The DOI matches its Crossref record; 32 of the 32 references it cites were found in a registry or an index.
Transition to invasion in breast cancer: a microfluidic in vitro model enables examination of spatial and temporal effects
Open accessAbstract
The transition of ductal carcinoma in situ (DCIS) to invasive ductal carcinoma (IDC) is a critical step in breast cancer progression. We introduce a simple microfluidic 3D compartmentalized system in which mammary epithelial cells (MCF-DCIS) are co-cultured with human mammary fibroblasts (HMFs), which promotes a transition from DCIS to IDC in vitro. The model enables control of both spatial (distance-dependence) and temporal (transition from larger clusters) aspects within the microenvironment, allowing recapitulation of the in vivo environment in ways not practical with existing experimental models. When HMFs were cultured some distance (0.5-1.5 mm) from the MCF-DCIS cells, we observed an initial morphological change, suggesting soluble factors can begin the transition. However, cell-cell contact with HMFs allowed the MCF-DCIS cells to complete the transition to invasion. Uniquely, the compartmentalized platform enables the analysis of the intrinsic second harmonic generation signal of collagen, providing a label-free quantitative analysis of DCIS-associated collagen remodeling. The arrayed microchannel-based model is compatible with existing infrastructure and, for the first time, provides a cost effective approach to test for inhibitors of pathways involved in DCIS progression to IDC allowing a screening approach to the identification of potential therapeutic targets. Importantly, the model can be easily adapted and generalized to a variety of cell-cell signaling studies.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The cited source says what the claim attributes to it.
In the citing paper
“The HMFs and MCF10-DCIS cells established a crosstalk at the interface between the cancerous and normal microtissue sections.”
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 [33]
The cited source says what the claim attributes to it.
In the citing paper
“MCF10-DCIS cancer cells adopted different shapes (i.e., their circularity, roundness, and aspect ratio significantly changed) as a function of their distance from the interface”
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 [33]
The cited source says what the claim attributes to it.
In the citing paper
“The change in shape of MCF710-DCIS cells, and their ability to remodel the matrix, suggested the onset of a DCIS to IDS transition.”
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 [33]
The cited source says what the claim attributes to it.
In the citing paper
“and the cell–cell contact between HMFs and MCF-DCIS cells favored the completed transition to an invasive phenotype.”
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 [33]
The cited source says what the claim attributes to it.
In the citing paper
“Clusters of cells in co-culture (HMF and MCF10-DCIS) affected the structure (physical appearance under the microscope) of the matrix significantly more than did monocultured MCF10-DCIS cells.”
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 [33]
The cited source says what the claim attributes to it.
In the citing paper
“This transition strongly depended on the distance between the cells, being more evident around the cell interfaces.”
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 [33]
The cited source says what the claim attributes to it.
In the citing paper
“Sung’s experimental results suggested an underlying two-step molecular mechanism for the transition from DCIS to IDS”
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 [33]
The cited source says what the claim attributes to it.
In the citing paper
“suggesting that soluble factors could initiate the transition”
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 [33]
The cited source says what the claim attributes to it.
In the citing paper
“An initial morphological change was first observed when HMFs were cultured at some distance (0.5–1.5 mm) from the MCF-DCIS cells”
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 [33]
In the citing paper
“Based on spheroids, Sung’s group proposed a 3D microfluidic model of breast cancer invasion using surface tension pumping to achieve the sequential loading of cells at different time points177.”
From Tumor-on-a-chip: from bioinspired design to biomedical application (2021) · cites this paper as [177]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
The distribution of secondary growths in cancer of the breast.
Paget, S. (1889) · The Lancet · doi:10.1016/s0140-6736(00)49915-0 · Cited by 5,277
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
Self-citationGaggioli, C., Hooper, S., Hidalgo-Carcedo, C., Grosse, R., Marshall, J. F., Harrington, K., & Sahai, E. (2007) · Nature Cell Biology · doi:10.1038/ncb1658 · Cited by 1,589
Interpreting Second-Harmonic Generation Images of Collagen I Fibrils
Williams, R. M., Zipfel, W. R., & Webb, W. W. (2004) · Biophysical Journal · doi:10.1529/biophysj.104.047308 · Cited by 847
Dynamic imaging of collagen and its modulation in tumors in vivo using second-harmonic generation
Brown, E. B., McKee, T. D., DiTomaso, E., Pluen, A., Seed, B., Boucher, Y., & Jain, R. K. (2003) · Nature Medicine · doi:10.1038/nm879 · Cited by 844
Reconstruction of functionally normal and malignant human breast tissues in mice
Kuperwasser, C., Chavarria, T. E., Wu, M., Magrane, G., Gray, J. W., Carey, L., Richardson, A. L., & Weinberg, R. A. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0401064101 · Cited by 807
Ductal Carcinoma in Situ of the Breast
Burstein, H. J., Polyák, K., Wong, J. S., Lester, S. C., & Kaelin, C. M. (2004) · New England Journal of Medicine · doi:10.1056/nejmra031301 · Cited by 769
Biological implications of polydimethylsiloxane-based microfluidic cell culture
Regehr, K. J., Domenech, M., Koepsel, J. T., Carver, K. C., Ellison-Zelski, S. J., Murphy, W. L., Schuler, L. A., Alarid, E. T., & Beebe, D. J. (2009) · Lab on a Chip · doi:10.1039/b903043c · Cited by 719
Self-citationThe actin cytoskeleton in cancer cell motility
Olson, M. F., & Sahai, E. A. (2008) · Clinical & Experimental Metastasis · doi:10.1007/s10585-008-9174-2 · Cited by 577
ErbB2, but not ErbB1, reinitiates proliferation and induces luminal repopulation in epithelial acini
Muthuswamy, S. K., Li, D., Lelièvre, S. A., Bissell, M. J., & Brugge, J. S. (2001) · Nature Cell Biology · doi:10.1038/ncb0901-785 · Cited by 554
Flagged first, then by citations
Cited by
Sorted by citations
Bhatia, S. N., & Ingber, D. E. (2014) · Nature Biotechnology · doi:10.1038/nbt.2989 · Cited by 3,305
The present and future role of microfluidics in biomedical research
Sackmann, E. K., Fulton, A. L., & Beebe, D. J. (2014) · Nature · doi:10.1038/nature13118 · Cited by 2,995
Self-citationFrom 3D cell culture to organs-on-chips
Huh, D., Hamilton, G. A., & Ingber, D. E. (2011) · Trends in Cell Biology · doi:10.1016/j.tcb.2011.09.005 · Cited by 1,834
A Human Disease Model of Drug Toxicity–Induced Pulmonary Edema in a Lung-on-a-Chip Microdevice
Huh, D., Leslie, D. C., Matthews, B. D., Fraser, J. P., Jurek, S., Hamilton, G. A., Thorneloe, K. S., McAlexander, M. A., & Ingber, D. E. (2012) · Science Translational Medicine · doi:10.1126/scitranslmed.3004249 · Cited by 993
Modelling cancer in microfluidic human organs-on-chips
Sontheimer-Phelps, A., Hassell, B. A., & Ingber, D. E. (2019) · Nature Reviews Cancer · doi:10.1038/s41568-018-0104-6 · Cited by 906
Engineers are from PDMS-land, Biologists are from Polystyrenia
Berthier, E., Young, E. W. K., & Beebe, D. J. (2012) · Lab on a Chip · doi:10.1039/c2lc20982a · Cited by 820
Self-citationIn Vitro Tumor Models: Advantages, Disadvantages, Variables, and Selecting the Right Platform
Katt, M. E., Placone, A. L., Wong, A. D., Xu, Z. S., & Searson, P. C. (2016) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2016.00012 · Cited by 754
Human 3D vascularized organotypic microfluidic assays to study breast cancer cell extravasation
Jeon, J. S., Bersini, S., Gilardi, M., Dubini, G., Charest, J. L., Moretti, M., & Kamm, R. D. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1417115112 · Cited by 723
Microfabrication of human organs-on-chips
Huh, D., Kim, H. J., Fraser, J. P., Shea, D. E., Khan, M., Bahinski, A., Hamilton, G. A., & Ingber, D. E. (2013) · Nature Protocols · doi:10.1038/nprot.2013.137 · Cited by 712
Microengineered physiological biomimicry: Organs-on-Chips
Huh, D., Torisawa, Y., Hamilton, G. A., Kim, H. J., & Ingber, D. E. (2012) · Lab on a Chip · doi:10.1039/c2lc40089h · Cited by 685
Engineered In Vitro Disease Models
Benam, K. H., Dauth, S., Hassell, B., Herland, A., Jain, A., Jang, K.-J., Karalis, K., Kim, H. J., MacQueen, L., Mahmoodian, R., et al. (2015) · Annual Review of Pathology: Mechanisms of Disease · doi:10.1146/annurev-pathol-012414-040418 · Cited by 554
A microfluidic 3D in vitro model for specificity of breast cancer metastasis to bone
Bersini, S., Jeon, J. S., Dubini, G., Arrigoni, C., Chung, S., Charest, J. L., Moretti, M., & Kamm, R. D. (2014) · Biomaterials · doi:10.1016/j.biomaterials.2013.11.050 · Cited by 534
Microfluidic 3D Cell Culture: Potential Application For Tissue-Based Bioassays
Li, X., Valadez, A., Zuo, P., & Nie, Z. (2012) · Bioanalysis · doi:10.4155/bio.12.133 · Cited by 329
Barbosa, M. A. G., Xavier, C. P. R., Pereira, R. F., Petrikaitė, V., & Vasconcelos, M. H. (2021) · Cancers · doi:10.3390/cancers14010190 · Cited by 285
Recent advances in microfluidic technologies for cell-to-cell interaction studies
Rothbauer, M., Zirath, H., & Ertl, P. (2018) · Lab on a Chip · doi:10.1039/c7lc00815e · Cited by 277
Tumor-on-a-chip: from bioinspired design to biomedical application
Liu, X., Fang, J., Huang, S., Wu, X., Xie, X., Wang, J., Liu, F., Zhang, M., Peng, Z., & Hu, N. (2021) · Microsystems & Nanoengineering · doi:10.1038/s41378-021-00277-8 · Cited by 246
Microfluidics‐based 3D cell culture models: Utility in novel drug discovery and delivery research
Gupta, N., Liu, J. R., Patel, B., Solomon, D. E., Vaidya, B., & Gupta, V. (2016) · Bioengineering & Translational Medicine · doi:10.1002/btm2.10013 · Cited by 244
Tumor cell migration in complex microenvironments
Polacheck, W. J., Zervantonakis, I. K., & Kamm, R. D. (2012) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-012-1115-1 · Cited by 229
Microfluidics: A New Tool for Modeling Cancer–Immune Interactions
Boussommier-Calleja, A., Li, R., Chen, M. B., Wong, S. C., & Kamm, R. D. (2016) · Trends in Cancer · doi:10.1016/j.trecan.2015.12.003 · Cited by 224
A microengineered pathophysiological model of early-stage breast cancer
Choi, Y., Hyun, E., Seo, J., Blundell, C., Kim, H. C., Lee, E., Lee, S. H., Moon, A., Moon, W. K., & Huh, D. (2015) · Lab on a Chip · doi:10.1039/c5lc00514k · Cited by 222
Organ-on-chip models of cancer metastasis for future personalized medicine: From chip to the patient
Caballero, D., Kaushik, S., Correlo, V. M., Oliveira, J. M., Reis, R. L., & Kundu, S. C. (2017) · Biomaterials · doi:10.1016/j.biomaterials.2017.10.005 · Cited by 221
Organ-on-a-Chip for Cancer and Immune Organs Modeling
Sun, W., Luo, Z., Lee, J., Kim, H., Lee, K., Tebon, P., Feng, Y., Dokmeci, M. R., Sengupta, S., & Khademhosseini, A. (2019) · Advanced Healthcare Materials · doi:10.1002/adhm.201801363 · Cited by 221
Biomedical Applications of Microfluidic Devices: A Review
Gharib, G., Bütün, İ., Muganlı, Z., Kozalak, G., Namlı, İ., Sarraf, S. S., Ahmadi, V. E., Toyran, E., van Wijnen, A. J., & Koşar, A. (2022) · Biosensors · doi:10.3390/bios12111023 · Cited by 246
Expansion of CTCs from early stage lung cancer patients using a microfluidic co-culture model
Zhang, Z., Shiratsuchi, H., Lin, J., Chen, G., Reddy, R. M., Azizi, E., Fouladdel, S., Chang, A. C., Lin, L., Jiang, H., et al. (2014) · Oncotarget · doi:10.18632/oncotarget.2592 · Cited by 207
Microfluidic Organ‐on‐a‐Chip Technology for Advancement of Drug Development and Toxicology
Caplin, J. D., Granados, N. G., James, M. R., Montazami, R., & Hashemi, N. (2015) · Advanced Healthcare Materials · doi:10.1002/adhm.201500040 · Cited by 205
Lazzari, G., Couvreur, P., & Mura, S. (2017) · Polymer Chemistry · doi:10.1039/c7py00559h · Cited by 209
Mechanobiology of Tumor Growth
Chaudhuri, P. K., Low, B. C., & Lim, C. T. (2018) · Chemical Reviews · doi:10.1021/acs.chemrev.8b00042 · Cited by 200
Microfluidic titer plate for stratified 3D cell culture
Trietsch, S. J., Israëls, G. D., Joore, J., Hankemeier, T., & Vulto, P. (2013) · Lab on a Chip · doi:10.1039/c3lc50210d · Cited by 189
Microfluidic 3D models of cancer
Sung, K. E., & Beebe, D. J. (2014) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2014.07.002 · Cited by 190
Self-citationTrujillo-de Santiago, G., Flores-Garza, B. G., Tavares-Negrete, J. A., Lara-Mayorga, I. M., González-Gamboa, I., Zhang, Y. S., Rojas-Martínez, A., Ortiz-López, R., & Álvarez, M. M. (2019) · Materials · doi:10.3390/ma12182945 · Cited by 184
“developed a simple tumor-on-chip to study a key step in breast cancer progression, namely the transition of ductal carcinoma in situ (DCIS) into invasive ductal carcinoma (IDC) [33].”
BackgroundInfluentialThree-dimensional in vitro cancer models: a short review
Wang, C., Tang, Z., Zhao, Y., Yao, R., Li, L., & Sun, W. (2014) · Biofabrication · doi:10.1088/1758-5082/6/2/022001 · Cited by 173
Microfluidic cell culture models for tissue engineering
Inamdar, N. K., & Borenstein, J. T. (2011) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2011.05.512 · Cited by 166
Cross talk between cancer and immune cells: exploring complex dynamics in a microfluidic environment
Businaro, L., De Ninno, A., Schiavoni, G., Lucarini, V., Ciasca, G., Gerardino, A., Belardelli, F., Gabriele, L., & Mattei, F. (2013) · Lab Chip · doi:10.1039/c2lc40887b · Cited by 162
Unger, C., Kramer, N., Walzl, A., Scherzer, M., Hengstschläger, M., & Dolznig, H. (2014) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2014.10.015 · Cited by 158
Heralding a new paradigm in 3D tumor modeling
Fong, E. L. S., Harrington, D. A., Farach‐Carson, M. C., & Yu, H. (2016) · Biomaterials · doi:10.1016/j.biomaterials.2016.08.052 · Cited by 156
Zhang, R., & Larsen, N. B. (2017) · Lab on a Chip · doi:10.1039/c7lc00926g · Cited by 154
Physiologically relevant organs on chips
Yum, K., Hong, S. G., Healy, K. E., & Lee, L. P. (2013) · Biotechnology Journal · doi:10.1002/biot.201300187 · Cited by 156
Shao, Y., & Fu, J. (2013) · Advanced Materials · doi:10.1002/adma.201304431 · Cited by 151
Young, E. W. K. (2013) · Integrative Biology · doi:10.1039/c3ib40076j · Cited by 145
Anguiano, M., Castilla, C., Maška, M., Ederra, C., Peláez, R., Morales, X., Muñoz-Arrieta, G., Mujika, M., Kozubek, M., Muñoz‐Barrutia, A., et al. (2017) · PLoS ONE · doi:10.1371/journal.pone.0171417 · Cited by 149
Bone-on-a-chip: Microfluidic technologies and microphysiologic models of bone tissue
Mansoorifar, A., Gordon, R., Bergan, R. C., & Bertassoni, L. E. (2021) · Advanced Functional Materials · doi:10.1002/adfm.202006796 · Cited by 142
Understanding the Impact of 2D and 3D Fibroblast Cultures on In Vitro Breast Cancer Models
Sung, K. E., Su, X., Berthier, E., Pehlke, C. A., Friedl, A., & Beebe, D. J. (2013) · PLoS ONE · doi:10.1371/journal.pone.0076373 · Cited by 145
Self-citationTherapy response testing of breast cancer in a 3D high-throughput perfused microfluidic platform
Lanz, H. L., Saleh, A., Kramer, B., Cairns, J., Ng, C. P., Yu, J., Trietsch, S. J., Hankemeier, T., Joore, J., Vulto, P., et al. (2017) · BMC Cancer · doi:10.1186/s12885-017-3709-3 · Cited by 135
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
Modeling Endometrial Cancer: Past, Present, and Future
Nyen, T. V., Moiola, C. P., Colás, E., Annibali, D., & Amant, F. C. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19082348 · Cited by 124
Metastasis in context: modeling the tumor microenvironment with cancer-on-a-chip approaches
Sleeboom, J. J. F., Eslami Amirabadi, H., Nair, P., Sahlgren, C. M., & den Toonder, J. M. J. (2018) · Disease Models & Mechanisms · doi:10.1242/dmm.033100 · Cited by 122
Platform for High-Throughput Testing of the Effect of Soluble Compounds on 3D Cell Cultures
Deiss, F. T., Mazzeo, A. D., Hong, E., Ingber, D. E., Derda, R., & Whitesides, G. M. (2013) · Analytical Chemistry · doi:10.1021/ac400161j · Cited by 119
Microfluidics and cancer: are we there yet?
Zhang, Z., & Nagrath, S. (2013) · Biomedical Microdevices · doi:10.1007/s10544-012-9734-8 · Cited by 123
D’Arcangelo, E., Wu, N. C., Cadavid, J. L., & McGuigan, A. P. (2020) · British Journal of Cancer · doi:10.1038/s41416-019-0705-1 · Cited by 117
A Practical Method for Patterning Lumens through ECM Hydrogels via Viscous Finger Patterning
Bischel, L. L., Lee, S., & Beebe, D. J. (2012) · SLAS TECHNOLOGY · doi:10.1177/2211068211426694 · Cited by 114
Self-citationMicrofluidic model of ductal carcinoma in situ with 3D, organotypic structure
Bischel, L. L., Beebe, D. J., & Sung, K. E. (2015) · BMC Cancer · doi:10.1186/s12885-015-1007-5 · Cited by 110
Self-citationIn vitro 3d cultures to model the tumor microenvironment
Fontana, F., Marzagalli, M., Sommariva, M., Gagliano, N., & Limonta, P. (2021) · Cancers · doi:10.3390/cancers13122970 · Cited by 103
Lugo-Cintrón, K. M., Gong, M. M., Ayuso, J. M., Tomko, L. A., Beebe, D. J., Virumbrales-Muñoz, M., & Ponik, S. M. (2020) · Cancers · doi:10.3390/cancers12051173 · Cited by 103
Self-citationOsuala, K. O., Sameni, M., Shah, S., Aggarwal, N., Simonait, M. L., Franco, O. E., Hong, Y., Hayward, S. W., Behbod, F., Mattingly, R. R., et al. (2015) · BMC Cancer · doi:10.1186/s12885-015-1576-3 · Cited by 101
The emergence of 3D bioprinting in organ-on-chip systems
Fetah, K., Tebon, P. J., Goudie, M. J., Eichenbaum, J., Ren, L. M., de Barros, N. R., Nasiri, R., Ahadian, S., Ashammakhi, N. A., Dokmeci, M. R., et al. (2019) · Progress in Biomedical Engineering · doi:10.1088/2516-1091/ab23df · Cited by 106
Workshop meeting report Organs-on-Chips: human disease models
van de Stolpe, A., & den Toonder, J. M. J. (2013) · Lab on a Chip · doi:10.1039/c3lc50248a · Cited by 99
Cook, C. D., Hill, A. S., Guo, M. G., Stockdale, L., Papps, J. P., Isaacson, K., Lauffenburger, D. A., & Griffith, L. G. (2017) · Integrative Biology · doi:10.1039/c6ib00245e · Cited by 93
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
Photodynamic Control of Bioactivity in a Nanofiber Matrix
Sur, S., Matson, J. B., Webber, M. J., Newcomb, C. J., & Stupp, S. I. (2012) · ACS Nano · doi:10.1021/nn304101x · Cited by 91
Drifka, C. R., Loeffler, A. G., Mathewson, K., Mehta, G. S., Keikhosravi, A., Liu, Y., Lemancik, S., Ricke, W. A., Weber, S. M., Kao, W. J., et al. (2016) · Journal of Histochemistry & Cytochemistry · doi:10.1369/0022155416659249 · Cited by 96
Self-citationZheng, F., Xiao, Y., Liu, H., Fan, Y., & Dao, M. (2021) · Advanced Biology · doi:10.1002/adbi.202000024 · Cited by 96
Microfluidic co-culture system for cancer migratory analysis and anti-metastatic drugs screening
Mi, S., Du, Z., Xu, Y., Wu, Z., Qian, X., Zhang, M., & Sun, W. (2016) · Scientific Reports · doi:10.1038/srep35544 · Cited by 85
Micro- and nanoengineering for stem cell biology: the promise with a caution
Gupta, K., Kim, D., Beebe, D. J., & Levchenko, A. (2011) · Trends in biotechnology · doi:10.1016/j.tibtech.2011.03.006 · Cited by 82
Self-citationRodenhizer, D., Dean, T., D'Arcangelo, E., & McGuigan, A. P. (2018) · Advanced Healthcare Materials · doi:10.1002/adhm.201701174 · Cited by 80
Toward the broad adoption of 3D tumor models in the cancer drug pipeline
Cox, M. C., Reese, L. M., Bickford, L. R., & Verbridge, S. S. (2015) · ACS Biomaterials Science & Engineering · doi:10.1021/acsbiomaterials.5b00172 · Cited by 80
Navigating the Collagen Jungle: The Biomedical Potential of Fiber Organization in Cancer
Ouellette, J. N., Drifka, C. R., Pointer, K. B., Liu, Y., Lieberthal, T. J., Kao, W. J., Kuo, J. S., Loeffler, A. G., & Eliceiri, K. W. (2021) · Bioengineering · doi:10.3390/bioengineering8020017 · Cited by 82
Self-citationMicroscale screening systems for 3D cellular microenvironments: platforms, advances, and challenges
Montanez-Sauri, S. I., Beebe, D. J., & Sung, K. E. (2014) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-014-1738-5 · Cited by 81
Self-citationThree-dimensional perfused cell culture
Li, Z., & Cui, Z. (2013) · Biotechnology Advances · doi:10.1016/j.biotechadv.2013.10.006 · Cited by 84
Montanez-Sauri, S. I., Sung, K. E., Berthier, E., & Beebe, D. J. (2013) · Integrative Biology · doi:10.1039/c3ib20225a · Cited by 80
Self-citationSeo, B. R., DelNero, P. F., & Fischbach, C. (2013) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2013.11.011 · Cited by 75
The importance of being a lumen
Bischel, L. L., Sung, K. E., Jiménez‐Torres, J. A., Mader, B. R., Keely, P. J., & Beebe, D. J. (2014) · The FASEB Journal · doi:10.1096/fj.13-243733 · Cited by 75
Self-citationOrgan on Chip Technology to Model Cancer Growth and Metastasis
Imparato, G., Urciuolo, F., & Netti, P. A. (2022) · Bioengineering · doi:10.3390/bioengineering9010028 · Cited by 77
Mimicking Human Pathophysiology in Organ‐on‐Chip Devices
Yeşil-Çeliktaş, Ö., Hassan, S., Miri, A. K., Maharjan, S., Al‐kharboosh, R., Quiñones‐Hinojosa, A., & Zhang, Y. S. (2018) · Advanced Biosystems · doi:10.1002/adbi.201800109 · Cited by 74
In vitro models of the metastatic cascade: from local invasion to extravasation
Bersini, S., Jeon, J. S., Moretti, M., & Kamm, R. D. (2014) · Drug Discovery Today · doi:10.1016/j.drudis.2013.12.006 · Cited by 71
Probing Embryonic Stem Cell Autocrine and Paracrine Signaling Using Microfluidics
Joel Voldman, B., & Przybyla, L. (2012) · DSpace@MIT (Massachusetts Institute of Technology) · Cited by 71
Tumor Microenvironment on a Chip: The Progress and Future Perspective
Ahn, J., Sei, Y. J., Jeon, N. L., & Kim, Y. (2017) · Bioengineering · doi:10.3390/bioengineering4030064 · Cited by 71
Powering ex vivo tissue models in microfluidic systems
McLean, I. C., Schwerdtfeger, L., Tobet, S. A., & Henry, C. S. (2018) · Lab on a Chip · doi:10.1039/c8lc00241j · Cited by 72
Multicellular 3D Models to Study Tumour-Stroma Interactions
Colombo, E. M., & Cattaneo, M. G. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22041633 · Cited by 72
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
Recent Advances of Organ-on-a-Chip in Cancer Modeling Research
Liu, X., Su, Q., Zhang, X., Yang, W., Ning, J., Jia, K., Xin, J., Li, H., Yu, L., Liao, Y., et al. (2022) · Biosensors · doi:10.3390/bios12111045 · Cited by 71
Zheng, C., Zhao, L., Chen, G., Zhou, Y., Pang, Y., & Huang, Y. (2012) · Analytical Chemistry · doi:10.1021/ac2032029 · Cited by 67
Cancer-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
Drifka, C. R., Eliceiri, K. W., Weber, S. M., & Kao, W. J. (2013) · Lab on a Chip · doi:10.1039/c3lc50487e · Cited by 64
Self-citationMicrofluidics for research and applications in oncology
Chaudhuri, P. K., Warkiani, M. E., Jing, T., Kenry, K., & Lim, C. T. (2015) · The Analyst · doi:10.1039/c5an00382b · Cited by 63
Breaking the mold: 3D cell cultures reshaping the future of cancer research
Cordeiro, S. Z., Oliveira, B. B. P. P., Valente, R., Ferreira, D., Luz, A., Baptista, P. V., & Fernandes, A. R. (2024) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2024.1507388 · Cited by 70
Tissue-engineered human 3D model of bladder cancer for invasion study and drug discovery
Goulet, C. R., Bernard, G., Chabaud, S., Couture, A., Langlois, A., Neveu, B., Pouliot, F., & Bolduc, S. (2017) · Biomaterials · doi:10.1016/j.biomaterials.2017.08.041 · Cited by 63
Cancer-Associated Fibroblasts in Breast Cancer Treatment Response and Metastasis
Fernández‐Nogueira, P., Fuster, G., Gutiérrez-Uzquiza, Á., Gascón, P., Carbó, N., & Bragado, P. (2021) · Cancers · doi:10.3390/cancers13133146 · Cited by 59
Advanced diagnostic aids for oral cancer
Madhura, M. G., Rao, R. S., Patil, S., Fageeh, H. N., Alhazmi, A. S., & Awan, K. H. (2020) · Disease-a-Month · doi:10.1016/j.disamonth.2020.101034 · Cited by 60
Mazio, C., Casale, C., Imparato, G., Urciuolo, F., & Netti, P. A. (2018) · Acta Biomaterialia · doi:10.1016/j.actbio.2018.04.028 · Cited by 53
Epitope topography controls bioactivity in supramolecular nanofibers
Sur, S., Tantakitti, F., Matson, J. B., & Stupp, S. I. (2015) · Biomaterials Science · doi:10.1039/c4bm00326h · Cited by 54
Nelson, A., Machado, H. L., & Schwertfeger, K. L. (2018) · Journal of Mammary Gland Biology and Neoplasia · doi:10.1007/s10911-018-9409-z · Cited by 52
Metabolic Switching of Tumor Cells under Hypoxic Conditions in a Tumor-on-a-chip Model
Palacio-Castañeda, V., Kooijman, L. J., Venzac, B., Verdurmen, W. P. R., & Gac, S. L. (2020) · Micromachines · doi:10.3390/mi11040382 · Cited by 54
Cancer-associated fibroblasts as target and tool in cancer therapeutics and diagnostics
Vlieghere, E. D., Verset, L., Demetter, P., Bracke, M., & Wever, O. D. (2015) · Archiv für Pathologische Anatomie und Physiologie und für Klinische Medicin · doi:10.1007/s00428-015-1818-4 · Cited by 50
Studying cancer metastasis: Existing models, challenges and future perspectives
van Marion, D. M. S., Domańska, U., Timmer‐Bosscha, H., & Walenkamp, A. (2015) · Critical Reviews in Oncology/Hematology · doi:10.1016/j.critrevonc.2015.08.009 · Cited by 48
The bone marrow niche in support of breast cancer dormancy
Walker, N. D., Patel, J. S., Munoz, J. L., Hu, M. D., Guiro, K., Sinha, G., & Rameshwar, P. (2015) · Cancer Letters · doi:10.1016/j.canlet.2015.10.033 · Cited by 47
Kaur, H., Mao, S., Shah, S. K., Gorski, D. H., Krawetz, S. A., Sloane, B. F., & Mattingly, R. R. (2013) · Expert Review of Molecular Diagnostics · doi:10.1586/erm.13.4 · Cited by 49
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
Self-citationMacaraniag, C., Luan, Q., Zhou, J., & Papautsky, I. (2022) · APL Bioengineering · doi:10.1063/5.0093806 · Cited by 47
Kaur, P., Ward, B., Saha, B., Young, L. L., Groshen, S. G., Techy, G. B., Lu, Y., Atkinson, R., Taylor, C. R., Ingram, M., et al. (2011) · Journal of Histochemistry & Cytochemistry · doi:10.1369/0022155411423680 · Cited by 46
Biomimetic tumor microenvironment on a microfluidic platform
Ma, H., Xu, H. M., & Qin, J. (2013) · Biomicrofluidics · doi:10.1063/1.4774070 · Cited by 46
Metadata
- Authors
- Sung, K. E., Yang, N., Pehlke, C., Keely, P. J., Eliceiri, K. W., Friedl, A., & Beebe, D. J.
- Affiliations
- University of Wisconsin–Madison (US)
- United States Department of Veterans Affairs (US)
- Corresponding author
- Beebe, David J.
- Venue
- Integr. Biol.
- Publisher
- Oxford University Press (OUP)
- Published
- 2011
- Volume
- 3
- Issue
- 4
- Pages
- 439-450
- ISSN
- 1757-9694 (ISSN-L)
- 1757-9708
- PMC
- PMC3094750
- OpenAlex
- W2103232525
- Cited by
- 226
- References
- 32
- Citations by year
- 2026: 1 · 2025: 6 · 2024: 4 · 2023: 8 · 2022: 14 · 2021: 19 · 2020: 22 · 2019: 12 · 2018: 20 · 2017: 22 · 2016: 15 · 2015: 19 · 2014: 18 · 2013: 23 · 2012: 16
- FWCI
- 8.66
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Integrative Biology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health
- National Cancer Institute (R01CA107012, R01CA114462, R33CA137673, K25CA104162)
- U.S. National Library of Medicine (T15LM007359)
- Topics
- Physical Sciences › Engineering › Biomedical Engineering › 3D Printing in Biomedical Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular Mechanics and Interactions
- Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
- Keywords
- ductal carcinoma in situ, invasive ductal carcinoma, breast cancer progression, mammary epithelial cells, cell-cell contact, collagen remodeling, second harmonic generation microscopy, microchannel arrays, therapeutic target screening, tumor microenvironment
- MeSH terms
- Actins, Animals, Breast Neoplasms, Cell Line, Collagen, Drug Combinations, Female, Fibroblasts, Humans, Laminin, Mice, Nude, Neoplasm Invasiveness, Proteoglycans, Time Factors, Cadherins, Extracellular Matrix Proteins, Coculture Techniques, Fibrillar Collagens, Collagen Type I, Collagen Type IV, Microscopy, Fluorescence, Multiphoton, Carcinoma, Ductal, Cell Line, Tumor, Microfluidic Analytical Techniques, Cell Proliferation, Mice
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.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
