Differentiation of progenitors in the liver: A matter of local choice

Journal of Clinical Investigation

Volumn 123, Issue 5, 2013, Pages 1867-1873

  Boulter, Luke ^a   Lu, Wei Yu ^a   Forbes, Stuart J ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

NOTCH RECEPTOR; WNT PROTEIN;

APOPTOSIS; CELL DIFFERENTIATION; CELL EXPANSION; CELL LINEAGE; HUMAN; IN VITRO STUDY; LIVER CANCER; LIVER CELL; LIVER DEVELOPMENT; LIVER REGENERATION; MOLECULAR MECHANICS; NONHUMAN; ONTOGENY; PHAGOCYTOSIS; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; CELL CYCLE; CELL DIFFERENTIATION; CELL LINEAGE; HEPATECTOMY; HUMANS; INFLAMMATION; LIGANDS; LIVER; LIVER NEOPLASMS; LIVER TRANSPLANTATION; LIVING DONORS; MICE; MITOSIS; NEOPLASMS; RATS; SIGNAL TRANSDUCTION; STEM CELLS;

EID: 84877135282     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI66026     Document Type: Review

References (83)

1. Barker N, et al. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature. 2007;449(7165):1003-1007.
2. Watt FM, Jensen KB. Epidermal stem cell diversity and quiescence. EMBO Mol Med. 2009;1(5):260-267.
3. Jensen KB, et al. Lrig1 expression defines a distinct multipotent stem cell population in mammalian epidermis. Cell Stem Cell. 2009;4(5):427-439.
4. Rawlins EL, et al. The role of Scgb1a1+ Clara cells in the long-term maintenance and repair of lung airway, but not alveolar, epithelium. Cell Stem Cell. 2009;4(6):525-534.
5. Marshall A, et al. Relation between hepatocyte G1 arrest, impaired hepatic regeneration, and fibrosis in chronic hepatitis C virus infection. Gastroenterology. 2005;128(1):33-42.
6. Yang S, et al. Oval cells compensate for damage and replicative senescence of mature hepatocytes in mice with fatty liver disease. Hepatology. 2004;39(2):403-411.
7. Espanol-Suner R, et al. Liver progenitor cells yield functional hepatocytes in response to chronic liver injury in mice. Gastroenterology. 2012; 143(6):1564-1575.
8. Fellous TG, et al. Locating the stem cell niche and tracing hepatocyte lineages in human liver. Hepatology. 2009;49(5):1655-1663.
9. Schotanus BA, van den Ingh TS, Penning LC, Rothuizen J, Roskams TA, Spee B. Cross-species immunohistochemical investigation of the activation of the liver progenitor cell niche in different types of liver disease. Liver Int. 2009;29(8):1241-1252.
10. Watt FM, Lo CC, Silva-Vargas V. Epidermal stem cells: an update. Curr Opin Genet Dev. 2006;16(5):518-524.
11. Watt FM. Epidermal stem cells: markers, patterning and the control of stem cell fate. Philos Trans R Soc Lond B Biol Sci. 1998;353(1370):831-837.
12. Sell S. The hepatocyte: heterogeneity and plasticity of liver cells. Int J Biochem Cell Biol. 2003;35(3):267-271.
13. Sell S. Comparison of liver progenitor cells in human atypical ductular reactions with those seen in experimental models of liver injury. Hepatology. 1998;27(2):317-331.
14. Cardinale V, et al. Multipotent stem/progenitor cells in human biliary tree give rise to hepatocytes, cholangiocytes, and pancreatic islets. Hepatology. 2011;54(6):2159-2172.
15. Carpino G, et al. Biliary tree stem/progenitor cells in glands of extrahepatic and intraheptic bile ducts: an anatomical in situ study yielding evidence of maturational lineages. J Anat. 2012;220(2):186-199.
16. Tirnitz-Parker JE, et al. Tumor necrosis factor-like weak inducer of apoptosis is a mitogen for liver progenitor cells. Hepatology. 2010;52(1):291-302.
17. Jakubowski A, et al. TWEAK induces liver progenitor cell proliferation. J Clin Invest. 2005;115(9):2330-2340.
18. Bird TG, Lorenzini S, Forbes SJ. Activation of stem cells in hepatic diseases. Cell Tissue Res. 2008;331(1):283-300.
19. Nguyen LN, et al. Transforming growth factor-beta differentially regulates oval cell and hepatocyte proliferation. Hepatology. 2007;45(1):31-41.
20. Wang X, Foster M, Al-Dhalimy M, Lagasse E, Finegold M, Grompe M. The origin and liver repopulating capacity of murine oval cells. Proc Natl Acad Sci U S A. 2003;100(suppl 1):11881-11888.
21. Dorrell C, et al. Surface markers for the murine oval cell response. Hepatology. 2008;48(4):1282-1291.
22. Dorrell C, et al. Prospective isolation of a bipotential clonogenic liver progenitor cell in adult mice. Genes Dev. 2011;25(11):1193-1203.
23. Okabe M, et al. Potential hepatic stem cells reside in EpCAM+ cells of normal and injured mouse liver. Development. 2009;136(11):1951-1960.
24. Kretzschmar K, Watt FM. Lineage tracing. Cell. 2012;148(1-2):33-45.
25. Sackett SD, et al. Foxl1 is a marker of bipotential hepatic progenitor cells in mice. Hepatology. 2009;49(3):920-929.
26. Harada N, et al. Intestinal polyposis in mice with a dominant stable mutation of the beta-catenin gene. EMBO J. 1999;18(21):5931-5942.
27. Kellendonk C, Opherk C, Anlag K, Schutz G, Tronche F. Hepatocyte-specific expression of Cre recombinase. Genesis. 2000;26(2):151-153.
28. Dor Y, Brown J, Martinez OI, Melton DA. Adult pancreatic beta-cells are formed by self-duplication rather than stem-cell differentiation. Nature. 2004;429(6987):41-46.
29. Furuyama K, et al. Continuous cell supply from a Sox9-expressing progenitor zone in adult liver, exocrine pancreas and intestine. Nat Genet. 2011;43(1):34-41.
30. Carpentier R, et al. Embryonic ductal plate cells give rise to cholangiocytes, periportal hepatocytes, and adult liver progenitor cells. Gastroenterology. 2011;141(4):1432-1438.
31. Arber N, Zajicek G, Ariel I. The streaming liver. II. Hepatocyte life history. Liver. 1988;8(2):80-87.
32. Zajicek G, Oren R, Weinreb M. The streaming liver. Liver. 1985;5(6):293-300.
33. Boulter L, et al. Macrophage-derived Wnt opposes Notch signaling to specify hepatic progenitor cell fate in chronic liver disease. Nat Med. 2012;18(4):572-579.
34. Yang L, et al. Fate-mapping evidence that hepatic stellate cells are epithelial progenitors in adult mouse livers. Stem Cells. 2008;26(8):2104-2113.
35. Kordes C, Sawitza I, Haussinger D. Hepatic and pancreatic stellate cells in focus. Biol Chem. 2009;390(10):1003-1012.
36. Kordes C, et al. CD133+ hepatic stellate cells are progenitor cells. Biochem Biophys Res Commun. 2007;352(2):410-417.
37. Chaffer CL, et al. Normal and neoplastic nonstem cells can spontaneously convert to a stem-like state. Proc Natl Acad Sci U S A. 2011;108(19):7950-7955.
38. Zhu NL, Wang J, Tsukamoto H. The Necdin-Wnt pathway causes epigenetic peroxisome proliferator-activated receptor gamma repression in hepatic stellate cells. J Biol Chem. 2010;285(40):30463-30471.
39. Jiang F, Parsons CJ, Stefanovic B. Gene expression profile of quiescent and activated rat hepatic stellate cells implicates Wnt signaling pathway in activation. J Hepatol. 2006;45(3):401-409.
40. Xiong WJ, et al. Wnt5a participates in hepatic stellate cell activation observed by gene expression profile and functional assays. World J Gastroenterol. 2012;18(15):1745-1752.
41. Chen Y, et al. Hedgehog controls hepatic stellate cell fate by regulating metabolism. Gastroenterology. 2012;143(5):1319-1329.
42. Handeli S, Simon JA. A small-molecule inhibitor of Tcf/beta-catenin signaling down-regulates PPARgamma and PPARdelta activities. Mol Cancer Ther. 2008;7(3):521-529.
43. Tsukamoto H, Zhu NL, Asahina K, Mann DA, Mann J. Epigenetic cell fate regulation of hepatic stellate cells. Hepatol Res. 2011;41(7):675-682.
44. Zeybel M, et al. Multigenerational epigenetic adaptation of the hepatic wound-healing response. Nat Med. 2012;18(9):1369-1377.
45. Fellous TG, et al. A methodological approach to tracing cell lineage in human epithelial tissues. Stem Cells. 2009;27(6):1410-1420.
46. Zaret KS, Grompe M. Generation and regeneration of cells of the liver and pancreas. Science. 2008;322(5907):1490-1494.
47. Antoniou A, et al. Intrahepatic bile ducts develop according to a new mode of tubulogenesis regulated by the transcription factor SOX9. Gastroenterology. 2009;136(7):2325-2333.
48. Beaudry JB, et al. Threshold levels of hepatocyte nuclear factor 6 (HNF-6) acting in synergy with HNF-4 and PGC-1alpha are required for time-specific gene expression during liver development. Mol Cell Biol. 2006;26(16):6037-6046.
49. Laudadio I, et al. A feedback loop between the liver-enriched transcription factor network and miR-122 controls hepatocyte differentiation. Gastroenterology. 2012;142(1):119-129.
50. Bray SJ. Notch signalling: a simple pathway becomes complex. Nat Rev Mol Cell Biol. 2006;7(9):678-689.
51. Ader T, Norel R, Levoci L, Rogler LE. Transcriptional profiling implicates TGFbeta/BMP and Notch signaling pathways in ductular differentiation of fetal murine hepatoblasts. Mech Dev. 2006;123(2):177-194.
52. Kodama Y, Hijikata M, Kageyama R, Shimotohno K, Chiba T. The role of notch signaling in the development of intrahepatic bile ducts. Gastroenterology. 2004;127(6):1775-1786.
53. Lorent K, Moore JC, Siekmann AF, Lawson N, Pack M. Reiterative use of the notch signal during zebrafish intrahepatic biliary development. Dev Dyn. 2010;239(3):855-864.
54. Hofmann JJ, Zovein AC, Koh H, Radtke F, Weinmaster G, Iruela-Arispe ML. Jagged1 in the portal vein mesenchyme regulates intrahepatic bile duct development: insights into Alagille syndrome. Development. 2010;137(23):4061- 4072.
55. Vanderpool C, Sparks EE, Huppert KA, Gannon M, Means AL, Huppert SS. Genetic interactions between hepatocyte nuclear factor-6 and Notch signaling regulate mouse intrahepatic bile duct development in vivo. Hepatology. 2012;55(1):233-243.
56. Tanimizu N, Miyajima A. Notch signaling controls hepatoblast differentiation by altering the expression of liver-enriched transcription factors. J Cell Sci. 2004;117(pt 15):3165-3174.
57. Kohler C, Bell AW, Bowen WC, Monga SP, Fleig W, Michalopoulos GK. Expression of Notch-1 and its ligand Jagged-1 in rat liver during liver regeneration. Hepatology. 2004;39(4):1056-1065.
58. Loomes KM, et al. Bile duct proliferation in liver-specific Jag1 conditional knockout mice: effects of gene dosage. Hepatology. 2007;45(2):323-330.
59. Lozier J, McCright B, Gridley T. Notch signaling regulates bile duct morphogenesis in mice. PLoS One. 2008;3(3):e1851.
60. McCright B, Lozier J, Gridley T. A mouse model of Alagille syndrome: Notch2 as a genetic modifier of Jag1 haploinsufficiency. Development. 2002;129(4):1075-1082.
61. Ryan MJ, et al. Bile duct proliferation in Jag1 fringe heterozygous mice identifies candidate modifiers of the alagille syndrome hepatic phenotype. Hepatology M. 2008;48(6):1989-1997.
62. Sparks EE, Huppert KA, Brown MA, Washington MK, Huppert SS. Notch signaling regulates formation of the 3-dimensional architecture of intrahepatic bile ducts in mice. Hepatology. 2010;51(4):1391-1400.
63. Goessling W, et al. APC mutant zebrafish uncover a changing temporal requirement for wnt signaling in liver development. Dev Biol. 2008;320(1):161-174.
64. Micsenyi A, Tan X, Sneddon T, Luo JH, Michalopoulos GK, Monga SP. Beta-catenin is temporally regulated during normal liver development. Gastroenterology. 2004;126(4):1134-1146.
65. Ober EA, Verkade H, Field HA, Stainier DY. Mesodermal Wnt2b signalling positively regulates liver specification. Nature. 2006;442(7103):688-691.
66. Decaens T, et al. Stabilization of beta-catenin affects mouse embryonic liver growth and hepatoblast fate. Hepatology. 2008;47(1):247-258.
67. Monga SP, Monga HK, Tan X, Mule K, Pediaditakis P, Michalopoulos GK. Beta-catenin antisense studies in embryonic liver cultures: role in proliferation, apoptosis, and lineage specification. Gastroenterology. 2003;124(1):202-216.
68. Burke ZD, Reed KR, Phesse TJ, Sansom OJ, Clarke AR, Tosh D. Liver zonation occurs through a betacatenin-dependent, c-Myc-independent mechanism. Gastroenterology. 2009;136(7):2316-2324.
69. Reed KR, et al. B-catenin deficiency, but not Myc deletion, suppresses the immediate phenotypes of APC loss in the liver. Proc Natl Acad Sci U S A. 2008;105(48):18919-18923.
70. Tan X, et al. Beta-catenin deletion in hepatoblasts disrupts hepatic morphogenesis and survival during mouse development. Hepatology. 2008;47(5):1667-1679.
71. Apte U, et al. beta-Catenin is critical for early postnatal liver growth. Am J Physiol Gastrointest Liver Physiol. 2007;292(6):G1578-G1585.
72. Ishikawa T, et al. Hepatocyte growth factor/c-met signaling is required for stem-cell-mediated liver regeneration in mice. Hepatology. 2012; 55(4):1215-1226.
73. Van Hul NK, barca-Quinones J, Sempoux C, Horsmans Y, Leclercq IA. Relation between liver progenitor cell expansion and extracellular matrix deposition in a CDE-induced murine model of chronic liver injury. Hepatology. 2009;49(5):1625-1635.
74. Lorenzini S, 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.
75. Spee B, et al. Characterisation of the liver progenitor cell niche in liver diseases: potential involvement of Wnt and Notch signalling. Gut. 2010;59(2):247-257.
76. Lin SL, et al. Macrophage Wnt7b is critical for kidney repair and regeneration. Proc Natl Acad Sci U S A. 2010;107(9):4194-4199.
77. Reddy SM, et al. Phagocytosis of apoptotic cells by macrophages induces novel signaling events leading to cytokine-independent survival and inhibition of proliferation: activation of Akt and inhibition of extracellular signal-regulated kinases 1 and 2. J Immunol. 2002;169(2):702-713.
78. Van HN, Lanthier N, Espanol SR, Abarca QJ, Van RN, Leclercq I. Kupffer cells influence parenchymal invasion and phenotypic orientation, but not the proliferation, of liver progenitor cells in a murine model of liver injury. Am J Pathol. 2011;179(4):1839-1850.
79. Clouston AD, Powell EE, Walsh MJ, Richardson MM, Demetris AJ, Jonsson JR. Fibrosis correlates with a ductular reaction in hepatitis C: roles of impaired replication, progenitor cells and steatosis. Hepatology. 2005;41(4):809-818.
80. Gouw AS, Clouston AD, Theise ND. Ductular reactions in human liver: Diversity at the interface. Hepatology. 2011;54(5):1853-1863.
81. Sekiya S, Suzuki A. Intrahepatic cholangiocarcinoma can arise from Notch-mediated conversion of hepatocytes. J Clin Invest. 2012;122(11):3914-3918.
82. Fan B, et al. Cholangiocarcinomas can originate from hepatocytes in mice. J Clin Invest. 2012;122(8):2911-2915.
83. Wei W, Chua MS, Grepper S, So S. Small molecule antagonists of Tcf4/beta-catenin complex inhibit the growth of HCC cells in vitro and in vivo. Int J Cancer. 2010;126(10):2426-2436.