2D- and 3D-Based Intestinal Stem Cell Cultures for Personalized Medicine
Open accessAbstract
Colorectal cancer (CRC) is one of the most common cancers that have high occurrence and death in both males and females. As various factors have been found to contribute to CRC development, personalized therapies are critical for efficient treatment. To achieve this purpose, the establishment of patient-derived tumor models is critical for diagnosis and drug test. The establishment of three-dimensional (3D) organoid cultures and two-dimensional (2D) monolayer cultures of patient-derived epithelial tissues is a breakthrough for expanding living materials for later use. This review provides an overview of the different types of 2D- and 3D-based intestinal stem cell cultures, their potential benefits, and the drawbacks in personalized medicine in treatment of the intestinal disorders.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Wnt/β-catenin signaling is essential to maintain intestinal organoid growth.
“Wnt/β-catenin signaling is essential to maintain intestinal organoid growth26,27”
From A PROTAC peptide induces durable β-catenin degradation and suppresses Wnt-dependent intestinal cancer (2020) · cites this paper as [27]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
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
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
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 · 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
In vitro propagation and transcriptional profiling of human mammary stem/progenitor cellsPreprint
Dontu, G., Abdallah, W. M., Foley, J. M., Jackson, K. W., Clarke, M. F., Kawamura, M., & Wicha, M. S. (2003) · Genes & Development · doi:10.1101/gad.1061803 · Cited by 2,413 · see citing works
Prospective Derivation of a Living Organoid Biobank of Colorectal Cancer Patients
van de Wetering, M., Francies, H. E., Francis, J. M., Bounova, G., Iorio, F., Pronk, A., van Houdt, W., van Gorp, J., Taylor-Weiner, A., Kester, L., et al. (2015) · Cell · doi:10.1016/j.cell.2015.03.053 · Cited by 2,408 · see citing works
Fusobacterium nucleatum Promotes Chemoresistance to Colorectal Cancer by Modulating Autophagy
Yu, T., Guo, F., Yu, Y., Sun, T., Ma, D., Han, J., Qian, Y., Kryczek, I., Sun, D., Nagarsheth, N., et al. (2017) · Cell · doi:10.1016/j.cell.2017.07.008 · Cited by 2,198 · see citing works
Self-citationStem cells, self-renewal, and differentiation in the intestinal epithelium.
van der Flier, L. G., & Clevers, H. (2009) · Annual Review of Physiology · doi:10.1146/annurev.physiol.010908.163145 · Cited by 1,859 · see citing works
The complex world of WNT receptor signalling
Niehrs, C. (2012) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3470 · Cited by 1,481 · see citing works
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 · see citing works
Schwank, G., Koo, B.-K., Sasselli, V., Dekkers, J. F., Heo, I., Demircan, T., Sasaki, N., Boymans, S., Cuppen, E., van der Ent, C. K., et al. (2013) · Cell Stem Cell · doi:10.1016/j.stem.2013.11.002 · Cited by 1,424 · see citing works
Adult intestinal stem cells: critical drivers of epithelial homeostasis and regeneration
Barker, N. (2013) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3721 · Cited by 1,334 · see citing works
Severity of inflammation is a risk factor for colorectal neoplasia in ulcerative colitis
Rutter, M., Saunders, B., Wilkinson, K., Rumbles, S., Schofield, G., Kamm, M., Williams, C., Price, A., Talbot, I., & Forbes, A. (2004) · Gastroenterology · doi:10.1053/j.gastro.2003.11.010 · Cited by 1,255 · see citing works
The intestinal crypt, a prototype stem cell compartment
Clevers, H. (2013) · Cell · doi:10.1016/j.cell.2013.07.004 · Cited by 1,223 · see citing works
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 · see citing works
Modeling colorectal cancer using CRISPR-Cas9–mediated engineering of human intestinal organoids
Matano, M., Date, S., Shimokawa, M., Takano, A., Fujii, M., Ohta, Y., Watanabe, T., Kanai, T., & Sato, T. (2015) · Nature Medicine · doi:10.1038/nm.3802 · Cited by 1,135 · see citing works
Sequential cancer mutations in cultured human intestinal stem cells
Drost, J., van Jaarsveld, R. H., Ponsioen, B., Zimberlin, C., van Boxtel, R., Buijs, A., Sachs, N., Overmeer, R. M., Offerhaus, G. J., Begthel, H., et al. (2015) · Nature · doi:10.1038/nature14415 · Cited by 1,067 · see citing works
A functional CFTR assay using primary cystic fibrosis intestinal organoids
Dekkers, J. F., Wiegerinck, C. L., de Jonge, H. R., Bronsveld, I., Janssens, H. M., de Winter-de Groot, K. M., Brandsma, A. M., de Jong, N. W. M., Bijvelds, M. J. C., Scholte, B. J., et al. (2013) · Nature Medicine · doi:10.1038/nm.3201 · Cited by 999 · see citing works
APC, Signal transduction and genetic instability in colorectal cancer
Fodde, R., Smits, R., & Clevers, H. (2001) · Nature Reviews Cancer · doi:10.1038/35094067 · Cited by 937 · see citing works
Three-Dimensional Cell Cultures in Drug Discovery and Development
Fang, Y., & Eglen, R. M. (2017) · SLAS Discovery · doi:10.1177/1087057117696795 · Cited by 849 · see citing works
High-fat diet enhances stemness and tumorigenicity of intestinal progenitors
Beyaz, S., Mana, M., Roper, J., Kedrin, D., Saadatpour, A., Hong, S., Bauer-Rowe, K. E., Xifaras, M. E., Akkad, A., Arias, E., et al. (2016) · Nature · doi:10.1038/nature17173 · Cited by 840 · see citing works
Gupta, R. B., Harpaz, N., Itzkowitz, S. H., Hossain, S., Matula, S. R., Kornbluth, A. A., Bodian, C., & Ullman, T. A. (2007) · Gastroenterology · doi:10.1053/j.gastro.2007.08.001 · Cited by 789 · see citing works
A distinct role for Lgr5+ stem cells in primary and metastatic colon cancer
Melo, F. D. S. E., Kurtova, A. V., Harnoss, J. M., Kljavin, N. M., Hoeck, J. D., Hung, J., Anderson, J. E., Storm, E. E., Modrusan, Z. D., Koeppen, H., et al. (2017) · Nature · doi:10.1038/nature21713 · Cited by 782 · see citing works
The Intestinal Microbiota in Colorectal Cancer.
Tilg, H., Adolph, T. E., Gerner, R. R., & Moschen, A. R. (2018) · Cancer Cell · doi:10.1016/j.ccell.2018.03.004 · Cited by 777 · cited 1× · see citing works
“Reference [34] [34] [34–36,39,47,58,59,63] [31,32,34] [47,55,59] [47,54,59] [47,50,53,59] [57]”
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 · see citing works
Tanaka, T., Kohno, H., Suzuki, R., Yamada, Y., Sugie, S., & Mori, H. (2003) · Cancer Science · doi:10.1111/j.1349-7006.2003.tb01386.x · Cited by 732 · see citing works
Experimental Models of Inflammatory Bowel Diseases
Kiesler, P., Fuss, I. J., & Strober, W. (2015) · Cellular and Molecular Gastroenterology and Hepatology · doi:10.1016/j.jcmgh.2015.01.006 · Cited by 719 · see citing works
Paneth Cells: Maestros of the Small Intestinal Crypts
Clevers, H. C., & Bevins, C. L. (2013) · Annual Review of Physiology · doi:10.1146/annurev-physiol-030212-183744 · Cited by 699 · see citing works
Neural stem cells and neurospheres—re-evaluating the relationship
Reynolds, B. A., & Rietze, R. L. (2005) · Nature Methods · doi:10.1038/nmeth758 · Cited by 674 · see citing works
Nerve Growth Factor Promotes Gastric Tumorigenesis through Aberrant Cholinergic Signaling
Hayakawa, Y., Sakitani, K., Konishi, M., Asfaha, S., Niikura, R., Tomita, H., Renz, B. W., Tailor, Y. H., Macchini, M., Middelhoff, M. A., et al. (2016) · Cancer Cell · doi:10.1016/j.ccell.2016.11.005 · Cited by 577 · see citing works
Precision medicine for cancer with next-generation functional diagnostics
Friedman, A. A., Letai, A., Fisher, D. E., & Flaherty, K. T. (2015) · Nature Reviews Cancer · doi:10.1038/nrc4015 · Cited by 570 · see citing works
SIGNALING PATHWAYS IN INTESTINAL DEVELOPMENT AND CANCER
Sancho, E., Batlle, E., & Clevers, H. C. (2004) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.20.010403.092805 · Cited by 531 · see citing works
VanDussen, K. L., Marinshaw, J. M., Shaikh, N., Miyoshi, H., Moon, C., Tarr, P. I., Ciorba, M. A., & Stappenbeck, T. S. (2015) · Gut · doi:10.1136/gutjnl-2013-306651 · Cited by 525 · see citing works
Interplay between metabolic identities in the intestinal crypt supports stem cell function
Rodríguez-Colman, M. J., Schewe, M., Meerlo, M., Stigter, E., Gerrits, J., Pras-Raves, M., Sacchetti, A., Hornsveld, M., Oost, K. C., Snippert, H. J., et al. (2017) · Nature · doi:10.1038/nature21673 · Cited by 522 · see citing works
Subepithelial telocytes are an important source of Wnts that supports intestinal crypts
Shoshkes-Carmel, M., Wang, Y. J., Wangensteen, K. J., Tóth, B., Kondo, A., Massasa, E. E., Itzkovitz, S., & Kaestner, K. H. (2018) · Nature · doi:10.1038/s41586-018-0084-4 · Cited by 519 · see citing works
Jess, T., Loftus, E. V., Velayos, F. S., Harmsen, W. S., Zinsmeister, A. R., Smyrk, T. C., Schleck, C. D., Tremaine, W. J., Melton, L. J., Munkholm, P. S., et al. (2006) · Gastroenterology · doi:10.1053/j.gastro.2005.12.037 · Cited by 497 · see citing works
Weeber, F., van de Wetering, M., Hoogstraat, M., Dijkstra, K. K., Krijgsman, O., Kuilman, T., Gadellaa-van Hooijdonk, C. G. M., van der Velden, D. L., Peeper, D. S., Cuppen, E. P. J. G., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1516689112 · Cited by 482 · see citing works
A Metabolite-Triggered Tuft Cell-ILC2 Circuit Drives Small Intestinal Remodeling
Schneider, C., O’Leary, C. E., von Moltke, J., Liang, H.-E., Ang, Q. Y., Turnbaugh, P. J., Radhakrishnan, S., Pellizzon, M., Ma, A., & Locksley, R. M. (2018) · Cell · doi:10.1016/j.cell.2018.05.014 · Cited by 478 · see citing works
Cancer Cell Lines for Drug Discovery and Development
Wilding, J. L., & Bodmer, W. F. (2014) · Cancer Research · doi:10.1158/0008-5472.can-13-2971 · Cited by 432 · see citing works
Current View: Intestinal Stem Cells and Signaling
Scoville, D. H., Sato, T., He, X., & Li, L. (2008) · Gastroenterology · doi:10.1053/j.gastro.2008.01.079 · Cited by 416 · see citing works
GLI1-expressing mesenchymal cells form the essential Wnt-secreting niche for colon stem cells
Değirmenci, B., Valenta, T., Dimitrieva, S., Hausmann, G., & Basler, K. (2018) · Nature · doi:10.1038/s41586-018-0190-3 · Cited by 381 · see citing works
Saxena, K., Blutt, S. E., Ettayebi, K., Zeng, X.-L., Broughman, J. R., Crawford, S. E., Karandikar, U. C., Sastri, N. P., Conner, M. E., Opekun, A. R., et al. (2016) · Journal of Virology · doi:10.1128/jvi.01930-15 · Cited by 375 · see citing works
Başak, O., Beumer, J., Wiebrands, K., Seno, H., van Oudenaarden, A., & Clevers, H. C. (2016) · Cell stem cell · doi:10.1016/j.stem.2016.11.001 · Cited by 350 · see citing works
Parasitic helminths induce fetal-like reversion in the intestinal stem cell niche
Nusse, Y. M., Savage, A. K., Marangoni, P., Huber, A. R., Landman, T. A., de Sauvage, F. J., Locksley, R. M., & Klein, O. D. (2018) · Nature · doi:10.1038/s41586-018-0257-1 · Cited by 333 · see citing works
Qi, Z., Li, Y., Zhao, B., Xu, C., Liu, Y., Li, H., Zhang, B., Wang, X., Yang, X., Xie, W., et al. (2017) · Nature Communications · doi:10.1038/ncomms13824 · Cited by 320 · see citing works
Self-citationDirect regulation of intestinal fate by Notch
Stanger, B. Z., Datar, R., Murtaugh, L. C., & Melton, D. A. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0505690102 · Cited by 294 · see citing works
Regulation and plasticity of intestinal stem cells during homeostasis and regeneration
Beumer, J., & Clevers, H. C. (2016) · Development · doi:10.1242/dev.133132 · Cited by 286 · see citing works
Enteroendocrine cells switch hormone expression along the crypt-to-villus BMP signalling gradient
Beumer, J., Artegiani, B., Post, Y., Reimann, F. M., Gribble, F. M., Nguyen, T. N., Zeng, H., van den Born, M., van Es, J. H., & Clevers, H. C. (2018) · Nature Cell Biology · doi:10.1038/s41556-018-0143-y · Cited by 280 · see citing works
Personalized Cancer Medicine: An Organoid Approach
Es, H. A., Montazeri, L., Aref, A. R., Vosough, M., & Baharvand, H. (2018) · Trends in biotechnology · doi:10.1016/j.tibtech.2017.12.005 · Cited by 277 · see citing works
Targeting mutant RAS in patient-derived colorectal cancer organoids by combinatorial drug screening
Verissimo, C. S., Overmeer, R. M., Ponsioen, B., Drost, J., Mertens, S., Verlaan-Klink, I., Gerwen, B. V., van der Ven, M., Wetering, M. V. D., Egan, D. A., et al. (2016) · eLife · doi:10.7554/elife.18489 · Cited by 263 · see citing works
Stem cell dynamics in homeostasis and cancer of the intestine
Vermeulen, L., & Snippert, H. J. G. (2014) · Nature reviews. Cancer · doi:10.1038/nrc3744 · Cited by 250 · see citing works
Adult mammalian stem cells: the role of Wnt, Lgr5 and R‐spondins
Schuijers, J., & Clevers, H. C. (2012) · The EMBO Journal · doi:10.1038/emboj.2012.149 · Cited by 247 · see citing works
Yissachar, N., Zhou, Y., Ung, L., Lai, N. Y., Mohan, J. F., Ehrlicher, A., Weitz, D. A., Kasper, D. L., Chiu, I. M., Mathis, D., et al. (2017) · Cell · doi:10.1016/j.cell.2017.02.009 · Cited by 242 · see citing works
TP53 loss creates therapeutic vulnerability in colorectal cancer
Liu, Y., Zhang, X., Han, C., Wan, G., Huang, X., Ivan, C., Jiang, D., Rodriguez‐Aguayo, C., Lopez‐Berestein, G., Rao, P. H., et al. (2015) · Nature · doi:10.1038/nature14418 · Cited by 240 · see citing works
Self-citationEPITHELIAL CELL MIGRATION IN THE INTESTINE
Heath, J. P. (1996) · Cell Biology International · doi:10.1006/cbir.1996.0018 · Cited by 205 · see citing works
Self-renewing Monolayer of Primary Colonic or Rectal Epithelial Cells
Wang, Y., DiSalvo, M., Gunasekara, D. B., Dutton, J. S., Proctor, A., Lebhar, M. S., Williamson, I., Speer, J. E., Howard, R. L., Smiddy, N. M., et al. (2017) · Cellular and Molecular Gastroenterology and Hepatology · doi:10.1016/j.jcmgh.2017.02.011 · Cited by 200 · see citing works
Modeling rotavirus infection and antiviral therapy using primary intestinal organoids
Yin, Y., Bijvelds, M. J. C., Dang, W., Xu, L., van der Eijk, A. A., Knipping, K., Tüysüz, N., Dekkers, J. F., Wang, Y., de Jonge, J., et al. (2015) · Antiviral Research · doi:10.1016/j.antiviral.2015.09.010 · Cited by 196 · see citing works
Cloning and variation of ground state intestinal stem cells
Wang, X., Yamamoto, Y., Wilson, L., Zhang, T., Howitt, B. E., Farrow, M. A., Kern, F., Ning, G., Yue, H., Khor, C. C., et al. (2015) · Nature · doi:10.1038/nature14484 · Cited by 187 · see citing works
Development and Characterization of a Human and Mouse Intestinal Epithelial Cell Monolayer Platform
Kozuka, K., He, Y., Koo-McCoy, S., Kumaraswamy, P., Nie, B., Shaw, K., Chan, P., Leadbetter, M., He, L., Lewis, J. G., et al. (2017) · Stem Cell Reports · doi:10.1016/j.stemcr.2017.10.013 · Cited by 179 · see citing works
Organoid culture systems to study host–pathogen interactions
Dutta, D., & Clevers, H. C. (2017) · Current Opinion in Immunology · doi:10.1016/j.coi.2017.07.012 · Cited by 178 · see citing works
Crosstalk between Wnt and Notch signaling in intestinal epithelial cell fate decision
Nakamura, T., Tsuchiya, K., & Watanabe, M. (2007) · Journal of Gastroenterology · doi:10.1007/s00535-007-2087-z · Cited by 173 · see citing works
Fletcher, S. M., McLaws, M.-L., & Ellis, J. T. (2013) · Journal of Public Health Research · doi:10.4081/jphr.2013.e9 · Cited by 172 · see citing works
Thorne, C. A., Chen, I. W., Sanman, L. E., Cobb, M. H., Wu, L. F., & Altschuler, S. J. (2018) · Developmental Cell · doi:10.1016/j.devcel.2018.01.024 · Cited by 165 · see citing works
Praharaj, P. P., Bhutia, S. K., Nagrath, S., Bitting, R. L., & Deep, G. (2018) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2017.12.005 · Cited by 147 · see citing works
Abba, K., Sinfield, R., Hart, C. A., & Garner, P. (2009) · BMC Infectious Diseases · doi:10.1186/1471-2334-9-88 · Cited by 114 · see citing works
Ex vivo culture of the intestinal epithelium: strategies and applications
Leushacke, M., & Barker, N. (2014) · Gut · doi:10.1136/gutjnl-2014-307204 · Cited by 113 · see citing works
Puzan, M. L., Hosic, S., Ghio, C., & Koppes, A. N. (2018) · Scientific Reports · doi:10.1038/s41598-018-24768-3 · Cited by 100 · see citing works
Bioengineered Systems and Designer Matrices That Recapitulate the Intestinal Stem Cell Niche
Wang, Y., Kim, R., Hinman, S. S., Zwarycz, B., Magness, S. T., & Allbritton, N. L. (2018) · Cellular and Molecular Gastroenterology and Hepatology · doi:10.1016/j.jcmgh.2018.01.008 · Cited by 70 · see citing works
Zhao, B. T., Qi, Z., Li, Y., Wang, C., Fu, W., & Chen, Y. (2015) · Nature Communications · doi:10.1038/ncomms8166 · Cited by 67 · see citing works
Self-citationOrganoid Center Strategies for Accelerating Clinical Translation
Takebe, T., Wells, J. M., Helmrath, M. A., & Zorn, A. M. (2018) · Cell stem cell · doi:10.1016/j.stem.2018.05.008 · Cited by 64 · see citing works
Li, Y., Liu, Y., Liu, B., Wang, J., Wei, S., Qi, Z., Wang, S., Fu, W., & Chen, Y. (2018) · Cell Discovery · doi:10.1038/s41421-018-0051-0 · Cited by 59 · see citing works
Self-citationDNA-Guided Precision Medicine for Cancer: A Case of Irrational Exuberance?
Voest, E. E., & Bernards, R. (2016) · Cancer Discovery · doi:10.1158/2159-8290.cd-15-1321 · Cited by 54 · see citing works
Tong, Z., Martyn, K., Yang, A. W., Yin, X., Mead, B. E., Joshi, N., Sherman, N. E., Langer, R., & Karp, J. M. (2017) · Biomaterials · doi:10.1016/j.biomaterials.2017.10.038 · Cited by 52 · see citing works
BMP signaling in homeostasis, transformation and inflammatory response of intestinal epithelium
Wang, S., & Chen, Y. (2018) · Science China Life Sciences · doi:10.1007/s11427-018-9310-7 · Cited by 52 · see citing works
Self-citationMonolayer culture of intestinal epithelium sustains Lgr5+ intestinal stem cells
Liu, Y., Qi, Z., Li, X., Du, Y., & Chen, Y. (2018) · Cell Discovery · doi:10.1038/s41421-018-0036-z · Cited by 51 · see citing works
Self-citationRegulation of intestinal stem cell fate specification
Qi, Z., & Chen, Y. (2015) · Science China Life Sciences · doi:10.1007/s11427-015-4859-7 · Cited by 45 · see citing works
Self-citationScott, A., Rouch, J. D., Jabaji, Z. B., Khalil, H. A., Solorzano, S., Lewis, M. S., Martı́n, M. G., Stelzner, M. G., & Dunn, J. (2016) · Journal of Pediatric Surgery · doi:10.1016/j.jpedsurg.2016.02.074 · Cited by 42 · see citing works
Organoids, organs-on-chips and other systems, and microbiota
May, S., Evans, S., & Parry, L. (2017) · Emerging Topics in Life Sciences · doi:10.1042/etls20170047 · Cited by 36 · see citing works
Spheroid cultures promote the stemness of corneal stromal cells
Li, H., Dai, Y., Shu, J.-C., Yu, R., Guo, Y., & Chen, J. (2014) · Tissue and Cell · doi:10.1016/j.tice.2014.10.008 · Cited by 35 · see citing works
Genetics of the Serrated Pathway to Colorectal Cancer
Kedrin, D., & Gala, M. K. (2015) · Clinical and Translational Gastroenterology · doi:10.1038/ctg.2015.12 · Cited by 33 · see citing works
From 3D Organoids back to 2D Enteroids
Braverman, J., & Yilmaz, Ö. H. (2018) · Developmental Cell · doi:10.1016/j.devcel.2018.02.016 · Cited by 28 · see citing works
Human Intestinal Microbiota and Colorectal Cancer: Moving Beyond Associative Studies
Jobin, C. (2017) · Gastroenterology · doi:10.1053/j.gastro.2017.10.030 · Cited by 21 · see citing works
Hippo signalling directs intestinal fate
Bouteiller, M. L., & Jensen, K. B. (2014) · Nature Cell Biology · doi:10.1038/ncb3086 · Cited by 16 · see citing works
Techniques in Embryoid Body Formation from Human Pluripotent Stem Cells
Shevde, N. K., & Mael, A. A. (2012) · Methods in molecular biology · doi:10.1007/978-1-62703-128-8_33 · Cited by 15 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Liao, H., Li, X., Zhao, L., Wang, Y., Wang, X., Wu, Y., Zhou, X., Fu, W., Liu, L., Hu, H.-G., et al. (2020) · Cell Discovery · doi:10.1038/s41421-020-0171-1 · Cited by 156 · see citing works
Self-citationUnderstanding cell‐cell communication and signaling in the colorectal cancer microenvironment
AlMusawi, S., Ahmed, M., & Nateri, A. S. (2021) · Clinical and Translational Medicine · doi:10.1002/ctm2.308 · Cited by 150 · see citing works
Organoids: a promising new in vitro platform in livestock and veterinary research
Kar, S. K., Wells, J. M., Ellen, E. D., PAS, M. F. W. T., Madsen, O., Groenen, M. A. M., & Woelders, H. (2021) · Veterinary Research · doi:10.1186/s13567-021-00904-2 · Cited by 81 · see citing works
The development of a functional human small intestinal epithelium model for drug absorption
Kwon, O., Jung, K. B., Lee, K., Son, Y. S., Lee, H., Kim, J.-J., Kim, K., Lee, S., Song, Y.-K., Jung, J., et al. (2021) · Science Advances · doi:10.1126/sciadv.abh1586 · Cited by 70 · see citing works
Photoacoustic imaging of cells in a three-dimensional microenvironment
Liu, W., & Li, P. (2020) · Journal of Biomedical Science · doi:10.1186/s12929-019-0594-x · Cited by 47 · see citing works
Reconstructing the tumor architecture into organoids
Luo, Z., Zhou, X., Mandal, K., He, N., Wennerberg, W., Qu, M., Jiang, X., Sun, W., & Khademhosseini, A. (2021) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2021.113839 · Cited by 49 · see citing works
Generation of 3D human gastrointestinal organoids: principle and applications
Zhang, M., Liu, Y., & Chen, Y. (2020) · Cell Regeneration · doi:10.1186/s13619-020-00040-w · Cited by 43 · see citing works
Self-citationSignore, M. A., Pascali, C. D., Giampetruzzi, L., Siciliano, P. A., & Francioso, L. N. (2021) · Sensing and Bio-Sensing Research · doi:10.1016/j.sbsr.2021.100443 · Cited by 41 · see citing works
Patient-derived Tumour Organoids: A Bridge between Cancer Biology and Personalised Therapy
Wu, W., Li, X., & Yu, S. (2022) · Acta Biomaterialia · doi:10.1016/j.actbio.2022.04.050 · Cited by 39 · see citing works
Mayorgas, A., Dotti, I., Martínez‐Picola, M., Esteller, M., Bonet-Rossinyol, Q., Ricart, E., Salas, A., & Martínez-Medina, M. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.646906 · Cited by 27 · see citing works
Donkers, J. M., van der Vaart, J. I., & van de Steeg, E. (2023) · Biomimetics · doi:10.3390/biomimetics8020226 · Cited by 25 · see citing works
From air pollution to cardiovascular diseases: the emerging role of epigenetics
Micheu, M.-M., Birsan, M., Szép, R., Keresztesi, Á., & Niță, I.-A. (2020) · Molecular Biology Reports · doi:10.1007/s11033-020-05570-9 · Cited by 25 · see citing works
Rubert, J., Gatto, P., Pancher, M., Sidarovich, V., Curti, C., Mena, P. R., Rio, D. D., Quattrone, A., & Mattivi, F. (2022) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.202101043 · Cited by 23 · see citing works
Agarwal, T., Onesto, V., Lamboni, L., Ansari, A., Maiti, T. K., Makvandi, P., Vosough, M., & Yang, G. (2021) · Bio-Design and Manufacturing · doi:10.1007/s42242-020-00120-5 · Cited by 23 · see citing works
Effect of air–liquid interface on cultured human intestinal epithelial cells
Sabapaty, A., Lin, P., & Dunn, J. (2023) · FASEB BioAdvances · doi:10.1096/fba.2023-00132 · Cited by 20 · see citing works
Toward better drug development: Three-dimensional bioprinting in toxicological research
Szűcs, D., Fekete, Z., Guba, M., Kemény, L. V., Jemnitz, K., Kis, E., & Veréb, Z. (2023) · International Journal of Bioprinting · doi:10.18063/ijb.v9i2.663 · Cited by 21 · see citing works
Advanced Cellular Models for Rare Disease Study: Exploring Neural, Muscle and Skeletal Organoids
Bombieri, C., Corsi, A., Trabetti, E., Ruggiero, A., Marchetto, G., Vattemi, G. N. A., Valenti, M. T., Zipeto, D., & Romanelli, M. G. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25021014 · Cited by 22 · see citing works
Biomaterials and biosensors in intestinal organoid culture, a progress review
Huang, J., Jiang, Y., Ren, Y., Liu, Y., Wu, X., Li, Z., & Ren, J. (2020) · Journal of Biomedical Materials Research Part A · doi:10.1002/jbm.a.36921 · Cited by 20 · see citing works
Self-citationDing, L., Yang, Y., Lu, Q., Qu, D., Chandrakesan, P., Feng, H., Chen, H., Chen, X., Liao, Z., Jian, D., et al. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232113354 · Cited by 20 · see citing works
Acosta, M. P., Jeong, S., Utrero‐Rico, A., Goncharov, T., Webster, J. D., Holler, E., Morales, G., Dellepiane, S., Levine, J. E., Rothenberg, M. E., et al. (2023) · Science Translational Medicine · doi:10.1126/scitranslmed.adf8366 · Cited by 20 · see citing works
Research on water resource carrying capacity of capital water conservation functional zone
Qin, J., Niu, J., & Niu, W. (2023) · Frontiers in Environmental Science · doi:10.3389/fenvs.2022.1108631 · Cited by 14 · see citing works
Label-free imaging of 3D pluripotent stem cell differentiation dynamics on chip
Atwell, S. X., Waibel, D., Boushehri, S. S., Wiedenmann, S., Marr, C., & Meier, M. (2023) · Cell Reports Methods · doi:10.1016/j.crmeth.2023.100523 · Cited by 13 · see citing works
de Jonge, H. R., Ardelean, M. C., Bijvelds, M. J. C., & Vergani, P. (2020) · FEBS Letters · doi:10.1002/1873-3468.13971 · Cited by 13 · see citing works
Machado, M., Costa, E. M., Silva, S., Rodríguez-Alcalá, L. M., Gomes, A., & Pintado, M. (2023) · Molecules · doi:10.3390/molecules28155923 · Cited by 8 · see citing works
Ramal‐Sanchez, M., Bravo-Trippetta, C., D’Antonio, V., Corvaglia, E., Kämpfer, A. A. M., Schins, R. P. F., Serafini, M., & Angelino, D. (2025) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1545261 · Cited by 7 · see citing works
Gibbons, J., Yoo, J. Y., Mutka, T., Groer, M. E., & Ho, T. T. B. (2021) · mSphere · doi:10.1128/msphere.00806-21 · Cited by 6 · see citing works
Emerging Prospects for the Study of Colorectal Cancer Stem Cells using Patient-derived Organoids
Ding, L., Yang, Y., Lu, Q., Cao, Z., & Weygant, N. (2022) · Current Cancer Drug Targets · doi:10.2174/1568009622666220117124546 · Cited by 5 · see citing works
Salivary gland bioengineering - yesterday, today, tomorrow!
Iyer, J. S., Pillai, S., Munguia-López, J. G., Zhang, Y., Mielkozorova, M., & Tran, S. D. (2023) · PubMed · doi:10.14670/hh-18-580 · Cited by 5 · see citing works
Häfliger, J., Morsy, Y., Scharl, M. M., & Wawrzyniak, M. (2022) · Stem Cell Reviews and Reports · doi:10.1007/s12015-021-10307-7 · Cited by 3 · see citing works
A 3D Alginate–Gelatin Co-Culture Model to Study Epithelial–Stromal Interactions in the Gut
Tselekouni, P., Garakani, M. M., Papa, S., Kim, S. Y., Avramoglu, R. K., Wertheimer, M. R., Ajji, A., Lakatos, P. L., & Rosenzweig, D. H. (2026) · Gels · doi:10.3390/gels12010070 · Cited by 2 · see citing works
Tight Junctions in the Inflamed Gut
Encarnacion‐Garcia, M. R., & Nava, P. (2022) · Springer eBooks · doi:10.1007/978-3-030-97204-2_6 · Cited by 2 · see citing works
Hydrogels as three-dimensional scaffold materials in tissue engineering and as organoid platforms
Munguia-López, J. G., Pillai, S., Zhang, Y., Kort-Mascort, J., Zhu, Z., Kinsella, J. M., & Tran, S. D. (2023) · Elsevier eBooks · doi:10.1016/b978-0-12-823948-3.00038-5 · Cited by 2 · see citing works
Molehin, D., Guinan, J., & Lopez, B. S. (2024) · Journal of Visualized Experiments · doi:10.3791/65901 · Cited by 2 · see citing works
He, Z.-B., & Duan, X. (2026) · Animals and zoonoses. · doi:10.1016/j.azn.2026.06.007 · Cited by 1 · see citing works
Molehin, D., Guinan, J., & Lopez, B. S. (2024) · doi:10.3791/65901-v
Personalized Medicine Frontiers
Mondal, S., Priya, S., Bora, J., Lata, S., Mahalka, A. K., & Malik, S. (2025) · doi:10.1002/9781394313785.ch13
Rader, A. G., & Ribeiro, C. M. S. (2026) · STAR Protocols · doi:10.1016/j.xpro.2026.104740
- Authors
- Liu, Y., & Chen, Y.-G.
- Affiliations
- Center for Life Sciences (CN)
- Corresponding author
- Chen, Ye-Guang
- Venue
- Cells
- Publisher
- MDPI AG
- Published
- 2018-11-22
- Volume
- 7
- Issue
- 12
- Pages
- 225
- ISSN
- 2073-4409 (ISSN-L)
- PMC
- PMC6316377
- OpenAlex
- W2901078894
- Cited by
- 37
- References
- 84
- Citations by year
- 2026: 3 · 2025: 2 · 2024: 2 · 2023: 10 · 2022: 6 · 2021: 8 · 2020: 6
- FWCI
- 0.37
- Type
- journal article
- Language
- en
- Open access
- gold
- dx.doi.org
- Licence
- Locations
- Cells (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, other-oa)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Natural Science Foundation of China (31330049)
- National Key Research and Development Program of China (2017YFA0103601)
- Topics
- Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
- Physical Sciences › Engineering › Biomedical Engineering › 3D Printing in Biomedical Research
- Health Sciences › Medicine › Oncology › Colorectal Cancer Treatments and Studies
- Keywords
- intestinal stem cells, colorectal cancer, organoids, patient-derived tumor models, monolayer culture, personalized medicine, drug testing, 3D cell culture
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 ›
Are you an author, or do you see a problem with this page? Request a review
