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Organoids as tools for fundamental discovery and translation—a Keystone Symposia report
dc.contributor.authorCable, Jennifer
dc.contributor.authorLutolf, Matthias P.
dc.contributor.authorFu, Jianping
dc.contributor.authorPark, Sunghee Estelle
dc.contributor.authorApostolou, Athanasia
dc.contributor.authorChen, Shuibing
dc.contributor.authorSong, Cheng Jack
dc.contributor.authorSpence, Jason R.
dc.contributor.authorLiberali, Prisca
dc.contributor.authorLancaster, Madeline
dc.contributor.authorMeier, Anna B.
dc.contributor.authorPek, Nicole Min Qian
dc.contributor.authorWells, James M.
dc.contributor.authorCapeling, Meghan M.
dc.contributor.authorUzquiano, Ana
dc.contributor.authorMusah, Samira
dc.contributor.authorHuch, Meritxell
dc.contributor.authorGouti, Mina
dc.contributor.authorHombrink, Pleun
dc.contributor.authorQuadrato, Giorgia
dc.contributor.authorUrenda, Jean-Paul
dc.date.accessioned2023-01-11T16:27:40Z
dc.date.available2024-01-11 11:27:38en
dc.date.available2023-01-11T16:27:40Z
dc.date.issued2022-12
dc.identifier.citationCable, Jennifer; Lutolf, Matthias P.; Fu, Jianping; Park, Sunghee Estelle; Apostolou, Athanasia; Chen, Shuibing; Song, Cheng Jack; Spence, Jason R.; Liberali, Prisca; Lancaster, Madeline; Meier, Anna B.; Pek, Nicole Min Qian; Wells, James M.; Capeling, Meghan M.; Uzquiano, Ana; Musah, Samira; Huch, Meritxell; Gouti, Mina; Hombrink, Pleun; Quadrato, Giorgia; Urenda, Jean-Paul (2022). "Organoids as tools for fundamental discovery and translation- a Keystone Symposia report." Annals of the New York Academy of Sciences 1518(1): 196-208.
dc.identifier.issn0077-8923
dc.identifier.issn1749-6632
dc.identifier.urihttps://hdl.handle.net/2027.42/175520
dc.description.abstractComplex three-dimensional in vitro organ-like models, or organoids, offer a unique biological tool with distinct advantages over two-dimensional cell culture systems, which can be too simplistic, and animal models, which can be too complex and may fail to recapitulate human physiology and pathology. Significant progress has been made in driving stem cells to differentiate into different organoid types, though several challenges remain. For example, many organoid models suffer from high heterogeneity, and it can be difficult to fully incorporate the complexity of in vivo tissue and organ development to faithfully reproduce human biology. Successfully addressing such limitations would increase the viability of organoids as models for drug development and preclinical testing. On April 3–6, 2022, experts in organoid development and biology convened at the Keystone Symposium “Organoids as Tools for Fundamental Discovery and Translation” to discuss recent advances and insights from this relatively new model system into human development and disease.Complex three-dimensional in vitro organ-like models, or organoids, offer a unique biological tool with distinct advantages over two-dimensional cell culture systems, which can be too simplistic, and animal models, which can be too complex and may fail to recapitulate human physiology and pathology. Significant progress has been made in driving stem cells to differentiate into different organoid types, though several challenges remain.
dc.publisherWiley Periodicals, Inc.
dc.subject.otherorganoids
dc.subject.othersingle-cell sequencing
dc.subject.otherdifferentiation
dc.subject.otherdevelopment
dc.subject.otherinflammatory bowel disease
dc.subject.otherkidney disease
dc.subject.othermicrofluidics
dc.titleOrganoids as tools for fundamental discovery and translation—a Keystone Symposia report
dc.typeArticle
dc.rights.robotsIndexNoFollow
dc.subject.hlbsecondlevelScience (General)
dc.subject.hlbtoplevelScience
dc.description.peerreviewedPeer Reviewed
dc.description.bitstreamurlhttp://deepblue.lib.umich.edu/bitstream/2027.42/175520/1/nyas14874.pdf
dc.description.bitstreamurlhttp://deepblue.lib.umich.edu/bitstream/2027.42/175520/2/nyas14874_am.pdf
dc.identifier.doi10.1111/nyas.14874
dc.identifier.sourceAnnals of the New York Academy of Sciences
dc.identifier.citedreferencePolioudakis, D., De La Torre-Ubieta, L., Langerman, J., Elkins, A. G., Shi, X. U., Stein, J. L., Vuong, C. K., Nichterwitz, S., Gevorgian, M., Opland, C. K., Lu, D., Connell, W., Ruzzo, E. K., Lowe, J. K., Hadzic, T., Hinz, F. I., Sabri, S., Lowry, W. E., Gerstein, M. B., … Geschwind, D. H. ( 2019 ). A single-cell transcriptomic atlas of human neocortical development during mid-gestation. Neuron, 103, 785 – 801.e8.
dc.identifier.citedreferenceQuijada, P., Trembley, M. A., & Small, E. M. ( 2020 ). The role of the epicardium during heart development and repair. Circulation Research, 126, 377 – 394.
dc.identifier.citedreferenceGeddes, G. C., Dimmock, D. P., Hehir, D. A., Helbling, D. C., Kirkpatrick, E., Loomba, R., Southern, J., Waknitz, M., Scharer, G., & Konduri, G. G. ( 2015 ). A novel FOXF1 mutation associated with alveolar capillary dysplasia and coexisting colobomas and hemihyperplasia. Journal of Perinatology, 35, 155 – 157.
dc.identifier.citedreferenceSen, P., Yang, Y., Navarro, C., Silva, I., Szafranski, P., Kolodziejska, K. E., Dharmadhikari, A. V., Mostafa, H., Kozakewich, H., Kearney, D., Cahill, J. B., Whitt, M., Bilic, M., Margraf, L., Charles, A., Goldblatt, J., Gibson, K., Lantz, P. E., Garvin, A. J., … & Stankiewicz, P. ( 2013 ). Novel FOXF1 mutations in sporadic and familial cases of alveolar capillary dysplasia with misaligned pulmonary veins imply a role for its DNA binding domain. Human Mutation, 34, 801 – 811.
dc.identifier.citedreferenceMúnera, J. O., Sundaram, N., Rankin, S. A., Hill, D., Watson, C., Mahe, M., Vallance, J. E., Shroyer, N. F., Sinagoga, K. L., Zarzoso-Lacoste, A., Hudson, J. R., Howell, J. C., Chatuvedi, P., Spence, J. R., Shannon, J. M., Zorn, A. M., Helmrath, M. A., & Wells, J. M. ( 2017 ). Differentiation of human pluripotent stem cells into colonic organoids via transient activation of BMP signaling. Cell Stem Cell, 21, 51 – 64.e6.
dc.identifier.citedreferenceEicher, A. K., Kechele, D. O., Sundaram, N., Berns, H. M., Poling, H. M., Haines, L. E., Sanchez, J. G., Kishimoto, K., Krishnamurthy, M., Han, L., Zorn, A. M., Helmrath, M. A., & Wells, J. M. ( 2022 ). Functional human gastrointestinal organoids can be engineered from three primary germ layers derived separately from pluripotent stem cells. Cell Stem Cell, 29, 36 – 51.e6.
dc.identifier.citedreferenceMccracken, K. W., Catã¡, E. M., Crawford, C. M., Sinagoga, K. L., Schumacher, M., Rockich, B. E., Tsai, Y.-H., Mayhew, C. N., Spence, J. R., Zavros, Y., & Wells, J. M. ( 2014 ). Modelling human development and disease in pluripotent stem-cell-derived gastric organoids. Nature, 516, 400 – 404.
dc.identifier.citedreferenceWorkman, M. J., Mahe, M. M., Trisno, S., Poling, H. M., Watson, C. L., Sundaram, N., Chang, C.-F., Schiesser, J., Aubert, P., Stanley, E. G., Elefanty, A. G., Miyaoka, Y., Mandegar, M. A., Conklin, B. R., Neunlist, M., Brugmann, S. A., Helmrath, M. A., & Wells, J. M. ( 2017 ). Engineered human pluripotent-stem-cell-derived intestinal tissues with a functional enteric nervous system. Nature Medicine, 23, 49 – 59.
dc.identifier.citedreferenceHan, L., Chaturvedi, P., Kishimoto, K., Koike, H., Nasr, T., Iwasawa, K., Giesbrecht, K., Witcher, P. C., Eicher, A., Haines, L., Lee, Y., Shannon, J. M., Morimoto, M., Wells, J. M., Takebe, T., & Zorn, A. M. ( 2020 ). Single cell transcriptomics identifies a signaling network coordinating endoderm and mesoderm diversification during foregut organogenesis. Nature Communication, 11, 4158.
dc.identifier.citedreferenceSpence, J. R., Mayhew, C. N., Rankin, S. A., Kuhar, M. F., Vallance, J. E., Tolle, K., Hoskins, E. E., Kalinichenko, V. V., Wells, S. I., Zorn, A. M., Shroyer, N. F., & Wells, J. M. ( 2011 ). Directed differentiation of human pluripotent stem cells into intestinal tissue in vitro. Nature, 470, 105 – 109.
dc.identifier.citedreferenceWatson, C. L., Mahe, M. M., Múnera, J., Howell, J. C., Sundaram, N., Poling, H. M., Schweitzer, J. I., Vallance, J. E., Mayhew, C. N., Sun, Y., Grabowski, G., Finkbeiner, S. R., Spence, J. R., Shroyer, N. F., Wells, J. M., & Helmrath, M. A. ( 2014 ). An in vivo model of human small intestine using pluripotent stem cells. Nature Medicine, 20, 1310 – 1314.
dc.identifier.citedreferenceCapeling, M. M., Czerwinski, M., Huang, S., Tsai, Y.-H., Wu, A., Nagy, M. S., Juliar, B., Sundaram, N., Song, Y., Han, W. M., Takayama, S., Alsberg, E., Garcia, A. J., Helmrath, M., Putnam, A. J., & Spence, J. R. ( 2019 ). Nonadhesive alginate hydrogels support growth of pluripotent stem cell-derived intestinal organoids. Stem Cell Reports, 12, 381 – 394.
dc.identifier.citedreferenceCruz-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., & García, A. J. ( 2017 ). Synthetic hydrogels for human intestinal organoid generation and colonic wound repair. Nature Cell Biology, 19, 1326 – 1335.
dc.identifier.citedreferenceCapeling, M. M., Huang, S., Childs, C. J., Wu, J. H., Tsai, Y. U.-H., Wu, A., Garg, N., Holloway, E. M., Sundaram, N., Bouffi, C., Helmrath, M., & Spence, J. R. ( 2022 ). Suspension culture promotes serosal mesothelial development in human intestinal organoids. Cell Reports, 38, 110379.
dc.identifier.citedreferenceUzquiano, A., Kedaigle, A. J., Pigoni, M., Paulsen, B., Adiconis, X., Kim, K., Faits, T., Nagaraja, S., Antón-Bolaños, N., Gerhardinger, C., Tucewicz, A., Murray, E., Jin, X., Buenrostro, J., Chen, F., Silvia Velasco, V., Regev, A., Levin, J. Z., & Arlotta, P. ( 2022 ). Single-cell multiomics atlas of organoid development uncovers longitudinal molecular programs of cellular diversification of the human cerebral cortex. bioRxiv 2022.03.17.484798.
dc.identifier.citedreferenceNikolaev, M., Mitrofanova, O., Broguiere, N., Geraldo, S., Dutta, D., Tabata, Y., Elci, B., Brandenberg, N., Kolotuev, I., Gjorevski, N., Clevers, H., & Lutolf, M. P. ( 2020 ). Homeostatic mini-intestines through scaffold-guided organoid morphogenesis. Nature, 585, 574 – 578.
dc.identifier.citedreferenceTrevino, A. E., Müller, F., Andersen, J., Sundaram, L., Kathiria, A., Shcherbina, A., Farh, K., Chang, H. Y., Pașca, A. M., Kundaje, A., Pașca, S. P., & Greenleaf, W. J. ( 2021 ). Chromatin and gene-regulatory dynamics of the developing human cerebral cortex at single-cell resolution. Cell, 184, 5053 – 5069.e23.
dc.identifier.citedreferenceDi Bella, D. J., Habibi, E., Stickels, R. R., Scalia, G., Brown, J., Yadollahpour, P., Yang, S. M., Abbate, C., Biancalani, T., Macosko, E. Z., Chen, F., Regev, A., & Arlotta, P. ( 2021 ). Molecular logic of cellular diversification in the mouse cerebral cortex. Nature, 595, 554 – 559.
dc.identifier.citedreferenceBonner, M. G., Gudapati, H., Mou, X., & Musah, S. ( 2022 ). Microfluidic systems for modeling human development. Development, 149, dev199463.
dc.identifier.citedreferenceMou, X., Shah, J., Bhattacharya, R., Kalejaiye, T. D., Sun, B., Hsu, P.-C., & Musah, S. ( 2022 ). A biomimetic electrospun membrane supports the differentiation and maturation of kidney epithelium from human stem cells. Bioengineering, 9, 188.
dc.identifier.citedreferenceMusah, S., Morin, S. A., Wrighton, P. J., Zwick, D. B., Jin, S., & Kiessling, L. L. ( 2012 ). Glycosaminoglycan-binding hydrogels enable mechanical control of human pluripotent stem cell self-renewal. ACS Nano, 6, 10168 – 10177.
dc.identifier.citedreferenceDerda, R., Musah, S., Orner, B. P., Klim, J. R., Li, L., & Kiessling, L. L. ( 2010 ). High-throughput discovery of synthetic surfaces that support proliferation of pluripotent cells. Journal of the American Chemical Society, 132, 1289 – 1295.
dc.identifier.citedreferenceMusah, S., Wrighton, P. J., Zaltsman, Y., Zhong, X., Zorn, S., Parlato, M. B., Hsiao, C., Palecek, S. P., Chang, Q., Murphy, W. L., & Kiessling, L. L. ( 2014 ). Substratum-induced differentiation of human pluripotent stem cells reveals the coactivator YAP is a potent regulator of neuronal specification. Proceedings of the National Academy of Sciences of the United States of America, 111, 13805 – 13810.
dc.identifier.citedreferenceRoye, Y., Bhattacharya, R., Mou, X., Zhou, Y., Burt, M. A., & Musah, S. ( 2021 ). A personalized glomerulus chip engineered from stem cell-derived epithelium and vascular endothelium. Micromachines, 12, 967.
dc.identifier.citedreferenceMusah, S., Mammoto, A., Ferrante, T. C., Jeanty, S. S. F., Hirano-Kobayashi, M., Mammoto, T., Roberts, K., Chung, S., Novak, R., Ingram, M., Fatanat-Didar, T., Koshy, S., Weaver, J. C., Church, G. M., & Ingber, D. E. ( 2017 ). Mature induced-pluripotent-stem-cell-derived human podocytes reconstitute kidney glomerular-capillary-wall function on a chip. Nature Biomedical Engineering, 1, 0069.
dc.identifier.citedreferenceMusah, S., Dimitrakakis, N., Camacho, D. M., Church, G. M., & Ingber, D. E. ( 2018 ). Directed differentiation of human induced pluripotent stem cells into mature kidney podocytes and establishment of a Glomerulus Chip. Nature Protocols, 13, 1662 – 1685.
dc.identifier.citedreferenceBurt, M., Bhattachaya, R., Okafor, A. E., & Musah, S. ( 2020 ). Guided differentiation of mature kidney podocytes from human induced pluripotent stem cells under chemically defined conditions. Journal of Visualized Experiments, 161, e61299.
dc.identifier.citedreferenceKalejaiye, T. D., Bhattacharya, R., Burt, M. A., Travieso, T., Okafor, A. E., Mou, X., Blasi, M., & Musah, S. ( 2021 ). BSG/CD147 and ACE2 receptors facilitate SARS-CoV-2 infection of human iPS cell-derived kidney podocytes. 2021.11.16.468893.
dc.identifier.citedreferenceBurt, M. A., Kalejaiye, T. D., Bhattacharya, R., Dimitrakakis, N., & Musah, S. ( 2021 ). Adriamycin-induced podocyte injury disrupts the YAP–TEAD1 axis and downregulates Cyr61 and CTGF expression. ACS Chemical Biology.
dc.identifier.citedreferenceBarker, N., Huch, M., Kujala, P., van de Wetering, M., Snippert, H. J., van Es, J. H., Sato, T., Stange, D. E., Begthel, H., van den Born, M., Danenberg, E., van den Brink, S., Korving, J., Abo, A., Peters, P. J., Wright, N., Poulsom, R., & Clevers, H. ( 2010 ). Lgr5(+ve) stem cells drive self-renewal in the stomach and build long-lived gastric units in vitro. Cell Stem Cell, 6, 25 – 36.
dc.identifier.citedreferenceHuch, M., Dorrell, C., Boj, S. F., Van Es, J. H., Li, V. S. W., Van De Wetering, M., Sato, T., Hamer, K., Sasaki, N., Finegold, M. J., Haft, A., Vries, R. G., Grompe, M., & Clevers, H. ( 2013 ). In vitro expansion of single Lgr5 + liver stem cells induced by Wnt-driven regeneration. Nature, 494, 247 – 250.
dc.identifier.citedreferenceHuch, M., Bonfanti, P., Boj, S. F., Sato, T., Loomans, C. J. M., Van De Wetering, M., Sojoodi, M., Li, V. S. W., Schuijers, J., Gracanin, A., Ringnalda, F., Begthel, H., Hamer, K., Mulder, J., Van Es, J. H., De Koning, E., Vries, R. G. J., Heimberg, H., & Clevers, H. ( 2013 ). Unlimited in vitro expansion of adult bi-potent pancreas progenitors through the Lgr5/R–spondin axis. Embo Journal, 32, 2708 – 2721.
dc.identifier.citedreferenceAloia, L., Mckie, M. A., Vernaz, G., Cordero-Espinoza, L.-A., Aleksieva, N., Van Den Ameele, J., Antonica, F., Font-Cunill, B., Raven, A., Aiese Cigliano, R., Belenguer, G., Mort, R. L., Brand, A. H., Zernicka-Goetz, M., Forbes, S. J., Miska, E. A., & Huch, M. ( 2019 ). Epigenetic remodelling licences adult cholangiocytes for organoid formation and liver regeneration. Nature Cell Biology, 21, 1321 – 1333.
dc.identifier.citedreferenceBroutier, L., Mastrogiovanni, G., Verstegen, M. M., Francies, H. E., Gavarr, L. M., Bradshaw, C. R., Allen, G. E., Arnes-Benito, R., Sidorova, O., Gaspersz, M. P., Georgakopoulos, N., Koo, B.-K., Dietmann, S., Davies, S. E., Praseedom, R. K., Lieshout, R., Ijzermans, J. N. M., Wigmore, S. J., Saeb-Parsy, K., … Huch, M. ( 2017 ). Human primary liver cancer-derived organoid cultures for disease modeling and drug screening. Nature Medicine, 23, 1424 – 1435.
dc.identifier.citedreferenceCordero-Espinoza, L. A., Dowbaj, A. M., Kohler, T. N., Strauss, B., Sarlidou, O., Belenguer, G., Pacini, C., Martins, N. P., Dobie, R., Wilson-Kanamori, J. R., Butler, R., Prior, N., Serup, P., Jug, F., Henderson, N. C., Hollfelder, F., & Huch, M. ( 2021 ). Dynamic cell contacts between periportal mesenchyme and ductal epithelium act as a rheostat for liver cell proliferation. Cell Stem Cell, 28, 1907 – 1921.e8.
dc.identifier.citedreferenceGouti, M., Tsakiridis, A., Wymeersch, F. J., Huang, Y., Kleinjung, J., Wilson, V., & Briscoe, J. ( 2014 ). In vitro generation of neuromesodermal progenitors reveals distinct roles for wnt signalling in the specification of spinal cord and paraxial mesoderm identity. PLoS Biology, 12, e1001937.
dc.identifier.citedreferenceGouti, M., Delile, J., Stamataki, D., Wymeersch, F. J., Huang, Y., Kleinjung, J., Wilson, V., & Briscoe, J. ( 2017 ). A gene regulatory network balances neural and mesoderm specification during vertebrate trunk development. Developmental Cell, 41, 243 – 261.e7.
dc.identifier.citedreferenceMetzis, V., Steinhauser, S., Pakanavicius, E., Gouti, M., Stamataki, D., Ivanovitch, K., Watson, T., Rayon, T., Mousavy Gharavy, S. N., Lovell-Badge, R., Luscombe, N. M., & Briscoe, J. ( 2018 ). Nervous system regionalization entails axial allocation before neural differentiation. Cell, 175, 1105 – 1118.e17.
dc.identifier.citedreferenceMartins, J. M. F., Nguyen, L. V. I. N., & Gouti, M. ( 2021 ). Humane neuromuskuläre Organoide — Anwendung und Perspektive. BIOspektrum, 27, 135 – 138.
dc.identifier.citedreferenceFaustino Martins, J.-M., Fischer, C., Urzi, A., Vidal, R., Kunz, S., Ruffault, P.-L., Kabuss, L., Hube, I., Gazzerro, E., Birchmeier, C., Spuler, S., Sauer, S., & Gouti, M. ( 2020 ). Self-organizing 3D human trunk neuromuscular organoids. Cell Stem Cell, 26, 172 – 186.e6.
dc.identifier.citedreferenceCullen, D. K., Gordián-Vélez, W. J., Struzyna, L. A., Jgamadze, D., Lim, J., Wofford, K. L., Browne, K. D., & Chen, H. I. ( 2019 ). Bundled three-dimensional human axon tracts derived from brain organoids. iScience, 21, 57 – 67.
dc.identifier.citedreferenceKirihara, T., Luo, Z., Chow, S. Y. A., Misawa, R., Kawada, J., Shibata, S., Khoyratee, F., Vollette, C. A., Volz, V., Levi, T., Fujii, T., & Ikeuchi, Y. ( 2019 ). A human induced pluripotent stem cell-derived tissue model of a cerebral tract connecting two cortical regions. iScience, 14, 301 – 311.
dc.identifier.citedreferenceOsaki, T., & Ikeuchi, Y. ( 2021 ). Advanced complexity and plasticity of neural activity in reciprocally connected human cerebral organoids. bioRxiv, 2021.02.16.431387.
dc.identifier.citedreferenceSato, 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., & Clevers, H. ( 2009 ). Single Lgr5 stem cells build crypt–villus structures in vitro without a mesenchymal niche. Nature, 459, 262 – 265.
dc.identifier.citedreferenceGjorevski, N., Nikolaev, M., Brown, T. E., Mitrofanova, O., Brandenberg, N., Delrio, F. W., Yavitt, F. M., Liberali, P., Anseth, K. S., & Lutolf, M. P. ( 2022 ). Tissue geometry drives deterministic organoid patterning. Science, 375, eaaw9021.
dc.identifier.citedreferenceShao, Y., Taniguchi, K., Gurdziel, K., Townshend, R. F., Xue, X., Yong, K. M. A., Sang, J., Spence, J. R., Gumucio, D. L., & Fu, J. ( 2017 ). Self-organized amniogenesis by human pluripotent stem cells in a biomimetic implantation-like niche. Nature Materials, 16, 419 – 425.
dc.identifier.citedreferenceShao, Y., Taniguchi, K., Townshend, R. F., Miki, T., Gumucio, D. L., & Fu, J. ( 2017 ). A pluripotent stem cell-based model for post-implantation human amniotic sac development. Nature Communication, 8, 208.
dc.identifier.citedreferenceZheng, Y., Xue, X., Shao, Y., Wang, S., Esfahani, S. N., Li, Z., Muncie, J. M., Lakins, J. N., Weaver, V. M., Gumucio, D. L., & Fu, J. ( 2019 ). Controlled modelling of human epiblast and amnion development using stem cells. Nature, 573, 421 – 425.
dc.identifier.citedreferencePark, S. E., Georgescu, A., & Huh, D. ( 2019 ). Organoids-on-a-chip. Science, 364, 960 – 965.
dc.identifier.citedreferenceMondrinos, M. J., Alisafaei, F., Yi, A. Y., Ahmadzadeh, H., Lee, I., Blundell, C., Seo, J., Osborn, M., Jeon, T.-J., Kim, S. M., Shenoy, V. B., & Huh, D. ( 2021 ). Surface-directed engineering of tissue anisotropy in microphysiological models of musculoskeletal tissue. Science Advances, 7, eabe9446.
dc.identifier.citedreferenceSeo, J., Byun, W. Y., Alisafaei, F., Georgescu, A., Yi, Y.-S., Massaro-Giordano, M., Shenoy, V. B., Lee, V., Bunya, V. Y., & Huh, D. ( 2019 ). Multiscale reverse engineering of the human ocular surface. Nature Medicine, 25, 1310 – 1318.
dc.identifier.citedreferencePark, J. Y., Mani, S., Clair, G., Olson, H. M., Paurus, V. L., Ansong, C. K., Blundell, C., Young, R., Kanter, J., Gordon, S., Yi, A. Y., Mainigi, M., & Huh, D. D. ( 2022 ). A microphysiological model of human trophoblast invasion during implantation. Nature Communication, 13, 1252.
dc.identifier.citedreferenceKim, H. J., Huh, D., Hamilton, G., & Ingber, D. E. ( 2012 ). Human gut-on-a-chip inhabited by microbial flora that experiences intestinal peristalsis-like motions and flow. Lab on a Chip, 12, 2165 – 2174.
dc.identifier.citedreferenceKasendra, M., Luc, R., Yin, J., Manatakis, D. V., Kulkarni, G., Lucchesi, C., Sliz, J., Apostolou, A., Sunuwar, L., Obrigewitch, J., Jang, K.-J., Hamilton, G. A., Donowitz, M., & Karalis, K. ( 2020 ). Duodenum Intestine-Chip for preclinical drug assessment in a human relevant model. eLife, 9, e50135.
dc.identifier.citedreferenceWorkman, M. J., Gleeson, J. P., Troisi, E. J., Estrada, H. Q., Kerns, S. J., Hinojosa, C. D., Hamilton, G. A., Targan, S. R., Svendsen, C. N., & Barrett, R. J. ( 2018 ). Enhanced utilization of induced pluripotent stem cell-derived human intestinal organoids using microengineered chips. Cellular and Molecular Gastroenterology and Hepatology, 5, 669 – 677.e2.
dc.identifier.citedreferenceManatakis, D. V., Vandevender, A., & Manolakos, E. S. ( 2021 ). An information-theoretic approach for measuring the distance of organ tissue samples using their transcriptomic signatures. Bioinformatics, 36, 5194 – 5204.
dc.identifier.citedreferenceApostolou, A., Panchakshari, R. A., Banerjee, A., Manatakis, D. V., Paraskevopoulou, M. D., Luc, R., Abu-Ali, G., Dimitriou, A., Lucchesi, C., Kulkarni, G., Maulana, T. I., Kasendra, M., Kerns, J. S., Bleck, B., Ewart, L., Manolakos, E. S., Hamilton, G. A., Giallourakis, C., & Karalis, K. ( 2021 ). A novel microphysiological colon platform to decipher mechanisms driving human intestinal permeability. Cellular and Molecular Gastroenterology and Hepatology, 12, 1719 – 1741.
dc.identifier.citedreferenceJarry, A., Malard, F., Bou-Hanna, C., Meurette, G., Mohty, M., Mosnier, J. F., Laboisse, C. L., & Bossard, C. ( 2017 ). Interferon-alpha promotes Th1 response and epithelial apoptosis via inflammasome activation in human intestinal mucosa. Cellular and Molecular Gastroenterology and Hepatology, 3, 72 – 81.
dc.identifier.citedreferenceParks, O. B., Pociask, D. A., Hodzic, Z., Kolls, J. K., & Good, M. ( 2015 ). Interleukin-22 signaling in the regulation of intestinal health and disease. Frontiers in Cell and Developmental Biology, 3, 85.
dc.identifier.citedreferenceMuñoz, M., Eidenschenk, C., Ota, N., Wong, K., Lohmann, U., Kühl, A. A., Wang, X., Manzanillo, P., Li, Y., Rutz, S., Zheng, Y., Diehl, L., Kayagaki, N., Van Lookeren-Campagne, M., Liesenfeld, O., Heimesaat, M., & Ouyang, W. ( 2015 ). Interleukin-22 induces interleukin-18 expression from epithelial cells during intestinal infection. Immunity, 42, 321 – 331.
dc.identifier.citedreferenceSabat, R., Ouyang, W., & Wolk, K. ( 2014 ). Therapeutic opportunities of the IL-22-IL-22R1 system. Nature Reviews Drug Discovery, 13, 21 – 38.
dc.identifier.citedreferenceYang, L., Han, Y., Nilsson-Payant, B. E., Gupta, V., Wang, P., Duan, X., Tang, X., Zhu, J., Zhao, Z., Jaffré, F., Zhang, T., Kim, T. W., Harschnitz, O., Redmond, D., Houghton, S., Liu, C., Naji, A., Ciceri, G., Guttikonda, S., … & Chen, S. ( 2020 ). A human pluripotent stem cell-based platform to study SARS-CoV-2 tropism and model virus infection in human cells and organoids. Cell Stem Cell, 27, 125 – 136.e7.
dc.identifier.citedreferenceHan, Y., Duan, X., Yang, L., Nilsson-Payant, B. E., Wang, P., Duan, F., Tang, X., Yaron, T. M., Zhang, T., Uhl, S., Bram, Y., Richardson, C., Zhu, J., Zhao, Z., Redmond, D., Houghton, S., Nguyen, D.-H. T., Xu, D., Wang, X., … Chen, S. ( 2021 ). Identification of SARS-CoV-2 inhibitors using lung and colonic organoids. Nature, 589, 270 – 275.
dc.identifier.citedreferenceDuan, X., Tang, X., Nair, M. S., Zhang, T., Qiu, Y., Zhang, W., Wang, P., Huang, Y., Xiang, J., Wang, H., Schwartz, R. E., Ho, D. D., Evans, T., & Chen, S. ( 2021 ). An airway organoid-based screen identifies a role for the HIF1α–glycolysis axis in SARS-CoV-2 infection. Cell Reports, 37, 109920.
dc.identifier.citedreferenceHan, Y., Zhu, J., Yang, L., Nilsson-Payant, B. E., Hurtado, R., Lacko, L. A., Sun, X., Gade, A. R., Higgins, C. A., Sisso, W. J., Dong, X., Wang, M., Chen, Z., Ho, D. D., Pitt, G. S., Schwartz, R. E., Tenoever, B. R., Evans, T., & Chen, S. ( 2022 ). SARS-CoV-2 infection induces ferroptosis of sinoatrial node pacemaker cells. Circulation Research, 130, 963 – 977.
dc.identifier.citedreferenceYang, L., Nilsson-Payant, B. E., Han, Y., Jaffré, F., Zhu, J., Wang, P., Zhang, T., Redmond, D., Houghton, S., Møller, R., Hoagland, D., Carrau, L., Horiuchi, S., Goff, M., Lim, J. K., Bram, Y., Richardson, C., Chandar, V., Borczuk, A., … Chen, S. ( 2021 ). Cardiomyocytes recruit monocytes upon SARS-CoV-2 infection by secreting CCL2. Stem Cell Reports, 16, 2565.
dc.identifier.citedreferenceYang, L., Han, Y., Jaffré, F., Nilsson-Payant, B. E., Bram, Y., Wang, P., Zhu, J., Zhang, T., Redmond, D., Houghton, S., Uhl, S., Borczuk, A., Huang, Y., Richardson, C., Chandar, V., Acklin, J. A., Lim, J. K., Chen, Z., Xiang, J., … Chen, S. ( 2021 ). An immuno-cardiac model for macrophage-mediated inflammation in COVID-19 hearts. Circulation Research, 129, 33 – 46.
dc.identifier.citedreferenceMorizane, R., Lam, A. Q., Freedman, B. S., Kishi, S., Valerius, M. T., & Bonventre, J. V. ( 2015 ). Nephron organoids derived from human pluripotent stem cells model kidney development and injury. Nature Biotechnology, 33, 1193 – 1200.
dc.identifier.citedreferenceFreedman, B. S., Brooks, C. R., Lam, A. Q., Fu, H., Morizane, R., Agrawal, V., Saad, A. F., Li, M. K., Hughes, M. R., Werff, R. V., Peters, D. T., Lu, J., Baccei, A., Siedlecki, A. M., Valerius, M. T., Musunuru, K., Mcnagny, K. M., Steinman, T. I., Zhou, J., … Bonventre, J. V. ( 2015 ). Modelling kidney disease with CRISPR-mutant kidney organoids derived from human pluripotent epiblast spheroids. Nature Communication, 6, 8715.
dc.identifier.citedreferenceCzerniecki, S. M., Cruz, N. M., Harder, J. L., Menon, R., Annis, J., Otto, E. A., Gulieva, R. E., Islas, L. V., Kim, Y. K., Tran, L. M., Martins, T. J., Pippin, J. W., Fu, H., Kretzler, M., Shankland, S. J., Himmelfarb, J., Moon, R. T., Paragas, N., & Freedman, B. S. ( 2018 ). High-throughput screening enhances kidney organoid differentiation from human pluripotent stem cells and enables automated multidimensional phenotyping. Cell Stem Cell, 22, 929 – 940.e4.
dc.identifier.citedreferencePrzepiorski, A., Sander, V., Tran, T., Hollywood, J. A., Sorrenson, B., Shih, J.-H., Wolvetang, E. J., Mcmahon, A. P., Holm, T. M., & Davidson, A. J. ( 2018 ). A simple bioreactor-based method to generate kidney organoids from pluripotent stem cells. Stem Cell Reports, 11, 470 – 484.
dc.identifier.citedreferenceKumar, S. V., Er, P. X., Lawlor, K. T., Motazedian, A., Scurr, M., Ghobrial, I., Combes, A. N., Zappia, L., Oshlack, A., Stanley, E. G., & Little, M. H. ( 2019 ). Kidney micro-organoids in suspension culture as a scalable source of human pluripotent stem cell-derived kidney cells. Development, 146, dev172361.
dc.identifier.citedreferenceTakasato, M., Er, P. X., Chiu, H. S., Maier, B., Baillie, G. J., Ferguson, C., Parton, R. G., Wolvetang, E. J., Roost, M. S., Chuva De Sousa Lopes, S. M., & Little, M. H. ( 2015 ). Kidney organoids from human iPS cells contain multiple lineages and model human nephrogenesis. Nature, 526, 564 – 568.
dc.identifier.citedreferenceTran, T., Song, C. J., Nguyen, T., Cheng, S.-Y., McMahon, J. A., Yang, R., Guo, Q., Der, B., Lindström, N. O., Lin, D. C.-H., & McMahon, A. P. ( 2022 ). A scalable organoid model of human autosomal dominant polycystic kidney disease for disease mechanism and drug discovery. Cell Stem Cell, 29 ( 7 ), 1083 – 1101.
dc.identifier.citedreferenceMiller, A. J., Yu, Q., Czerwinski, M., Tsai, Y. U.-H., Conway, R. F., Wu, A., Holloway, E. M., Walker, T., Glass, I. A., Treutlein, B., Camp, J. G., & Spence, J. R. ( 2020 ). In vitro and in vivo development of the human airway at single-cell resolution. Developmental Cell, 53, 117 – 128.e6.
dc.identifier.citedreferenceYu, Q., Kilik, U., Holloway, E. M., Tsai, Y. U.-H., Harmel, C., Wu, A., Wu, J. H., Czerwinski, M., Childs, C. J., He, Z., Capeling, M. M., Huang, S., Glass, I. A., Higgins, P. D. R., Treutlein, B., Spence, J. R., & Camp, J. G. ( 2021 ). Charting human development using a multi-endodermal organ atlas and organoid models. Cell, 184, 3281 – 3298.e22.
dc.identifier.citedreferenceMayr, U., Serra, D., & Liberali, P. ( 2019 ). Exploring single cells in space and time during tissue development, homeostasis and regeneration. Development, 146, dev176727.
dc.identifier.citedreferenceXavier Da Silveira Dos Santos, A., & Liberali, P. ( 2019 ). From single cells to tissue self-organization. FEBS Journal, 286, 1495 – 1513.
dc.identifier.citedreferenceSerra, D., Mayr, U., Boni, A., Lukonin, I., Rempfler, M., Challet Meylan, L., Stadler, M. B., Strnad, P., Papasaikas, P., Vischi, D., Waldt, A., Roma, G., & Liberali, P. ( 2019 ). Self-organization and symmetry breaking in intestinal organoid development. Nature, 569, 66 – 72.
dc.identifier.citedreferenceBenito-Kwiecinski, S., Giandomenico, S. L., Sutcliffe, M., Riis, E. S., Freire-Pritchett, P., Kelava, I., Wunderlich, S., Martin, U., Wray, G. A., Mcdole, K., & Lancaster, M. A. ( 2021 ). An early cell shape transition drives evolutionary expansion of the human forebrain. Cell, 184, 2084 – 2102.e19.
dc.identifier.citedreferenceKelava, I., Chiaradia, I., Pellegrini, L., Kalinka, A. T., & Lancaster, M. A. ( 2022 ). Androgens increase excitatory neurogenic potential in human brain organoids. Nature, 602, 112 – 116.
dc.identifier.citedreferenceGaspard, N., Bouschet, T., Hourez, R., Dimidschstein, J., Naeije, G., Van Den Ameele, J., Espuny-Camacho, I., Herpoel, A., Passante, L., Schiffmann, S. N., Gaillard, A., & Vanderhaeghen, P. ( 2008 ). An intrinsic mechanism of corticogenesis from embryonic stem cells. Nature, 455, 351 – 357.
dc.identifier.citedreferenceVan Den Ameele, J., Tiberi, L., Vanderhaeghen, P., & Espuny-Camacho, I. ( 2014 ). Thinking out of the dish: What to learn about cortical development using pluripotent stem cells. Trends in Neuroscience, 37, 334 – 342.
dc.identifier.citedreferenceLuo, C., Lancaster, M. A., Castanon, R., Nery, J. R., Knoblich, J. A., & Ecker, J. R. ( 2016 ). Cerebral organoids recapitulate epigenomic signatures of the human fetal brain. Cell Reports, 17, 3369 – 3384.
dc.identifier.citedreferenceBhaduri, A., Andrews, M. G., Mancia Leon, W., Jung, D., Shin, D., Allen, D., Jung, D., Schmunk, G., Haeussler, M., Salma, J., Pollen, A. A., Nowakowski, T. J., & Kriegstein, A. R. ( 2020 ). Cell stress in cortical organoids impairs molecular subtype specification. Nature, 578, 142 – 148.
dc.identifier.citedreferenceTanaka, Y., Cakir, B., Xiang, Y., Sullivan, G. J., & Park, I. N.-H. ( 2020 ). Synthetic analyses of single-cell transcriptomes from multiple brain organoids and fetal brain. Cell Reports, 30, 1682 – 1689.e3.
dc.identifier.citedreferenceRossi, G., Broguiere, N., Miyamoto, M., Boni, A., Guiet, R., Girgin, M., Kelly, R. G., Kwon, C., & Lutolf, M. P. ( 2021 ). Capturing cardiogenesis in gastruloids. Cell Stem Cell, 28, 230 – 240.e6.
dc.identifier.citedreferenceDrakhlis, L., Biswanath, S., Farr, C.-M., Lupanow, V., Teske, J., Ritzenhoff, K., Franke, A., Manstein, F., Bolesani, E., Kempf, H., Liebscher, S., Schenke-Layland, K., Hegermann, J., Nolte, L., Meyer, H., De La Roche, J., Thiemann, S., Wahl-Schott, C., Martin, U., & Zweigerdt, R. ( 2021 ). Human heart-forming organoids recapitulate early heart and foregut development. Nature Biotechnology, 39, 737 – 746.
dc.identifier.citedreferenceSilva, A. C., Matthys, O. B., Joy, D. A., Kauss, M. A., Natarajan, V., Lai, M. H., Turaga, D., Blair, A. P., Alexanian, M., Bruneau, B. G., & Mcdevitt, T. C. ( 2021 ). Co-emergence of cardiac and gut tissues promotes cardiomyocyte maturation within human iPSC-derived organoids. Cell Stem Cell, 28, 2137 – 2152.e6.
dc.identifier.citedreferenceHofbauer, P., Jahnel, S. M., Papai, N., Giesshammer, M., Deyett, A., Schmidt, C., Penc, M., Tavernini, K., Grdseloff, N., Meledeth, C., Ginistrelli, L. C., Ctortecka, C., Alic, E., Novatchkova, M., & Mendjan, S. ( 2021 ). Cardioids reveal self-organizing principles of human cardiogenesis. Cell, 184, 3299 – 3317.e22.
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