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Leading malignant cells initiate collective epithelial cell invasion in a three-dimensional heterotypic tumor spheroid model
Open accessAbstract
Solid tumors consist of genetically and phenotypically diverse subpopulations of cancer cells with unique capacities for growth, differentiation, and invasion. While the molecular and microenvironmental bases for heterogeneity are increasingly appreciated, the outcomes of such intratumor heterogeneity, particularly in the context of tumor invasion and metastasis, remain poorly understood. To study heterotypic cell-cell interactions and elucidate the biological consequences of intratumor heterogeneity, we developed a tissue-engineered multicellular spheroid (MCS) co-culture model that recapitulates the cellular diversity and fully three-dimensional cell-cell and cell-matrix interactions that characterize human carcinomas. We found that "invasion-competent" malignant cells induced the collective invasion of otherwise "invasion-incompetent" epithelial cells, and that these two cell types consistently exhibited distinct leader and follower roles during invasion. Analysis of extracellular matrix (ECM) microarchitecture revealed that malignant cell invasion was accompanied by extensive ECM remodeling including matrix alignment and proteolytic track-making. Inhibition of cell contractility- and proteolysis-mediated matrix reorganization prevented leader-follower behavior and malignant cell-induced epithelial cell invasion. These results indicate that heterogeneous subpopulations within a tumor may possess specialized roles during tumor progression and suggest that complex interactions among the various subpopulations of cancer cells within a tumor may regulate critical aspects of tumor biology and affect clinical outcome.
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“it was recently demonstrated that alignment directs tumor invasion in hydrogels containing anisotropic structures”
From Cancer-on-chip models for metastasis: importance of the tumor microenvironment (2024) · cites this paper as [29]
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Cites
Hallmarks of Cancer: The Next Generation
Hanahan, D., & Weinberg, R. A. (2011) · Cell · doi:10.1016/j.cell.2011.02.013 · Cited by 66,590
Intratumor Heterogeneity and Branched Evolution Revealed by Multiregion Sequencing
Gerlinger, M., Rowan, A. J., Horswell, S., Larkin, J., Endesfelder, D., Gronroos, E., Martinez, P., Matthews, N., Stewart, A., Tarpey, P., et al. (2012) · New England Journal of Medicine · doi:10.1056/nejmoa1113205 · Cited by 7,774
Epithelial–mesenchymal transitions in tumour progression
Thiery, J. P. (2002) · Nature reviews. Cancer · doi:10.1038/nrc822 · Cited by 6,767
Nowell, P. C. (1976) · Science · doi:10.1126/science.959840 · Cited by 6,471
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
Self-citationTumour-cell invasion and migration: diversity and escape mechanisms
Friedl, P., & Wolf, K. (2003) · Nature reviews. Cancer · doi:10.1038/nrc1075 · Cited by 3,350
The third dimension bridges the gap between cell culture and live tissue
Pampaloni, F., Reynaud, E. G., & Stelzer, E. H. K. (2007) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2236 · Cited by 2,817
Collective cell migration in morphogenesis, regeneration and cancer
Friedl, P., & Gilmour, D. T. (2009) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2720 · Cited by 2,804
Bissell, M. J., & Radisky, D. (2001) · Nature Reviews Cancer · doi:10.1038/35094059 · Cited by 2,180
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Self-citationThree-dimensional organotypic culture: experimental models of mammalian biology and disease
Shamir, E. R., & Ewald, A. J. (2014) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3873 · Cited by 719
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Han, W., Chen, S., Yuan, W., Fan, Q., Tian, J., Wang, X., Chen, L., Zhang, X., Wei, W., Liu, R., et al. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1610347113 · Cited by 376
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Chastney, M. R., Kaivola, J., Leppänen, V., & Ivaska, J. (2024) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-024-00777-1 · Cited by 249
Zhang, J., Goliwas, K. F., Wang, W., Taufalele, P., Bordeleau, F., & Reinhart‐King, C. A. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1809964116 · Cited by 183
Self-citationThe Mechanics of Single Cell and Collective Migration of Tumor Cells
Lintz, M., Muñoz, A., & Reinhart‐King, C. A. (2016) · Journal of Biomechanical Engineering · doi:10.1115/1.4035121 · Cited by 166
Self-citationDecoding leader cells in collective cancer invasion
Mercedes, S. A. V., Bocci, F., Levine, H., Onuchic, J. N., Jolly, M. K., & Wong, P. K. (2021) · Nature reviews. Cancer · doi:10.1038/s41568-021-00376-8 · Cited by 153
Staunton, J. R., Doss, B. L., Lindsay, S. M., & Ros, R. (2016) · Scientific Reports · doi:10.1038/srep19686 · Cited by 149
Engineered models to parse apart the metastatic cascade
Hapach, L. A., Mosier, J. A., Wang, W., & Reinhart‐King, C. A. (2019) · npj Precision Oncology · doi:10.1038/s41698-019-0092-3 · Cited by 143
Self-citationThree-dimensional collagen matrix induces a mechanosensitive invasive epithelial phenotype
Carey, S. P., Martin, K. E., & Reinhart‐King, C. A. (2017) · Scientific Reports · doi:10.1038/srep42088 · Cited by 131
Self-citationCarey, S. P., Goldblatt, Z. E., Martin, K. E., Romero, B., Williams, R. M., & Reinhart‐King, C. A. (2016) · Integrative Biology · doi:10.1039/c6ib00030d · Cited by 114
Self-citationTensile Forces Originating from Cancer Spheroids Facilitate Tumor Invasion
Kopanska, K. S., Alcheikh, Y., Staneva, R., Vignjevic, D. M., & Betz, T. (2016) · PLoS ONE · doi:10.1371/journal.pone.0156442 · Cited by 116
Commander, R., Wei, C., Sharma, A., Mouw, J. K., Burton, L. J., Summerbell, E. R., Mahboubi, D., Peterson, R. J., Konen, J. M., Zhou, W., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-15219-7 · Cited by 117
Lu, Y., Song, W., An, D., Kim, B. J., Schwartz, R. E., Wu, M., & Ma, M. (2014) · Journal of Materials Chemistry B · doi:10.1039/c4tb01735h · Cited by 113
Embedded Spheroids as Models of the Cancer Microenvironment
Tevis, K. M., Colson, Y. L., & Grinstaff, M. W. (2017) · Advanced Biosystems · doi:10.1002/adbi.201700083 · Cited by 109
Comparative mechanisms of cancer cell migration through 3D matrix and physiological microtracks
Carey, S. P., Rahman, A., Kraning-Rush, C. M., Romero, B., Somasegar, S., Torre, O. M., Williams, R. M., & Reinhart‐King, C. A. (2014) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00225.2014 · Cited by 103
Self-citationIlluminating breast cancer invasion: diverse roles for cell–cell interactions
Cheung, K. J., & Ewald, A. J. (2014) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2014.07.003 · Cited by 99
Yamashita, N., Tokunaga, E., Iimori, M., Inoue, Y., Tanaka, K., Kitao, H., Saeki, H., Oki, E., & Maehara, Y. (2018) · Clinical Breast Cancer · doi:10.1016/j.clbc.2018.02.002 · Cited by 95
Peela, N., Truong, D. D., Saini, H., Chu, H., Mashaghi, S., Ham, S. L., Singh, S. K., Tavana, H., Mosadegh, B., & Nikkhah, M. (2017) · Biomaterials · doi:10.1016/j.biomaterials.2017.04.017 · Cited by 97
An emerging tumor invasion mechanism about the collective cell migration.
Yang, Y., Zheng, H., Zhan, Y., & Fan, S. (2019) · PubMed Central · Cited by 89
Extracellular matrix determinants and the regulation of cancer cell invasion stratagems
WILLIS, A. L., SABEH, F., LI, X. ‐., & WEISS, S. J. (2013) · Journal of Microscopy · doi:10.1111/jmi.12064 · Cited by 85
Klymenko, Y., Kim, O., Loughran, E. A., Yang, J., Lombard, R., Alber, M., & Stack, M. S. (2017) · Oncogene · doi:10.1038/onc.2017.171 · Cited by 84
Collective cancer cell invasion induced by coordinated contractile stresses
Valencia, A. M. J., Wu, P.-H., Yogurtcu, O. N., Rao, P. P., DiGiacomo, J. W., Godet, I., He, L., Lee, M.-H., Gilkes, D. M., Sun, S. X., et al. (2015) · Oncotarget · doi:10.18632/oncotarget.5874 · Cited by 76
Learning the dynamics of cell–cell interactions in confined cell migration
Brückner, D. B., Arlt, N., Fink, A., Ronceray, P., Rädler, J. O., & Broedersz, C. P. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2016602118 · Cited by 95
Goliwas, K. F., Libring, S., Berestesky, E. D., Gholizadeh, S., Schwager, S. C., Frost, A. R., Gaborski, T. R., Zhang, J., & Reinhart‐King, C. A. (2023) · Journal of Cell Science · doi:10.1242/jcs.260419 · Cited by 79
Self-citationCollective forces of tumor spheroids in three-dimensional biopolymer networks
Mark, C., Grundy, T. J., Strissel, P. L., Böhringer, D., Grummel, N., Gerum, R. C., Steinwachs, J., Hack, C. C., Beckmann, M. W., Eckstein, M., et al. (2020) · eLife · doi:10.7554/elife.51912 · Cited by 77
Cell-ECM Interactions in Tumor Invasion
He, X., Lee, B., & Jiang, Y. (2016) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-42023-3_4 · Cited by 79
Mulligan, J. A., Untracht, G. R., Chandrasekaran, S. N., Brown, C. N., & Adie, S. G. (2015) · IEEE Journal of Selected Topics in Quantum Electronics · doi:10.1109/jstqe.2015.2481705 · Cited by 76
Seo, B. R., DelNero, P. F., & Fischbach, C. (2013) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2013.11.011 · Cited by 75
Koikawa, K., Ohuchida, K., Ando, Y., Kibe, S., Nakayama, H., Takesue, S., Endo, S., Abe, T., Okumura, T., Iwamoto, C., et al. (2018) · Cancer Letters · doi:10.1016/j.canlet.2018.03.031 · Cited by 72
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Hapach, L. A., Carey, S. P., Schwager, S. C., Taufalele, P., Wang, W., Mosier, J. A., Ortiz-Otero, N., McArdle, T. J., Goldblatt, Z. E., Lampi, M. C., et al. (2021) · Cancer Research · doi:10.1158/0008-5472.can-20-1799 · Cited by 70
Self-citationCancer-on-chip models for metastasis: importance of the tumor microenvironment
Jouybar, M., de Winde, C. M., Wolf, K., Friedl, P., Mebius, R. E., & den Toonder, J. M. J. (2024) · Trends in Biotechnology · doi:10.1016/j.tibtech.2023.10.001 · Cited by 66
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Campos, D. F. D., Lindsay, C. D., Roth, J. G., LeSavage, B. L., Seymour, A. J., Krajina, B. A., Ribeiro, R. D. C., Costa, P. F., Blaeser, A., & Heilshorn, S. C. (2020) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2020.00374 · Cited by 68
Iwamoto, C., Ohuchida, K., Shinkawa, T., Okuda, S., Otsubo, Y., Okumura, T., Sagara, A., Koikawa, K., Ando, Y., Shindo, K., et al. (2021) · Cancer Letters · doi:10.1016/j.canlet.2021.04.013 · Cited by 65
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Tabdanov, E. D., Puram, V. V., Zhovmer, A. S., & Provenzano, P. P. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.09.030 · Cited by 63
Bilandzic, M., Rainczuk, A., Green, E., Fairweather, N., Jobling, T. W., Plebanski, M., & Stephens, A. N. (2019) · Cancers · doi:10.3390/cancers11091228 · Cited by 63
Ferruzzi, J., Sun, M., Gkousioudi, A., Pilvar, A., Roblyer, D. M., Zhang, Y., & Zaman, M. H. (2019) · Scientific Reports · doi:10.1038/s41598-019-50268-z · Cited by 60
Huang, Y., Ma, Y., Wu, C., Shiau, C., Segall, J. E., & Wu, M. (2020) · Scientific Reports · doi:10.1038/s41598-020-66528-2 · Cited by 64
Orchestration of Collective Migration and Metastasis by Tumor Cell Clusters
Yamamoto, A., Doak, A. E., & Cheung, K. J. (2022) · Annual Review of Pathology Mechanisms of Disease · doi:10.1146/annurev-pathmechdis-031521-023557 · Cited by 60
Bimodal sensing of guidance cues in mechanically distinct microenvironments
Tabdanov, E. D., Puram, V. V., Win, Z., Alamgir, A., Alford, P. W., & Provenzano, P. P. (2018) · Nature Communications · doi:10.1038/s41467-018-07290-y · Cited by 59
Klymenko, Y., Johnson, J. K., Bos, B., Lombard, R., Campbell, L., Loughran, E. A., & Stack, M. S. (2017) · Neoplasia · doi:10.1016/j.neo.2017.04.002 · Cited by 61
Dynamics of Tissue-Induced Alignment of Fibrous Extracellular Matrix
Piotrowski-Daspit, A. S., Nerger, B. A., Wolf, A. E., Sundaresan, S., & Nelson, C. M. (2017) · Biophysical Journal · doi:10.1016/j.bpj.2017.06.046 · Cited by 60
The role of tumor microenvironment in collective tumor cell invasion
Wu, J., Sheng, S., Liang, X., & Tang, Y. (2017) · Future Oncology · doi:10.2217/fon-2016-0501 · Cited by 59
3D modeling of cancer stem cell niche
He, J., Xiong, L., Li, Q., Lin, L., Miao, X., Yan, S., Hong, Z., Yang, L., Wen, Y., & Deng, X. (2017) · Oncotarget · doi:10.18632/oncotarget.19847 · Cited by 59
Dynamics of 3D carcinoma cell invasion into aligned collagen
Ray, A., Morford, R. K., Ghaderi, N., Odde, D. J., & Provenzano, P. P. (2018) · Integrative Biology · doi:10.1039/c7ib00152e · Cited by 52
Spatarelu, C.-P., Zhang, H., Nguyen, D., Han, X., Liu, R., Guo, Q., Notbohm, J., Fan, J., Liu, L., & Chen, Z. (2019) · ACS Biomaterials Science & Engineering · doi:10.1021/acsbiomaterials.8b01428 · Cited by 52
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Devanny, A. J., Vancura, M. B., & Kaufman, L. J. (2021) · Molecular Biology of the Cell · doi:10.1091/mbc.e21-07-0357 · Cited by 48
Drifka, C. R., Loeffler, A. G., Esquibel, C. R., Weber, S. M., Eliceiri, K. W., & Kao, W. J. (2016) · Biomedical Microdevices · doi:10.1007/s10544-016-0128-1 · Cited by 51
Kassianidou, E., Probst, D., Jäger, J., Lee, S., Roguet, A.-L., Schwarz, U. S., & Kumar, S. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.04.035 · Cited by 47
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Self-citationMulligan, J. A., Feng, X., & Adie, S. G. (2019) · Scientific Reports · doi:10.1038/s41598-019-40608-4 · Cited by 46
Tumour heterogeneity promotes collective invasion and cancer metastatic dissemination
Hallou, A., Jennings, J., & Kabla, A. (2017) · Royal Society Open Science · doi:10.1098/rsos.161007 · Cited by 41
Clustering and jamming in epithelial–mesenchymal co-cultures
Castro, M. G., Leggett, S. E., & Wong, I. Y. (2016) · Soft Matter · doi:10.1039/c6sm01287f · Cited by 40
Koikawa, K., Ohuchida, K., Takesue, S., Ando, Y., Kibe, S., Nakayama, H., Endo, S., Abe, T., Okumura, T., Horioka, K., et al. (2017) · Cancer Letters · doi:10.1016/j.canlet.2017.10.010 · Cited by 42
Local alignment vectors reveal cancer cell-induced ECM fiber remodeling dynamics
Lee, B., Konen, J. M., Wilkinson, S. C., Marcus, A. I., & Jiang, Y. (2017) · Scientific Reports · doi:10.1038/srep39498 · Cited by 44
Qin, Z., Hou, H., Fu, F., Wu, J., Han, B., Yang, W., Zhang, L., Cao, J., Jin, X., Cheng, S., et al. (2017) · Reproductive Toxicology · doi:10.1016/j.reprotox.2017.08.014 · Cited by 39
Bordeleau, F., Alcoser, T. A., & Reinhart‐King, C. A. (2013) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00283.2013 · Cited by 37
Self-citationMulligan, J. A., Bordeleau, F., Reinhart‐King, C. A., & Adie, S. G. (2017) · Biomedical Optics Express · doi:10.1364/boe.8.001152 · Cited by 33
Self-citationLalli, M. L., & Asthagiri, A. R. (2015) · Cellular and Molecular Bioengineering · doi:10.1007/s12195-015-0383-x · Cited by 34
Collective cell migration modes in development, tissue repair and cancer
Cheung, K. J., & Horne‐Badovinac, S. (2025) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-025-00858-9 · Cited by 34
Fingering instabilities in tissue invasion: an active fluid model
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Wu, Y., Zhou, Y., Qin, X., & Liu, Y. (2021) · Biomicrofluidics · doi:10.1063/5.0062697 · Cited by 33
Sáenz‐de‐Santa‐María, I., Celada, L., & Chiara, M. (2020) · Cells · doi:10.3390/cells9030731 · Cited by 31
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Lorenzi, F. D., Hansen, N., Theek, B., Daware, R., Motta, A., Breuel, S., Nasehi, R., Baumeister, J., Schöneberg, J., Stojanovic, N. M., et al. (2023) · Advanced Materials · doi:10.1002/adma.202303196 · Cited by 33
Ford, A. J., Orbach, S. M., & Rajagopalan, P. (2019) · Biomaterials · doi:10.1016/j.biomaterials.2019.03.044 · Cited by 29
Cui, Y., Lee, P. C. K., Reardon, J. J., Wang, A., Lynch, S., Otero, J. J., Sizemore, G. M., & Winter, J. O. (2023) · Journal of Materials Chemistry B · doi:10.1039/d3tb00066d · Cited by 28
Carrasco-Mantis, A., Ranđelović, T., Castro-Abril, H. A., Ochoa, I., Doblaré, M., & Sanz‐Herrera, J. A. (2023) · Computers in Biology and Medicine · doi:10.1016/j.compbiomed.2023.106897 · Cited by 28
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Bruggeman, J. W., Köster, J., van Pelt, A. M. M., Speijer, D., & Hamer, G. (2022) · BioEssays · doi:10.1002/bies.202200112 · Cited by 28
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Parigoris, E., Lee, S., Mertz, D. R., Turner, M. C., Liu, A. Y., Sentosa, J., Djomehri, S. I., Chang, H. C., Luker, K. E., Luker, G. D., et al. (2020) · Advanced Healthcare Materials · doi:10.1002/adhm.202000810 · Cited by 24
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Perrin, L., & Gligorijevic, B. (2022) · Physical Biology · doi:10.1088/1478-3975/aca0d8 · Cited by 21
What makes leader cells arise: Intrinsic properties and support from neighboring cells
Chen, B., Wu, J., Ya-jie Tang, A., Tang, Y., & Liang, X. (2020) · Journal of Cellular Physiology · doi:10.1002/jcp.29828 · Cited by 20
Hapach, L. A., Wang, W., Schwager, S. C., Pokhriyal, D., Fabiano, E. D., & Reinhart‐King, C. A. (2023) · Breast Cancer Research · doi:10.1186/s13058-023-01696-3 · Cited by 18
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Leggett, S. E., Khoo, A., & Wong, I. Y. (2017) · Biomaterials Science · doi:10.1039/c7bm00272f · Cited by 18
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Suhail, Y., Maziarz, J. D., Novin, A., Dighe, A., Afzal, J. M., Wagner, G. P., & Gupta, K. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2111256119 · Cited by 18
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Wu, N. C., Cadavid, J. L., Tan, X., Latour, S., Scaini, S., Makhijani, P., McGaha, T. L., Ailles, L., & McGuigan, A. P. (2022) · Biomaterials · doi:10.1016/j.biomaterials.2022.121417 · Cited by 16
Wu, Y., Li, Y., Zheng, L., Wang, P., Liu, Y., Wu, Y., & Gong, Z. (2019) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2019.110077 · Cited by 17
Desa, D. E., Wu, W., Brown, R. M., Brown, E. B., Hill, R. L., Turner, B. M., & Brown, E. B. (2022) · Cancers · doi:10.3390/cancers14040857 · Cited by 16
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Zanotelli, M. R., Miller, J. P., Wang, W., Ortiz, I., Tahon, E., Bordeleau, F., & Reinhart‐King, C. A. (2024) · Biomaterials · doi:10.1016/j.biomaterials.2024.122682 · Cited by 16
Self-citationPajić‐Lijaković, I., Eftimie, R., Milivojevic, M. S., & Bordas, S. (2023) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2022.12.010 · Cited by 16
Simpson, M. J., Haridas, P., & McElwain, D. L. S. (2014) · PLoS ONE · doi:10.1371/journal.pone.0085488 · Cited by 16
The rearrangement of co-cultured cellular model systems via collective cell migration
Pajić‐Lijaković, I., Eftimie, R., Milivojevic, M. S., & Bordas, S. (2022) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2022.10.002 · Cited by 15
Burchett, A. A., Siri, S., Li, J., Lü, X., & Datta, M. (2024) · Cellular and Molecular Bioengineering · doi:10.1007/s12195-024-00824-z · Cited by 14
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Metadata
- Authors
- Carey, S. P., Starchenko, A., McGregor, A. L., & Reinhart-King, C. A.
- Affiliations
- Cornell University (US)
- ORCID
- Starchenko, Alina
- Venue
- Clinical & Experimental Metastasis
- Published
- 2013-01-18
- Volume
- 30
- Issue
- 5
- Pages
- 615-630
- ISSN
- 0262-0898 (ISSN-L)
- 1573-7276
- PMC
- PMC3646083
- OpenAlex
- W2143947514
- Cited by
- 174
- References
- 81
- Citations by year
- 2026: 12 · 2025: 10 · 2024: 13 · 2023: 16 · 2022: 12 · 2021: 12 · 2020: 12 · 2019: 18 · 2018: 15 · 2017: 16 · 2016: 18 · 2015: 8 · 2014: 7 · 2013: 5
- FWCI
- 6.79
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Clinical & Experimental Metastasis (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Science Foundation
- Barbara Ann Karmanos Cancer Institute
- National Cancer Institute (U54CA143876)
- Division of Civil, Mechanical and Manufacturing Innovation
- Topics
- Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular Mechanics and Interactions
- Physical Sciences › Mathematics › Modeling and Simulation › Mathematical Biology Tumor Growth
- Keywords
- intratumoral heterogeneity, collective cell invasion, leader-follower behavior, cancer cells, epithelial cells, tumor spheroids, extracellular matrix remodeling, proteolysis, cell contractility, cell-matrix interactions, tumor progression, metastasis
- MeSH terms
- Epithelial Cells, Extracellular Matrix, Female, Humans, Models, Biological, Neoplasm Invasiveness, Spheroids, Cellular, Cell Line, Tumor, Tumor Microenvironment
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