Building consensus on definition and nomenclature of hepatic, pancreatic, and biliary organoids

Cell Stem Cell - Tập 28 - Trang 816-832 - 2021
Ary Marsee1, Floris J.M. Roos2, Monique M.A. Verstegen3
1Department of Clinical Sciences, Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands
2Department of Surgery, Erasmus MC-University Medical Center, Rotterdam, the Netherlands
3Department of Surgery, Erasmus MC University Medical Center, Rotterdam, The Netherlands

Tài liệu tham khảo

Achilli, 2012, Advances in the formation, use and understanding of multi-cellular spheroids, Expert Opin. Biol. Ther., 12, 1347, 10.1517/14712598.2012.707181 Aizarani, 2019, A human liver cell atlas reveals heterogeneity and epithelial progenitors, Nature, 572, 199, 10.1038/s41586-019-1373-2 Akbari, 2019, Robust, long-term culture of endoderm-derived hepatic organoids for disease modeling, Stem Cell Reports, 13, 627, 10.1016/j.stemcr.2019.08.007 Aloia, 2019, Epigenetic remodelling licences adult cholangiocytes for organoid formation and liver regeneration, Nat. Cell Biol., 21, 1321, 10.1038/s41556-019-0402-6 Arnaoutova, 2012, Basement membrane matrix (BME) has multiple uses with stem cells, Stem Cell Rev. Rep., 8, 163, 10.1007/s12015-011-9278-y Banales, 2009, The cAMP effectors Epac and protein kinase a (PKA) are involved in the hepatic cystogenesis of an animal model of autosomal recessive polycystic kidney disease (ARPKD), Hepatology, 49, 160, 10.1002/hep.22636 Banales, 2020, Cholangiocarcinoma 2020: the next horizon in mechanisms and management, Nat. Rev. Gastroenterol. Hepatol., 17, 557, 10.1038/s41575-020-0310-z Baron, 2016, A single-cell transcriptomic map of the human and mouse pancreas reveals inter- and intra-cell population structure, Cell Syst., 3, 346, 10.1016/j.cels.2016.08.011 Bell, 2016, Characterization of primary human hepatocyte spheroids as a model system for drug-induced liver injury, liver function and disease, Sci. Rep., 6, 25187, 10.1038/srep25187 Bock, 2021, The organoid cell atlas, Nat. Biotechnol., 39, 13, 10.1038/s41587-020-00762-x Boj, 2015, Organoid models of human and mouse ductal pancreatic cancer, Cell, 160, 324, 10.1016/j.cell.2014.12.021 Bonfanti, 2015, Ex vivo expansion and differentiation of human and mouse fetal pancreatic progenitors are modulated by epidermal growth factor, Stem Cells Dev., 24, 1766, 10.1089/scd.2014.0550 Breunig, 2021, Modeling plasticity and dysplasia of pancreatic ductal organoids derived from human pluripotent stem cells, Cell Stem Cell, 28, 10.1016/j.stem.2021.03.005 Broguiere, 2018, Growth of epithelial organoids in a defined hydrogel, Adv. Mater., 30, e1801621, 10.1002/adma.201801621 Broutier, 2016, Culture and establishment of self-renewing human and mouse adult liver and pancreas 3D organoids and their genetic manipulation, Nat. Protoc., 11, 1724, 10.1038/nprot.2016.097 Broutier, 2017, Human primary liver cancer-derived organoid cultures for disease modeling and drug screening, Nat. Med., 23, 1424, 10.1038/nm.4438 Chen, 2012, Rapid generation of mature hepatocyte-like cells from human induced pluripotent stem cells by an efficient three-step protocol, Hepatology, 55, 1193, 10.1002/hep.24790 Cui, 2017, Advances in multicellular spheroids formation, J. R. Soc. Interface, 14, 20160877, 10.1098/rsif.2016.0877 Dai, 2016, CRISPR-Cas9 for in vivo gene therapy: promise and hurdles, Mol. Ther. Nucleic Acids, 5, e349, 10.1038/mtna.2016.58 Deng, 2018, Chronic liver injury induces conversion of biliary epithelial cells into hepatocytes, Cell Stem Cell, 23, 114, 10.1016/j.stem.2018.05.022 Dianat, 2014, Generation of functional cholangiocyte-like cells from human pluripotent stem cells and HepaRG cells, Hepatology, 60, 700, 10.1002/hep.27165 Dorrell, 2014, The organoid-initiating cells in mouse pancreas and liver are phenotypically and functionally similar, Stem Cell Res. (Amst.), 13, 275, 10.1016/j.scr.2014.07.006 Fan, 2015, Bioengineering thymus organoids to restore thymic function and induce donor-specific immune tolerance to allografts, Mol. Ther., 23, 1262, 10.1038/mt.2015.77 Fennema, 2013, Spheroid culture as a tool for creating 3D complex tissues, Trends Biotechnol., 31, 108, 10.1016/j.tibtech.2012.12.003 Forner, 2018, Hepatocellular carcinoma, Lancet, 391, 1301, 10.1016/S0140-6736(18)30010-2 Fowler, 2013, Combined hepatocellular and cholangiocarcinoma (biphenotypic) tumors: imaging features and diagnostic accuracy of contrast-enhanced CT and MRI, AJR Am. J. Roentgenol., 201, 332, 10.2214/AJR.12.9488 Georgakopoulos, 2020, Long-term expansion, genomic stability and in vivo safety of adult human pancreas organoids, BMC Dev. Biol., 20, 4, 10.1186/s12861-020-0209-5 Ghurburrun, 2018, Liver and pancreas: do similar embryonic development and tissue organization lead to similar mechanisms of tumorigenesis?, Gene Expr., 18, 149, 10.3727/105221618X15216414278706 Giancola, 2012, Cell therapy: cGMP facilities and manufacturing, Muscles Ligaments Tendons J., 2, 243 Giobbe, 2019, Extracellular matrix hydrogel derived from decellularized tissues enables endodermal organoid culture, Nat. Commun., 10, 5658, 10.1038/s41467-019-13605-4 Greggio, 2013, Artificial three-dimensional niches deconstruct pancreas development in vitro, Development, 140, 4452, 10.1242/dev.096628 Guan, 2017, Human hepatic organoids for the analysis of human genetic diseases, JCI Insight, 2, e94954, 10.1172/jci.insight.94954 Haegebarth, 2009, Wnt signaling, lgr5, and stem cells in the intestine and skin, Am. J. Pathol., 174, 715, 10.2353/ajpath.2009.080758 Hanna, 2016, Advanced therapy medicinal products: current and future perspectives, J. Mark. Access Health Policy, 4 Hannan, 2013, Production of hepatocyte-like cells from human pluripotent stem cells, Nat. Protoc., 8, 430, 10.1038/nprot.2012.153 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 Hohwieler, 2017, Human pluripotent stem cell-derived acinar/ductal organoids generate human pancreas upon orthotopic transplantation and allow disease modelling, Gut, 66, 473, 10.1136/gutjnl-2016-312423 Hu, 2018, Long-term expansion of functional mouse and human hepatocytes as 3D organoids, Cell, 175, 1591, 10.1016/j.cell.2018.11.013 Huang, 2015, Ductal pancreatic cancer modeling and drug screening using human pluripotent stem cell- and patient-derived tumor organoids, Nat. Med., 21, 1364, 10.1038/nm.3973 Huang, 2021, Commitment and oncogene-induced plasticity of human stem cell-derived pancreatic acinar and ductal organoids, Cell Stem Cell, 28, 10.1016/j.stem.2021.03.022 Huch, 2015, Modeling mouse and human development using organoid cultures, Development, 142, 3113, 10.1242/dev.118570 Huch, 2013, In vitro expansion of single Lgr5+ liver stem cells induced by Wnt-driven regeneration, Nature, 494, 247, 10.1038/nature11826 Huch, 2013, Unlimited in vitro expansion of adult bi-potent pancreas progenitors through the Lgr5/R-spondin axis, EMBO J., 32, 2708, 10.1038/emboj.2013.204 Huch, 2015, Long-term culture of genome-stable bipotent stem cells from adult human liver, Cell, 160, 299, 10.1016/j.cell.2014.11.050 Hughes, 2010, Matrigel: a complex protein mixture required for optimal growth of cell culture, Proteomics, 10, 1886, 10.1002/pmic.200900758 Kim, 2020, Human organoids: model systems for human biology and medicine, Nat. Rev. Mol. Cell Biol., 21, 571, 10.1038/s41580-020-0259-3 Koike, 2019, Modelling human hepato-biliary-pancreatic organogenesis from the foregut-midgut boundary, Nature, 574, 112, 10.1038/s41586-019-1598-0 Kolbe, 2019, Mutual zonated interactions of Wnt and Hh signaling are orchestrating the metabolism of the adult liver in mice and human, Cell Rep., 29, 4553, 10.1016/j.celrep.2019.11.104 Kumar, 2019, Kidney micro-organoids in suspension culture as a scalable source of human pluripotent stem cell-derived kidney cells, Development, 146, dev172361, 10.1242/dev.172361 Lampis, 2018, MIR21 drives resistance to heat shock protein 90 inhibition in cholangiocarcinoma, Gastroenterology, 154, 1066, 10.1053/j.gastro.2017.10.043 Lancaster, 2014, Organogenesis in a dish: modeling development and disease using organoid technologies, Science, 345, 1247125, 10.1126/science.1247125 Lau, 2020, Organoid models of gastrointestinal cancers in basic and translational research, Nat. Rev. Gastroenterol. Hepatol., 17, 203, 10.1038/s41575-019-0255-2 Lee, 2008, MicroRNA15a modulates expression of the cell-cycle regulator Cdc25A and affects hepatic cystogenesis in a rat model of polycystic kidney disease, J. Clin. Invest., 118, 3714, 10.1172/JCI34922 Leung, 2018, Recent advances in Lgr5+ stem cell research, Trends Cell Biol., 28, 380, 10.1016/j.tcb.2018.01.010 Lo, 2009, Ethical issues in stem cell research, Endocr. Rev., 30, 204, 10.1210/er.2008-0031 Lo, 2020, Applications of organoids for cancer biology and precision medicine, Nat. Can., 1, 761, 10.1038/s43018-020-0102-y Loomans, 2018, Expansion of adult human pancreatic tissue yields organoids harboring progenitor cells with endocrine differentiation potential, Stem Cell Reports, 10, 712, 10.1016/j.stemcr.2018.02.005 Lugli, 2016, R-spondin 1 and noggin facilitate expansion of resident stem cells from non-damaged gallbladders, EMBO Rep., 17, 769, 10.15252/embr.201642169 Manco, 2019, Reactive cholangiocytes differentiate into proliferative hepatocytes with efficient DNA repair in mice with chronic liver injury, J. Hepatol., 70, 1180, 10.1016/j.jhep.2019.02.003 McCauley, 2017, Pluripotent stem cell-derived organoids: using principles of developmental biology to grow human tissues in a dish, Development, 144, 958, 10.1242/dev.140731 Mun, 2019, Generation of expandable human pluripotent stem cell-derived hepatocyte-like liver organoids, J. Hepatol., 71, 970, 10.1016/j.jhep.2019.06.030 Nikolaev, 2020, Homeostatic mini-intestines through scaffold-guided organoid morphogenesis, Nature, 585, 574, 10.1038/s41586-020-2724-8 Nuciforo, 2018, Organoid models of human liver cancers derived from tumor needle biopsies, Cell Rep., 24, 1363, 10.1016/j.celrep.2018.07.001 Ober, 2018, Development of the liver: Insights into organ and tissue morphogenesis, J. Hepatol., 68, 1049, 10.1016/j.jhep.2018.01.005 Ogawa, 2015, Directed differentiation of cholangiocytes from human pluripotent stem cells, Nat. Biotechnol., 33, 853, 10.1038/nbt.3294 Ootani, 2009, Sustained in vitro intestinal epithelial culture within a Wnt-dependent stem cell niche, Nat. Med., 15, 701, 10.1038/nm.1951 Osakada, 2009, Stepwise differentiation of pluripotent stem cells into retinal cells, Nat. Protoc., 4, 811, 10.1038/nprot.2009.51 Ouchi, 2019, Modeling steatohepatitis in humans with pluripotent stem cell-derived organoids, Cell Metab., 30, 374, 10.1016/j.cmet.2019.05.007 Ovando-Roche, 2018, Use of bioreactors for culturing human retinal organoids improves photoreceptor yields, Stem Cell Res. Ther., 9, 156, 10.1186/s13287-018-0907-0 Palikuqi, 2020, Adaptable haemodynamic endothelial cells for organogenesis and tumorigenesis, Nature, 585, 426, 10.1038/s41586-020-2712-z Peng, 2018, Inflammatory cytokine TNFα promotes the long-term expansion of primary hepatocytes in 3D culture, Cell, 175, 1607, 10.1016/j.cell.2018.11.012 Phelan, 2018, Mini and customized low-cost bioreactors for optimized high-throughput generation of tissue organoids, Stem Cell Investig., 5, 33, 10.21037/sci.2018.09.06 Planas-Paz, 2019, YAP, but not RSPO-LGR4/5, signaling in biliary epithelial cells promotes a ductular reaction in response to liver injury, Cell Stem Cell, 25, 39, 10.1016/j.stem.2019.04.005 Porter, 2020, Current concepts in tumour-derived organoids, Br. J. Cancer, 123, 1209, 10.1038/s41416-020-0993-5 Prior, 2019, Liver organoids: from basic research to therapeutic applications, Gut, 68, 2228, 10.1136/gutjnl-2019-319256 Prior, 2019, Lgr5+ stem and progenitor cells reside at the apex of a heterogeneous embryonic hepatoblast pool, Development, 146, dev174557, 10.1242/dev.174557 Przepiorski, 2018, A simple bioreactor-based method to generate kidney organoids from pluripotent stem cells, Stem Cell Reports, 11, 470, 10.1016/j.stemcr.2018.06.018 Ramli, 2020, Human pluripotent stem cell-derived organoids as models of liver disease, Gastroenterology, 159, 1471, 10.1053/j.gastro.2020.06.010 Raven, 2017, Cholangiocytes act as facultative liver stem cells during impaired hepatocyte regeneration, Nature, 547, 350, 10.1038/nature23015 Rimland, 2021, Regional differences in human biliary tissues and corresponding in vitro-derived organoids, Hepatology, 73, 247, 10.1002/hep.31252 Roos, 2021, Human bile contains cholangiocyte organoid-initiating cells which expand as functional cholangiocytes in non-canonical Wnt stimulating conditions, Front. Cell Dev. Biol., 8, 630492, 10.3389/fcell.2020.630492 Ryan, 2014, Pancreatic adenocarcinoma, N. Engl. J. Med., 371, 2140, 10.1056/NEJMra1404198 Saito, 2019, Establishment of patient-derived organoids and drug screening for biliary tract carcinoma, Cell Rep., 27, 1265, 10.1016/j.celrep.2019.03.088 Saltsman, 2020, A Human Organoid Model of Aggressive Hepatoblastoma for Disease Modeling and Drug Testing, Cancers (Basel), 12, 2668, 10.3390/cancers12092668 Sampaziotis, 2015, Cholangiocytes derived from human induced pluripotent stem cells for disease modeling and drug validation, Nat. Biotechnol., 33, 845, 10.1038/nbt.3275 Sampaziotis, 2017, Reconstruction of the mouse extrahepatic biliary tree using primary human extrahepatic cholangiocyte organoids, Nat. Med., 23, 954, 10.1038/nm.4360 Sampaziotis, 2021, Cholangiocyte organoids can repair bile ducts after transplantation in the human liver, Science, 371, 839, 10.1126/science.aaz6964 Sato, 2009, Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche, Nature, 459, 262, 10.1038/nature07935 Sato, 2011, Long-term expansion of epithelial organoids from human colon, adenoma, adenocarcinoma, and Barrett’s epithelium, Gastroenterology, 141, 1762, 10.1053/j.gastro.2011.07.050 Schaub, 2018, De novo formation of the biliary system by TGFβ-mediated hepatocyte transdifferentiation, Nature, 557, 247, 10.1038/s41586-018-0075-5 Schleicher, 2015, Zonation of hepatic fatty acid metabolism - the diversity of its regulation and the benefit of modeling, Biochim. Biophys. Acta, 1851, 641, 10.1016/j.bbalip.2015.02.004 Schneeberger, 2020, Large-scale production of LGR5-positive bipotential human liver stem cells, Hepatology, 72, 257, 10.1002/hep.31037 Schuijers, 2012, Adult mammalian stem cells: the role of Wnt, Lgr5 and R-spondins, EMBO J., 31, 2685, 10.1038/emboj.2012.149 Seino, 2018, Human Pancreatic Tumor Organoids Reveal Loss of Stem Cell Niche Factor Dependence during Disease Progression, Cell Stem Cell, 22, 454, 10.1016/j.stem.2017.12.009 Shamir, 2014, Three-dimensional organotypic culture: experimental models of mammalian biology and disease, Nat. Rev. Mol. Cell Biol., 15, 647, 10.1038/nrm3873 Shinozawa, 2021, High-fidelity drug-induced liver injury screen using human pluripotent stem cell-derived organoids, Gastroenterology, 160, 831, 10.1053/j.gastro.2020.10.002 Si-Tayeb, 2010, Highly efficient generation of human hepatocyte-like cells from induced pluripotent stem cells, Hepatology, 51, 297, 10.1002/hep.23354 Simian, 2017, Organoids: a historical perspective of thinking in three dimensions, J. Cell Biol., 216, 31, 10.1083/jcb.201610056 Soroka, 2019, Bile-derived organoids from patients with primary sclerosing cholangitis recapitulate their inflammatory immune profile, Hepatology, 70, 871, 10.1002/hep.30470 Sorrentino, 2020, Mechano-modulatory synthetic niches for liver organoid derivation, Nat. Commun., 11, 3416, 10.1038/s41467-020-17161-0 Spence, 2009, Sox17 regulates organ lineage segregation of ventral foregut progenitor cells, Dev. Cell, 17, 62, 10.1016/j.devcel.2009.05.012 Spence, 2011, Directed differentiation of human pluripotent stem cells into intestinal tissue in vitro, Nature, 470, 105, 10.1038/nature09691 Strand, 2010, Perspectives on tissue interactions in development and disease, Curr. Mol. Med., 10, 95, 10.2174/156652410791065363 Sun, 2020, AXIN2+ pericentral hepatocytes have limited contributions to liver homeostasis and regeneration, Cell Stem Cell, 26, 97, 10.1016/j.stem.2019.10.011 Takahashi, 2006, Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors, Cell, 126, 663, 10.1016/j.cell.2006.07.024 Takahashi, 2007, Induction of pluripotent stem cells from adult human fibroblasts by defined factors, Cell, 131, 861, 10.1016/j.cell.2007.11.019 Takebe, 2013, Vascularized and functional human liver from an iPSC-derived organ bud transplant, Nature, 499, 481, 10.1038/nature12271 Takebe, 2015, Vascularized and complex organ buds from diverse tissues via mesenchymal cell-driven condensation, Cell Stem Cell, 16, 556, 10.1016/j.stem.2015.03.004 Takebe, 2017, Massive and reproducible production of liver buds entirely from human pluripotent stem cells, Cell Rep., 21, 2661, 10.1016/j.celrep.2017.11.005 Tysoe, 2019, Isolation and propagation of primary human cholangiocyte organoids for the generation of bioengineered biliary tissue, Nat. Protoc., 14, 1884, 10.1038/s41596-019-0168-0 van de Wetering, 2015, Prospective derivation of a living organoid biobank of colorectal cancer patients, Cell, 161, 933, 10.1016/j.cell.2015.03.053 Verstegen, 2020, Human extrahepatic and intrahepatic cholangiocyte organoids show region-specific differentiation potential and model cystic fibrosis-related bile duct disease, Sci. Rep., 10, 21900, 10.1038/s41598-020-79082-8 Vyas, 2018, Self-assembled liver organoids recapitulate hepatobiliary organogenesis in vitro, Hepatology, 67, 750, 10.1002/hep.29483 Wang, 2015, Self-renewing diploid Axin2(+) cells fuel homeostatic renewal of the liver, Nature, 524, 180, 10.1038/nature14863 Wang, 2019, Human ESC-derived expandable hepatic organoids enable therapeutic liver repopulation and pathophysiological modeling of alcoholic liver injury, Cell Res., 29, 1009, 10.1038/s41422-019-0242-8 Wang, 2020, Long-term expansion of pancreatic islet organoids from resident Procr+ progenitors, Cell, 180, 1198, 10.1016/j.cell.2020.02.048 Wollny, 2016, Single-cell analysis uncovers clonal acinar cell heterogeneity in the adult pancreas, Dev. Cell, 39, 289, 10.1016/j.devcel.2016.10.002 Wong, 2012, Directed differentiation of human pluripotent stem cells into mature airway epithelia expressing functional CFTR protein, Nat. Biotechnol., 30, 876, 10.1038/nbt.2328 Wu, 2019, Generation of hepatobiliary organoids from human induced pluripotent stem cells, J. Hepatol., 70, 1145, 10.1016/j.jhep.2018.12.028 Xu, 2019, Targeted disruption of HLA genes via CRISPR-Cas9 generates iPSCs with enhanced immune compatibility, Cell Stem Cell, 24, 566, 10.1016/j.stem.2019.02.005 Ye, 2020, A chemically defined hydrogel for human liver organoid culture, Adv. Funct. Mater., 30, 2000893, 10.1002/adfm.202000893 Yoshihara, 2020, Immune-evasive human islet-like organoids ameliorate diabetes, Nature, 586, 606, 10.1038/s41586-020-2631-z Yusa, 2011, Targeted gene correction of α1-antitrypsin deficiency in induced pluripotent stem cells, Nature, 478, 391, 10.1038/nature10424 Zhang, 2018, In vitro expansion of primary human hepatocytes with efficient liver repopulation capacity, Cell Stem Cell, 23, 806, 10.1016/j.stem.2018.10.018