Recapitulation of complex transport and action of drugs at the tumor microenvironment using tumor-microenvironment-on-chip
Open accessAbstract
Targeted delivery aims to selectively distribute drugs to targeted tumor tissues but not to healthy tissues. This can address many clinical challenges by maximizing the efficacy but minimizing the toxicity of anti-cancer drugs. However, a complex tumor microenvironment poses various barriers hindering the transport of drugs and drug delivery systems. New tumor models that allow for the systematic study of these complex environments are highly desired to provide reliable test beds to develop drug delivery systems for targeted delivery. Recently, research efforts have yielded new in vitro tumor models, the so called tumor-microenvironment-on-chip, that recapitulate certain characteristics of the tumor microenvironment. These new models show benefits over other conventional tumor models, and have the potential to accelerate drug discovery and enable precision medicine. However, further research is warranted to overcome their limitations and to properly interpret the data obtained from these models. In this article, key features of the in vivo tumor microenvironment that are relevant to drug transport processes for targeted delivery were discussed, and the current status and challenges for developing in vitro transport model systems were reviewed.
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Tumor stromal tissues act as a dynamic source and reservoir of cytokines and growth factors that influence tumor progression and pharmacological responses.
“In addition to their remarkable internal heterogeneity, the tumor stromal tissues (i.e., the tissues surrounding the tumor), act as a dynamic source (and reservoir) of various cytokines and growth factors that influence tumor progression and pharmacological responses [19].”
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 [19]
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Siegel, R., Naishadham, D., & Jemal, A. (2013) · CA A Cancer Journal for Clinicians · doi:10.3322/caac.21166 · Cited by 11,825 · see citing works
Siegel, R., Ma, J., Zou, Z., & Jemal, A. (2014) · CA: A Cancer Journal for Clinicians · doi:10.3322/caac.21208 · Cited by 11,499 · see citing works
Microenvironmental regulation of tumor progression and metastasis
Quail, D. F., & Joyce, J. A. (2013) · Nature Medicine · doi:10.1038/nm.3394 · Cited by 7,994 · see citing works
Matsumura, Y., & Maeda, H. (1986) · PubMed · Cited by 6,771 · see citing works
Normalization of Tumor Vasculature: An Emerging Concept in Antiangiogenic Therapy
Jain, R. K. (2005) · Science · doi:10.1126/science.1104819 · Cited by 5,527 · cited 1× · see citing works
“Recently, a strategy to normalize the tumor vasculature to achieve improved drug delivery throughout the tumor tissue has been proposed [54,55].”
Signet-Ring Cell Carcinoma of the Colon: A Case Report and Review of the Literature
Park, P. Y., Goldin, T. A., Chang, J. C. S., Markman, M. M., & Kundranda, M. N. (2015) · Case Reports in Oncology · doi:10.1159/000441772 · Cited by 5,273 · see citing works
Core Signaling Pathways in Human Pancreatic Cancers Revealed by Global Genomic Analyses
Jones, S., Zhang, X., Parsons, D. W., Lin, J. C.-H., Leary, R. J., Angenendt, P., Mankoo, P., Carter, H., Kamiyama, H., Jimeno, A., et al. (2008) · Science · doi:10.1126/science.1164368 · Cited by 3,969 · see citing works
Fang, J. Q., Nakamura, H., & Maeda, H. (2010) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2010.04.009 · Cited by 3,573 · see citing works
BIOCHEMISTRY OF MULTIDRUG RESISTANCE MEDIATED BY THE MULTIDRUG TRANSPORTER
Gottesman, M. M., & PASTAN, I. (1993) · Annual Review of Biochemistry · doi:10.1146/annurev.bi.62.070193.002125 · Cited by 3,515 · see citing works
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 · see citing works
Danhier, F., Féron, O., & Véronique Préat, A. (2010) · Journal of Controlled Release · doi:10.1016/j.jconrel.2010.08.027 · Cited by 2,827 · see citing works
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 · see citing works
Özdemir, B. C., Pentcheva-Hoang, T., Carstens, J. L., Zheng, X., Wu, C.-C., Simpson, T. R., Laklai, H., Sugimoto, H., Kahlert, C., Novitskiy, S. V., et al. (2014) · Cancer Cell · doi:10.1016/j.ccr.2014.04.005 · Cited by 2,681 · see citing works
Distant metastasis occurs late during the genetic evolution of pancreatic cancer
Yachida, S., Jones, S., Bozic, I., Antal, T., Leary, R., Fu, B., Kamiyama, M., Hruban, R. H., Eshleman, J. R., Nowak, M. A., et al. (2010) · Nature · doi:10.1038/nature09515 · Cited by 2,502 · see citing works
Regulation of transport pathways in tumor vessels: Role of tumor type and microenvironment
Hobbs, S. K., Monsky, W. L., Yuan, F., Roberts, W. G., Griffith, L., Torchilin, V. P., & Jain, R. K. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.8.4607 · Cited by 2,438 · see citing works
High Interstitial Fluid Pressure - an Obstacle in Cancer Therapy
Heldin, C.-H., Rubin, K., Pietras, K., & Östman, A. (2004) · Nature reviews. Cancer · doi:10.1038/nrc1456 · Cited by 2,222 · see citing works
Provenzano, P. P., Cuevas, C., Chang, A. E., Goel, V. K., Von Hoff, D. D., & Hingorani, S. R. (2012) · Cancer Cell · doi:10.1016/j.ccr.2012.01.007 · Cited by 2,195 · see citing works
Intra-tumour heterogeneity: a looking glass for cancer?
Marusyk, A., Almendro, V., & Polyák, K. (2012) · Nature reviews. Cancer · doi:10.1038/nrc3261 · Cited by 2,003 · see citing works
Targeted drug delivery to tumors: Myths, reality and possibility
Bae, Y. H., & Park, K. (2011) · Journal of Controlled Release · doi:10.1016/j.jconrel.2011.06.001 · Cited by 1,947 · see citing works
Self-citationModeling Tissue Morphogenesis and Cancer in 3D
Yamada, K. M., & Cukierman, E. (2007) · Cell · doi:10.1016/j.cell.2007.08.006 · Cited by 1,751 · see citing works
Spheroid-based drug screen: Considerations and practical approach
Friedrich, J., Seidel, C., Ebner, R., & Kunz-Schughart, L. A. (2009) · Nature Protocols · doi:10.1038/nprot.2008.226 · Cited by 1,742 · see citing works
Vascular permeability in a human tumor xenograft: molecular size dependence and cutoff size.
Yuan, F., Dellian, M., Fukumura, D., Leunig, M., Berk, D. A., Torchilin, V. P., & Jain, R. K. (1995) · PubMed · Cited by 1,706 · see citing works
Mediating Tumor Targeting Efficiency of Nanoparticles Through Design
Perrault, S. D., Walkey, C., Jennings, T. L., Fischer, H. C., & Chan, W. C. W. (2009) · Nano Letters · doi:10.1021/nl900031y · Cited by 1,516 · see citing works
Transport of molecules in the tumor interstitium: a review.
Jain, R. K. (1987) · PubMed · Cited by 1,357 · see citing works
The patterns and dynamics of genomic instability in metastatic pancreatic cancer
Campbell, P. J., Yachida, S., Mudie, L. J., Stephens, P. J., Pleasance, E. D., Stebbings, L. A., Morsberger, L. A., Latimer, C., McLaren, S., Lin, M.-L., et al. (2010) · Nature · doi:10.1038/nature09460 · Cited by 1,317 · see citing works
Role of extracellular matrix assembly in interstitial transport in solid tumors.
Netti, P. A., Berk, D. A., Swartz, M. A., Grodzinsky, A. J., & Jain, R. K. (2000) · PubMed · Cited by 1,165 · see citing works
Sherman, M. H., Yu, R. T., Engle, D. D., Ding, N., Atkins, A. R., Tiriac, H., Collisson, E. A., Connor, F., Van Dyke, T., Kozlov, S., et al. (2014) · Cell · doi:10.1016/j.cell.2014.08.007 · Cited by 1,158 · see citing works
Chauhan, V. P., Stylianopoulos, T., Martin, J. D., Popović, Z., Chen, O., Kamoun, W. S., Bawendi, M. G., Fukumura, D., & Jain, R. K. (2012) · Nature Nanotechnology · doi:10.1038/nnano.2012.45 · Cited by 1,101 · see citing works
Multistage nanoparticle delivery system for deep penetration into tumor tissue
Wong, C., Stylianopoulos, T., Cui, J., Martin, J. D., Chauhan, V. P., Jiang, W., Popović, Z., Jain, R. K., Bawendi, M. G., & Fukumura, D. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1018382108 · Cited by 1,067 · see citing works
Kenny, P. A., Lee, G. Y., Myers, C. A., Neve, R. M., Semeiks, J. R., Spellman, P. T., Lorenz, K., Lee, E. H., Barcellos‐Hoff, M. H., PETERSEN, O. W., et al. (2008) · eScholarship (California Digital Library) · Cited by 1,039 · see citing works
Dobrovolskaia, M. A., Aggarwal, P., Hall, J. B., & McNeil, S. E. (2008) · Molecular Pharmaceutics · doi:10.1021/mp800032f · Cited by 1,022 · see citing works
High-throughput 3D spheroid culture and drug testing using a 384 hanging drop array
Tung, Y.-C., Hsiao, A. Y., Allen, S. G., Torisawa, Y.-S., Ho, M., & Takayama, S. (2011) · The Analyst · doi:10.1039/c0an00609b · Cited by 969 · see citing works
Kelm, J. M., Timmins, N. E., Brown, C. J., Fussenegger, M., & Nielsen, L. K. (2003) · Biotechnology and Bioengineering · doi:10.1002/bit.10655 · Cited by 934 · see citing works
Dynamic interplay between the collagen scaffold and tumor evolution
Egeblad, M., Rasch, M. G., & Weaver, V. M. (2010) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2010.08.015 · Cited by 898 · see citing works
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 · see citing works
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 836 · see citing works
Protein Corona Fingerprinting Predicts the Cellular Interaction of Gold and Silver Nanoparticles
Walkey, C., Olsen, J. B., Song, F., Liu, R., Guo, H., Olsen, D. W. H., Cohen, Y., Emili, A., & Chan, W. C. W. (2014) · ACS Nano · doi:10.1021/nn406018q · Cited by 824 · see citing works
Engineering tumors with 3D scaffolds
Fischbach, C., Chen, R., Matsumoto, T., Schmelzle, T., Brugge, J. S., Polverini, P. J., & Mooney, D. J. (2007) · Nature Methods · doi:10.1038/nmeth1085 · Cited by 823 · see citing works
The journey of a drug-carrier in the body: An anatomo-physiological perspective
Bertrand, N., & Leroux, J. (2011) · Journal of Controlled Release · doi:10.1016/j.jconrel.2011.09.098 · Cited by 713 · see citing works
Maximizing mouse cancer models
Frese, K. K., & Tuveson, D. A. (2007) · Nature reviews. Cancer · doi:10.1038/nrc2192 · Cited by 711 · see citing works
Microfluidic technologies for accelerating the clinical translation of nanoparticles
Valencia, P. M., Farokhzad, O. C., Karnik, R., & Langer, R. (2012) · Nature Nanotechnology · doi:10.1038/nnano.2012.168 · Cited by 704 · see citing works
Feldmann, G., Dhara, S., Fendrich, V., Bedja, D., Beaty, R. M., Mullendore, M. E., Karikari, C. A., Alvarez, H., Iacobuzio–Donahue, C. A., Jimeno, A., et al. (2007) · Cancer Research · doi:10.1158/0008-5472.can-06-3281 · Cited by 685 · see citing works
The role of stroma in pancreatic cancer: Diagnostic and therapeutic implications
Erkan, M., Hausmann, S., Michalski, C. W., Fingerle, A. A., Dobritz, M., Kleeff, J., & Friess, H. (2012) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2012.115 · Cited by 662 · see citing works
Müller, M., Meijer, C., Zaman, G. J., Borst, P., Scheper, R. J., Mulder, N. H., de Vries, E. G., & Jansen, P. L. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.26.13033 · Cited by 617 · see citing works
Three-dimensional tissue culture models in cancer biology
Kim, J. B. (2005) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2005.05.002 · Cited by 613 · see citing works
Pluen, A., Boucher, Y., Ramanujan, S., McKee, T. D., Gohongi, T., di Tomaso, E., Brown, E. B., Izumi, Y., Campbell, R. B., Berk, D. A., et al. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.081626898 · Cited by 604 · see citing works
Tumor-stroma interactions in pancreatic ductal adenocarcinoma
Mahadevan, D., & Hoff, D. D. V. (2007) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-06-0686 · Cited by 602 · see citing works
Loessner, D., Stok, K. S., Lutolf, M. P., Hutmacher, D. W., Clements, J. A., & Rizzi, S. C. (2010) · Biomaterials · doi:10.1016/j.biomaterials.2010.07.064 · Cited by 602 · see citing works
KRAS, Hedgehog, Wnt and the twisted developmental biology of pancreatic ductal adenocarcinoma
Morris, J. P., Wang, S. C., & Hebrok, M. (2010) · Nature reviews. Cancer · doi:10.1038/nrc2899 · Cited by 567 · see citing works
Diffusion and Convection in Collagen Gels: Implications for Transport in the Tumor Interstitium
Ramanujan, S., Pluen, A., McKee, T. D., Brown, E. B., Boucher, Y., & Jain, R. K. (2002) · Biophysical Journal · doi:10.1016/s0006-3495(02)73933-7 · Cited by 554 · see citing works
Facing the Truth about Nanotechnology in Drug Delivery
Park, K. (2013) · ACS Nano · doi:10.1021/nn404501g · Cited by 545 · see citing works
Self-citationLymphatic and interstitial flow in the tumour microenvironment: linking mechanobiology with immunity
Swartz, M. A., & Lund, A. W. (2012) · Nature Reviews Cancer · doi:10.1038/nrc3186 · Cited by 544 · see citing works
Litman, T., Brangi, M., Hudson, E., Fetsch, P. A., Abati, A. D., Ross, D. D., Miyake, K., Resau, J. H., & Bates, S. E. (2000) · Journal of Cell Science · doi:10.1242/jcs.113.11.2011 · Cited by 538 · see citing works
Multifunctional Nanoparticles for Drug Delivery and Molecular Imaging
Bao, G., Mitragotri, S., & Tong, S. (2013) · Annual Review of Biomedical Engineering · doi:10.1146/annurev-bioeng-071812-152409 · Cited by 537 · see citing works
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 · see citing works
Interstitial flow influences direction of tumor cell migration through competing mechanisms
Polacheck, W. J., Charest, J. L., & Kamm, R. D. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1103581108 · Cited by 509 · see citing works
Photoswitchable Nanoparticles for Triggered Tissue Penetration and Drug Delivery
Tong, R., Hemmati, H. D., Langer, R., & Kohane, D. S. (2012) · Journal of the American Chemical Society · doi:10.1021/ja211888a · Cited by 478 · see citing works
Structural basis of gene regulation by the tetracycline inducible Tet repressor-operator system.
Saenger, W., Hinrichs, W., Orth, P., Schnappinger, D., & Hillen, W. (2000) · Nature Structural Biology · doi:10.1038/73324 · Cited by 462 · see citing works
Analysis on the current status of targeted drug delivery to tumors
Kwon, I. K., Lee, S. C., Han, B., & Park, K. (2012) · Journal of Controlled Release · doi:10.1016/j.jconrel.2012.07.010 · Cited by 404 · see citing works
Self-citationEngineering microscale cellular niches for three-dimensional multicellular co-cultures
Huang, C. P., Lu, J., Seon, H., Lee, A. P., Flanagan, L. A., Kim, H.-Y., Putnam, A. J., & Jeon, N. L. (2009) · Lab on a Chip · doi:10.1039/b818401a · Cited by 384 · see citing works
Biological applications of microfluidic gradient devices
Kim, S., Kim, H. J., & Jeon, N. L. (2010) · Integrative Biology · doi:10.1039/c0ib00055h · Cited by 366 · cited 1× · see citing works
“In these models, cancer cells or spheroids were cultured within polymeric matrices to mimic cell-matrix interactions in vivo, allowing for the generation of spatial gradients of growth factors and pH [100, 128, 131-135].”
(1999) · PubMed · Cited by 348 · see citing works
Robey, R. W., Medina-Pérez, W. Y., Nishiyama, K., Lahusen, T. J., Miyake, K., Litman, T., Senderowicz, A. M., Ross, D. D., & Bates, S. E. (2001) · PubMed · Cited by 341 · see citing works
Weigelt, B., Lo, A. T., Park, C. C., Gray, J. W., & Bissell, M. J. (2009) · Breast Cancer Research and Treatment · doi:10.1007/s10549-009-0502-2 · Cited by 336 · see citing works
Allikmets, R. (1996) · Human Molecular Genetics · doi:10.1093/hmg/5.10.1649 · Cited by 334 · see citing works
Tumour-on-a-chip provides an optical window into nanoparticle tissue transport
Albanese, A., Lam, A. K., Sykes, E. A., Rocheleau, J. V., & Chan, W. C. W. (2013) · Nature Communications · doi:10.1038/ncomms3718 · Cited by 330 · see citing works
Hyaluronan, fluid pressure, and stromal resistance in pancreas cancer
Provenzano, P. P., & Hingorani, S. R. (2013) · British Journal of Cancer · doi:10.1038/bjc.2012.569 · Cited by 323 · see citing works
Microfluidic system for formation of PC-3 prostate cancer co-culture spheroids
Hsiao, A. Y., Torisawa, Y.-S., Tung, Y.-C., Sud, S., Taichman, R. S., Pienta, K. J., & Takayama, S. (2009) · Biomaterials · doi:10.1016/j.biomaterials.2009.02.047 · Cited by 323 · see citing works
Nanomaterials for Cancer Therapy and Imaging
Bae, K. H., Chung, H. J., & Park, T. G. (2011) · Molecules and Cells · doi:10.1007/s10059-011-0051-5 · Cited by 312 · see citing works
Reversal of resistance by GF120918 in cell lines expressing the ABC half-transporter, MXR
de Bruin, M., Miyake, K., Litman, T., Robey, R. W., & Bates, S. E. (1999) · Cancer Letters · doi:10.1016/s0304-3835(99)00182-2 · Cited by 298 · see citing works
Can cancer be reversed by engineering the tumor microenvironment?
Ingber, D. E. (2008) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2008.03.016 · Cited by 294 · see citing works
Mechetner, E. B., Kyshtoobayeva, A. S., Zonis, S., Kim, H. J., Stroup, R., Garcia, R., Parker, R. J., & Fruehauf, J. P. (1998) · PubMed · Cited by 291 · see citing works
Unraveling the microenvironmental influences on the normal mammary gland and breast cancer
Weigelt, B., & Bissell, M. J. (2008) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2008.03.013 · Cited by 274 · see citing works
Pancreatic cancer–associated stroma production
Korc, M. (2007) · The American Journal of Surgery · doi:10.1016/j.amjsurg.2007.05.004 · Cited by 268 · see citing works
Self-citationTubeless microfluidic angiogenesis assay with three-dimensional endothelial-lined microvessels
Bischel, L. L., Young, E. W. K., Mader, B. R., & Beebe, D. J. (2012) · Biomaterials · doi:10.1016/j.biomaterials.2012.11.005 · Cited by 266 · see citing works
Netti, P. A., Baxter, L. T., Boucher, Y., Skalak, R., & Jain, R. K. (1995) · PubMed · Cited by 265 · see citing works
Multicellular spheroids as an in vitro tumor model
Hamilton, G. (1998) · Cancer Letters · doi:10.1016/s0304-3835(98)00198-0 · Cited by 259 · see citing works
Grantab, R., Sivananthan, S., & Tannock, I. F. (2006) · Cancer Research · doi:10.1158/0008-5472.can-05-3077 · Cited by 254 · see citing works
(1992) · PubMed · Cited by 252 · see citing works
Computer-Controlled Microcirculatory Support System for Endothelial Cell Culture and Shearing
Song, J. W., Gu, W., Futai, N., Warner, K. A., Nor, J. E., & Takayama, S. (2005) · Analytical Chemistry · doi:10.1021/ac050131o · Cited by 249 · see citing works
Genetically Engineered Models Have Advantages over Xenografts for Preclinical Studies
Becher, O. J., & Holland, E. C. (2006) · Cancer Research · doi:10.1158/0008-5472.can-05-3827 · Cited by 244 · see citing works
Kanapathipillai, M., Brock, A., & Ingber, D. E. (2014) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2014.05.005 · Cited by 234 · see citing works
Acinar Cells Contribute to the Molecular Heterogeneity of Pancreatic Intraepithelial Neoplasia
Zhu, L., Shi, G., Schmidt, C. M., Hruban, R. H., & Konieczny, S. F. (2007) · American Journal Of Pathology · doi:10.2353/ajpath.2007.061176 · Cited by 213 · see citing works
Self-citationLipids as a Target for Drugs Modulating Multidrug Resistance of Cancer Cells
Hendrich, A. B., & Michalak, K. (2003) · Current Drug Targets · doi:10.2174/1389450033347172 · Cited by 206 · see citing works
Coherent angular motion in the establishment of multicellular architecture of glandular tissues
Tanner, K., Mori, H., Mroue, R. M., Bruni‐Cardoso, A., & Bissell, M. J. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1119578109 · Cited by 204 · see citing works
Enhancement of fluid filtration across tumor vessels: Implication for delivery of macromolecules
Netti, P. A., Hamberg, L. M., Babich, J. W., Kierstead, D., Graham, W. A., Hunter, G. J. S., Wolf, G. L., Fischman, A. J., Boucher, Y., & Jain, R. K. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.6.3137 · Cited by 203 · see citing works
Tumor models for efficacy determination
Teicher, B. A. (2006) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-06-0391 · Cited by 194 · see citing works
Pancreatic Cancer Stroma: Friend or Foe?
Gore, J., & Korc, M. (2014) · Cancer Cell · doi:10.1016/j.ccr.2014.05.026 · Cited by 189 · see citing works
Self-citationCheng, J.-Z., Sharma, R., Yang, Y., Singhal, S. S., Sharma, A., Saini, M. K., Singh, S. V., Zimniak, P., Awasthi, S., & Awasthi, Y. C. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m106838200 · Cited by 185 · see citing works
An agarose-based microfluidic platform with a gradient buffer for 3D chemotaxis studies
Haessler, U., Kalinin, Y. V., Swartz, M. A., & Wu, M. (2009) · Biomedical Microdevices · doi:10.1007/s10544-009-9299-3 · Cited by 180 · see citing works
“Targeting” nanoparticles: The constraints of physical laws and physical barriers
Florence, A. T. (2012) · Journal of Controlled Release · doi:10.1016/j.jconrel.2012.03.022 · Cited by 179 · see citing works
Two-photon fluorescence correlation microscopy reveals the two-phase nature of transport in tumors
Alexandrakis, G., Brown, E. B., Tong, R. T., McKee, T. D., Campbell, R. B., Boucher, Y., & Jain, R. K. (2004) · Nature Medicine · doi:10.1038/nm981 · Cited by 178 · see citing works
Fibroblast alignment under interstitial fluid flow using a novel 3-D tissue culture model
Ng, C. P., & Swartz, M. A. (2003) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.01008.2002 · Cited by 175 · see citing works
Feng, D., Nagy, J. A., Pyne, K., Hammel, I., Dvorak, H. F., & Dvořàk, A. M. (1999) · Microcirculation · doi:10.1111/j.1549-8719.1999.tb00085.x · Cited by 175 · see citing works
Shi, G., Zhu, L., Sun, Y., Bettencourt, R., Damsz, B., Hruban, R. H., & Konieczny, S. F. (2009) · Gastroenterology · doi:10.1053/j.gastro.2008.12.066 · Cited by 168 · see citing works
Self-citationSimulation of complex transport of nanoparticles around a tumor using tumor-microenvironment-on-chip
Kwak, B., Ozcelikkale, A., Shin, C. S., Park, K., & Han, B. (2014) · Journal of Controlled Release · doi:10.1016/j.jconrel.2014.08.027 · Cited by 165 · see citing works
Self-citationMonsky, W. L., Carreira, C. M., Tsuzuki, Y., Gohongi, T., Fukumura, D., & Jain, R. K. (2002) · PubMed · Cited by 161 · see citing works
Multidrug Resistance/P-Glycoprotein and Breast Cancer: Review and Meta-Analysis
Clarke, R. C., Leonessa, F., & Trock, B. J. (2005) · Seminars in Oncology · doi:10.1053/j.seminoncol.2005.09.009 · Cited by 159 · see citing works
Tumor Models for Efficacy Determination
Teicher, B. A. (2008) · AACR Education book · doi:10.1158/aacr.edb-mct-06-0391 · Cited by 155 · see citing works
Higashi, Y., Kanekura, T., & Kanzaki, T. (2000) · International Journal of Cancer · doi:10.1002/(sici)1097-0215(20000601)86:5 · Cited by 155 · see citing works
Funamoto, K., Zervantonakis, I. K., Liu, Y., Ochs, C. J., Kim, C., & Kamm, R. D. (2012) · Lab on a Chip · doi:10.1039/c2lc40306d · Cited by 151 · see citing works
Sinicrope, F. A., Dudeja, P. K., Bissonnette, B. M., Safa, A. R., & Brasitus, T. A. (1992) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)73996-9 · Cited by 142 · see citing works
Biomechanical regulation of cell orientation and fate
Lopez, J. I., Mouw, J. K., & Weaver, V. M. (2008) · Oncogene · doi:10.1038/onc.2008.348 · Cited by 141 · see citing works
Role of tumor vascular architecture in drug delivery
Narang, A. S., & Varia, S. A. (2011) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2011.04.002 · Cited by 141 · see citing works
Shin, C. S., Kwak, B., Han, B., & Park, K. (2013) · Molecular Pharmaceutics · doi:10.1021/mp300595a · Cited by 135 · see citing works
Self-citationTransvascular drug delivery in solid tumors
Fan, Y. (1998) · Seminars in Radiation Oncology · doi:10.1016/s1053-4296(98)80042-8 · Cited by 132 · see citing works
Fournier, M. V., Martin, K. J., Kenny, P. A., Xhaja, K., Bosch, I., Yaswen, P., & Bissell, M. J. (2006) · Cancer Research · doi:10.1158/0008-5472.can-06-0515 · Cited by 129 · see citing works
Davies, C. D. L., Berk, D. A., Pluen, A., & Jain, R. K. (2002) · British Journal of Cancer · doi:10.1038/sj.bjc.6600270 · Cited by 121 · see citing works
Walsh, C. L., Babin, B. M., Kasinskas, R. W., Foster, J. A., McGarry, M. J., & Forbes, N. S. (2008) · Lab on a Chip · doi:10.1039/b810571e · Cited by 121 · see citing works
The molecular and cellular heterogeneity of pancreatic ductal adenocarcinoma
Samuel, N., & Hudson, T. J. (2011) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2011.215 · Cited by 119 · see citing works
Lowering of tumor interstitial fluid pressure specifically augments efficacy of chemotherapy
Salnikov, A. V., Iversen, V. V., Koisti, M. J., Sundberg, C., Johansson, L. O. M., Stuhr, L. E. B., Sjöquist, M., Ahlström, H. K., Reed, R. K., & Rubin, K. (2003) · The FASEB Journal · doi:10.1096/fj.02-1201fje · Cited by 116 · see citing works
Stromal reengineering to treat pancreas cancer
Stromnes, I. M., DelGiorno, K. E., Greenberg, P. D., & Hingorani, S. R. (2014) · Carcinogenesis · doi:10.1093/carcin/bgu115 · Cited by 116 · see citing works
Influence of stress on extracellular matrix and integrin biology
Jean, C., Gravelle, P., Fournié, J., & Laurent, G. (2011) · Oncogene · doi:10.1038/onc.2011.27 · Cited by 110 · see citing works
Feng, D., Nagy, J. A., Pyne, K., Hammel, I., Dvorak, H. F., & Dvořàk, A. M. (1999) · Microcirculation · doi:10.1080/713773925 · Cited by 107 · see citing works
Rapid Generation of In Vitro Multicellular Spheroids for the Study of Monoclonal Antibody Therapy
Phung, Y., Barbone, D., Broaddus, V. C., & Ho, M. (2011) · Journal of Cancer · doi:10.7150/jca.2.507 · Cited by 99 · see citing works
Tumor Engineering: The Other Face of Tissue Engineering
Ghajar, C. M., & Bissell, M. J. (2010) · Tissue Engineering Part A · doi:10.1089/ten.tea.2010.0135 · Cited by 96 · see citing works
Increased AP-1 activity in drug resistant human breast cancer MCF-7 cells
Daschner, P. J., Ciolino, H. P., Plouzek, C. A., & Yeh, G. C. (1999) · Breast Cancer Research and Treatment · doi:10.1023/a:1006138803392 · Cited by 94 · see citing works
MRP and MDR1 gene expression in primary breast carcinomas.
Filipits, M., Suchomel, R. W., Dekan, G., Haider, K., Valdimarsson, G., Depisch, D., & Pirker, R. (1996) · PubMed · Cited by 94 · see citing works
The tumor microenvironment: focus on myeloma
Dalton, W. J. (2003) · Cancer Treatment Reviews · doi:10.1016/s0305-7372(03)00077-x · Cited by 90 · see citing works
Callaghan, R., Stafford, A. R., & Epand, R. M. (1993) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/0167-4889(93)90217-d · Cited by 85 · see citing works
Vredenburg, M., Ojima, I., Veith, J. M., Pera, P. J., Kee, K., Cabral, F., Sharma, A. B., Kanter, P. M., Greco, W. R., & Bernacki, R. J. (2001) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/93.16.1234 · Cited by 82 · see citing works
Damia, G. L. M., & D’Incalci, M. (2009) · European Journal of Cancer · doi:10.1016/j.ejca.2009.08.008 · Cited by 81 · see citing works
Chekhun, V. F., Kulik, G. I., Yurchenko, O. V., Tryndyak, V., Todor, I. N., Luniv, L. S., Tregubova, N. A., Pryzimirska, T. V., Montgomery, B. A., Rusetska, N., et al. (2005) · Cancer Letters · doi:10.1016/j.canlet.2005.01.038 · Cited by 81 · see citing works
Jin, J., Wang, F., Wei, H., & Liu, G.-T. (2004) · Cancer Chemotherapy and Pharmacology · doi:10.1007/s00280-004-0868-0 · Cited by 80 · see citing works
Challenges in pre-clinical testing of anti-cancer drugs in cell culture and in animal models
HogenEsch, H., & Nikitin, A. Y. (2012) · Journal of Controlled Release · doi:10.1016/j.jconrel.2012.02.031 · Cited by 79 · see citing works
Wosikowski, K., Regis, J. T., Robey, R. W., Alvarez, M. G., Buters, J., Gudas, J. M., & Bates, S. E. (1995) · PubMed · Cited by 71 · see citing works
Naito, M., Tsuge, H., Kuroko, C., Koyama, T., Tomida, A., Tatsuta, T., Heike, Y., & TSURUO, T. (1993) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/85.4.311 · Cited by 67 · see citing works
MOLECULAR GENETIC ALTERATIONS IN DUCTAL PANCREATIC ADENOCARCINOMAS
Kern, S. E. (2000) · Medical Clinics of North America · doi:10.1016/s0025-7125(05)70251-0 · Cited by 64 · see citing works
Peptide transport by the multidrug resistance protein MRP1.
de Jong, M. C., Slootstra, J. W., Scheffer, G. L., Schroeijers, A. B., Puijk, W. C., Dinkelberg, R., Kool, M., Broxterman, H. J., Meloen, R. H., & Scheper, R. J. (2001) · PubMed · Cited by 61 · see citing works
Reversal of multidrug resistance of tumor cells.
Szabó, D., Keyzer, H., Kaiser, H. E., & Molnar, J. A. (2000) · PubMed · Cited by 60 · see citing works
Shen, K., Luk, S. O., Hicks, D. F., Elman, J. S., Bohr, S., Iwamoto, Y., Murray, R. M., Peña, K. C., Wang, F., Şeker, E., et al. (2014) · Nature Communications · doi:10.1038/ncomms6662 · Cited by 56 · see citing works
Özçelikkale, A., Ghosh, S., & Han, B. (2013) · Molecular Pharmaceutics · doi:10.1021/mp3005947 · Cited by 55 · see citing works
Self-citationBansal, R., Post, E., Proost, J. H., de Jager-Krikken, A., Poelstra, K., & Prakash, J. (2011) · Journal of Controlled Release · doi:10.1016/j.jconrel.2011.05.027 · Cited by 55 · see citing works
Aszalós, A., Thompson, K., Jj, Y., & Dd, R. (1999) · PubMed · Cited by 49 · see citing works
Signaling Pathways in Pancreatic Cancer
Preis, M., & Korc, M. (2011) · Critical Reviews in Eukaryotic Gene Expression · doi:10.1615/critreveukargeneexpr.v21.i2.20 · Cited by 47 · see citing works
Self-citationChambers, S. K., Hait, W. N., Kacinski, B. M., Keyes, S. R., & Handschumacher, R. E. (1989) · PubMed · Cited by 47 · see citing works
Yang, L., Cho, C., Yan, X., Henthorn, T. K., Lillehei, K. O., Cobb, W. N., & Ng, K. (2001) · Pharmaceutical Research · doi:10.1023/a:1013025625156 · Cited by 46 · see citing works
Gore, J., Craven, K. E., Wilson, J. L., Coté, G. A., Cheng, M., Nguyen, H. V., Cramer, H. M., Sherman, S., & Korc, M. (2015) · Oncotarget · doi:10.18632/oncotarget.3233 · Cited by 45 · see citing works
Self-citationChoudhury, D., Mo, X., Iliescu, C., Tan, L., Tong, W. H., & Yu, H. (2011) · Biomicrofluidics · doi:10.1063/1.3593407 · Cited by 45 · see citing works
Simulated Microgravity Culture System for a 3-D Carcinoma Tissue Model
Nakamura, K., Kuga, H., Morisaki, T., Baba, E., Sato, N., Mizumoto, K., Sueishi, K., Tanaka, M., & Katano, M. (2002) · BioTechniques · doi:10.2144/02335rr02 · Cited by 33 · see citing works
Hait, W. N., & Yang, J. (2005) · Seminars in Oncology · doi:10.1053/j.seminoncol.2005.09.011 · Cited by 31 · see citing works
Ferreira, M. U., Gyémánt, N., Madureira, A., Tanaka, M., Koós, K., Didžiapetris, R., & Molnar, J. A. (2005) · PubMed · Cited by 31 · see citing works
Ford, J. M., Yang, J., & Hait, W. N. (1991) · PubMed · Cited by 30 · see citing works
Guldberg, P., Kirkin, A. F., Grønbæk, K., Straten, P. T., Ahrenkiel, V., & Zeuthen, J. (1997) · International Journal of Cancer · doi:10.1002/(sici)1097-0215(19970904)72:5 · Cited by 30 · see citing works
Tijerina, M., Fowers, K. D., Kopečková, P., & Kopec̆ek, J. (2000) · Biomaterials · doi:10.1016/s0142-9612(00)00161-7 · Cited by 29 · see citing works
Breuzard, G., Piot, O., Angiboust, J., Manfait, M., Candeil, L., Rio, M. D., & Millot, J. M. (2005) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2005.01.098 · Cited by 27 · see citing works
Characteristics of P388/VMDRC.04, a simple, sensitive model for studying P-glycoprotein antagonists.
Yang, J., Goldenberg, S., Gottesman, M. M., & Hait, W. N. (1994) · PubMed · Cited by 26 · see citing works
Overcoming MDR by Ultrasound-Induced Hyperthermia and P-Glycoprotein Modulation
Yang, L., Lillehei, K. O., Cobb, W. N., Christians, U., & Ng, K. (2001) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.2001.5938 · Cited by 21 · see citing works
Jin, B., Ko, E., Namkung, W., & Verkman, A. S. (2013) · Lab on a Chip · doi:10.1039/c3lc50821h · Cited by 16 · see citing works
Mano, Y., Suzuki, H., Terasaki, T., Iwahashi, T., Ono, K., Naito, M., Tsuruo, T., & Sugiyama, Y. (1997) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(24)37000-4 · Cited by 7 · see citing works
Engineering of tumor microenvironments
Hutmacher, D. W., & Cukierman, E. (2014) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2014.11.001 · Cited by 6 · see citing works
Complex Transport Around Tumor: Need for Realistic In Vitro Tumor Transport Model
Han, B. (2013) · Springer eBooks · doi:10.1007/978-1-4614-7876-8_25 · Cited by 2 · see citing works
Self-citation
Flagged first, then by citations
6 of the 158 references couldn’t be matched to a known paper.
Research works printed but not linked: 4
- [48]Monsky W Yuan F Fukumura D Torchilin V Jain RK Topical superfusion of vascular endothelial growth factor increases tumor vessel endothelial pore size Proceedings of the American Association for Cancer Research Annual Meeting 1997 38 52
- [59]Rubin K Sjoquist M Gustafsson A-M Isaksson B Salvessen G Reed RK Lowering of tumoral interstitial fluid pressure by prostaglandin E1 is paralleled by an increased uptake of Cr-EDTA Int. J. Cancer 2000 86 636 643 10797284
- [64]Stein U Walther W Lemm M Naundorf H Fichtner I Development and characterization of novel human multidrug resistant mammary carcinoma lines in vitro and in vivo Int. J. Cancer 1997 72 885 891 9311609
- [146]Noe-Kim V Ozcelikkale A Han B An in vitro microfluidic tumor model to mimic ductal carninoma in situ, Proceedings of the 2015 Summer Biomechanics Bioengineering and BIotransport Conference 2015 SB3C2015 673
Cited by
Sorted by citations
Targeting Tumor Microenvironment for Cancer Therapy
Roma-Rodrigues, C., Mendes, R., Baptista, P. V., & Fernandes, A. R. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20040840 · Cited by 1,187 · see citing works
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 · see citing works
Nanomedicine: An effective tool in cancer therapy
Aftab, S., Shah, A., Nadhman, A., Kurbanoğlu, S., Özkan, S. A., Dionysiou, D. D., Shukla, S. S., & Aminabhavi, T. M. (2018) · International Journal of Pharmaceutics · doi:10.1016/j.ijpharm.2018.02.007 · Cited by 209 · see citing works
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 · see citing works
“Modified from Han et al., 2016 [19].”
BackgroundCardoso, B. D., Castanheira, E. M. S., Lanceros-Méndez, S., & Cardoso, V. F. (2023) · Advanced Healthcare Materials · doi:10.1002/adhm.202202936 · Cited by 168 · see citing works
Ex Vivo Tumor Culture Systems for Functional Drug Testing and Therapy Response Prediction
Meijer, T. G., Naipal, K. A. T., Jager, A., & van Gent, D. C. (2017) · Future Science OA · doi:10.4155/fsoa-2017-0003 · Cited by 163 · see citing works
Drug screening in 3D in vitro tumor models: overcoming current pitfalls of efficacy read‐outs
Santo, V. E., Rebelo, S. P., Estrada, M. F., Alves, P. M., Boghaert, E. R., & Brito, C. (2016) · Biotechnology Journal · doi:10.1002/biot.201600505 · Cited by 103 · see citing works
Wang, Y., Luan, Z., Zhao, C., Bai, C., & Yang, K. (2019) · European Journal of Pharmaceutical Sciences · doi:10.1016/j.ejps.2019.105136 · Cited by 95 · see citing works
In vitromicrofluidic models of tumor microenvironment to screen transport of drugs and nanoparticles
Özçelikkale, A., Moon, H., Linnes, M. P., & Han, B. (2017) · Wiley Interdisciplinary Reviews Nanomedicine and Nanobiotechnology · doi:10.1002/wnan.1460 · Cited by 88 · see citing works
Self-citationPuls, T. J., Tan, X., Whittington, C. F., & Voytik‐Harbin, S. L. (2017) · PLoS ONE · doi:10.1371/journal.pone.0188870 · Cited by 73 · see citing works
Tumor-on-a-chip platform to interrogate the role of macrophages in tumor progression
Bi, Y., Shirure, V. S., Liu, R., Cunningham, C., Ding, L., Meacham, J. M., Goedegebuure, S. P., George, S. C., & Fields, R. C. (2020) · Integrative Biology · doi:10.1093/intbio/zyaa017 · Cited by 71 · see citing works
3D Immunocompetent Organ‐on‐a‐Chip Models
Maharjan, S., Cecen, B., & Zhang, Y. S. (2020) · Small Methods · doi:10.1002/smtd.202000235 · Cited by 62 · see citing works
Lipid-Nucleic Acid Complexes: Physicochemical Aspects and Prospects for Cancer Treatment
Gaspar, R., Coelho, F., & Silva, B. F. B. (2020) · Molecules · doi:10.3390/molecules25215006 · Cited by 57 · see citing works
Tumor-microenvironment-on-a-chip: the construction and application
Xu, H., Wen, J., Yang, J., Zhou, S., Li, Y., Xu, K., Li, W., & Li, S. (2024) · Cell Communication and Signaling · doi:10.1186/s12964-024-01884-4 · Cited by 54 · see citing works
Shin, K., Klosterhoff, B. S., & Han, B. (2016) · Molecular Pharmaceutics · doi:10.1021/acs.molpharmaceut.6b00131 · Cited by 53 · see citing works
Self-citationDynamic Microenvironment Induces Phenotypic Plasticity of Esophageal Cancer Cells Under Flow
Calibasi Kocal, G., Güven, S., Foygel, K., Goldman, A., Chen, P., Sengupta, S., Paulmurugan, R., Baskin, Y., & Demirci, U. (2016) · Scientific Reports · doi:10.1038/srep38221 · Cited by 52 · see citing works
Fluid flow to mimic organ function in 3D in vitro models
Juste-Lanas, Y., Hervás-Raluy, S., García‐Aznar, J. M., & González‐Loyola, A. (2023) · APL Bioengineering · doi:10.1063/5.0146000 · Cited by 50 · see citing works
Mimicking Tumors: Toward More Predictive In Vitro Models for Peptide- and Protein-Conjugated Drugs
van den Brand, D., Massuger, L. F. A. G., Brock, R. E., & Verdurmen, W. P. R. (2017) · Bioconjugate Chemistry · doi:10.1021/acs.bioconjchem.6b00699 · Cited by 48 · see citing works
Micro-engineering and nano-engineering approaches to investigate tumour ecosystems
Kim, M., Panagiotakopoulou, M., Chen, C., Ruiz, S. B., Ganesh, K., Tammela, T., & Heller, D. A. (2023) · Nature reviews. Cancer · doi:10.1038/s41568-023-00593-3 · Cited by 49 · see citing works
Plou, J., Molina-Martínez, B., García‐Astrain, C., Langer, J., Garcı́a, I., Ercilla, A., Perumal, G., Carracedo, A., & Liz‐Marzán, L. M. (2021) · Nano Letters · doi:10.1021/acs.nanolett.1c03070 · Cited by 43 · see citing works
Evaluating Nanoparticles in Preclinical Research Using Microfluidic Systems
Zhu, D., Long, Q., Xu, Y., & Xing, J. (2019) · Micromachines · doi:10.3390/mi10060414 · Cited by 41 · see citing works
Current and Emerging 3D Models to Study Breast Cancer
Roberts, S., Peyman, S. A., & Speirs, V. (2019) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-20301-6_22 · Cited by 30 · see citing works
An engineered pancreatic cancer model with intra-tumoral heterogeneity of driver mutations
Moon, H., Özçelikkale, A., Yang, Y., Elzey, B. D., Konieczny, S. F., & Han, B. (2020) · Lab on a Chip · doi:10.1039/d0lc00707b · Cited by 27 · see citing works
Self-citationBioprinting and its Use in Tumor-On-A-Chip Technology for Cancer Drug Screening: A Review
Fang, L., Liu, Y., Qiu, J., & Wan, W. (2022) · International Journal of Bioprinting · doi:10.18063/ijb.v8i4.603 · Cited by 26 · see citing works
Hydrogels as a New Platform to Recapitulate the Tumor Microenvironment
Ermis, M., Çalamak, S., Calibasi‐Kocal, G., Güven, S., Durmus, N. G., Rizvi, I., Hasan, T. G., Hasırcı, N., Hasırcı, V., & Demirci, U. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-813339-2.00015-3 · Cited by 24 · see citing works
Advances in Computational Fluid Mechanics in Cellular Flow Manipulation: A Review
Arabghahestani, M., Poozesh, S., & Akafuah, N. K. (2019) · Applied Sciences · doi:10.3390/app9194041 · Cited by 21 · see citing works
Zhou, L., Liu, L., Chang, M. A., Ma, C., Chen, W., & Chen, P. (2023) · Biosensors and Bioelectronics · doi:10.1016/j.bios.2023.115064 · Cited by 20 · see citing works
Engineering Heterogeneous Tumor Models for Biomedical Applications
Wu, Z., Huang, D., Wang, J., Zhao, Y., Sun, W., & Shen, X. (2023) · Advanced Science · doi:10.1002/advs.202304160 · Cited by 19 · see citing works
Engineering of biomaterials for tumor modeling
Choi, S. R., Yang, Y., Huang, K., Kong, H., Flick, M. J., & Han, B. (2020) · Materials Today Advances · doi:10.1016/j.mtadv.2020.100117 · Cited by 19 · see citing works
Self-citationMicrophysiological systems for human aging research
Park, S., Laskow, T. C., Chen, J., Guha, P., Dawn, B., & Kim, D. (2024) · Aging Cell · doi:10.1111/acel.14070 · Cited by 20 · see citing works
Clay, N. E., Shin, K., Özçelikkale, A., Lee, M. K., Rich, M. H., Kim, D. H., Han, B., & Kong, H. (2016) · ACS Biomaterials Science & Engineering · doi:10.1021/acsbiomaterials.6b00379 · Cited by 17 · see citing works
Self-citationLiang, T.-L., Li, R., Mai, C.-T., Guan, X., Li, J., Wang, X., Ma, L.-R., Zhang, F., Wang, J., He, F., et al. (2021) · Phytomedicine · doi:10.1016/j.phymed.2021.153831 · Cited by 14 · see citing works
Microfluidic-enabled self-organized tumor model for in vitro cytotoxicity assessment of doxorubicin
Yang, Y., Liu, S., Chen, C., Huang, H., Tao, L., Qian, Z., & Li, W. (2020) · Biomedical Microdevices · doi:10.1007/s10544-020-00523-2 · Cited by 15 · see citing works
Lee, G., Kim, S. J., & Park, J. (2024) · Advanced Healthcare Materials · doi:10.1002/adhm.202303716 · Cited by 14 · see citing works
Advances in Microfluidic Bioprinting for Multi-Material Multi-Cellular Tissue Constructs
Chand, R., Kamei, K., & Vijayavenkataraman, S. (2025) · Cell Therapy & Engineering Connect · doi:10.69709/cellengc.2024.111335 · Cited by 14 · see citing works
Complex Effects of Tumor Microenvironment on the Tumor Disposition of carrier-mediated Agents
Lucas, A. T., Price, L., Schorzman, A. N., & Zamboni, W. C. (2017) · Nanomedicine · doi:10.2217/nnm-2017-0101 · Cited by 14 · see citing works
Taurine and proline promote lung tumour growth by co-regulating Azgp1/mTOR signalling pathway
Liang, T.-L., Chen, Y., Zhou, N.-J., Shu, X., Mi, J., Ma, G.-Y., Xiao, Y., Yang, X., Huang, C., Li, J., et al. (2025) · npj Precision Oncology · doi:10.1038/s41698-025-00872-2 · Cited by 8 · see citing works
Nanoparticles and Microfluidic Devices in Cancer Research
Maia, F. R., Reis, R. L., & Oliveira, J. M. (2020) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-36588-2_10 · Cited by 8 · see citing works
Engineered tumor models for cancer biology and treatment
Moon, H., & Han, B. (2020) · Elsevier eBooks · doi:10.1016/b978-0-08-102983-1.00015-6 · Cited by 7 · see citing works
Self-citationBreast tumor-on-chip: from the tumor microenvironment to medical applications
Liu, Y., Liu, R., Liu, H., Lyu, T., Chen, K., Jin, K., & Tian, Y. (2023) · The Analyst · doi:10.1039/d3an01295f · Cited by 6 · see citing works
DCDA: CircRNA–Disease Association Prediction with Feed-Forward Neural Network and Deep Autoencoder
Turgut, H., Turanlı, B., & Boz, B. (2023) · Interdisciplinary Sciences Computational Life Sciences · doi:10.1007/s12539-023-00590-y · Cited by 6 · see citing works
A Systems Approach to Biomechanics, Mechanobiology, and Biotransport
Peirce, S. M., Sander, E. A., Fisher, M. B., Deymier, A. C., LaDisa, J. F., O’Connell, G. D., Corr, D. T., Han, B., Singh, A. K., Wilson, S. E., et al. (2024) · Journal of Biomechanical Engineering · doi:10.1115/1.4064547 · Cited by 6 · see citing works
Self-citationChoi, S. R., Mellican, S., Roberts, T. J., Kang, S., Elzey, B. D., Kong, H., Davis, C. S., Fishel, M. L., Flick, M. J., Wolberg, A. S., et al. (2026) · Acta Biomaterialia · doi:10.1016/j.actbio.2026.03.023 · Cited by 4 · see citing works
Self-citationLi, Y., Yang, T., Liu, S., Chen, C., Qian, Z., & Yang, Y. (2024) · Journal of Biophotonics · doi:10.1002/jbio.202300552 · Cited by 4 · see citing works
Asenjo‐Sanz, I., Del-Corte, M., Pinacho‐Olaciregui, J., González‐Burgos, M., González, E., Verde‐Sesto, E., Arbe, A., Colmenero, J., & Pomposo, J. A. (2019) · Med One · doi:10.20900/mo.20190013 · Cited by 4 · see citing works
Investigation of tumour environments through advancements in microtechnology and nanotechnology
Liu, Z., Fan, Y. L., Cui, M., Wang, X., & Zhao, P. (2024) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2024.117230 · Cited by 3 · see citing works
Alatawi, H., Nair, H. H., Raza, A., Vélez, E. D., Sharma, A. K., & Narayan, S. (2026) · Cancers · doi:10.3390/cancers18071166 · Cited by 2 · see citing works
Kang, S. J., Yoon, M. S., Lee, J. M., Jo, M. J., Jin, C. E., & Shin, D. H. (2026) · Advanced Science · doi:10.1002/advs.77137 · Cited by 2 · see citing works
Zhang, W., Jiang, T., Zhang, H., Fang, W., Li, X., & Xie, K. (2025) · Cellular Oncology · doi:10.1007/s13402-025-01084-3 · Cited by 3 · see citing works
Taurine and proline promote lung tumour growth by co-regulating Azgp1/mTOR signalling pathwayPreprint
Pan, H., Li, R.-Z., Liang, T., Mi, J., Ma, G.-Y., Xiao, Y., Yang, X., Huang, C., Li, J., Xie, Y., et al. (2024) · Research Square · doi:10.21203/rs.3.rs-4563639/v1
Saikia, T., Khanam, A., Ahmed, N., Bharali, A., Kalita, T., Rajak, P., Sahu, B. P., & Patowary, L. (2024) · Current Cancer Therapy Reviews · doi:10.2174/0115733947341257241018150125
Importance of microfluidics in cancer modeling
Suryavanshi, P., Dharwad, P., & Bodas, D. (2024) · Elsevier eBooks · doi:10.1016/b978-0-323-95533-1.00010-2
How are pancreatic tumors innervated?
Nguyen, T. T. H. (2017) · doi:10.70675/cddec815z4e10z4727z99cez3311438335a2
- Authors
- Han, B., Qu, C., Park, K., Konieczny, S. F., & Korc, M.
- Affiliations
- Purdue University West Lafayette (US)
- Indiana University Indianapolis (US)
- Corresponding author
- Han, Bumsoo
- Venue
- Cancer Letters
- Publisher
- Elsevier BV
- Published
- 2016-09
- Volume
- 380
- Issue
- 1
- Pages
- 319-329
- ISSN
- 0304-3835 (ISSN-L)
- PMC
- PMC4902790
- OpenAlex
- W2193304129
- Cited by
- 53
- References
- 158
- Citations by year
- 2026: 3 · 2025: 3 · 2024: 9 · 2023: 7 · 2022: 1 · 2021: 3 · 2020: 8 · 2019: 7 · 2018: 2 · 2017: 6 · 2016: 4
- FWCI
- 0.31
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Cancer Letters (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- IUScholarWorks (Indiana University) (submittedVersion)
- Purdue University Indianapolis (Indiana University) (submittedVersion)
- Funders
- NIH (HHSN261201400021C, CA129287, CA124586, CA075059, UL1 TR000006)
- Walther Cancer Foundation
- Purdue University
- Topics
- Physical Sciences › Engineering › Biomedical Engineering › 3D Printing in Biomedical Research
- Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
- Physical Sciences › Materials Science › Biomaterials › Nanoparticle-Based Drug Delivery
- Keywords
- tumor microenvironment, drug transport, targeted drug delivery, in vitro tumor model, drug delivery systems, anticancer agents, precision medicine, drug discovery
- MeSH terms
- Animals, Antineoplastic Agents, Biological Transport, Drug Carriers, Humans, Micromanipulation, Pancreatic Neoplasms, Drug Delivery Systems, Drug Resistance, Neoplasm, Carcinoma, Pancreatic Ductal, Microchip Analytical Procedures, Microfluidic Analytical Techniques, Cell Proliferation, Drug Discovery, Lab-On-A-Chip Devices, Molecular Targeted Therapy, Tumor Microenvironment
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