Gastroenterology
Volume 136, Issue 7 , Pages 2325-2333 , June 2009

Intrahepatic Bile Ducts Develop According to a New Mode of Tubulogenesis Regulated by the Transcription Factor SOX9

  • Aline Antoniou

      Affiliations

    • Université catholique de Louvain, de Duve Institute, Brussels, Belgium
    • ,
  • Peggy Raynaud

      Affiliations

    • Université catholique de Louvain, de Duve Institute, Brussels, Belgium
    • ,
  • Sabine Cordi

      Affiliations

    • Université catholique de Louvain, de Duve Institute, Brussels, Belgium
    • ,
  • Yiwei Zong

      Affiliations

    • Division of Gastroenterology, Abramson Family Cancer Research Institute, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania
    • ,
  • François Tronche

      Affiliations

    • CNRS UMR 7148, Institut de Biologie, Collège de France, Paris, France
    • ,
  • Ben Z. Stanger

      Affiliations

    • Division of Gastroenterology, Abramson Family Cancer Research Institute, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania
    • ,
  • Patrick Jacquemin

      Affiliations

    • Université catholique de Louvain, de Duve Institute, Brussels, Belgium
    • ,
  • Christophe E. Pierreux

      Affiliations

    • Université catholique de Louvain, de Duve Institute, Brussels, Belgium
    • ,
  • Frederic Clotman

      Affiliations

    • Université catholique de Louvain, de Duve Institute, Brussels, Belgium
    • ,
  • Frederic P. Lemaigre

      Affiliations

    • Université catholique de Louvain, de Duve Institute, Brussels, Belgium
    • Corresponding Author InformationReprint requests Address requests for reprints to: F. P. Lemaigre, MD, Université catholique de Louvain, de Duve Institute, Avenue Hippocrate 75/7529, 1200 Brussels, Belgium. fax: (32) 2 764 7507

Received 28 August 2008 ,Accepted 6 February 2009.

References 

  1. Kamath BM, Piccoli DA. Heritable disorders of the bile ducts. Gastroenterol Clin North Am. 2003;32:857–875
  2. Lemaigre F, Zaret KS. Liver development update: new embryo models, cell lineage control, and morphogenesis. Curr Opin Genet Dev. 2004;14:582–590
  3. Zhao R, Duncan SA. Embryonic development of the liver. Hepatology. 2005;41:956–967
  4. Shiojiri N. The origin of intrahepatic bile duct cells in the mouse. J Embryol Exp Morphol. 1984;79:25–39
  5. Van Eyken P, Sciot R, Callea F, et al. The development of the intrahepatic bile ducts in man: a keratin-immunohistochemical study. Hepatology. 1988;8:1586–1595
  6. Crawford JM. Development of the intrahepatic biliary tree. Semin Liver Dis. 2002;22:213–226
  7. Lemaigre FP. Development of the biliary tract. Mech Dev. 2003;120:81–87
  8. Clotman F, Lannoy VJ, Reber M, et al. The Onecut transcription factor Hnf6 is required for normal development of the biliary tract. Development. 2002;129:1819–1828
  9. Clotman F, Jacquemin P, Plumb-Rudewiez N, et al. Control of liver cell fate decision by a gradient of TGFβ signaling modulated by Onecut transcription factors. Genes Dev. 2005;19:1849–1854
  10. Hunter MP, Wilson CM, Jiang X, et al. The homeobox gene Hhex is essential for proper hepatoblast differentiation and bile duct morphogenesis. Dev Biol. 2007;308:355–367
  11. Yamasaki H, Sada A, Iwata T, et al. Suppression of C/EBPα expression in periportal hepatoblasts may stimulate biliary cell differentiation through increased Hnf6 and Hnf1β expression. Development. 2006;133:4233–4243
  12. Coffinier C, Gresh L, Fiette L, et al. Bile system morphogenesis defects and liver dysfunction upon targeted deletion of HNF1β. Development. 2002;129:1829–1838
  13. Decaens T, Godard C, de Reyniès A, et al. Stabilization of β-catenin affects mouse embryonic liver growth and hepatoblast fate. Hepatology. 2008;47:247–258
  14. Tan X, Yuan Y, Zeng G, et al. Beta-catenin deletion in hepatoblasts disrupts hepatic morphogenesis and survival during mouse development. Hepatology. 2008;47:1667–1679
  15. Kodama Y, Hijikata M, Kageyama R, et al. The role of notch signaling in the development of intrahepatic bile ducts. Gastroenterology. 2004;127:1775–1786
  16. Lozier J, McCright B, Gridley T. Notch signaling regulates bile duct morphogenesis in mice. PLoS One. 2008;3:e1851
  17. Geisler F, Nagl F, Mazur PK, et al. Liver-specific inactivation of Notch2, but not Notch1, compromises intrahepatic bile duct development in mice. Hepatology. 2008;48:607–616
  18. Bastide P, Darido C, Pannequin J, et al. Sox9 regulates cell proliferation and is required for Paneth cell differentiation in the intestinal epithelium. J Cell Biol. 2007;178:635–648
  19. Mori-Akiyama Y, van den Born M, van Es JH, et al. SOX9 is required for the differentiation of Paneth cells in the intestinal epithelium. Gastroenterology. 2007;133:539–546
  20. Seymour PA, Feude KK, Tran MN, et al. SOX9 is required for maintenance of the pancreatic progenitor cell pool. Proc Natl Acad Sci U S A. 2007;104:1865–1870
  21. Kist R, Schrewe H, Balling R, et al. Conditional inactivation of Sox9: a mouse model for campomelic dysplasia. Genesis. 2002;32:121–123
  22. Kellendonk C, Opherk C, Anlag K, et al. Hepatocyte-specific expression of Cre recombinase. Genesis. 2000;26:151–153
  23. Jacquemin P, Durviaux SM, Jensen J, et al. Transcription factor hepatocyte nuclear factor 6 regulates pancreatic endocrine cell differentiation and controls expression of the proendocrine gene ngn3. Mol Cell Biol. 2000;20:4445–4454
  24. van Eyll JM, Pierreux CE, Lemaigre FP, et al. Shh-dependent differentiation of intestinal tissue from embryonic pancreas by activin A. J Cell Sci. 2004;117:2077–2086
  25. Margagliotti S, Clotman F, Pierreux CE, et al. The Onecut transcription factors HNF-6/OC-1 and OC-2 regulate early liver expansion by controlling hepatoblast migration. Dev Biol. 2007;311:579–589
  26. Plumb-Rudewiez N, Clotman F, Strick-Marchand H, et al. The transcription factor HNF-6/OC-1 inhibits the stimulation of the HNF-3α/Foxa1 gene by TGFβ in mouse liver. Hepatology. 2004;40:1266–1274
  27. Lubarsky B, Krasnow MA. Tube morphogenesis: making and shaping biological tubes. Cell. 2003;112:19–28
  28. Martin-Belmonte F, Mostov KE. Regulation of cell polarity during epithelial morphogenesis. Curr Opin Cell Biol. 2008;20:227–234
  29. Hogan BL, Kolodziej PA. Molecular mechanisms of tubulogenesis. Nat Rev Genet. 2002;3:513–523
  30. Chung SY, Andrew DJ. The formation of epithelial tubes. J Cell Sci. 2008;121:3501–3504
  31. Lorena D, Darby IA, Gadeau A-P. Osteopontin expression in normal and fibrotic liver (Altered liver healing in osteopontin-deficient mice). J Hepatol. 2006;44:383–390
  32. Tanimizu N, Miyajima A, Mostov KE. Liver progenitor cells develop cholangiocyte-type epithelial polarity in three-dimensional culture. Mol Biol Cell. 2007;18:1472–1479
  33. Hanley KP, Oakley F, Sugden S, et al. Ectopic SOX9 mediates extracellular matrix deposition characteristic of organ fibrosis. J Biol Chem. 2008;283:14063–14071

 Conflicts of interest The authors disclose no conflicts.

 Funding Supported by the Interuniversity Attraction Poles Program (Belgian Science Policy; to F.L.), the D.G. Higher Education and Scientific Research of the French Community of Belgium (to F.L.), the Alphonse and Jean Forton Fund (to F.L.), and the Fund for Scientific Medical Research (to F.L.); and by NIH grant DK076583 (to B.Z.S.).A.A. and P.R. hold fellowships from the Université catholique de Louvain. F.C., C.P., and P.J. are research associates of the F.R.S.-F.N.R.S.

PII: S0016-5085(09)00300-X

doi: 10.1053/j.gastro.2009.02.051

Gastroenterology
Volume 136, Issue 7 , Pages 2325-2333 , June 2009

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