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Directed differentiation of human pluripotent stem cells into intestinal tissue in vitro
Open accessAbstract
Studies in embryonic development have guided successful efforts to direct the differentiation of human embryonic and induced pluripotent stem cells (PSCs) into specific organ cell types in vitro. For example, human PSCs have been differentiated into monolayer cultures of liver hepatocytes and pancreatic endocrine cells that have therapeutic efficacy in animal models of liver disease and diabetes, respectively. However, the generation of complex three-dimensional organ tissues in vitro remains a major challenge for translational studies. Here we establish a robust and efficient process to direct the differentiation of human PSCs into intestinal tissue in vitro using a temporal series of growth factor manipulations to mimic embryonic intestinal development. This involved activin-induced definitive endoderm formation, FGF/Wnt-induced posterior endoderm pattering, hindgut specification and morphogenesis, and a pro-intestinal culture system to promote intestinal growth, morphogenesis and cytodifferentiation. The resulting three-dimensional intestinal ‘organoids’ consisted of a polarized, columnar epithelium that was patterned into villus-like structures and crypt-like proliferative zones that expressed intestinal stem cell markers. The epithelium contained functional enterocytes, as well as goblet, Paneth and enteroendocrine cells. Using this culture system as a model to study human intestinal development, we identified that the combined activity of WNT3A and FGF4 is required for hindgut specification whereas FGF4 alone is sufficient to promote hindgut morphogenesis. Our data indicate that human intestinal stem cells form de novo during development. We also determined that NEUROG3, a pro-endocrine transcription factor that is mutated in enteric anendocrinosis, is both necessary and sufficient for human enteroendocrine cell development in vitro. PSC-derived human intestinal tissue should allow for unprecedented studies of human intestinal development and disease.
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Cites
Takahashi, K., & Yamanaka, S. (2006) · Cell · doi:10.1016/j.cell.2006.07.024 · Cited by 26,673
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
Kroon, E., Martinson, L. A., Kadoya, K., Bang, A. G., Kelly, O. G., Eliazer, S., Young, H., Richardson, M., Smart, N. G., Cunningham, J., et al. (2008) · Nature Biotechnology · doi:10.1038/nbt1393 · Cited by 1,843
Derivation of human embryonic stem cells in defined conditions
Ludwig, T. E., Levenstein, M. E., Jones, J. M., Berggren, W. T., Mitchen, E. R., Frane, J. L., Crandall, L. J., Daigh, C. A., Conard, K. R., Piekarczyk, M. S., et al. (2006) · Nature Biotechnology · doi:10.1038/nbt1177 · Cited by 1,114
Vertebrate Endoderm Development and Organ Formation
Zorn, A. M., & Wells, J. M. (2009) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.042308.113344 · Cited by 812
Self-citationFeeder-independent culture of human embryonic stem cells
Ludwig, T. E., Bergendahl, V., Levenstein, M. E., Yu, J., Probasco, M. D., & Thomson, J. A. (2006) · Nature Methods · doi:10.1038/nmeth902 · Cited by 681
Cited by
Wnt/β-Catenin Signaling, Disease, and Emerging Therapeutic Modalities
Nusse, R., & Clevers, H. (2017) · Cell · doi:10.1016/j.cell.2017.05.016 · Cited by 4,342
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
Human organoids: model systems for human biology and medicine
Kim, J., Koo, B.-K., & Knoblich, J. A. (2020) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-020-0259-3 · Cited by 2,187
Organoid modeling of the tumor immune microenvironment
Neal, J. T., Li, X., Zhu, J., Giangarra, V., Grzeskowiak, C. L., Ju, J., Liu, I. H., Chiou, S.-H., Salahudeen, A. A., Smith, A. R., et al. (2018) · Cell · doi:10.1016/j.cell.2018.11.021 · Cited by 1,556
Induced pluripotent stem cell technology: a decade of progress.
Shi, Y., Inoue, H., Wu, J. C., & Yamanaka, S. (2017) · Nature Reviews Drug Discovery · doi:10.1038/nrd.2016.245 · Cited by 1,525
Organoids as an in vitro model of human development and disease
Fatehullah, A., Tan, S. H., & Barker, N. (2016) · Nature Cell Biology · doi:10.1038/ncb3312 · Cited by 1,508
Hofer, M., & Lutolf, M. P. (2021) · Nature Reviews Materials · doi:10.1038/s41578-021-00279-y · Cited by 1,184
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
Growing Self-Organizing Mini-Guts from a Single Intestinal Stem Cell: Mechanism and Applications
Sato, T., & Clevers, H. (2013) · Science · doi:10.1126/science.1234852 · Cited by 1,170
Synthetic alternatives to Matrigel
Aisenbrey, E. A., & Murphy, W. L. (2020) · Nature Reviews Materials · doi:10.1038/s41578-020-0199-8 · Cited by 1,016
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
Self-citationA 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
Disease modeling in stem cell-derived 3D organoid systems
Dutta, D., Heo, I., & Clevers, H. (2017) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2017.02.007 · Cited by 838
Three-Dimensional Cell Cultures in Drug Discovery and Development
Fang, Y., & Eglen, R. M. (2017) · SLAS Discovery · doi:10.1177/1087057117696795 · Cited by 849
Three-dimensional organotypic culture: experimental models of mammalian biology and disease
Shamir, E. R., & Ewald, A. J. (2014) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3873 · Cited by 719
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
Self-citationCorrò, C., Novellasdemunt, L., & Li, V. S. W. (2020) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00120.2020 · Cited by 561
Modeling Steatohepatitis in Humans with Pluripotent Stem Cell-Derived Organoids
Ouchi, R., Togo, S., Kimura, M., Shinozawa, T., Koido, M., Koike, H., Thompson, W., Karns, R. A., Mayhew, C. N., McGrath, P. S., et al. (2019) · Cell Metabolism · doi:10.1016/j.cmet.2019.05.007 · Cited by 537
Self-citationEngineered In Vitro Disease Models
Benam, K. H., Dauth, S., Hassell, B., Herland, A., Jain, A., Jang, K.-J., Karalis, K., Kim, H. J., MacQueen, L., Mahmoodian, R., et al. (2015) · Annual Review of Pathology: Mechanisms of Disease · doi:10.1146/annurev-pathol-012414-040418 · Cited by 554
Screening out irrelevant cell-based models of disease
Horvath, P., Aulner, N., Bickle, M., Davies, A. M., Nery, E. D., Ebner, D., Montoya, M. C., Östling, P., Pietiäinen, V., Price, L. S., et al. (2016) · Nature Reviews Drug Discovery · doi:10.1038/nrd.2016.175 · Cited by 525
Alexeev, E. E., Lanis, J. M., Kao, D. J., Campbell, E. L., Kelly, C. J., Battista, K. D., Gerich, M. E., Jenkins, B. R., Walk, S. T., Kominsky, D. J., et al. (2018) · The American Journal of Pathology · doi:10.1016/j.ajpath.2018.01.011 · Cited by 532
Induced Pluripotent Stem Cells Meet Genome Editing
Hockemeyer, D., & Jaenisch, R. (2016) · Cell Stem Cell · doi:10.1016/j.stem.2016.04.013 · Cited by 499
“For one, it became evident that many protocols that were developed for the differentiation of hPSCs into functional tissue resulted in embryonic rather than adult human cell types (Bedada et al., 2015; Forster et al., 2014; Hrvatin et al., 2014; Spence et al., 2011; Takebe et al., 2013).”
BackgroundControlling Epithelial Polarity: A Human Enteroid Model for Host-Pathogen Interactions
Co, J. Y., Margalef-Català, M., Li, X., Mah, A. T., Kuo, C. J., Monack, D. M., & Amieva, M. R. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.01.108 · Cited by 488
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
Takebe, T., & Wells, J. M. (2019) · Science · doi:10.1126/science.aaw7567 · Cited by 417
Self-citationThe hope and the hype of organoid research
Huch, M., Knoblich, J. A., Lutolf, M. P., & Martinez-Arias, A. (2017) · Development · doi:10.1242/dev.150201 · Cited by 409
Sun, W., Starly, B., Daly, A. C., Burdick, J. A., Groll, J., Skeldon, G., Shu, W., Sakai, Y., Shinohara, M., Nishikawa, M., et al. (2020) · Biofabrication · doi:10.1088/1758-5090/ab5158 · Cited by 426
Crespo, M., Vilar, E., Tsai, S.-Y., Chang, K., Amin, S., Srinivasan, T., Zhang, T., Pipalia, N. H., Chen, H. J., Witherspoon, M., et al. (2017) · Nature Medicine · doi:10.1038/nm.4355 · Cited by 399
High-Fidelity Drug-Induced Liver Injury Screen Using Human Pluripotent Stem Cell–Derived Organoids
Shinozawa, T., Kimura, M., Cai, Y., Saiki, N., Yoneyama, Y., Ouchi, R., Koike, H., Maezawa, M., Zhang, R.-R., Dunn, A., et al. (2021) · Gastroenterology · doi:10.1053/j.gastro.2020.10.002 · Cited by 378
Kim, S., Min, S., Choi, Y. S., Jo, S.-H., Jung, J. H., Han, K., Kim, J., An, S., Ji, Y. W., Kim, Y.-G., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-29279-4 · Cited by 375
Orlova, V. V., van den Hil, F. E., Petrus-Reurer, S., Drabsch, Y., ten Dijke, P., & Mummery, C. L. (2014) · Nature Protocols · doi:10.1038/nprot.2014.102 · Cited by 365
Organoids in immunological research
Bar-Ephraim, Y. E., Kretzschmar, K., & Clevers, H. (2020) · Nature Reviews Immunology · doi:10.1038/s41577-019-0248-y · Cited by 361
Human disease models in drug development
Loewa, A., Feng, J. J., & Hedtrich, S. (2023) · Nature Reviews Bioengineering · doi:10.1038/s44222-023-00063-3 · Cited by 331
Modelling human hepato-biliary-pancreatic organogenesis from the foregut–midgut boundary
Koike, H., Iwasawa, K., Ouchi, R., Maezawa, M., Giesbrecht, K., Saiki, N., Ferguson, A., Kimura, M., Thompson, W. L., Wells, J. M., et al. (2019) · Nature · doi:10.1038/s41586-019-1598-0 · Cited by 325
Self-citationMcCauley, H. A., & Wells, J. M. (2017) · Development · doi:10.1242/dev.140731 · Cited by 322
Self-citationBuilding consensus on definition and nomenclature of hepatic, pancreatic, and biliary organoids
Marsee, A., Roos, F. J. M., Verstegen, M. M. A., Marsee, A., Roos, F., Verstegen, M., Clevers, H., Vallier, L., Takebe, T., Huch, M., et al. (2021) · Cell Stem Cell · doi:10.1016/j.stem.2021.04.005 · Cited by 310
Multi-lineage human iPSC-derived platforms for disease modeling and drug discovery
Sharma, A., Sances, S., Workman, M. J., & Svendsen, C. N. (2020) · Cell Stem Cell · doi:10.1016/j.stem.2020.02.011 · Cited by 296
Phenotypic landscape of intestinal organoid regeneration
Lukonin, I., Serra, D., Challet Meylan, L., Volkmann, K., Baaten, J., Zhao, R., Meeusen, S., Colman, K., Maurer, F., Stadler, M. B., et al. (2020) · Nature · doi:10.1038/s41586-020-2776-9 · Cited by 283
Growth 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
Cellular and epigenetic drivers of stem cell ageing
Ermolaeva, M., Neri, F., Ori, A., & Rudolph, K. L. (2018) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-018-0020-3 · Cited by 272
Modeling of fibrotic lung disease using 3D organoids derived from human pluripotent stem cells
Strikoudis, A., Cieślak, A., Loffredo, L., Chen, Y.-W., Patel, N., Saqi, A., Lederer, D. J., & Snoeck, H.-W. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.05.077 · Cited by 242
Workman, M. J., Gleeson, J. P., Troisi, E. J., Estrada, H. Q., Kerns, S. J., Hinojosa, C. D., Hamilton, G. A., Targan, S. R., Svendsen, C. N., & Barrett, R. J. (2018) · Cellular and Molecular Gastroenterology and Hepatology · doi:10.1016/j.jcmgh.2017.12.008 · Cited by 246
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
Self-citationPérez-González, C., Ceada, G., Greco, F., Matejčić, M., Gómez-González, M., Castro, N., Menendez, A., Kale, S., Krndija, D., Clark, A. G., et al. (2021) · Nature Cell Biology · doi:10.1038/s41556-021-00699-6 · Cited by 225
Organs-on-a-chip: a new tool for drug discovery
Polini, A., Prodanov, L., Bhise, N. S., Manoharan, V., Dokmeci, M. R., & Khademhosseini, A. (2014) · Expert Opinion on Drug Discovery · doi:10.1517/17460441.2014.886562 · Cited by 223
A Roadmap for Human Liver Differentiation from Pluripotent Stem Cells
Ang, L. T., Tan, A. K. Y., Autio, M. I., Goh, S. H., Choo, S. H., Lee, K. L., Tan, J., Pan, B., Lee, J. J. H., Lum, J. J., et al. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.01.087 · Cited by 220
Bioengineering Approaches for the Advanced Organoid Research
Yi, S. A., Zhang, Y., Rathnam, C., Pongkulapa, T., & Lee, K. (2021) · Advanced Materials · doi:10.1002/adma.202007949 · Cited by 218
Drug discovery through stem cell-based organoid models
Ranga, A., Gjorevski, N., & Lutolf, M. P. (2014) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2014.02.006 · Cited by 195
A nomenclature for intestinal in vitro cultures
Stelzner, M., Helmrath, M., Dunn, J. C. Y., Henning, S. J., Houchen, C. W., Kuo, C., Lynch, J., Li, L., Magness, S. T., Martin, M. G., et al. (2012) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00493.2011 · Cited by 195
Applications of organoids for cancer biology and precision medicine
Lo, Y.-H., Karlsson, K., & Kuo, C. J. (2020) · Nature Cancer · doi:10.1038/s43018-020-0102-y · Cited by 182
Baker, M. (2011) · Nature · doi:10.1038/471661a · Cited by 188
Human enteroids as an ex-vivo model of host–pathogen interactions in the gastrointestinal tract
Foulke-Abel, J., In, J., Kovbasnjuk, O., Zachos, N. C., Ettayebi, K., Blutt, S. E., Hyser, J. M., Zeng, X.-L., Crawford, S. E., Broughman, J. R., et al. (2014) · Experimental Biology and Medicine · doi:10.1177/1535370214529398 · Cited by 179
Finkbeiner, S. R., Freeman, J. J., Wieck, M. M., El-Nachef, W., Altheim, C. H., Tsai, Y.-H., Huang, S., Dyal, R., White, E. S., Grikscheit, T. C., et al. (2015) · Biology Open · doi:10.1242/bio.013235 · Cited by 174
Self-citationPEG-4MAL hydrogels for human organoid generation, culture, and in vivo delivery
Cruz-Acuña, R., Quirós, M., Huang, S., Siuda, D., Spence, J. R., Nusrat, A., & García, A. J. (2018) · Nature Protocols · doi:10.1038/s41596-018-0036-3 · Cited by 168
Self-citationOgawa, S., Surapisitchat, J., Virtanen, C., Ogawa, M., Niapour, M., Sugamori, K. S., Wang, S., Tamblyn, L., Guillemette, C., Hoffmann, E., et al. (2013) · Development · doi:10.1242/dev.090266 · Cited by 161
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
Organoids in gastrointestinal diseases: From experimental models to clinical translation
Günther, C., Winner, B., Neurath, M. F., & Stappenbeck, T. S. (2022) · Gut · doi:10.1136/gutjnl-2021-326560 · Cited by 145
Establishment of intestinal organoid cultures modeling injury-associated epithelial regeneration
Qu, M., Xiong, L., Lyu, Y., Zhang, X., Shen, J., Guan, J., Chai, P., Lin, Z., Nie, B., Li, C., et al. (2021) · Cell Research · doi:10.1038/s41422-020-00453-x · Cited by 138
Complex Tissue and Disease Modeling using hiPSCs
Passier, R., Orlova, V., & Mummery, C. (2016) · Cell Stem Cell · doi:10.1016/j.stem.2016.02.011 · Cited by 142
Vascularized microfluidic organ-chips for drug screening, disease models and tissue engineering
Osaki, T., Sivathanu, V., & Kamm, R. D. (2018) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2018.03.011 · Cited by 141
Human stomach-on-a-chip with luminal flow and peristaltic-like motility
Lee, K. K., McCauley, H. A., Broda, T. R., Kofron, M. J., Wells, J. M., & Hong, C. I. (2018) · Lab on a Chip · doi:10.1039/c8lc00910d · Cited by 129
Self-citationJung, K. B., Lee, H., Son, Y. S., Lee, M.-O., Kim, Y.-D., Oh, S. J., Kwon, O., Cho, S., Cho, H.-S., Kim, D.-S., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-05450-8 · Cited by 125
The Gut-Brain Axis in Inflammatory Bowel Disease—Current and Future Perspectives
Günther, C., Rothhammer, V., Karow, M., Neurath, M., & Winner, B. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22168870 · Cited by 123
Cancer research using organoid technology
Kretzschmar, K. (2021) · Journal of Molecular Medicine · doi:10.1007/s00109-020-01990-z · Cited by 120
Enteroviruses: A Gut-Wrenching Game of Entry, Detection, and Evasion
Wells, A. I., & Coyne, C. B. (2019) · Viruses · doi:10.3390/v11050460 · Cited by 109
Human Organoids for Predictive Toxicology Research and Drug Development
Matsui, T., & Shinozawa, T. (2021) · Frontiers in Genetics · doi:10.3389/fgene.2021.767621 · Cited by 109
Schneeberger, K., Spee, B., Costa, P., Sachs, N., Clevers, H., & Malda, J. (2017) · Biofabrication · doi:10.1088/1758-5090/aa6121 · Cited by 100
Intestinal organoids: A new paradigm for engineering intestinal epithelium in vitro
Rahmani, S., Breyner, N. M., Su, H.-M., Verdu, E. F., & Didar, T. F. (2019) · Biomaterials · doi:10.1016/j.biomaterials.2018.12.006 · Cited by 98
Extracellular matrix requirements for gastrointestinal organoid cultures
Rezakhani, S., Gjorevski, N., & Lutolf, M. P. (2021) · Biomaterials · doi:10.1016/j.biomaterials.2021.121020 · Cited by 100
Organoids in image-based phenotypic chemical screens
Lukonin, I., Zinner, M., & Liberali, P. (2021) · Experimental & Molecular Medicine · doi:10.1038/s12276-021-00641-8 · Cited by 99
The Intestinal Barrier in Parkinson’s Disease: Current State of Knowledge
van IJzendoorn, S. C. D., & Derkinderen, P. (2019) · Journal of Parkinson’s Disease · doi:10.3233/jpd-191707 · Cited by 97
Miura, S., & Suzuki, A. (2017) · Cell Stem Cell · doi:10.1016/j.stem.2017.08.020 · Cited by 91
Advanced human developmental toxicity and teratogenicity assessment using human organoid models
Li, M., Gong, J., Gao, L., Zou, T., Kang, J., & Xu, H. (2022) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2022.113429 · Cited by 84
Generation of intestinal organoids derived from human pluripotent stem cells for drug testing
Yoshida, S., Miwa, H., Kawachi, T., Kume, S., & Takahashi, K. (2020) · Scientific Reports · doi:10.1038/s41598-020-63151-z · 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
Next-Generation Liver Medicine Using Organoid Models
Akbari, S., Arslan, N., Senturk, S., & Erdal, E. (2019) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2019.00345 · Cited by 72
Dye, B. R., Youngblood, R. L., Oakes, R. S., Kasputis, T., Clough, D. W., Spence, J. R., & Shea, L. D. (2020) · Biomaterials · doi:10.1016/j.biomaterials.2020.119757 · Cited by 75
Self-citationGenetic engineering in organoids
Teriyapirom, I., Batista-Rocha, A. S., & Koo, B.-K. (2021) · Journal of Molecular Medicine · doi:10.1007/s00109-020-02029-z · Cited by 68
Present Application and Perspectives of Organoid Imaging Technology
Fei, K., Zhang, J., Yuan, J., & Xiao, P. (2022) · Bioengineering · doi:10.3390/bioengineering9030121 · Cited by 65
Evolving Concepts and Translational Relevance of Enteroendocrine Cell Biology
Drucker, D. J. (2016) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2015-3449 · Cited by 63
Human iPSC-liver organoid transplantation reduces fibrosis through immunomodulation
Tadokoro, T., Murata, S., Kato, M., Ueno, Y., Tsuchida, T., Okumura, A., Kuse, Y., Konno, T., Uchida, Y., Yamakawa, Y., et al. (2024) · Science Translational Medicine · doi:10.1126/scitranslmed.adg0338 · Cited by 58
A hollow fiber system for simple generation of human brain organoids
Zhu, Y., Wang, L., Yin, F., Yu, Y., Wang, Y., Liu, H., Wang, H., Sun, N., Liu, H., & Qin, J. (2017) · Integr. Biol. · doi:10.1039/c7ib00080d · Cited by 55
Scalable Production and Cryostorage of Organoids Using Core–Shell Decoupled Hydrogel Capsules
Lu, Y., Fu, D., An, D., Chiu, A., Schwartz, R., Nikitin, A. Y., & Ma, M. (2017) · Advanced Biosystems · doi:10.1002/adbi.201700165 · Cited by 51
Son, Y. S., Ki, S. J., Thanavel, R., Kim, J., Lee, M., Kim, J., Jung, C., Han, T., Cho, H., Ryu, C., et al. (2020) · The FASEB Journal · doi:10.1096/fj.202000063r · Cited by 45
A Pillar and Perfusion Plate Platform for Robust Human Organoid Culture and Analysis
Kang, S., Kimura, M., Shrestha, S., Lewis, P., Lee, S., Cai, Y., Joshi, P., Acharya, P., Liu, J., Yang, Y., et al. (2024) · Advanced Healthcare Materials · doi:10.1002/adhm.202302502 · Cited by 44
Self-citationFarewell to Animal Testing: Innovations on Human Intestinal Microphysiological Systems
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“For this purpose we utilized a protocol developed by Wells and colleagues that employs sequential stimulation of NODAL and FGF4R /WNT3A to mimic early development and drive endodermal specification first into mid- and hindgut prior to differentiation into intestinal epithelium (Fig 2A) [20].”
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Metadata
- Authors
- 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., Shroyer, N. F., & Wells, J. M.
- Venue
- Nature
- Published
- 2010-12-12
- Volume
- 470
- Issue
- 7332
- Pages
- 105-109
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W2143296478
- Cited by
- 1,922
- References
- 6
- FWCI
- 19.85
- Type
- journal article
- Language
- en
- Open access
- green
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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Data sources
Bibliographic data: Semantic Scholar, OpenAlex, Crossref.
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.
