Dynamics of 3D carcinoma cell invasion into aligned collagen
Open accessAbstract
Carcinoma cells frequently expand and invade from a confined lesion, or multicellular clusters, into and through the stroma on the path to metastasis, often with an efficiency dictated by the architecture and composition of the microenvironment. Specifically, in desmoplastic carcinomas such as those of the breast, aligned collagen tracks provide contact guidance cues for directed cancer cell invasion. Yet, the evolving dynamics of this process of invasion remains poorly understood, in part due to difficulties in continuously capturing both spatial and temporal heterogeneity and progression to invasion in experimental systems. Therefore, to study the local invasion process from cell dense clusters into aligned collagen architectures found in solid tumors, we developed a novel engineered 3D invasion platform that integrates an aligned collagen matrix with a cell dense tumor-like plug. Using multiphoton microscopy and quantitative analysis of cell motility, we track the invasion of cancer cells from cell-dense bulk clusters into the pre-aligned 3D matrix, and define the temporal evolution of the advancing invasion fronts over several days. This enables us to identify and probe cell dynamics in key regions of interest: behind, at, and beyond the edge of the invading lesion at distinct time points. Analysis of single cell migration identifies significant spatial heterogeneity in migration behavior between cells in the highly cell-dense region behind the leading edge of the invasion front and cells at and beyond the leading edge. Moreover, temporal variations in motility and directionality are also observed between cells within the cell-dense tumor-like plug and the leading invasive edge as its boundary extends into the anisotropic collagen over time. Furthermore, experimental results combined with mathematical modeling demonstrate that in addition to contact guidance, physical crowding of cells is a key regulating factor orchestrating variability in single cell migration during invasion into anisotropic ECM. Thus, our novel platform enables us to capture spatio-temporal dynamics of cell behavior behind, at, and beyond the invasive front and reveals heterogeneous, local interactions that lead to the emergence and maintenance of the advancing front.
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ECM anisotropy is a hallmark in many cancers.
“Because ECM anisotropy is a hallmark in many cancers”
From Cancer-on-chip models for metastasis: importance of the tumor microenvironment (2024) · cites this paper as [23]
Alignment directs tumor invasion in hydrogels containing anisotropic structures generated by mechanical strain or by adding collagen-free tracks.
“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 [23]
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Cites
CellProfiler: image analysis software for identifying and quantifying cell phenotypes
Carpenter, A. E., Jones, T. R., Lamprecht, M. R., Clarke, C., Kang, I. H., Friman, O., Guertin, D. A., Chang, J. H., Lindquist, R. A., Moffat, J., et al. (2006) · Genome biology · doi:10.1186/gb-2006-7-10-r100 · Cited by 5,077 · see citing works
A pyramid approach to subpixel registration based on intensity
Thévenaz, P., Ruttimann, U. E., & Unser, M. A. (1998) · IEEE Transactions on Image Processing · doi:10.1109/83.650848 · Cited by 3,097 · see citing works
Brownian dynamics with hydrodynamic interactions
Ermak, D., & McCammon, J. (1978) · The Journal of Chemical Physics · doi:10.1063/1.436761 · Cited by 2,238 · see citing works
Cancer Invasion and the Microenvironment: Plasticity and Reciprocity
Friedl, P., & Alexander, S. (2011) · Cell · doi:10.1016/j.cell.2011.11.016 · Cited by 1,940 · see citing works
Collagen reorganization at the tumor-stromal interface facilitates local invasion
Provenzano, P. P., Eliceiri, K. W., Campbell, J. M., Inman, D. R., White, J. G., & Keely, P. J. (2006) · BMC Medicine · doi:10.1186/1741-7015-4-38 · Cited by 1,804 · see citing works
Self-citationCollagen density promotes mammary tumor initiation and progression
Provenzano, P. P., Inman, D. R., Eliceiri, K. W., Knittel, J. G., Yan, L., Rueden, C., White, J. G., & Keely, P. J. (2008) · BMC Medicine · doi:10.1186/1741-7015-6-11 · Cited by 1,364 · see citing works
Self-citationAligned Collagen Is a Prognostic Signature for Survival in Human Breast Carcinoma
Conklin, M. W., Eickhoff, J. C., Riching, K. M., Pehlke, C. A., Eliceiri, K. W., Provenzano, P. P., Friedl, A., & Keely, P. J. (2011) · American Journal Of Pathology · doi:10.1016/j.ajpath.2010.11.076 · Cited by 1,293 · see citing works
Self-citationTorres, E. T. R., Condeelis, J. S., & Patsialou, A. (2011) · Nature reviews. Cancer · doi:10.1038/nrc3078 · Cited by 900 · see citing works
Models of dispersal in biological systems
Othmer, H. G., Dunbar, S. R., & Alt, W. (1988) · Journal of Mathematical Biology · doi:10.1007/bf00277392 · Cited by 861 · see citing works
Collective Invasion in Breast Cancer Requires a Conserved Basal Epithelial Program
Cheung, K. J., Gabrielson, E. W., Werb, Z., & Ewald, A. J. (2013) · Cell · doi:10.1016/j.cell.2013.11.029 · Cited by 838 · see citing works
Goetz, J. G., Minguet, S., Navarro-Lérida, I., Lazcano, J. J., Samaniego, R., Calvo, E., Tello, M., Osteso-Ibáñez, T., Pellinen, T., Echarri, A., et al. (2011) · Cell · doi:10.1016/j.cell.2011.05.040 · Cited by 720 · see citing works
Physical influences of the extracellular environment on cell migration
Charras, G., & Sahai, E. A. (2014) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3897 · Cited by 678 · see citing works
Provenzano, P. P., Inman, D. R., Eliceiri, K. W., & Keely, P. J. (2009) · Oncogene · doi:10.1038/onc.2009.299 · Cited by 667 · see citing works
Self-citationContact inhibition of locomotion in vivo controls neural crest directional migration
Carmona‐Fontaine, C., Matthews, H. K., Kuriyama, S., Moreno, M., Dunn, G., Parsons, M., Stern, C. D., & Mayor, R. (2008) · Nature · doi:10.1038/nature07441 · Cited by 615 · see citing works
Matrix nanotopography as a regulator of cell function
Kim, D., Provenzano, P. P., Smith, C. L., & Levchenko, A. (2012) · The Journal of Cell Biology · doi:10.1083/jcb.201108062 · Cited by 576 · see citing works
Self-citationMicroregional extracellular matrix heterogeneity in brain modulates glioma cell invasion
Bellail, A. C., HUNTER, S. B., Brat, D. J., Tan, C., & Meir, E. G. V. (2004) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2004.01.013 · Cited by 527 · see citing works
Continuous growth of mean tumor diameter in a subset of grade II gliomas
Mandonnet, E., Delattre, J., Tanguy, M., Swanson, K. R., Carpentier, A. F., Duffau, H., Cornu, P., Effenterre, R. V., Alvord, E. C., & Capelle, L. (2003) · Annals of Neurology · doi:10.1002/ana.10528 · Cited by 493 · see citing works
Provenzano, P. P., Inman, D. R., Eliceiri, K. W., Trier, S. M., & Keely, P. J. (2008) · Biophysical Journal · doi:10.1529/biophysj.108.133116 · Cited by 493 · see citing works
Self-citationWang, W., Wyckoff, J. B., Frohlich, V. C., Oleynikov, Y., Hüttelmaier, S., Zavadil, J., C̆ermák, L., Böttinger, E. P., Singer, R. H., White, J. G., et al. (2002) · PubMed · Cited by 417 · see citing works
Bredfeldt, J. S., Liu, Y., Pehlke, C. A., Conklin, M. W., Szulczewski, J. M., Inman, D. R., Keely, P. J., Nowak, R. D., Mackie, T., & Eliceiri, K. W. (2014) · Journal of Biomedical Optics · doi:10.1117/1.jbo.19.1.016007 · Cited by 413 · see citing works
Zhang, K., Corsa, C. A. S., Ponik, S. M., Prior, J. L., Piwnica-Worms, D. R., Eliceiri, K. W., Keely, P. J., & Longmore, G. D. (2013) · Nature Cell Biology · doi:10.1038/ncb2743 · Cited by 393 · see citing works
Lyons, T. R., O’Brien, J., Borges, V. F., Conklin, M. W., Keely, P. J., Eliceiri, K. W., Marusyk, A., Tan, A. C., & Schedin, P. S. (2011) · Nature Medicine · doi:10.1038/nm.2416 · Cited by 381 · see citing works
Intravital third harmonic generation microscopy of collective melanoma cell invasion
Weigelin, B., Bakker, G., & Friedl, P. (2012) · IntraVital · doi:10.4161/intv.21223 · Cited by 360 · see citing works
Ray, A., Lee, O., Win, Z., Edwards, R. M., Alford, P. W., Kim, D.-H., & Provenzano, P. P. (2017) · Nature Communications · doi:10.1038/ncomms14923 · Cited by 293 · see citing works
Self-citationSwanson, K. R., Alvord, E. C., & Murray, J. D. (2002) · British Journal of Cancer · doi:10.1038/sj.bjc.6600021 · Cited by 249 · see citing works
Kato, M., Suzuki, T., Suzuki, Y., Terasawa, Y., Sasano, H., & Arai, Y. (2004) · The Journal of Urology · doi:10.1097/01.ju.0000136315.80057.99 · Cited by 175 · see citing works
Carey, S. P., Starchenko, A., McGregor, A. L., & Reinhart-King, C. A. (2013) · Clinical & Experimental Metastasis · doi:10.1007/s10585-013-9565-x · Cited by 174 · see citing works
Enhanced Directional Migration of Cancer Stem Cells in 3D Aligned Collagen Matrices
Ray, A., Slama, Z. M., Morford, R. K., Madden, S. A., & Provenzano, P. P. (2017) · Biophysical Journal · doi:10.1016/j.bpj.2017.01.007 · Cited by 170 · see citing works
Self-citationOptimal estimation of cell movement indices from the statistical analysis of cell tracking data
Dickinson, R. B., & Tranquillo, R. T. (1993) · AIChE Journal · doi:10.1002/aic.690391210 · Cited by 158 · see citing works
Contact guidance on oriented collagen gels
Dunn, G., & Ebendal, T. (1978) · Experimental Cell Research · doi:10.1016/0014-4827(78)90196-9 · Cited by 143 · see citing works
Drifka, C. R., Tod, J., Loeffler, A. G., Liu, Y., Thomas, G. J., Eliceiri, K. W., & Kao, W. J. (2015) · Modern Pathology · doi:10.1038/modpathol.2015.97 · Cited by 138 · see citing works
Breast Cancer Cell Invasion into a Three Dimensional Tumor-Stroma Microenvironment
Truong, D., Puleo, J., Llave, A., Mouneimne, G., Kamm, R. D., & Nikkhah, M. (2016) · Scientific Reports · doi:10.1038/srep34094 · Cited by 135 · see citing works
Provenzano, P. P., Inman, D. R., Eliceiri, K. W., Beggs, H. E., & Keely, P. J. (2008) · American Journal Of Pathology · doi:10.2353/ajpath.2008.080308 · Cited by 134 · see citing works
Self-citationHarms, B. D., Bassi, G. M., Horwitz, A. R., & Lauffenburger, D. A. (2005) · Biophysical Journal · doi:10.1529/biophysj.104.047365 · Cited by 124 · see citing works
Konen, J. M., Summerbell, E. R., Dwivedi, B., Galior, K. D., Hou, Y., Rusnak, L. E., Chen, A., Saltz, J. H., Zhou, W., Boise, L., et al. (2017) · Nature Communications · doi:10.1038/ncomms15078 · Cited by 121 · see citing works
Contact guidance induced organization of extracellular matrix
Manwaring, M. E., Walsh, J. F., & Tresco, P. A. (2003) · Biomaterials · doi:10.1016/j.biomaterials.2003.10.043 · Cited by 110 · see citing works
Beck, J. N., Singh, A., Rothenberg, A. R., Elisseeff, J. H., & Ewald, A. J. (2013) · Biomaterials · doi:10.1016/j.biomaterials.2013.08.077 · Cited by 108 · see citing works
Grinnell, F., Rocha, L. B., Iucu, C., Rhee, S., & Jiang, H. (2005) · Experimental Cell Research · doi:10.1016/j.yexcr.2005.10.001 · Cited by 102 · see citing works
Processing of type I collagen gels using nonenzymatic glycation
Roy, R., Boskey, A. L., & Bonassar, L. J. (2009) · Journal of Biomedical Materials Research Part A · doi:10.1002/jbm.a.32231 · Cited by 97 · see citing works
Miron-Mendoza, M., Seemann, J., & Grinnell, F. (2008) · Molecular Biology of the Cell · doi:10.1091/mbc.e07-09-0930 · Cited by 79 · see citing works
Blacher, S., Erpicum, C., Lenoir, B., Paupert, J., Moraes, G., Orménèse, S., Bullinger, E., & Noël, A. (2014) · PLoS ONE · doi:10.1371/journal.pone.0097019 · Cited by 66 · see citing works
Shining new light on 3D cell motility and the metastatic process
Provenzano, P. P., Eliceiri, K. W., & Keely, P. J. (2009) · Trends in Cell Biology · doi:10.1016/j.tcb.2009.08.009 · Cited by 57 · see citing works
Self-citationMultiscale Cues Drive Collective Cell Migration
Nam, K., Kim, P., Wood, D. K., Kwon, S., Provenzano, P. P., & Kim, D. (2016) · Scientific Reports · doi:10.1038/srep29749 · Cited by 53 · see citing works
Self-citationCastle, B. T., & Odde, D. J. (2013) · Biophysical Journal · doi:10.1016/j.bpj.2013.10.009 · Cited by 44 · see citing works
Self-citationAn experimental model for assessing fibroblast migration in 3‐D collagen matrices
Karamichos, D., Lakshman, N., & Petroll, W. M. (2008) · Cell Motility and the Cytoskeleton · doi:10.1002/cm.20326 · Cited by 43 · see citing works
Lee, M. W., Downes, A., Chau, Y.-Y., Serrels, B., Hastie, N. D., Elfick, A. P. D., Brunton, V. G., Frame, M. C., & Serrels, A. (2015) · IntraVital · doi:10.1080/21659087.2015.1055430 · Cited by 41 · see citing works
Intravital characterization of tumor cell migration in pancreatic cancer
Beerling, E., Oosterom, I., Voest, E. E., Lolkema, M. P., & van Rheenen, J. (2016) · IntraVital · doi:10.1080/21659087.2016.1261773 · Cited by 36 · see citing works
Massey, S. C., Assanah, M. C., Lopez, K. A., Canoll, P., & Swanson, K. R. (2012) · Journal of The Royal Society Interface · doi:10.1098/rsif.2012.0030 · Cited by 32 · see citing works
Mason, B. N., & Reinhart‐King, C. A. (2013) · Organogenesis · doi:10.4161/org.24942 · Cited by 28 · see citing works
A Brownian dynamics tumor progression simulator with application to glioblastoma
Klank, R. L., Rosenfeld, S. S., & Odde, D. J. (2018) · Convergent Science Physical Oncology · doi:10.1088/2057-1739/aa9e6e · Cited by 24 · see citing works
Self-citationMultiphoton fluorescence lifetime imaging of chemotherapy distribution in solid tumors
Carlson, M., Watson, A. L., Anderson, L. K., Largaespada, D. A., & Provenzano, P. P. (2017) · Journal of Biomedical Optics · doi:10.1117/1.jbo.22.11.116010 · Cited by 24 · see citing works
Self-citationWang, B., Wang, H.-W., Guo, H., Anderson, E., Tang, Q., Wu, T., Falola, R. A., Smith, T., Andrews, P. M., & Chen, Y. (2017) · Journal of Biomedical Optics · doi:10.1117/1.jbo.22.12.121706 · Cited by 18 · see citing works
Flagged first, then by citations
Research works printed but not linked: 5
- [1]Roussos ET Condeelis JS Patsialou A Nat Rev Cancer 2011 11 573 587 21779009 PMC4030706
- [14]Wang W Wyckoff JB Frohlich VC Oleynikov Y Huttelmaier S Zavadil J Cermak L Bottinger EP Singer RH White JG Segall JE Condeelis JS Cancer research 2002 62 6278 6288 12414658
- [32]Carmona-Fontaine C Matthews HK Kuriyama S Moreno M Dunn GA Parsons M Stern CD Mayor R Nature 2008 456 957 961 19078960 PMC2635562
- [49]Dickinson RB Tranquillo RT Journal 1993 39 1995 2010
- [51]Ermak D McCammon J Journal of Chemical Physics 1978 69 1352 1360
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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 133 · see citing works
Comba, A., Faisal, S. M., Dunn, P., Argento, A. E., Hollon, T. C., Al‐Holou, W. N., Varela, M. L., Zamler, D. B., Quass, G. L., Apostolides, P. F., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-31340-1 · Cited by 112 · see citing works
Obesity, sleep apnea, and cancer
Almendros, I., Martínez‐García, M. Á., Farré, R., & Gozal, D. (2020) · International Journal of Obesity · doi:10.1038/s41366-020-0549-z · Cited by 88 · see citing works
The neuroendocrine transition in prostate cancer is dynamic and dependent on ASCL1
Romero, R., Chu, T., González-Robles, T. J., Smith, P., Xie, Y., Kaur, H., Yoder, S., Zhao, H., Mao, C., Kang, W., et al. (2024) · Nature Cancer · doi:10.1038/s43018-024-00838-6 · Cited by 85 · see citing works
Ray, A., & Provenzano, P. P. (2021) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2021.05.004 · Cited by 80 · see citing works
Self-citationStromal architecture directs early dissemination in pancreatic ductal adenocarcinoma
Ray, A., Callaway, M. K., Rodríguez-Merced, N. J., Crampton, A. L., Carlson, M., Emme, K. B., Ensminger, E. A., Kinne, A. A., Schrope, J. H., Rasmussen, H. R., et al. (2021) · JCI Insight · doi:10.1172/jci.insight.150330 · Cited by 65 · see citing works
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 · see citing works
Engineering the Extracellular Matrix to Model the Evolving Tumor Microenvironment
Micek, H. M., Visetsouk, M. R., Masters, K. S. B., & Kreeger, P. K. (2020) · iScience · doi:10.1016/j.isci.2020.101742 · Cited by 53 · see citing works
Carpino, G., Overi, D., Melandro, F., Grimaldi, A., Cardinale, V., Matteo, S. D., Mennini, G., Rossi, M., Alvaro, D., Barnaba, V., et al. (2019) · Clinical Proteomics · doi:10.1186/s12014-019-9257-x · Cited by 53 · see citing works
Szulczewski, J. M., Inman, D. R., Proestaki, M., Notbohm, J., Burkel, B. M., & Ponik, S. M. (2021) · Acta Biomaterialia · doi:10.1016/j.actbio.2021.04.053 · Cited by 47 · see citing works
Alkmin, S., Brodziski, R., Simon, H., Hinton, D. A., Goldsmith, R. H., Patankar, M. S., & Campagnola, P. J. (2020) · Cancers · doi:10.3390/cancers12061390 · Cited by 45 · see citing works
Asem, M., Young, A., Oyama, C., Zerda, A. C. D. L., Liu, Y., Ravosa, M. J., Gupta, V. G., Jewell, A., Khabele, D., & Stack, M. S. (2020) · Scientific Reports · doi:10.1038/s41598-020-68639-2 · Cited by 46 · see citing works
Walimbe, T., & Panitch, A. (2020) · Bioengineering · doi:10.3390/bioengineering7040156 · Cited by 45 · see citing works
Role of extracellular matrix architecture and signaling in melanoma therapeutic resistance
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Engineering fiber anisotropy within natural collagen hydrogels
Ahmed, A., Joshi, I. M., Mansouri, M., Ahamed, N. N. N., Hsu, M.-C., Gaborski, T. R., & Abhyankar, V. V. (2021) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00036.2021 · Cited by 41 · see citing works
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Su, C., Burchett, A. A., Dunworth, M., Choi, J. S., Ewald, A. J., Ahn, E. H., & Kim, D. (2021) · Biomaterials · doi:10.1016/j.biomaterials.2021.120922 · Cited by 37 · see citing works
Local extensional flows promote long-range fiber alignment in 3D collagen hydrogels
Ahmed, A., Mansouri, M., Joshi, I. M., Byerley, A. M., Day, S. W., Gaborski, T. R., & Abhyankar, V. V. (2022) · Biofabrication · doi:10.1088/1758-5090/ac7824 · Cited by 27 · see citing works
An in-silico study of cancer cell survival and spatial distribution within a 3D microenvironment
Cortesi, M., Liverani, C., Mercatali, L., Ibrahim, T., & Giordano, E. (2020) · Scientific Reports · doi:10.1038/s41598-020-69862-7 · Cited by 24 · see citing works
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Joshi, I. M., Mansouri, M., Ahmed, A., Silva, D. D., Simon, R. A., Esmaili, P., Desa, D. E., Elias, T. M., Brown, E. B., & Abhyankar, V. V. (2023) · Advanced Functional Materials · doi:10.1002/adfm.202308071 · Cited by 24 · see citing works
Azimzade, Y., Saberi, A. A., & Sahimi, M. (2019) · Physical review. E · doi:10.1103/physreve.99.062414 · Cited by 23 · see citing works
Zhovmer, A. S., Manning, A., Smith, C., Hayes, J. B., Burnette, D. T., Wang, J., Cartagena‐Rivera, A. X., Dokholyan, N. V., Singh, R. K., & Tabdanov, E. D. (2021) · ACS Nano · doi:10.1021/acsnano.1c04435 · Cited by 19 · see citing works
Kunze, P., Kreiss, L. A., Novosadová, V., Roehe, A. V., Steinmann, S. M., Procházka, J., Geppert, C. I., Hartmann, A., Schürmann, S., Friedrich, O., et al. (2022) · Cancers · doi:10.3390/cancers14102364 · Cited by 16 · see citing works
Alkmin, S., Brodziski, R., Simon, H., Hinton, D. A., Goldsmith, R. H., Patankar, M. S., & Campagnola, P. J. (2019) · Acta Biomaterialia · doi:10.1016/j.actbio.2019.09.037 · Cited by 16 · see citing works
Chen, D., Du, Y. M., Llewellyn, J., Bonna, A., Zuo, B., Janmey, P. A., Farndale, R. W., & Wells, R. G. (2024) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2024.107968 · Cited by 14 · see citing works
Geiger, F., Schnitzler, L. G., Brugger, M. S., Westerhausen, C., & Engelke, H. (2022) · PLoS ONE · doi:10.1371/journal.pone.0264571 · Cited by 13 · see citing works
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Conte, M. L., & Loy, N. (2023) · SIAM Journal on Applied Mathematics · doi:10.1137/22m1506389 · Cited by 9 · see citing works
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Azimzade, Y., & Saberi, A. A. (2019) · Journal of Statistical Mechanics Theory and Experiment · doi:10.1088/1742-5468/ab4983 · Cited by 4 · see citing works
Residual stress and osmotic swelling of the periodontal ligament
Nedrelow, D. S., Damodaran, K. V., Thurston, T. A., Beyer, J. P., & Barocas, V. H. (2021) · Biomechanics and Modeling in Mechanobiology · doi:10.1007/s10237-021-01493-x · Cited by 4 · see citing works
Pamonag, M., Hinson, A., Burton, E. J., Jafari, N., Sales, D. J., Babcock, S., Basha, R., Hu, X., & Kubow, K. E. (2022) · PLoS ONE · doi:10.1371/journal.pone.0265403 · Cited by 3 · see citing works
Cancer-Associated Fibroblasts and Their Role in Cancer Progression
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Comba, A., Faisal, S. M., Dunn, P. J., Argento, A. E., Hollon, T. C., Al‐Holou, W. N., Varela, M. L., Zamler, D. B., Quass, G. L., Apostolides, P. F., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.12.01.404970 · Cited by 2 · see citing works
Ley, A. W. Y., Bersie-Larson, L. M., Adhikari, S., Provenzano, P. P., Dorfman, K. D., & Barocas, V. H. (2026) · Cellular and Molecular Bioengineering · doi:10.1007/s12195-026-00922-0 · Cited by 1 · see citing works
Self-citationÖnal, S., Alkaisi, M. M., & Nock, V. (2024) · Heliyon · doi:10.1016/j.heliyon.2024.e41433 · Cited by 1 · see citing works
Potter, M., & Richardson, W. J. (2021) · Acta Biomaterialia · doi:10.1016/j.actbio.2021.09.049 · Cited by 1 · see citing works
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Shamsan, G. A., Liu, C. J., Braman, B. C., Li, R., Rathe, S. K., Sarver, A. L., Ghaderi, N., McMahon, M. M., Klank, R. L., Tschida, B. R., et al. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.06.26.497270 · Cited by 1 · see citing works
Self-citationMicrotubule-based control of glioma cell migration mechanics
Prahl, L. S. (2018) · University of Minnesota Digital Conservancy (University of Minnesota)
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Leineweber, W. D., & Fraley, S. I. (2022) · SSRN Electronic Journal · doi:10.2139/ssrn.4152108
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Sharma, S., & Nain, A. S. (2022) · Royal Society of Chemistry eBooks · doi:10.1039/9781839166013-00030
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Mierke, C. T. (2022) · Royal Society of Chemistry eBooks · doi:10.1039/9781839166013-00060
Qin, S., Cheng, W., Peng, M.-Y., Cai, C., Lei, Q., Huang, R., Cheng, Y.-J., Liu, W.-L., Ma, Y., Zhang, A., et al. (2026) · Biomaterials · doi:10.1016/j.biomaterials.2026.124017
Glioblastoma Subtypes Exhibit Distinct Migration Mechanics and Immune Responses
Shamsan, G. A., Liu, C. J., Braman, B. C., Li, R., Rathe, S. K., Sarver, A. L., Ghaderi, N., McMahon, M. M., Klank, R. L., Tschida, B. R., et al. (2026) · Cancer Research Communications · doi:10.1158/2767-9764.crc-25-0579 · Cited by 1 · see citing works
Self-citationDecoding Post-Transcriptional Networks Governing the Melanoma Extracellular Matrix
Katsoulieris, E. N., Ioannou, P., & Afratis, N. A. (2026) · Cancers · doi:10.3390/cancers18142326
- Authors
- Ray, A., Morford, R. K., Ghaderi, N., Odde, D. J., & Provenzano, P. P.
- Affiliations
- University of Minnesota (US)
- Corresponding author
- Provenzano, Paolo. P.
- Venue
- Integrative Biology
- Publisher
- Oxford University Press (OUP)
- Published
- 2018
- Volume
- 10
- Issue
- 2
- Pages
- 100-112
- ISSN
- 1757-9694 (ISSN-L)
- 1757-9708
- PMC
- PMC6004317
- OpenAlex
- W2781758570
- Cited by
- 52
- References
- 52
- Citations by year
- 2026: 5 · 2024: 5 · 2023: 6 · 2022: 13 · 2021: 9 · 2020: 7 · 2019: 6 · 2018: 1
- FWCI
- 3.19
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Integrative Biology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Cancer Institute (R01CA181385, U54CA210190)
- American Cancer Society (RSG-14-171-01-CSM)
- Directorate for Engineering (00039202)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular Mechanics and Interactions
- Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
- Physical Sciences › Mathematics › Modeling and Simulation › Mathematical Biology Tumor Growth
- Keywords
- tumor invasion, desmoplasia, contact guidance, single-cell migration, cell crowding, breast cancer
- MeSH terms
- Breast Neoplasms, Carcinoma, Cell Movement, Collagen, Extracellular Matrix, Female, Humans, Models, Biological, Neoplasm Invasiveness, Imaging, Three-Dimensional, Microscopy, Fluorescence, Multiphoton, Cell Line, Tumor, Systems Biology
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