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Created: 09 Sep 2015

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Volume 9, April 2017

Newsletter

3D at Purdue

3D in Focus

3D in Publications

3D in Meetings

3D at Purdue

A 3D culture model for studying
bone cell biology and bone tissue formation

The most numerous cell type in the skeleton is the osteocyte, an important regulator of bone-forming osteoblasts and bone-resorbing osteoclasts. Although surrounded by a mineralized matrix, these cells are sensitive to both chemical and mechanical stimuli transmitted through the fluid-filled canaliculi and lacunae surrounding their dendritic cellular processes and the cell bodies, respectively (Fig. 1). Given the osteocytes’ influential role in regulating other bone cells, it seems likely that these cells would play a central role in understanding the cellular causes for skeletal disease, including bone wasting diseases, like osteoporosis, and in developing treatments for these diseases. Because osteocytes reside within a 3D syncytium within the mineralized bone matrix, it is difficult to gain access to large numbers of isolated cells for traditional high throughput molecular biomarker analyses, and attempts to recapitulate these cells’ physiological environment and cellular syncytium in vitro have been few. However, should we ever hope to study osteocyte biology in a controlled environment, optimize drug delivery methods to these cells, produce an individualized-medicine approach to skeletal disease, or develop novel osteocyte-driven methods for bone healing and regeneration, we must be able to capture the unique features of the osteocyte’s 3D extracellular matrix environment.

To address this problem, we began collaborating with Drs. Sherry Voytik-Harbin and Eric Nauman in 2013 to develop a 3D collagen-mineral matrix in which we could seed bone marrow stromal cells (BMSCs) or osteoblasts in vitro and stimulate these cells to produce bone matrix de novo, which would induce differentiation to osteocytes. We use oligomeric porcine skin collagen developed by Dr. Harbin’s laboratory and precipitated hydroxyapatite (HA) as the fundamental components of the extracellular matrix. To date, we have been harvesting primary cells (osteoblasts and BMSCs) from mT/mG x DMP1-Cre mice that express membrane tomato in all of their cells, except those expressing the DMP1-driven Cre, which express enhanced green fluorescent protein (EGFP). In the skeleton, DMP-1 expression is generally limited to late osteoblasts and early osteocytes, so harnessing these genetic mouse models is a useful way to monitor osteocyte differentiation in our cultures. We are presently in the differentiation optimization phase of our work, testing the effects of different amounts of exogenous HA (14mg/mL, 28mg/mL) and varying collagen stiffness (corresponding to 250 Pa and 500 Pa shear storage modulus) on osteocyte differentiation using both primary osteoblasts and BMSCs.

Our first steps in this optimization process are to determine how well the varying ECM conditions promote (1) de novo bone formation, (2) osteocyte differentiation, and (3) establishment of a 3D lacunar-canalicular network of osteocytes. De novo bone formation would also likely cause changes in matrix material properties, so we can measure culture compressive stiffness as a proxy for tissue-level changes in the culture matrix. To assess osteocyte differentiation, we have conducted cell counts for 3D HA-collagen constructs cultured for 3 days, 28 days or 56 days. Cells are characterized using confocal microscopy based upon their dominant cell membrane fluorescence, expressing either membrane tomato, membrane EGFP, or transitioning cells that express a combination of membrane tomato and EGFP, which appear yellow when the confocal color channels are merged (Figure 2). Current sample sizes per culture condition are fairly low (n=2-3), but preliminary data suggest that osteoblasts cultured in the HA-collagen scaffolds differentiate toward osteocytes over the 56d culture period. The degree of differentiation appears to be greater in the cultures with greater amounts of HA, relative to cultures with no HA, suggesting that the HA is an important influence in this differentiation process. The greatest percentages of green osteocytes are found in the cultures composed of 500 Pa collagen and 14 mg/ml HA. While the BMSCs started the culture period with a greater percentage of green cells than did the osteoblast cultures, they did not increase in percentage over the 56d culture period as consistently as the osteoblasts did. Similarly, the compressive stiffness of the MSC cultures did not change over the 56d period, unlike the osteoblasts cultured under certain culture conditions (250 Pa, 28 mg/ml HA; 500 Pa, 14 mg/ml HA; 500 Pa, 28 mg/ml HA), which showed a progressive increase in compressive stiffness over the 56d culture period. Increased stiffness over the culture period suggests that the matrix is changing in some way, most likely due to de novo bone formation by osteoblasts, which then become entrapped in the bone matrix as osteocytes.

Future research efforts will be focused on assessing changes in bone mineral density in the 3D cultures by computed tomography and studying physiochemical properties by Raman spectroscopy. We will also be assessing osteoblast differentiation to osteocytes, bone formation, and establishment of a bone-like lacunar-canalicular system using gene expression analyses and bone histomorphometry.

Figure 1: Cortical bone from a mouse vertebra. Osteocytes and their dendritic cytoplasmic processes lie within lacunae and canaliculi. Osteocytes differentiate from osteoblasts lying on the bone surface near the periosteum. The labeled cell (*) is an early differentiating osteocyte. Green and red (faint) fluorescence is derived genetically and results from a cross between mT/mG mice and DMP1-8kb-Cre mice. Blue fluorescence is DAPI, which indicates the cell nucleus. Scale bar = 10um.

Figure 2: Three-day osteoblast 3D culture in collagen with a 500 Pa shear storage modulus and 14 mg/ml hydroxyapatite (HA) content. Even after three days, cells are beginning to transition in color from red (osteoblast) to green (osteocyte, arrowheads) and extend dendritic processes (arrows). The (*) indicates autofluorescent HA particles. Scale bar = 40um.

Russell P. Main
Assistant Professor
Department of Basic Medical Sciences, Purdue College of Veterinary Medicine
Weldon School of Biomedical Engineering

3D in Focus

One of the technical challenges holding back our understanding of spermatogenesis is the lack of an in vitro system that recapitulates this phenomenon. The system will be useful for work related to testicular toxicity, infertility, animal conservation, preservation of endangered species, etc. The testis has about 250 lobules, each containing one to four highly coiled seminiferous tubules. The seminiferous tubules are composed of an internal epithelium formed of Sertoli cells, needed for germ cell differentiation, and external layers of smooth muscle-like cells known as peritubular cells. The objective of the article highlighted in this newsletter is to use the “Three-Layer Gradient System” to generate testicular organoids with functional blood–testis barrier for germ cell establishment and proliferation that more closely represent the in vivo germ-to-somatic cell associations.

Featured article: Joao Pedro Alves-Lopes, Olle Soder, Jan-Bernd Stukenborg Testicular organoid generation by a novel in vitro three-layer gradient system Biomaterials 130 (2017) 76 - 89

Our summary: Cell suspensions containing different cell types were prepared by enzymatic dissociation of testes from 5-, 20- and 60-day post-partum (dpp) Sprague Dawley rats. The cells were cultured within a drop of Matrigel, which was placed between two cell-free layers of Matrigel; one beneath and one as overlay. The cells, primarily Sertoli cells, reorganized into seminiferous-like structures, in the form of sphere-tubular structures (STSs). The reorganization of cells was not observed if only one layer of Matrigel was used. The histological arrangement of Sertoli cells, similar to that in vivo, was determined by periodic acid-Schiff staining as well as immunofluorescence staining against transcription factor Sox9. A functional blood–testis barrier in STSs was demonstrated by the impermeability to 0.4% Evans Blue dye and the expressions of ZO-1 and occludin tight junction proteins. Additionally, differentiation of germ cells, indicated by the presence of chains of undifferentiated germ cells (protein promyelocytic leukaemia zinc-finger positive cells), connecting with germ cells (vasa positive cells), was observed in the STSs culture. It is also interesting to note that agents known to affect germ cell differentiation and maintenance in vivo (by altering tight junctions in blood-testis barrier for instance), had similar effect on the cells in STSs.

In summary, the “Three-Layer Gradient System” is a novel approach to generate rat testicular organoids resembling seminiferous-like structures in vitro. As proposed by the authors, the formation of the organoids might be linked to the concepts of molecular diffusion and concentration gradient in the three layers of Matrigel (see Figure). The gradients are indeed absent in the conventional 3D models, where cells are equally distributed in one layer of supportive scaffold.

Next possible steps: Spermatogenesis is the production of spermatozoids from primordial germ cells through spermatogonia, the vasa-positive cells. The STSs represents only the early part of the process and additions to the model are necessary to reproduce the later steps in the process. The concepts of molecular diffusion and concentration gradient in the “Three-Layer Gradient System” are yet to be demonstrated; indeed, it is intriguing that placing cells in-between layers of scaffolds as in the “Three-Layer Gradient System” may be a better alternative to the one-layer conventional approach in 3D cell culture; whether the extent of the gradient or heterogeneity of the gradient that might exist based on the geometry of the STS 3D culture is important might be worth investigating.

Figure Schematic representation of molecular diffusion and concentration gradients in the sphere-tubular structure “Three-Layer Gradient System” (Adapted from Biomaterials 130 (2017) 76 – 89)

3D in Publications

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

Reviews

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3D in Publications

Complete List

Abecasis, B., Aguiar, T., Arnault, E., Costa, R., Gomes-Alves, P., Aspegren, A., Serra, M., and Alves, P. M. (2017). Expansion of 3D human induced pluripotent stem cell aggregates in bioreactors: Bioprocess intensification and scaling-up approaches. J Biotechnol 246, 81-93.

Alves-Lopes, J. P., Soder, O., and Stukenborg, J. B. (2017). Testicular organoid generation by a novel in vitro three-layer gradient system. Biomaterials 130, 76-89.

Amann, E., Wolff, P., Breel, E., van Griensven, M., and Balmayor, E. R. (2017). Hyaluronic acid facilitates chondrogenesis and matrix deposition of human adipose derived mesenchymal stem cells and human chondrocytes co-cultures. Acta Biomater 52, 130-144.

Anabazhagan, A. N., Chatterjee, I., Priyamvada, S., Kumar, A., Tyagi, S., Saksena, S., Alrefai, W. A., Dudeja, P. K., and Gill, R. K. (2017). Methods to Study Epithelial Transport Protein Function and Expression in Native Intestine and Caco-2 Cells Grown in 3D. J Vis Exp.

Andilla, J., Jorand, R., Olarte, O. E., Dufour, A. C., Cazales, M., Montagner, Y. L., Ceolato, R., Riviere, N., Olivo-Marin, J. C., Loza-Alvarez, P., and Lorenzo, C. (2017). Imaging tissue-mimic with light sheet microscopy: A comparative guideline. Sci Rep 7, 44939.

Arai, E., Parmar, V. M., Sahu, B., Perusek, L., Parmar, T., and Maeda, A. (2017). Docosahexaenoic acid promotes differentiation of photoreceptor cells in three-dimensional neural retinas. Neurosci Res.

Ashraf, S., Han, I. B., Park, H., and Lee, S. H. (2017). Role of RHEB in Regulating Differentiation Fate of Mesenchymal Stem Cells for Cartilage and Bone Regeneration. Int J Mol Sci 18.

Bach, F. C., Miranda-Bedate, A., van Heel, F. W., Riemers, F. M., Muller, M. C., Creemers, L. B., Ito, K., Benz, K., Meij, B. P., and Tryfonidou, M. A. (2017). Bone Morphogenetic Protein-2, But Not Mesenchymal Stromal Cells, Exert Regenerative Effects on Canine and Human Nucleus Pulposus Cells. Tissue Eng Part A 23, 233-242.

Bae, Y. J., Kwon, Y. R., Kim, H. J., Lee, S., and Kim, Y. J. (2017). Enhanced differentiation of mesenchymal stromal cells by three-dimensional culture and azacitidine. Blood Res 52, 18-24.

Bartfeld, S., and Clevers, H. (2017). Stem cell-derived organoids and their application for medical research and patient treatment. J Mol Med (Berl).

Benmerzoug, S., and Quesniaux, V. F. (2017). Bioengineered 3D Models for Studying Human Cell-Tuberculosis Interactions. Trends Microbiol.

Bhattacharyya, S., Sekar, V., Majumder, B., Mehrotra, D. G., Banerjee, S., Bhowmick, A. K., Alam, N., Mandal, G. K., Biswas, J., Majumder, P. K., and Murmu, N. (2017). CDKN2A-p53 mediated antitumor effect of Lupeol in head and neck cancer. Cell Oncol (Dordr) 40, 145-155.

Binner, M., Bray, L. J., Friedrichs, J., Freudenberg, U., Tsurkan, M. V., and Werner, C. (2017). Cell-instructive starPEG-heparin-collagen composite matrices. Acta Biomater 53, 70-80.

Bodenberger, N., Kubiczek, D., Paul, P., Preising, N., Weber, L., Bosch, R., Hausmann, R., Gottschalk, K. E., and Rosenau, F. (2017). Beyond bread and beer: whole cell protein extracts from baker's yeast as a bulk source for 3D cell culture matrices. Appl Microbiol Biotechnol 101, 1907-1917.

Bottagisio, M., Lopa, S., Granata, V., Talo, G., Bazzocchi, C., Moretti, M., and Barbara Lovati, A. (2017). Different combinations of growth factors for the tenogenic differentiation of bone marrow mesenchymal stem cells in monolayer culture and in fibrin-based three-dimensional constructs. Differentiation 95, 44-53.

Bray, L. J., Binner, M., Korner, Y., von Bonin, M., Bornhauser, M., and Werner, C. (2017). A three-dimensional ex vivo tri-culture model mimics cell-cell interactions between acute myeloid leukemia and the vascular niche. Haematologica.

Brunelli, M., Perrault, C. M., and Lacroix, D. (2017). Short bursts of cyclic mechanical compression modulate tissue formation in a 3D hybrid scaffold. J Mech Behav Biomed Mater 71, 165-174.

Burian, E., Probst, F., Palla, B., Riedel, C., Saller, M. M., Cornelsen, M., Konig, F., Schieker, M., and Otto, S. (2017). Effect of hypoxia on the proliferation of porcine bone marrow-derived mesenchymal stem cells and adipose-derived mesenchymal stem cells in 2- and 3-dimensional culture. J Craniomaxillofac Surg 45, 414-419.

Cao, Y., Hjort, M., Chen, H., Birey, F., Leal-Ortiz, S. A., Han, C. M., Santiago, J. G., Pasca, S. P., Wu, J. C., and Melosh, N. A. (2017). Nondestructive nanostraw intracellular sampling for longitudinal cell monitoring. Proc Natl Acad Sci U S A 114, E1866-e1874.

Carreras, M. P., and Wang, S. (2017). A Multifunctional Microfluidic Platform for Generation, Trapping and Release of Droplets in a Double Laminar Flow. J Biotechnol.

Carter, E. P., Gopsill, J. A., Gomm, J. J., Jones, J. L., and Grose, R. P. (2017). A 3D in vitro model of the human breast duct: a method to unravel myoepithelial-luminal interactions in the progression of breast cancer. Breast Cancer Res 19, 50.

Casey, J., Yue, X., Nguyen, T. D., Acun, A., Zellmer, V. R., Zhang, S., and Zorlutuna, P. (2017). 3D hydrogel-based microwell arrays as a tumor microenvironment model to study breast cancer growth. Biomed Mater 12, 025009.

Cevenini, L., Calabretta, M. M., Lopreside, A., Branchini, B. R., Southworth, T. L., Michelini, E., and Roda, A. (2017). Bioluminescence Imaging of Spheroids for High-throughput Longitudinal Studies on 3D Cell Culture Models. Photochem Photobiol 93, 531-535.

Cha, H. J., Choi, J. H., Park, I. C., Kim, C. H., An, S. K., Kim, T. J., and Lee, J. H. (2017). Selective FGFR inhibitor BGJ398 inhibits phosphorylation of AKT and STAT3 and induces cytotoxicity in sphere-cultured ovarian cancer cells. Int J Oncol.

Chai, Y. C., Bolander, J., Papantoniou, I., Patterson, J., Vleugels, J., Schrooten, J., and Luyten, F. P. (2017). Harnessing the Osteogenicity of In Vitro Stem Cell-Derived Mineralized Extracellular Matrix as 3D Biotemplate to Guide Bone Regeneration. Tissue Eng Part A.

Chen, J., Yuan, Z., Liu, Y., Zheng, R., Dai, Y., Tao, R., Xia, H., Liu, H., Zhang, Z., Zhang, W., et al. (2017a). Improvement of In Vitro Three-Dimensional Cartilage Regeneration by a Novel Hydrostatic Pressure Bioreactor. Stem Cells Transl Med 6, 982-991.

Chen, Y. W., Huang, S. X., de Carvalho, A., Ho, S. H., Islam, M. N., Volpi, S., Notarangelo, L. D., Ciancanelli, M., Casanova, J. L., Bhattacharya, J., et al. (2017b). A three-dimensional model of human lung development and disease from pluripotent stem cells. Nat Cell Biol.

Chiew, G. G., Wei, N., Sultania, S., Lim, S., and Luo, K. Q. (2017). Bioengineered three-dimensional co-culture of cancer cells and endothelial cells: A model system for dual analysis of tumor growth and angiogenesis. Biotechnol Bioeng.

Chimenti, I., Pagano, F., Angelini, F., Siciliano, C., Mangino, G., Picchio, V., De Falco, E., Peruzzi, M., Carnevale, R., Ibrahim, M., et al. (2017). Human Lung Spheroids as In Vitro Niches of Lung Progenitor Cells with Distinctive Paracrine and Plasticity Properties. Stem Cells Transl Med 6, 767-777.

Collins, S. J., and Haigh, C. L. (2017). Simplified Murine 3D Neuronal Cultures for Investigating Neuronal Activity and Neurodegeneration. Cell Biochem Biophys 75, 3-13.

Cook, C. D., Hill, A. S., Guo, M., Stockdale, L., Papps, J. P., Isaacson, K. B., Lauffenburger, D. A., and Griffith, L. G. (2017). Local remodeling of synthetic extracellular matrix microenvironments by co-cultured endometrial epithelial and stromal cells enables long-term dynamic physiological function. Integr Biol (Camb).

Correia, C. R., Santos, T. C., Pirraco, R. P., Cerqueira, M. T., Marques, A. P., Reis, R. L., and Mano, J. F. (2017). In vivo osteogenic differentiation of stem cells inside compartmentalized capsules loaded with co-cultured endothelial cells. Acta Biomater 53, 483-494.

Costantini, M., Testa, S., Mozetic, P., Barbetta, A., Fuoco, C., Fornetti, E., Tamiro, F., Bernardini, S., Jaroszewicz, J., Swieszkowski, W., et al. (2017). Microfluidic-enhanced 3D bioprinting of aligned myoblast-laden hydrogels leads to functionally organized myofibers in vitro and in vivo. Biomaterials 131, 98-110.

Dang, Q., Liu, K., Zhang, Z., Liu, C., Liu, X., Xin, Y., Cheng, X., Xu, T., Cha, D., and Fan, B. (2017). Fabrication and evaluation of thermosensitive chitosan/collagen/alpha, beta-glycerophosphate hydrogels for tissue regeneration. Carbohydr Polym 167, 145-157.

Das, T., Nair, R. R., Green, R., Padhee, S., Howell, M., Banerjee, J., Mohapatra, S. S., and Mohapatra, S. (2017). Actinomycin D Down-regulates SOX2 Expression and Induces Death in Breast Cancer Stem Cells. Anticancer Res 37, 1655-1663.

de Avila, A. I., Moreno, E., Perales, C., and Domingo, E. (2017). Favipiravir can evoke lethal mutagenesis and extinction of foot-and-mouth disease virus. Virus Res 233, 105-112.

de Matos Candido-Bacani, P., Ezan, F., de Oliveira Figueiredo, P., de Fatima Cepa Matos, M., Rodrigues Garcez, F., Silva Garcez, W., and Baffet, G. (2017). [1-9-NalphaC]-crourorb A1 isolated from Croton urucurana latex induces G2/M cell cycle arrest and apoptosis in human hepatocarcinoma cells. Toxicol Lett.

DeCicco RePass, M. A., Chen, Y., Lin, Y., Zhou, W., Kaplan, D. L., and Ward, H. D. (2017). Novel Bioengineered Three-Dimensional Human Intestinal Model for Long-Term Infection of Cryptosporidium parvum. Infect Immun 85.

Ding, Q., Subramanian, I., Luckhardt, T. R., Che, P., Waghray, M., Zhao, X., Bone, N., Kurundkar, A. R., Hecker, L., Hu, M., et al. (2017). Focal Adhesion Kinase Signaling Determines the Fate of Lung Epithelial Cells in Response to TGF-beta. Am J Physiol Lung Cell Mol Physiol, ajplung.00121.02016.

Dos Santos, A. F., Terra, L. F., Wailemann, R. A., Oliveira, T. C., Gomes, V. M., Mineiro, M. F., Meotti, F. C., Bruni-Cardoso, A., Baptista, M. S., and Labriola, L. (2017). Methylene blue photodynamic therapy induces selective and massive cell death in human breast cancer cells. BMC Cancer 17, 194.

Dou, X. Q., and Feng, C. L. (2017). Amino Acids and Peptide-Based Supramolecular Hydrogels for Three-Dimensional Cell Culture. Adv Mater 29.

Drobnik, J., Pietrucha, K., Kudzin, M., Mader, K., Szymanski, J., and Szczepanowska, A. (2017). Comparison of various types of collagenous scaffolds applied for embryonic nerve cell culture. Biologicals 46, 74-80.

Duisit, J., Orlando, G., Debluts, D., Maistriaux, L., Xhema, D., de Bisthoven, Y. J., Galli, C., Peloso, A., Behets, C., Lengele, B., and Gianello, P. (2017). Decellularization of the Porcine Ear Generates a Biocompatible, Nonimmunogenic Extracellular Matrix Platform for Face Subunit Bioengineering. Ann Surg.

Dunlop, E. A., Johnson, C. E., Wiltshire, M., Errington, R. J., and Tee, A. R. (2017). Targeting protein homeostasis with nelfinavir/salinomycin dual therapy effectively induces death of mTORC1 hyperactive cells. Oncotarget.

Dutta, D., Heo, I., and Clevers, H. (2017). Disease Modeling in Stem Cell-Derived 3D Organoid Systems. Trends Mol Med.

Edgar, J. M., Robinson, M., and Willerth, S. M. (2017). Fibrin hydrogels induce mixed dorsal/ventral spinal neuron identities during differentiation of human induced pluripotent stem cells. Acta Biomater 51, 237-245.

Egawa, N., Shindo, A., Liang, A. C., Du, Y., Xing, C., Lo, E. K., Itoh, K., Kinoshita, H., Maki, T., Takahashi, R., et al. (2017). A novel three-dimensional culture system for oligodendrocyte precursor cells. Stem Cells Dev.

Egger, D., Spitz, S., Fischer, M., Handschuh, S., Glosmann, M., Friemert, B., Egerbacher, M., and Kasper, C. (2017). Application of a Parallelizable Perfusion Bioreactor for Physiologic 3D Cell Culture. Cells Tissues Organs.

Eliasson, P., Svensson, R. B., Giannopoulos, A., Eismark, C., Kjaer, M., Schjerling, P., and Heinemeier, K. M. (2017). Simvastatin and atorvastatin reduce the mechanical properties of tendon constructs in vitro and introduce catabolic changes in the gene expression pattern. PLoS One 12, e0172797.

Ellis, B. W., Acun, A., Can, U. I., and Zorlutuna, P. (2017). Human iPSC-derived myocardium-on-chip with capillary-like flow for personalized medicine. Biomicrofluidics 11, 024105.

Erndt-Marino, J. D., and Hahn, M. S. (2017). Probing the response of human osteoblasts following exposure to sympathetic neuron-like PC-12 cells in a 3D coculture model. J Biomed Mater Res A 105, 984-990.

Espinoza-Sanchez, N. A., Chimal-Ramirez, G. K., Mantilla, A., and Fuentes-Panana, E. M. (2017). IL-1beta, IL-8, and Matrix Metalloproteinases-1, -2, and -10 Are Enriched upon Monocyte-Breast Cancer Cell Cocultivation in a Matrigel-Based Three-Dimensional System. Front Immunol 8, 205.

Espuny-Camacho, I., Arranz, A. M., Fiers, M., Snellinx, A., Ando, K., Munck, S., Bonnefont, J., Lambot, L., Corthout, N., Omodho, L., et al. (2017). Hallmarks of Alzheimer's Disease in Stem-Cell-Derived Human Neurons Transplanted into Mouse Brain. Neuron 93, 1066-1081.e1068.

Fang, Y., and Eglen, R. M. (2017). Three-Dimensional Cell Cultures in Drug Discovery and Development. SLAS Discov, 2472555217696795.

Fiocco, L., Elsayed, H., Badocco, D., Pastore, P., Bellucci, D., Cannillo, V., Detsch, R., Boccaccini, A., and Bernardo, E. (2017). Direct ink writing of silica-bonded calcite scaffolds from preceramic polymers and fillers. Biofabrication.

Fong, E. L., Toh, T. B., Yu, H., and Chow, E. K. (2017). 3D Culture as a Clinically Relevant Model for Personalized Medicine. SLAS Technol, 2472630317697251.

Freeman, F. E., and McNamara, L. M. (2017). Endochondral Priming: A Developmental Engineering Strategy for Bone Tissue Regeneration. Tissue Eng Part B Rev 23, 128-141.

Fu, J., Fernandez, D., Ferrer, M., Titus, S. A., Buehler, E., and Lal-Nag, M. A. (2017). RNAi High-Throughput Screening of Single- and Multi-Cell-Type Tumor Spheroids: A Comprehensive Analysis in Two and Three Dimensions. SLAS Discov, 2472555217696796.

Furuhata, Y., Yoshitomi, T., Kikuchi, Y., Sakao, M., and Yoshimoto, K. (2017). Osteogenic Lineage Commitment of Adipose-Derived Stem Cells Is Predetermined by Three-Dimensional Cell Accumulation on Micropatterned Surface. ACS Appl Mater Interfaces.

Futrega, K., Atkinson, K., Lott, W. B., and Doran, M. R. (2017). Spheroid Coculture of Hematopoietic Stem/Progenitor Cells and Monolayer Expanded Mesenchymal Stem/Stromal Cells in Polydimethylsiloxane Microwells Modestly Improves In Vitro Hematopoietic Stem/Progenitor Cell Expansion. Tissue Eng Part C Methods 23, 200-218.

Gabbott, C. M., Zhou, Z. X., Han, G. X., and Sun, T. (2017). A novel scale-down cell culture and imaging design for the mechanistic insight of cell colonisation within porous substrate. J Microsc.

Gao, J., Tang, C., Elsawy, M. A., Smith, A. M., Miller, A. F., and Saiani, A. (2017). Controlling Self-Assembling Peptide Hydrogel Properties through Network Topology. Biomacromolecules 18, 826-834.

Gheibi, P., Son, K. J., Stybayeva, G., and Revzin, A. (2017). Harnessing endogenous signals from hepatocytes using a low volume multi-well plate. Integr Biol (Camb).

Giacomelli, E., Bellin, M., Sala, L., van Meer, B. J., Tertoolen, L. G., Orlova, V. V., and Mummery, C. L. (2017). Three-dimensional cardiac microtissues composed of cardiomyocytes and endothelial cells co-differentiated from human pluripotent stem cells. Development 144, 1008-1017.

Gibot, L., Galbraith, T., Bourland, J., Rogic, A., Skobe, M., and Auger, F. A. (2017). Tissue-engineered 3D human lymphatic microvascular network for in vitro studies of lymphangiogenesis. Nat Protoc 12, 1077-1088.

Gonzalez-Avalos, P., Murnseer, M., Deeg, J., Bachmann, A., Spatz, J., Dooley, S., Eils, R., and Gladilin, E. (2017). Quantification of substrate and cellular strains in stretchable 3D cell cultures: an experimental and computational framework. J Microsc.

Gonzalez-Fernandez, T., Sathy, B. N., Hobbs, C., Cunniffe, G. M., McCarthy, H. O., Dunne, N. J., Nicolosi, V., O'Brien, F. J., and Kelly, D. J. (2017). Mesenchymal Stem Cell Fate Following Non-viral Gene Transfection Strongly Depends on the Choice of Delivery Vector. Acta Biomater.

Govoni, M., Berardi, A., Muscari, C., Campardelli, R., Bonafe, F., Guarnieri, C., Reverchon, E., Giordano, E., Maffulli, N., and Della Porta, G. (2017). An engineered multiphase 3D microenvironment to ensure the controlled delivery of cyclic strain and hGDF-5 for the tenogenic commitment of hBMSCs. Tissue Eng Part A.

Gruber, H. E., Marrero, E., Ingram, J. A., Hoelscher, G. L., and Hanley, E. N., Jr. (2017). Constitutive expression of IL-22 in the human intervertebral disc and its reduction by exposure to pro-inflammatory cytokines in vitro. Biotech Histochem 92, 222-229.

Guduric, V., Metz, C., Siadous, R., Bareille, R., Levato, R., Engel, E., Fricain, J. C., Devillard, R., Luzanin, O., and Catros, S. (2017). Layer-by-layer bioassembly of cellularized polylactic acid porous membranes for bone tissue engineering. J Mater Sci Mater Med 28, 78.

Gugutkov, D., Awaja, F., Belemezova, K., Keremidarska, M., Krasteva, N., Kuyrkchiev, S., GallegoFerrer, G., Seker, S., Elcin, A. E., Elcin, Y. M., and Altankov, G. (2017). Osteogenic Differentiation of Mesenchymal Stem Cells using Hybrid Nanofibers with Different Configurations and Dimensionality. J Biomed Mater Res A.

Gurumurthy, B., Bierdeman, P. C., and Janorkar, A. V. (2017). Spheroid model for functional osteogenic evaluation of human adipose derived stem cells. J Biomed Mater Res A 105, 1230-1236.

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Reviews

Bartfeld, S., and Clevers, H. (2017). Stem cell-derived organoids and their application for medical research and patient treatment. J Mol Med (Berl).

Benmerzoug, S., and Quesniaux, V. F. (2017). Bioengineered 3D Models for Studying Human Cell-Tuberculosis Interactions. Trends Microbiol.

Dou, X. Q., and Feng, C. L. (2017). Amino Acids and Peptide-Based Supramolecular Hydrogels for Three-Dimensional Cell Culture. Adv Mater 29.

Dutta, D., Heo, I., and Clevers, H. (2017). Disease Modeling in Stem Cell-Derived 3D Organoid Systems. Trends Mol Med.

Fang, Y., and Eglen, R. M. (2017). Three-Dimensional Cell Cultures in Drug Discovery and Development. SLAS Discov, 2472555217696795.

Fong, E. L., Toh, T. B., Yu, H., and Chow, E. K. (2017). 3D Culture as a Clinically Relevant Model for Personalized Medicine. SLAS Technol, 2472630317697251.

Hill, D. R., and Spence, J. R. (2017). Gastrointestinal Organoids: Understanding the Molecular Basis of the Host-Microbe Interface. Cell Mol Gastroenterol Hepatol 3, 138-149.

Kim, Y. Y., Tamadon, A., and Ku, S. Y. (2017). Potential Use of Antiapoptotic Proteins and Noncoding RNAs for Efficient In Vitro Follicular Maturation and Ovarian Bioengineering. Tissue Eng Part B Rev 23, 142-158.

Lee, S. H., Shim, K. Y., Kim, B., and Sung, J. H. (2017). Hydrogel-Based Three-Dimensional Cell Culture for Organ-on-a-Chip Applications. Biotechnol Prog.