Growth of Epithelial Organoids in a Defined Hydrogel
Open accessAbstract
Epithelial organoids are simplified models of organs grown in vitro from embryonic and adult stem cells. They are widely used to study organ development and disease, and enable drug screening in patient‐derived primary tissues. Current protocols, however, rely on animal‐ and tumor‐derived basement membrane extract (BME) as a 3D scaffold, which limits possible applications in regenerative medicine. This prompted us to study how organoids interact with their matrix, and to develop a well‐defined hydrogel that supports organoid generation and growth. It is found that soft fibrin matrices provide suitable physical support, and that naturally occurring Arg‐Gly‐Asp (RGD) adhesion domains on the scaffold, as well as supplementation with laminin‐111, are key parameters required for robust organoid formation and expansion. The possibility to functionalize fibrin via factor XIII‐mediated anchoring also allows to covalently link fluorescent nanoparticles to the matrix for 3D traction force microscopy. These measurements suggest that the morphogenesis of budding intestinal organoids results from internal pressure combined with higher cell contractility in the regions containing differentiated cells compared to the regions containing stem cells. Since the fibrin/laminin matrix supports long‐term expansion of all tested murine and human epithelial organoids, this hydrogel can be widely used as a defined equivalent to BME.
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?
Other matrices with defined compositions, such as recombinant human collagen, fibrin, or synthetic hydrogels, have been explored as alternatives to Matrigel.
“Therefore, other matrices with defined compositions64 have been explored as alternative matrices to Matrigel, such as recombinant human collagen62, fibrin65, or synthetic hydrogels3,63.”
From Organoids (2022) · cites this paper as [64]
Fibrin supplemented with laminin-111 is capable of supporting various murine and human epithelial organoids.
“Other examples are vitrified collagen I for human intestinal organoids86 and murine renal organoids87, as well as fibrin supplemented with laminin-111 capable of supporting various murine and human epithelial organoids88.”
From Towards organoid culture without Matrigel (2021) · cites this paper as [88]
A Matrigel culture system had a pore size smaller than 200 nm, or the resolution limit of their confocal microscope, but a fibrin-based material had a pore size closer to 4 microns; these materials had comparable elastic moduli and colony-forming efficiency.
“Broguiere and coworkers found that a Matrigel culture system had a pore size smaller than 200 nm, or the resolution limit of their confocal microscope, but that a fibrin-based material had a pore size closer to 4 microns; these materials had comparable elastic moduli and colony-forming efficiency88.”
From Towards organoid culture without Matrigel (2021) · cites this paper as [88]
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
Modeling Development and Disease with Organoids
Clevers, H. (2016) · Cell · doi:10.1016/j.cell.2016.05.082 · Cited by 3,196 · 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
Patient-derived organoids model treatment response of metastatic gastrointestinal cancers
Vlachogiannis, G., Hedayat, S., Vatsiou, A., Jamin, Y., Fernández-Mateos, J., Khan, K., Lampis, A., Eason, K., Huntingford, I., Burke, R., et al. (2018) · Science · doi:10.1126/science.aao2774 · Cited by 2,096 · see citing works
A living biobank of breast cancer organoids captures disease heterogeneity
Sachs, N., de Ligt, J., Kopper, O., Gogola, E., Bounova, G., Weeber, F., Balgobind, A. V., Wind, K., Gracanin, A., Begthel, H., et al. (2018) · Cell · doi:10.1016/j.cell.2017.11.010 · Cited by 1,973 · see citing works
Designing Cell-Compatible Hydrogels for Biomedical Applications
Seliktar, D. (2012) · Science · doi:10.1126/science.1214804 · Cited by 1,930 · see citing works
Directed differentiation of human pluripotent stem cells into intestinal tissue in vitro
Spence, J., Mayhew, C., Rankin, S., Kuhar, M., Vallance, J. E., Tolle, K., Hoskins, E. E., Kalinichenko, V., Wells, S., Zorn, A., et al. (2010) · Nature · doi:10.1038/nature09691 · Cited by 1,850 · see citing works
Matrigel: Basement membrane matrix with biological activity
Kleinman, H. K., & Martin, G. R. (2005) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2005.05.004 · Cited by 1,673 · see citing works
Matrigel: A complex protein mixture required for optimal growth of cell culture
Hughes, C. S., Postovit, L. M., & Lajoie, G. A. (2010) · PROTEOMICS · doi:10.1002/pmic.200900758 · Cited by 1,534 · see citing works
Eiraku, M., Watanabe, K., Matsuo-Takasaki, M., Kawada, M., Yonemura, S., Matsumura, M., Wataya, T., Nishiyama, A., Muguruma, K., & Sasai, Y. (2008) · Cell Stem Cell · doi:10.1016/j.stem.2008.09.002 · Cited by 1,522 · see citing works
Lutolf, M. P., Lauer-Fields, J. L., Schmoekel, H. G., Metters, A. T., Weber, F. E., Fields, G. B., & Hubbell, J. A. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0737381100 · Cited by 1,508 · see citing works
Human primary liver cancer–derived organoid cultures for disease modeling and drug screening
Broutier, L., Mastrogiovanni, G., Verstegen, M. M., Francies, H. E., Gavarró, L. M., Bradshaw, C. R., Allen, G. E., Arnes-Benito, R., Sidorova, O., Gaspersz, M. P., et al. (2017) · Nature Medicine · doi:10.1038/nm.4438 · Cited by 1,471 · see citing works
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 · 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
Self-citationSingle-cell messenger RNA sequencing reveals rare intestinal cell types
Grün, D., Lyubimova, A., Kester, L., Wiebrands, K., Basak, O., Sasaki, N., Clevers, H., & van Oudenaarden, A. (2015) · Nature · doi:10.1038/nature14966 · Cited by 1,234 · 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
Broutier, L., Andersson-Rolf, A., Hindley, C. J., Boj, S. F., Clevers, H., Koo, B.-K., & Huch, M. (2016) · Nature Protocols · doi:10.1038/nprot.2016.097 · Cited by 834 · see citing works
Vukicevic, S., Kleinman, H. K., Luyten, F. P., Roberts, A. B., Roche, N. S., & Reddi, A. H. (1992) · Experimental Cell Research · doi:10.1016/0014-4827(92)90397-q · Cited by 696 · see citing works
Raeber, G. P., Lütolf, M. P., & Hubbell, J. A. (2005) · Biophysical Journal · doi:10.1529/biophysj.104.050682 · Cited by 576 · see citing works
Niche-independent high-purity cultures of Lgr5+ intestinal stem cells and their progeny
Yin, X., Farin, H. F., van Es, J. H., Clevers, H. C., Langer, R., & Karp, J. M. (2013) · Nature Methods · doi:10.1038/nmeth.2737 · Cited by 571 · see citing works
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 · see citing works
Modeling mouse and human development using organoid cultures
Huch, M., & Koo, B. (2015) · Development · doi:10.1242/dev.118570 · Cited by 543 · see citing works
Mills, R. J., Titmarsh, D. M., Koenig, X., Parker, B. L., Ryall, J. G., Quaife-Ryan, G. A., Voges, H. K., Hodson, M. P., Ferguson, C., Drowley, L., et al. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1707316114 · Cited by 478 · see citing works
Enzymatic incorporation of bioactive peptides into fibrin matrices enhances neurite extension
Schense, J. C., Bloch, J., Aebischer, P., & Hubbell, J. A. (2000) · Nature Biotechnology · doi:10.1038/74473 · Cited by 339 · see citing works
Fibrin Sealant: Past, Present, and Future: A Brief Review
Spotnitz, W. D. (2009) · World Journal of Surgery · doi:10.1007/s00268-009-0252-7 · Cited by 339 · see citing works
Schütte, M., Risch, T., Abdavi-Azar, N., Boehnke, K., Schumacher, D., Keil, M., Yildirimman, R., Jandrasits, C., Borodina, T. A., Amstislavskiy, V. S., et al. (2017) · Nature Communications · doi:10.1038/ncomms14262 · Cited by 333 · see citing works
Human matrix metalloproteinase specificity studies using collagen sequence-based synthetic peptides
Nagase, H., & Fields, G. B. (1996) · Biopolymers · doi:10.1002/(sici)1097-0282(1996)40:4 · Cited by 318 · see citing works
Cross-Linking Exogenous Bifunctional Peptides into Fibrin Gels with Factor XIIIa
Schense, J. C., & Hubbell, J. A. (1998) · Bioconjugate Chemistry · doi:10.1021/bc9800769 · Cited by 311 · see citing works
The amino acid sequence of the α-chain of human fibrinogen
Doolittle, R. F., Watt, K. W. K., Cottrell, B. A., Strong, D. D., & Riley, M. (1979) · Nature · doi:10.1038/280464a0 · Cited by 305 · see citing works
Enzymatic formation of modular cell-instructive fibrin analogs for tissue engineering
Ehrbar, M., Rizzi, S. C., Hlushchuk, R., Djonov, V., Zisch, A. H., Hubbell, J. A., Weber, F. E., & Lütolf, M. P. (2007) · Biomaterials · doi:10.1016/j.biomaterials.2007.03.027 · Cited by 233 · see citing works
Cerina, F., Zhu, Z., Chessa, A., & Riccaboni, M. (2015) · PLoS ONE · doi:10.1371/journal.pone.0134025 · Cited by 229 · see citing works
Sakiyama‐Elbert, S. E., Schense, J. C., & Hubbell, J. A. (1999) · The FASEB Journal · doi:10.1096/fasebj.13.15.2214 · Cited by 190 · see citing works
Advancing Intestinal Organoid Technology Toward Regenerative Medicine
Nakamura, T., & Sato, T. (2017) · Cellular and Molecular Gastroenterology and Hepatology · doi:10.1016/j.jcmgh.2017.10.006 · Cited by 118 · see citing works
Novel enzymatically cross-linked hyaluronan hydrogels support the formation of 3D neuronal networks
Broguière, N., Isenmann, L., & Zenobi‐Wong, M. (2016) · Biomaterials · doi:10.1016/j.biomaterials.2016.04.036 · Cited by 116 · see citing works
Self-citationÖztürk, E., Arlov, Ø., Aksel, S., Li, L., Ornitz, D. M., Skjåk‐Bræk, G., & Zenobi‐Wong, M. (2016) · Advanced Functional Materials · doi:10.1002/adfm.201600092 · Cited by 96 · see citing works
Self-citationUltrasoft Alginate Hydrogels Support Long-Term Three-Dimensional Functional Neuronal Networks
Palazzolo, G., Broguière, N., Cenciarelli, O., Dermutz, H., & Zenobi‐Wong, M. (2015) · Tissue Engineering Part A · doi:10.1089/ten.tea.2014.0518 · Cited by 52 · see citing works
Self-citationTodorov, I., Omori, K., Pascual, M., Rawson, J., Nair, I., Valiente, L., Vuong, T., Matsuda, T., Orr, C., Ferreri, K., et al. (2006) · Pancreas · doi:10.1097/01.mpa.0000202945.78331.93 · Cited by 42 · see citing works
Zhu, Z., Puliga, M., Cerina, F., Chessa, A., & Riccaboni, M. (2015) · PLoS ONE · doi:10.1371/journal.pone.0126699 · Cited by 38 · see citing works
Ząbczyk, M., Blombäck, M., Majewski, J., Karkowski, G., Wallén, H., Undas, A., & He, S. (2014) · Thrombosis and Haemostasis · doi:10.1160/th14-07-0591 · Cited by 32 · see citing works
Flagged first, then by citations
Research works printed but not linked: 42
- H. Clevers, Cell 2016, 165, 1586.
- G. Vlachogiannis, S. Hedayat, A. Vatsiou, Y. Jamin, J. Fernández-Mateos, K. Khan, A. Lampis, K. Eason, I. Huntingford, R. Burke, M. Rata, D.-M. Koh, N. Tunariu, D. Collins, S. Hulkki-Wilson, C. Ragulan, I. Spiteri, S. Y. Moorcraft, I. Chau, S. Rao, D. Watkins, N. Fotiadis, M. Bali, M. Darvish-Damavandi, H. Lote, Z. Eltahir, E. C. Smyth, R. Begum, P. A. Clarke, J. C. Hahne, M. Dowsett, J. de Bono, P. Workman, A. Sadanandam, M. Fassan, O. J. Sansom, S. Eccles, N. Starling, C. Braconi, A. Sottoriva, S. P. Robinson, D. Cunningham, N. Valeri, Science 2018, 359, 920.
- N. Sachs, J. de Ligt, O. Kopper, E. Gogola, G. Bounova, F. Weeber, A. V. Balgobind, K. Wind, A. Gracanin, H. Begthel, J. Korving, R. van Boxtel, A. A. Duarte, D. Lelieveld, A. van Hoeck, R. F. Ernst, F. Blokzijl, I. J. Nijman, M. Hoogstraat, M. van de Ven, D. A. Egan, V. Zinzalla, J. Moll, S. F. Boj, E. E. Voest, L. Wessels, P. J. van Diest, S. Rottenberg, R. G. J. Vries, E. Cuppen, H. Clevers, Cell 2018, 172, 373.e10.
- M. Schutte, T. Risch, N. Abdavi-Azar, K. Boehnke, D. Schumacher, M. Keil, R. Yildiriman, C. Jandrasits, T. Borodina, V. Amstislavskiy, C. L. Worth, C. Schweiger, S. Liebs, M. Lange, H.-J. Warnatz, L. M. Butcher, J. E. Barrett, M. Sultan, C. Wierling, N. Golob-Schwarzl, S. Lax, S. Uranitsch, M. Becker, Y. Welte, J. L. Regan, M. Silvestrov, I. Kehler, A. Fusi, T. Kessler, R. Herwig, U. Landegren, D. Wienke, M. Nilsson, J. A. Velasco, P. Garin-Chesa, C. Reinhard, S. Beck, R. Schäfer, C. R. A. Regenbrecht, D. Henderson, B. Lange, J. Haybaeck, U. Keilholz, J. Hoffmann, H. Lehrach, M.-L. Yaspo, Nat. Commun. 2017, 8, 14262.
- M. van de Wetering, H. Francies, J. Francis, G. Bounova, F. Iorio, A. Pronk, W. van Houdt, J. van Gorp, A. Taylor-Weiner, L. Kester, A. McLaren-Douglas, J. Blokker, S. Jaksani, S. Bartfeld, R. Volckman, P. van Sluis, V. Li, S. Seepo, C. Sekhar Pedamallu, K. Cibulskis, S. Carter, A. McKenna, M. Lawrence, L. Lichtenstein, C. Stewart, J. Koster, R. Versteeg, A. van Oudenaarden, J. Saez-Rodriguez, R. Vries, G. Getz, L. Wessels, M. Stratton, U. McDermott, M. Meyerson, M. Garnett, H. Clevers, Cell 2015, 161, 933.
- L. Broutier, G. Mastrogiovanni, M. M. Verstegen, H. E. Francies, L. M. Gavarró, C. R. Bradshaw, G. E. Allen, R. Arnes-Benito, O. Sidorova, M. P. Gaspersz, N. Georgakopoulos, B.-K. Koo, S. Dietmann, S. E. Davies, R. K. Praseedom, R. Lieshout, J. N. M. IJzermans, S. J. Wigmore, K. Saeb-Parsy, M. J. Garnett, L. J. van der Laan, M. Huch, Nat. Med. 2017, 23, 1424.
- R. J. Mills, D. M. Titmarsh, X. Koenig, B. L. Parker, J. G. Ryall, G. A. Quaife-Ryan, H. K. Voges, M. P. Hodson, C. Ferguson, L. Drowley, A. T. Plowright, E. J. Needham, Q.-D. Wang, P. Gregorevic, M. Xin, W. G. Thomas, R. G. Parton, L. K. Nielsen, B. S. Launikonis, D. E. James, D. A. Elliott, E. R. Porrello, J. E. Hudson, Proc. Natl. Acad. Sci. USA 2017, 114, E8372.
- G. Schwank, B.-K. Koo, V. Sasselli, J. Dekkers, I. Heo, T. Demircan, N. Sasaki, S. Boymans, E. Cuppen, C. van der Ent, E. Nieuwenhuis, J. Beekman, H. Clevers, Cell Stem Cell 2013, 13, 653.
- T. Nakamura, T. Sato, Cell. Mol. Gastroenterol. Hepatol. 2018, 5, 51.
- T. Sato, R. G. Vries, H. J. Snippert, M. van de Wetering, N. Barker, D. E. Stange, J. H. van Es, A. Abo, P. Kujala, P. J. Peters, H. Clevers, Nature 2009, 459, 262.
- D. Grün, A. Lyubimova, L. Kester, K. Wiebrands, O. Basak, N. Sasaki, H. Clevers, A. van Oudenaarden, Nature 2015, 525, 251.
- M. Huch, B.-K. Koo, Development 2015, 142, 3113.
- J. R. Spence, C. N. Mayhew, S. A. Rankin, M. F. Kuhar, J. E. Vallance, K. Tolle, E. E. Hoskins, V. V. Kalinichenko, S. I. Wells, A. M. Zorn, N. F. Shroyer, J. M. Wells, Nature 2011, 470, 105.
- T. Nakano, S. Ando, N. Takata, M. Kawada, K. Muguruma, K. Sekiguchi, K. Saito, S. Yonemura, M. Eiraku, Y. Sasai, Cell Stem Cell 2012, 10, 771.
- M. A. Lancaster, M. Renner, C.-A. Martin, D. Wenzel, L. S. Bicknell, M. E. Hurles, T. Homfray, J. M. Penninger, A. P. Jackson, J. A. Knoblich, Cell Stem Cell 2008, 3, 519.
- M. Eiraku, K. Watanabe, M. Matsuo-Takasaki, M. Kawada, S. Yonemura, M. Matsumura, T. Wataya, A. Nishiyama, K. Muguruma, Y. Sasai, Cell Stem Cell 2008, 3, 519.
- M. A. Lancaster, J. A. Knoblich, Proteomics 2010, 10, 1886.
- C. S. Hughes, L. M. Postovit, G. a. Lajoie, Proteomics 2010, 10, 1886.
- S. Vukicevic, H. K. Kleinman, F. P. Luyten, A. B. Roberts, N. S. Roche, A. Reddi, Exp. Cell Res. 1992, 202, 1.
- H. K. Kleinman, G. R. Martin, Semin. Cancer Biol. 2005, 15, 378.
- D. Seliktar, Science 2012, 336, 1124.
- N. Gjorevski, N. Sachs, A. Manfrin, S. Giger, M. E. Bragina, P. Ordóñez-Morán, H. Clevers, M. P. Lutolf, Nature 2016, 539, 560.
- R. Cruz-Acuña, M. Quirós, A. E. Farkas, P. H. Dedhia, S. Huang, D. Siuda, V. García-Hernández, A. J. Miller, J. R. Spence, A. Nusrat, A. J. García, Nat. Cell Biol. 2017, 19, 1326.
- M. Ehrbar, S. C. Rizzi, R. Hlushchuk, V. Djonov, A. H. Zisch, J. A. Hubbell, F. E. Weber, M. P. Lutolf, Biomaterials 2007, 28, 3856.
- N. Broguiere, L. Isenmann, M. Zenobi-Wong, Biomaterials 2016, 99, 47.
- G. Palazzolo, N. Broguiere, O. Cenciarelli, H. Dermutz, M. Zenobi-Wong, Tissue Eng., Part A 2015, 21, 2177.
- W. D. Spotnitz, World J. Surg. 2010, 34, 632.
- H. Nagase, G. B. Fields, Biopolymers 1996, 40, 339.
- M. P. Lutolf, J. L. Lauer-Fields, H. G. Schmoekel, A. T. Metters, F. E. Weber, G. B. Fields, J. A. Hubbell, Proc. Natl. Acad. Sci. USA 2003, 100, 5413.
- E. Öztürk, Ø. Arlov, S. Aksel, L. Li, D. M. Ornitz, G. Skjak-Braek, M. Zenobi-Wong, Adv. Funct. Mater. 2016, 26, 3649.
- J. Zhu, L. Liang, Y. Jiao, L. Liu, PLoS One 2015, 10, 1.
- M. Z bczyk, M. Blombäck, J. Majewski, G. Karkowski, H. N. Wallen, A. Undas, S. He, Thromb. Haemostasis 2015, 113, 851.
- G. Raeber, M. Lutolf, J. Hubbell, Biophys. J. 2005, 89, 1374.
- J. F. Dekkers, C. L. Wiegerinck, H. R. de Jonge, I. Bronsveld, H. M. Janssens, K. M. de Winter-de Groot, A. M. Brandsma, N. W. M. de Jong, M. J. C. Bijvelds, B. J. Scholte, E. E. S. Nieuwenhuis, S. van den Brink, H. Clevers, C. K. van der Ent, S. Middendorp, J. M. Beekman, Nat. Med. 2013, 19, 939.
- I. Todorov, K. Omori, M. Pascual, J. Rawson, I. Nair, L. Valiente, T. Vuong, T. Matsuda, C. Orr, K. Ferreri, C. V. Smith, F. Kandeel, Y. Mullen, Pancreas 2006, 32, 130.
- S. E. Sakiyama, J. C. Schense, J. A. Hubbell, FASEB J. 1999, 13, 2214.
- J. C. Schense, J. Bloch, P. Aebischer, J. A. Hubbell, Nat. Biotechnol. 2000, 18, 415.
- M. van de Wetering, H. Francies, J. Francis, G. Bounova, F. Iorio, A. Pronk, W. van Houdt, J. van Gorp, A. Taylor-Weiner, L. Kester, A. McLaren-Douglas, J. Blokker, S. Jaksani, S. Bartfeld, R. Volckman, P. van Sluis, V. Li, S. Seepo, C. Sekhar Pedamallu, K. Cibulskis, S. Carter, A. McKenna, M. Lawrence, L. Lichtenstein, C. Stewart, J. Koster, R. Versteeg, A. van Oudenaarden, J. Saez-Rodriguez, R. Vries, G. Getz, L. Wessels, M. Stratton, U. McDermott, M. Meyerson, M. Garnett, H. Clevers, Cell 2015, 161, 933.
- L. Broutier, A. Andersson-Rolf, C. J. Hindley, S. F. Boj, H. Clevers, B.-K. Koo, M. Huch, Nat. Protoc. 2016, 11, 1724.
- J. C. Schense, J. A. Hubbell, Bioconjug. Chem. 1999, 10, 75.
- R. F. Doolittle, K. W. K. Watt, B. A. Cottrell, D. D. Strong, M. Riley, Nature 1979, 280, 464.
- X. Yin, H. F. Farin, J. H. van Es, H. Clevers, R. Langer, J. M. Karp, Nat. Methods 2014, 11, 106. Adv. Mater. 2018, 30, 1801621
Cited by
Sorted by citations
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 · see citing works
Hofer, M., & Lutolf, M. P. (2021) · Nature Reviews Materials · doi:10.1038/s41578-021-00279-y · Cited by 1,184 · see citing works
Zhao, Z., Chen, X., Dowbaj, A. M., Sljukic, A., Bratlie, K., Lin, L., Fong, E. L. S., Balachander, G. M., Chen, Z., Soragni, A., et al. (2022) · Nature Reviews Methods Primers · doi:10.1038/s43586-022-00174-y · Cited by 1,001 · see citing works
Next-generation cancer organoids
LeSavage, B. L., Suhar, R. A., Broguière, N., Lütolf, M. P., & Heilshorn, S. C. (2021) · Nature Materials · doi:10.1038/s41563-021-01057-5 · Cited by 462 · see citing works
Engineered materials for organoid systems
Kratochvil, M. J., Seymour, A. J., Li, T. L., Pașca, S. P., Kuo, C. J., & Heilshorn, S. C. (2019) · Nature Reviews Materials · doi:10.1038/s41578-019-0129-9 · Cited by 413 · see citing works
Towards organoid culture without Matrigel
Kozlowski, M. T., Crook, C. J., & Ku, H. T. (2021) · Communications Biology · doi:10.1038/s42003-021-02910-8 · Cited by 409 · see citing works
Self-healing conductive hydrogels: preparation, properties and applications
Deng, Z., Wang, H., Ma, P. X., & Guo, B. (2019) · Nanoscale · doi:10.1039/c9nr09283h · Cited by 385 · see citing works
Engineering Stem Cell Self-organization to Build Better Organoids
Brassard, J. A., & Lütolf, M. P. (2019) · Cell stem cell · doi:10.1016/j.stem.2019.05.005 · Cited by 379 · see citing works
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 · see citing works
Advances in Hydrogels in Organoids and Organs‐on‐a‐Chip
Liu, H., Wang, Y., Cui, K., Guo, Y., Zhang, X., & Qin, J. (2019) · Advanced Materials · doi:10.1002/adma.201902042 · Cited by 353 · see citing works
Building 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 · see citing works
Self-citationSynthetic dynamic hydrogels promote degradation-independent in vitro organogenesis
Chrisnandy, A., Blondel, D., Rezakhani, S., Broguiere, N., & Lutolf, M. P. (2022) · Nature Materials · doi:10.1038/s41563-021-01136-7 · Cited by 237 · see citing works
Engineering Multi‐Cellular Spheroids for Tissue Engineering and Regenerative Medicine
Kim, S., Kim, E. M., Yamamoto, M., Park, H., & Shin, H. (2020) · Advanced Healthcare Materials · doi:10.1002/adhm.202000608 · Cited by 233 · see citing works
Pérez-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 · see citing works
Mechano-modulatory synthetic niches for liver organoid derivation
Sorrentino, G., Rezakhani, S., Yildiz, E., Nuciforo, S., Heim, M. H., Lutolf, M. P., & Schoonjans, K. (2020) · Nature Communications · doi:10.1038/s41467-020-17161-0 · Cited by 224 · see citing works
Self-citationBioengineering 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 · see citing works
Crosstalk between Bone and Nerves within Bone
Wan, Q., Qin, W., Ma, Y., Shen, M., Li, J., Zhang, Z., Chen, J., Tay, F. R., Niu, L., & Jiao, K. (2021) · Advanced Science · doi:10.1002/advs.202003390 · Cited by 214 · see citing works
AI-enabled organoids: Construction, analysis, and application
Bai, L., Wu, Y., Li, G., Zhang, W., Zhang, H., & Su, J. (2023) · Bioactive Materials · doi:10.1016/j.bioactmat.2023.09.005 · Cited by 216 · see citing works
A Droplet Microfluidic System to Fabricate Hybrid Capsules Enabling Stem Cell Organoid Engineering
Liu, H., Wang, Y., Wang, H., Zhao, M., Tao, T., Zhang, X., & Qin, J. (2020) · Advanced Science · doi:10.1002/advs.201903739 · Cited by 191 · see citing works
Mechanics of 3D Cell–Hydrogel Interactions: Experiments, Models, and Mechanisms
Vernerey, F. J., Sridhar, S. L., Muralidharan, A., & Bryant, S. J. (2021) · Chemical Reviews · doi:10.1021/acs.chemrev.1c00046 · Cited by 183 · see citing works
In Vitro three-dimensional (3D) cell culture tools for spheroid and organoid models
Lee, S., Koo, I.-S., Hwang, H. J., & Lee, D. W. (2023) · SLAS DISCOVERY · doi:10.1016/j.slasd.2023.03.006 · Cited by 184 · see citing works
Hernandez‐Gordillo, V., Kassis, T., Lampejo, A. O., Choi, G., Gamboa, M. E., Gnecco, J. S., Brown, A., Breault, D. T., Carrier, R. L., & Griffith, L. G. (2019) · Biomaterials · doi:10.1016/j.biomaterials.2020.120125 · Cited by 177 · see citing works
Organoids to model liver disease
Nuciforo, S., & Heim, M. H. (2021) · JHEP Reports · doi:10.1016/j.jhepr.2020.100198 · Cited by 164 · see citing works
Self-citationA Chemically Defined Hydrogel for Human Liver Organoid Culture
Ye, S., Boeter, J. W. B., Mihajlovic, M., van Steenbeek, F. G., van Wolferen, M. E., Oosterhoff, L. A., Marsee, A., Caiazzo, M., van der Laan, L. J. W., Penning, L. C., et al. (2020) · Advanced Functional Materials · doi:10.1002/adfm.202000893 · Cited by 165 · see citing works
IFlowPlate—A Customized 384‐Well Plate for the Culture of Perfusable Vascularized Colon Organoids
Rajasekar, S., Lin, D. S. Y., Abdul, L., Liu, A. W. K., Sotra, A., Zhang, F., & Zhang, B. (2020) · Advanced Materials · doi:10.1002/adma.202002974 · Cited by 167 · see citing works
Promising Applications of Tumor Spheroids and Organoids for Personalized Medicine
Gilazieva, Z., Ponomarev, A. S., Rutland, C. S., Rizvanov, A. A., & Solovyeva, V. V. (2020) · Cancers · doi:10.3390/cancers12102727 · Cited by 150 · see citing works
Cell therapy for advanced liver diseases: repair or rebuild
Dwyer, B. J., Macmillan, M. T., Brennan, P. N., & Forbes, S. J. (2021) · Journal of Hepatology · doi:10.1016/j.jhep.2020.09.014 · Cited by 141 · 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
Advances in Spheroids and Organoids on a Chip
Fang, G., Chen, Y., Lu, H., & Jin, D. (2023) · Advanced Functional Materials · doi:10.1002/adfm.202215043 · Cited by 127 · see citing works
Decellularized Extracellular Matrix for Remodeling Bioengineering Organoid's Microenvironment
Zhu, L., Yuhan, J., Yu, H., Zhang, B., Huang, K., & Zhu, L. (2023) · Small · doi:10.1002/smll.202207752 · Cited by 123 · see citing works
Recent advances in defined hydrogels in organoid research
Gan, Z., Qin, X., Liu, H., Liu, J., & Qin, J. (2023) · Bioactive Materials · doi:10.1016/j.bioactmat.2023.06.004 · Cited by 127 · see citing works
Engineering the Extracellular Matrix for Organoid Culture
Heo, J. H., Kang, D., Seo, S. J., & Jin, Y. (2022) · International Journal of Stem Cells · doi:10.15283/ijsc21190 · Cited by 116 · see citing works
Long-term expansion, genomic stability and in vivo safety of adult human pancreas organoids
Georgakopoulos, N., Prior, N., Angres, B., Mastrogiovanni, G., Cagan, A., Harrison, D., Hindley, C. J., Arnes-Benito, R., Liau, S.-S., Curd, A., et al. (2020) · BMC Developmental Biology · doi:10.1186/s12861-020-0209-5 · Cited by 112 · see citing works
Composite Hydrogels in Three-Dimensional in vitro Models
Zhao, Z., Vizetto‐Duarte, C., Moay, Z. K., Setyawati, M. I., Rakshit, M., Kathawala, M. H., & Ng, K. W. (2020) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2020.00611 · Cited by 109 · see citing works
Engineering Hydrogels for the Development of Three-Dimensional In Vitro Models
Maji, S., & Lee, H. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23052662 · Cited by 111 · see citing works
Polymer Hydrogels to Guide Organotypic and Organoid Cultures
Magno, V., Meinhardt, A., & Werner, C. (2020) · Advanced Functional Materials · doi:10.1002/adfm.202000097 · Cited by 106 · see citing works
Modeling Cell Communication in Cancer With Organoids: Making the Complex Simple
Fiorini, E., Veghini, L., & Corbo, V. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.00166 · Cited by 103 · see citing works
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 · see citing works
Engineered Microsystems for Spheroid and Organoid Studies
Kang, S., Kim, D., Lee, J., Takayama, S., & Park, J. Y. (2021) · Advanced Healthcare Materials · doi:10.1002/adhm.202001284 · Cited by 100 · see citing works
Patient-derived organoids in translational oncology and drug screening
Yang, R., & Yu, Y. (2023) · Cancer Letters · doi:10.1016/j.canlet.2023.216180 · Cited by 99 · see citing works
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 · see citing works
Biologically inspired approaches to enhance human organoid complexity
Holloway, E. M., Capeling, M. M., & Spence, J. R. (2019) · Development · doi:10.1242/dev.166173 · Cited by 96 · see citing works
Ruiter, F. A. A., Morgan, F. L. C., Roumans, N. J. T., Schumacher, A., Slaats, G. G. G., Moroni, L., LaPointe, V. L. S., & Baker, M. B. (2022) · Advanced Science · doi:10.1002/advs.202200543 · Cited by 92 · see citing works
Modelling metabolic diseases and drug response using stem cells and organoids
Hu, W., & Lazar, M. A. (2022) · Nature Reviews Endocrinology · doi:10.1038/s41574-022-00733-z · Cited by 98 · see citing works
Axon Growth of CNS Neurons in Three Dimensions Is Amoeboid and Independent of Adhesions
Santos, T. E., Schaffran, B., Broguière, N., Meyn, L., Zenobi‐Wong, M., & Bradke, F. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.107907 · Cited by 94 · see citing works
Self-citationKim, S. K., Kim, Y. H., Park, S., & Cho, S. (2021) · Acta Biomaterialia · doi:10.1016/j.actbio.2021.03.002 · Cited by 92 · see citing works
Organ-on-Chip Approaches for Intestinal 3D In Vitro Modeling
Pimenta, J. M., Ribeiro, R. D. C., Almeida, R., Costa, P. F., da Silva, M. A., & Pereira, B. (2021) · Cellular and Molecular Gastroenterology and Hepatology · doi:10.1016/j.jcmgh.2021.08.015 · Cited by 92 · see citing works
Fang, G., Lu, H., de la Fuente, L. R., Law, A. M. K., Lin, G., Jin, D., & Gallego‐Ortega, D. (2021) · Advanced Science · doi:10.1002/advs.202102418 · Cited by 91 · see citing works
Yavitt, F. M., Brown, T. E., Hushka, E. A., Brown, M. E., Gjorevski, N., Dempsey, P. J., Lütolf, M. P., & Anseth, K. S. (2020) · Advanced Materials · doi:10.1002/adma.201905366 · Cited by 89 · see citing works
Standardization of organoid culture in cancer research
Zhou, C., Wu, Y., Wang, Z., Liu, Y., Yu, J., Wang, W., Chen, S., Wu, W., Wang, J., Qian, G., et al. (2023) · Cancer Medicine · doi:10.1002/cam4.5943 · Cited by 84 · see citing works
One-step synthesis of composite hydrogel capsules to support liver organoid generation from hiPSCs
Wang, Y., Liu, H., Zhang, M., Wang, H., Chen, W., & Qin, J. (2020) · Biomaterials Science · doi:10.1039/d0bm01085e · Cited by 78 · see citing works
Shi, H.-Y., Kowalczewski, A., Vu, D., Liu, X.-Y., Salekin, A., Yang, H.-X., & Ma, Z. (2023) · Medicine in Novel Technology and Devices · doi:10.1016/j.medntd.2023.100276 · Cited by 77 · see citing works
A thermo-responsive collagen-nanocellulose hydrogel for the growth of intestinal organoids
Curvello, R., Alves, D., Abud, H. E., & Garnier, G. (2021) · Materials Science and Engineering C · doi:10.1016/j.msec.2021.112051 · Cited by 74 · see citing works
Engineered Plant‐Based Nanocellulose Hydrogel for Small Intestinal Organoid Growth
Curvello, R., Kerr, G., Micati, D., Chan, W. H., Raghuwanshi, V. S., Rosenbluh, J., Abud, H. E., & Garnier, G. (2020) · Advanced Science · doi:10.1002/advs.202002135 · Cited by 72 · see citing works
Scalise, M., Marino, F., Salerno, L., Cianflone, E., Molinaro, C., Salerno, N., Angelis, A. D., Viglietto, G., Urbanek, K., & Torella, D. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222413180 · Cited by 67 · see citing works
Biomaterial-guided stem cell organoid engineering for modeling development and diseases
Hoang, P., & Ma, Z. (2021) · Acta Biomaterialia · doi:10.1016/j.actbio.2021.01.026 · Cited by 70 · see citing works
Modeling nonalcoholic fatty liver disease on a liver lobule chip with dual blood supply
Du, K., Li, S., Li, C., Li, P., Miao, C., Luo, T., Qiu, B., & Ding, W. (2021) · Acta Biomaterialia · doi:10.1016/j.actbio.2021.07.013 · Cited by 69 · see citing works
Geuens, T., Ruiter, F. A. A., Schumacher, A., Morgan, F. L. C., Rademakers, T., Wiersma, L. E., van den Berg, C. W., Rabelink, T. J., Baker, M. B., & LaPointe, V. L. S. (2021) · Biomaterials · doi:10.1016/j.biomaterials.2021.120976 · Cited by 67 · see citing works
Polyisocyanide Hydrogels as a Tunable Platform for Mammary Gland Organoid Formation
Zhang, Y., Tang, C., Span, P. N., Rowan, A. E., Aalders, T. W., Schalken, J. A., Adema, G. J., Kouwer, P. H. J., Zegers, M. M., & Ansems, M. (2020) · Advanced Science · doi:10.1002/advs.202001797 · Cited by 66 · see citing works
Xu, X., Feng, Q., Ma, X., Deng, Y., Zhang, K., Ooi, H. S., Yang, B., Zhang, Z., Feng, B., & Bian, L. (2022) · Biomaterials · doi:10.1016/j.biomaterials.2022.121802 · Cited by 67 · see citing works
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 65 · see citing works
Microstructured Hydrogels to Guide Self‐Assembly and Function of Lung Alveolospheres
Loebel, C., Weiner, A. I., Eiken, M. K., Katzen, J. B., Morley, M. P., Bala, V., Cardenas‐Diaz, F. L., Davidson, M. D., Shiraishi, K., Basil, M. C., et al. (2022) · Advanced Materials · doi:10.1002/adma.202202992 · Cited by 64 · see citing works
A Review of Single-Cell Adhesion Force Kinetics and Applications
Shinde, A. S., Illath, K., Gupta, P., Shinde, P., Lim, K., Nagai, M., & Santra, T. S. (2021) · Cells · doi:10.3390/cells10030577 · Cited by 63 · see citing works
Chooi, W. H., Ng, C. Y., Ow, V., Harley, J., Ng, W., Hor, J., Low, K. E., Malleret, B., Xue, K., & Ng, S. (2022) · Advanced Healthcare Materials · doi:10.1002/adhm.202202342 · Cited by 62 · see citing works
Xu, C., Yang, K., Zhu, G., Ou, C., Jiang, J. S., Zhuravlev, E., & Zhang, Y. (2023) · Materials Chemistry Frontiers · doi:10.1039/d3qm00902e · Cited by 62 · see citing works
Advancing Tissue Decellularized Hydrogels for Engineering Human Organoids
Moura, B. S., Monteiro, M. V., Ferreira, L. P., Lavrador, P., Gaspar, V. M., & Mano, J. F. (2022) · Advanced Functional Materials · doi:10.1002/adfm.202202825 · Cited by 63 · see citing works
Reproducible extracellular matrices for tumor organoid culture: challenges and opportunities
Li, K., He, Y., Jin, X., Jin, K., & Qian, J. (2025) · Journal of Translational Medicine · doi:10.1186/s12967-025-06349-x · Cited by 68 · see citing works
Strategies to overcome the limitations of current organoid technology - engineered organoids
Fan, X., Hou, K., Liu, G., Shi, R., Wang, W., & Liang, G. (2025) · Journal of Tissue Engineering · doi:10.1177/20417314251319475 · Cited by 58 · see citing works
April-Monn, S., Wiedmer, T., Skowronska, M., Maire, R., Lena, M. S., Trippel, M. A., Domenico, A. D., Muffatti, F., Andreasi, V., Capurso, G., et al. (2020) · Neuroendocrinology · doi:10.1159/000507669 · Cited by 58 · see citing works
Liu, Y., Huang, J., Li, S., Li, Z., Chen, C., Qu, G., Chen, K., Teng, Y., Ma, R., Wu, X., et al. (2023) · Biomaterials Science · doi:10.1039/d3bm01645e · Cited by 59 · see citing works
Engineered organoids for biomedical applications
de Barros, N. R., Wang, C., Maity, S., Peirsman, A., Nasiri, R., Herland, A., Ermis, M., Kawakita, S., de Carvalho, B. G., Kouchehbaghi, N. H., et al. (2023) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2023.115142 · Cited by 54 · see citing works
Advancing Organoid Engineering for Tissue Regeneration and Biofunctional Reconstruction
Jin, H., Xue, Z., Liu, J., Ma, B., Yang, J., & Lei, L. (2024) · Biomaterials Research · doi:10.34133/bmr.0016 · Cited by 53 · see citing works
Meng, F., Shen, C., Yang, L., Ni, C., Huang, J., Lin, K., Cao, Z., Xu, S., Cui, W., Wang, X., et al. (2022) · Cell Regeneration · doi:10.1186/s13619-022-00137-4 · Cited by 50 · see citing works
Development of a deep learning based image processing tool for enhanced organoid analysis
Park, T., Kim, T. K., Han, Y. D., Kim, K., Kim, H., & Kim, H. S. (2023) · Scientific Reports · doi:10.1038/s41598-023-46485-2 · Cited by 51 · see citing works
A bioengineering perspective on modelling the intestinal epithelial physiology in vitro
Antfolk, M., & Jensen, K. B. (2020) · Nature Communications · doi:10.1038/s41467-020-20052-z · Cited by 52 · see citing works
Digesting the mechanobiology of the intestinal epithelium
Gonzalez, C. P., Ceada, G., Matejčić, M., & Trepat, X. (2021) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2021.10.005 · Cited by 49 · see citing works
Engineering the 3D structure of organoids
Moss, S. P., Bakırcı, E., & Feinberg, A. W. (2024) · Stem Cell Reports · doi:10.1016/j.stemcr.2024.11.009 · Cited by 51 · see citing works
Frappart, P., & Hofmann, T. G. (2020) · Cancers · doi:10.3390/cancers12102750 · Cited by 48 · see citing works
Wallaschek, N., Niklas, C., Pompaiah, M., Wiegering, A., Germer, C., Kircher, S., Brändlein, S., Maurus, K., Rosenwald, A., Yan, H. H. N., et al. (2019) · Journal of Molecular Biology · doi:10.1016/j.jmb.2019.05.031 · Cited by 45 · see citing works
Engineered biomimetic hydrogels for organoids
Li, Y., Saiding, Q., Wang, Z., & Cui, W. (2023) · Progress in Materials Science · doi:10.1016/j.pmatsci.2023.101216 · Cited by 45 · see citing works
Synthetic Matrices for Intestinal Organoid Culture: Implications for Better Performance
Poudel, H., Sanford, K., Szwedo, P. K., Pathak, R., & Ghosh, A. (2021) · ACS Omega · doi:10.1021/acsomega.1c05136 · Cited by 45 · see citing works
Intestinal Stem Cell-on-Chip to Study Human Host-Microbiota Interaction
Siwczak, F., Loffet, E. A., Kaminska, M., Koceva, H., Mahé, M. M., & Mosig, A. S. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.798552 · Cited by 44 · see citing works
van Tienderen, G. S., Koerkamp, B. G., IJzermans, J. N. M., van der Laan, L. J. W., & Verstegen, M. M. A. (2019) · Cancers · doi:10.3390/cancers11111706 · Cited by 43 · see citing works
Hydrogels to engineer tumor microenvironments in vitro
Fernando, K., Kwang, L. G., Lim, J. T. C., & Fong, E. L. S. (2021) · Biomaterials Science · doi:10.1039/d0bm01943g · Cited by 43 · see citing works
Extracellular Matrix-Based Hydrogels to Tailoring Tumor Organoids
Lee, H. J., Mun, S., Pham, D. M., & Kim, P. (2021) · ACS Biomaterials Science & Engineering · doi:10.1021/acsbiomaterials.0c01801 · Cited by 43 · see citing works
Composition and Mechanism of Three-Dimensional Hydrogel System in Regulating Stem Cell Fate
Ma, J., & Huang, C. (2020) · Tissue Engineering Part B Reviews · doi:10.1089/ten.teb.2020.0021 · Cited by 42 · see citing works
Recent advances in chemically defined and tunable hydrogel platforms for organoid culture
Agarwal, T., Celikkin, N., Costantini, M., Maiti, T. K., & Makvandi, P. (2021) · Bio-Design and Manufacturing · doi:10.1007/s42242-021-00126-7 · Cited by 42 · see citing works
Biomaterials for intestinal organoid technology and personalized disease modeling
Hirota, A., AlMusawi, S., Nateri, A. S., Ordóñez‐Morán, P., & Imajo, M. (2021) · Acta Biomaterialia · doi:10.1016/j.actbio.2021.05.010 · Cited by 41 · see citing works
3D multicellular systems in disease modelling: From organoids to organ-on-chip
Goldrick, C., Guri, I., Herrera-Oropeza, G. E., O’Brien-Gore, C., Roy, E., Wojtynska, M., & Spagnoli, F. M. (2023) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2023.1083175 · Cited by 42 · see citing works
Exploiting CRISPR Cas9 in Three-Dimensional Stem Cell Cultures to Model Disease
Gopal, S., Rodrigues, A. L., & Dordick, J. S. (2020) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2020.00692 · Cited by 44 · see citing works
Special review series on 3D organotypic culture models: Introduction and historical perspective
Hayden, P. J., & Harbell, J. W. (2020) · In Vitro Cellular & Developmental Biology - Animal · doi:10.1007/s11626-020-00500-2 · Cited by 41 · see citing works
<i>In vitro</i> functional models for human liver diseases and drug screening: beyond animal testing
Paradiso, A., Volpi, M., Rinoldi, C., Celikkin, N., Contessi Negrini, N., Bilgen, M., Dallera, G., Pierini, F., Costantini, M., Święszkowski, W., et al. (2023) · Biomaterials Science · doi:10.1039/d1bm01872h · Cited by 40 · see citing works
Bioactive peptides for boosting stem cell culture platform: Methods and applications
Dayem, A. A., Lee, S. B., Lim, K. M., Kim, A., Shin, H. J., Vellingiri, B., Kim, Y. B., & Cho, S. (2023) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2023.114376 · Cited by 40 · see citing works
Recent Advances in Gut‐ and Gut–Organ‐Axis‐on‐a‐Chip Models
Kim, R., & Sung, J. H. (2024) · Advanced Healthcare Materials · doi:10.1002/adhm.202302777 · Cited by 42 · see citing works
Biomaterial-assisted organoid technology for disease modeling and drug screening
Shao, Y., Wang, J., Jin, A., Jiang, S., Lei, L., & Liu, L. (2024) · Materials Today Bio · doi:10.1016/j.mtbio.2024.101438 · Cited by 42 · see citing works
Rethinking Matrigel: The Complex Journey to Matrix Alternatives in Organoid Culture
Wolff, L., & Hendrix, S. (2025) · Advanced Science · doi:10.1002/advs.202508734 · Cited by 44 · see citing works
Collagen Microfibers Induce Blood Capillary Orientation and Open Vascular Lumen
Liu, H., Kitano, S., Irie, S., Levato, R., & Matsusaki, M. (2020) · Advanced Biosystems · doi:10.1002/adbi.202000038 · Cited by 38 · see citing works
Recent Advancements in Regenerative Approaches for Thymus Rejuvenation
Sharma, H., & Moroni, L. (2021) · Advanced Science · doi:10.1002/advs.202100543 · Cited by 39 · see citing works
Ma, P., Chen, Y., Lai, X., Zheng, J., Ye, E., Loh, X. J., Zhao, Y., Parikh, B. H., Su, X., You, M., et al. (2021) · Macromolecular Bioscience · doi:10.1002/mabi.202100191 · Cited by 39 · see citing works
Işık, M., Okesola, B. O., Eylem, C. C., Koçak, E., Nemutlu, E., D’Este, M., Mata, Á., & Derkuş, B. (2023) · Acta Biomaterialia · doi:10.1016/j.actbio.2023.09.040 · Cited by 36 · see citing works
- Authors
- Broguiere, N., Isenmann, L., Hirt, C., Ringel, T., Placzek, S., Cavalli, E., Ringnalda, F., Villiger, L., Züllig, R., Lehmann, R., Rogler, G., Heim, M. H., Schüler, J., Zenobi‐Wong, M., & Schwank, G.
- Affiliations
- Department of Health Sciences and Technology ETH Zürich Otto‐Stern‐Weg 7 8093 Zürich Switzerland
- ETH Zurich (CH)
- University Hospital Zurich (CH)
- University of Zurich (CH)
- University of Basel (CH)
- Charles River Research Services Germany GmbH Am Flughafen 12 79108 Freiburg im Breisgau Germany
- Corresponding author
- Zenobi‐Wong, Marcy
- Schwank, Gerald
- ORCID
- Venue
- Advanced Materials
- Publisher
- Wiley
- Published
- 2018-09-10
- Volume
- 30
- Issue
- 43
- Pages
- e1801621-e1801621
- ISSN
- 0935-9648 (ISSN-L)
- 1521-4095
- OpenAlex
- W2890540126
- Cited by
- 282
- References
- 40
- Citations by year
- 2026: 22 · 2025: 38 · 2024: 39 · 2023: 43 · 2022: 35 · 2021: 47 · 2020: 40 · 2019: 17 · 2018: 1
- FWCI
- 9.92
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Advanced Materials (publishedVersion, cc-by-nc)
- PubMed (publishedVersion)
- Zurich Open Repository and Archive (University of Zurich) (acceptedVersion, cc-by-nc)
- Repository for Publications and Research Data (ETH Zurich) (submittedVersion, cc-by-nc)
- Zurich Open Repository and Archive (University of Zurich) (submittedVersion, cc-by-nc)
- ETH Zürich Research Collection
- Zurich Open Repository and Archive (University of Zurich)
- Funders
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (31003A_160230)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Medicine › Hydrogels: synthesis, properties, applications
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular Mechanics and Interactions
- Physical Sciences › Engineering › Biomedical Engineering › 3D Printing in Biomedical Research
- Keywords
- epithelial organoids, fibrin gel, laminin-111, traction force microscopy, organoid morphogenesis, cell contractility, intestinal organoids, organoid expansion
- MeSH terms
- Animals, Cell Adhesion, Cell Line, Epithelium, Fibrin, Humans, Intestine, Small, Laminin, Liver, Mice, Inbred C57BL, Mice, Transgenic, Organoids, Pancreas, Stem Cells, Surface Properties, Hydrogels, Tissue Culture Techniques, Tissue Scaffolds
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
