Emerging roles of Notch signaling in liver disease

Hepatology

Volumn 61, Issue 1, 2015, Pages 382-392

  Geisler, Fabian ^a   Strazzabosco, Mario ^b,c  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF MILANO BICOCCA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

NOTCH RECEPTOR;

ARTICLE; BILE DUCT CARCINOMA; CELL FATE; CELL FUNCTION; CELLS BY BODY ANATOMY; CLINICAL PRACTICE; GAIN OF FUNCTION MUTATION; HEPATITIS; HOMEOSTASIS; HUMAN; IN VITRO STUDY; LIVER CANCER; LIVER CARCINOGENESIS; LIVER CELL; LIVER CELL CARCINOMA; LIVER DEVELOPMENT; LIVER DISEASE; LIVER FIBROSIS; LIVER HOMEOSTASIS; LIVER METABOLISM; LIVER REGENERATION; LIVER REPAIR; LIVER TUMOR; MAMMAL CELL; METABOLISM; NONHUMAN; NOTCH SIGNALING; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STEM CELL; TISSUE REPAIR; ANIMAL; GROWTH, DEVELOPMENT AND AGING; LIVER;

ANIMALS; HUMANS; LIVER; LIVER NEOPLASMS; LIVER REGENERATION; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION;

EID: 84920997369     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.27268     Document Type: Article

References (61)

1. Fortini ME. Notch signaling: the core pathway and its posttranslational regulation. Dev Cell 2009;16:633-647.
2. Kopan R, Ilagan MX. The canonical Notch signaling pathway: unfolding the activation mechanism. Cell 2009;137:216-233.
3. Andersson ER, Sandberg R, Lendahl U. Notch signaling: simplicity in design, versatility in function. Development 2011;138:3593-3612.
4. Gridley T. Notch signaling and inherited disease syndromes. Hum Mol Genet 2003;12 Spec No 1:R9-13.
5. Li L, Krantz ID, Deng Y, Genin A, Banta AB, Collins CC, et al. Alagille syndrome is caused by mutations in human Jagged1, which encodes a ligand for Notch1. Nat Genet 1997;16:243-251.
6. Oda T, Elkahloun AG, Pike BL, Okajima K, Krantz ID, Genin A, et al. Mutations in the human Jagged1 gene are responsible for Alagille syndrome. Nat Genet 1997;16:235-242.
7. McCright B, Lozier J, Gridley T. A mouse model of Alagille syndrome: Notch2 as a genetic modifier of Jag1 haploinsufficiency. Development 2002;129:1075-1082.
8. Kodama Y, Hijikata M, Kageyama R, Shimotohno K, Chiba T. The role of notch signaling in the development of intrahepatic bile ducts. Gastroenterology 2004;127:1775-1786.
9. Loomes KM, Russo P, Ryan M, Nelson A, Underkoffler L, Glover C, et al. Bile duct proliferation in liver-specific Jag1 conditional knockout mice: effects of gene dosage. Hepatology 2007;45:323-330.
10. Lozier J, McCright B, Gridley T. Notch signaling regulates bile duct morphogenesis in mice. PLoS One 2008;3:e1851.
11. Geisler F, Nagl F, Mazur PK, Lee M, Zimber-Strobl U, Strobl LJ, et al. Liver-specific inactivation of Notch2, but not Notch1, compromises intrahepatic bile duct development in mice. Hepatology 2008;48:607-616.
12. Zong Y, Panikkar A, Xu J, Antoniou A, Raynaud P, Lemaigre F, Stanger BZ. Notch signaling controls liver development by regulating biliary differentiation. Development 2009;136:1727-1739.
13. Sparks EE, Huppert KA, Brown MA, Washington MK, Huppert SS. Notch signaling regulates formation of the three-dimensional architecture of intrahepatic bile ducts in mice. Hepatology 2010;51:1391-1400.
14. 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;137:4061-4072.
15. Lorent K, Moore JC, Siekmann AF, Lawson N, Pack M. Reiterative use of the notch signal during zebrafish intrahepatic biliary development. Dev Dyn 2010;239:855-864.
16. McDaniell R, Warthen DM, Sanchez-Lara PA, Pai A, Krantz ID, Piccoli DA, Spinner NB. NOTCH2 mutations cause Alagille syndrome, a heterogeneous disorder of the notch signaling pathway. Am J Hum Genet 2006;79:169-173.
17. Jeliazkova P, Jors S, Lee M, Zimber-Strobl U, Ferrer J, Schmid RM, et al. Canonical Notch2 signaling determines biliary cell fates of embryonic hepatoblasts and adult hepatocytes independent of Hes1. Hepatology 2013;57:2469-2479.
18. Novotny NM, Zetterman RK, Antonson DL, Vanderhoof JA. Variation in liver histology in Alagille's syndrome. Am J Gastroenterol 1981;75:449-450.
19. Fabris L, Cadamuro M, Guido M, Spirli C, Fiorotto R, Colledan M, et al. Analysis of liver repair mechanisms in Alagille syndrome and biliary atresia reveals a role for notch signaling. Am J Pathol 2007;171:641-653.
20. Tchorz JS, Kinter J, Muller M, Tornillo L, Heim MH, Bettler B. Notch2 signaling promotes biliary epithelial cell fate specification and tubulogenesis during bile duct development in mice. Hepatology 2009;50:971-879.
21. Tanimizu N, Miyajima A. Notch signaling controls hepatoblast differentiation by altering the expression of liver-enriched transcription factors. J Cell Sci 2004;117:3165-3174.
22. Zong Y, Stanger BZ. Molecular mechanisms of liver and bile duct development. Wiley Interdiscip Rev Dev Biol 2012;1:643-655.
23. Raynaud P, Carpentier R, Antoniou A, Lemaigre FP. Biliary differentiation and bile duct morphogenesis in development and disease. Int J Biochem Cell Biol 2011;43:245-256.
24. 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;39:1056-1065.
25. Wang L, Wang CM, Hou LH, Dou GR, Wang YC, Hu XB, et al. Disruption of the transcription factor recombination signal-binding protein-Jkappa (RBP-J) leads to veno-occlusive disease and interfered liver regeneration in mice. Hepatology 2009;49:268-277.
26. Dill MT, Rothweiler S, Djonov V, Hlushchuk R, Tornillo L, Terracciano L, et al. Disruption of Notch1 induces vascular remodeling, intussusceptive angiogenesis, and angiosarcomas in livers of mice. Gastroenterology 2012;142:967-977.e2.
27. Croquelois A, Blindenbacher A, Terracciano L, Wang X, Langer I, Radtke F, Heim MH. Inducible inactivation of Notch1 causes nodular regenerative hyperplasia in mice. Hepatology 2005;41:487-496.
28. Gouw AS, Clouston AD, Theise ND. Ductular reactions in human liver: diversity at the interface. Hepatology 2011;54:1853-1863.
29. Spee B, Carpino G, Schotanus BA, Katoonizadeh A, Vander Borght S, Gaudio E, Roskams T. Characterisation of the liver progenitor cell niche in liver diseases: potential involvement of Wnt and Notch signalling. Gut 2010;59:247-257.
30. Boulter L, Govaere O, Bird TG, Radulescu S, Ramachandran P, Pellicoro A, et al. Macrophage-derived Wnt opposes Notch signaling to specify hepatic progenitor cell fate in chronic liver disease. Nat Med 2012;18:572-579.
31. Fiorotto R, Raizner A, Morell CM, Torsello B, Scirpo R, Fabris L, et al. Notch signaling regulates tubular morphogenesis during repair from biliary damage in mice. J Hepatol 2013;59:124-130.
32. Malato Y, Naqvi S, Schurmann N, Ng R, Wang B, Zape J, et al. Fate tracing of mature hepatocytes in mouse liver homeostasis and regeneration. J Clin Invest 2011;121:4850-4860.
33. Español-Suñer R, Carpentier R, Van Hul N, Legry V, Achouri Y, Cordi S, et al. Liver progenitor cells yield functional hepatocytes in response to chronic liver injury in mice. Gastroenterology 2012;143:1564-1575.e7.
34. Williams MJ, Clouston AD, Forbes SJ. Links between hepatic fibrosis, ductular reaction, and progenitor cell expansion. Gastroenterology 2014;146:349-356.
35. Yanger K, Zong Y, Maggs LR, Shapira SN, Maddipati R, Aiello NM, et al. Robust cellular reprogramming occurs spontaneously during liver regeneration. Genes Dev 2013;27:719-724.
36. Tanimizu N, Nishikawa Y, Ichinohe N, Akiyama H, Mitaka T. Sry HMG box protein 9-positive (Sox9+) epithelial cell adhesion molecule-negative (EpCAM-) biphenotypic cells derived from hepatocytes are involved in mouse liver regeneration. J Biol Chem 2014;289:7589-7598.
37. Sekiya S, Suzuki A. Intrahepatic cholangiocarcinoma can arise from Notch-mediated conversion of hepatocytes. J Clin Invest 2012;122:3914-3918.
38. Fan B, Malato Y, Calvisi DF, Naqvi S, Razumilava N, Ribback S, et al. Cholangiocarcinomas can originate from hepatocytes in mice. J Clin Invest 2012;122:2911-2915.
39. Sawitza I, Kordes C, Reister S, Haussinger D. The niche of stellate cells within rat liver. Hepatology 2009;50:1617-1624.
40. Chen Y, Zheng S, Qi D, Guo J, Zhang S, Weng Z. Inhibition of Notch signaling by a gamma-secretase inhibitor attenuates hepatic fibrosis in rats. PLoS One 2012;7:e46512.
41. Outtz HH, Wu JK, Wang X, Kitajewski J. Notch1 deficiency results in decreased inflammation during wound healing and regulates vascular endothelial growth factor receptor-1 and inflammatory cytokine expression in macrophages. J Immunol 2010;185:4363-4373.
42. Zhang Q, Wang C, Liu Z, Liu X, Han C, Cao X, Li N. Notch signal suppresses Toll-like receptor-triggered inflammatory responses in macrophages by inhibiting extracellular signal-regulated kinase 1/2-mediated nuclear factor kappaB activation. J Biol Chem 2012;287:6208-6217.
43. Xu H, Zhu J, Smith S, Foldi J, Zhao B, Chung AY, et al. Notch-RBP-J signaling regulates the transcription factor IRF8 to promote inflammatory macrophage polarization. Nat Immunol 2012;13:642-650.
44. Lee JS, Heo J, Libbrecht L, Chu IS, Kaposi-Novak P, Calvisi DF, et al. A novel prognostic subtype of human hepatocellular carcinoma derived from hepatic progenitor cells. Nat Med 2006;12:410-416.
45. Strazzabosco M, Fabris L. Notch signaling in hepatocellular carcinoma: guilty in association! Gastroenterology 2012;143:1430-1434.
46. Zender S, Nickeleit I, Wuestefeld T, Sorensen I, Dauch D, Bozko P, et al. A critical role for notch signaling in the formation of cholangiocellular carcinomas. Cancer Cell 2013;23:784-795.
47. Villanueva A, Alsinet C, Yanger K, Hoshida Y, Zong Y, Toffanin S, et al. Notch signaling is activated in human hepatocellular carcinoma and induces tumor formation in mice. Gastroenterology 2012;143:1660-1669.e7.
48. Dill MT, Tornillo L, Fritzius T, Terracciano L, Semela D, Bettler B, et al. Constitutive Notch2 signaling induces hepatic tumors in mice. Hepatology 2013;57:1607-1619.
49. El Khatib M, Bozko P, Palagani V, Malek NP, Wilkens L, Plentz RR. Activation of Notch signaling is required for cholangiocarcinoma progression and is enhanced by inactivation of p53 in vivo. PLoS One 2013;8:e77433.
50. Michalopoulos GK, Barua L, Bowen WC. Transdifferentiation of rat hepatocytes into biliary cells after bile duct ligation and toxic biliary injury. Hepatology 2005;41:535-544.
51. Gurlevik E, Fleischmann-Mundt B, Armbrecht N, Longerich T, Woller N, Kloos A, et al. Adjuvant gemcitabine therapy improves survival in a locally induced, R0-resectable model of metastatic intrahepatic cholangiocarcinoma. Hepatology 2013;58:1031-1041.
52. Holczbauer A, Factor VM, Andersen JB, Marquardt JU, Kleiner DE, Raggi C, et al. Modeling pathogenesis of primary liver cancer in lineage-specific mouse cell types. Gastroenterology 2013;145:221-231.
53. Dumble ML, Croager EJ, Yeoh GC, Quail EA. Generation and characterization of p53 null transformed hepatic progenitor cells: oval cells give rise to hepatocellular carcinoma. Carcinogenesis 2002;23:435-445.
54. Yamashita T, Wang XW. Cancer stem cells in the development of liver cancer. J Clin Invest 2013;123:1911-1918.
55. Ishimura N, Bronk SF, Gores GJ. Inducible nitric oxide synthase up-regulates Notch-1 in mouse cholangiocytes: implications for carcinogenesis. Gastroenterology 2005;128:1354-1368.
56. Pajvani UB, Shawber CJ, Samuel VT, Birkenfeld AL, Shulman GI, Kitajewski J, Accili D. Inhibition of Notch signaling ameliorates insulin resistance in a FoxO1-dependent manner. Nat Med 2011;17:961-967.
57. Pajvani UB, Qiang L, Kangsamaksin T, Kitajewski J, Ginsberg HN, Accili D. Inhibition of Notch uncouples Akt activation from hepatic lipid accumulation by decreasing mTorc1 stability. Nat Med 2013;19:1054-1060.
58. Morell CM, Strazzabosco M. Notch signaling and new therapeutic options in liver disease. J Hepatol 2014;60:885-890.
59. Heitzler P. Biodiversity and noncanonical Notch signaling. Curr Top Dev Biol 2010;92:457-481.
60. Antoniou A, Raynaud P, Cordi S, Zong YW, Tronche F, Stanger BZ, et al. Intrahepatic bile ducts develop according to a new mode of tubulogenesis regulated by the transcription factor SOX9. Gastroenterology 2009;136:2325-2333.
61. Viatour P, Ehmer U, Saddic LA, Dorrell C, Andersen JB, Lin C, et al. Notch signaling inhibits hepatocellular carcinoma following inactivation of the RB pathway. J Exp Med 2011;208:1963-1976.