374
Views
3
CrossRef citations to date
0
Altmetric
Review

Developing models of cholangiocarcinoma to close the translational gap in cancer research

& ORCID Icon
Pages 439-450 | Received 08 Dec 2020, Accepted 26 Jan 2021, Published online: 14 Feb 2021

References

  • Banales JM, Marin JJG, Lamarca A, et al. Cholangiocarcinoma 2020: the next horizon in mechanisms and management. Nat Rev Gastroenterol Hepatol. 2020;17:557–588.
  • Wong MCS, Jiang JY, Goggins WB, et al. International incidence and mortality trends of liver cancer: a global profile. Scientific Reports. 2017;7(1):45846. .
  • Florio AA, Ferlay J, Znaor A, et al. Global trends in intrahepatic and extrahepatic cholangiocarcinoma incidence from 1993 to 2012. Cancer. 2020;126(11):2666–2678. .
  • Forner A, Vidili G, Rengo M, et al. Clinical presentation, diagnosis and staging of cholangiocarcinoma. Liver International. 2019;39(S1):98–107. .
  • Rizvi S, Gores GJ. Pathogenesis, Diagnosis, and Management of Cholangiocarcinoma. Gastroenterology. 2013;145(6):1215–1229.
  • Simile MM, Bagella P, Vidili G, et al. Targeted therapies in cholangiocarcinoma: emerging evidence from clinical trials. Medicina (Kaunas). 2019 8;55(2):42.
  • Abou-Alfa GK, Macarulla T, Javle MM, et al. Ivosidenib in IDH1-mutant, chemotherapy-refractory cholangiocarcinoma (ClarIDHy): a multicentre, randomised, double-blind, placebo-controlled, phase 3 study. The Lancet Oncology. 2020;21(6):796–807. .
  • Abou-Alfa GK, Sahai V, Hollebecque A, et al. Pemigatinib for previously treated, locally advanced or metastatic cholangiocarcinoma: a multicentre, open-label, phase 2 study. The Lancet Oncology. 2020;21(5):671–684. .
  • Bertuccio P, Malvezzi M, Carioli G, et al. Global trends in mortality from intrahepatic and extrahepatic cholangiocarcinoma. J Hepatol. 2019;71(1):104–114. .
  • Barner-Rasmussen N, Pukkala E, Jussila A, et al. Epidemiology, risk of malignancy and patient survival in primary sclerosing cholangitis: a population-based study in Finland. Scand J Gastroenterol. 2020;55(1):74–81. .
  • Lorenzini S, Bird TG, Boulter L, et al. Characterisation of a stereotypical cellular and extracellular adult liver progenitor cell niche in rodents and diseased human liver. Gut. 2010;59(5):645–654. .
  • Boulter L, Guest RV, Kendall TJ, et al. WNT signaling drives cholangiocarcinoma growth and can be pharmacologically inhibited. Journal of Clinical Investigation. 2015;125(3):1269–1285. .
  • Fabris L, Perugorria MJ, Mertens J, et al. The tumour microenvironment and immune milieu of cholangiocarcinoma. Liver Int. 2019;39(Suppl 1):63–78.
  • Zhang M, Yang H, Wan L, et al. Single-cell transcriptomic architecture and intercellular crosstalk of human intrahepatic cholangiocarcinoma. J Hepatol. 2020;73(5):1118–1130.
  • Ong CK, Subimerb C, Pairojkul C, et al. Exome sequencing of liver flukeg-associated cholangiocarcinoma. Nat Genet. 2012;44(6):690–693.
  • Jusakul A, Cutcutache I, Yong CH, et al. Whole-genome and epigenomic landscapes of etiologically distinct subtypes of cholangiocarcinoma. Cancer Discov. 2017;7(10):1116–1135.
  • Chan-On W, Nairismägi ML, Ong CK, et al. Exome sequencing identifies distinct mutational patterns in liver fluke-related and non-infection-related bile duct cancers. Nat Genet. 2013;45(12):1474–1478.
  • Goyal L, Govindan A, Sheth RA, et al. Prognosis and Clinicopathologic Features of Patients With Advanced Stage Isocitrate Dehydrogenase (IDH) Mutant and IDH Wild‐Type Intrahepatic Cholangiocarcinoma. Oncologist. 2015;20(9):1019–1027.
  • Graham RP, Barr Fritcher EG, Pestova E, et al. Fibroblast growth factor receptor 2 translocations in intrahepatic cholangiocarcinoma. Hum Pathol. 2014;45(8):1630–1638.
  • Tariq N, McNamara MG, Valle JW. Biliary tract cancers: current knowledge, clinical candidates and future challenges. Cancer Manag Res. 2019;11:2623–2642.
  • Kendall T, Verheij J, Gaudio E, et al. Anatomical, histomorphological and molecular classification of cholangiocarcinoma. Liver Int. 2019;39:7–18.
  • Malenica I, Donadon M, Lleo A. Molecular and Immunological Characterization of Biliary Tract Cancers: a Paradigm Shift Towards a Personalized Medicine. Cancers (Basel). 2020;12:2190.
  • Churi CR, Shroff R, Wang Y, et al. Mutation profiling in cholangiocarcinoma: prognostic and therapeutic implications. PLoS One. 2014;9:1–23.
  • Xue TC, Zhang BH, Ye SL, et al. Differentially expressed gene profiles of intrahepatic cholangiocarcinoma, hepatocellular carcinoma, and combined hepatocellular-cholangiocarcinoma by integrated microarray analysis. Tumor Biol. 2015;36:5891–5899.
  • Boulter L, Guest RV, Kendall TJ, et al. WNT signalling drives cholangiocarcinoma growth and can be pharmacologically inhibited. J Clin Investig. 2014;125:1269–1285.
  • Zender S, Nickeleit I, Wuestefeld T, et al. A critical role for notch signaling in the formation of cholangiocellular carcinomas. Cancer Cell. 2013;23:784–795.
  • Guest RV, Boulter L, Dwyer BJ, et al. Notch3 drives development and progression of cholangiocarcinoma. Proc Natl Acad Sci. 2016;113:12250–12255.
  • Isomoto H, Kobayashi S, Werneburg NW, et al. Interleukin 6 upregulates myeloid cell leukemia-1 expression through a STAT3 pathway in cholangiocarcinoma cells. Hepatology. 2005;42:1329–1338.
  • Sia D, Hoshida Y, Villanueva A, et al. Integrative molecular analysis of intrahepatic cholangiocarcinoma reveals 2 classes that have different outcomes. Gastroenterology. 2013;144:829–840.
  • R V G, Boulter L, Dwyer BJ, et al. Notch3 drives development and progression of cholangiocarcinoma. . Proc Natl Acad Sci. 2016;113:3–8.
  • Sirica AE, Zhang Z, Lai GH, et al. A novel “patient-like” model of cholangiocarcinoma progression based on bile duct inoculation of tumorigenic rat cholangiocyte cell lines. Hepatology. 2008;47(4):1178–1190.
  • Mancarella S, Serino G, Dituri F, et al. Crenigacestat, a selective NOTCH1 inhibitor, reduces intrahepatic cholangiocarcinoma progression by blocking VEGFA/DLL4/MMP13 axis. Cell Death Differ. 2020;27(8):2330–2343.
  • Kitagawa K, Moriya K, Kaji K, et al. Atorvastatin augments gemcitabine-mediated anti-cancer effects by inhibiting yes-associated protein in human cholangiocarcinoma cells. Int J Mol Sci. 2020;21:1–15.
  • Saqub H, Proetsch-Gugerbauer H, Bezrookove V, et al. Dinaciclib, a cyclin-dependent kinase inhibitor, suppresses cholangiocarcinoma growth by targeting CDK2/5/9. Sci Rep. 2020;10:1–13.
  • Dwyer BJ, Jarman EJ, Gogoi-Tiwari J, et al. TWEAK/Fn14 signalling promotes cholangiocarcinoma niche formation and progression. J Hepatol. 2020;S0168-S8278(20):33771–33775.
  • Yanagihara K, Kamada N, Tsumuraya M, et al. Establishment and Characterization of the Human Cholangiocarcinoma Cell Line HChol-Y1 in a Serum-Free, Chemically Defined Medium. J Natl Cancer Inst. 1985;75:29–35.
  • Lai GH, Zhang Z, Shen XN, et al. erbB-2/neu transformed rat cholangiocytes recapitulate key cellular and molecular features of human bile duct cancer. Gastroenterology. 2005;129:2047–2057.
  • Zabron A, Edwards RJ, Khan SA. The challenge of cholangiocarcinoma : dissecting the molecular mechanisms of an insidious cancer. Dis Model Mech. 2013;292:281–292.
  • Method of the Year. Organoids. Nat Methods. 2017;2018(15):1.
  • Modeling Development CH. Disease with Organoids. Cell. 2016;165:1586–1597.
  • Huch M, Knoblich JA, Lutolf MP, et al. The hope and the hype of organoid research. Dev. 2017;144:938–941.
  • Abdel Fattah AR, Ranga A. Nanoparticles as Versatile Tools for Mechanotransduction in Tissues and Organoids. Front Bioeng Biotechnol. 2020;8:1–12.
  • Simian M, Bissell MJ. Organoids: a historical perspective of thinking in three dimensions. J Cell Biol. 2017;216:31–40.
  • Kim J, Koo BK, Knoblich JA. Human organoids: model systems for human biology and medicine. Nat Rev Mol Cell Biol. 2020;21(10):571–584.
  • Huch M, Gehart H, Van Boxtel R, et al. Long-term culture of genome-stable bipotent stem cells from adult human liver. Cell. 2015;160:299–312.
  • Huch M, Dorrell C, Boj SF, et al. In vitro expansion of single Lgr5 + liver stem cells induced by Wnt-driven regeneration. Nature. 2013;494:247–250.
  • Wu F, Wu D, Ren Y, et al. Generation of hepatobiliary organoids from human induced pluripotent stem cells. J Hepatol. 2019;70:1145–1158.
  • Sampaziotis F, De BMC, Madrigal P, et al. Cholangiocytes derived from human induced pluripotent stem cells for disease modeling and drug validation. . Front Bioeng Biotechnol. 2016;33:845–852.
  • Prior N, Hindley CJ, Rost F, et al. Lgr5+ stem and progenitor cells reside at the apex of a heterogeneous embryonic hepatoblast pool. Dev. 2019;146.dev174557
  • Prior N, Inacio P, Huch M. Liver organoids: from basic research to therapeutic applications. Gut. 2019;68:2228–2237.
  • Sampaziotis F, Justin AW, Tysoe OC, et al. Reconstruction of the mouse extrahepatic biliary tree using primary human extrahepatic cholangiocyte organoids. Nat Med. 2017;23:954–963.
  • Ford MJ, Yeyati PL, Mali GR, et al. A Cell/Cilia Cycle Biosensor for Single-Cell Kinetics Reveals Persistence of Cilia after G1/S Transition Is a General Property in Cells and Mice. Dev Cell. 2018;47:509–523.e5.
  • Vyas D, Baptista PM, Brovold M, et al. Self-assembled liver organoids recapitulate hepatobiliary organogenesis in vitro. Hepatology. 2018;67:750–761.
  • Andersson ER, Chivukula IV, Hankeova S, et al. Mouse Model of Alagille Syndrome and Mechanisms of Jagged1 Missense Mutations. Gastroenterology. 2018;154:1080–1095.
  • Yang L, Han Y, Nilsson-Payant BE, et al. 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. 2020;27(1)125–136.
  • Zhao B, Ni C, Gao R, et al. Recapitulation of SARS-CoV-2 infection and cholangiocyte damage with human liver ductal organoids. Protein Cell. 2020;11(10):771–775.
  • Soroka CJ, Assis DN, Boyer JL. Patient-derived organoids from human bile: an in vitro method to study cholangiopathies. Methods Mol Biol. 2019;1981:363–372.
  • Broutier L, Mastrogiovanni G, Verstegen MMA, et al. Human primary liver cancer-derived organoid cultures for disease modeling and drug screening. Nat Med. 2017;23:1424–1435.
  • Saito Y, Muramatsu T, Kanai Y, et al. Establishment of Patient-Derived Organoids and Drug Screening for Biliary Tract Carcinoma. Cell Rep. 2019;27:1265–1276.e4.
  • Lampis A, Carotenuto P, Vlachogiannis G, et al. MIR21 Drives Resistance to Heat Shock Protein 90 Inhibition in Cholangiocarcinoma. Gastroenterology. 2018;154:1066–1079.
  • Yao Y, Xu X, Yang L, et al. Patient-Derived Organoids Predict Chemoradiation Responses of Locally Advanced Rectal Cancer. Cell Rep. 2020;e6:17–26.
  • Guo B, Li L, Guo J, et al. M2 tumor-associated macrophages produce interleukin-17 to suppress oxaliplatin-induced apoptosis in hepatocellular carcinoma. Oncotarget. 2017;8:44465–44476.
  • Dijkstra KK, Cattaneo CM, Weeber F, et al. Generation of Tumor-Reactive T Cells by Co-culture of Peripheral Blood Lymphocytes and Tumor Organoids. Cell. 2018;174:1586–1598.e12.
  • Neal JT, Li X, Zhu J, et al. Organoid Modeling of the Tumor Immune Microenvironment. Cell. 2018;175:1972–1988.e16.
  • Van De Wetering M, Francies HE, Francis JM, et al. Prospective derivation of a living organoid biobank of colorectal cancer patients. Cell. 2015;161:933–945.
  • Amato F, Rae C, Prete MG, et al. Cholangiocarcinoma Disease Modelling Through Patients Derived Organoids. Cells. 2020;9:832.
  • Qin X, Sufi J, Vlckova P, et al. Cell-type-specific signaling networks in heterocellular organoids. Nat Methods. 2020;7(3):335–342.
  • Giobbe GG, Crowley C, Luni C, et al. Extracellular matrix hydrogel derived from decellularized tissues enables endodermal organoid culture. Nat Commun. 2019;10(1):5658.
  • Mollica PA, Booth-Creech EN, Reid JA, et al. 3D bioprinted mammary organoids and tumoroids in human mammary derived ECM hydrogels. Acta Biomater. 2019;95:201–213.
  • Verna L, Whysner J, Williams GMN. Nitrosodiethylamine mechanistic data and risk assessment: bioactivation, DNA-adduct formation, mutagenicity, and tumor initiation. Pharmacol Ther. 1996;71:57–81.
  • Yang H, Li TWH, Peng J, et al. A mouse model of cholestasis-associated cholangiocarcinoma and transcription factors involved in progression. Gastroenterology. 2011;141:378–388.
  • Loeuillard E, Fischbach SR, Gores GJ, et al. Animal models of cholangiocarcinoma. Biochim Biophys Acta Mol Basis Dis. 2019;1865:982–992.
  • Mariotti V, Strazzabosco M, Fabris L, et al. Animal models of biliary injury and altered bile acid metabolism. Biochim Biophys Acta Mol Basis Dis. 2018;1864:1254–1261.
  • Aller MA, Arias JL, Prieto I, et al. Bile duct ligation: step-by-step to cholangiocyte inflammatory tumorigenesis. Eur J Gastroenterol Hepatol. 2010;22:651–661.
  • Von Tungeln LS, Walker NJ, Olson GR, et al. Low dose assessment of the carcinogenicity of furan in male F344/N Nctr rats in a 2-year gavage study. Food Chem Toxicol. 2017;99:170–181.
  • Elmore LW, Sirica AE. Phenotypic Characterization of Metaplastic Intestinal Glands and Ductular Hepatocytes in Cholangiofibrotic Lesions Rapidly Induced in the Caudate Liver Lobe of Rats Treated with Furan. Cancer Res. 1991;51:5752–5759.
  • Maronpot RR, Giles HD, Dykes DJ, et al. Furan-induced hepatic cholangiocarcinomas in Fischer 344 rats. Toxicol Pathol. 1991;19:561–570.
  • Cadamuro M, Brivio S, Stecca T, et al. Animal models of cholangiocarcinoma: what they teach us about the human disease. Clin Res Hepatol Gastroenterol. 2018;42:403–415.
  • Becker FF. Thioacetamide hepatocarcinogenesis. J Natl Cancer Inst. 1983.71(3):553-8.
  • Dasgupta A, Chatterjee R, Roy Chowdhury J. Thioacetamide-Induced Hepatocarcinoma in Rat. Oncology. 1981;38(4):249-53
  • Praet MM, Roels HJ. Histogenesis of cholangiomas and cholangiocarcinomas in thioacetamide fed rats. 1984;26(1):3-14.. Exp Pathol..
  • Hajovsky H, Hu G, Koen Y, et al. Metabolism and toxicity of thioacetamide and thioacetamide S-Oxide in rat hepatocytes. Chem Res Toxicol. 2012;25:1955–1963.
  • Yeh CN, Maitra A, Lee KF, et al. Thioaceatamide-induced intestinal-type cholangiocarcinoma in rat: an animal model recapitulating the multi-stage progression of human cholangiocarcinoma. Carcinogenesis. 2004;25:631–636.
  • Sander JD, Joung JKCRISPR. Cas systems for editing, regulating and targeting genomes. Nat Biotechnol. 2014;32(4):347–355.
  • Banales JM, Huebert RC, Karlsen T, et al. Cholangiocyte pathobiology. Nat Rev Gastroenterol Hepatol. 2019 16(5):269–281
  • Schaub JR, Huppert KA, Kurial SNT, et al. De novo formation of the biliary system by TGFβ-mediated hepatocyte transdifferentiation. Nature. 2018;557(7704):247–251.
  • Raven A, Lu WY, Man TY, et al. Cholangiocytes act as facultative liver stem cells during impaired hepatocyte regeneration. Nature. 2017;547(7663):350–354.
  • Chen X, Calvisi DF. Hydrodynamic Transfection for Generation of Novel Mouse Models for Liver Cancer Research. Am J Pathol. 2014;184:912–923.
  • Jackson EL, Willis N, Mercer K, et al. Analysis of lung tumor initiation and progression using conditional expression of oncogenic K-ras. Genes Dev. 2001;15(24):3243–3248.
  • Falix FA, Weeda VB, Labruyere WT, et al. Hepatic Notch2 deficiency leads to bile duct agenesis perinatally and secondary bile duct formation after weaning. Dev Biol. 2014;396(2):201–213.
  • El Khatib M, Bozko P, Palagani V, et al. Activation of Notch signaling is required for cholangiocarcinoma progression and is enhanced by inactivation of p53 in vivo. PLoS One. 2013;8(10):e77433.
  • Benhamouche S, Curto M, Saotome I, et al. Nf2/Merlin controls progenitor homeostasis and tumorigenesis in the liver. Genes Dev. 2010;24:1718–1730.
  • Newsome JR, Venkatramani R, Heczey A, et al. Cholangiocarcinoma among children and adolescents: a review of the literature and surveillance, epidemiology, and end results program database analysis. J Pediatr Gastroenterol Nutr. 2018;66(1):e12–e18.
  • Means AL, Xu Y, Zhao A, et al. A CK19CreERT knockin mouse line allows for conditional DNA recombination in epithelial cells in multiple endodermal organs. Genesis. 2008;46:318–323.
  • Kopp JL, Dubois CL, Schaffer AE, et al. Sox9+ ductal cells are multipotent progenitors throughout development but do not produce new endocrine cells in the normal or injured adult pancreas. Development. 2011;138(4):653–665.
  • Jörs S, Jeliazkova P, Ringelhan M, et al. Lineage fate of ductular reactions in liver injury and carcinogenesis. J Clin Invest. 2015;125(6):2445–2457.
  • Xu X, Kobayashi S, Qiao W, et al. Induction of intrahepatic cholangiocellular carcinoma by liver-specific disruption of Smad4 and Pten in mice. J Clin Invest. 2006;116(7):1843–1852.
  • Hill MA, Alexander WB, Guo B, et al.Kras and Tp53 Mutations Cause Cholangiocyte- and Hepatocyte-Derived Cholangiocarcinoma. 2018;4445–4452.
  • Guest RV, Boulter L, Kendall TJ, et al. Cell lineage tracing reveals a biliary origin of intrahepatic cholangiocarcinoma. Cancer Res. 2014;74(4):1005–1010.
  • Lannagan TR, Jackstadt R, Leedham SJ, et al. Advances in colon cancer research: in vitro and animal models. Curr Opin Genet Dev. 2021;66:50–56.
  • Suda T, Liu D. Hydrodynamic gene delivery: its principles and applications. Mol Ther. 2007;15:2063–2069.
  • Liu F, Song YK, Liu D. Hydrodynamics-based transfection in animals by systemic administration of plasmid DNA. Gene Ther. 1999;6:1258–1266.
  • Zhang G, Budker V, Wolff JA. High levels of foreign gene expression in hepatocytes after tail vein injections of naked plasmid DNA. Hum Gene Ther. 1999;10:1735–1737.
  • Zhang G, Gao X, Song YK, et al. Hydroporation as the mechanism of hydrodynamic delivery. Gene Ther. 2004;11(8) 675–682.
  • Fan B, Chen X, Willenbring H, et al. Cholangiocarcinomas can originate from hepatocytes in mice. J. Clin. Invest. 2012;122:2911–2915.
  • Evert M, Dombrowski F, Ribback S, et al. On the Role of Notch1 and Adult Hepatocytes in Murine Intrahepatic Cholangiocarcinoma Development. Hepatology. 2013;58:1857–1859.
  • Wang J, Dong M, Xu Z, et al. Notch2 controls hepatocyte-derived cholangiocarcinoma formation in mice. Oncogene. 2018; 37(24) 3229–3242.
  • Weber J, Öllinger R, Friedrich M, et al. CRISPR/Cas9 somatic multiplex-mutagenesis for high-Throughput functional cancer genomics in mice. Proc Natl Acad Sci U S A. 2015;112(45):13982–13987.
  • Gürlevik E, Fleischmann-Mundt B, Armbrecht N, et al. Adjuvant gemcitabine therapy improves survival in a locally induced, R0-resectable model of metastatic intrahepatic cholangiocarcinoma. Hepatology. 2013;58:1031–1041.
  • Mohr R, Özdirik B, Knorr J, et al. In vivo models for cholangiocarcinoma—What can we learn for human disease? Int J Mol Sci. 2020;21:1–15.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.