Progress and perspective of organoid technology in cancer-related translational medicine

Rossi, 2018, Progress and potential in organoid research, Nat. Rev. Genet., 19, 671, 10.1038/s41576-018-0051-9 Yoshida, 2020, Applications of patient-derived tumor xenograft models and tumor organoids, J. Hematol. Oncol., 13, 4, 10.1186/s13045-019-0829-z Wilson, 1907, New method by which sponges may be artificially reared, Science, 25, 912, 10.1126/science.25.649.912 Lancaster, 2014, Organogenesis in a dish: modeling development and disease using organoid technologies, Science, 345, 10.1126/science.1247125 Dutta, 2017, Disease modeling in stem cell-derived 3D organoid systems, Trends Mol. Med., 23, 393, 10.1016/j.molmed.2017.02.007 Artegiani, 2018, Use and application of 3D-organoid technology, Hum. Mol. Genet., 27, 10.1093/hmg/ddy187 Sato, 2009, Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche, Nature, 459, 262, 10.1038/nature07935 Sachs, 2018, A living biobank of breast cancer organoids captures disease heterogeneity, Cell, 172, 1, 10.1016/j.cell.2017.11.010 Fan, 2019, Emerging organoid models: leaping forward in cancer research, J. Hematol. Oncol., 12, 142, 10.1186/s13045-019-0832-4 Xu, 2018, Organoid technology and applications in cancer research, J. Hematol. Oncol., 11, 116, 10.1186/s13045-018-0662-9 Schutgens, 2020, Human organoids: tools for understanding biology and treating diseases, Annu. Rev. Pathol., 15, 211, 10.1146/annurev-pathmechdis-012419-032611 Drost, 2018, Organoids in cancer research, Nat. Rev. Cancer, 18, 407, 10.1038/s41568-018-0007-6 Wang, 2019, CD9 identifies pancreatic cancer stem cells and modulates glutamine metabolism to fuel tumour growth, Nat. Cell Biol., 21, 1425, 10.1038/s41556-019-0407-1 Tuveson, 2019, Cancer modeling meets human organoid technology, Science, 364, 952, 10.1126/science.aaw6985 Hendriks, 2021, Establishment of human fetal hepatocyte organoids and CRISPR-Cas9-based gene knockin and knockout in organoid cultures from human liver, Nat. Protoc., 16, 182, 10.1038/s41596-020-00411-2 Boj, 2015, Organoid models of human and mouse ductal pancreatic cancer, Cell, 160, 324, 10.1016/j.cell.2014.12.021 Koike, 2021, Engineering human hepato-biliary-pancreatic organoids from pluripotent stem cells, Nat. Protoc., 16, 919, 10.1038/s41596-020-00441-w Velasco, 2019, Individual brain organoids reproducibly form cell diversity of the human cerebral cortex, Nature, 570, 523, 10.1038/s41586-019-1289-x Qu, 2021, Establishment of intestinal organoid cultures modeling injury-associated epithelial regeneration, Cell Res, 31, 259, 10.1038/s41422-020-00453-x Drost, 2016, Organoid culture systems for prostate epithelial and cancer tissue, Nat. Protoc., 11, 347, 10.1038/nprot.2016.006 Hai, 2020, Generation of genetically engineered mouse lung organoid models for squamous cell lung cancers allows for the study of combinatorial immunotherapy, Clin. Cancer Res. Off. J. Am. Assoc. Cancer Res., 26, 3431, 10.1158/1078-0432.CCR-19-1627 Nikolaev, 2020, Homeostatic mini-intestines through scaffold-guided organoid morphogenesis, Nature, 585, 574, 10.1038/s41586-020-2724-8 Artegiani, 2020, Fast and efficient generation of knock-in human organoids using homology-independent CRISPR-Cas9 precision genome editing, Nat. Cell Biol., 22, 321, 10.1038/s41556-020-0472-5 Matano, 2015, Modeling colorectal cancer using CRISPR-Cas9-mediated engineering of human intestinal organoids, Nat. Med., 21, 256, 10.1038/nm.3802 Xiao, 2020, Evidence for gastrointestinal infection of SARS-CoV-2, Gastroenterology, 158, 10.1053/j.gastro.2020.02.055 Wang, 2020, Clinical characteristics of 138 hospitalized patients with 2019 novel coronavirus-infected pneumonia in Wuhan, China, JAMA, 323, 1061, 10.1001/jama.2020.1585 Zhou, 2020, Infection of bat and human intestinal organoids by SARS-CoV-2, Nat. Med., 26, 1077, 10.1038/s41591-020-0912-6 Lamers, 2020, SARS-CoV-2 productively infects human gut enterocytes, Science, 369, 50, 10.1126/science.abc1669 Prior, 2019, Liver organoids: from basic research to therapeutic applications, Gut, 68, 2228, 10.1136/gutjnl-2019-319256 Hu, 2018, Long-term expansion of functional mouse and human hepatocytes as 3D organoids, Cell, 175, 10.1016/j.cell.2018.11.013 Aloia, 2019, Epigenetic remodelling licences adult cholangiocytes for organoid formation and liver regeneration, Nat. Cell Biol., 21, 1321, 10.1038/s41556-019-0402-6 Wu, 2019, Generation of hepatobiliary organoids from human induced pluripotent stem cells, J. Hepatol., 70, 1145, 10.1016/j.jhep.2018.12.028 Schneeberger, 2020, Large-scale production of LGR5-positive bipotential human liver stem cells, Hepatology (Baltimore Md), 72, 257, 10.1002/hep.31037 Sun, 2019, Modelling liver cancer initiation with organoids derived from directly reprogrammed human hepatocytes, Nat. Cell Biol., 21, 1015, 10.1038/s41556-019-0359-5 Gkatzis, 2018, Use of three-dimensional organoids and lung-on-a-chip methods to study lung development, regeneration and disease, Eur. Respir. J., 52, 10.1183/13993003.00876-2018 Dost, 2020, Organoids model transcriptional hallmarks of oncogenic KRAS activation in lung epithelial progenitor cells, Cell stem Cell, 27, 10.1016/j.stem.2020.07.022 Kim, 2019, Patient-derived lung cancer organoids as in vitro cancer models for therapeutic screening, Nat. Commun., 10, 3991, 10.1038/s41467-019-11867-6 Shi, 2020, Organoid cultures as preclinical models of non-small cell lung cancer. clinical cancer research: an official journal of the american association for, Cancer Res., 26, 1162 Sachs, 2019, Long-term expanding human airway organoids for disease modeling. The, EMBO J., 38, 10.15252/embj.2018100300 Han, 2021, Identification of SARS-CoV-2 inhibitors using lung and colonic organoids, Nature, 589, 270, 10.1038/s41586-020-2901-9 Huang, 2014, Efficient generation of lung and airway epithelial cells from human pluripotent stem cells, Nat. Biotechnol., 32, 84, 10.1038/nbt.2754 Chen, 2019, Generation of pulmonary neuroendocrine cells and SCLC-like tumors from human embryonic stem cells, J. Exp. Med., 216, 674, 10.1084/jem.20181155 Tiriac, 2019, Organoid models for translational pancreatic cancer research, Curr. Opin. Genet. Dev., 54, 10.1016/j.gde.2019.02.003 Engle, 2019, The glycan CA19-9 promotes pancreatitis and pancreatic cancer in mice, Sci. (N. Y., NY), 364, 1156, 10.1126/science.aaw3145 Tiriac, 2018, Organoid profiling identifies common responders to chemotherapy in pancreatic cancer, Cancer Discov., 8, 1112, 10.1158/2159-8290.CD-18-0349 Driehuis, 2019, Pancreatic cancer organoids recapitulate disease and allow personalized drug screening, Proc. Natl. Acad. Sci. USA, 10.1073/pnas.1911273116 Vlachogiannis, 2018, Patient-derived organoids model treatment response of metastatic gastrointestinal cancers, Sci. (N. Y., NY), 359, 920, 10.1126/science.aao2774 Dekkers, 2020, Modeling breast cancer using CRISPR-Cas9-mediated engineering of human breast organoids, J. Natl. Cancer Inst., 112, 540, 10.1093/jnci/djz196 Yan, 2018, A comprehensive human gastric cancer organoid biobank captures tumor subtype heterogeneity and enables therapeutic screening, Cell Stem Cell, 23, 10.1016/j.stem.2018.09.016 Rosenbluth, 2020, Organoid cultures from normal and cancer-prone human breast tissues preserve complex epithelial lineages, Nat. Commun., 11, 1711, 10.1038/s41467-020-15548-7 Miao, 2020, Next-generation surrogate wnts support organoid growth and deconvolute frizzled pleiotropy in vivo, Cell Stem Cell, 27, 10.1016/j.stem.2020.07.020 Rios, 2019, Intraclonal plasticity in mammary tumors revealed through large-scale single-cell resolution 3D imaging, Cancer Cell, 35, 953, 10.1016/j.ccell.2019.05.011 Lee, 2018, Tumor evolution and drug response in patient-derived organoid models of bladder, Cancer Cell., 173 Mullenders, 2019, Mouse and human urothelial cancer organoids: A tool for bladder cancer research, Proc. Natl. Acad. Sci. USA, 116, 4567, 10.1073/pnas.1803595116 Bi, 2021, Successful patient-derived organoid culture of gynecologic cancers for disease modeling and drug sensitivity testing, Cancers (Basel), 13, 10.3390/cancers13122901 Bi, 2020, Characterization of a TP53 somatic variant of unknown function from an ovarian cancer patient using organoid culture and computational modeling, Clin. Obstet. Gynecol., 63, 109, 10.1097/GRF.0000000000000516 Trujillo, 2019, Complex oscillatory waves emerging from cortical organoids model early human brain network development, Cell stem Cell, 25, 10.1016/j.stem.2019.08.002 Low, 2019, Generation of human PSC-derived kidney organoids with patterned nephron segments and a de novo vascular network, Cell Stem Cell, 25, 10.1016/j.stem.2019.06.009 Kupfer, 2020, In situ expansion, differentiation, and electromechanical coupling of human cardiac muscle in a 3D bioprinted, chambered organoid, Circ. Res., 127, 207, 10.1161/CIRCRESAHA.119.316155 Kopper, 2019, An organoid platform for ovarian cancer captures intra- and interpatient heterogeneity, Nat. Med., 25, 838, 10.1038/s41591-019-0422-6 Calandrini, 2020, An organoid biobank for childhood kidney cancers that captures disease and tissue heterogeneity, Nat. Commun., 11, 1310, 10.1038/s41467-020-15155-6 Wimmer, 2019, Human blood vessel organoids as a model of diabetic vasculopathy, Nature, 565, 505, 10.1038/s41586-018-0858-8 Monteil, 2020, Inhibition of SARS-CoV-2 infections in engineered human tissues using clinical-grade soluble human ACE2, Cell, 181, 10.1016/j.cell.2020.04.004 Homan, 2019, Flow-enhanced vascularization and maturation of kidney organoids in vitro, Nat. Methods, 16, 255, 10.1038/s41592-019-0325-y Wimmer, 2019, Generation of blood vessel organoids from human pluripotent stem cells, Nat. Protoc., 14, 3082, 10.1038/s41596-019-0213-z Schnalzger, 2019, 3D model for CAR-mediated cytotoxicity using patient-derived colorectal cancer organoids, EMBO J., 38, 10.15252/embj.2018100928 Beshiri, 2018, A PDX/organoid biobank of advanced prostate cancers captures genomic and phenotypic heterogeneity for disease modeling and therapeutic screening, Clin. Cancer Res.: Off. J. Am. Assoc. Cancer Res., 24, 4332, 10.1158/1078-0432.CCR-18-0409 Driehuis, 2019, Oral mucosal organoids as a potential platform for personalized cancer therapy, Cancer Discov., 9, 852, 10.1158/2159-8290.CD-18-1522 Dijkstra, 2018, Generation of tumor-reactive T cells by co-culture of peripheral blood lymphocytes and tumor organoids, Cell, 174, 10.1016/j.cell.2018.07.009 Cattaneo, 2020, Tumor organoid-T-cell coculture systems, Nat. Protoc., 15, 15, 10.1038/s41596-019-0232-9 Neal, 2018, Organoid modeling of the tumor immune microenvironment, Cell, 175, 10.1016/j.cell.2018.11.021 Park, 2019, Huh D. Organoids-on-a-chip, Science, 364, 960, 10.1126/science.aaw7894 Sontheimer-Phelps, 2019, Modelling cancer in microfluidic human organs-on-chips, Nat. Rev. Cancer, 19, 65, 10.1038/s41568-018-0104-6 Shirure, 2018, Tumor-on-a-chip platform to investigate progression and drug sensitivity in cell lines and patient-derived organoids, Lab Chip, 18, 3687, 10.1039/C8LC00596F Jung, 2019, A one-stop microfluidic-based lung cancer organoid culture platform for testing drug sensitivity, Lab Chip, 19, 2854, 10.1039/C9LC00496C Truong, 2019, A human organotypic microfluidic tumor model permits investigation of the interplay between patient-derived fibroblasts and breast cancer cells, Cancer Res., 79, 3139, 10.1158/0008-5472.CAN-18-2293 Uhl, 2019, Microfluidic device for expedited tumor growth towards drug evaluation, Lab Chip, 19, 1458, 10.1039/C8LC01250D Fujii, 2019, Modeling human digestive diseases with CRISPR-Cas9-modified organoids, Gastroenterology, 156, 562, 10.1053/j.gastro.2018.11.048 Chakraborty, 2020, Significance of and co-loss in aggressive prostate cancer progression. Clinical cancer research: an official journal of the American Association for, Clin. Cancer Res. Off. J. Am. Assoc. Cancer Res., 26, 2047, 10.1158/1078-0432.CCR-19-1570 Bian, 2018, Genetically engineered cerebral organoids model brain tumor formation, Nat. Methods, 15, 631, 10.1038/s41592-018-0070-7 Michels, 2020, Pooled in vitro and in vivo CRISPR-Cas9 screening identifies tumor suppressors in human colon organoids, Cell Stem Cell, 26, 10.1016/j.stem.2020.04.003 Yavitt, 2020, The effect of thiol structure on allyl sulfide photodegradable hydrogels and their application as a degradable scaffold for organoid passaging, Adv. Mater., 32, 10.1002/adma.201905366 Mollica, 2019, 3D bioprinted mammary organoids and tumoroids in human mammary derived ECM hydrogels, Acta Biomater., 95, 201, 10.1016/j.actbio.2019.06.017 Ye, 2020, Organoids to study immune functions, immunological diseases and immunotherapy, Cancer Lett., 477, 31, 10.1016/j.canlet.2020.02.027 Holokai, 2020, Murine- and human-derived autologous organoid/immune cell co-cultures as pre-clinical models of pancreatic ductal adenocarcinoma, Cancers, 12, 10.3390/cancers12123816