Liver development update: New embryo models, cell lineage control, and morphogenesis

Current Opinion in Genetics and Development

Volumn 14, Issue 5, 2004, Pages 582-590

  Lemaigre, Frederic ^a   Zaret, Kenneth S ^b  

^a Ave Hippocrate 75/7529 B 1200 B

^b FOX CHASE CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR;

ANGIOGENESIS; BILE DUCT; CELL FATE; CELL INTERACTION; CELL LINEAGE; EMBRYO; EMBRYO DEVELOPMENT; EPITHELIUM; GENE MUTATION; GENE TARGETING; GENETIC ANALYSIS; GENOME; HEPATIC ARTERY; HEPATOBILIARY SYSTEM; HUMAN; LIVER CELL; LIVER DEVELOPMENT; LIVER SINUSOID; MESODERM; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

ANIMALS; CELL LINEAGE; ENDODERM; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; LIVER; MODELS, BIOLOGICAL; MORPHOGENESIS;

EID: 5444247776     PISSN: 0959437X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.gde.2004.08.004     Document Type: Review

References (74)

1. R. Gualdi, P. Bossard, M. Zheng, Y. Hamada, J.R. Coleman, and K.S. Zaret Hepatic specification of the gut endoderm in vitro: cell signalling and transcriptional control Genes Dev 10 1996 1670 1682
2. J. Jung, M. Zheng, M. Goldfarb, and K.S. Zaret Initiation of mammalian liver development from endoderm by fibroblasts growth factors Science 284 1999 1998 2003
3. N.M. Le Douarin An experimental analysis of liver development Med Biol 53 1975 427 455
4. S. Fukuda-Taira Hepatic induction in the avian embryo: specificity of reactive endoderm and inductive mesoderm J Embryol Exp Morphol 63 1981 111 125
5. J.M. Rossi, N.R. Dunn, Hogan BLM, and K.S. Zaret Distinct mesodermal signals, including BMP's from the septum transversum mesenchyme, are required in combination for hepatogenesis from the endoderm Genes Dev 15 2001 1998 2009
6. K. Matsumoto, H. Yoshitomi, J. Rossant, and K.S. Zaret Liver organogenesis promoted by endothelial cells prior to vascular function Science 294 2001 559 563
7. A. Kamiya, T. Kinoshita, Y. Ito, T. Matsui, Y. Morikawa, E. Senba, K. Nakashima, T. Taga, K. Yoshida, T. Kishimoto, and A. Miyajima Fetal liver development requires a paracrine action of oncostatin M through the gp130 signal transducer EMBO J 18 1999 2127 2136
8. K.S. Zaret Regulatory phases of early liver development: paradigms of organogenesis Nat Rev Genet 3 2002 499 512
9. S.A. Duncan Mechanisms controlling early development of the liver Mech Dev 120 2003 19 33
10. N. Shiojiri Analysis of differentiation of hepatocytes and bile duct cells in developing mouse liver by albumin immunofluorescence Dev Growth Differ 26 1984 555 561
11. N. Shiojiri, S. Inujima, K. Ishikawa, K. Terada, and M. Mori Cell lineage analysis during liver development using the spf(ash)-heterozygous mouse Lab Invest 81 2001 17 25
12. A.M. Zorn, and J. Mason Gene expression in the embryonic Xenopus liver Mech Dev 103 2001 153 157
13. P. Bossard, and K.S. Zaret Repressive and restrictive mesodermal interactions with gut endoderm: possible relation to Meckel's Diverticulum Development 127 2000 4915 4923
14. Y. Chen, K. Jurgens, T. Hollemann, M. Claussen, G. Ramadori, and T. Pieler Cell-autonomous and signal-dependent expression of liver and intestine marker genes in pluripotent precursor cells from Xenopus embryos Mech Dev 120 2003 277 288 This extensive study screened 1500 cDNAs for their liver and gut expression pattern and then tested the induction of selected genes under various perturbations of Xenopus animal cap development in vitro. This paper and [12] go a long way towards establishing the study of liver development in the frog embryo system.
15. A.M. Zorn, K. Butler, and J.B. Gurdon Anterior endomesoderm specification in Xenopus by Wnt/b signalling pathways Dev Biol 209 1999 282 297
16. K.E. Pilcher, and P.A. Krieg Expression of the Wnt inhibitor, sFRP5, in the gut endoderm of Xenopus Gene Expr Patterns 2 2002 369 372
17. K.R. Finley, J. Tennessen, and W. Shawlot The mouse secreted frizzled-related protein 5 gene is expressed in the anterior visceral endoderm and foregut endoderm during early post-implantation development Gene Expr Patterns 3 2003 681 684
18. M.J. Marvin, G. Di Rocco, A. Gardiner, S.M. Bush, and A.B. Lassar Inhibition of Wnt activity induces heart formation from posterior mesoderm Genes Dev 15 2001 316 327
19. S.P. Monga, H.K. Monga, X. Tan, K. Mule, P. Pediaditakis, and G.K. Michalopoulos Beta-catenin antisense studies in embryonic liver cultures: role in proliferation, apoptosis, and lineage specification Gastroenterology 124 2003 202 216
20. S. Suksaweang, C.M. Lin, T.X. Jiang, M.W. Hughes, R.B. Widelitz, and C.M. Chuong Morphogenesis of chicken liver: identification of localized growth zones and the role of beta-catenin/Wnt in size regulation Dev Biol 266 2004 109 122
21. W. Zhang, T.A. Yatskievych, R.K. Baker, and P.B. Antin Regulation of Hex gene expression and initial stages of avian hepatogenesis by Bmp and Fgf signaling Dev Biol 268 2004 312 326
22. T.M. Schultheiss, Burch JBE, and A.B. Lassar A role for bone morphogenetic proteins in the induction of cardiac myogenesis Genes Dev 11 1997 451 462
23. Y. Furuta, D.W. Piston, and B.L. Hogan Bone morphogenetic proteins (BMPs) as regulators of dorsal forebrain development Development 124 1997 2203 2212
24. J.H. Fair, B.A. Cairns, M. Lapaglia, J. Wang, A.A. Meyer, H. Kim, S. Hatada, O. Smithies, and L. Pevny Induction of hepatic differentiation in embryonic stem cells by co-culture with embryonic cardiac mesoderm Surgery 134 2003 189 196 An interesting merge between developmental biology and stem cell differentiation. The authors used GFP-marked ES cells in co-cultures with chick cardiogenic mesodem, the latter being the normal inducer of the liver, and obtained GFP+ cells that expressed endodermal transcription factors and several early liver-specific genes. This study illustrates the feasibility of using embryonic inductive tissue, rather than synthetic culture conditions, to guide stem cell differentiation.
25. Z. Sun, and N. Hopkins vhnf1, the MODY5 and familial GCKD-associated gene, regulates regional specification of the zebrafish gut, pronephros, and hindbrain Genes Dev 15 2001 3217 3229
26. A.N. Mayer, and M.C. Fishman Nil per os encodes a conserved RNA recognition motif protein required for morphogenesis and cytodifferentiation of digestive organs in zebrafish Development 130 2003 3917 3928
27. D. Stafford, and V. Prince Retinoic Acid signaling is required for a critical early step in zebrafish pancreatic development Curr Biol 12 2002 1215 1220 An impressive study that combines genetics with pharmacological approaches. The authors find that RA signaling is required for normal liver and pancreas bud emergence and that zebrafish embryos treated with exogenous RA exhibit an anterior shift in liver and pancreas markers. This is the first study to identify a signal that controls the anterior-posterior position of the liver.
28. S. Korzh, A. Emelyanov, and V. Korzh Developmental analysis of ceruloplasmin gene and liver formation in zebrafish Mech Dev 103 2001 137 139
29. ••].
30. Y. Litingtung, L. Lei, H. Westphal, and C. Chiang Sonic hedgehog is essential to foregut development Nat Genet 20 1998 58 61
31. •] see the liver primordia forming separate from the gut tube. Field et al. also investigate the role of endothelial cells in zebrafish liver development.
32. D.T. Odom, N. Zizlsperger, D.B. Gordon, G.W. Bell, N.J. Rinaldi, H.L. Murray, T.L. Volkert, J. Schreiber, P.A. Rolfe, and D.K. Gifford Control of pancreas and liver gene expression by HNF transcription factors Science 303 2004 1378 1381 A truly impressive study to investigate the binding of HNF1α, HNF4α, and HNF6 transcription factors to promoter sites of >15,000 genes in human hepatocytes and pancreas cells. Details are discussed in the text of this review. The authors' website, listed in Box 1, is worth a visit for anyone interested in the results or contemplating this sort of analysis.
33. J. Li, G. Ning, and S.A. Duncan Mammalian hepatocyte differentiation requires the transcription factor HNF-4alpha Genes Dev 14 2000 464 474
34. C. Plescia, C. Rogler, and L. Rogler Genomic expression analysis implicates Wnt signaling pathway and extracellular matrix alterations in hepatic specification and differentiation of murine hepatic stem cells Differentiation 68 2001 254 269
35. A. Jochheim, A. Cieslak, T. Hillemann, T. Cantz, J. Scharf, M.P. Manns, and M. Ott Multi-stage analysis of differential gene expression in BALB/C mouse liver development by high-density microarrays Differentiation 71 2003 62 72
36. N. Kelley-Loughnane, G.E. Sabla, C. Ley-Ebert, B.J. Aronow, and J.A. Bezerra Independent and overlapping transcriptional activation during liver development and regeneration in mice Hepatology 35 2002 525 534
37. P.M. Petkov, J. Zavadil, D. Goetz, T. Chu, R. Carver, C.E. Rogler, E.P. Bottinger, D.A. Shafritz, and M.D. Dabeva Gene expression pattern in hepatic stem/progenitor cells during rat fetal development using complementary DNA microarrays Hepatology 39 2004 617 627
38. A.A. Sharov, Y. Piao, R. Matoba, D.B. Dudekula, Y. Qian, V. VanBuren, G. Falco, P.R. Martin, C.A. Stagg, and U.C. Bassey Transcriptome analysis of mouse stem cells and early embryos PLoS Biol 1 2003 E74
39. B. McCright, J. Lozier, and T. Gridley A mouse model of Alagille syndrome: Notch2 as a genetic modifier of Jag1 haploinsufficiency Development 129 2002 1075 1082
40. S.S. Nijjar, H.A. Crosby, L. Wallace, S.G. Hubscher, and A.J. Strain Notch receptor expression in adult human liver: a possible role in bile duct formation and hepatic neovascularization Hepatology 34 2001 1184 1192
41. K.M. Loomes, D.B. Taichman, C.L. Glover, P.T. Williams, J.E. Markowitz, D.A. Piccoli, H.S. Baldwin, and R.J. Oakey Characterization of Notch receptor expression in the developing mammalian heart and liver Am J Med Genet 112 2002 181 189
42. C.H. Jensen, E.I. Jauho, E. Santoni-Rugiu, U. Holmskov, B. Teisner, N. Tygstrup, and H.C. Bisgaard Transit-amplifying ductular (oval) cells and their hepatocytic progeny are characterized by a novel and distinctive expression of delta-like protein/preadipocyte factor 1/fetal antigen 1 Am J Pathol 164 2004 1347 1359
43. C. Kohler, A.W. Bell, W.C. Bowen, S.P. Monga, W. Fleig, and G.K. Michalopoulos Expression of Notch-1 and its ligand Jagged-1 in rat liver during liver regeneration Hepatology 39 2004 1056 1065
44. N. Tanimizu, M. Nishikawa, H. Saito, T. Tsujimura, and A. Miyajima Isolation of hepatoblasts based on the expression of Dlk/Pref-1 J Cell Sci 116 2003 1775 1786
45. M. Weinstein, S.P. Monga, Y. Liu, S.G. Brodie, Y. Tang, C. Li, L. Mishra, and C.X. Deng Smad proteins and hepatocyte growth factor control parallel regulatory pathways that converge on beta1-integrin to promote normal liver development Mol Cell Biol 21 2001 5122 5131
46. Y. Tang, V. Katuri, A. Dillner, B. Mishra, C.X. Deng, and L. Mishra Disruption of transforming growth factor-beta signaling in ELF beta-spectrin-deficient mice Science 299 2003 574 577
47. A. Suzuki, Y.W. Zheng Yw, S. Kaneko, M. Onodera, K. Fukao, H. Nakauchi, and H. Taniguchi Clonal identification and characterization of self-renewing pluripotent stem cells in the developing liver J Cell Biol 156 2002 173 184
48. A. Suzuki, A. Iwama, H. Miyashita, H. Nakauchi, and H. Taniguchi Role for growth factors and extracellular matrix in controlling differentiation of prospectively isolated hepatic stem cells Development 130 2003 2513 2524 Using an elegant isolation procedure, the authors cultured cells with hepatic stem cell properties (see [47]) and showed how the cells can be used to address the role of extracellular signals and transcription factors in early steps of hepatic differentiation.
49. F. Clotman, V.J. Lannoy, M. Reber, S. Cereghini, D. Cassiman, P. Jacquemin, T. Roskams, G.G. Rousseau, and F.P. Lemaigre The onecut transcription factor HNF6 is required for normal development of the biliary tract Development 129 2002 1819 1828
50. •] describe how embryonic liver cell lines can be obtained reproducibly. The cells express the set of liver-enriched transcription factors and can be induced to differentiate both in vivo or in vitro under well-defined conditions. The technique of cell isolation can be adapted to transgenic or knockout livers, and thus liver progenitor cell lines can be derived with different genotypes.
51. •] by demonstrating in vivo the bipotent character of the cells isolated from embryonic liver.
52. N. Shiojiri Development and differentiation of bile ducts in the mammalian liver Microsc Res Tech 39 1997 328 335
53. F.P. Lemaigre Development of the biliary tract Mech Dev 120 2003 81 87
54. M.F. Offield, T.L. Jetton, P.A. Labosky, M. Ray, R.W. Stein, M.A. Magnuson, B.L. Hogan, and C.V.E. Wright PDX-1 is required for pancreatic outgrowth and differentiation of the rostral duodenum Development 122 1996 983 995
55. -/- mice. In these mice, the extrahepatic bile ducts differentiate into pancreatic exocrine acini and endocrine islets, the latter most likely developing as a result of ectopic derepression of the proendocrine gene Ngn3. This work shows the unexpected developmental plasticity of the extrahepatic bile ducts and establishes a molecular relationship between the pancreas and the extrahepatic biliary tract.
56. H. Edlund Pancreatic organogenesis-developmental mechanisms and implications for therapy Nat Rev Genet 3 2002 524 532
57. V.V. Kalinichenko, Y. Zhou, D. Bhattacharyya, W. Kim, B. Shin, K. Bambal, and R.H. Costa Haploinsufficiency of the mouse Forkhead Box f1 gene causes defects in gall bladder development J Biol Chem 277 2002 12369 12374
58. V.V. Kalinichenko, D. Bhattacharyya, Y. Zhou, G.A. Gusarova, W. Kim, B. Shin, and R.H. Costa Foxf1+/- mice exhibit defective stellate cell activation and abnormal liver regeneration following CCl4 injury Hepatology 37 2003 107 117
59. C. Coffinier, L. Gresh, L. Fiette, F. Tronche, G. Schutz, C. Babinet, M. Pontoglio, M. Yaniv, and J. Barra Bile system morphogenesis defects and liver dysfunction upon targeted deletion of HNF1beta Development 129 2002 1829 1838
60. T. Watnick, and G. Germino From cilia to cyst Nat Genet 34 2003 355 356
61. T.V. Masyuk, B.Q. Huang, C.J. Ward, A.I. Masyuk, D. Yuan, P.L. Splinter, R. Punyashthiti, E.L. Ritman, V.E. Torres, P.C. Harris, and N.F. LaRusso Defects in cholangiocyte fibrocystin expression and ciliary structure in the PCK rat Gastroenterology 125 2003 1303 1310 Masyuk et al. provide the first description of the primary cilium in cholangiocytes, as well as its abnormal structure in a rat model deficient in fibrocystin expression.
62. L.F. Onuchic, L. Furu, Y. Nagasawa, X. Hou, T. Eggermann, Z. Ren, C. Bergmann, J. Senderek, E. Esquivel, and R. Zeltner PKHD1, the polycystic kidney and hepatic disease 1 gene, encodes a novel large protein containing multiple immunoglobulin-like plexin-transcription-factor domains and parallel beta-helix 1 repeats Am J Hum Genet 70 2002 1305 1317
63. C.J. Ward, M.C. Hogan, S. Rossetti, D. Walker, T. Sneddon, X. Wang, V. Kubly, J.M. Cunningham, R. Bacallao, and M. Ishibashi The gene mutated in autosomal recessive polycystic kidney disease encodes a large, receptor-like protein Nat Genet 30 2002 259 269
64. T. Hiesberger, Y. Bai, X. Shao, B.T. McNally, A.M. Sinclair, X. Tian, S. Somlo, and P. Igarashi Mutation of hepatocyte nuclear factor-1beta inhibits Pkhd1 gene expression and produces renal cysts in mice J Clin Invest 113 2004 814 825
65. L. Gresh, E. Fischer, A. Reimann, M. Tanguy, S. Garbay, X. Shao, T. Hiesberger, L. Fiette, P. Igarashi, M. Yaniv, and M. Pontoglio A transcriptional network in polycystic kidney disease EMBO J 23 2004 1657 1668 The phenotype of a kidney-specific inactivation of HNF1β is here studied in detail. The lack of HNF1β results in reduced expression of cystic disease genes, which are shown by chromatin immunoprecipitations to be direct targets of HNF1β. The same transcriptional network is likely to function in biliary cells.
66. J.P. Drenth, J.A. Martina, R.H. Te Morsche, J.B. Jansen, and J.S. Bonifacino Molecular characterization of hepatocystin, the protein that is defective in autosomal dominant polycystic liver disease Gastroenterology 126 2004 1819 1827
67. S. Davila, L. Furu, A.G. Gharavi, X. Tian, T. Onoe, Q. Qian, A. Li, Y. Cai, P.S. Kamath, and B.F. King Mutations in SEC63 cause autosomal dominant polycystic liver disease Nat Genet 36 2004 575 577
68. D. Huangfu, A. Liu, A.S. Rakeman, N.S. Murcia, L. Niswander, and K.V. Anderson Hedgehog signalling in the mouse requires intraflagellar transport proteins Nature 426 2003 83 87 The paper provides evidence that intraflagellar transport proteins, which are associated with the primary cilium, are required for Hedgehog signaling in the nervous system. This works opens new questions as to the possible role of Hedgehog in biliary tract development.
69. L. Libbrecht, D. Cassiman, V. Desmet, and T. Roskams The correlation between portal myofibroblasts and development of intrahepatic bile ducts and arterial branches in human liver Liver 22 2002 252 258
70. T.V. Masyuk, E.L. Ritman, and N.F. LaRusso Hepatic artery and portal vein remodeling in rat liver: vascular response to selective cholangiocyte proliferation Am J Pathol 162 2003 1175 1182 Using a digital three-dimensional reconstruction of the vascular and biliary tree of the liver, the authors show how portal vein and hepatic artery branch proliferation parallels bile duct proliferation.
71. F. Clotman, L. Libbrecht, L. Gresh, M. Yaniv, T. Roskams, G.G. Rousseau, and F.P. Lemaigre Hepatic artery malformations associated with a primary defect in intrahepatic bile duct development J Hepatol 39 2003 686 692 The paper provides the first description of hepatic artery branch development in mice. The authors also studied hepatic artery development in mice deficient in HNF6 or HNF1β and showed the requirement for normal intrahepatic bile duct development to allow hepatic artery formation. The transgenic mice displayed arterial anomalies similar to those found in human Meckel and Jeune syndromes, two genetic diseases with ductal plate malformations, and thus represent a new model to investigate the mechanism of hepatic artery formation.
72. S.A. Duncan, A. Nagy, and W. Chan Murine gastrulation requires HNF-4 regulated gene expression in the visceral endoderm: tetraploid rescue of Hnf-4(-/-) embryos Development 124 1997 279 287
73. F. Parviz, C. Matullo, W.D. Garrison, L. Savatski, J.W. Adamson, G. Ning, K.H. Kaestner, J.M. Rossi, K.S. Zaret, and S.A. Duncan Hepatocyte nuclear factor 4alpha controls the development of a hepatic epithelium and liver morphogenesis Nat Genet 34 2003 292 296 We made a conditional knockout of the HNF4α gene in fetal liver and reported deficiencies in hepatocyte differentiation and epithelialization, and a consequent failure to develop a sinusoidal endothelium. They also showed that ectopic expression of HNF4α in fibroblast cells is sufficient to induce epithelialization, but insufficient to induce liver-specific genes. Thus, HNF4α must be integrated into the network of other hepatic nuclear factors to promote hepatic differentiation.
74. N. Tanimizu, and A. Miyajima Notch signaling controls hepatoblast differentiation by altering the expression of liver-enriched transcription factors J Cell Sci 117 2004 3165 3174