Embryology of the Liver and Intrahepatic Biliary Tract
Frédéric P. Lemaigre
Search for more papers by this authorFrédéric P. Lemaigre
Search for more papers by this authorJuan Rodés MD
Director General, Hospital Clinic; Professor of Medicine, University of Barcelona, Barcelona, Spain
Search for more papers by this authorJean-Pierre Benhamou MD
Professor of Hepatology, Université Denis Diderot Paris 7, Assistance Publique — Hôpitaux de Paris and Inserm U773, Service d'Hépatologie, Hôpital Beaujon, Clichy, France
Search for more papers by this authorAndres T. Blei MD
Professor of Medicine and Surgery, Northwestern University, Feinberg School of Medicine, Chicago, IL, USA
Search for more papers by this authorJürg Reichen MD
Professor of Medicine, University of Bern; Chief of Hepatology, University Hospital, Bern, Switzerland
Search for more papers by this authorMario Rizzetto MD
Professor of Gastroenterology, University of Turin, Turin, Italy
Search for more papers by this authorSummary
This chapter contains section titled:
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From Endoderm to Hepatoblast
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Expansion of the Liver Bud
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Differentiation of Hepatoblasts into Hepatocytes or Biliary Cells
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Maturation of Hepatocytes
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Development of the Intrahepatic Bile Ducts
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Vascular Development in the Liver
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References
References
- Wells JM, Melton DA (1999) Vertebrate endoderm development. Annu Rev Cell Dev Biol 15, 393–410.
- Grapin-Botton A, Melton DA (2000) Endoderm development: from patterning to organogenesis. Trends Genet 16, 124–130.
- Zaret KS (2002) Regulatory phases of early liver development: paradigms of organogenesis. Nature Rev Genet 3, 499–512.
- Lemaigre F, Zaret KS (2004) Liver development update: new embryo models, cell lineage control, and morphogenesis. Curr Opin Genet Dev 14, 582–590.
- Zhao R, Duncan SA (2005) Embryonic development of the liver. Hepatology 41, 956–967.
-
Shiojiri N
(1997)
Development and differentiation of bile ducts in the mammalian liver.
Microsc Res Tech
39,
328–335.
10.1002/(SICI)1097-0029(19971115)39:4<328::AID-JEMT3>3.0.CO;2-D CAS PubMed Web of Science® Google Scholar
-
Lemaigre FP
(2003)
Development of the biliary tract.
Mech Dev
20,
81–87.
10.1016/S0925-4773(02)00334-9 Google Scholar
- Costa RH, Kalinichenko VV, Holterman AX et al. (2003) Transcription factors in liver development, differentiation, and regeneration. Hepatology 38, 1331–1347.
- Schrem H, Klempnauer J, Borlak J (2002) Liver-enriched transcription factors in liver function and development. Part I: the hepatocyte nuclear factor network and liver-specific gene expression. Pharmacol Rev 54, 129–158.
- Schrem H, Klempnauer J, Borlak J (2004) Liver-enriched transcription factors in liver function and development. Part II: the C/EBPs and D site-binding protein in cell cycle control, carcinogenesis, circadian gene regulation, liver regeneration, apoptosis, and liver-specific gene regulation. Pharmacol Rev 56, 291–330.
- Gualdi R, Bossard P, Zheng M et al. (1996) Hepatic specification of the gut endoderm in vitro: cell signaling and transcriptional control. Genes Dev 10, 1670–1682.
- Bossard P, Zaret KS (1998) GATA transcription factors as potentiators of gut endoderm differentiation. Development 125, 4909–4917.
- Cirillo LA, Lin FR, Cuesta I et al. (2002) Opening of compacted chromatin by early developmental transcription factors HNF3 (FoxA) and GATA-4. Mol Cell 9, 279–289.
- LeDouarin NM (1975) An experimental analysis of liver development. Med Biol 53, 427–455.
- Jung J, Zheng M, Goldfarb M et al. (1999) Initiation of mammalian liver development from endoderm by fibroblast growth factors. Science 284, 1998–2003.
- Serls AE, Doherty S, Parvatiyar P et al. (2005) Different thresholds of fibroblast growth factors pattern the ventral foregut into liver and lung. Development 132, 35–47.
- Rossi JM, Dunn NR, Hogan BL et al. (2001) Distinct mesodermal signals, including BMPs from the septum transversum mesenchyme, are required in combination for hepatogenesis from the endoderm. Genes Dev 15, 1998–2009.
- Keng VW, Yagi H, Ikawa M et al. (2000) Homeobox gene Hex is essential for onset of mouse embryonic liver development and differentiation of the monocyte lineage. Biochem Biophys Res Commun 276, 1155–1161.
- Martinez Barbera JP, Clements M, Thomas P et al. (2000) The homeobox gene Hex is required in definitive endodermal tissues for normal forebrain, liver and thyroid formation. Development 127, 2433–2445.
- Sosa-Pineda B, Wigle JT, Oliver G (2000) Hepatocyte migration during liver development requires Prox1. Nature Genet 25, 254–255.
- Zhao R, Watt AJ, Li J et al. (2005) GATA6 is essential for embryonic development of the liver but dispensable for early heart formation. Mol Cell Biol 25, 2622–2631.
- Matsumoto K, Yoshitomi H, Rossant J et al. (2001) Liver organogenesis promoted by endothelial cells prior to vascular function. Science 294, 559–563.
- Krupczak-Hollis K, Wang X, Kalinichenko VV et al. (2004) The mouse Forkhead Box m1 transcription factor is essential for hepatoblast mitosis and development of intrahepatic bile ducts and vessels during liver morphogenesis. Dev Biol 276, 74–88.
- Reimold AM, Etkin A, Clauss I et al. (2000) An essential role in liver development for transcription factor XBP-1. Genes Dev 14, 152–157.
- Monga SP, Monga HK, Tan X et al. (2003) Beta-catenin antisense studies in embryonic liver cultures: role in proliferation, apoptosis, and lineage specification. Gastroenterology 124, 202–216.
- Hentsch B, Lyons I, Li R et al. (1996) Hlx homeo box gene is essential for an inductive tissue interaction that drives expansion of embryonic liver and gut. Genes Dev 10, 70–79.
- Schmidt C, Bladt F, Goedecke S et al. (1995) Scatter factor/hepatocyte growth factor is essential for liver development. Nature 373, 699–702.
- Uehara Y, Minowa O, Mori C et al. (1995) Placental defect and embryonic lethality in mice lacking hepatocyte growth factor/scatter factor. Nature 373, 702–705.
- Bladt F, Riethmacher D, Isenmann S et al. (1995) Essential role for the c-met receptor in the migration of myogenic precursor cells into the limb bud. Nature 376, 768–771.
- Hilberg F, Aguzzi A, Howells N et al. (1993) C-jun is essential for normal mouse development and hepatogenesis. Nature 365, 179–181.
- Hussain SZ, Sneddon T, Tan X et al. (2004) Wnt impacts growth and differentiation in ex vivo liver development. Exp Cell Res 292, 157–169.
- Weinstein M, Monga SP, Liu Y et al. (2001) Smad proteins and hepatocyte growth factor control parallel regulatory pathways that converge on beta1-integrin to promote normal liver development. Mol Cell Biol 21, 5122–5131
- Fassler R, Meyer M (1995) Consequences of lack of beta 1 integrin gene expression in mice. Genes Dev 9, 1896–1908.
- Beg AA, Sha WC, Bronson RT et al. (1995) Embryonic lethality and liver degeneration in mice lacking the RelA component of NF-KB. Nature 376, 167–170.
- Li Q, Van Antwerp D, Mercurio F et al. (1999) Severe liver degeneration in mice lacking the IkappaB kinase 2 gene. Science 284, 321–325.
- Li ZW, Chu W, Hu Y et al. (1999) The IKKbeta subunit of IkappaB kinase (IKK) is essential for nuclear factor kappaB activation and prevention of apoptosis. J Exp Med 189, 1839–1845.
- Rudolph D, Yeh WC, Wakeham A et al. (2000) Severe liver degeneration and lack of NF-kappaB activation in NEMO/IKKgamma-deficient mice. Genes Dev 14, 854–862.
- Doi TS, Marino MW, Takahashi T et al. (1999) Absence of tumor necrosis factor rescues RelA-deficient mice from embryonic lethality. Proc Natl Acad Sci USA 96, 2994–2999.
- Rosenfeld ME, Prichard L, Shiojiri N et al. (2000) Prevention of hepatic apoptosis and embryonic lethality in RelA/TNFR-1 double knockout mice. Am J Pathol 156, 997–1007.
- Li J, Ning G, Duncan SA (2000) Mammalian hepatocyte differentiation requires the transcription factor HNF-4alpha. Genes Dev 14, 464–474.
- Clotman F, Lannoy VJ, Reber M et al. (2002) The onecut transcription factor HNF6 is required for normal development of the biliary tract. Development 129, 1819–1828.
- Coffinier C, Gresh L, Fiette L et al. (2002) Bile system morphogenesis defects and liver dysfunction upon targeted deletion of HNF1beta. Development 129, 1829–1838.
- Plumb-Rudewiez N, Clotman F, Strick-Marchand H et al. (2004) The transcription factor HNF-6/OC-1 inhibits the stimulation of the HNF-3oc/Foxa1 gene by TGF|3 in mouse liver. Hepatology 40, 1266–1274.
- Clotman F, Jacquemin P, Plumb-Rudewiez N et al. (2005) Control of liver cell fate decision by a gradient of TGF|3 signaling modulated by Onecut transcription factors. Genes Dev 19, 1849–1854.
- McCright B, Lozier J, Gridley T (2002) A mouse model of Alagille syndromeP: Notch2 as a genetic modifier of Jag1 haploinsufficiency. Development 129, 1075–1082.
- Tanimizu N, Miyajima A (2004) Notch signaling controls hepatoblast differentiation by altering the expression of liver-enriched transcription factors. J Cell Sci 117, 3165–3174.
- Couvelard A, Bringuier AF, Dauge MC et al. (1998) Expression of integrins during liver organogenesis in humans. Hepatology 27, 839–847.
- Odom DT, Zizlsperger N, Gordon DB et al. (2004) Control of pancreas and liver gene expression by HNF transcription factors. Science 303, 1378–1381.
- Parviz F, Matullo C, Garrison WD et al. (2003) Hepatocyte nuclear factor 4alpha controls the development of a hepatic epithelium and liver morphogenesis. Nature Genet 34, 292–296.
- Lekstrom-Himes J, Xanthopoulos KG (1998) Biological role of the CCAAT/enhancer-binding protein family of transcription factors. J Biol Chem 273, 28545–28548.
- Jacquemin P, Durviaux SM, Jensen J et al. (2000) Transcription factor hepatocyte nuclear factor 6 regulates pancreatic endocrine cell differentiation and controls expression of the proendocrine gene ngn3. Mol Cell Biol 20, 4445–4454.
- Lannoy VJ, Decaux JF, Pierreux CE et al. (2002) Liver glucokinase gene expression is controlled by the onecut transcription factor hepatocyte nuclear factor-6. Diabetologia 45, 1136–1141.
- Kinoshita T, Miyajima A (2002) Cytokine regulation of liver development. Biochim Biophys Acta 1592, 303–312.
- Kamiya A, Kinoshita T, Ito Y et al. (1999) Fetal liver development requires a paracrine action of oncostatin M through the gp130 signal transducer. EMBO J 18, 2127–2136.
- Kinoshita T, Sekiguchi T, Xu MJ et al. (1999) Hepatic differentiation induced by oncostatin M attenuates fetal liver haematopoiesis. Proc Natl Acad Sci USA 96, 7265–7270.
- Anzai H, Kamiya A, Shirato H et al. (2003) Impaired differentiation of fetal hepatocytes in homozygous jumonji mice. Mech Dev 120, 791–800.
- Bouzin C, Clotman F, Renauld JC et al. (2003) The onecut transcription factor hepatocyte nuclear factor-6 controls B lymphopoiesis in fetal liver. J Immunol 171, 1297–1303.
- Kodama Y, Hijikata M, Kageyama R et al. (2004) The role of notch signaling in the development of intrahepatic bile ducts. Gastroenterology 127, 1775–1786.
- Fabris L, Strazzabosco M, Crosby HA et al. (2000) Characterization and isolation of ductular cells coexpressing neural cell adhesion molecule and Bcl-2 from primary cholangiopathies and ductal plate malformations. Am J Pathol 156, 1599–1612.
- Terada T, Nakanuma Y (1995) Detection of apoptosis and expression of apoptosis-related proteins during human intrahepatic bile duct development. Am J Pathol 146, 67–74.
- Terada T, Nakanuma Y (1994) Expression of tenascin, type IV collagen and laminin during human intrahepatic bile duct development and in intrahepatic cholangiocarcinoma. Histopathology 25, 143–150.
- Masyuk TV, Huang BQ, Ward CJ et al. (2003) Defects in cholangio-cyte fibrocystin expression and ciliary structure in the PCK rat. Gastroenterology 125, 1303–1310.
- Moser M, Matthiesen S, Kirfel J et al. (2005) A mouse model for cystic biliary dysgenesis in autosomal recessive polycystic kidney disease (ARPKD). Hepatology 41, 1113–1121.
- Lassau JP, Bastian D (1983) Organogenesis of the venous structures of the human liver: a hemodynamic theory. Anat Clin 5, 97–102.
- Gouysse G, Couvelard A, Frachon S et al. (2002) Relationship between vascular development and vascular differentiation during liver organogenesis in humans. J Hepatol 37, 730–740.
- Couvelard A, Scoazec JY, Dauge, MC et al. (1996) Structural and functional differentiation of sinusoidal endothelial cells during liver organogenesis in humans. Blood 87, 4568–4580.
- Wandzioch E, Kolterud A, Jacobsson M et al. (2004) Lhx2-/- mice develop liver fibrosis. Proc Natl Acad Sci USA 101, 16549–16554.
- Geerts A (2001) History, heterogeneity, developmental biology, and functions of quiescent hepatic stellate cells. Semin Liver Dis 21, 311–335
- Clotman F, Libbrecht L, Gresh L et al. (2003) Hepatic artery malformations associated with a primary defect in intrahepatic bile duct development. J Hepatol 39, 686–692.
- Libbrecht L, Cassiman D, Desmet V et al. (2002) The correlation between portal myofibroblasts and development of intrahepatic bile ducts and arterial branches in human liver. Liver 22, 252–258.
- Masyuk TV, Ritman EL, LaRusso NF (2003) Hepatic artery and portal vein remodeling in rat liver: vascular response to selective cholangio-cyte proliferation. Am J Pathol 162, 1175–1182.