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Human 3D vascularized organotypic microfluidic assays to study breast cancer cell extravasation
Open accessAbstract
Significance: The cancer biology seed-and-soil paradigm recognizes the existence of organ-specific patterns of metastasization that drive the spread of selected primary tumors toward specific secondary loci. However, despite efforts to model the organotypic microenvironment, the organ specificity of cancer metastases needs to be elucidated. The relevance of this study lies in the generation of a human vascularized organ-specific microenvironment, which can be used to investigate and tune the extravasation process of metastatic tumor cells. Furthermore, beyond mimicking the pro- or antimetastatic signatures of different microenvironments, our microfluidic model provides insights into different properties of organ-specific endothelia. This study paves the way toward advanced in vitro models to screen for highly tailored organ-specific therapeutics and investigate key molecular pathways involved in organ-specific metastases.
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“Through this, it was shown that adenosine played an important role in promoting tumor cells extravasation.”
From Microfluidic modelling of the tumor microenvironment for anti-cancer drug development (2019) · cites this paper as [98]
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“By blocking A3 adenosine receptors, cancer cells were observed to have a reduced extravasation rate.”
From Microfluidic modelling of the tumor microenvironment for anti-cancer drug development (2019) · cites this paper as [98]
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“Endothelial cells displayed morphological features similar to in vivo conditions, contrasting to poorly aligned cells grown in 2D cultures or deprived of fl ow.”
From 3D In Vitro Model (R)evolution: Unveiling Tumor–Stroma Interactions (2021) · cites this paper as [78]
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“This micro fl uidic device not only promoted the perfusable culture of four different cells types but also proved to be an appropriate platform for monitoring cancer cell extravasation in real time.”
From 3D In Vitro Model (R)evolution: Unveiling Tumor–Stroma Interactions (2021) · cites this paper as [78]
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“The results indicated inhibitory role of adenosine on extravasation as blocking A3 adenosine receptors increased extravasation rates of breast cancer cells into the myoblast, mimicking microenvironments compared with untreated cells [57].”
From Tumor microenvironment complexity and therapeutic implications at a glance (2020) · cites this paper as [57]
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“Fortunately, with the development of biofabrication techniques, microfluidic and 3D bioprinting technologies have been employed to create more in vivo‐like perfusable 3D tumor models in the biomimetic matrix.[ 72 , 161 ]”
From 3D Biomimetic Models to Reconstitute Tumor Microenvironment In Vitro: Spheroids, Organoids, and Tumor‐on‐a‐Chip (2023) · cites this paper as [161]
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“CoC models can be applied to elucidate these effects, and researchers have developed vascularized CoC models to study extravasation to bone [74][75][76], brain [77,78], and other organs [79]”
From Cancer-on-chip models for metastasis: importance of the tumor microenvironment (2024) · cites this paper as [75]
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Citations
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
The pathogenesis of cancer metastasis: the ‘seed and soil’ hypothesis revisited
Fidler, I. J. (2003) · Nature Reviews Cancer · doi:10.1038/nrc1098 · Cited by 4,686
Dissemination and growth of cancer cells in metastatic sites
Chambers, A. F., Groom, A. C., & MacDonald, I. C. (2002) · Nature reviews. Cancer · doi:10.1038/nrc865 · Cited by 4,018
Tumor Metastasis: Molecular Insights and Evolving Paradigms
Valastyan, S., & Weinberg, R. A. (2011) · Cell · doi:10.1016/j.cell.2011.09.024 · Cited by 4,011
Cell Migration: A Physically Integrated Molecular Process
Lauffenburger, D. A., & Horwitz, A. F. (1996) · Cell · doi:10.1016/s0092-8674(00)81280-5 · Cited by 3,915
Metastasis: from dissemination to organ-specific colonization
Nguyen, D. X., Bos, P. D., & Massagué, J. (2009) · Nature reviews. Cancer · doi:10.1038/nrc2622 · Cited by 2,716
Molecular regulation of vessel maturation
Jain, R. K. (2003) · Nature Medicine · doi:10.1038/nm0603-685 · Cited by 2,594
Tumor Self-Seeding by Circulating Cancer Cells
Kim, M.-Y., Oskarsson, T., Acharyya, S., Nguyen, D. X., Zhang, X. H.-F., Norton, L., & Massagué, J. (2009) · Cell · doi:10.1016/j.cell.2009.11.025 · Cited by 1,335
Crossing the endothelial barrier during metastasis
Reymond, N., d'Água, B. B., & Ridley, A. J. (2013) · Nature Reviews Cancer · doi:10.1038/nrc3628 · Cited by 922
Three-dimensional microfluidic model for tumor cell intravasation and endothelial barrier function
Zervantonakis, I. K., Hughes-Alford, S. K., Charest, J. L., Condeelis, J. S., Gertler, F. B., & Kamm, R. D. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1210182109 · Cited by 872
Self-citation
Cited by
Sorted by citations
Tumor microenvironment complexity and therapeutic implications at a glance
Baghban, R., Roshangar, L., Jahanban-Esfahlan, R., Seidi, K., Ebrahimi-Kalan, A., Jaymand, M., Kolahian, S., Javaheri, T., & Zare, P. (2020) · Cell Communication and Signaling · doi:10.1186/s12964-020-0530-4 · Cited by 1,784
“The results indicated inhibitory role of adenosine on extravasation as blocking A3 adenosine receptors increased extravasation rates of breast cancer cells into the myoblast, mimicking microenvironments compared with untreated cells [57] .”
Organs-on-chips: into the next decade
Low, L. A., Mummery, C., Berridge, B. R., Austin, C. P., & Tagle, D. A. (2021) · Nature Reviews Drug Discovery · doi:10.1038/s41573-020-0079-3 · Cited by 1,029
Advances in organ-on-a-chip engineering
Zhang, B., Korolj, A., Lai, B. F. L., & Radisic, M. (2018) · Nature Reviews Materials · doi:10.1038/s41578-018-0034-7 · Cited by 1,017
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
Organs-on-a-Chip: A Fast Track for Engineered Human Tissues in Drug Development
Ronaldson-Bouchard, K., & Vunjak-Novakovic, G. (2018) · Cell Stem Cell · doi:10.1016/j.stem.2018.02.011 · Cited by 657
3D Cell Culture Systems: Tumor Application, Advantages, and Disadvantages
Habanjar, O., Diab‐Assaf, M., Caldefie‐Chezet, F., & Delort, L. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222212200 · Cited by 590
Organ-on-a-chip devices advance to market
Zhang, B., & Radisic, M. (2017) · Lab on a Chip · doi:10.1039/c6lc01554a · Cited by 437
3D In Vitro Model (R)evolution: Unveiling Tumor–Stroma Interactions
Rodrigues, J., Heinrich, M. A., Teixeira, L. M., & Prakash, J. (2021) · Trends in Cancer · doi:10.1016/j.trecan.2020.10.009 · Cited by 405
“In another study, a 3D microvascular network of endothelial cells was generated in bone- or muscle-mimicking microenvironments with osteo-differentiated cells or smooth muscle MSCs, respectively [78].”
BackgroundChen, M. B., Whisler, J. A., Fröse, J., Yu, C., Shin, Y., & Kamm, R. D. (2017) · Nature Protocols · doi:10.1038/nprot.2017.018 · Cited by 385
Self-citationTumor microenvironment: barrier or opportunity towards effective cancer therapy
Tiwari, A., Trivedi, R., & Lin, S. (2022) · Journal of Biomedical Science · doi:10.1186/s12929-022-00866-3 · Cited by 399
Organ-on-a chip systems: microengineering to biomimic living systems
Zheng, F., Fu, F., Cheng, Y., Wang, C., Zhao, Y., & Gu, Z. (2016) · Small · doi:10.1002/smll.201503208 · Cited by 338
A vascularized and perfused organ-on-a-chip platform for large-scale drug screening applications
Phan, D. T. T., Wang, X., Craver, B. M., Sobrino, A., Zhao, D., Chen, J. C., Lee, L. Y. N., George, S. C., Lee, A. P., & Hughes, C. C. W. (2017) · Lab on a Chip · doi:10.1039/c6lc01422d · Cited by 325
Engineering cancer microenvironments for in vitro 3-D tumor models
Asghar, W., El Assal, R., Shafiee, H., Pitteri, S., Paulmurugan, R., & Demirci, U. (2015) · Materials Today · doi:10.1016/j.mattod.2015.05.002 · Cited by 316
Investigation of human trophoblast invasion in vitro
Abbas, Y., Turco, M. Y., Burton, G. J., & Moffett, A. (2020) · Human Reproduction Update · doi:10.1093/humupd/dmaa017 · Cited by 331
Shirure, V. S., Bi, Y., Curtis, M. B., Lezia, A., Goedegebuure, M. M., Goedegebuure, S. P., Aft, R., Fields, R. C., & George, S. C. (2018) · Lab on a Chip · doi:10.1039/c8lc00596f · Cited by 316
Organ-on-a-chip platforms: a convergence of advanced materials, cells, and microscale technologies
Ahadian, S., Civitarese, R., Bannerman, D., Mohammadi, M. H., Lu, R., Wang, E., Davenport‐Huyer, L., Lai, B., Zhang, B., Zhao, Y., et al. (2018) · Advanced Healthcare Materials · doi:10.1002/adhm.201700506 · Cited by 315
Mouse models of metastasis: progress and prospects
Gómez-Cuadrado, L., Tracey, N., Ma, R., Qian, B., & Brunton, V. G. (2017) · Disease Models & Mechanisms · doi:10.1242/dmm.030403 · Cited by 316
Could 3D models of cancer enhance drug screening?
Brancato, V., Oliveira, J. M., Correlo, V. M., Reis, R. L., & Kundu, S. C. (2019) · Biomaterials · doi:10.1016/j.biomaterials.2019.119744 · Cited by 290
Three-dimensional in vitro culture models in oncology research
Jubelin, C., Muñoz-García, J., Griscom, L., Cochonneau, D., Ollivier, E., Heymann, M., Vallette, F. M., Oliver, L., & Heymann, D. (2022) · Cell & Bioscience · doi:10.1186/s13578-022-00887-3 · Cited by 314
3D Bioprinted in vitro metastatic models via reconstruction of tumor microenvironments
Meng, F., Meyer, C. M., Joung, D., Vallera, D. A., McAlpine, M. C., & Panoskaltsis‐Mortari, A. (2019) · Advanced Materials · doi:10.1002/adma.201806899 · Cited by 262
Integrating perfusable vascular networks with a three-dimensional tissue in a microfluidic device
Nashimoto, Y., Hayashi, T., Kunita, I., Nakamasu, A., Torisawa, Y.-S., Nakayama, M., Takigawa-Imamura, H., Kotera, H., Nishiyama, K., Miura, T., et al. (2017) · Integrative Biology · doi:10.1039/c7ib00024c · Cited by 266
Bioprinting the Cancer Microenvironment
Zhang, Y. S., Duchamp, M., Öklü, R., Ellisen, L. W., Langer, R., & Khademhosseini, A. (2016) · ACS Biomaterials Science & Engineering · doi:10.1021/acsbiomaterials.6b00246 · Cited by 254
Organs-on-a-chip models for biological research
Vunjak-Novakovic, G., Ronaldson-Bouchard, K., & Radisic, M. (2021) · Cell · doi:10.1016/j.cell.2021.08.005 · Cited by 248
“Breast cancers have similarly been modeled to show propensity for metastasis to bone (Jeon et al., 2015), a result commonly seen clinically but difficult to model in animal systems.”
BackgroundMicrofluidic modelling of the tumor microenvironment for anti-cancer drug development
Shang, M., Soon, R. H., Lim, C. T., Khoo, B. L., & Han, J. (2019) · Lab on a Chip · doi:10.1039/c8lc00970h · Cited by 227
Human bone perivascular niche-on-a-chip for studying metastatic colonization
Marturano-Kruik, A., Nava, M. M., Yeager, K. J., Chramiec, A. G., Hao, L. Y., Robinson, S. T., Guo, E. X., Raimondi, M. T., & Vunjak‐Novakovic, G. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1714282115 · Cited by 228
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
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
Tumour-on-a-chip: microfluidic models of tumour morphology, growth and microenvironment
Tsai, H.-F., Trubelja, A., Shen, A. Q., & Bao, G. (2017) · Journal of The Royal Society Interface · doi:10.1098/rsif.2017.0137 · Cited by 214
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
Breast Cancer: A Molecularly Heterogenous Disease Needing Subtype-Specific Treatments
Testa, U., Castelli, G., & Pelosi, E. (2020) · Medical Sciences · doi:10.3390/medsci8010018 · Cited by 238
Breast cancer models: Engineering the tumor microenvironment
Bahcecioglu, G., Basara, G., Ellis, B. W., Ren, X., & Zorlutuna, P. (2020) · Acta Biomaterialia · doi:10.1016/j.actbio.2020.02.006 · Cited by 213
Emerging organoid models: leaping forward in cancer research
Fan, H., Demirci, U., & Chen, P. (2019) · Journal of Hematology & Oncology · doi:10.1186/s13045-019-0832-4 · Cited by 199
Engineering Vascularized Organoid-on-a-Chip Models
Shirure, V. S., Hughes, C. C. W., & George, S. C. (2021) · Annual Review of Biomedical Engineering · doi:10.1146/annurev-bioeng-090120-094330 · Cited by 200
3D Printing of Organs-On-Chips
Yi, H., Lee, H., & Cho, D. (2017) · Bioengineering · doi:10.3390/bioengineering4010010 · Cited by 203
Trujillo-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
“[30,56,62,65-68,70-72,85,189-192] [22,23,29,32,43,50,5559,63,64,165,177,194] [21,27,28,47,64]”
Chin, L., Xia, Y., Discher, D. E., & Janmey, P. A. (2016) · Current Opinion in Chemical Engineering · doi:10.1016/j.coche.2016.01.011 · Cited by 181
Advances in Engineering Human Tissue Models
Moysidou, C., Barberio, C., & Owens, R. M. (2021) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2020.620962 · Cited by 193
Metastatic disease in head & neck oncology
Pisani, P., Airoldi, M., Allais, A., Valletti, P. A., Battista, M., Benazzo, M., Briatore, R., Cacciola, S., Cocuzza, S. G., Colombo, A., et al. (2020) · Acta Otorhinolaryngologica Italica · doi:10.14639/0392-100x-suppl.1-40-2020 · Cited by 197
Ayuso, J. M., Rehman, S., Virumbrales-Muñoz, M., McMinn, P. H., Geiger, P. G., Fitzgerald, C., Heaster, T. M., Skala, M. C., & Beebe, D. J. (2021) · Science Advances · doi:10.1126/sciadv.abc2331 · Cited by 174
A biomimetic pancreatic cancer on-chip reveals endothelial ablation via ALK7 signaling
Nguyen, D.-H. T., Lee, E., Alimperti, S., Norgard, R. J., Wong, A., Lee, J. J.-K., Eyckmans, J., Stanger, B. Z., & Chen, C. S. (2019) · Science Advances · doi:10.1126/sciadv.aav6789 · Cited by 172
Integrated gut/liver microphysiological systems elucidates inflammatory inter‐tissue crosstalk
Chen, W. L. K., Edington, C., Suter, E., Yu, J., Velazquez, J. J., Velazquez, J. G., Shockley, M., Large, E. M., Venkataramanan, R., Hughes, D. J., et al. (2017) · Biotechnology and Bioengineering · doi:10.1002/bit.26370 · Cited by 172
Engineering 3D Hydrogels for Personalized In Vitro Human Tissue Models
Liaw, C., Ji, S., & Güvendiren, M. (2018) · Advanced Healthcare Materials · doi:10.1002/adhm.201701165 · Cited by 171
Microfluidics Enabled Bottom-Up Engineering of 3D Vascularized Tumor for Drug Discovery
Agarwal, P., Wang, H., Sun, M., Xu, J., Zhao, S., Liu, Z., Gooch, K. J., Zhao, Y., Lu, X., & He, X. (2017) · ACS Nano · doi:10.1021/acsnano.7b00824 · Cited by 168
Cochrane, A., Albers, H. J., Passier, R. C., Mummery, C. L., van den Berg, A., Orlova, V. V., & van der Meer, A. D. (2018) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2018.06.007 · Cited by 173
IFlowPlate—A Customized 384‐Well Plate for the Culture of Perfusable Vascularized Colon Organoids
Rajasekar, S., Lin, D. S. Y., Abdul, L., Liu, A. W. K., Sotra, A., Zhang, F., & Zhang, B. (2020) · Advanced Materials · doi:10.1002/adma.202002974 · Cited by 167
Cardiovascular organ-on-a-chip platforms for drug discovery and development
Ribas, J., Sadeghi, H., Manbachi, A., Leijten, J., Brinegar, K., Zhang, Y. S., Ferreira, L., & Khademhosseini, A. (2016) · Applied In Vitro Toxicology · doi:10.1089/aivt.2016.0002 · Cited by 161
Hydrogel Network Dynamics Regulate Vascular Morphogenesis
Zhao, W., Schnellmann, R., Pruitt, H. C., & Gerecht, S. (2020) · Cell stem cell · doi:10.1016/j.stem.2020.08.005 · Cited by 166
The 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
Vasculature-On-A-Chip for In Vitro Disease Models
Kim, S., Kim, W., Lim, S., & Jeon, J. S. (2017) · Bioengineering · doi:10.3390/bioengineering4010008 · Cited by 168
Self-citationA review of microfluidic approaches for investigating cancer extravasation during metastasis
Ma, Y.-H. V., Middleton, K., You, L., & Sun, Y. (2018) · Microsystems & Nanoengineering · doi:10.1038/micronano.2017.104 · Cited by 154
3D Bioprinting of Breast Cancer Models for Drug Resistance Study
Wang, Y., Shi, W., Kuss, M., Mirza, S., Qi, D., Krasnoslobodtsev, A., Zeng, J., Band, H., Band, V., & Duan, B. (2018) · ACS Biomaterials Science & Engineering · doi:10.1021/acsbiomaterials.8b01277 · Cited by 157
In Vitro Microfluidic Models for Neurodegenerative Disorders
Osaki, T., Shin, Y., Sivathanu, V., Campisi, M., & Kamm, R. D. (2017) · Advanced Healthcare Materials · doi:10.1002/adhm.201700489 · Cited by 155
Self-citationCD47 Promotes Tumor Invasion and Metastasis in Non-small Cell Lung Cancer
Zhao, H., Wang, J., Kong, X., Li, E., Liu, Y., Du, X., Kang, Z., Tang, Y. C., Kuang, Y., Yang, Z., et al. (2016) · Scientific Reports · doi:10.1038/srep29719 · Cited by 152
Mechanical properties of human tumour tissues and their implications for cancer development
Massey, A. E., Stewart, J. M., Smith, C., Parvini, C. H., McCormick, M., Do, K., & Cartagena‐Rivera, A. X. (2024) · Nature Reviews Physics · doi:10.1038/s42254-024-00707-2 · Cited by 166
Microfluidic Organ/Body-on-a-Chip Devices at the Convergence of Biology and Microengineering
Perestrelo, A. R., Águas, A. C., Rainer, A., & Forte, G. (2015) · Sensors · doi:10.3390/s151229848 · Cited by 152
Biochemical analysis on microfluidic chips
Wu, J., He, Z., Chen, Q., & Lin, J. (2016) · TrAC Trends in Analytical Chemistry · doi:10.1016/j.trac.2016.03.013 · Cited by 155
Truong, D., Fiorelli, R., Barrientos, E. S., Melendez, E. L., Sanai, N., Mehta, S., & Nikkhah, M. (2019) · Biomaterials · doi:10.1016/j.biomaterials.2018.07.048 · Cited by 150
Microfluidic Tumor–Vascular Model to Study Breast Cancer Cell Invasion and Intravasation
Nagaraju, S., Truong, D., Mouneimne, G., & Nikkhah, M. (2018) · Advanced Healthcare Materials · doi:10.1002/adhm.201701257 · Cited by 147
Review: in vitro microvessel models
Bogorad, M. I., DeStefano, J., Karlsson, J., Wong, A. D., Gerecht, S., & Searson, P. C. (2015) · Lab on a Chip · doi:10.1039/c5lc00832h · Cited by 145
Bone remodelling in vitro: Where are we headed?
Kohli, N., Ho, S., Brown, S. J., Sawadkar, P., Sharma, V., Snow, M., & García‐Gareta, E. (2018) · Bone · doi:10.1016/j.bone.2018.01.015 · Cited by 157
Evaluating natural killer cell cytotoxicity against solid tumors using a microfluidic model
Ayuso, J. M., Truttschel, R., Gong, M. M., Humayun, M., Virumbrales-Munoz, M., Vitek, R., Felder, M., Gillies, S. D., Sondel, P., Wisinski, K. B., et al. (2019) · OncoImmunology · doi:10.1080/2162402x.2018.1553477 · Cited by 142
Vascularized microfluidic organ-chips for drug screening, disease models and tissue engineering
Osaki, T., Sivathanu, V., & Kamm, R. D. (2018) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2018.03.011 · Cited by 141
Self-citationBone-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
Fabrication of 3D Biomimetic Microfluidic Networks in Hydrogels
Heintz, K. A., Bregenzer, M. E., Mantle, J. L., Lee, K. H., West, J. L., & Slater, J. H. (2016) · Advanced Healthcare Materials · doi:10.1002/adhm.201600351 · Cited by 142
Designing Microgels for Cell Culture and Controlled Assembly of Tissue Microenvironments
Caldwell, A. S., Aguado, B. A., & Anseth, K. S. (2019) · Advanced Functional Materials · doi:10.1002/adfm.201907670 · Cited by 139
Álvarez, M. M., Aizenberg, J., Analoui, M., Andrews, A. M., Bisker, G., Boyden, E. S., Kamm, R. D., Karp, J. M., Mooney, D. J., Öklü, R., et al. (2017) · ACS Nano · doi:10.1021/acsnano.7b01493 · Cited by 137
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
Self-citationTumor organoid models in precision medicine and investigating cancer-stromal interactions
Xu, R., Zhou, X., Wang, S., & Trinkle, C. (2021) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2020.107668 · Cited by 134
Mimicking tumor microenvironment by 3D bioprinting: 3D cancer modeling
Shukla, P., Yeleswarapu, S., Heinrich, M. A., Prakash, J., & Pati, F. (2022) · Biofabrication · doi:10.1088/1758-5090/ac6d11 · Cited by 140
3D-printed fluidic networks as vasculature for engineered tissue
Kinstlinger, I. S., & Miller, J. S. (2016) · Lab on a Chip · doi:10.1039/c6lc00193a · Cited by 141
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
Lin, Z., Luo, G., Du, W., Kong, T., Liu, C., & Liu, Z. (2019) · Small · doi:10.1002/smll.201903899 · Cited by 134
Emerging trends in organ-on-a-chip systems for drug screening
Wang, Y., Gao, Y., Pan, Y., Zhou, D., Liu, Y., Yin, Y. B., Yang, J., Wang, Y., & Song, Y. (2023) · Acta Pharmaceutica Sinica B · doi:10.1016/j.apsb.2023.02.006 · Cited by 132
Endothelial Regulation of Drug Transport in a 3D Vascularized Tumor Model
Haase, K., Offeddu, G. S., Gillrie, M. R., & Kamm, R. D. (2020) · Advanced Functional Materials · doi:10.1002/adfm.202002444 · Cited by 126
Self-citationMetastasis of circulating tumor cells: Favorable soil or suitable biomechanics, or both?
Azevedo, A. S., Follain, G., Patthabhiraman, S., Harlepp, S., & Goetz, J. G. (2015) · Cell Adhesion & Migration · doi:10.1080/19336918.2015.1059563 · Cited by 132
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Lara, R. P., & Annabi, N. (2016) · Lab on a Chip · doi:10.1039/c6lc00718j · Cited by 130
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Piccolo, N. D., Shirure, V. S., Bi, Y., Goedegebuure, S. P., Gholami, S., Hughes, C. C. W., Fields, R. C., & George, S. C. (2021) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2021.05.008 · Cited by 134
Jackson, E., & Lu, H. (2016) · Integrative Biology · doi:10.1039/c6ib00039h · Cited by 132
Engineering the pre-metastatic niche
Aguado, B. A., Bushnell, G. G., Rao, S. S., Jeruss, J. S., & Shea, L. D. (2017) · Nature Biomedical Engineering · doi:10.1038/s41551-017-0077 · Cited by 131
Barata, D. B., van Blitterswijk, C., & Habibović, P. (2015) · Acta Biomaterialia · doi:10.1016/j.actbio.2015.09.009 · Cited by 128
Hydrogel microfabrication technology toward three dimensional tissue engineering
Yanagawa, F., Sugiura, S., & Kanamori, T. (2016) · Regenerative Therapy · doi:10.1016/j.reth.2016.02.007 · Cited by 126
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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
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Wan, L., Neumann, C. A., & LeDuc, P. R. (2020) · Lab on a Chip · doi:10.1039/c9lc00550a · Cited by 120
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Ahn, J., Yoon, M.-J., Hong, S.-H., Cha, H., Lee, D., Koo, H. S., Ko, J., Lee, J., Oh, S., Jeon, N. L., et al. (2021) · Human Reproduction · doi:10.1093/humrep/deab186 · Cited by 118
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Zhao, Q., Cui, H., Wang, Y., & Du, X. (2019) · Small · doi:10.1002/smll.201903798 · Cited by 118
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Xiao, Y., Kim, D., Dura, B., Zhang, K., Yan, R., Li, H., Han, E., Ip, J., Zou, P., Liu, J., et al. (2019) · Advanced Science · doi:10.1002/advs.201801531 · Cited by 115
Shiwarski, D. J., Hudson, A. R., Tashman, J. W., Bakırcı, E., Moss, S., Coffin, B. D., & Feinberg, A. W. (2025) · Science Advances · doi:10.1126/sciadv.adu5905 · Cited by 125
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Li, W., Zhou, Z., Zhou, X., Khoo, B. L., Gunawan, R., Chin, Y. R., Zhang, L., Yi, C., Guan, X., & Yang, M. (2023) · Advanced Healthcare Materials · doi:10.1002/adhm.202202609 · Cited by 119
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Modugno, F. D., Colosi, C., Trono, P., Antonacci, G., Ruocco, G., & Nisticò, P. (2019) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-019-1086-2 · Cited by 115
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Miller, C. P., Tsuchida, C., Zheng, Y., Himmelfarb, J., & Akilesh, S. (2018) · Neoplasia · doi:10.1016/j.neo.2018.02.011 · Cited by 105
Wang, X., Sun, Q., & Pei, J. (2018) · Micromachines · doi:10.3390/mi9100493 · Cited by 106
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Park, D., Lee, J., Chung, J. J., Jung, Y., & Kim, S. H. (2020) · Trends in Biotechnology · doi:10.1016/j.tibtech.2019.06.006 · Cited by 105
Lee, J. B., Wang, X., Faley, S. L., Baer, B. B., Balikov, D. A., Sung, H., & Bellan, L. M. (2016) · Advanced Healthcare Materials · doi:10.1002/adhm.201500792 · Cited by 110
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Ho, Y. T., Kamm, R. D., & Kah, J. C. Y. (2018) · Nanoscale · doi:10.1039/c8nr02393j · Cited by 102
Self-citationLai, B. F. L., Lu, R. X. Z., Huyer, L. D., Kakinoki, S., Yazbeck, J., Wang, E. Y., Wu, Q., Zhang, B., & Radisic, M. (2021) · Nature Protocols · doi:10.1038/s41596-020-00490-1 · Cited by 102
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Metadata
- Authors
- Jeon, J. S., Bersini, S., Gilardi, M., Dubini, G., Charest, J. L., Moretti, M., & Kamm, R. D.
- Affiliations
- Massachusetts Institute of Technology (US)
- IRCCS Ospedale Galeazzi - Sant'Ambrogio (IT)
- Politecnico di Milano (IT)
- Draper Laboratory (US)
- ORCID
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2014-12-18
- Volume
- 112
- Issue
- 1
- Pages
- 214-219
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC4291627
- OpenAlex
- W2081560083
- Semantic Scholar
- f475569e9cefbccc34378d56e185a60e479f18b8
- Cited by
- 723
- References
- 44
- Citations by year
- 2026: 28 · 2025: 44 · 2024: 53 · 2023: 71 · 2022: 79 · 2021: 85 · 2020: 83 · 2019: 71 · 2018: 77 · 2017: 59 · 2016: 52 · 2015: 21
- FWCI
- 22.85
- Type
- journal article
- Language
- en
- Update notices
- correction (2015-02-02)
- Open access
- bronze
- doi.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Virtual Community of Pathological Anatomy (University of Castilla La Mancha) (submittedVersion, other-oa)
- BOA (University of Milano-Bicocca) (submittedVersion)
- DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc)
- Funders
- HHS | NIH | National Cancer Institute (R33 CA174550-01, R21 CA140096)
- Topics
- Physical Sciences › Engineering › Biomedical Engineering › 3D Printing in Biomedical Research
- Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular Mechanics and Interactions
- Keywords
- breast cancer, tumor cell extravasation, organ-specific metastasis, microvascular permeability, A3 adenosine receptor, drug screening, personalized medicine
- MeSH terms
- Adenosine, Animals, Breast Neoplasms, Capillary Permeability, Extravasation of Diagnostic and Therapeutic Materials, Female, Humans, Stress, Mechanical, Shear Strength, Microfluidics, Cell Line, Tumor, Mice, Microvessels, Cellular Microenvironment, Human Umbilical Vein Endothelial Cells
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