Organoids from adult liver and pancreas: Stem cell biology and biomedical utility

Developmental Biology

Volumn 420, Issue 2, 2016, Pages 251-261

  Hindley, Christopher J ^a,b   Cordero Espinoza, Lucía ^a,c   Huch, Meritxell ^a,c  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

3D cultures; Liver; Niche signals; Organoid; Pancreas; Stem cell

Indexed keywords

ADULT; BIOMEDICINE; CELL CULTURE TECHNIQUE; CELL DIFFERENTIATION; CELL FUNCTION; CELL MATURATION; CELL POPULATION; CELL PROLIFERATION; CELL THERAPY; CYTOLOGY; DEVELOPMENTAL BIOLOGY; DISEASE MODEL; EMBRYO DEVELOPMENT; EMBRYONAL TISSUE; GENE THERAPY; HUMAN; IN VITRO STUDY; LIVER CELL; LIVER DEVELOPMENT; LIVER FUNCTION; MORPHOGENESIS; NONHUMAN; PANCREAS CELL; PANCREAS FUNCTION; PHYSIOLOGICAL PROCESS; PRIORITY JOURNAL; REGENERATIVE MEDICINE; REVIEW; SIGNAL TRANSDUCTION; STEM CELL; STROMA CELL; TISSUE CULTURE; ANIMAL; BIOLOGICAL MODEL; BIOLOGICAL THERAPY; EMBRYOLOGY; GROWTH, DEVELOPMENT AND AGING; LIVER; LIVER REGENERATION; ORGAN CULTURE TECHNIQUE; ORGANOGENESIS; ORGANOID; PANCREAS; PROCEDURES;

ANIMALS; CELL- AND TISSUE-BASED THERAPY; GENETIC THERAPY; HUMANS; LIVER; LIVER REGENERATION; MODELS, BIOLOGICAL; ORGAN CULTURE TECHNIQUES; ORGANOGENESIS; ORGANOIDS; PANCREAS; SIGNAL TRANSDUCTION; STEM CELLS;

EID: 84996772853     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2016.06.039     Document Type: Review

References (119)

1. Akhurst, B., et al. A modified choline-deficient, ethionine-supplemented diet protocol effectively induces oval cells in mouse liver. Hepatology 34:3 (2001), 519–522.
2. Al-Hasani, K., et al. Adult duct-lining cells can reprogram into β-like cells able to counter repeated cycles of toxin-induced diabetes. Dev. Cell 26:1 (2013), 86–100.
3. Aloia, L., McKie, M.A., Huch, M., Cellular plasticity in the adult liver and stomach. J. Physiol, 2016, 10.1113/JP271769 and PMID: 27028579.
4. Apelqvist, A., et al. Notch signalling controls pancreatic cell differentiation. Nature 400:6747 (1999), 877–881.
5. Asrani, S.K., et al. Underestimation of liver-related mortality in the United States. Gastroenterology, 145(2), 2013 p. 375-82.e1-2.
6. Assy, N., et al. Randomized controlled trial of total immunosuppression withdrawal in liver transplant recipients: role of ursodeoxycholic acid. Transplantation 83:12 (2007), 1571–1576.
7. Barker, N., et al. Lgr5(+ve) stem cells drive self-renewal in the stomach and build long-lived gastric units in vitro. Cell Stem Cell 6:1 (2010), 25–36.
8. Beer, R.L., Parsons, M.J., Rovira, M., Centroacinar cells: at the center of pancreas regeneration. Dev. Biol. 413:1 (2016), 8–15.
9. Bhushan, A., et al. Fgf10 is essential for maintaining the proliferative capacity of epithelial progenitor cells during early pancreatic organogenesis. Development 128:24 (2001), 5109–5117.
10. Blanpain, C., Fuchs, E., Stem cell plasticity. Plasticity of epithelial stem cells in tissue regeneration. Science, 344(6189), 2014, 1242281.
11. Boj, S.F., et al. Organoid models of human and mouse ductal pancreatic cancer. Cell 160:1–2 (2015), 324–338.
12. Boulter, L., et al. Macrophage-derived Wnt opposes Notch signaling to specify hepatic progenitor cell fate in chronic liver disease. Nat. Med. 18:4 (2012), 572–579.
13. Byass, P., The global burden of liver disease: a challenge for methods and for public health. BMC Med., 12, 2014, 159.
14. Campbell, J.S., et al. Platelet-derived growth factor C induces liver fibrosis, steatosis, and hepatocellular carcinoma. Proc. Natl. Acad. Sci. USA 102:9 (2005), 3389–3394.
15. Chen, J.M., The cultivation in fluid medium of organised liver, pancreas and other tissues of foetal rats. Exp. Cell Res. 7:2 (1954), 518–529.
16. Chen, L., et al. HSCs play a distinct role in different phases of oval cell-mediated liver regeneration. Cell Biochem. Funct. 30:7 (2012), 588–596.
17. Cheng, L., et al. Low incidence of DNA sequence variation in human induced pluripotent stem cells generated by nonintegrating plasmid expression. Cell Stem Cell 10:3 (2012), 337–344.
18. Collombat, P., et al. The ectopic expression of Pax4 in the mouse pancreas converts progenitor cells into alpha and subsequently beta cells. Cell 138:3 (2009), 449–462.
19. de Lau, W., et al. The R-spondin/Lgr5/Rnf43 module: regulator of Wnt signal strength. Genes Dev. 28:4 (2014), 305–316.
20. Deutsch, G., et al. A bipotential precursor population for pancreas and liver within the embryonic endoderm. Development 128:6 (2001), 871–881.
21. Dholakia, S., et al. Advances in pancreas transplantation. J. R. Soc. Med. 109:4 (2016), 141–146.
22. Ding, B.S., et al. Inductive angiocrine signals from sinusoidal endothelium are required for liver regeneration. Nature 468:7321 (2010), 310–315.
23. Dor, Y., et al. Adult pancreatic beta-cells are formed by self-duplication rather than stem-cell differentiation. Nature 429:6987 (2004), 41–46.
24. Dorrell, C., et al. Prospective isolation of a bipotential clonogenic liver progenitor cell in adult mice. Genes Dev. 25:11 (2011), 1193–1203.
25. Dorrell, C., et al. The organoid-initiating cells in mouse pancreas and liver are phenotypically and functionally similar. Stem Cell Res. 13:2 (2014), 275–283.
26. Duncan, A.W., Dorrell, C., Grompe, M., Stem cells and liver regeneration. Gastroenterology 137:2 (2009), 466–481.
27. Elsässer, H.P., Adler, G., Kern, H.F., Time course and cellular source of pancreatic regeneration following acute pancreatitis in the rat. Pancreas 1:5 (1986), 421–429.
28. Farber, E., Similarities in the sequence of early histological changes induced in the liver of the rat by ethionine, 2-acetylamino-fluorene, and 3′-methyl-4-dimethylaminoazobenzene. Cancer Res. 16:2 (1956), 142–148.
29. Fausto, N., Campbell, J.S., The Role of Hepatocytes and Oval Cells In Liver Regeneration and Repopulation. Mech Dev. 120:1 (2003), 117–130.
30. Feng, D., Interleukin-22 promotes proliferation of liver stem/progenitor cells in mice and patients with chronic hepatitis B virus infection. Gastroenterology 143:1 (2012), 188–198.
31. Font-Burgada, J., et al. Hybrid periportal hepatocytes regenerate the injured liver without giving rise to cancer. Cell 162:4 (2015), 766–779.
32. Fraczek, J., et al. Primary hepatocyte cultures for pharmaco-toxicological studies: at the busy crossroad of various anti-dedifferentiation strategies. Arch. Toxicol. 87:4 (2013), 577–610.
33. Furuyama, K., et al. Continuous cell supply from a Sox9-expressing progenitor zone in adult liver, exocrine pancreas and intestine. Nat. Genet. 43:1 (2011), 34–41.
34. Ghaneh, P., Costello, E., Neoptolemos, J.P., Biology and management of pancreatic cancer. Postgrad. Med. J. 84:995 (2008), 478–497.
35. Gianani, R., et al. Dimorphic histopathology of long-standing childhood-onset diabetes. Diabetologia 53:4 (2010), 690–698.
36. Gittes, G.K., et al. Lineage-specific morphogenesis in the developing pancreas: role of mesenchymal factors. Development 122:2 (1996), 439–447.
37. Gouzi, M., et al. Neurogenin3 initiates stepwise delamination of differentiating endocrine cells during pancreas development. Dev. Dyn. 240:3 (2011), 589–604.
38. Gradwohl, G., et al. neurogenin3 is required for the development of the four endocrine cell lineages of the pancreas. Proc. Natl. Acad. Sci. USA 97:4 (2000), 1607–1611.
39. Greggio, C., et al. Artificial three-dimensional niches deconstruct pancreas development in vitro. Development 140:21 (2013), 4452–4462.
40. Gu, G., Dubauskaite, J., Melton, D.A., Direct evidence for the pancreatic lineage: NGN3+ cells are islet progenitors and are distinct from duct progenitors. Development 129:10 (2002), 2447–2457.
41. Gualdi, R., et al. Hepatic specification of the gut endoderm in vitro: cell signaling and transcriptional control. Genes Dev. 10:13 (1996), 1670–1682.
42. Hindley, C.J., Mastrogiovanni, G., Huch, M., The plastic liver: differentiated cells, stem cells, every cell?. J. Clin. Investig. 124:12 (2014), 5099–5102.
43. Hoppo, T., et al. Thy1-positive mesenchymal cells promote the maturation of CD49f-positive hepatic progenitor cells in the mouse fetal liver. Hepatology 39:5 (2004), 1362–1370.
44. Huang, L., et al. Ductal pancreatic cancer modeling and drug screening using human pluripotent stem cell- and patient-derived tumor organoids. Nat. Med. 21:11 (2015), 1364–1371.
45. Huch, M., et al. In vitro expansion of single Lgr5+ liver stem cells induced by Wnt-driven regeneration. Nature 494:7436 (2013), 247–250.
46. Huch, M., et al. Unlimited in vitro expansion of adult bi-potent pancreas progenitors through the Lgr5/R-spondin axis. EMBO J. 32:20 (2013), 2708–2721.
47. Huch, M., et al. Long-term culture of genome-stable bipotent stem cells from adult human liver. Cell 160:1–2 (2015), 299–312.
48. Huch, M., Regenerative biology: the versatile and plastic liver. Nature 517:7533 (2015), 155–156.
49. Huch, M., Koo, B.-K., Modeling mouse and human development using organoid cultures. Development 142:18 (2015), 3113–3125.
50. Huch, M., Dollé, L., The plastic cellular states of liver cells: are EpCAM and Lgr5 fit for purpose?. Hepatology, 2016 10.1002/hep.28469.
51. Inada, A., et al. Carbonic anhydrase II-positive pancreatic cells are progenitors for both endocrine and exocrine pancreas after birth. Proc. Natl. Acad. Sci. USA 105:50 (2008), 19915–19919.
52. Jennings, R.E., et al. Development of the human pancreas from foregut to endocrine commitment. Diabetes 62:10 (2013), 3514–3522.
53. Jensen, J., et al. Control of endodermal endocrine development by Hes-1. Nat. Genet. 24:1 (2000), 36–44.
54. Jin, L., et al. Colony-forming cells in the adult mouse pancreas are expandable in Matrigel and form endocrine/acinar colonies in laminin hydrogel. Proc. Natl. Acad. Sci. USA 110:10 (2013), 3907–3912.
55. Jin, L., et al. In vitro multilineage differentiation and self-renewal of single pancreatic colony-forming cells from adult C57BL/6 mice. Stem Cells Dev. 23:8 (2014), 899–909.
56. Jung, J., et al. Initiation of mammalian liver development from endoderm by fibroblast growth factors. Science 284:5422 (1999), 1998–2003.
57. Kamiya, a, et al. Fetal liver development requires a paracrine action of oncostatin M through the gp130 signal transducer. EMBO J. 18:8 (1999), 2127–2136.
58. Koo, B.K., Clevers, H., Stem cells marked by the R-spondin receptor LGR5. Gastroenterology 147:2 (2014), 289–302.
59. Kopinke, D., et al. Lineage tracing reveals the dynamic contribution of Hes1+ cells to the developing and adult pancreas. Development 138:3 (2011), 431–441.
60. Kopp, J.L., Grompe, M., Sander, M., Stem cells versus plasticity in liver and pancreas regeneration. Nat. Cell Biol. 18:3 (2016), 238–245.
61. Kudira, R., et al. P2X1 regulated IL-22 secretion by innate lymphoid cells is required for efficient liver regeneration. Hepatology 63:6 (2016), 2004–2017.
62. Kuijk, E.W., et al. Generation and characterization of rat liver stem cell lines and their engraftment in a rat model of liver failure. Sci. Rep., 6, 2016 p. 22154-22154.
63. Lajtha, L.G., Stem cell concepts. Differentiation 14:1–2 (1979), 23–34.
64. Laursen, L., A preventable cancer. Nature 516:7529 (2014), S2–S3.
65. Lee, J., et al. Expansion and conversion of human pancreatic ductal cells into insulin-secreting endocrine cells. Elife, 2013, 2 (p. e00940).
66. Lee, W.M., Acute liver failure. N. Engl. J. Med. 329:25 (1993), 1862–1872.
67. Lindemans, C.A., et al. Interleukin-22 promotes intestinal-stem-cell-mediated epithelial regeneration. Nature 528:7583 (2015), 560–564.
68. Lucas, A.L., et al. Global Trends in Pancreatic Cancer Mortality From 1980 Through 2013 and Predictions for 2017. Clin. Gastroenterol. Hepatol., S1542-3565(16), 2016 30269–5.
69. Ma, D.F., et al. Polyclonal origin of hormone-producing cell populations evaluated as a direct in situ demonstration in EGFP/BALB/C chimeric mice. J. Endocrinol. 207:1 (2010), 17–25.
70. Malato, Y., et al. Fate tracing of mature hepatocytes in mouse liver homeostasis and regeneration. J. Clin. Investig. 121:12 (2011), 4850–4860.
71. Matano, M., et al. Modeling colorectal cancer using CRISPR-Cas9-mediated engineering of human intestinal organoids. Nat. Med. 21:3 (2015), 256–262.
72. Matsui, T., et al. K-Ras mediates cytokine-induced formation of E-cadherin-based adherens junctions during liver development. EMBO J. 21:5 (2002), 1021–1030.
73. Matsumoto, K., et al. Liver organogenesis promoted by endothelial cells prior to vascular function. Science 294:5542 (2001), 559–563.
74. McCracken, K.W., et al. Generating human intestinal tissue from pluripotent stem cells in vitro. Nat. Protoc. 6:12 (2011), 1920–1928.
75. McCracken, K.W., et al. Modelling human development and disease in pluripotent stem-cell-derived gastric organoids. Nature 516:7531 (2014), 400–404.
76. Mesa, Kailin R., Rompolas, P., Greco, V., The dynamic duo: niche/stem cell interdependency. Stem Cell Rep. 4:6 (2015), 961–966.
77. Michalopoulos, G.K., DeFrances, M.C., Liver regeneration. Science 276:5309 (1997), 60–66.
78. Miyajima, A., Tanaka, M., Itoh, T., Stem/progenitor cells in liver development, homeostasis, regeneration, and reprogramming. Cell Stem Cell 14:5 (2014), 561–574.
79. Miyao, M., et al. Pivotal role of liver sinusoidal endothelial cells in NAFLD/NASH progression. Lab. Invest. 95:10 (2015), 1130–1144.
80. Nantasanti, S., et al. Disease modeling and gene therapy of copper storage disease in canine hepatic organoids. Stem Cell Rep. 5:5 (2015), 895–907.
81. Nibourg, G.A., et al. Proliferative human cell sources applied as biocomponent in bioartificial livers: a review. Expert Opin. Biol. Ther. 12:7 (2012), 905–921.
82. Onitsuka, I., Tanaka, M., Miyajima, A., Characterization and functional analyses of hepatic mesothelial cells in mouse liver development. Gastroenterology 138:4 (2010), 1525–1535 1535e1-6.
83. Oshima, Y., et al. Isolation of mouse pancreatic ductal progenitor cells expressing CD133 and c-Met by flow cytometric cell sorting. Gastroenterology 132:2 (2007), 720–732.
84. Paku, S., et al. Origin and structural evolution of the early proliferating oval cells in rat liver. Am. J. Pathol. 158:4 (2001), 1313–1323.
85. Petersen, B.E., Zajac, V.F., Michalopoulos, G.K., Bile ductular damage induced by methylene dianiline inhibits oval cell activation. Am. J. Pathol. 151:4 (1997), 905–909.
86. Preisegger, K.H., et al. Atypical ductular proliferation and its inhibition by transforming growth factor beta1 in the 3,5-diethoxycarbonyl-1,4-dihydrocollidine mouse model for chronic alcoholic liver disease. Lab. Investig. 79:2 (1999), 103–109.
87. Pritchard, M.T., Nagy, L.E., Hepatic fibrosis is enhanced and accompanied by robust oval cell activation after chronic carbon tetrachloride administration to Egr-1-deficient mice. Am. J. Pathol. 176:6 (2010), 2743–2752.
88. Ritsma, L., et al. Intestinal crypt homeostasis revealed at single-stem-cell level by in vivo live imaging. Nature 507:7492 (2014), 362–365.
89. Rocha, Ana S., et al. The angiocrine factor Rspondin3 is a key determinant of liver zonation. Cell Rep. 13:9 (2015), 1757–1764.
90. Rodríguez-Seguel, E., et al. Mutually exclusive signaling signatures define the hepatic and pancreatic progenitor cell lineage divergence. Genes Dev. 27:17 (2013), 1932–1946.
91. Rossi, J.M., et al. Distinct mesodermal signals, including BMPs from the septum transversum mesenchyme, are required in combination for hepatogenesis from the endoderm. Genes Dev. 15:15 (2001), 1998–2009.
92. Sampaziotis, F., et al. Cholangiocytes derived from human induced pluripotent stem cells for disease modeling and drug validation. Nat. Biotechnol. 33:8 (2015), 845–852.
93. Sancho, R., et al. Loss of Fbw7 reprograms adult pancreatic ductal cells into α, δ, and β cells. Cell Stem Cell 15:2 (2014), 139–153.
94. Sangiorgi, E., Capecchi, M.R., Bmi1 lineage tracing identifies a self-renewing pancreatic acinar cell subpopulation capable of maintaining pancreatic organ homeostasis. Proc. Natl. Acad. Sci. USA 106:17 (2009), 7101–7106.
95. Sato, T., et al. Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 459:7244 (2009), 262–265.
96. Schaub, J.R., et al. Evidence against a stem cell origin of new hepatocytes in a common mouse model of chronic liver injury. Cell Rep. 8:4 (2014), 933–939.
97. Schöls, L., Mecke, D., Gebhardt, R., Reestablishment of the heterogeneous distribution of hepatic glutamine synthetase during regeneration after CCl4-intoxication. Histochemistry 94:1 (1990), 49–54.
98. Schwank, G., et al. Functional repair of CFTR by CRISPR/Cas9 in intestinal stem cell organoids of cystic fibrosis patients. Cell Stem Cell 13:6 (2013), 653–658.
99. Serls, A.E., et al. Different thresholds of fibroblast growth factors pattern the ventral foregut into liver and lung. Development 132:1 (2005), 35–47.
100. Shin, S., et al. Foxl1-Cre-marked adult hepatic progenitors have clonogenic and bilineage differentiation potential. Genes Dev. 25:11 (2011), 1185–1192.
101. Snykers, S., et al. In vitro differentiation of embryonic and adult stem cells into hepatocytes: state of the art. Stem Cells 27:3 (2009), 577–605.
102. Takase, H.M., et al. FGF7 is a functional niche signal required for stimulation of adult liver progenitor cells that support liver regeneration. Genes Dev. 27:2 (2013), 169–181.
103. Takebe, T., et al. Vascularized and functional human liver from an iPSC-derived organ bud transplant. Nature 499:7459 (2013), 481–484.
104. Takebe, T., et al. Vascularized and complex organ buds from diverse tissues via mesenchymal cell-driven condensation. Cell Stem Cell 16:5 (2015), 556–565.
105. Teta, M., et al. Very slow turnover of beta-cells in aged adult mice. Diabetes 54:9 (2005), 2557–2567.
106. Teta, M., et al. Growth and regeneration of adult beta cells does not involve specialized progenitors. Dev. Cell 12:5 (2007), 817–826.
107. Van de Casteele, M., et al. Partial duct ligation: β-cell proliferation and beyond. Diabetes 63:8 (2014), 2567–2577.
108. van de Wetering, M., et al. Prospective derivation of a living organoid biobank of colorectal cancer patients. Cell 161:4 (2015), 933–945.
109. Wang, B., et al. Self-renewing diploid Axin2(+) cells fuel homeostatic renewal of the liver. Nature 524:7564 (2015), 180–185.
110. Watson, C.L., et al. An in vivo model of human small intestine using pluripotent stem cells. Nat. Med. 20:11 (2014), 1310–1314.
111. Weaver, C.V., Sorenson, R.L., Kaung, H.C., Immunocytochemical localization of insulin-immunoreactive cells in the pancreatic ducts of rats treated with trypsin inhibitor. Diabetologia 28:10 (1985), 781–785.
112. Westphalen, C.B., et al. Dclk1 defines quiescent pancreatic progenitors that promote injury-induced regeneration and tumorigenesis. Cell Stem Cell 18:4 (2016), 441–455.
113. Xu, X., et al. Beta cells can be generated from endogenous progenitors in injured adult mouse pancreas. Cell 132:2 (2008), 197–207.
114. Yanger, K., et al. Adult hepatocytes are generated by self-duplication rather than stem cell differentiation. Cell Stem Cell 15:3 (2014), 340–349.
115. Yimlamai, D., et al. Hippo pathway activity influences liver cell fate. Cell 157:6 (2014), 1324–1338.
116. Zaret, K.S., Grompe, M., Generation and regeneration of cells of the liver and pancreas. Science 322:5907 (2008), 1490–1494.
117. Zhou, Q., et al. A multipotent progenitor domain guides pancreatic organogenesis. Dev. Cell 13:1 (2007), 103–114.
118. Zhou, Q., et al. In vivo reprogramming of adult pancreatic exocrine cells to beta-cells. Nature 455:7213 (2008), 627–632.
119. Zorn, A.M., Wells, J.M., Vertebrate endoderm development and organ formation. Annu. Rev. Cell Dev. Biol. 25 (2009), 221–251.