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Created: 09 Sep 2015

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Volume 5, August 2016

Newsletter

3D at Purdue

3D in Focus

3D in Publications

3D in Meetings

3D at Purdue

Multi-cellular, Multi-niche 3D Culture to Mimic the Brain Tumor Microenvironment

Glioblastoma (GBM), the most common adult primary brain tumor, has a mean life expectancy of about 15 months even with aggressive surgery, radiation and chemotherapy. Both drug resistance and a highly invasive phenotype contribute to the lethality of this cancer. Typically, by the time a neurosurgeon has an opportunity to intervene, cancer cells have already migrated throughout most of the brain. Like many cancer cells, GBM develops a dynamic relationship with the cell microenvironment to support tumor growth, migration and drug resistance. GBM cells find productive paths of migration along blood vessels and white matter tracts, and neighboring support cells, including normal astrocytes and pericytes, may support the survival and migration.

In order to tease out the role of the remodeled extracellular matrix and cell-cell interactions in GBM, we created 3D multicellular and multiniche cell culture models. A tunable oligomeric collagen I (Geniphys) forms the base of the system to control the mechanical properties using a chemically well-defined, but natural material. We find that GBM migration is most productive when the matrix is tuned to match the storage modulus range of the normal brain. Hyaluronan (HA) is integrated with the collagen to mimic the chemical content of the brain, which is HA rich. Basement membrane coated microfibers are embedded in the culture to structurally mimic blood vessels. We observe that GBM cells alter their migration mode from a mesenchymal migration phenotype into a highly productive, collective migration when they encounter a pseudovessel. Finally, human normal astrocytes and/or endothelial cells are also included as a coculture with the GBM cells in the matrix. As predicted but never before shown, we see that astrocytes further enhance the migration of the GBM cells in 3D. Both cell types alter the response to drugs, with different effects depending on the background characteristics of the starting tumor, which can vary widely from patient to patient.

In the end, we hope to build a 3D tissue model of GBM that can better predict therapy outcomes and facilitate the design of multipronged strategies to finally beat glioblastoma in the clinic.

Jenna Rickus, PhD

Professor, Agriculture and Biological Engineering, Biomedical Engineering

Herrera-Perez M. Voytik-Harbin SL, Rickus JL. “Extracellular Matrix Properties Regulate the Migratory Response of Glioblastoma Stem Cells in Three-Dimensional Culture.” Tissue Eng Part A. 2015 Oct;21(19-20):2572-82. http://www.ncbi.nlm.nih.gov/pubmed/26161688

Funded with support from the Purdue Center for Cancer Research and the IUPUI Center for the Cure of Glioblastoma.

3D in Focus

3D cell cultures should provide conditions for cells to differentiate into physiologically relevant tissue structures. Therefore, it is thought that 3D cell culture systems offer a better alternative for drug screening than conventional 2D culture methods. Improved understanding and characterization of 3D cell culture models are essential for further application in drug screening/discovery studies. One of the critical elements in 3D cell culture is the extracellular matrix since it greatly impacts the biological characteristic of cells in the culture system. This matter is addressed in the following article by Edmondson et al., which we will discuss in today’s newsletter. For those who attended, or plan to attend, future workshops on basics of 3D cell culture with gels, notably to induce tumor formation, this article is an example of how the type of matrix strongly influences cells in culture, and it highlights the importance of testing matrices for best mimicry of in vivo situations.

Edmondson R, Adcock AF, Yang L (2016) “Influence of Matrices on 3D-Cultured Prostate Cancer Cells' Drug Response and Expression of Drug-Action Associated Proteins.” PLoS ONE 11(6): e0158116.

In the study reported here, human prostate cancer LNCaP and DU145 cells were cultured in two biologically-derived matrices, Matrigel and Cultrex BME, and one synthetic matrix, the Alvetex scaffold. Both Matrigel and Cultrex BME are from Engelbreth-Holm-Swarm (EHS) sarcoma and rich in basement membrane type of extracellular matrix proteins including laminin, collagen IV, as well as growth factors such as epidermal growth factor and insulin-like growth factor. It seems that the main difference in this study for the choice of these two matrices was the protein concentration that was 8 – 12 mg/ml for Matrigel and 15 to 17 mg/ml for Cultrex BME. Alvetex is a synthetic, highly porous polystyrene scaffold. Note that EHS-derived gels provide natural extracellular matrix molecules to which cells react; with the polystyrene scaffold, the cells need to be able to synthesize and deposit the matrix molecules that they need for their survival and thrive, which is often the case with cancer cells.

DU145 and LNCaP cells in 3D culture proliferated at a slower rate than cells placed in 2D (standard) cultures. When comparing the effect of each matrix, DU145 cells proliferated at the highest rate in Alvedex, followed by Matrigel and Cultrex BME. Whereas, for LNCaP cells, the decreasing order for impact on proliferation was Matrigel, Alvedex and Cultrex BME. Moreover, DU145 cells formed round-shaped spheroids in both Matrigel and Cultrex BME, but failed to form spheroid structures in Alvetex. Whereas, LNCaP cells formed mass-type spheroids in all three types of matrices.

The responses of tumor cells to anticancer drugs docetaxel and rapamycin in 3D culture were investigated. As shown in many other publications with different cell models and drugs, DU145 and LNCaP cells cultured in all three types of matrices were more resistant to docetaxel than those cultured in 2D. DU145 cells in Alvetex showed the highest resistance to docetaxel among the three types of matrices, while LNCaP cells showed similar response in all matrices. DU145 cells cultured in Matrigel and Cultrex BME were more sensitive to rapamycin that those cultured in Alvetex and in 2D (the latter two conditions triggered similar response to the drug). Unlike DU145 cells, LNCaP cells cultured in Matrigel and Cultrex BME were more resistant to rapamycin than those in Alvetex and 2D culture (the latter two conditions triggered similar response to the drug).

The authors speculated that the expressions of b-III tubulin and EGFR correlated with the response of DU145 cells to docetaxel and rapamycin, respectively. The expression of b-III tubulin followed a decreasing trend for cells cultured in Alvetex, Matrigel, BME, and 2D culture. Decreasing EGFR expression was observed in the following order, Alvetex, 2D culture, Matrigel, and BME.

Our conclusions:

Although this is a simple study and no suggestion regarding the role of the specific matrices in the biological response of cells can be proposed, the data from this study indicate that the type of matrix (even if in theory similar, as shown for Matrigel and Cultrex BME) will influence many cell features, such as morphology, proliferation, drug sensitivity, as well as gene expression. Furthermore, the impact of matrices is also cell line related.

There has been a lot of interest recently in applying 3D culture model in drug screening studies. The cells in 3D culture are cultured in a variety of conditions, as suggested by the present study, known to influence cellular characteristics and behavior. Therefore, further characterization and standardization of the 3D culture models will be critical for drug screening assays. There is a lot of work ahead of us.

3D in Publications

Complete List -- 3D culture related articles on PubMed (last 2 months)

Reviews

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Organ/Tissue/Cell

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3D in Publications

Complete List

Abbott, R. D., Wang, R. Y., Reagan, M. R., Chen, Y., Borowsky, F. E., Zieba, A., Marra, K. G., Rubin, J. P., Ghobrial, I. M., and Kaplan, D. L. (2016). The Use of Silk as a Scaffold for Mature, Sustainable Unilocular Adipose 3D Tissue Engineered Systems. Adv Healthc Mater 5, 1667-1677.

Aguilar, A., Pertuy, F., Eckly, A., Strassel, C., Collin, D., Gachet, C., Lanza, F., and Leon, C. (2016). Importance of environmental stiffness for megakaryocyte differentiation and proplatelet formation. Blood.

Anthony, G., and Lee, J. A. (2016). An Optimized Small Tissue Handling System for Immunohistochemistry and In Situ Hybridization. PLoS One 11, e0159991.

Appert-Collin, A., Bennasroune, A., Jeannesson, P., Terryn, C., Fuhrmann, G., Morjani, H., and Dedieu, S. (2016). Role of LRP-1 in cancer cell migration in 3-dimensional collagen matrix. Cell Adh Migr, 0.

Arjmand, F., Khanmohammadi, M., Arasteh, S., Mohammadzadeh, A., Kazemnejad, S., and Akhondi, M. M. (2016). Extended Culture of Encapsulated Human Blastocysts in Alginate Hydrogel Containing Decidualized Endometrial Stromal Cells in the Presence of Melatonin. Mol Biotechnol.

Arrigoni, C., Bongio, M., Talo, G., Bersini, S., Enomoto, J., Fukuda, J., and Moretti, M. (2016). Rational Design of Prevascularized Large 3D Tissue Constructs Using Computational Simulations and Biofabrication of Geometrically Controlled Microvessels. Adv Healthc Mater 5, 1617-1626.

Arya, A. D., Hallur, P. M., Karkisaval, A. G., Gudipati, A., Rajendiran, S., Dhavale, V., Ramachandran, B., Jayaprakash, A., Gundiah, N., and Chaubey, A. (2016). Gelatin Methacrylate Hydrogels as Biomimetic Three-Dimensional Matrixes for Modeling Breast Cancer Invasion and Chemoresponse in Vitro. ACS Appl Mater Interfaces.

Atsumi, S., Nosaka, C., Adachi, H., Kimura, T., Kobayashi, Y., Takada, H., Watanabe, T., Ohba, S., Inoue, H., Kawada, M., et al. (2016). New anti-cancer chemicals Ertredin and its derivatives, regulate oxidative phosphorylation and glycolysis and suppress sphere formation in vitro and tumor growth in EGFRvIII-transformed cells. BMC Cancer 16, 496.

Baek, N., Seo, O. W., Lee, J., Hulme, J., and An, S. S. (2016). Real-time monitoring of cisplatin cytotoxicity on three-dimensional spheroid tumor cells. Drug Des Devel Ther 10, 2155-2165.

Bao, J., Wu, Q., Wang, Y., Li, Y., Li, L., Chen, F., Wu, X., Xie, M., and Bu, H. (2016). Enhanced hepatic differentiation of rat bone marrow-derived mesenchymal stem cells in spheroidal aggregate culture on a decellularized liver scaffold. Int J Mol Med 38, 457-465.

Basso, F. G., Soares, D. G., de Souza Costa, C. A., and Hebling, J. (2016). Low-level laser therapy in 3D cell culture model using gingival fibroblasts. Lasers Med Sci 31, 973-978.

Bauer, J., Bussen, M., Wise, P., Wehland, M., Schneider, S., and Grimm, D. (2016). Searching the literature for proteins facilitates the identification of biological processes, if advanced methods of analysis are linked: a case study on microgravity-caused changes in cells. Expert Rev Proteomics 13, 697-705.

Bautista, C. A., Park, H. J., Mazur, C. M., Aaron, R. K., and Bilgen, B. (2016). Effects of Chondroitinase ABC-Mediated Proteoglycan Digestion on Decellularization and Recellularization of Articular Cartilage. PLoS One 11, e0158976.

Bhat, R., Belardi, B., Mori, H., Kuo, P., Tam, A., Hines, W. C., Le, Q. T., Bertozzi, C. R., and Bissell, M. J. (2016). Nuclear repartitioning of galectin-1 by an extracellular glycan switch regulates mammary morphogenesis. Proc Natl Acad Sci U S A 113, E4820-4827.

Bielecka, Z. F., Maliszewska-Olejniczak, K., Safir, I. J., Szczylik, C., and Czarnecka, A. M. (2016). Three-dimensional cell culture model utilization in cancer stem cell research. Biol Rev Camb Philos Soc.

Booij, T. H., Klop, M. J., Yan, K., Szantai-Kis, C., Szokol, B., Orfi, L., van de Water, B., Keri, G., and Price, L. S. (2016). Development of a 3D Tissue Culture-Based High-Content Screening Platform That Uses Phenotypic Profiling to Discriminate Selective Inhibitors of Receptor Tyrosine Kinases. J Biomol Screen.

Branco da Cunha, C., Klumpers, D. D., Koshy, S. T., Weaver, J. C., Chaudhuri, O., Seruca, R., Carneiro, F., Granja, P. L., and Mooney, D. J. (2016). CD44 alternative splicing in gastric cancer cells is regulated by culture dimensionality and matrix stiffness. Biomaterials 98, 152-162.

Brooks, J. C., Ford, K. I., Holder, D. H., Holtan, M. D., and Easley, C. J. (2016). Macro-to-micro interfacing to microfluidic channels using 3D-printed templates: application to time-resolved secretion sampling of endocrine tissue. Analyst.

Broutier, L., Andersson-Rolf, A., Hindley, C. J., Boj, S. F., Clevers, H., Koo, B. K., and Huch, M. (2016). Culture and establishment of self-renewing human and mouse adult liver and pancreas 3D organoids and their genetic manipulation. Nat Protoc 11, 1724-1743.

Carapuca, E. F., Gemenetzidis, E., Feig, C., Bapiro, T. E., Williams, M. D., Wilson, A. S., Delvecchio, F. R., Arumugam, P., Grose, R. P., Lemoine, N. R., et al. (2016). Anti-stromal treatment together with chemotherapy targets multiple signalling pathways in pancreatic adenocarcinoma. J Pathol 239, 286-296.

Castro, N. J., Tan, W. N., Shen, C., and Zhang, L. G. (2016). Simulated Body Fluid Nucleation of Three-Dimensional Printed Elastomeric Scaffolds for Enhanced Osteogenesis. Tissue Eng Part A 22, 940-948.

Chen, C., Mehl, B. T., Sell, S. A., and Martin, R. S. (2016a). Use of electrospinning and dynamic air focusing to create three-dimensional cell culture scaffolds in microfluidic devices. Analyst.

Chen, K., Wu, M., Guo, F., Li, P., Chan, C. Y., Mao, Z., Li, S., Ren, L., Zhang, R., and Huang, T. J. (2016b). Rapid formation of size-controllable multicellular spheroids via 3D acoustic tweezers. Lab Chip 16, 2636-2643.

Chennell, G., Willows, R. J., Warren, S. C., Carling, D., French, P. M., Dunsby, C., and Sardini, A. (2016). Imaging of Metabolic Status in 3D Cultures with an Improved AMPK FRET Biosensor for FLIM. Sensors (Basel) 16.

Colak, B., Da Silva, J. C., Soares, T. A., and Gautrot, J. E. (2016). Impact of the Molecular Environment on Thiol-Ene Coupling For Biofunctionalization and Conjugation. Bioconjug Chem.

Coleman, C. N., Higgins, G. S., Brown, J. M., Baumann, M., Kirsch, D. G., Willers, H., Prasanna, P. G., Dewhirst, M. W., Bernhard, E. J., and Ahmed, M. M. (2016). Improving the Predictive Value of Preclinical Studies in Support of Radiotherapy Clinical Trials. Clin Cancer Res 22, 3138-3147.

Cook, C. A., Huri, P. Y., Ginn, B. P., Gilbert-Honick, J., Somers, S. M., Temple, J. P., Mao, H. Q., and Grayson, W. L. (2016). Characterization of a novel bioreactor system for 3D cellular mechanobiology studies. Biotechnol Bioeng 113, 1825-1837.

Czulkies, B. A., Mastroianni, J., Lutz, L., Lang, S., Schwan, C., Schmidt, G., Lassmann, S., Zeiser, R., Aktories, K., and Papatheodorou, P. (2016). Loss of LSR affects epithelial barrier integrity and tumor xenograft growth of CaCo-2 cells. Oncotarget.

da Silva, E. J., Zaia, A. A., and Peters, O. A. (2016). Cytocompatibility of calcium silicate-based sealers in a three-dimensional cell culture model. Clin Oral Investig.

DuVall, J. A., Cabaniss, S. T., Angotti, M. L., Moore, J. H., Abhyankar, M., Shukla, N., Mills, D. L., Kessel, B. G., Garner, G. T., Swami, N. S., and Landers, J. P. (2016). Rapid detection of Clostridium difficile via magnetic bead aggregation in cost-effective polyester microdevices with cell phone image analysis. Analyst.

El-Ashmawy, M., Coquelin, M., Luitel, K., Batten, K., and Shay, J. W. (2016). Organotypic culture in three dimensions prevents radiation-induced transformation in human lung epithelial cells. Sci Rep 6, 31669.

Elamparithi, A., Punnoose, A. M., and Kuruvilla, S. (2016). Electrospun type 1 collagen matrices preserving native ultrastructure using benign binary solvent for cardiac tissue engineering. Artif Cells Nanomed Biotechnol 44, 1318-1325.

Esch, M. B., Ueno, H., Applegate, D. R., and Shuler, M. L. (2016). Modular, pumpless body-on-a-chip platform for the co-culture of GI tract epithelium and 3D primary liver tissue. Lab Chip 16, 2719-2729.

Fecher, D., Hofmann, E., Buck, A., Bundschuh, R., Nietzer, S., Dandekar, G., Walles, T., Walles, H., Luckerath, K., and Steinke, M. (2016). Human Organotypic Lung Tumor Models: Suitable For Preclinical 18F-FDG PET-Imaging. PLoS One 11, e0160282.

Ferroni, M., Giusti, S., Nascimento, D., Silva, A., Boschetti, F., and Ahluwalia, A. (2016). Modeling the fluid-dynamics and oxygen consumption in a porous scaffold stimulated by cyclic squeeze pressure. Med Eng Phys 38, 725-732.

Filipowska, J., Reilly, G. C., and Osyczka, A. M. (2016). A single short session of media perfusion induces osteogenesis in hBMSCs cultured in porous scaffolds, dependent on cell differentiation stage. Biotechnol Bioeng 113, 1814-1824.

Fitzgerald, K. A., Guo, J., Raftery, R. M., Castano, I. M., Curtin, C. M., Gooding, M., Darcy, R., Brien, F. J., and Driscoll, C. M. (2016). Nanoparticle-mediated siRNA delivery assessed in a 3D co-culture model simulating prostate cancer bone metastasis. Int J Pharm.

Follin, B., Juhl, M., Cohen, S., Perdersen, A. E., Kastrup, J., and Ekblond, A. (2016). Increased Paracrine Immunomodulatory Potential of Mesenchymal Stromal Cells in Three-Dimensional Culture. Tissue Eng Part B Rev 22, 322-329.

Fong, A. H., Romero-Lopez, M., Heylman, C. M., Keating, M., Tran, D., Sobrino, A., Tran, A. Q., Pham, H. H., Fimbres, C., Gershon, P. D., et al. (2016). Three-dimensional adult cardiac extracellular matrix promotes maturation of human induced pluripotent stem cell-derived cardiomyocytes. Tissue Eng Part A.

Froehlich, K., Haeger, J. D., Heger, J., Pastuschek, J., Photini, S. M., Yan, Y., Lupp, A., Pfarrer, C., Mrowka, R., Schleussner, E., et al. (2016). Generation of Multicellular Breast Cancer Tumor Spheroids: Comparison of Different Protocols. J Mammary Gland Biol Neoplasia.

Galdon, G., Atala, A., and Sadri-Ardekani, H. (2016). In Vitro Spermatogenesis: How Far from Clinical Application? Curr Urol Rep 17, 49.

Ganapathy, K., Sowmithra, S., Bhonde, R., and Datta, I. (2016). By Changing Dimensionality, Sequential Culturing of Midbrain Cells, rather than Two-Dimensional Culture, Generates a Neuron-Glia Ratio Closer to in vivo Adult Midbrain. Cells Tissues Organs 201, 445-463.

Gao, B., Wang, L., Han, S., Pingguan-Murphy, B., Zhang, X., and Xu, F. (2016). Engineering of microscale three-dimensional pancreatic islet models in vitro and their biomedical applications. Crit Rev Biotechnol 36, 619-629.

Gimenez, A., Uriarte, J. J., Vieyra, J., Navajas, D., and Alcaraz, J. (2016). Elastic properties of hydrogels and decellularized tissue sections used in mechanobiology studies probed by atomic force microscopy. Microsc Res Tech.

Goncalves, P. R., Rocha-Brito, K. J., Fernandes, M. R., Abrantes, J. L., Duran, N., and Ferreira-Halder, C. V. (2016). Violacein induces death of RAS-mutated metastatic melanoma by impairing autophagy process. Tumour Biol.

Goppert, B., Sollich, T., Abaffy, P., Cecilia, A., Heckmann, J., Neeb, A., Backer, A., Baumbach, T., Gruhl, F. J., and Cato, A. C. (2016). Superporous Poly(ethylene glycol) Diacrylate Cryogel with a Defined Elastic Modulus for Prostate Cancer Cell Research. Small 12, 3985-3994.

Hagiwara, M., Kawahara, T., and Nobata, R. (2016). Tissue in Cube: In Vitro 3D Culturing Platform with Hybrid Gel Cubes for Multidirectional Observations. Adv Healthc Mater 5, 1566-1571.

Han, S., Wang, B., Li, X., Xiao, Z., Han, J., Zhao, Y., Fang, Y., Yin, Y., Chen, B., and Dai, J. (2016). Bone marrow-derived mesenchymal stem cells in three-dimensional culture promote neuronal regeneration by neurotrophic protection and immunomodulation. J Biomed Mater Res A 104, 1759-1769.

He, X., and Toth, T. L. (2016). In vitro culture of ovarian follicles from Peromyscus. Semin Cell Dev Biol.

Hillebrand, L. E., Bengsch, F., Hochrein, J., Hulsdunker, J., Bender, J., Follo, M., Busch, H., Boerries, M., and Reinheckel, T. (2016). Proteolysis-a characteristic of tumor-initiating cells in murine metastatic breast cancer. Oncotarget.

Hisha, H., and Ueno, H. (2016). Organoid Culture of Lingual Epithelial Cells in a Three-Dimensional Matrix. Methods Mol Biol.

Hynds, R. E., Butler, C. R., Janes, S. M., and Giangreco, A. (2016). Expansion of Human Airway Basal Stem Cells and Their Differentiation as 3D Tracheospheres. Methods Mol Biol.

Ingthorsson, S., Andersen, K., Hilmarsdottir, B., Maelandsmo, G. M., Magnusson, M. K., and Gudjonsson, T. (2016). HER2 induced EMT and tumorigenicity in breast epithelial progenitor cells is inhibited by coexpression of EGFR. Oncogene 35, 4244-4255.

Ishii, T., Saito, H., Komizu, Y., Tomoshige, R., and Matsushita, T. (2016). Effects of macroporous hydroxyapatite carriers on the growth and function of human hepatoblasts derived from fetal hepatocytes. J Biosci Bioeng 122, 240-245.

Ivanovska, J., Zehnder, T., Lennert, P., Sarker, B., Boccaccini, A. R., Hartmann, A., Schneider-Stock, R., and Detsch, R. (2016). Biofabrication of 3D Alginate-Based Hydrogel for Cancer Research: Comparison of Cell Spreading, Viability, and Adhesion Characteristics of Colorectal HCT116 Tumor Cells. Tissue Eng Part C Methods 22, 708-715.

Jellali, R., Duval, J. L., and Leclerc, E. (2016). Analysis of the biocompatibility of perfluoropolyether dimethacrylate network using an organotypic method. Mater Sci Eng C Mater Biol Appl 65, 295-302.

Jenkins, J., Papkovsky, D. B., and Dmitriev, R. I. (2016). The Ca2+/Mn2+-transporting SPCA2 pump is regulated by oxygen and cell density in colon cancer cells. Biochem J 473, 2507-2518.

Jennewein, M., Bubel, M., Guthorl, S., Metzger, W., Weigert, M., Pohlemann, T., and Oberringer, M. (2016). Two- and three-dimensional co-culture models of soft tissue healing: pericyte-endothelial cell interaction. Cell Tissue Res 365, 279-293.

Jeon, H., Kang, K., Park, S. A., Kim, W. D., Paik, S. S., Lee, S. H., Jeong, J., and Choi, D. (2016). Generation of Multilayered 3D Structures of HepG2 Cells Using a Bio-printing Technique. Gut Liver.

Jeong, S. Y., Lee, J. H., Shin, Y., Chung, S., and Kuh, H. J. (2016). Co-Culture of Tumor Spheroids and Fibroblasts in a Collagen Matrix-Incorporated Microfluidic Chip Mimics Reciprocal Activation in Solid Tumor Microenvironment. PLoS One 11, e0159013.

Jha, R., Wu, Q., Singh, M., Preininger, M. K., Han, P., Ding, G., Cho, H. C., Jo, H., Maher, K. O., Wagner, M. B., and Xu, C. (2016). Simulated Microgravity and 3D Culture Enhance Induction, Viability, Proliferation and Differentiation of Cardiac Progenitors from Human Pluripotent Stem Cells. Sci Rep 6, 30956.

Jo, J., Xiao, Y., Sun, A. X., Cukuroglu, E., Tran, H. D., Goke, J., Tan, Z. Y., Saw, T. Y., Tan, C. P., Lokman, H., et al. (2016). Midbrain-like Organoids from Human Pluripotent Stem Cells Contain Functional Dopaminergic and Neuromelanin-Producing Neurons. Cell Stem Cell 19, 248-257.

Jobe, N. P., Rosel, D., Dvorankova, B., Kodet, O., Lacina, L., Mateu, R., Smetana, K., and Brabek, J. (2016). Simultaneous blocking of IL-6 and IL-8 is sufficient to fully inhibit CAF-induced human melanoma cell invasiveness. Histochem Cell Biol 146, 205-217.

Kapyla, E., Delgado, S. M., and Kasko, A. M. (2016). Shape-Changing Photodegradable Hydrogels for Dynamic 3D Cell Culture. ACS Appl Mater Interfaces 8, 17885-17893.

Karimi, M., Bahrami, S., Mirshekari, H., Basri, S. M., Nik, A. B., Aref, A. R., Akbari, M., and Hamblin, M. R. (2016). Microfluidic systems for stem cell-based neural tissue engineering. Lab Chip 16, 2551-2571.

Karnevi, E., Rosendahl, A. H., Hilmersson, K. S., Saleem, M. A., and Andersson, R. (2016). Impact by pancreatic stellate cells on epithelial-mesenchymal transition and pancreatic cancer cell invasion: Adding a third dimension in vitro. Exp Cell Res 346, 206-215.

Kawakami, M., Ishikawa, H., Tanaka, A., and Mataga, I. (2016). Induction and differentiation of adipose-derived stem cells from human buccal fat pads into salivary gland cells. Hum Cell 29, 101-110.

Kazantseva, J., Ivanov, R., Gasik, M., Neuman, T., and Hussainova, I. (2016). Graphene-augmented nanofiber scaffolds demonstrate new features in cells behaviour. Sci Rep 6, 30150.

Kilian, T., Fidler, F., Kasten, A., Nietzer, S., Landgraf, V., Weiss, K., Walles, H., Westphal, F., Hackenberg, S., Gruttner, C., and Steinke, M. (2016). Stem cell labeling with iron oxide nanoparticles: impact of 3D culture on cell labeling maintenance. Nanomedicine (Lond) 11, 1957-1970.

Ko, K. R., and Frampton, J. P. (2016). Developments in 3D neural cell culture models: the future of neurotherapeutics testing? Expert Rev Neurother 16, 739-741.

Kriston-Vizi, J., and Flotow, H. (2016). Getting the whole picture: High content screening using three-dimensional cellular model systems and whole animal assays. Cytometry A.

Kropp, C., Kempf, H., Halloin, C., Robles-Diaz, D., Franke, A., Scheper, T., Kinast, K., Knorpp, T., Joos, T. O., Haverich, A., et al. (2016). Impact of Feeding Strategies on the Scalable Expansion of Human Pluripotent Stem Cells in Single-Use Stirred Tank Bioreactors. Stem Cells Transl Med.

Kulasinghe, A., Perry, C., Warkiani, M. E., Blick, T., Davies, A., O'Byrne, K., Thompson, E. W., Nelson, C. C., Vela, I., and Punyadeera, C. (2016). Short term ex-vivo expansion of circulating head and neck tumour cells. Oncotarget.

Kumeria, T., Maher, S., Wang, Y., Kaur, G., Wang, L., Erkelens, M., Forward, P., Lambert, M. F., Evdokiou, A., and Losic, D. (2016). Naturally Derived Iron Oxide Nanowires from Bacteria for Magnetically Triggered Drug Release and Cancer Hyperthermia in 2D and 3D Culture Environments: Bacteria Biofilm to Potent Cancer Therapeutic. Biomacromolecules 17, 2726-2736.

Laughter, M. R., Ammar, D. A., Bardill, J. R., Pena, B., Kahook, M. Y., Lee, D. J., and Park, D. (2016). A Self-Assembling Injectable Biomimetic Microenvironment Encourages Retinal Ganglion Cell Axon Extension in Vitro. ACS Appl Mater Interfaces 8, 20540-20548.

Lee, D. W., Oh, W. Y., Yi, S. H., Ku, B., Lee, M. Y., Cho, Y. H., and Yang, M. (2016a). Estimation of Bisphenol A -Human Toxicity by 3D Cell Culture Arrays,High Throughput Alternatives to Animal Tests. Toxicol Lett.

Lee, G. H., Park, Y. E., Cho, M., Park, H., and Park, J. Y. (2016b). Magnetic force-assisted self-locking metallic bead array for fabrication of diverse concave microwell geometries. Lab Chip.

Lee, M., Ahn, J. I., Ahn, J. Y., Yang, W. S., Hubbell, J. A., Lim, J. M., and Lee, S. T. (2016c). Difference in suitable mechanical properties of three-dimensional, synthetic scaffolds for self-renewing mouse embryonic stem cells of different genetic backgrounds. J Biomed Mater Res B Appl Biomater.

Lee, W., and Park, J. (2016). 3D patterned stem cell differentiation using thermo-responsive methylcellulose hydrogel molds. Sci Rep 6, 29408.

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