Homogeneous and organized differentiation within embryoid bodies induced by microsphere-mediated delivery of small molecules
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Cell specification and tissue formation during embryonic development are precisely controlled by the local concentration and temporal presentation of morphogenic factors. Similarly, pluripotent embryonic stem cells can be induced to differentiate in vitro into specific phenotypes in response to morphogen treatment. Embryonic stem cells (ESCs) are commonly differentiated as 3D spheroids referred to as embryoid bodies (EBs); however, differentiation of cells within EBs is typically heterogeneous and disordered. In this study, we demonstrate that in contrast to soluble morphogen treatment, delivery of morphogenic factors directly within EB microenvironments in a spatiotemporally controlled manner using polymer microspheres yields homogeneous, synchronous and organized ESC differentiation. Degradable PLGA microspheres releasing retinoic acid were incorporated directly within EBs and induced the formation of cystic spheroids uniquely resembling the phenotype and structure of early streak mouse embryos (E6.75), with an exterior of FOXA2+ visceral endoderm enveloping an epiblast-like layer of OCT4+ cells. These results demonstrate that controlled morphogen presentation to stem cells using degradable microspheres more efficiently directs cell differentiation and tissue formation than simple soluble delivery methods and presents a unique route to study the spatiotemporal effects of morphogenic factors on embryonic developmental processes in vitro.
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The spatiotemporal release of RA by polymeric microparticles incorporated within embryonic bodies, derived from human embryonic stem cells, was reported to induce cell differentiation and tissue formation resembling the phenotype and structure of early human embryos.
“The spatiotemporal release of RA by polymeric microparticles incorporated within embryonic bodies, derived from human embryonic stem cells, was reported to induce cell differentiation and tissue formation resembling the phenotype and structure of early human embryos7.”
From Advances and challenges in retinoid delivery systems in regenerative and therapeutic medicine (2020) · cites this paper as [7]
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Cites
Embryonic Stem Cell Lines Derived from Human Blastocysts
Thomson, J. A., Itskovitz‐Eldor, J., Shapiro, S. S., Waknitz, M. A., Swiergiel, J. J., Marshall, V. S., & Jones, J. M. (1998) · Science · doi:10.1126/science.282.5391.1145 · Cited by 15,947 · see citing works
In silico prediction of protein-protein interactions in human macrophages
Souiai, O., Guerfali, F. Z., Miled, S. B., Brun, C., & Benkahla, A. (2014) · BMC Research Notes · doi:10.1186/1756-0500-7-157 · Cited by 10,785 · see citing works
Significance analysis of microarrays applied to the ionizing radiation response
Tusher, V. G., Tibshirani, R., & Chu, G. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.091062498 · Cited by 10,568 · see citing works
Establishment in culture of pluripotential cells from mouse embryos
Evans, M. J., & Kaufman, M. H. (1981) · Nature · doi:10.1038/292154a0 · Cited by 8,623 · see citing works
Martin, G. R. (1981) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.78.12.7634 · Cited by 5,756 · see citing works
Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function
Chiang, C. C., Litingtung, Y., Lee, E., Young, K. E., Corden, J. L., Westphal, H., & Beachy, P. A. (1996) · Nature · doi:10.1038/383407a0 · Cited by 3,062 · see citing works
Myeloid leukaemia inhibitory factor maintains the developmental potential of embryonic stem cells
Williams, R. L., Hilton, D. J., Pease, S., Willson, T. A., Stewart, C. L., Gearing, D. P., Wagner, E. F., Metcalf, D., Nicola, N. A., & Gough, N. M. (1988) · Nature · doi:10.1038/336684a0 · Cited by 1,997 · see citing works
Doetschman, T., Eistetter, H. R., Katz, M., Schmidt, W., & Kemler, R. (1985) · Development · doi:10.1242/dev.87.1.27 · Cited by 1,962 · see citing works
Bone morphogenetic protein-4 is required for mesoderm formation and patterning in the mouse.Preprint
Winnier, G. E., Blessing, M., Labosky, P. A., & Hogan, B. L. M. (1995) · Genes & Development · doi:10.1101/gad.9.17.2105 · Cited by 1,789 · see citing works
Polymeric system for dual growth factor delivery
Richardson, T. P., Peters, M. C., Ennett, A. B., & Mooney, D. J. (2001) · Nature Biotechnology · doi:10.1038/nbt1101-1029 · Cited by 1,753 · see citing works
Itskovitz‐Eldor, J., Schuldiner, M., Kenyagin‐Karsenti, D., Eden, A., Yanuka, O., Amit, M., Soreq, H., & Benvenisty, N. (2000) · Molecular Medicine · doi:10.1007/bf03401776 · Cited by 1,502 · see citing works
Embryonic Stem Cells Express Neuronal Properties in Vitro
Bain, G., Kitchens, D. L., Yao, M., Huettner, J. E., & Gottlieb, D. I. (1995) · Developmental Biology · doi:10.1006/dbio.1995.1085 · Cited by 1,168 · see citing works
Schuldiner, M., Yanuka, O., Itskovitz‐Eldor, J., Melton, D. A., & Benvenisty, N. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.21.11307 · Cited by 1,132 · see citing works
Embryonic retinoic acid synthesis is essential for early mouse post-implantation development
Niederreither, K., Subbarayan, V., Dollé, P., & Chambon, P. (1999) · Nature Genetics · doi:10.1038/7788 · Cited by 1,111 · see citing works
Clonal analysis of epiblast fate during germ layer formation in the mouse embryo
Lawson, K. A., Meneses, J. J., & Pedersen, R. A. (1991) · Development · doi:10.1242/dev.113.3.891 · Cited by 881 · see citing works
Palmieri, S. L., Peter, W. K., Hess, H., & Schöler, H. R. (1994) · Developmental Biology · doi:10.1006/dbio.1994.1312 · Cited by 617 · see citing works
Nodal signalling in the epiblast patterns the early mouse embryo
Brennan, J., Lu, C. C., Norris, D. P., Rodríguez, T. A., Beddington, R. S. P., & Robertson, E. J. (2001) · Nature · doi:10.1038/35082103 · Cited by 551 · see citing works
Generation of purified neural precursors from embryonic stem cells by lineage selection
Li, M., Pevny, L., Lovell-Badge, R. H., & Smith, A. G. (1998) · Current Biology · doi:10.1016/s0960-9822(98)70399-9 · Cited by 461 · see citing works
In vitro differentiation of embryonic stem cells into glial cells and functional neurons
Fraichard, A., Chassande, O., Bilbaut, G., Dehay, C., Savatier, P., & Samarut, J. (1995) · Journal of Cell Science · doi:10.1242/jcs.108.10.3181 · Cited by 420 · see citing works
Retinoic acid synthesis and hindbrain patterning in the mouse embryo
Niederreither, K., Vermot, J., Schuhbaur, B., Chambon, P., & Dollé, P. (2000) · Development · doi:10.1242/dev.127.1.75 · Cited by 378 · see citing works
Vallier, L., Reynolds, D. S., & Pedersen, R. A. (2004) · Developmental Biology · doi:10.1016/j.ydbio.2004.08.031 · Cited by 350 · see citing works
Okada, Y., Shimazaki, T., Sobue, G., & Okano, H. (2004) · Developmental Biology · doi:10.1016/j.ydbio.2004.07.038 · Cited by 333 · see citing works
Ciruna, B. G., Schwartz, L., Harpal, K., Yamaguchi, T. P., & Rossant, J. (1997) · Development · doi:10.1242/dev.124.14.2829 · Cited by 328 · see citing works
Dufort, D., Schwartz, L., Harpal, K., & Rossant, J. (1998) · Development · doi:10.1242/dev.125.16.3015 · Cited by 327 · see citing works
A role for chemistry in stem cell biology
Ding, S., & Schultz, P. G. (2004) · Nature Biotechnology · doi:10.1038/nbt987 · Cited by 310 · see citing works
Primitive streak formation in mice is preceded by localized activation of Brachyury and Wnt3
Rivera‐Pérez, J. A., & Magnuson, T. (2005) · Developmental Biology · doi:10.1016/j.ydbio.2005.09.012 · Cited by 293 · see citing works
Rathjen, J., Lake, J.-A., Bettess, M. D., Washington, J. M., Chapman, G., & Rathjen, P. D. (1999) · Journal of Cell Science · doi:10.1242/jcs.112.5.601 · Cited by 292 · see citing works
Engineering the embryoid body microenvironment to direct embryonic stem cell differentiation
Bratt‐Leal, A. M., Carpenedo, R. L., & McDevitt, T. C. (2009) · Biotechnology Progress · doi:10.1002/btpr.139 · Cited by 272 · see citing works
Self-citationComplex Regulation of cyp26a1 Creates a Robust Retinoic Acid Gradient in the Zebrafish Embryo
White, R. J., Nie, Q. H., Lander, A. D., & Schilling, T. F. (2007) · PLoS Biology · doi:10.1371/journal.pbio.0050304 · Cited by 257 · see citing works
The effect of matrix composition of 3D constructs on embryonic stem cell differentiation
Battista, S., Guarnieri, D., Borselli, C., Zeppetelli, S., Borzacchiello, A., Mayol, L., Gerbasio, D., Keene, D. R., Ambrosio, L., & Netti, P. A. (2005) · Biomaterials · doi:10.1016/j.biomaterials.2005.04.003 · Cited by 245 · see citing works
Bain, G., Ray, W. J., Yao, M., & Gottlieb, D. I. (1996) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1996.0957 · Cited by 228 · see citing works
Burdsal, C. A., Damsky, C. H., & Pedersen, R. A. (1993) · Development · doi:10.1242/dev.118.3.829 · Cited by 207 · see citing works
Carpenedo, R. L., Sargent, C. Y., & McDevitt, T. C. (2007) · Stem Cells · doi:10.1634/stemcells.2006-0523 · Cited by 198 · see citing works
Self-citationDistinct roles for visceral endoderm during embryonic mouse development
Bielińska, M., Narita, N., & Wilson, D. B. (1999) · The International Journal of Developmental Biology · doi:10.1387/ijdb.10410899 · Cited by 182 · see citing works
Rathjen, J., Haines, B. P., Hudson, K. M., Nesci, A., Dunn, S., & Rathjen, P. D. (2002) · Development · doi:10.1242/dev.129.11.2649 · Cited by 162 · see citing works
Retinoic acid induces Pdx1-positive endoderm in differentiating mouse embryonic stem cells.
Micallef, S., Janes, M. E., Knezevic, K., Davis, R., Elefanty, A., & Stanley, E. (2005) · Diabetes · doi:10.2337/diabetes.54.2.301 · Cited by 150 · see citing works
Hidaka, K., Lee, J., Kim, H. S., Ihm, C. H., Iio, A., Ogawa, M., Nishikawa, S., Kodama, I., & Morisaki, T. (2003) · The FASEB Journal · doi:10.1096/fj.02-0104fje · Cited by 147 · see citing works
Li, X., Chen, Y., Schéele, S., Arman, E., Haffner‐Krausz, R., Ekblom, P., & Lonai, P. (2001) · The Journal of Cell Biology · doi:10.1083/jcb.153.4.811 · Cited by 139 · see citing works
Transplantation of brain cells assembled around a programmable synthetic microenvironment
Mahoney, M. J., & Saltzman, W. M. (2001) · Nature Biotechnology · doi:10.1038/nbt1001-934 · Cited by 134 · see citing works
Engineering the Stem Cell Microenvironment
Metallo, C. M., Mohr, J. C., Detzel, C. J., de Pablo, J. J., Wie, B. V., & Palecek, S. P. (2007) · Biotechnology Progress · doi:10.1021/bp060350a · Cited by 133 · see citing works
Pfister, S., Steiner, K. A., & Tam, P. (2007) · Gene Expression Patterns · doi:10.1016/j.modgep.2007.01.005 · Cited by 121 · see citing works
Differentiating Embryonic Stem Cells into Embryoid Bodies
Höpfl, G., Gassmann, M., & Desbaillets, I. (2004) · Humana Press eBooks · doi:10.1385/1-59259-741-6:079 · Cited by 114 · see citing works
Sachlos, E., & Auguste, D. T. (2008) · Biomaterials · doi:10.1016/j.biomaterials.2008.08.012 · Cited by 114 · see citing works
Preparation of poly(?-lactide-co-glycolide) microspheres encapsulating all-trans retinoic acid
Jeong, Y.-I. (2003) · International Journal of Pharmaceutics · doi:10.1016/s0378-5173(03)00207-2 · Cited by 94 · see citing works
Retinoic acid receptors interfere with the TGF-β/Smad signaling pathway in a ligand-specific manner
Pendaries, V., Verrecchia, F., Michel, S., & Mauviel, A. (2003) · Oncogene · doi:10.1038/sj.onc.1206913 · Cited by 82 · see citing works
Bruce, S. J., Gardiner, B., Burke, L. J., Gongora, M., Grimmond, S. M., & Perkins, A. C. (2007) · BMC Genomics · doi:10.1186/1471-2164-8-365 · Cited by 70 · see citing works
Cao, Z., Flanders, K. C., Bertolette, D. C., Lyakh, L. A., Würthner, J., Parks, W. T., Letterio, J. J., Ruscetti, F. W., & Roberts, A. B. (2002) · Blood · doi:10.1182/blood-2002-05-1549 · Cited by 66 · see citing works
Pachernı́k, J., Bryja, V., Ešner, M., Kubala, L., Dvořák, P., & Hampl, A. (2005) · Physiological Research · doi:10.33549/physiolres.930526 · Cited by 65 · see citing works
Human Embryoid Bodies Containing Nano‐ and Microparticulate Delivery Vehicles
Ferreira, L., Squier, T., Park, H., Choe, H. K., Kohane, D. S., & Langer, R. (2008) · Advanced Materials · doi:10.1002/adma.200702404 · Cited by 64 · see citing works
Goncalves, M. B., Boyle, J., Webber, D. J., Hall, S., Minger, S., & Corcoran, J. (2005) · Developmental Biology · doi:10.1016/j.ydbio.2004.10.015 · Cited by 55 · see citing works
Irioka, T., Watanabe, K., Mizusawa, H., Mizuseki, K., & Sasai, Y. (2004) · Developmental Brain Research · doi:10.1016/j.devbrainres.2004.10.004 · Cited by 45 · see citing works
O’Shea, K. S. (2001) · Blood Cells Molecules and Diseases · doi:10.1006/bcmd.2001.0435 · Cited by 25 · see citing works
Quinn, G., Ochiya, T., Terada, M., & Yoshida, T. (2000) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.2000.3602 · Cited by 19 · see citing works
ISHIKAWA, T., YAGYU, K., & Seguchi, H. (1986) · Journal of Electron Microscopy · doi:10.1093/oxfordjournals.jmicro.a050564 · Cited by 4 · see citing works
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Rossi, G., Manfrin, A., & Lutolf, M. P. (2018) · Nature Reviews Genetics · doi:10.1038/s41576-018-0051-9 · Cited by 1,182 · see citing works
Bioinspired Materials for Controlling Stem Cell Fate
Fisher, O. Z., Khademhosseini, A., Langer, R., & Peppas, N. A. (2009) · Accounts of Chemical Research · doi:10.1021/ar900226q · Cited by 315 · see citing works
Baraniak, P. R., & McDevitt, T. C. (2011) · Cell and Tissue Research · doi:10.1007/s00441-011-1215-5 · Cited by 273 · see citing works
Self-citationControlling Stem Cell Fate with Material Design
Marklein, R. A., & Burdick, J. A. (2009) · Advanced Materials · doi:10.1002/adma.200901055 · Cited by 242 · see citing works
Self-citationDiStefano, T. J., Chen, H. Y., Panebianco, C. J., Kaya, K. D., Brooks, M. J., Gieser, L. M., Morgan, N. Y., Pohida, T., & Swaroop, A. (2017) · Stem Cell Reports · doi:10.1016/j.stemcr.2017.11.001 · Cited by 195 · see citing works
Elbert, D. L. (2011) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2011.04.001 · Cited by 191 · see citing works
Bratt‐Leal, A. M., Carpenedo, R. L., Ungrin, M., Zandstra, P. W., & McDevitt, T. C. (2010) · Biomaterials · doi:10.1016/j.biomaterials.2010.08.113 · Cited by 164 · see citing works
Self-citationMass Transfer Limitations in Embryoid Bodies during Human Embryonic Stem Cell Differentiation
Winkle, A. P. V., Gates, I. D., & Kallos, M. S. (2012) · Cells Tissues Organs · doi:10.1159/000330691 · Cited by 156 · see citing works
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Valdoz, J. C., Johnson, B. C., Jacobs, D. J., Franks, N. A., Dodson, E. L., Sanders, C., Cribbs, C. G., & Ry, P. M. V. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222312690 · Cited by 153 · see citing works
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Anh, N. T. V., McKinney, J. M., Miller, T., Bongiorno, T., & McDevitt, T. C. (2014) · Acta Biomaterialia · doi:10.1016/j.actbio.2014.11.028 · Cited by 144 · see citing works
Self-citationAdvances and challenges in retinoid delivery systems in regenerative and therapeutic medicine
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Shao, Y., Sang, J., & Fu, J. (2015) · Biomaterials · doi:10.1016/j.biomaterials.2015.01.078 · Cited by 113 · see citing works
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Sargent, C. Y., Berguig, G. Y., Kinney, M. A., Hiatt, L. A., Carpenedo, R. L., Berson, R. E., & McDevitt, T. C. (2009) · Biotechnology and Bioengineering · doi:10.1002/bit.22578 · Cited by 109 · see citing works
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Self-citationLim, J. J., Hammoudi, T. M., Bratt‐Leal, A. M., Hamilton, S. K., Kepple, K. L., Bloodworth, N. C., McDevitt, T. C., & Temenoff, J. S. (2010) · Acta Biomaterialia · doi:10.1016/j.actbio.2010.10.009 · Cited by 103 · see citing works
Self-citationAbbasalizadeh, S., & Baharvand, H. (2013) · Biotechnology Advances · doi:10.1016/j.biotechadv.2013.08.009 · Cited by 95 · see citing works
Geometric Control of Cardiomyogenic Induction in Human Pluripotent Stem Cells
Bauwens, C. L., Song, H., Thavandiran, N., Ungrin, M., Massé, S., Nanthakumar, K., Séguin, C. A., & Zandstra, P. W. (2011) · Tissue Engineering Part A · doi:10.1089/ten.tea.2010.0563 · Cited by 93 · see citing works
Application of biomaterials to advance induced pluripotent stem cell research and therapy
Tong, Z.-X., Solanki, A., Hamilos, A. E., Levy, O., Wen, K., Yin, X., & Karp, J. (2015) · EMBO Journal · doi:10.15252/embj.201490756 · Cited by 97 · see citing works
Mechanical Control of Stem Cell Differentiation
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Kinney, M. A., Hookway, T. A., Wang, Y., & McDevitt, T. C. (2013) · Annals of Biomedical Engineering · doi:10.1007/s10439-013-0953-9 · Cited by 84 · see citing works
Self-citationIzumikawa, T., Sato, B., & Kitagawa, H. (2014) · Scientific Reports · doi:10.1038/srep03701 · Cited by 79 · see citing works
Differentiation Patterns of Embryonic Stem Cells in Two- versus Three-Dimensional Culture
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Zimmermann, J. A., Hettiaratchi, M. H., & McDevitt, T. C. (2016) · Stem Cells Translational Medicine · doi:10.5966/sctm.2016-0044 · Cited by 77 · see citing works
Self-citationA microparticle approach to morphogen delivery within pluripotent stem cell aggregates
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Self-citationPark, J. S., Yang, H. N., Woo, D. G., Jeon, S. Y., & Park, K.-H. (2010) · Biomaterials · doi:10.1016/j.biomaterials.2010.08.088 · Cited by 71 · see citing works
Magnetic manipulation and spatial patterning of multi-cellular stem cell aggregates
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Sart, S., Ma, T., & Li, Y. (2013) · Tissue Engineering Part A · doi:10.1089/ten.tea.2012.0690 · Cited by 64 · see citing works
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Kojima, N., Takeuchi, S., & Sakai, Y. (2012) · Biomaterials · doi:10.1016/j.biomaterials.2012.02.065 · Cited by 42 · see citing works
Design Principles for Pluripotent Stem Cell-Derived Organoid Engineering
Silva, T. P., Cotovio, J. P., Bekman, E., Carmo‐Fonseca, M., Cabral, J. M. S., & Fernandes, T. G. (2019) · Stem Cells International · doi:10.1155/2019/4508470 · Cited by 41 · see citing works
Amhare, A. F., Lei, J., Deng, H., Lv, Y., Han, J., & Zhang, L. (2020) · Journal of drug targeting · doi:10.1080/1061186x.2020.1833018 · Cited by 41 · see citing works
Microfluidic-based patterning of embryonic stem cells for in vitro development studies
Suri, S., Singh, A. K., Anh, N. T. V., Bratt‐Leal, A. M., McDevitt, T. C., & Lu, H. (2013) · Lab on a Chip · doi:10.1039/c3lc50663k · Cited by 40 · see citing works
Self-citationZeng, D., Ou, D., Wei, T., Ding, L., Liu, X., Hu, X., Li, X., & Zheng, Q. (2013) · BMC Cell Biology · doi:10.1186/1471-2121-14-5 · Cited by 39 · see citing works
Solorio, L. D., Vieregge, E. L., Dhami, C. D., & Alsberg, E. (2012) · Tissue Engineering Part B Reviews · doi:10.1089/ten.teb.2012.0252 · Cited by 39 · see citing works
Soleas, J. P., Paz, A., Marcus, P., McGuigan, A. P., & Waddell, T. K. (2012) · BioMed Research International · doi:10.1155/2012/982971 · Cited by 39 · see citing works
Biomimetic materials design for cardiac tissue regeneration
Dunn, D. A., Hodge, A. J., & Lipke, E. A. (2013) · Wiley Interdisciplinary Reviews Nanomedicine and Nanobiotechnology · doi:10.1002/wnan.1241 · Cited by 38 · see citing works
Huang, W.-C., Lin, C., Chiu, T.-W., & Chen, S. (2022) · ACS Applied Materials & Interfaces · doi:10.1021/acsami.2c11362 · Cited by 35 · see citing works
DNA microbeads for spatio-temporally controlled morphogen release within organoids
Afting, C., Walther, T., Drozdowski, O. M., Schlagheck, C., Schwarz, U. S., Wittbrodt, J., & Göpfrich, K. (2024) · Nature Nanotechnology · doi:10.1038/s41565-024-01779-y · Cited by 38 · see citing works
Nguyen, A. H., Wang, Y., White, D. E., Platt, M. O., & McDevitt, T. C. (2015) · Biomaterials · doi:10.1016/j.biomaterials.2015.10.043 · Cited by 34 · see citing works
Self-citationQutachi, O., Shakesheff, K. M., & Buttery, L. D. K. (2013) · Journal of Controlled Release · doi:10.1016/j.jconrel.2013.02.029 · Cited by 34 · see citing works
p120 Catenin-Mediated Stabilization of E-Cadherin Is Essential for Primitive Endoderm Specification
Pieters, T., Goossens, S., Haenebalcke, L., Andries, V., Stryjewska, A., Rycke, R. M. D., Lemeire, K., Hochepied, T., Huylebroeck, D., Berx, G., et al. (2016) · PLoS Genetics · doi:10.1371/journal.pgen.1006243 · Cited by 34 · see citing works
Cryopreservation of pluripotent stem cell aggregates in defined protein‐free formulation
Sart, S., Ma, T., & Li, Y. (2013) · Biotechnology progress (Print) · doi:10.1002/btpr.1653 · Cited by 38 · see citing works
Context Clues: The Importance of Stem Cell–Material Interactions
Khalil, A. S., Xie, A. W., & Murphy, W. L. (2013) · ACS Chemical Biology · doi:10.1021/cb400801m · Cited by 33 · see citing works
Progress and Prospects for Stem Cell Engineering
Ashton, R. S., Keung, A. J., Peltier, J., & Schaffer, D. V. (2011) · Annual Review of Chemical and Biomolecular Engineering · doi:10.1146/annurev-chembioeng-061010-114105 · Cited by 32 · see citing works
Esfandiari, F., Ashtiani, M. K., Tabar, M. S., Saber, M., Daemi, H., Ghanian, M. H., Shahverdi, A., & Baharvand, H. (2016) · Macromolecular Bioscience · doi:10.1002/mabi.201600284 · Cited by 32 · see citing works
Design Approaches for Generating Organ Constructs
Xia, Y. F., & Belmonte, J. C. I. (2019) · Cell stem cell · doi:10.1016/j.stem.2019.05.016 · Cited by 32 · see citing works
Controlled embryoid body formation via surface modification and avidin–biotin cross-linking
Gothard, D., Roberts, S. J., Shakesheff, K. M., & Buttery, L. D. K. (2009) · Cytotechnology · doi:10.1007/s10616-010-9255-3 · Cited by 31 · see citing works
Targeted Delivery of Bioactive Molecules for Vascular Intervention and Tissue Engineering
Strobel, H. A., Qendro, E. I., Alsberg, E., & Rolle, M. W. (2018) · Frontiers in Pharmacology · doi:10.3389/fphar.2018.01329 · Cited by 32 · see citing works
Gomez, J. C., Edgar, J. M., Agbay, A. M., Bibault, E., Montgomery, A., Mohtaram, N. K., & Willerth, S. M. (2015) · Cellular and Molecular Bioengineering · doi:10.1007/s12195-015-0401-z · Cited by 29 · see citing works
Agbay, A. M., la Vega, L. D., Nixon, G., & Willerth, S. M. (2018) · Biomedical Materials · doi:10.1088/1748-605x/aaaa77 · Cited by 29 · see citing works
Strobel, H. A., Dikina, A. D., Levi, K., Solorio, L. D., Alsberg, E., & Rolle, M. W. (2016) · Tissue Engineering Part A · doi:10.1089/ten.tea.2016.0260 · Cited by 28 · see citing works
Qi, H., Huang, G., Han, Y. L., Lin, W., Li, X., Wang, S., Lu, T. J., & Xu, F. (2016) · Critical Reviews in Biotechnology · doi:10.3109/07388551.2014.922917 · Cited by 26 · see citing works
Gupta, A., Kulkarni, S., Soman, S., Saha, M., Kulkarni, J., Rana, K., Dhas, N. L., Farhana, S. A., Tiyyagura, P. K., Pandey, A. P., et al. (2024) · International Journal of Pharmaceutics · doi:10.1016/j.ijpharm.2024.124687 · Cited by 26 · see citing works
Engineering biomaterials to control the neural differentiation of stem cells
Zimmermann, J. A., & Schaffer, D. V. (2019) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2019.05.007 · Cited by 26 · see citing works
Repina, N. A., Bao, X., Zimmermann, J. A., Joy, D. A., Kane, R. S., & Schaffer, D. V. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/665695 · Cited by 26 · see citing works
Zhang, Y., Mao, H., Gao, C., Li, S., Shuai, Q., Xu, J., Xu, K., Cao, L., Lang, R., Gu, Z., et al. (2016) · Advanced Healthcare Materials · doi:10.1002/adhm.201600114 · Cited by 25 · see citing works
Nsiah, B. A., Ahsan, T., Griffiths, S., Cooke, M. T., Nerem, R. M., & McDevitt, T. C. (2013) · Tissue Engineering Part A · doi:10.1089/ten.tea.2013.0243 · Cited by 25 · see citing works
Self-citationBuschke, D. G., Squirrell, J. M., Ansari, H., Smith, M. A., Rueden, C., Williams, J. C., Lyons, G. E., Kamp, T. J., Eliceiri, K. W., & Ogle, B. M. (2010) · Microscopy and Microanalysis · doi:10.1017/s1431927610000280 · Cited by 23 · see citing works
Functional Biomaterials for Controlling Stem Cell Differentiation
Phadke, A., Chang, C., & Varghese, S. (2010) · Studies in mechanobiology, tissue engineering and biomaterials · doi:10.1007/8415_2010_2 · Cited by 23 · see citing works
Wang, Y., Wu, J.-Y., Chou, P.-J., Chen, C., Wang, C.-Z., Ho, M.-L., Chang, J.-K., Yeh, M.-L., & Chen, C.-H. (2013) · Cytotherapy · doi:10.1016/j.jcyt.2013.07.015 · Cited by 22 · see citing works
Biomaterials and bioengineering to guide tissue morphogenesis in epithelial organoids
Jeon, E. Y., Sorrells, L., & Abaci, H. E. (2022) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2022.1038277 · Cited by 19 · see citing works
Application of Synthetic Biology to Regenerative Medicine
Cachat, É., & Davies, J. A. (2011) · Journal of Bioengineering and Biomedical Sciences · doi:10.4172/2155-9538.s2-003 · Cited by 19 · see citing works
la Vega, L. D., Karmirian, K., & Willerth, S. M. (2018) · Advanced Biosystems · doi:10.1002/adbi.201800133 · Cited by 19 · see citing works
Design Principles for Engineering of Tissues from Human Pluripotent Stem Cells
Rubio, O., Hookway, T. A., & McDevitt, T. C. (2016) · Current Stem Cell Reports · doi:10.1007/s40778-016-0030-z · Cited by 18 · see citing works
Self-citationControlled local presentation of matrix proteins in microparticle–laden cell aggregates
Bernard, A. B., Chapman, R. Z., & Anseth, K. S. (2013) · Biotechnology and Bioengineering · doi:10.1002/bit.25153 · Cited by 18 · see citing works
Ahmad, T., Shin, Y. M., Lee, J.-K., Shin, H. J., Perikamana, S. K. M., & Shin, H. (2018) · Journal of Industrial and Engineering Chemistry · doi:10.1016/j.jiec.2018.06.017 · Cited by 17 · see citing works
Khalil, A. S., Yu, X., Dang, P. N., Alsberg, E., & Murphy, W. L. (2019) · Acta Biomaterialia · doi:10.1016/j.actbio.2019.04.038 · Cited by 17 · see citing works
Fitzgerald, S. J., Cobb, J. S., & Janorkar, A. V. (2020) · Journal of Biomedical Materials Research Part B Applied Biomaterials · doi:10.1002/jbm.b.34631 · Cited by 17 · see citing works
Zhang, L., Wan, Z., Yuan, Z., Yang, J., Zhang, Y., Cai, Q., Huang, J., & Zhao, Y. (2022) · Journal of Materials Chemistry B · doi:10.1039/d2tb00359g · Cited by 14 · see citing works
1.4.6 The baryon octet and (Omega-)
Re’em, T. T., & Cohen, S. (2005) · Springer eBooks · doi:10.1007/10201111_8 · Cited by 14 · see citing works
A Novel Cell Penetrating Peptide for the Differentiation of Human Neural Stem Cells
Ma, W., Jin, G., Gehret, P. M., Chada, N. C., & Suh, W. H. (2018) · Biomolecules · doi:10.3390/biom8030048 · Cited by 13 · see citing works
Fosslien, E. (2009) · Dose-Response · doi:10.2203/dose-response.09-013.fosslien · Cited by 13 · see citing works
Fridley, K. M., Nair, R., & McDevitt, T. C. (2014) · Tissue Engineering Part C Methods · doi:10.1089/ten.tec.2013.0392 · Cited by 13 · see citing works
Self-citationGeuss, L. R., Wu, D. C., Ramamoorthy, D., Alford, C. D., & Suggs, L. J. (2014) · PLoS ONE · doi:10.1371/journal.pone.0113982 · Cited by 13 · see citing works
Systems Biology Characterization of Engineered Tissues
Rajagopalan, P., Kasif, S., & Murali, T. M. (2013) · Annual Review of Biomedical Engineering · doi:10.1146/annurev-bioeng-071811-150120 · Cited by 13 · see citing works
Current Technologies Based on the Knowledge of the Stem Cells Microenvironments
Mawad, D., Figtree, G. A., & Gentile, C. (2017) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-69194-7_13 · Cited by 13 · see citing works
Microfluidic sorting of microtissues
Buschke, D. G., Resto, P. J., Schumacher, N., Cox, B., Tallavajhula, A., Vivekanandan, A., Eliceiri, K. W., Williams, J. C., & Ogle, B. M. (2012) · Biomicrofluidics · doi:10.1063/1.3692765 · Cited by 12 · see citing works
Embryonic stem cells as a cell source for tissue engineering
Khademhosseini, A., Ashammakhi, N. A., Karp, J. M., Gerecht, S., Ferreira, L., Annabi, N., Darabi, M. A., Sirabella, D., Vunjak‐Novakovic, G., & Langer, R. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-818422-6.00027-7 · Cited by 12 · see citing works
Current strategies and opportunities to manufacture cells for modeling human lungs
Varma, R., Soleas, J. P., Waddell, T. K., Karoubi, G., & McGuigan, A. P. (2020) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2020.08.005 · Cited by 10 · see citing works
Guo, Q., Chen, J., Bu, Q., Zhang, J., Ruan, M. Q., Chen, X., Zhao, M., Tu, X., & Zhao, C. (2024) · Materials Today Bio · doi:10.1016/j.mtbio.2024.101111 · Cited by 10 · see citing works
Ferguson, R., & Subramanian, V. (2018) · Stem Cell Research · doi:10.1016/j.scr.2018.02.003 · Cited by 9 · see citing works
Biofunctional Hydrogels for Three-Dimensional Stem Cell Culture
Wilson, J. L., & McDevitt, T. C. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-802734-9.00022-6 · Cited by 8 · see citing works
Self-citationBiomaterials-based approaches to model embryogenesis
Spiteri, C., Caprettini, V., & Chiappini, C. (2020) · Biomaterials Science · doi:10.1039/d0bm01485k · Cited by 8 · see citing works
- Authors
- Carpenedo, R. L., Bratt-Leal, A. M., Marklein, R. A., Seaman, S. A., Bowen, N. J., McDonald, J. F., & McDevitt, T. C.
- Affiliations
- Georgia Institute of Technology (US)
- Corresponding author
- McDevitt, Todd C.
- Venue
- Biomaterials
- Publisher
- Elsevier BV
- Published
- 2009-05
- Volume
- 30
- Issue
- 13
- Pages
- 2507-2515
- ISSN
- 0142-9612 (ISSN-L)
- PMC
- PMC2921510
- OpenAlex
- W2071071731
- Cited by
- 133
- References
- 53
- Citations by year
- 2026: 1 · 2024: 5 · 2023: 3 · 2022: 5 · 2021: 3 · 2020: 9 · 2019: 6 · 2018: 9 · 2017: 4 · 2016: 6 · 2015: 7 · 2014: 10 · 2013: 18 · 2012: 14
- FWCI
- 6.30
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Biomaterials (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Science Foundation
- National Institute of General Medical Sciences (T32GM008433)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Pluripotent Stem Cells Research
- Health Sciences › Medicine › Surgery › Tissue Engineering and Regenerative Medicine
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- embryoid bodies, embryonic stem cell differentiation, polymer microspheres, PLGA microspheres, retinoic acid, visceral endoderm, epiblast-like cells, FOXA2, Oct4, embryonic development, tissue formation
- MeSH terms
- Animals, Cell Differentiation, Cells, Cultured, Gene Expression Regulation, Microscopy, Electron, Scanning, Microspheres, Tretinoin, Gene Expression Profiling, Mice, Embryonic Stem Cells
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