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Engineering Stem Cell Self-organization to Build Better Organoids
Open accessAbstract
Organoids form through self-organization processes in which initially homogeneous populations of stem cells spontaneously break symmetry and undergo in-vivo-like pattern formation and morphogenesis, though the processes controlling this are poorly characterized. While these in vitro self-organized tissues far exceed the microscopic and functional complexity obtained by current tissue engineering technologies, they are non-physiological in shape and size and have limited function and lifespan. Here, we discuss how engineering efforts for guiding stem-cell-based development at multiple stages can form the basis for the assembly of highly complex and rationally designed self-organizing multicellular systems with increased robustness and physiological relevance.
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Cites
Matrix elasticity directs stem cell lineage specification
Engler, A. J., Sen, S., Sweeney, H. L., & Discher, D. E. (2006) · Cell · doi:10.1016/j.cell.2006.06.044 · Cited by 13,915
The chemical basis of morphogenesis
Turing, A. M. (1952) · Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences · doi:10.1098/rstb.1952.0012 · Cited by 11,733
Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche
Sato, T., Vries, R. G., Snippert, H. J., van de Wetering, M., Barker, N., Stange, D. E., van Es, J. H., Abo, A., Kujala, P., Peters, P. J., et al. (2009) · Nature · doi:10.1038/nature07935 · Cited by 7,204
Role of YAP/TAZ in mechanotransduction
Dupont, S., Morsut, L., Aragona, M., Enzo, E., Giulitti, S., Cordenonsi, M., Zanconato, F., Le Digabel, J., Forcato, M., Bicciato, S., et al. (2011) · Nature · doi:10.1038/nature10137 · Cited by 5,979
Geometric Control of Cell Life and Death
Chen, C. S., Mrksich, M., Huang, S., Whitesides, G. M., & Ingber, D. E. (1997) · Science · doi:10.1126/science.276.5317.1425 · Cited by 4,657
Sato, T., Stange, D. E., Ferrante, M., Vries, R. G. J., van Es, J. H., van den Brink, S., van Houdt, W. J., Pronk, A., van Gorp, J., Siersema, P. D., et al. (2011) · Gastroenterology · doi:10.1053/j.gastro.2011.07.050 · Cited by 3,753
Bhatia, S. N., & Ingber, D. E. (2014) · Nature Biotechnology · doi:10.1038/nbt.2989 · Cited by 3,305
Modeling Development and Disease with Organoids
Clevers, H. (2016) · Cell · doi:10.1016/j.cell.2016.05.082 · Cited by 3,196
Organogenesis in a dish: Modeling development and disease using organoid technologies
Lancaster, M. A., & Knoblich, J. A. (2014) · Science · doi:10.1126/science.1247125 · Cited by 2,931
Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts
Sato, T., van Es, J. H., Snippert, H. J., Stange, D. E., Vries, R. G., van den Born, M., Barker, N., Shroyer, N. F., van de Wetering, M., & Clevers, H. (2011) · Nature · doi:10.1038/nature09637 · Cited by 2,510
Hydrogels with tunable stress relaxation regulate stem cell fate and activity
Chaudhuri, O., Gu, L., Klumpers, D., Darnell, M., Bencherif, S. A., Weaver, J. C., Huebsch, N., Lee, H.-P., Lippens, E., Duda, G. N., et al. (2016) · Nature Materials · doi:10.1038/nmat4489 · Cited by 2,443
Vascularized and functional human liver from an iPSC-derived organ bud transplant
Takebe, T., Sekine, K., Enomura, M., Koike, H., Kimura, M., Ogaeri, T., Zhang, R.-R., Ueno, Y., Zheng, Y.-W., Koike, N., et al. (2013) · Nature · doi:10.1038/nature12271 · Cited by 2,170
Self-organizing optic-cup morphogenesis in three-dimensional culture
Eiraku, M., Takata, N., Ishibashi, H., Kawada, M., Sakakura, E., Okuda, S., Sekiguchi, K., Adachi, T., & Sasai, Y. (2011) · Nature · doi:10.1038/nature09941 · Cited by 2,001
Directed differentiation of human pluripotent stem cells into intestinal tissue in vitro
Spence, J. R., Mayhew, C. N., Rankin, S. A., Kuhar, M. F., Vallance, J. E., Tolle, K., Hoskins, E. E., Kalinichenko, V. V., Wells, S. I., Zorn, A. M., et al. (2011) · Nature · doi:10.1038/nature09691 · Cited by 1,922
Rapid casting of patterned vascular networks for perfusable engineered three-dimensional tissues
Miller, J. S., Stevens, K. R., Yang, M. T., Baker, B. M., Nguyen, D.-H. T., Cohen, D. M., Toro, E., Chen, A. A., Galie, P. A., Yu, X., et al. (2012) · Nature Materials · doi:10.1038/nmat3357 · Cited by 1,917
Photodegradable Hydrogels for Dynamic Tuning of Physical and Chemical Properties
Kloxin, A. M., Kasko, A. M., Salinas, C. N., & Anseth, K. S. (2009) · Science · doi:10.1126/science.1169494 · Cited by 1,748
Lgr5+ve Stem Cells Drive Self-Renewal in the Stomach and Build Long-Lived Gastric Units In Vitro
Barker, N., Huch, M., Kujala, P., van de Wetering, M., Snippert, H. J., van Es, J. H., Sato, T., Stange, D. E., Begthel, H., van den Born, M., et al. (2010) · Cell Stem Cell · doi:10.1016/j.stem.2009.11.013 · Cited by 1,547
Self-formation of optic cups and storable stratified neural retina from human ESCs
Nakano, T., Ando, S., Takata, N., Kawada, M., Muguruma, K., Sekiguchi, K., Saito, K., Yonemura, S., Eiraku, M., & Sasai, Y. (2012) · Cell stem cell · doi:10.1016/j.stem.2012.05.009 · Cited by 1,447
Designer matrices for intestinal stem cell and organoid culture
Gjorevski, N., Sachs, N., Manfrin, A., Giger, S., Bragina, M. E., Ordóñez-Morán, P., Clevers, H., & Lutolf, M. P. (2016) · Nature · doi:10.1038/nature20168 · Cited by 1,426
Assembly of functionally integrated human forebrain spheroids
Birey, F., Andersen, J., Makinson, C. D., Islam, S., Wei, W., Huber, N., Fan, H. C., Metzler, K. R. C., Panagiotakos, G., Thom, N., et al. (2017) · Nature · doi:10.1038/nature22330 · Cited by 1,365
Scaffold-free vascular tissue engineering using bioprinting
Norotte, C., Marga, F. S., Niklason, L. E., & Forgacs, G. (2009) · Biomaterials · doi:10.1016/j.biomaterials.2009.06.034 · Cited by 1,339
Advanced maturation of human cardiac tissue grown from pluripotent stem cells
Ronaldson-Bouchard, K., Ma, S. P., Yeager, K., Chen, T., Song, L., Sirabella, D., Morikawa, K., Teles, D., Yazawa, M., & Vunjak-Novakovic, G. (2018) · Nature · doi:10.1038/s41586-018-0016-3 · Cited by 1,272
Progress and potential in organoid research
Rossi, G., Manfrin, A., & Lutolf, M. P. (2018) · Nature Reviews Genetics · doi:10.1038/s41576-018-0051-9 · Cited by 1,182
Engineering Customized Cell Sensing and Response Behaviors Using Synthetic Notch Receptors
Morsut, L., Roybal, K. T., Xiong, X., Gordley, R. M., Coyle, S. M., Thomson, M., & Lim, W. A. (2016) · Cell · doi:10.1016/j.cell.2016.01.012 · Cited by 1,000
Modelling human development and disease in pluripotent stem-cell-derived gastric organoids
McCracken, K. W., Catá, E. M., Crawford, C. M., Sinagoga, K. L., Schumacher, M., Rockich, B. E., Tsai, Y.-H., Mayhew, C. N., Spence, J. R., Zavros, Y., et al. (2014) · Nature · doi:10.1038/nature13863 · Cited by 980
Biowire: a platform for maturation of human pluripotent stem cell–derived cardiomyocytes
Nunes, S. S., Miklas, J. W., Liu, J., Aschar-Sobbi, R., Xiao, Y., Zhang, B., Jiang, J., Massé, S., Gagliardi, M., Hsieh, A., et al. (2013) · Nature Methods · doi:10.1038/nmeth.2524 · Cited by 952
Materials as stem cell regulators
Murphy, W. L., McDevitt, T. C., & Engler, A. J. (2014) · Nature Materials · doi:10.1038/nmat3937 · Cited by 947
Flow-enhanced vascularization and maturation of kidney organoids in vitro
Homan, K. A., Gupta, N., Kroll, K. T., Kolesky, D. B., Skylar-Scott, M., Miyoshi, T., Mau, D., Valerius, M. T., Ferrante, T., Bonventre, J. V., et al. (2019) · Nature Methods · doi:10.1038/s41592-019-0325-y · Cited by 939
Sustained in vitro intestinal epithelial culture within a Wnt-dependent stem cell niche
Ootani, A., Li, X., Sangiorgi, E., Ho, Q. T., Ueno, H., Toda, S., Sugihara, H., Fujimoto, K., Weissman, I. L., Capecchi, M. R., et al. (2009) · Nature Medicine · doi:10.1038/nm.1951 · Cited by 906
A method to recapitulate early embryonic spatial patterning in human embryonic stem cells
Warmflash, A., Sorre, B., Etoc, F., Siggia, E. D., & Brivanlou, A. H. (2014) · Nature Methods · doi:10.1038/nmeth.3016 · Cited by 885
Engineering of functional, perfusable 3D microvascular networks on a chip
Kim, S., Lee, H., Chung, M., & Jeon, N. L. (2013) · Lab on a Chip · doi:10.1039/c3lc41320a · Cited by 872
In vitro generation of human pluripotent stem cell derived lung organoids
Dye, B. R., Hill, D. R., Ferguson, M. A., Tsai, Y.-H., Nagy, M. S., Dyal, R., Wells, J. M., Mayhew, C. N., Nattiv, R., Klein, O. D., et al. (2015) · eLife · doi:10.7554/elife.05098 · Cited by 819
Guided self-organization and cortical plate formation in human brain organoids
Lancaster, M. A., Corsini, N. S., Wolfinger, S., Gustafson, E. H., Phillips, A. W., Burkard, T. R., Otani, T., Livesey, F. J., & Knoblich, J. A. (2017) · Nature Biotechnology · doi:10.1038/nbt.3906 · Cited by 783
Development of a primary human Small Intestine-on-a-Chip using biopsy-derived organoids
Kasendra, M., Tovaglieri, A., Sontheimer-Phelps, A., Jalili-Firoozinezhad, S., Bein, A., Chalkiadaki, A., Scholl, W., Zhang, C., Rickner, H., Richmond, C. A., et al. (2018) · Scientific Reports · doi:10.1038/s41598-018-21201-7 · Cited by 754
Barcellos-Hoff, M. H., Aggeler, J., Ram, T. G., & Bissell, M. J. (1989) · Development · doi:10.1242/dev.105.2.223 · Cited by 711
A fluid-to-solid jamming transition underlies vertebrate body axis elongation
Mongera, A., Rowghanian, P., Gustafson, H. J., Shelton, E., Kealhofer, D. A., Carn, E. K., Serwane, F., Lucio, A. A., Giammona, J., & Campàs, O. (2018) · Nature · doi:10.1038/s41586-018-0479-2 · Cited by 711
Isolation and in vitro expansion of human colonic stem cells
Jung, P., Sato, T., Merlos-Suárez, A., Barriga, F. M., Iglesias, M., Rossell, D., Auer, H., Gallardo, M., Blasco, M. A., Sancho, E., et al. (2011) · Nature Medicine · doi:10.1038/nm.2470 · Cited by 709
Xiang, Y., Tanaka, Y., Patterson, B., Kang, Y.-J., Govindaiah, G., Roselaar, N., Cakir, B., Kim, K.-Y., Lombroso, A. P., Hwang, S.-M., et al. (2017) · Cell Stem Cell · doi:10.1016/j.stem.2017.07.007 · Cited by 698
YAP/TAZ-Dependent Reprogramming of Colonic Epithelium Links ECM Remodeling to Tissue Regeneration
Yui, S., Azzolin, L., Maimets, M., Pedersen, M. T., Fordham, R. P., Hansen, S. L., Larsen, H. L., Guiu, J., Alves, M. R. P., Rundsten, C. F., et al. (2018) · Cell Stem Cell · doi:10.1016/j.stem.2017.11.001 · Cited by 681
Writing in the granular gel medium
Bhattacharjee, T., Zehnder, S. M., Rowe, K. G., Jain, S., Nixon, R. M., Sawyer, W. G., & Angelini, T. E. (2015) · Science Advances · doi:10.1126/sciadv.1500655 · Cited by 635
Workman, M. J., Mahe, M. M., Trisno, S., Poling, H. M., Watson, C. L., Sundaram, N., Chang, C.-F., Schiesser, J., Aubert, P., Stanley, E. G., et al. (2017) · Nature Medicine · doi:10.1038/nm.4233 · Cited by 626
del Corral, R. D., Olivera-Martinez, I., Goriely, A., Gale, E., Maden, M., & Storey, K. (2003) · Neuron · doi:10.1016/s0896-6273(03)00565-8 · Cited by 614
Tissue Geometry Determines Sites of Mammary Branching Morphogenesis in Organotypic Cultures
Nelson, C. M., VanDuijn, M. M., Inman, J. L., Fletcher, D. A., & Bissell, M. J. (2006) · Science · doi:10.1126/science.1131000 · Cited by 608
Building epithelial architecture: insights from three-dimensional culture models
O'Brien, L. E., Zegers, M. M. P., & Mostov, K. E. (2002) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm859 · Cited by 596
Self-organization and symmetry breaking in intestinal organoid development
Serra, D., Mayr, U., Boni, A., Lukonin, I., Rempfler, M., Challet Meylan, L., Stadler, M. B., Strnad, P., Papasaikas, P., Vischi, D., et al. (2019) · Nature · doi:10.1038/s41586-019-1146-y · Cited by 561
Synthetic hydrogels for human intestinal organoid generation and colonic wound repair
Cruz-Acuña, R., Quirós, M., Farkas, A. E., Dedhia, P. H., Huang, S., Siuda, D., García-Hernández, V., Miller, A. J., Spence, J. R., Nusrat, A., et al. (2017) · Nature Cell Biology · doi:10.1038/ncb3632 · Cited by 558
Blastocyst-like structures generated solely from stem cells
Rivron, N. C., Frias-Aldeguer, J., Vrij, E. J., Boisset, J.-C., Korving, J., Vivié, J., Truckenmüller, R. K., van Oudenaarden, A., van Blitterswijk, C. A., & Geijsen, N. (2018) · Nature · doi:10.1038/s41586-018-0051-0 · Cited by 530
Visualization of a short-range Wnt gradient in the intestinal stem-cell niche
Farin, H. F., Jordens, I., Mosa, M. H., Basak, O., Korving, J., Tauriello, D. V. F., de Punder, K., Angers, S., Peters, P. J., Maurice, M. M., et al. (2016) · Nature · doi:10.1038/nature16937 · Cited by 525
Multi-axial self-organization properties of mouse embryonic stem cells into gastruloids
Beccari, L., Moris, N., Girgin, M., Turner, D. A., Baillie-Johnson, P., Cossy, A.-C., Lutolf, M. P., Duboule, D., & Arias, A. M. (2018) · Nature · doi:10.1038/s41586-018-0578-0 · Cited by 511
Self-citationSelf-formation of functional adenohypophysis in three-dimensional culture
Suga, H., Kadoshima, T., Minaguchi, M., Ohgushi, M., Soen, M., Nakano, T., Takata, N., Wataya, T., Muguruma, K., Miyoshi, H., et al. (2011) · Nature · doi:10.1038/nature10637 · Cited by 498
hESC-Derived Thalamic Organoids Form Reciprocal Projections When Fused with Cortical Organoids
Xiang, Y., Tanaka, Y., Cakir, B., Patterson, B., Kim, K.-Y., Sun, P., Kang, Y.-J., Zhong, M., Liu, X., Patra, P., et al. (2019) · Cell Stem Cell · doi:10.1016/j.stem.2018.12.015 · Cited by 485
Cytosystems dynamics in self-organization of tissue architecture
Sasai, Y. (2013) · Nature · doi:10.1038/nature11859 · Cited by 483
Wylie, R. G., Ahsan, S., Aizawa, Y., Maxwell, K. L., Morshead, C. M., & Shoichet, M. S. (2011) · Nature Materials · doi:10.1038/nmat3101 · Cited by 480
van den Brink, S. C., Baillie-Johnson, P., Balayo, T., Hadjantonakis, A.-K., Nowotschin, S., Turner, D. A., & Martinez Arias, A. (2014) · Development · doi:10.1242/dev.113001 · Cited by 478
Programming self-organizing multicellular structures with synthetic cell-cell signaling
Toda, S., Blauch, L. R., Tang, S. K. Y., Morsut, L., & Lim, W. A. (2018) · Science · doi:10.1126/science.aat0271 · Cited by 470
Czerniecki, S. M., Cruz, N. M., Harder, J. L., Menon, R., Annis, J., Otto, E. A., Gulieva, R. E., Islas, L. V., Kim, Y. K., Tran, L. M., et al. (2018) · Cell Stem Cell · doi:10.1016/j.stem.2018.04.022 · Cited by 465
Vascularized and Complex Organ Buds from Diverse Tissues via Mesenchymal Cell-Driven Condensation
Takebe, T., Enomura, M., Yoshizawa, E., Kimura, M., Koike, H., Ueno, Y., Matsuzaki, T., Yamazaki, T., Toyohara, T., Osafune, K., et al. (2015) · Cell Stem Cell · doi:10.1016/j.stem.2015.03.004 · Cited by 457
Fully functional bioengineered tooth replacement as an organ replacement therapy
Ikeda, E., Morita, R., Nakao, K., Ishida, K., Nakamura, T., Takano-Yamamoto, T., Ogawa, M., Mizuno, M., Kasugai, S., & Tsuji, T. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0902944106 · Cited by 447
A photoreversible protein-patterning approach for guiding stem cell fate in three-dimensional gels
DeForest, C. A., & Tirrell, D. A. (2015) · Nature Materials · doi:10.1038/nmat4219 · Cited by 432
Spatiotemporal hydrogel biomaterials for regenerative medicine
Brown, T. E., & Anseth, K. S. (2017) · Chemical Society Reviews · doi:10.1039/c7cs00445a · Cited by 428
Emergence of Patterned Stem Cell Differentiation Within Multicellular Structures
Ruiz, S. A., & Chen, C. S. (2008) · Stem Cells · doi:10.1634/stemcells.2008-0432 · Cited by 415
McKinnon, D. D., Domaille, D. W., Cha, J. N., & Anseth, K. S. (2014) · Advanced Materials · doi:10.1002/adma.201303680 · Cited by 414
Next-Generation Regenerative Medicine: Organogenesis from Stem Cells in 3D Culture
Sasai, Y. (2013) · Cell Stem Cell · doi:10.1016/j.stem.2013.04.009 · Cited by 401
Fordham, R. P., Yui, S., Hannan, N. R. F., Soendergaard, C., Madgwick, A., Schweiger, P. J., Nielsen, O. H., Vallier, L., Pedersen, R. A., Nakamura, T., et al. (2013) · Cell Stem Cell · doi:10.1016/j.stem.2013.09.015 · Cited by 399
Hwang, Y.-S., Chung, B. G., Ortmann, D., Hattori, N., Moeller, H.-C., & Khademhosseini, A. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0905550106 · Cited by 397
Engineering biological structures of prescribed shape using self-assembling multicellular systems
Jakab, K., Neagu, A., Mironov, V., Markwald, R. R., & Forgacs, G. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0400164101 · Cited by 394
Fabrication of functional three-dimensional tissues by stacking cell sheets in vitro
Haraguchi, Y., Shimizu, T., Sasagawa, T., Sekine, H., Sakaguchi, K., Kikuchi, T., Sekine, W., Sekiya, S., Yamato, M., Umezu, M., et al. (2012) · Nature Protocols · doi:10.1038/nprot.2012.027 · Cited by 385
Wang, Y., Gunasekara, D. B., Reed, M. I., DiSalvo, M., Bultman, S. J., Sims, C. E., Magness, S. T., & Allbritton, N. L. (2017) · Biomaterials · doi:10.1016/j.biomaterials.2017.03.005 · Cited by 373
Generation of functional thyroid from embryonic stem cells
Antonica, F., Kasprzyk, D. F., Opitz, R., Iacovino, M., Liao, X.-H., Dumitrescu, A. M., Refetoff, S., Peremans, K., Manto, M., Kyba, M., et al. (2012) · Nature · doi:10.1038/nature11525 · Cited by 359
A Balance between Secreted Inhibitors and Edge Sensing Controls Gastruloid Self-Organization
Etoc, F., Metzger, J., Ruzo, A., Kirst, C., Yoney, A., Ozair, M. Z., Brivanlou, A. H., & Siggia, E. D. (2016) · Developmental Cell · doi:10.1016/j.devcel.2016.09.016 · Cited by 343
Generation of inner ear organoids containing functional hair cells from human pluripotent stem cells
Koehler, K. R., Nie, J., Longworth-Mills, E., Liu, X.-P., Lee, J., Holt, J. R., & Hashino, E. (2017) · Nature Biotechnology · doi:10.1038/nbt.3840 · Cited by 341
Specification of positional identity in forebrain organoids
Cederquist, G. Y., Asciolla, J. J., Tchieu, J., Walsh, R. M., Cornacchia, D., Resh, M. D., & Studer, L. (2019) · Nature Biotechnology · doi:10.1038/s41587-019-0085-3 · Cited by 332
McCauley, H. A., & Wells, J. M. (2017) · Development · doi:10.1242/dev.140731 · Cited by 322
Programmed assembly of 3-dimensional microtissues with defined cellular connectivity
Gartner, Z. J., & Bertozzi, C. R. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0900717106 · Cited by 315
In situ cell manipulation through enzymatic hydrogel photopatterning
Mosiewicz, K. A., Kolb, L., van der Vlies, A. J., Martino, M. M., Lienemann, P. S., Hubbell, J. A., Ehrbar, M., & Lutolf, M. P. (2013) · Nature Materials · doi:10.1038/nmat3766 · Cited by 308
A Localized Wnt Signal Orients Asymmetric Stem Cell Division in Vitro
Habib, S. J., Chen, B.-C., Tsai, F.-C., Anastassiadis, K., Meyer, T., Betzig, E., & Nusse, R. (2013) · Science · doi:10.1126/science.1231077 · Cited by 303
Turbulence Activates Platelet Biogenesis to Enable Clinical Scale Ex Vivo Production
Ito, Y., Nakamura, S., Sugimoto, N., Shigemori, T., Kato, Y., Ohno, M., Sakuma, S., Ito, K., Kumon, H., Hirose, H., et al. (2018) · Cell · doi:10.1016/j.cell.2018.06.011 · Cited by 296
Engineering Organoid Vascularization
Grebenyuk, S., & Ranga, A. (2019) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2019.00039 · Cited by 295
Artificial three-dimensional niches deconstruct pancreas development in vitro
Greggio, C., De Franceschi, F., Figueiredo-Larsen, M., Gobaa, S., Ranga, A., Semb, H., Lutolf, M., & Grapin-Botton, A. (2013) · Development · doi:10.1242/dev.096628 · Cited by 287
Self-citationGrowth of Epithelial Organoids in a Defined Hydrogel
Broguiere, N., Isenmann, L., Hirt, C., Ringel, T., Placzek, S., Cavalli, E., Ringnalda, F., Villiger, L., Züllig, R., Lehmann, R., et al. (2018) · Advanced Materials · doi:10.1002/adma.201801621 · Cited by 282
Biomaterials and engineered microenvironments to control YAP/TAZ-dependent cell behaviour
Brusatin, G., Panciera, T., Gandin, A., Citron, A., & Piccolo, S. (2018) · Nature Materials · doi:10.1038/s41563-018-0180-8 · Cited by 272
Functional lacrimal gland regeneration by transplantation of a bioengineered organ germ
Hirayama, M., Ogawa, M., Oshima, M., Sekine, Y., Ishida, K., Yamashita, K., Ikeda, K., Shimmura, S., Kawakita, T., Tsubota, K., et al. (2013) · Nature Communications · doi:10.1038/ncomms3497 · Cited by 261
Controlled-size embryoid body formation in concave microwell arrays
Choi, Y. Y., Chung, B. G., Lee, D. H., Khademhosseini, A., Kim, J.-H., & Lee, S.-H. (2010) · Biomaterials · doi:10.1016/j.biomaterials.2010.01.115 · Cited by 252
Fully functional hair follicle regeneration through the rearrangement of stem cells and their niches
Toyoshima, K.-E., Asakawa, K., Ishibashi, N., Toki, H., Ogawa, M., Hasegawa, T., Irié, T., Tachikawa, T., Sato, A., Takeda, A., et al. (2012) · Nature Communications · doi:10.1038/ncomms1784 · Cited by 250
Programmed synthesis of three-dimensional tissues
Todhunter, M. E., Jee, N. Y., Hughes, A. J., Coyle, M. C., Cerchiari, A., Farlow, J., Garbe, J. C., LaBarge, M. A., Desai, T. A., & Gartner, Z. J. (2015) · Nature Methods · doi:10.1038/nmeth.3553 · Cited by 247
3D niche microarrays for systems-level analyses of cell fate
Ranga, A., Gobaa, S., Okawa, Y., Mosiewicz, K., Negro, A., & Lutolf, M. P. (2014) · Nature Communications · doi:10.1038/ncomms5324 · Cited by 238
Self-citationSelf-organized amniogenesis by human pluripotent stem cells in a biomimetic implantation-like niche
Shao, Y., Taniguchi, K., Gurdziel, K., Townshend, R. F., Xue, X., Yong, K. M. A., Sang, J., Spence, J. R., Gumucio, D. L., & Fu, J. (2017) · Nature Materials · doi:10.1038/nmat4829 · Cited by 236
Ribes, V., & Briscoe, J. (2009) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a002014 · Cited by 232
Nonadhesive Alginate Hydrogels Support Growth of Pluripotent Stem Cell-Derived Intestinal Organoids
Capeling, M. M., Czerwinski, M., Huang, S., Tsai, Y.-H., Wu, A., Nagy, M. S., Juliar, B., Sundaram, N., Song, Y., Han, W. M., et al. (2019) · Stem Cell Reports · doi:10.1016/j.stemcr.2018.12.001 · Cited by 226
Neural tube morphogenesis in synthetic 3D microenvironments
Ranga, A., Girgin, M., Meinhardt, A., Eberle, D., Caiazzo, M., Tanaka, E. M., & Lutolf, M. P. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1603529113 · Cited by 221
3D Reconstitution of the Patterned Neural Tube from Embryonic Stem Cells
Meinhardt, A., Eberle, D., Tazaki, A., Ranga, A., Niesche, M., Wilsch-Bräuninger, M., Stec, A., Schackert, G., Lutolf, M., & Tanaka, E. M. (2014) · Stem Cell Reports · doi:10.1016/j.stemcr.2014.09.020 · Cited by 215
Self-citationMechanics-guided embryonic patterning of neuroectoderm tissue from human pluripotent stem cells
Xue, X., Sun, Y., Resto-Irizarry, A. M., Yuan, Y., Aw Yong, K. M., Zheng, Y., Weng, S., Shao, Y., Chai, Y., Studer, L., et al. (2018) · Nature Materials · doi:10.1038/s41563-018-0082-9 · Cited by 210
In Situ Patterning of Microfluidic Networks in 3D Cell‐Laden Hydrogels
Brandenberg, N., & Lutolf, M. P. (2016) · Advanced Materials · doi:10.1002/adma.201601099 · Cited by 192
Self-citationHair Follicle Development in Mouse Pluripotent Stem Cell-Derived Skin Organoids
Lee, J., Bӧscke, R., Tang, P.-C., Hartman, B. H., Heller, S., & Koehler, K. R. (2018) · Cell Reports · doi:10.1016/j.celrep.2017.12.007 · Cited by 187
Multiscale assembly for tissue engineering and regenerative medicine
Guven, S., Chen, P., Inci, F., Tasoglu, S., Erkmen, B., & Demirci, U. (2015) · Trends in Biotechnology · doi:10.1016/j.tibtech.2015.02.003 · Cited by 186
Wang, Y., Kim, R., Gunasekara, D. B., Reed, M. I., DiSalvo, M., Nguyen, D. L., Bultman, S. J., Sims, C. E., Magness, S. T., & Allbritton, N. L. (2018) · Cellular and Molecular Gastroenterology and Hepatology · doi:10.1016/j.jcmgh.2017.10.007 · Cited by 185
Decoding of position in the developing neural tube from antiparallel morphogen gradients
Zagorski, M., Tabata, Y., Brandenberg, N., Lutolf, M. P., Tkačik, G., Bollenbach, T., Briscoe, J., & Kicheva, A. (2017) · Science · doi:10.1126/science.aam5887 · Cited by 183
Self-citationCellular control of tissue architectures using a three-dimensional tissue fabrication technique
Tsuda, Y., Shimizu, T., Yamato, M., Kikuchi, A., Sasagawa, T., Sekiya, S., Kobayashi, J., Chen, G., & Okano, T. (2007) · Biomaterials · doi:10.1016/j.biomaterials.2007.08.002 · Cited by 180
Hill, D. R., Huang, S., Nagy, M. S., Yadagiri, V. K., Fields, C., Mukherjee, D., Bons, B., Dedhia, P. H., Chin, A. M., Tsai, Y.-H., et al. (2017) · eLife · doi:10.7554/elife.29132 · Cited by 175
Wells, J. M., & Spence, J. R. (2014) · Development · doi:10.1242/dev.097386 · Cited by 174
Liquid-like Solids Support Cells in 3D
Bhattacharjee, T., Gil, C. J., Marshall, S. L., Urueña, J. M., O’Bryan, C. S., Carstens, M., Keselowsky, B., Palmer, G. D., Ghivizzani, S., Gibbs, C. P., et al. (2016) · ACS Biomaterials Science & Engineering · doi:10.1021/acsbiomaterials.6b00218 · Cited by 165
Morphogen interpretation: concentration, time, competence, and signaling dynamics
Sagner, A., & Briscoe, J. (2017) · WIREs Developmental Biology · doi:10.1002/wdev.271 · Cited by 165
Guye, P., Ebrahimkhani, M. R., Kipniss, N. H., Velazquez, J. J., Schoenfeld, E., Kiani, S., Griffith, L. G., & Weiss, R. (2016) · Nature Communications · doi:10.1038/ncomms10243 · Cited by 162
Tewary, M., Ostblom, J., Prochazka, L., Zulueta-Coarasa, T., Shakiba, N., Fernandez-Gonzalez, R., & Zandstra, P. W. (2017) · Development · doi:10.1242/dev.149658 · Cited by 158
Perspective: The promise of multi-cellular engineered living systems
Kamm, R. D., Bashir, R., Arora, N., Dar, R. D., Gillette, M. U., Griffith, L. G., Kemp, M. L., Kinlaw, K., Levin, M. G., Martin, A. C., et al. (2018) · APL Bioengineering · doi:10.1063/1.5038337 · Cited by 156
Development-on-chip: in vitro neural tube patterning with a microfluidic device
Demers, C. J., Soundararajan, P., Chennampally, P., Cox, G. A., Briscoe, J., Collins, S. D., & Smith, R. L. (2016) · Development · doi:10.1242/dev.126847 · Cited by 149
Candiello, J., Grandhi, T. S. P., Goh, S. K., Vaidya, V., Lemmon-Kishi, M., Eliato, K. R., Ros, R., Kumta, P. N., Rege, K., & Banerjee, I. (2018) · Biomaterials · doi:10.1016/j.biomaterials.2018.05.031 · Cited by 146
Intestinal epithelial organoids fuse to form self-organizing tubes in floating collagen gels
Sachs, N., Tsukamoto, Y., Kujala, P., Peters, P. J., & Clevers, H. C. (2017) · Development · doi:10.1242/dev.143933 · Cited by 146
Self-Organization and Branching Morphogenesis of Primary Salivary Epithelial Cells
Wei, C., Larsen, M., Hoffman, M. P., & Yamada, K. M. (2007) · Tissue Engineering · doi:10.1089/ten.2006.0123 · Cited by 139
InVERT molding for scalable control of tissue microarchitecture
Stevens, K. R., Ungrin, M., Schwartz, R. E., Ng, S., Carvalho, B., Christine, K. S., Chaturvedi, R. R., Li, C. Y., Zandstra, P. W., Chen, C. S., et al. (2013) · Nature Communications · doi:10.1038/ncomms2853 · Cited by 137
Heemskerk, I., Burt, K., Miller, M., Chhabra, S., Guerra, M. C., Liu, L., & Warmflash, A. (2019) · eLife · doi:10.7554/elife.40526 · Cited by 135
Laurent, J., Blin, G., Chatelain, F., Vanneaux, V., Fuchs, A., Larghero, J., & Théry, M. (2017) · Nature Biomedical Engineering · doi:10.1038/s41551-017-0166-x · Cited by 120
Developmentally inspired human ‘organs on chips’
Ingber, D. E. (2018) · Development · doi:10.1242/dev.156125 · Cited by 120
Mechanically induced development and maturation of human intestinal organoids in vivo
Poling, H. M., Wu, D. X.-Y., Brown, N. E., Baker, M. L., Hausfeld, T. A., Huynh, N., Chaffron, S., Dunn, J., Hogan, S. P., Wells, J. M., et al. (2018) · Nature Biomedical Engineering · doi:10.1038/s41551-018-0243-9 · Cited by 114
Physical control of tissue morphogenesis across scales
Stooke‐Vaughan, G. A., & Campàs, O. (2018) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2018.09.002 · Cited by 114
Generation of stomach tissue from mouse embryonic stem cells
Noguchi, T.-A. K., Ninomiya, N., Sekine, M., Komazaki, S., Wang, P., Asashima, M., & Kurisaki, A. (2015) · Nature Cell Biology · doi:10.1038/ncb3200 · Cited by 110
Cachat, É., Liu, W., Martin, K., Yuan, X., Yin, H., Hohenstein, P., & Davies, J. A. (2016) · Scientific Reports · doi:10.1038/srep20664 · Cited by 95
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 87
A Modular Approach to Sensitized Two‐Photon Patterning of Photodegradable Hydrogels
Lunzer, M., Shi, L., Andriotis, O. G., Gruber, P., Marković, M., Thurner, P. J., Ossipov, D. A., Liska, R., & Ovsianikov, A. (2018) · Angewandte Chemie International Edition · doi:10.1002/anie.201808908 · Cited by 87
Understanding the Mechanobiology of Early Mammalian Development through Bioengineered Models
Vianello, S., & Lütolf, M. P. (2019) · Developmental Cell · doi:10.1016/j.devcel.2019.02.024 · Cited by 84
Single-cell genomics to guide human stem cell and tissue engineering
Camp, J. G., Wollny, D., & Treutlein, B. (2018) · Nature Methods · doi:10.1038/s41592-018-0113-0 · Cited by 82
The physics of organoids: a biophysical approach to understanding organogenesis
Dahl-Jensen, S., & Grapin-Botton, A. (2017) · Development · doi:10.1242/dev.143693 · Cited by 81
Kim, K.-S., Utoh, R., Ohashi, K., Kikuchi, T., & Okano, T. (2015) · Journal of Tissue Engineering and Regenerative Medicine · doi:10.1002/term.2102 · Cited by 81
3D high throughput screening and profiling of embryoid bodies in thermoformed microwell plates
Vrij, E., Espinoza, S., Heilig, M. A., Kolew, A., Schneider, M., van Blitterswijk, C., Truckenmüller, R. K., & Rivron, N. C. (2016) · Lab on a Chip · doi:10.1039/c5lc01499a · Cited by 77
Blin, G., Wisniewski, D., Picart, C., Théry, M., Pucéat, M., & Lowell, S. (2018) · Development · doi:10.1242/dev.166025 · Cited by 67
Bioinspired Hydrogels for 3D Organoid Culture
Blondel, D., & Lütolf, M. P. (2019) · CHIMIA International Journal for Chemistry · doi:10.2533/chimia.2019.81 · Cited by 67
Protein-engineered scaffolds for in vitro 3D culture of primary adult intestinal organoids
DiMarco, R. L., Dewi, R. E., Bernal, G., Kuo, C., & Heilshorn, S. C. (2015) · Biomaterials Science · doi:10.1039/c5bm00108k · Cited by 66
Directed Assembly and Development of Material‐Free Tissues with Complex Architectures
Vrij, E., Rouwkema, J., LaPointe, V. L. S., van Blitterswijk, C., Truckenmüller, R. K., & Rivron, N. C. (2016) · Advanced Materials · doi:10.1002/adma.201505723 · Cited by 65
A process engineering approach to increase organoid yield
Arora, N., Alsous, J. I., Guggenheim, J. W., Mak, M., Múnera, J. O., Wells, J. M., Kamm, R. D., Asada, H. H., Shvartsman, S. Y., & Griffith, L. G. (2017) · Development · doi:10.1242/dev.142919 · Cited by 64
Theory of mechanochemical patterning in biphasic biological tissues
Recho, P., Hallou, A., & Hannezo, É. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1813255116 · Cited by 64
Shin, H.-S., Hong, H. J., Koh, W., & Lim, J. (2018) · ACS Biomaterials Science & Engineering · doi:10.1021/acsbiomaterials.8b00894 · Cited by 60
Spheroid and Tissue Assembly via Click Chemistry in Microfluidic Flow
O’Brien, P. J., Luo, W., Rogozhnikov, D., Chen, J., & Yousaf, M. N. (2015) · Bioconjugate Chemistry · doi:10.1021/acs.bioconjchem.5b00376 · Cited by 51
Self-Organized Shuttling: Generating Sharp Dorsoventral Polarity in the Early Drosophila Embryo
Haskel‐Ittah, M., Ben‐Zvi, D., Branski-Arieli, M., Schejter, E. D., Shilo, B., & Barkai, N. (2012) · Cell · doi:10.1016/j.cell.2012.06.044 · Cited by 50
Mouse fetal intestinal organoids: new model to study epithelial maturation from suckling to weaning
Keuper-Navis, M., Garcia, T. M., Renes, I. B., Vermeulen, J. L. M., Meisner, S., Wildenberg, M. E., BRINK, G. R. V. D., van Elburg, R. M., & Muncan, V. (2018) · EMBO Reports · doi:10.15252/embr.201846221 · Cited by 50
Zhao, W., Loh, W., Droujinine, I. A., Teo, W., Kumar, N., Schäfer, S., Cui, C. H., Zhang, L., Sarkar, D., Karnik, R., et al. (2011) · The FASEB Journal · doi:10.1096/fj.10-178384 · Cited by 47
Programming Morphogenesis through Systems and Synthetic Biology
Velazquez, J. J., Su, E. Y., Cahan, P., & Ebrahimkhani, M. R. (2017) · Trends in biotechnology · doi:10.1016/j.tibtech.2017.11.003 · Cited by 47
Tissue mechanics regulates form, function, and dysfunction
Anlaş, A. A., & Nelson, C. M. (2018) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2018.05.012 · Cited by 47
Yajima, Y., Lee, C. N., Yamada, M., Utoh, R., & Seki, M. (2018) · Journal of Bioscience and Bioengineering · doi:10.1016/j.jbiosc.2018.01.022 · Cited by 45
Roles of Diffusion Dynamics in Stem Cell Signaling and Three-Dimensional Tissue Development
McMurtrey, R. J. (2017) · Stem Cells and Development · doi:10.1089/scd.2017.0066 · Cited by 38
Multiscale microenvironmental perturbation of pluripotent stem cell fate and self-organization
Tabata, Y., & Lutolf, M. P. (2017) · Scientific Reports · doi:10.1038/srep44711 · Cited by 37
Spatiotemporal mosaic self-patterning of pluripotent stem cells using CRISPR interference
Libby, A. R. G., Joy, D. A., So, P.-L., Mandegar, M. A., Muncie, J. M., Mendoza-Camacho, F. N., Weaver, V. M., Conklin, B. R., & McDevitt, T. C. (2018) · eLife · doi:10.7554/elife.36045 · Cited by 33
In Vitro Polarization of Colonoids to Create an Intestinal Stem Cell Compartment
Attayek, P. J., Ahmad, A. A., Wang, Y., Williamson, I., Sims, C. E., Magness, S. T., & Allbritton, N. L. (2016) · PLoS ONE · doi:10.1371/journal.pone.0153795 · Cited by 31
Cerchiari, A. E., Garbe, J. C., Todhunter, M. E., Jee, N. Y., Pinney, J. R., LaBarge, M. A., Desai, T. A., & Gartner, Z. J. (2014) · Tissue Engineering Part C Methods · doi:10.1089/ten.tec.2014.0450 · Cited by 25
Photopatterning of Multifunctional Hydrogels to Direct Adult Neural Precursor Cells
Tsurkan, M. V., Wetzel, R., Pérez‐Hernández, H. R., Chwalek, K., Kozlova, A., Freudenberg, U., Kempermann, G., Zhang, Y., Lasagni, A. F., & Werner, C. (2014) · Advanced Healthcare Materials · doi:10.1002/adhm.201400395 · Cited by 23
Functional ectodermal organ regeneration as the next generation of organ replacement therapy
Ikeda, E., Ogawa, M., Takeo, M., & Tsuji, T. (2019) · Open Biology · doi:10.1098/rsob.190010 · Cited by 15
Javaherian, S., D’Arcangelo, E., Slater, B., Zulueta-Coarasa, T., Fernández‐González, R., & McGuigan, A. P. (2015) · Integrative Biology · doi:10.1039/c4ib00272e · Cited by 12
Author response: In vitro generation of human pluripotent stem cell derived lung organoids
Dye, B. R., Hill, D. R., Ferguson, M. A. H., Tsai, Y.-H., Nagy, M. S., Dyal, R., Wells, J. M., Mayhew, C. N., Nattiv, R., Klein, O. D., et al. (2015) · eLife · doi:10.7554/elife.05098.029 · Cited by 7
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Metadata
- Authors
- Brassard, J. A., & Lutolf, M. P.
- Venue
- Cell Stem Cell
- Publisher
- Elsevier BV
- Published
- 2019-06
- Volume
- 24
- Issue
- 6
- Pages
- 860-876
- ISSN
- 1875-9777 (ISSN-L)
- 1934-5909
- OpenAlex
- W2948284511
- Cited by
- 373
- References
- 147
- FWCI
- 14.43
- Type
- journal article
- Language
- en
- Open access
- bronze
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Contains information from the Semantic Scholar Academic Graph Datasets, made available under the ODC Attribution License (ODC-BY 1.0).
Semantic Scholar’s data is described in: Kinney, R., et al. (2023). The Semantic Scholar Open Data Platform. arXiv:2301.10140.