Generation of Mouse and Human Organoid-Forming Intestinal Progenitor Cells by Direct Lineage Reprogramming
Open accessAbstract
Intestinal organoids hold great promise as a valuable tool for studying and treating intestinal diseases. The currently available sources of human intestinal organoids, tissue fragments or pluripotent stem cells, involve invasive procedures or complex differentiation protocols, respectively. Here, we show that a set of four transcription factors, Hnf4α, Foxa3, Gata6, and Cdx2, can directly reprogram mouse fibroblasts to acquire the identity of fetal intestine-derived progenitor cells (FIPCs). These induced FIPCs (iFIPCs) form spherical organoids that develop into adult-type budding organoids containing cells with intestinal stem cell properties. The resulting stem cells produce all intestinal epithelial cell lineages and undergo self-renewing cell divisions. After transplantation, the induced spherical and budding organoids can reconstitute colonic and intestinal epithelia, respectively. The same combination of four defined transcription factors can also induce human iFIPCs. This alternative approach for producing intestinal organoids may well facilitate application for disease analysis and therapy development.
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Patient-specific organoid engineering by using reprogramming cells for regenerative therapy has progressed.
“patient‐specific organoid engineering by using reprogramming cells for regenerative therapy has progressed.[ 20 ]”
From Sweat Gland Organoids Originating from Reprogrammed Epidermal Keratinocytes Functionally Recapitulated Damaged Skin (2021) · cites this paper as [20]
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Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources
Huang, D. W., Sherman, B. T., & Lempicki, R. A. (2009) · Nature Protocols · doi:10.1038/nprot.2008.211 · Cited by 35,890 · see citing works
Huang, D. W., Sherman, B. T., & Lempicki, R. A. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkn923 · Cited by 14,108 · see citing works
Bioconductor: open software development for computational biology and bioinformatics
Gentleman, R., Carey, V., Bates, D., Bolstad, B., Dettling, M., Dudoit, S., Ellis, B., Gautier, L., Ge, Y., Gentry, J., et al. (2004) · Genome Biology · doi:10.1186/gb-2004-5-10-r80 · Cited by 13,133 · see citing works
Bolstad, B. M., Irizarry, R. A., Åstrand, M., & Speed, T. P. (2003) · Bioinformatics · doi:10.1093/bioinformatics/19.2.185 · Cited by 8,185 · see citing works
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 · see citing works
REVIGO summarizes and visualizes long lists of gene ontology terms
Supek, F., Bošnjak, M., Škunca, N., & Šmuc, T. (2011) · PLoS ONE · doi:10.1371/journal.pone.0021800 · Cited by 6,264 · see citing works
limma: Linear Models for Microarray Data
Smyth, G. K. (2005) · Statistics for Biology and Health · doi:10.1007/0-387-29362-0_23 · Cited by 5,796 · see citing works
Identification of stem cells in small intestine and colon by marker gene Lgr5
Barker, N., van Es, J. H., Kuipers, J., Kujala, P., van den Born, M., Cozijnsen, M., Haegebarth, A., Korving, J., Begthel, H., Peters, P. J., et al. (2007) · Nature · doi:10.1038/nature06196 · Cited by 5,687 · see citing works
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 · see citing works
Bioinformatics and Computational Biology Solutions Using R and Bioconductor
Gentleman, R. C., Carey, V. J., Huber, W. K., Irizarry, R. A., & Dudoit, S. (2005) · Statistics in the health sciences · doi:10.1007/0-387-29362-0 · Cited by 3,470 · see citing works
Direct conversion of fibroblasts to functional neurons by defined factors
Vierbuchen, T., Ostermeier, A., Pang, Z. P., Kokubu, Y., Südhof, T. C., & Wernig, M. (2010) · Nature · doi:10.1038/nature08797 · Cited by 3,017 · see citing works
‘Green mice’ as a source of ubiquitous green cells
Okabe, M., Ikawa, M., Kominami, K., Nakanishi, T., & Nishimune, Y. (1997) · FEBS Letters · doi:10.1016/s0014-5793(97)00313-x · Cited by 2,581 · see citing works
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 · see citing works
Direct reprogramming of fibroblasts into functional cardiomyocytes by defined factors
Ieda, M., Fu, J.-D., Delgado-Olguin, P., Vedantham, V., Hayashi, Y., Bruneau, B. G., & Srivastava, D. (2010) · Cell · doi:10.1016/j.cell.2010.07.002 · Cited by 2,454 · see citing works
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. A., Hoskins, E. E., Kalinichenko, V. V., Wells, S. I., Zorn, A. M., et al. (2010) · Nature · doi:10.1038/nature09691 · Cited by 1,911 · see citing works
Plat-E: an efficient and stable system for transient packaging of retroviruses
MORITA, S., Kojima, T., & Kitamura, T. (2000) · Gene Therapy · doi:10.1038/sj.gt.3301206 · Cited by 1,660 · see citing works
Pioneer transcription factors: establishing competence for gene expression
Zaret, K. S., & Carroll, J. S. (2011) · Genes & Development · doi:10.1101/gad.176826.111 · Cited by 1,589 · see citing works
Opening of Compacted Chromatin by Early Developmental Transcription Factors HNF3 (FoxA) and GATA-4
Cirillo, L. A., Lin, F. R., Cuesta, I., Friedman, D., Jarník, M., & Zaret, K. S. (2002) · Molecular Cell · doi:10.1016/s1097-2765(02)00459-8 · Cited by 1,188 · see citing works
Induction of functional hepatocyte-like cells from mouse fibroblasts by defined factors
Huang, P., He, Z., Ji, S., Sun, H., Xiang, D., Liu, C., Hu, Y., Wang, X., & Hui, L. (2011) · Nature · doi:10.1038/nature10116 · Cited by 864 · see citing works
Direct conversion of mouse fibroblasts to hepatocyte-like cells by defined factors
Sekiya, S., & Suzuki, A. (2011) · Nature · doi:10.1038/nature10263 · Cited by 846 · see citing works
Self-citationFunctional engraftment of colon epithelium expanded in vitro from a single adult Lgr5+ stem cell
Yui, S., Nakamura, T., Sato, T., Nemoto, Y., Mizutani, T., Zheng, X., Ichinose, S., Nagaishi, T., Okamoto, R., Tsuchiya, K., et al. (2012) · Nature Medicine · doi:10.1038/nm.2695 · Cited by 805 · see citing works
Organizing cell renewal in the intestine: stem cells, signals and combinatorial control
Crosnier, C., Stamataki, D., & Lewis, J. H. (2006) · Nature Reviews Genetics · doi:10.1038/nrg1840 · Cited by 756 · see citing works
Direct Reprogramming of Fibroblasts into Neural Stem Cells by Defined Factors
Han, D., Tàpia, N., Hermann, A., Hemmer, K., Höing, S., Araúzo-Bravo, M. J., Zaehres, H., Wu, G., Frank, S., Moritz, S., et al. (2012) · Cell stem cell · doi:10.1016/j.stem.2012.02.021 · Cited by 514 · see citing works
Luche, H., Weber, O., Nageswara Rao, T., Blum, C., & Fehling, H. J. (2007) · European Journal of Immunology · doi:10.1002/eji.200636745 · Cited by 482 · see citing works
Direct conversion of mouse fibroblasts to self-renewing, tripotent neural precursor cells
Lujan, E., Chanda, S., Ahlenius, H., Südhof, T. C., & Wernig, M. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1121003109 · Cited by 421 · see citing works
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 397 · see citing works
Generation of oligodendroglial cells by direct lineage conversion
Yang, N., Zuchero, J. B., Ahlenius, H., Marro, S. G., Ng, Y. H., Vierbuchen, T., Hawkins, J. S., Geissler, R. H., Barres, B. A., & Wernig, M. (2013) · Nature Biotechnology · doi:10.1038/nbt.2564 · Cited by 303 · see citing works
Najm, F. J., Lager, A. M., Zaremba, A., Wyatt, K., Caprariello, A. V., Factor, D. C., Karl, R. T., Maeda, T., Miller, R. H., & Tesar, P. J. (2013) · Nature Biotechnology · doi:10.1038/nbt.2561 · Cited by 268 · see citing works
Dissecting Engineered Cell Types and Enhancing Cell Fate Conversion via CellNet
Morris, S. A., Cahan, P., Li, H., Zhao, A., Roman, A. K. S., Shivdasani, R. A., Collins, J. J., & Daley, G. Q. (2014) · Cell · doi:10.1016/j.cell.2014.07.021 · Cited by 267 · see citing works
Primary Mouse Small Intestinal Epithelial Cell Cultures
Sato, T., & Clevers, H. C. (2012) · Methods in molecular biology · doi:10.1007/978-1-62703-125-7_19 · Cited by 251 · see citing works
福田, 将., Mizutani, T., Mochizuki, W., Matsumoto, T., Nozaki, K., Sakamaki, Y., Ichinose, S., Okada, Y., Tanaka, T., Watanabe, M., et al. (2014) · Genes & Development · doi:10.1101/gad.245233.114 · Cited by 178 · see citing works
Reprogramming Fibroblasts into Bipotential Hepatic Stem Cells by Defined Factors
Yu, B., He, Z., You, P., Han, Q., Xiang, D., Chen, F., Wang, M., Liu, C., Lin, X., Borjigin, U., et al. (2013) · Cell stem cell · doi:10.1016/j.stem.2013.06.017 · Cited by 177 · see citing works
Lalit, P. A., Salick, M. R., Nelson, D. O., Squirrell, J. M., Shafer, C. M., Patel, N. G., Saeed, I., Schmuck, E. G., Markandeya, Y. S., Wong, R., et al. (2016) · Cell stem cell · doi:10.1016/j.stem.2015.12.001 · Cited by 173 · see citing works
Direct Reprogramming of Murine Fibroblasts to Hematopoietic Progenitor Cells
Batta, K., Florkowska, M., Kouskoff, V., & Lacaud, G. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.11.002 · Cited by 169 · see citing works
Kim, Y. J., Lim, H., Li, Z., Oh, Y., Kovlyagina, I., Choi, I.-Y., Dong, X.-Z., & Lee, G. (2014) · Cell Stem Cell · doi:10.1016/j.stem.2014.07.013 · Cited by 142 · see citing works
Cdx2 regulates patterning of the intestinal epithelium
Grainger, S. J., Savory, J. G. A., & Lohnes, D. (2010) · Developmental Biology · doi:10.1016/j.ydbio.2009.12.025 · Cited by 125 · see citing works
Transformation of intestinal stem cells into gastric stem cells on loss of transcription factor Cdx2
Simmini, S., Bialecka, M., Huch, M., Kester, L. A., van de Wetering, M., Sato, T., Beck, F., van Oudenaarden, A., Clevers, H. C., & Deschamps, J. (2014) · Nature Communications · doi:10.1038/ncomms6728 · Cited by 105 · see citing works
Direct Induction of Trophoblast Stem Cells from Murine Fibroblasts
Kubaczka, C., Senner, C. E., Cierlitza, M., Araúzo-Bravo, M. J., Kuckenberg, P., Peitz, M., Hemberger, M., & Schorle, H. (2015) · Cell stem cell · doi:10.1016/j.stem.2015.08.005 · Cited by 97 · see citing works
Benchetrit, H., Herman, S., van Wietmarschen, N., Wu, T., Makedonski, K., Maoz, N., Yom-Tov, N., Stave, D., Lasry, R., Zayat, V., et al. (2015) · Cell stem cell · doi:10.1016/j.stem.2015.08.006 · Cited by 96 · see citing works
GATA4 and GATA6 regulate intestinal epithelial cytodifferentiation during development
Walker, E. M., Thompson, C. A., & Battle, M. A. (2014) · Developmental Biology · doi:10.1016/j.ydbio.2014.05.017 · Cited by 79 · see citing works
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Modeling neoplastic disease with spheroids and organoids
Zanoni, M., Cortesi, M., Zamagni, A., Arienti, C., Pignatta, S., & Tesei, A. (2020) · Journal of Hematology & Oncology · doi:10.1186/s13045-020-00931-0 · Cited by 265 · see citing works
Xu, H., Jiao, Y., Qin, S., Zhao, W., Chu, Q., & Wu, K. (2018) · Experimental Hematology and Oncology · doi:10.1186/s40164-018-0122-9 · Cited by 184 · see citing works
Charting human development using a multi-endodermal organ atlas and organoid models
Yu, Q., Kilik, U., Holloway, E. M., Tsai, Y.-H., Harmel, C., Wu, A., Wu, J. H., Czerwinski, M. J., Childs, C. J., He, Z., et al. (2021) · Cell · doi:10.1016/j.cell.2021.04.028 · Cited by 145 · see citing works
Transplantation of intestinal organoids into a mouse model of colitis
Watanabe, S., Kobayashi, S., Ogasawara, N., Okamoto, R., Nakamura, T., Watanabe, M., Jensen, K. B., & Yui, S. (2022) · Nature Protocols · doi:10.1038/s41596-021-00658-3 · Cited by 143 · see citing works
Research Progress, Challenges, and Breakthroughs of Organoids as Disease Models
Huang, Y., Huang, Z., Tang, Z., Chen, Y., Huang, M., Liu, H., Huang, W., Ye, Q., & Jia, B. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.740574 · Cited by 128 · see citing works
Inflation-collapse dynamics drive patterning and morphogenesis in intestinal organoids
Tallapragada, N. P., Cambra, H. M., Wald, T., Jalbert, S. K., Abraham, D. M., Klein, O. D., & Klein, A. M. (2021) · Cell stem cell · doi:10.1016/j.stem.2021.04.002 · Cited by 94 · see citing works
Stem cell-derived intestinal organoids: a novel modality for IBD
Tian, C., Yang, M., Xu, H., Zhu, M., Yue, N.-N., Zhang, Y., Shi, R., Yao, J., Wang, L., Liang, Y.-J., et al. (2023) · Cell Death Discovery · doi:10.1038/s41420-023-01556-1 · Cited by 85 · see citing works
Human Pluripotent Stem Cell-Derived Endoderm for Modeling Development and Clinical Applications
Yiangou, L., Ross, A., Goh, K. J., & Vallier, L. (2018) · Cell stem cell · doi:10.1016/j.stem.2018.03.016 · Cited by 76 · see citing works
3D Cell Culture—Can It Be As Popular as 2D Cell Culture?
Sun, M., Liu, A., Yang, X.-F., Gong, J.-X., Yu, M.-F., Yao, X., Wang, H., & He, Y. (2021) · Advanced NanoBiomed Research · doi:10.1002/anbr.202000066 · Cited by 66 · see citing works
Capybara: A computational tool to measure cell identity and fate transitions
Kong, W., Fu, Y. C., Holloway, E. M., Garipler, G., Yang, X., Mazzoni, E. O., & Morris, S. A. (2022) · Cell stem cell · doi:10.1016/j.stem.2022.03.001 · Cited by 61 · see citing works
Engineering Biomaterials with Micro/Nanotechnologies for Cell Reprogramming
Fang, J., Hsueh, Y., Soto, J., Sun, W., Wang, J., Gu, Z., Khademhosseini, A., & Li, S. (2020) · ACS Nano · doi:10.1021/acsnano.9b04837 · Cited by 60 · see citing works
Hansen, S. L., Larsen, H. L., Pikkupeura, L. M., Maciag, G., Guiu, J., Müller, I., Clement, D. L., Mueller, C., Johansen, J. V., Helin, K., et al. (2023) · Science Advances · doi:10.1126/sciadv.adg4055 · Cited by 55 · see citing works
Oral Organoids: Progress and Challenges
Gao, X., Wu, Y., Liao, L., & Tian, W. (2021) · Journal of Dental Research · doi:10.1177/0022034520983808 · Cited by 56 · see citing works
Geiser, P., Martino, M. L. D., Ventayol, P. S., Eriksson, J., Sima, E., Al-Saffar, A. K., Ahl, D., Phillipson, M., Webb, D., Sundbom, M., et al. (2021) · mBio · doi:10.1128/mbio.02684-20 · Cited by 52 · see citing works
Lee, M. J., Lee, J., Ha, J., Kim, G. W., Kim, H., Lee, S., Koo, B., & Park, Y. (2024) · Experimental & Molecular Medicine · doi:10.1038/s12276-024-01312-0 · Cited by 56 · see citing works
Organoid Transplantation Can Improve Reproductive Prognosis by Promoting Endometrial Repair in Mice
Zhang, H., Xu, D., Li, Y., Lan, J., Zhu, Y., Cao, J., Hu, M., Yuan, J., He, J. P., Li, G., et al. (2022) · International Journal of Biological Sciences · doi:10.7150/ijbs.69410 · Cited by 48 · see citing works
Generation of Human iPSC–Derived Intestinal Epithelial Cell Monolayers by CDX2 Transduction
Takayama, K., Negoro, R., Yamashita, T., Kawai, K., Ichikawa, M., Mori, T., Nakatsu, N., Harada, K., Ito, S., Yamada, H., et al. (2019) · Cellular and Molecular Gastroenterology and Hepatology · doi:10.1016/j.jcmgh.2019.06.004 · Cited by 47 · see citing works
Intestinal Organoid Culture in Polymer Film‐Based Microwell Arrays
Kakni, P., Hueber, R., Knoops, K., López‐Iglesias, C., Truckenmüller, R. K., Habibović, P., & Giselbrecht, S. (2020) · Advanced Biosystems · doi:10.1002/adbi.202000126 · Cited by 45 · see citing works
Wang, L., Li, B., Bo, X., Yi, X., Xiao, X., & Zheng, Q. (2022) · Experimental & Molecular Medicine · doi:10.1038/s12276-022-00767-3 · Cited by 44 · see citing works
Pikkupeura, L. M., Bressan, R. B., Guiu, J., Chen, Y., Maimets, M., Mayer, D., Schweiger, P. J., Hansen, S. L., Maciag, G. J., Larsen, H. L., et al. (2023) · Science Advances · doi:10.1126/sciadv.adf9460 · Cited by 43 · see citing works
Sun, X., Xiang, J., Chen, R., Geng, Z., Wang, L., Liu, Y., Ji, S., Chen, H., Li, Y., Zhang, C., et al. (2021) · Advanced Science · doi:10.1002/advs.202103079 · Cited by 42 · see citing works
Restoring aged stem cell functionality: Current progress and future directions
Spehar, K., Pan, A., & Beerman, I. (2020) · Stem Cells · doi:10.1002/stem.3234 · Cited by 45 · see citing works
Recent progress in organoid culture to model intestinal epithelial barrier functions
Nakamura, T. (2018) · International Immunology · doi:10.1093/intimm/dxy065 · Cited by 38 · see citing works
The prognostic potential of CDX2 in colorectal cancer: Harmonizing biology and clinical practice
Badia-Ramentol, J., Gimeno-Valiente, F., Duréndez-Saéz, E., Martínez‐Ciarpaglini, C., Linares, J., Iglesias, M., Cervantes, A. M. R., Calon, A., & Tarazona, N. (2023) · Cancer Treatment Reviews · doi:10.1016/j.ctrv.2023.102643 · Cited by 36 · see citing works
Takashima, Y., Horisawa, K., Udono, M., Ohkawa, Y., & Suzuki, A. (2018) · Cancer Science · doi:10.1111/cas.13798 · Cited by 35 · see citing works
Self-citationDirect cell-fate conversion of somatic cells: Toward regenerative medicine and industries
Horisawa, K., & Suzuki, A. (2020) · Proceedings of the Japan Academy Series B · doi:10.2183/pjab.96.012 · Cited by 34 · see citing works
Self-citationBusch, M., Brouwer, H., Aalderink, G., Bredeck, G., Kämpfer, A. A. M., Schins, R. P. F., & Bouwmeester, H. (2023) · Frontiers in Toxicology · doi:10.3389/ftox.2023.1112212 · Cited by 33 · see citing works
Organoids for Advanced Therapeutics and Disease Models
Kim, S., Cho, A., Min, S., Kim, S., & Cho, S. (2018) · Advanced Therapeutics · doi:10.1002/adtp.201800087 · Cited by 33 · 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
Generation of Budding-Like Intestinal Organoids from Human Induced Pluripotent Stem Cells
Onozato, D., Ogawa, I., Kida, Y., Mizuno, S., Hashita, T., Iwao, T., & Matsunaga, T. (2021) · Journal of Pharmaceutical Sciences · doi:10.1016/j.xphs.2021.03.014 · Cited by 31 · see citing works
Organoids as regenerative medicine for inflammatory bowel disease
Hammerhøj, A., Chakravarti, D., Sato, T., Jensen, K. B., & Nielsen, O. H. (2024) · iScience · doi:10.1016/j.isci.2024.110118 · Cited by 34 · see citing works
Cell therapy for liver disorders: past, present and future
Ortuño‐Costela, M. D. C., Pinzani, M., & Vallier, L. (2025) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-025-01050-2 · Cited by 32 · see citing works
Inada, H., Udono, M., Matsuda‐Ito, K., Horisawa, K., Ohkawa, Y., Miura, S., Goya, T., Yamamoto, J., Nagasaki, M., Ueno, K., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-19041-z · Cited by 30 · see citing works
Self-citationNguyen, R., Bae, S. D. W., Zhou, G., Read, S. A., Ahlenstiel, G., George, J., & Qiao, L. (2020) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2020.188350 · Cited by 27 · see citing works
Gómez, D. P., & Boudreau, F. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.732137 · Cited by 25 · see citing works
Li, J., Xu, X., Tiwari, M., Chen, Y., Fuller, M. R., Bansal, V., Tamayo, P., Das, S., Ghosh, P., & Sen, G. L. (2021) · Nature Communications · doi:10.1038/s41467-021-21067-w · Cited by 24 · see citing works
Intestinal epithelial organoids: regeneration and maintenance of the intestinal epithelium
Oda, M., Hatano, Y., & Sato, T. (2022) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2022.101977 · Cited by 23 · see citing works
Tissue-location-specific transcription programs drive tumor dependencies in colon cancer
Yang, L., Tu, L., Bisht, S., Mao, Y., Petkovich, D. A., Thursby, S.-J., Liang, J., Patel, N., Yen, R.-W. C., Largent, T., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-45605-4 · Cited by 20 · see citing works
Reprogramming cellular identity during intestinal regeneration
Larsen, H. L., & Jensen, K. B. (2021) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2021.05.005 · Cited by 19 · see citing works
Brief summary of the current protocols for generating intestinal organoids
Miura, S., & Suzuki, A. (2018) · Development Growth & Differentiation · doi:10.1111/dgd.12559 · Cited by 16 · see citing works
Self-citationMiura, S., Horisawa, K., Iwamori, T., Tsujino, S., Inoue, K., Karasawa, S., Yamamoto, J., Ohkawa, Y., Sekiya, S., & Suzuki, A. (2024) · Nature Communications · doi:10.1038/s41467-024-47869-2 · Cited by 16 · see citing works
Self-citationLimitations and challenges of direct cell reprogramming in vitro and in vivo.
Zhang, Y.-X., Chen, S., Li, Y.-M., & Zheng, Y. (2022) · PubMed · doi:10.14670/hh-18-458 · Cited by 16 · see citing works
Discovery of non-genomic drivers of YAP signaling modulating the cell plasticity in CRC tumor lines
Ogasawara, N., Kano, Y., Yoneyama, Y., Kobayashi, S., Watanabe, S. P., Kirino, S., Velez-Bravo, F. D., Hong, Y., Ostapiuk, A., Lutsik, P., et al. (2024) · iScience · doi:10.1016/j.isci.2024.109247 · Cited by 14 · see citing works
Mechanisms for intestinal regeneration
Dubrovsky, G., & Dunn, J. (2018) · Current Opinion in Pediatrics · doi:10.1097/mop.0000000000000630 · Cited by 14 · see citing works
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Liu, Y., Bertels, S., Reischl, M., Peravali, R., Bastmeyer, M., Popova, A. A., & Levkin, P. A. (2022) · Advanced Healthcare Materials · doi:10.1002/adhm.202200718 · Cited by 13 · see citing works
Modeling Human Organ Development and Diseases With Fetal Tissue–Derived Organoids
Liang, J., Li, X., Dong, Y., & Zhao, B. T. (2022) · Cell Transplantation · doi:10.1177/09636897221124481 · Cited by 13 · see citing works
Gut aging: A wane from the normal to repercussion and gerotherapeutic strategies
Abankwah, J. K., Wang, Y., Wang, J., Enechojo, O. S., Pozzo, L. D., Chu, X., & Bian, Y. (2024) · Heliyon · doi:10.1016/j.heliyon.2024.e37883 · Cited by 13 · see citing works
Conversion of human and mouse fibroblasts into lung-like epithelial cells
Wong, A. P., Shojaie, S., Liang, Q., Xia, S., Paola, M. D., Ahmadi, S., Bilodeau, C., Garner, J., Post, M., Duchesneau, P., et al. (2019) · Scientific Reports · doi:10.1038/s41598-019-45195-y · Cited by 12 · see citing works
Däullary, T., Imdahl, F., Dietrich, O., Hepp, L., Krammer, T., Fey, C., Neuhaus, W., Metzger, M., Vogel, J., Westermann, A. J., et al. (2023) · Gut Microbes · doi:10.1080/19490976.2023.2186109 · Cited by 12 · see citing works
A Concise Review of Organoid Tissue Engineering: Regenerative Applications and Precision Medicine
Makesh, K. Y., Navaneethan, A., Ajay, M., Munuswamy‐Ramanujam, G., Chinnasamy, A., Gnanasampanthapandian, D., & Palaniyandi, K. (2025) · Organoids · doi:10.3390/organoids4030016 · Cited by 12 · see citing works
Ye, B., Yang, L., Liu, B., Liu, N., Fan, D., Li, H., Sun, L., Du, Y., Wang, S., Tian, Y., et al. (2022) · Cellular and Molecular Immunology · doi:10.1038/s41423-022-00842-9 · Cited by 10 · see citing works
Umeyama, T., Matsuda, T., & Nakashima, K. (2024) · Cells · doi:10.3390/cells13080707 · Cited by 10 · see citing works
Yu, Q., Kilik, U., Holloway, E. M., Tsai, Y.-H., Wu, A., Wu, J. H., Czerwinski, M. J., Childs, C. J., He, Z., Glass, I. A., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.07.24.219147 · Cited by 10 · see citing works
Lee, M. J., Lee, J., Ha, J., Kim, G., Kim, H., Lee, S., Koo, B., & Park, Y. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.09.16.558039 · Cited by 10 · see citing works
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Wang, L., Ye, Z., & Jang, Y.-Y. (2021) · Experimental Biology and Medicine · doi:10.1177/1535370220985808 · Cited by 9 · see citing works
Katada, R., Tanaka, J., Takamatsu, K., Hata, K., Yasuhara, R., Ohnuma, S., Takakura, I., Nishimura, R., Shirota, T., & Mishima, K. (2021) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2021.11.064 · Cited by 9 · see citing works
TRANSDIRE: data-driven direct reprogramming by a pioneer factor-guided trans-omics approach
Eguchi, R., Hamano, M., Iwata, M., Nakamura, T., Oki, S., & Yamanishi, Y. (2022) · Bioinformatics · doi:10.1093/bioinformatics/btac209 · Cited by 9 · see citing works
Cbl and Cbl-b ubiquitin ligases are essential for intestinal epithelial stem cell maintenance
Zutshi, N., Mohapatra, B. C., Mondal, P., An, W., Goetz, B. T., Wang, S., Li, S., Storck, M. D., Mercer, D. F. F., Black, A. R., et al. (2024) · iScience · doi:10.1016/j.isci.2024.109912 · Cited by 13 · see citing works
The role of pioneer transcription factors in the induction of direct cellular reprogramming
Horisawa, K., & Suzuki, A. (2023) · Regenerative Therapy · doi:10.1016/j.reth.2023.06.002 · Cited by 9 · see citing works
Self-citationInnovative approaches in skin therapy: The rise of organoid cultivation
Zhou, R., Luo, X., Chen, S., Jia, K., Yu, H., Huang, Z., Tan, Y., Ma, M., Zhao, J., Xing, J., et al. (2025) · Chemical Engineering Journal · doi:10.1016/j.cej.2025.162248 · Cited by 6 · see citing works
Sakib, S., & Zou, S. (2024) · Langmuir · doi:10.1021/acs.langmuir.3c02741 · Cited by 6 · see citing works
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Toyosaki, M., Homma, K., Suzuki, S., Muraoka, N., Hashimoto, H., Goshima, N., Ieda, M., & Sasaki, J. (2020) · Scientific Reports · doi:10.1038/s41598-020-78523-8 · Cited by 7 · see citing works
Goya, T., Horisawa, K., Udono, M., Ohkawa, Y., Ogawa, Y., Sekiya, S., & Suzuki, A. (2022) · Hepatology Communications · doi:10.1002/hep4.1911 · Cited by 6 · see citing works
Self-citationCho, J., Lee, M. J., Park, J. Y., Lee, J., Lee, S., Chung, C., Koo, B., & Park, Y. (2025) · Journal of Visualized Experiments · doi:10.3791/68529 · Cited by 5 · see citing works
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Sun, S., Yang, F., Wang, S., Guo, J., Liu, X., Ge, N., & Wang, G. (2020) · Endoscopic Ultrasound · doi:10.4103/eus.eus_79_20 · Cited by 5 · see citing works
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Wei, H., Li, Y., Li, L., Hu, Q., Shi, M., Cheng, L., Jiang, X., Zhou, Y., Chen, S., Ji, Y., et al. (2023) · Journal of Biological Engineering · doi:10.1186/s13036-023-00348-6 · Cited by 5 · see citing works
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Fang, M., Liu, L., Zhou, H., Li, Y., & Zheng, Y. (2020) · World Journal of Stem Cells · doi:10.4252/wjsc.v12.i8.752 · Cited by 4 · see citing works
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Huang, Y., He, K., & Chen, Y. (2024) · Infectious Microbes & Diseases · doi:10.1097/im9.0000000000000153 · Cited by 3 · see citing works
Murayama, R., Horisawa, K., Miura, S., Taniguchi, S., Shu, J., Takahashi, M., Izumi, Y., Bamba, T., Ishigami, K., & Suzuki, A. (2025) · Aging Cell · doi:10.1111/acel.70197 · Cited by 2 · see citing works
Self-citationHorisawa, K., Miura, S., Araki, H., Miura, F., Ito, T., & Suzuki, A. (2023) · Scientific Reports · doi:10.1038/s41598-023-49546-8 · Cited by 2 · see citing works
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Morita, A., Ishii, M., Asakura, T., Yotsukura, M., Hegab, A. E., Kusumoto, T., Namkoong, H., Ogawa, T., Nakatake, Y., Oda, M., et al. (2025) · npj Regenerative Medicine · doi:10.1038/s41536-025-00411-4 · Cited by 3 · see citing works
Hamano, M., Nakamura, T., Ito, R., Shimada, Y., Iwata, M., Takeshita, J., Eguchi, R., & Yamanishi, Y. (2024) · Bioinformatics · doi:10.1093/bioinformatics/btae048 · Cited by 1 · see citing works
Zhang, S., Liu, S., Qin, Y., Zhao, S., & Liu, H. (2025) · Coordination Chemistry Reviews · doi:10.1016/j.ccr.2025.217309 · Cited by 1 · see citing works
The emerging roles of intestinal organoid models in inflammatory bowel disease research
Leach, S. T., Wheeler, T., Bowcock, N. L., Aitchison, A., Lemberg, D. A., & Day, A. S. (2026) · Expert Review of Gastroenterology & Hepatology · doi:10.1080/17474124.2026.2635421 · Cited by 1 · see citing works
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Nio, Y., & Takebe, T. (2019) · Current human cell research and applications · doi:10.1007/978-981-13-3672-0_9 · Cited by 1 · see citing works
Miura, S., & Suzuki, A. (2020) · Methods in molecular biology · doi:10.1007/978-1-0716-0747-3_14 · Cited by 1 · see citing works
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Nakauka‐Ddamba, A., & Lengner, C. J. (2017) · Cell stem cell · doi:10.1016/j.stem.2017.09.011
Venkatasubramanian, P. B. (2018) · doi:10.18174/448425
Mohamed, M. S., Elbadry, M. I., & Yao, C. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-821269-1.00006-0
Tissue-location specific transcription programs drive tumor initiation dependencies in colon cancerPreprint
Easwaran, H., Yang, L., Tu, L., Petkovich, D. A., Thursby, S.-J., Bisht, S., Mao, Y., Gabrielson, K. L., Yen, R.-W. C., Largent, T., et al. (2023) · Research Square · doi:10.21203/rs.3.rs-2846349/v1
Ahmed, S. M., Awwad, A., Eddy, N., Weber, G., Shahid, Z., Sethi, Z., Labampa, J., Murphy, R., Roth, E. W., Gustafson, K., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.09.23.614374
Epithelial–Mesenchymal Transition Functions as a Driver for the Direct Conversion of Somatic Cells
Motohashi, T., Aoki, H., Kunisada, T., & Osawa, M. (2025) · Stem Cells and Development · doi:10.1089/scd.2024.0181
Suzuki, R., Horisawa, K., Maehara, K., Ohkawa, Y., & Suzuki, A. (2025) · Bioinformatics and Biology Insights · doi:10.1177/11779322251365042
Self-citationShi, X., Mekis, G., Simms, K. J., Gao, B., & Zhang, P. (2025) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2025.108959 · Cited by 1 · see citing works
Wei, H., Li, Y., Li, L., Hu, Q., Shi, M., Cheng, L., Jiang, X., Zhou, Y., Chen, S., Ji, Y., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22715340
Wei, H., Li, Y., Li, L., Hu, Q., Shi, M., Cheng, L., Jiang, X., Zhou, Y., Chen, S., Ji, Y., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22715337
Wei, H., Li, Y., Li, L., Hu, Q., Shi, M., Cheng, L., Jiang, X., Zhou, Y., Chen, S., Ji, Y., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22715352
Kawasaki, R., Takemoto, K., & Hamano, M. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.01.28.702229
Doğan, L. A. (2026) · Çukurova medical journal (Online)/Çukurova medical journal · doi:10.17826/cumj.1843737
Revisiting organoids and animal models in IBD
Balakrishnan, D. D., Tiwari, R., Goswami, S., Narang, H., & Ahuja, V. (2026) · Trends Open · doi:10.1016/j.treopn.2026.06.018
Goto, N., Miura, S., Kawamata, M., Horisawa, K., Suzuki, R., Miyata, T., Taniguchi, N., & Suzuki, A. (2026) · Stem Cell Reports · doi:10.1016/j.stemcr.2026.103056
Self-citation
- Authors
- Miura, S., & Suzuki, A.
- Affiliations
- Kyushu University (JP)
- Corresponding author
- Suzuki, Atsushi
- ORCID
- Suzuki, Atsushi
- Venue
- Cell Stem Cell
- Publisher
- Elsevier BV
- Published
- 2017-10
- Volume
- 21
- Issue
- 4
- Pages
- 456-471.e5
- ISSN
- 1875-9777 (ISSN-L)
- 1934-5909
- OpenAlex
- W2758459988
- Cited by
- 91
- References
- 40
- Citations by year
- 2026: 5 · 2025: 10 · 2024: 12 · 2023: 14 · 2022: 11 · 2021: 14 · 2020: 12 · 2019: 4 · 2018: 8 · 2017: 1
- FWCI
- 2.79
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell stem cell (publishedVersion)
- PubMed (publishedVersion)
- Kyushu University Institutional Repository (QIR) (Kyushu University) (submittedVersion)
- Institutional Repositories DataBase (IRDB) (submittedVersion)
- Funders
- Japan Society for the Promotion of Science (16H01850, 23112002, 25713014, FDG6J02459)
- Ministry of Education, Culture, Sports, Science and Technology
- Core Research for Evolutional Science and Technology
- Japan Agency for Medical Research and Development
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Pluripotent Stem Cells Research
- Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Digestive system and related health
- Keywords
- intestinal organoids, intestinal progenitor cells, fibroblast reprogramming, transcription factors, HNF4α, FOXA3, GATA6, CDX2, intestinal stem cells, organoid transplantation, self-renewal, human organoids
- MeSH terms
- Cell Self Renewal, Animals, Colon, Embryo, Mammalian, Fetus, Fibroblasts, Humans, Intestinal Mucosa, Intestines, Organoids, Regeneration, Stem Cells, Transcription Factors, Spheroids, Cellular, Cell Lineage, Transgenes, Gene Silencing, Stem Cell Transplantation, Receptors, G-Protein-Coupled, Tissue Culture Techniques, Cell Proliferation, Mice, Cellular Reprogramming
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