Prox1 ablation in hepatic progenitors causes defective hepatocyte specification and increases biliary cell commitment

Development (Cambridge)

Volumn 141, Issue 3, 2014, Pages 538-547

  Seth, Asha ^a   Ye, Jianming ^a   Yu, Nanjia ^a   Guez, Fanny ^a   Bedford, David C ^a   Neale, Geoffrey A ^a   Cordi, Sabine ^b   Brindle, Paul K ^a   Lemaigre, Frederic P ^b   Kaestner, Klaus H ^c   Sosa Pineda, Beatriz ^a  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^b DE DUVE INSTITUTE   (Belgium)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Hepatic precursors; Liver; Mouse; Prox1; TGF

Indexed keywords

HOMEODOMAIN PROTEIN; PROX1 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BILIARY HYPERPLASIA; BILIARY TRACT DISEASE; CELL DIFFERENTIATION; FETUS LIVER; GENE DELETION; IMMUNOHISTOCHEMISTRY; INTRAHEPATIC BILE DUCT; LIVER CELL; LIVER DEVELOPMENT; LIVER DISEASE; LIVER PARENCHYMA; MORPHOGENESIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

HEPATIC PRECURSORS; LIVER; MOUSE; PROX1; TGFΒ;

AGING; ANIMALS; ANIMALS, NEWBORN; BILE DUCTS; CELL COUNT; CELL LINEAGE; CHORISTOMA; EPITHELIAL CELLS; FETUS; GENE DELETION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEPATOCYTE NUCLEAR FACTOR 4; HEPATOCYTES; HOMEODOMAIN PROTEINS; LIVER; MICE; SIGNAL TRANSDUCTION; SOX9 TRANSCRIPTION FACTOR; STEM CELLS; TRANSFORMING GROWTH FACTOR BETA; TUMOR SUPPRESSOR PROTEINS;

EID: 84892689481     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.099481     Document Type: Article

References (49)

1. Antoniou, A., Raynaud, P., Cordi, S., Zong, Y., Tronche, F., Stanger, B. Z., Jacquemin, P., Pierreux, C. E., Clotman, F. and Lemaigre, F. P. (2009). Intrahepatic bile ducts develop according to a new mode of tubulogenesis regulated by the transcription factor SOX9. Gastroenterology 136, 2325-2333.
2. Bataller, R. and Brenner, D. A. (2005). Liver fibrosis. J. Clin. Invest. 115, 209-218.
3. Burke, Z. and Oliver, G. (2002). Prox1 is an early specific marker for the developing liver and pancreas in the mammalian foregut endoderm. Mech. Dev. 118, 147-155.
4. Carey, G. B. and Chang, N. S. (1998). Cloning and characterization of a transforming growth factor beta 1-induced anti-apoptotic adhesion protein TIF2. Biochem. Biophys. Res. Commun. 249, 283-286.
5. Charest-Marcotte, A., Dufour, C. R., Wilson, B. J., Tremblay, A. M., Eichner, L. J., Arlow, D. H., Mootha, V. K. and Giguère, V. (2010). The homeobox protein Prox1 is a negative modulator of ERRalpha/PGC-1alpha bioenergetic functions. Genes Dev. 24, 537-542.
6. Chen, Q., Dowhan, D. H., Liang, D., Moore, D. D. and Overbeek, P. A. (2002). CREB-binding protein/p300 co-activation of crystallin gene expression. J. Biol. Chem. 277, 24081-24089.
7. Choksi, S. P., Southall, T. D., Bossing, T., Edoff, K., de Wit, E., Fischer, B. E., van Steensel, B., Micklem, G. and Brand, A. H. (2006). Prospero acts as a binary switch between self-renewal and differentiation in Drosophila neural stem cells. Dev. Cell 11, 775-789.
8. Clotman, F., Jacquemin, P., Plumb-Rudewiez, N., Pierreux, C. E., Van der Smissen, P., Dietz, H. C., Courtoy, P. J., Rousseau, G. G. and Lemaigre, F. P. (2005). Control of liver cell fate decision by a gradient of TGF beta signaling modulated by Onecut transcription factors. Genes Dev. 19, 1849-1854.
9. Cui, W., Tomarev, S. I., Piatigorsky, J., Chepelinsky, A. B. and Duncan, M. K. (2004). Mafs, Prox1, and Pax6 can regulate chicken betaB1-crystallin gene expression. J. Biol. Chem. 279, 11088-11095.
10. Dennler, S., André, J., Verrecchia, F. and Mauviel, A. (2009). Cloning of the human GLI2 Promoter: transcriptional activation by transforming growth factor-beta via SMAD3/beta-catenin cooperation. J. Biol. Chem. 284, 31523-31531.
11. Desmet, V., Roskams, T. and Van Eyken, P. (1995). Ductular reaction in the liver. Pathol. Res. Pract. 191, 513-524.
12. Dudas, J., Papoutsi, M., Hecht, M., Elmaouhoub, A., Saile, B., Christ, B., Tomarev, S. I., von Kaisenberg, C. S., Schweigerer, L., Ramadori, G. et al. (2004). The homeobox transcription factor Prox1 is highly conserved in embryonic hepatoblasts and in adult and transformed hepatocytes, but is absent from bile duct epithelium. Anat. Embryol. (Berl.) 208, 359-366.
13. Harvey, N. L., Srinivasan, R. S., Dillard, M. E., Johnson, N. C., Witte, M. H., Boyd, K., Sleeman, M. W. and Oliver, G. (2005). Lymphatic vascular defects promoted by Prox1 haploinsufficiency cause adult-onset obesity. Nat. Genet. 37, 1072-1081.
14. Hassan, B., Li, L., Bremer, K. A., Chang, W., Pinsonneault, J. and Vaessin, H. (1997). Prospero is a panneural transcription factor that modulates homeodomain protein activity. Proc. Natl. Acad. Sci. USA 94, 10991-10996.
15. Hunter, M. P., Wilson, C. M., Jiang, X., Cong, R., Vasavada, H., Kaestner, K. H. and Bogue, C. W. (2007). The homeobox gene Hhex is essential for proper hepatoblast differentiation and bile duct morphogenesis. Dev. Biol. 308, 355-367.
16. Kyrmizi, I., Hatzis, P., Katrakili, N., Tronche, F., Gonzalez, F. J. and Talianidis, I. (2006). Plasticity and expanding complexity of the hepatic transcription factor network during liver development. Genes Dev. 20, 2293-2305.
17. Lavado, A., Lagutin, O. V., Chow, L. M., Baker, S. J. and Oliver, G. (2010). Prox1 is required for granule cell maturation and intermediate progenitor maintenance during brain neurogenesis. PLoS Biol. 8, e1000460.
18. Lee, C. S., Friedman, J. R., Fulmer, J. T. and Kaestner, K. H. (2005). The initiation of liver development is dependent on Foxa transcription factors. Nature 435, 944-947.
19. Lemaigre, F. P. (2009). Mechanisms of liver development: concepts for understanding liver disorders and design of novel therapies. Gastroenterology 137, 62-79.
20. Lozier, J., McCright, B. and Gridley, T. (2008). Notch signaling regulates bile duct morphogenesis in mice. PLoS ONE 3, e1851.
21. Lüdtke, T. H., Christoffels, V. M., Petry, M. and Kispert, A. (2009). Tbx3 promotes liver bud expansion during mouse development by suppression of cholangiocyte differentiation. Hepatology 49, 969-978.
22. Nakamura, T., Takio, K., Eto, Y., Shibai, H., Titani, K. and Sugino, H. (1990). Activinbinding protein from rat ovary is follistatin. Science 247, 836-838.
23. Postic, C., Shiota, M., Niswender, K. D., Jetton, T. L., Chen, Y., Moates, J. M., Shelton, K. D., Lindner, J., Cherrington, A. D. and Magnuson, M. A. (1999). Dual roles for glucokinase in glucose homeostasis as determined by liver and pancreatic beta cell-specific gene knock-outs using Cre recombinase. J. Biol. Chem. 274, 305-315.
24. Qin, J., Gao, D. M., Jiang, Q. F., Zhou, Q., Kong, Y. Y., Wang, Y. and Xie, Y. H. (2004). Prospero-related homeobox (Prox1) is a corepressor of human liver receptor homolog-1 and suppresses the transcription of the cholesterol 7-alpha-hydroxylase gene. Mol. Endocrinol. 18, 2424-2439.
25. Raynaud, P., Tate, J., Callens, C., Cordi, S., Vandersmissen, P., Carpentier, R., Sempoux, C., Devuyst, O., Pierreux, C. E., Courtoy, P. et al. (2011). A classification of ductal plate malformations based on distinct pathogenic mechanisms of biliary dysmorphogenesis. Hepatology 53, 1959-1966.
26. Shiojiri, N. and Sugiyama, Y. (2004). Immunolocalization of extracellular matrix components and integrins during mouse liver development. Hepatology 40, 346-355.
27. Si-Tayeb, K., Lemaigre, F. P. and Duncan, S. A. (2010). Organogenesis and development of the liver. Dev. Cell 18, 175-189.
28. Song, K. H., Li, T. and Chiang, J. Y. (2006). A Prospero-related homeodomain protein is a novel co-regulator of hepatocyte nuclear factor 4alpha that regulates the cholesterol 7alpha-hydroxylase gene. J. Biol. Chem. 281, 10081-10088.
29. Sosa-Pineda, B., Wigle, J. T. and Oliver, G. (2000). Hepatocyte migration during liver development requires Prox1. Nat. Genet. 25, 254-255.
30. Spence, J. R., Lange, A. W., Lin, S. C., Kaestner, K. H., Lowy, A. M., Kim, I., Whitsett, J. A. and Wells, J. M. (2009). Sox17 regulates organ lineage segregation of ventral foregut progenitor cells. Dev. Cell 17, 62-74.
31. Srinivas, S., Watanabe, T., Lin, C. S., William, C. M., Tanabe, Y., Jessell, T. M. and Costantini, F. (2001). Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev. Biol. 1, 4.
32. Srinivasan, R. S., Geng, X., Yang, Y., Wang, Y., Mukatira, S., Studer, M., Porto, M. P., Lagutin, O. and Oliver, G. (2010). The nuclear hormone receptor Coup-TFII is required for the initiation and early maintenance of Prox1 expression in lymphatic endothelial cells. Genes Dev. 24, 696-707.
33. Strazzabosco, M. and Fabris, L. (2012). Development of the bile ducts: essentials for the clinical hepatologist. J. Hepatol. 56, 1159-1170.
34. Suzuki, A., Sekiya, S., Büscher, D., Izpisúa Belmonte, J. C. and Taniguchi, H. (2008). Tbx3 controls the fate of hepatic progenitor cells in liver development by suppressing p19ARF expression. Development 135, 1589-1595.
35. Szweras, M., Liu, D., Partridge, E. A., Pawling, J., Sukhu, B., Clokie, C., Jahnen-Dechent, W., Tenenbaum, H. C., Swallow, C. J., Grynpas, M. D. et al. (2002). alpha 2-HS glycoprotein/fetuin, a transforming growth factor-beta/bone morphogenetic protein antagonist, regulates postnatal bone growth and remodeling. J. Biol. Chem. 277, 19991-19997.
36. Tanimizu, N. and Miyajima, A. (2004). Notch signaling controls hepatoblast differentiation by altering the expression of liver-enriched transcription factors. J. Cell Sci. 117, 3165-3174.
37. Tanimizu, N., Nishikawa, M., Saito, H., Tsujimura, T. and Miyajima, A. (2003). Isolation of hepatoblasts based on the expression of Dlk/Pref-1. J. Cell Sci. 116, 1775-1786.
38. Tanimizu, N., Miyajima, A. and Mostov, K. E. (2007). Liver progenitor cells develop cholangiocyte-type epithelial polarity in three-dimensional culture. Mol. Biol. Cell 18, 1472-1479.
39. Tanimizu, N., Kikkawa, Y., Mitaka, T. and Miyajima, A. (2012). α1-and α5-containing laminins regulate the development of bile ducts via β1 integrin signals. J. Biol. Chem. 287, 28586-28597.
40. Tchorz, J. S., Kinter, J., Müller, M., Tornillo, L., Heim, M. H. and Bettler, B. (2009). Notch2 signaling promotes biliary epithelial cell fate specification and tubulogenesis during bile duct development in mice. Hepatology 50, 871-879.
41. Uemura, M., Hara, K., Shitara, H., Ishii, R., Tsunekawa, N., Miura, Y., Kurohmaru, M., Taya, C., Yonekawa, H., Kanai-Azuma, M. et al. (2010). Expression and function of mouse Sox17 gene in the specification of gallbladder/bile-duct progenitors during early foregut morphogenesis. Biochem. Biophys. Res. Commun. 391, 357-363.
42. Wang, J., Elghazi, L., Parker, S. E., Kizilocak, H., Asano, M., Sussel, L. and Sosa-Pineda, B. (2004). The concerted activities of Pax4 and Nkx2.2 are essential to initiate pancreatic beta-cell differentiation. Dev. Biol. 266, 178-189.
43. Wang, J., Kilic, G., Aydin, M., Burke, Z., Oliver, G. and Sosa-Pineda, B. (2005). Prox1 activity controls pancreas morphogenesis and participates in the production of "secondary transition" pancreatic endocrine cells. Dev. Biol. 286, 182-194.
44. Westmoreland, J. J., Wang, Q., Bouzaffour, M., Baker, S. J. and Sosa-Pineda, B. (2009). Pdk1 activity controls proliferation, survival, and growth of developing pancreatic cells. Dev. Biol. 334, 285-298.
45. Westmoreland, J. J., Kilic, G., Sartain, C., Sirma, S., Blain, J., Rehg, J., Harvey, N. and Sosa-Pineda, B. (2012). Pancreas-specific deletion of Prox1 affects development and disrupts homeostasis of the exocrine pancreas. Gastroenterology 142, 999-1009, e6.
46. Wigle, J. T. and Oliver, G. (1999). Prox1 function is required for the development of the murine lymphatic system. Cell 98, 769-778.
47. Yamasaki, H., Sada, A., Iwata, T., Niwa, T., Tomizawa, M., Xanthopoulos, K. G., Koike, T. and Shiojiri, N. (2006). Suppression of C/EBPalpha expression in periportal hepatoblasts may stimulate biliary cell differentiation through increased Hnf6 and Hnf1b expression. Development 21, 4233-4243.
48. Zaret, K. S. (2002). Regulatory phases of early liver development: paradigms of organogenesis. Nat. Rev. Genet. 3, 499-512.
49. Zong, Y., Panikkar, A., Xu, J., Antoniou, A., Raynaud, P., Lemaigre, F. and Stanger, B. Z. (2009). Notch signaling controls liver development by regulating biliary differentiation. Development 136, 1727-1739.