U., & Choi, B.-R. (2018) · PLOS ONE · doi:10.1371/journal.pone.0196714 · Cited by 57
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Roy, V., Magne, B., Vaillancourt-Audet, M., Blais, M., Chabaud, S., Grammond, E., Piquet, L., Fradette, J., Laverdière, I., Moulin, V. J., et al. (2020) · BioMed Research International · doi:10.1155/2020/6051210 · Cited by 57
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Doctor, A., Seifert, V., Ullrich, M., Hauser, S., & Pietzsch, J. (2020) · Cancers · doi:10.3390/cancers12102765 · Cited by 53
Patient-derived xenografts as preclinical neuroblastoma models
Braekeveldt, N., & Bexell, D. (2017) · Cell and Tissue Research · doi:10.1007/s00441-017-2687-8 · Cited by 54
Theiner, S., Malderen, S. J. M. V., Acker, T. V., Legin, A. A., Keppler, B. K., Vanhaecke, F., & Koellensperger, G. (2017) · Analytical Chemistry · doi:10.1021/acs.analchem.7b02681 · Cited by 54
Tian, L., Gao, J., Garcia, I. M., Chen, H. J., Castaldi, A., & Chen, Y. (2020) · Wiley Interdisciplinary Reviews Developmental Biology · doi:10.1002/wdev.399 · Cited by 54
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Ma, Z., Li, N., Zhang, B., Hui, Y., Zhang, Y., Lü, P., Pi, J., & Liu, Z. (2020) · Journal of Nanobiotechnology · doi:10.1186/s12951-020-00681-8 · Cited by 49
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Arora, J., Sauer, S. J., Tarpley, M., Vermeulen, P. B., Rypens, C., Laere, S. V., Williams, K. P., Devi, G. R., & Dewhirst, M. W. (2017) · Oncotarget · doi:10.18632/oncotarget.15667 · Cited by 47
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3D hanging spheroid plate for high-throughput CAR T cell cytotoxicity assay
Chen, Z., Han, S., Sanny, A., Chan, D. L.-K., van Noort, D., Lim, W., Tan, A. H., & Park, S. (2022) · Journal of Nanobiotechnology · doi:10.1186/s12951-021-01213-8 · Cited by 46
Luo, J., Cao, J., Ma, G., Wang, X., Sun, Y., Zhang, C., Shi, Z., Zeng, Y., Zhang, T., & Huang, P. (2022) · ACS Applied Materials & Interfaces · doi:10.1021/acsami.2c08951 · Cited by 47
Fabrication of Cell Spheroids for 3D Cell Culture and Biomedical Applications
Park, S. Y., Hong, H. J., & Lee, H. J. (2022) · BioChip Journal · doi:10.1007/s13206-022-00086-9 · Cited by 50
Cancer stem cells as targets for DC-based immunotherapy of colorectal cancer
Szaryńska, M., Olejniczak-Kęder, A., Kobiela, J., Łaski, D., Śledziński, Z., & Kmieć, Z. (2018) · Scientific Reports · doi:10.1038/s41598-018-30525-3 · Cited by 46
Reddy, T. S., Privér, S. H., Rao, V. V., Mirzadeh, N., & Bhargava, S. K. (2018) · Dalton Transactions · doi:10.1039/c8dt01724g · Cited by 46
Yoshimatsu, Y., Noguchi, R., Tsuchiya, R., Kito, F., Sei, A., Sugaya, J., Nakagawa, M., Yoshida, A., Iwata, S., Kawai, A., et al. (2020) · Human Cell · doi:10.1007/s13577-019-00312-x · Cited by 46
Stenberg, V. Y., Larsen, R. H., Ma, L., Peng, Q., Juzenas, P., Bruland, Ø. S., & Juzeniene, A. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22094815 · Cited by 45
Bringing 3D tumor models to the clinic – predictive value for personalized medicine
Halfter, K., & Mayer, B. (2017) · Biotechnology Journal · doi:10.1002/biot.201600295 · Cited by 48
Engineered hydrogels for brain tumor culture and therapy
Thakor, J., Ahadian, S., Niakan, A. A., Banton, E. A., Nasrollahi, F., Hasani‐Sadrabadi, M. M., & Khademhosseini, A. (2020) · Bio-Design and Manufacturing · doi:10.1007/s42242-020-00084-6 · Cited by 43
Magnetic molding of tumor spheroids: emerging model for cancer screening
Perez, J. E., Nagle, I., & Wilhelm, C. (2020) · Biofabrication · doi:10.1088/1758-5090/abc670 · Cited by 52
SpheroidJ: An Open-Source Set of Tools for Spheroid Segmentation
Lacalle, D., Castro-Abril, H. A., Ranđelović, T., Domínguez, C., Heras, J., Mata, E. J., Mata, G., Méndez, Y., Pascual, V., & Ochoa, I. (2020) · Computer Methods and Programs in Biomedicine · doi:10.1016/j.cmpb.2020.105837 · Cited by 44
Zhang, Y., Wang, Z., Hu, Q., Luo, H., Lu, B., Gao, Y., Qiao, Z., Zhou, Y., Fang, Y., Gu, J., et al. (2022) · Small · doi:10.1002/smll.202200364 · Cited by 46
Advances in the application of 3D tumor models in precision oncology and drug screening
Guan, X., & Huang, S. (2022) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2022.1021966 · Cited by 45
Monfort, T., Azzollini, S., Brogard, J., Clémençon, M., Slembrouck-Brec, A., Forster, V., Picaud, S. A., Goureau, O., Reichman, S., Thouvenin, O., et al. (2023) · Communications Biology · doi:10.1038/s42003-023-05378-w · Cited by 48
In vitro characterization of spheres derived from colorectal cancer cell lines
Olejniczak-Kęder, A., Szaryńska, M., & Kmieć, Z. (2017) · International Journal of Oncology · doi:10.3892/ijo.2017.4206 · Cited by 45
Totti, S., Allenby, M. C., Santos, S. B. D., Mantalaris, A., & Velliou, E. G. (2018) · RSC Advances · doi:10.1039/c8ra02633e · Cited by 44
Short-Term Ex Vivo Culture of CTCs from Advance Breast Cancer Patients: Clinical Implications
Carmona-Ule, N., González-Conde, M., Abuín, C., Cueva, J. F., Palacios, P., López‐López, R., Costa, C., & Dávila-Ibáñez, A. B. (2021) · Cancers · doi:10.3390/cancers13112668 · Cited by 42
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 45
SpheroidPicker for automated 3D cell culture manipulation using deep learning
Grexa, I., Diósdi, Á., Harmati, M., Kriston, A., Moshkov, N., Buzás, K., Pietiäinen, V., Koós, K., & Horváth, P. (2021) · Scientific Reports · doi:10.1038/s41598-021-94217-1 · Cited by 43
Harnessing the power of artificial intelligence for human living organoid research
Wang, H., Li, X., You, X., & Zhao, G. (2024) · Bioactive Materials · doi:10.1016/j.bioactmat.2024.08.027 · Cited by 43
Jacobi, N., Seeboeck, R., Hofmann, E., Schweiger, H., Smolinska, V., Mohr, T., Boyer, A., Sommergruber, W., Lechner, P., Pichler-Huebschmann, C., et al. (2017) · Oncotarget · doi:10.18632/oncotarget.22475 · Cited by 43
Eglen, R. M., & Reisine, T. (2019) · SLAS TECHNOLOGY · doi:10.1177/2472630318803275 · Cited by 43
Remote Control in Formation of 3D Multicellular Assemblies Using Magnetic Forces
Jafari, J., Han, X., Palmer, J. A., Tran, P. A., & O’Connor, A. J. (2019) · ACS Biomaterials Science & Engineering · doi:10.1021/acsbiomaterials.9b00297 · Cited by 43
Hydrogels to engineer tumor microenvironments in vitro
Fernando, K., Kwang, L. G., Lim, J. T. C., & Fong, E. L. S. (2021) · Biomaterials Science · doi:10.1039/d0bm01943g · Cited by 44
Extracellular Matrix-Based Hydrogels to Tailoring Tumor Organoids
Lee, H. J., Mun, S., Pham, D. M., & Kim, P. (2021) · ACS Biomaterials Science & Engineering · doi:10.1021/acsbiomaterials.0c01801 · Cited by 44
Li, C., Li, J., Li, Y., Li, L., Luo, Y.-L., Li, J., Zhang, Y., Wang, Y., Liu, X., Zhou, X., et al. (2021) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.1c02620 · Cited by 42
3D tumor spheroids: morphological alterations a yardstick to anti-cancer drug response
Senrung, A., Lalwani, S., Janjua, D., Tripathi, T., Kaur, J., Ghuratia, N., Aggarwal, N., Chhokar, A., Yadav, J., Chaudhary, A., et al. (2023) · In vitro models · doi:10.1007/s44164-023-00059-8 · Cited by 48
Lee, J., Kim, K., Ryu, T. Y., Jung, C., Lee, M., Lim, J. H., Park, K., Kim, D., Son, M., Hamamoto, R., et al. (2021) · Molecular Oncology · doi:10.1002/1878-0261.13050 · Cited by 42
Sawant, S. S., Patil, S. M., Shukla, S. K., Kulkarni, N. S., Gupta, V., & Kunda, N. K. (2021) · Drug Delivery and Translational Research · doi:10.1007/s13346-021-01088-0 · Cited by 42
A pH-sensitive liposome formulation of a peptidomimetic-Dox conjugate for targeting HER2 + cancer
Sonju, J. J., Dahal, A., Singh, S. S., Gu, X., Johnson, W. D., Muthumula, C. M. R., Meyer, S. A., & Jois, S. D. S. (2021) · International Journal of Pharmaceutics · doi:10.1016/j.ijpharm.2021.121364 · Cited by 42
Li, M., Yao, M., Wang, W., Wan, P., Chu, X., Zheng, Y., Yang, K., & Zhang, Y. (2020) · Acta Biomaterialia · doi:10.1016/j.actbio.2020.11.019 · Cited by 40
Ravi, K., Manoharan, T. J. M., Wang, K.-C., Pockaj, B. A., & Nikkhah, M. (2023) · Biomaterials · doi:10.1016/j.biomaterials.2023.122428 · Cited by 45
Metadata
- Authors
- Nath, S., & Devi, G. R.
- Affiliations
- Duke University (US)
- Corresponding author
- Devi, Gayathri R.
- ORCID
- Devi, Gayathri R.
- Venue
- Pharmacology & Therapeutics
- Publisher
- Elsevier BV
- Published
- 2016-07
- Volume
- 163
- Pages
- 94-108
- ISSN
- 0163-7258 (ISSN-L)
- PMC
- PMC4961208
- OpenAlex
- W2332155194
- Cited by
- 919
- References
- 175
- Citations by year
- 2026: 67 · 2025: 95 · 2024: 100 · 2023: 92 · 2022: 110 · 2021: 125 · 2020: 137 · 2019: 81 · 2018: 63 · 2017: 38 · 2016: 11
- FWCI
- 6.47
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Pharmacology & Therapeutics (acceptedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- NIH (CA014236)
- Department of Defense (W81XWH-13-1-0047)
- 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
- tumor spheroids, tumor cell culture, cell-matrix interactions, tumor heterogeneity, tumor-host interaction, high-throughput drug screening, anticancer drug discovery
- MeSH terms
- Antineoplastic Agents, Cell Communication, Cell Movement, Flow Cytometry, Humans, Microscopy, Electron, Scanning, Neoplasm Invasiveness, Neoplasms, Tumor Cells, Cultured, Microscopy, Confocal, Spheroids, Cellular, Cell Culture Techniques, Hydrogels, Tumor Microenvironment
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