Combinatorial microenvironmental regulation of liver progenitor differentiation by Notch ligands, TGFβ, and extracellular matrix

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Kaylan, Kerim B ^a   Ermilova, Viktoriya ^a   Yada, Ravi Chandra ^a   Underhill, Gregory H ^a  

^a United States of America   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DLK1 PROTEIN, MOUSE; GREEN FLUORESCENT PROTEIN; JAG1 PROTEIN, MOUSE; LIGAND; NOTCH RECEPTOR; PROTEIN JAGGED 1; SCLEROPROTEIN; SIGNAL PEPTIDE; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL; BILE DUCT; CELL DIFFERENTIATION; CELL LINE; COCULTURE; CYTOLOGY; DRUG EFFECTS; EMBRYONIC STEM CELL; FLUORESCENCE MICROSCOPY; GENE EXPRESSION; GENETICS; IMMUNOBLOTTING; LIVER; LIVER CELL; METABOLISM; MOUSE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; TUMOR MICROENVIRONMENT;

ANIMALS; BILE DUCTS; CELL DIFFERENTIATION; CELL LINE; CELLULAR MICROENVIRONMENT; COCULTURE TECHNIQUES; EMBRYONIC STEM CELLS; EXTRACELLULAR MATRIX PROTEINS; GENE EXPRESSION; GREEN FLUORESCENT PROTEINS; HEPATOCYTES; IMMUNOBLOTTING; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; JAGGED-1 PROTEIN; LIGANDS; LIVER; MICE; MICROSCOPY, FLUORESCENCE; RECEPTORS, NOTCH; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; TRANSFORMING GROWTH FACTOR BETA;

EID: 84963642820     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep23490     Document Type: Article

References (68)

1. Zong, Y. et al. Notch signaling controls liver development by regulating biliary differentiation. Development 136, 1727-1739, doi: 10.1242/dev.029140 (2009).
2. Clotman, F. et al. Control of liver cell fate decision by a gradient of TGF beta signaling modulated by Onecut transcription factors. Genes Dev 19, 1849-1854, doi: 10.1101/gad.340305 (2005).
3. Kodama, Y., Hijikata, M., Kageyama, R., Shimotohno, K., Chiba, T. The role of notch signaling in the development of intrahepatic bile ducts. Gastroenterology 127, 1775-1786 (2004).
4. Tanimizu, N., Miyajima, A. Notch signaling controls hepatoblast differentiation by altering the expression of liver-enriched transcription factors. J Cell Sci 117, 3165-3174, doi: 10.1242/jcs.01169 (2004).
5. Clotman, F., Lemaigre, F. P. Control of hepatic differentiation by activin/TGFbeta signaling. Cell Cycle 5, 168-171 (2006).
6. Hofmann, J. J. et al. Jagged1 in the portal vein mesenchyme regulates intrahepatic bile duct development: insights into Alagille syndrome. Development 137, 4061-4072, doi: 10.1242/dev.052118 (2010).
7. Jeliazkova, P. et al. Canonical Notch2 signaling determines biliary cell fates of embryonic hepatoblasts and adult hepatocytes independent of Hes1. Hepatology 57, 2469-2479, doi: 10.1002/hep.26254 (2013).
8. Lozier, J., McCright, B., Gridley, T. Notch signaling regulates bile duct morphogenesis in mice. PLoS One 3, e1851, doi: 10.1371/journal.pone.0001851 (2008).
9. Tchorz, J. S. et al. Notch2 signaling promotes biliary epithelial cell fate specification and tubulogenesis during bile duct development in mice. Hepatology 50, 871-879, doi: 10.1002/hep.23048 (2009).
10. Loomes, K. M. et al. Bile duct proliferation in liver-specific Jag1 conditional knockout mice: effects of gene dosage. Hepatology 45, 323-330 (2007).
11. Li, L. et al. Alagille syndrome is caused by mutations in human Jagged1, which encodes a ligand for Notch1. Nat Genet 16, 243-251, doi: 10.1038/ng0797-243 (1997).
12. Oda, T. et al. Mutations in the human Jagged1 gene are responsible for Alagille syndrome. Nat Genet 16, 235-242, doi: 10.1038/ng0797-235 (1997).
13. McDaniell, R. et al. NOTCH2 mutations cause Alagille syndrome, a heterogeneous disorder of the notch signaling pathway. Am J Hum Genet 79, 169-173, doi: 10.1086/505332 (2006).
14. Alagille, D. et al. Syndromic paucity of interlobular bile ducts (Alagille syndrome or arteriohepatic dysplasia): review of 80 cases. J Pediatr 110, 195-200 (1987).
15. Tanimizu, N., Miyajima, A., Mostov, K. E. Liver progenitor cells develop cholangiocyte-type epithelial polarity in threedimensional culture. Mol Biol Cell 18, 1472-1479, doi: 10.1091/mbc.E06-09-0848 (2007).
16. Yanai, M. et al. FGF signaling segregates biliary cell-lineage from chick hepatoblasts cooperatively with BMP4 and ECM components in vitro. Dev Dyn 237, 1268-1283, doi: 10.1002/dvdy.21520 (2008).
17. Tanimizu, N., Kikkawa, Y., Mitaka, T., Miyajima, A. alpha1-and alpha5-containing laminins regulate the development of bile ducts via beta1 integrin signals. J Biol Chem 287, 28586-28597, doi: 10.1074/jbc.M112.350488 (2012).
18. Hanley, K. P. et al. Ectopic SOX9 mediates extracellular matrix deposition characteristic of organ fibrosis. J Biol Chem 283, 14063-14071, doi: 10.1074/jbc.M707390200 (2008).
19. Poncy, A. et al. Transcription factors SOX4 and SOX9 cooperatively control development of bile ducts. Dev Biol, doi: 10.1016/j. ydbio.2015.05.012 (2015).
20. Roskams, T. A. et al. Nomenclature of the finer branches of the biliary tree: canals, ductules, and ductular reactions in human livers. Hepatology 39, 1739-1745, doi: 10.1002/hep.20130 (2004).
21. Gouw, A. S., Clouston, A. D., Theise, N. D. Ductular reactions in human liver: diversity at the interface. Hepatology 54, 1853-1863, doi: 10.1002/hep.24613 (2011).
22. Boulter, L. et al. Macrophage-derived Wnt opposes Notch signaling to specify hepatic progenitor cell fate in chronic liver disease. Nat Med 18, 572-579, doi: 10.1038/nm.2667 (2012).
23. Lorenzini, S. et al. Characterisation of a stereotypical cellular and extracellular adult liver progenitor cell niche in rodents and diseased human liver. Gut 59, 645-654, doi: 10.1136/gut.2009.182345 (2010).
24. Van Hul, N. K., Abarca-Quinones, J., Sempoux, C., Horsmans, Y., Leclercq, I. A. Relation between liver progenitor cell expansion and extracellular matrix deposition in a CDE-induced murine model of chronic liver injury. Hepatology 49, 1625-1635, doi: 10.1002/hep.22820 (2009).
25. Williams, M. J., Clouston, A. D., Forbes, S. J. Links between hepatic fibrosis, ductular reaction, and progenitor cell expansion. Gastroenterology 146, 349-356, doi: 10.1053/j.gastro.2013.11.034 (2014).
26. Artavanis-Tsakonas, S., Rand, M. D., Lake, R. J. Notch signaling: cell fate control and signal integration in development. Science 284, 770-776 (1999).
27. Bray, S. J. Notch signalling: a simple pathway becomes complex. Nat Rev Mol Cell Biol 7, 678-689, doi: 10.1038/nrm2009 (2006).
28. Andersson, E. R., Sandberg, R., Lendahl, U. Notch signaling: simplicity in design, versatility in function. Development 138, 3593-3612, doi: 10.1242/dev.063610 (2011).
29. Varnum-Finney, B. et al. The Notch ligand, Jagged-1, influences the development of primitive hematopoietic precursor cells. Blood 91, 4084-4091 (1998).
30. Varnum-Finney, B. et al. Immobilization of Notch ligand, Delta-1, is required for induction of Notch signaling. Journal of Cell Science 113, 4313-4318 (2000).
31. Tran, I. T. et al. Blockade of individual Notch ligands and receptors controls graft-versus-host disease. J Clin Invest 123, 1590-1604, doi: 10.1172/JCI65477 (2013).
32. Wu, Y. et al. Therapeutic antibody targeting of individual Notch receptors. Nature 464, 1052-1057, doi: 10.1038/nature08878 (2010).
33. Nickoloff, B. J. et al. Jagged-1 mediated activation of notch signaling induces complete maturation of human keratinocytes through NF-kappaB and PPARgamma. Cell Death Differ 9, 842-855, doi: 10.1038/sj.cdd.4401036 (2002).
34. Flaim, C. J., Chien, S., Bhatia, S. N. An extracellular matrix microarray for probing cellular differentiation. Nat Methods 2, 119-125, doi: 10.1038/nmeth736 (2005).
35. Brafman, D. A., Chien, S., Willert, K. Arrayed cellular microenvironments for identifying culture and differentiation conditions for stem, primary and rare cell populations. Nat Protoc 7, 703-717, doi: 10.1038/nprot.2012.017 (2012).
36. Underhill, G. H., Flaim, C. J., Bhatia, S. N. In Methods in Bioengineering: Stem Cell Bioengineering Artech House Methods in Bioengineering (eds. Biju Parekkadan & Martin Yarmush) 63-73 (Artech House Publishers, Boston, MA, 2009).
37. Strick-Marchand, H., Weiss, M. C. Inducible differentiation and morphogenesis of bipotential liver cell lines from wild-type mouse embryos. Hepatology 36, 794-804, doi: 10.1053/jhep.2002.36123 (2002).
38. Strick-Marchand, H., Morosan, S., Charneau, P., Kremsdorf, D., Weiss, M. C. Bipotential mouse embryonic liver stem cell lines contribute to liver regeneration and differentiate as bile ducts and hepatocytes. P Natl Acad Sci USA 101, 8360-8365, doi: 10.1073/pnas.0401092101 (2004).
39. Carpentier, R. et al. Embryonic ductal plate cells give rise to cholangiocytes, periportal hepatocytes, and adult liver progenitor cells. Gastroenterology 141, 1432-1438, 1438 e1431-1434, doi: 10.1053/j.gastro.2011.06.049 (2011).
40. Inman, G. J. et al. SB-431542 is a potent and specific inhibitor of transforming growth factor-beta superfamily type I activin receptor-like kinase (ALK) receptors ALK4, ALK5, and ALK7. Mol Pharmacol 62, 65-74, doi: 10.1124/mol.62.1.65 (2002).
41. Hynes, R. O. The extracellular matrix: not just pretty fibrils. Science 326, 1216-1219, doi: 10.1126/science.1176009 (2009).
42. Boulter, L. et al. Macrophage-derived Wnt opposes Notch signaling to specify hepatic progenitor cell fate in chronic liver disease. Nat. Med. 18, 572-579 (2012).
43. Leong, K. G. et al. Activated Notch4 inhibits angiogenesis: role of beta 1-integrin activation. Mol Cell Biol 22, 2830-2841 (2002).
44. Estrach, S. et al. Laminin-binding integrins induce Dll4 expression and Notch signaling in endothelial cells. Circ Res 109, 172-182, doi: 10.1161/CIRCRESAHA.111.240622 (2011).
45. Martinez-Hernandez, A., Amenta, P. S. The hepatic extracellular matrix. II. Ontogenesis, regeneration and cirrhosis. Virchows Arch A Pathol Anat Histopathol 423, 77-84 (1993).
46. Bardot, B., Mok, L. P., Thayer, T., Ahimou, F., Wesley, C. The Notch amino terminus regulates protein levels and Delta-induced clustering of Drosophila Notch receptors. Exp Cell Res 304, 202-223, doi: 10.1016/j.yexcr.2004.10.030 (2005).
47. Ader, T., Norel, R., Levoci, L., Rogler, L. E. Transcriptional profiling implicates TGFbeta/BMP and Notch signaling pathways in ductular differentiation of fetal murine hepatoblasts. Mech Dev 123, 177-194, doi: 10.1016/j.mod.2005.10.003 (2006).
48. Blokzijl, A. et al. Cross-talk between the Notch and TGF-beta signaling pathways mediated by interaction of the Notch intracellular domain with Smad3. J Cell Biol 163, 723-728, doi: 10.1083/jcb.200305112 (2003).
49. Zavadil, J., Cermak, L., Soto-Nieves, N., Bottinger, E. P. Integration of TGF-beta/Smad and Jagged1/Notch signalling in epithelialto-mesenchymal transition. EMBO J 23, 1155-1165, doi: 10.1038/sj.emboj.7600069 (2004).
50. Ortica, S., Tarantino, N., Aulner, N., Israel, A., Gupta-Rossi, N. The 4 Notch receptors play distinct and antagonistic roles in the proliferation and hepatocytic differentiation of liver progenitors. FASEB J 28, 603-614 (2014).
51. Falix, F. A. et al. Hepatic Notch2 deficiency leads to bile duct agenesis perinatally and secondary bile duct formation after weaning. Dev Biol 396, 201-213, doi: 10.1016/j.ydbio.2014.10.002 (2014).
52. Geisler, F. et al. Liver-specific inactivation of Notch2, but not Notch1, compromises intrahepatic bile duct development in mice. Hepatology 48, 607-616, doi: 10.1002/hep.22381 (2008).
53. LaVoie, M. J., Selkoe, D. J. The Notch ligands, Jagged and Delta, are sequentially processed by alpha-secretase and presenilin/gamma-secretase and release signaling fragments. J Biol Chem 278, 34427-34437, doi: 10.1074/jbc.M302659200 (2003).
54. Six, E. et al. The Notch ligand Delta1 is sequentially cleaved by an ADAM protease and gamma-secretase. Proc Natl Acad Sci USA 100, 7638-7643, doi: 10.1073/pnas.1230693100 (2003).
55. Bordonaro, M., Tewari, S., Atamna, W., Lazarova, D. L. The Notch ligand Delta-like 1 integrates inputs from TGFbeta/Activin and Wnt pathways. Exp Cell Res 317, 1368-1381, doi: 10.1016/j.yexcr.2011.03.019 (2011).
56. Hiratochi, M. et al. The Delta intracellular domain mediates TGF-beta/Activin signaling through binding to Smads and has an important bi-directional function in the Notch-Delta signaling pathway. Nucleic Acids Res 35, 912-922, doi: 10.1093/nar/gkl1128 (2007).
57. del Alamo, D., Rouault, H., Schweisguth, F. Mechanism and significance of cis-inhibition in Notch signalling. Curr Biol 21, R40-47, doi: 10.1016/j.cub.2010.10.034 (2011).
58. Shimojo, H., Ohtsuka, T., Kageyama, R. Oscillations in notch signaling regulate maintenance of neural progenitors. Neuron 58, 52-64, doi: 10.1016/j.neuron.2008.02.014 (2008).
59. Eddison, M., Le Roux, I., Lewis, J. Notch signaling in the development of the inner ear: lessons from Drosophila. Proc Natl Acad Sci USA 97, 11692-11699, doi: 10.1073/pnas.97.22.11692 (2000).
60. Timmerman, L. A. et al. Notch promotes epithelial-mesenchymal transition during cardiac development and oncogenic transformation. Genes Dev 18, 99-115, doi: 10.1101/gad.276304 (2004).
61. Yu, Y. et al. A comparative analysis of liver transcriptome suggests divergent liver function among human, mouse and rat. Genomics 96, 281-289, doi: 10.1016/j.ygeno.2010.08.003 (2010).
62. Ye, J. et al. Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction. BMC Bioinformatics 13, 134, doi: 10.1186/1471-2105-13-134 (2012).
63. R Core Team (2014). R: A Language and Environment for Statistical Computing. (2014). < http://www.R-project.org/>.
64. Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat Methods 9, 676-682, doi: 10.1038/nmeth.2019 (2012).
65. Schneider, C. A., Rasband, W. S., Eliceiri, K. W. NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9, 671-675 (2012).
66. Kamentsky, L. et al. Improved structure, function and compatibility for CellProfiler: modular high-throughput image analysis software. Bioinformatics 27, 1179-1180, doi: 10.1093/bioinformatics/btr095 (2011).
67. Wickham, H. ggplot2: Elegant Graphics for Data Analysis. Use R 1-212, doi: 10.1007/978-0-387-98141-3 (2009).
68. Wickham, H. The Split-Apply-Combine Strategy for Data Analysis. J Stat Softw 40, 1-29 (2011).