Beta-catenin signaling in hepatic development and progenitors: Which way does the WNT blow?

Developmental Dynamics

Volumn 240, Issue 3, 2011, Pages 486-500

  Lade, Abigale G ^a   Monga, Satdarshan P S ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Beta catenin; Cancer; Differentiation; Liver development; Proliferation; Stem cells; Wnt

Indexed keywords

BETA CATENIN; FRIZZLED PROTEIN; PROTEIN TYROSINE KINASE; WNT PROTEIN;

CARCINOGENESIS; CELL DIFFERENTIATION; CELL EXPANSION; CELL MATURATION; CELL PROLIFERATION; DNA FLANKING REGION; ENDODERM; EXPERIMENTAL ANIMAL; HOMEOSTASIS; HUMAN; LIVER DEVELOPMENT; LIVER REGENERATION; MORPHOGENESIS; NONHUMAN; PATHOPHYSIOLOGY; PERINATAL PERIOD; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; STEM CELL;

ANIMALS; BETA CATENIN; HUMANS; LIVER; STEM CELLS; WNT PROTEINS;

DANIO RERIO;

EID: 79951642278     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.22522     Document Type: Review

References (178)

1. Aberle H, Butz S, Stappert J, Weissig H, Kemler R, Hoschuetzky H. 1994. Assembly of the cadherin-catenin complex in vitro with recombinant proteins. J Cell Sci 107: 3655-3663.
2. Aberle H, Schwartz H, Hoschuetzky H, Kemler R. 1996. Single amino acid substitutions in proteins of the armadillo gene family abolish their binding to alpha-catenin. J Biol Chem 271: 1520-1526.
3. Aberle H, Bauer A, Stappert J, Kispert A, Kemler R. 1997. beta-catenin is a target for the ubiquitin-proteasome pathway. Embo J 16: 3797-3804.
4. Ang SL, Wierda A, Wong D, Stevens KA, Cascio S, Rossant J, Zaret KS. 1993. The formation and maintenance of the definitive endoderm lineage in the mouse: involvement of HNF3/forkhead proteins. Development 119: 1301-1315.
5. Aoki TO, David NB, Minchiotti G, Saint-Etienne L, Dickmeis T, Persico GM, Strahle U, Mourrain P, Rosa FM. 2002. Molecular integration of casanova in the Nodal signalling pathway controlling endoderm formation. Development 129: 275-286.
6. Apte U, Zeng G, Muller P, Tan X, Micsenyi A, Cieply B, Dai C, Liu Y, Kaestner KH, Monga SP. 2006. Activation of Wnt/beta-catenin pathway during hepatocyte growth factor-induced hepatomegaly in mice. Hepatology 44: 992-1002.
7. Apte U, Zeng G, Thompson MD, Muller P, Micsenyi A, Cieply B, Kaestner KH, Monga SP. 2007. beta-Catenin is critical for early postnatal liver growth. Am J Physiol Gastrointest Liver Physiol 292: G1578-1585.
8. Apte U, Thompson MD, Cui S, Liu B, Cieply B, Monga SP. 2008. Wnt/beta-catenin signaling mediates oval cell response in rodents. Hepatology 47: 288-295.
9. Arceci RJ, King AA, Simon MC, Orkin SH, Wilson DB. 1993. Mouse GATA-4: a retinoic acid-inducible GATA-binding transcription factor expressed in endodermally derived tissues and heart. Mol Cell Biol 13: 2235-2246.
10. Arnold SJ, Hofmann UK, Bikoff EK, Robertson EJ. 2008. Pivotal roles for eomesodermin during axis formation, epithelium-to-mesenchyme transition and endoderm specification in the mouse. Development 135: 501-511.
11. Barrow JR, Howell WD, Rule M, Hayashi S, Thomas KR, Capecchi MR, McMahon AP. 2007. Wnt3 signaling in the epiblast is required for proper orientation of the anteroposterior axis. Dev Biol 312: 312-320.
12. Battle MA, Konopka G, Parviz F, Gaggl AL, Yang C, Sladek FM, Duncan SA. 2006. Hepatocyte nuclear factor 4alpha orchestrates expression of cell adhesion proteins during the epithelial transformation of the developing liver. Proc Natl Acad Sci USA 103: 8419-8424.
13. Bayha E, Jorgensen MC, Serup P, Grapin-Botton A. 2009. Retinoic acid signaling organizes endodermal organ specification along the entire antero-posterior axis. PLoS One 4: e5845.
14. Behrens J, von Kries JP, Kuhl M, Bruhn L, Wedlich D, Grosschedl R, Birchmeier W. 1996. Functional interaction of beta-catenin with the transcription factor LEF-1. Nature 382: 638-642.
15. Ben-Haim N, Lu C, Guzman-Ayala M, Pescatore L, Mesnard D, Bischofberger M, Naef F, Robertson EJ, Constam DB. 2006. The nodal precursor acting via activin receptors induces mesoderm by maintaining a source of its convertases and BMP4. Dev Cell 11: 313-323.
16. Benhamouche S, Decaens T, Godard C, Chambrey R, Rickman DS, Moinard C, Vasseur-Cognet M, Kuo CJ, Kahn A, Perret C, Colnot S. 2006. Apc tumor suppressor gene is the "zonation-keeper" of mouse liver. Dev Cell 10: 759-770.
17. Berg T, Rountree CB, Lee L, Estrada J, Sala FG, Choe A, Veltmaat JM, De Langhe S, Lee R, Tsukamoto H, Crooks GM, Bellusci S, Wang KS. 2007. Fibroblast growth factor 10 is critical for liver growth during embryogenesis and controls hepatoblast survival via beta-catenin activation. Hepatology 46: 1187-1197.
18. Bhanot P, Brink M, Samos CH, Hsieh JC, Wang Y, Macke JP, Andrew D, Nathans J, Nusse R. 1996. A new member of the frizzled family from Drosophila functions as a Wingless receptor. Nature 382: 225-230.
19. Bi Y, Huang J, He Y, Zhu GH, Su Y, He BC, Luo J, Wang Y, Kang Q, Luo Q, Chen L, Zuo GW, Jiang W, Liu B, Shi Q, Tang M, Zhang BQ, Weng Y, Huang A, Zhou L, Feng T, Luu HH, Haydon RC, He TC, Tang N. 2009. Wnt antagonist SFRP3 inhibits the differentiation of mouse hepatic progenitor cells. J Cell Biochem 108: 295-303.
20. Bort R, Signore M, Tremblay K, Martinez Barbera JP, Zaret KS. 2006. Hex homeobox gene controls the transition of the endoderm to a pseudostratified, cell emergent epithelium for liver bud development. Dev Biol 290: 44-56.
21. Brembeck FH, Schwarz-Romond T, Bakkers J, Wilhelm S, Hammerschmidt M, Birchmeier W. 2004. Essential role of BCL9-2 in the switch between beta-catenin's adhesive and transcriptional functions. Genes Dev 18: 2225-2230.
22. Brennan J, Lu CC, Norris DP, Rodriguez TA, Beddington RS, Robertson EJ. 2001. Nodal signalling in the epiblast patterns the early mouse embryo. Nature 411: 965-969.
23. Brennan J, Norris DP, Robertson EJ. 2002. Nodal activity in the node governs left-right asymmetry. Genes Dev 16: 2339-2344.
24. Burke ZD, Tosh D. 2006. The Wnt/beta-catenin pathway: master regulator of liver zonation? Bioessays 28: 1072-1077.
25. Butler SL, Dong H, Cardona D, Jia M, Zheng R, Zhu H, Crawford JM, Liu C. 2008. The antigen for Hep Par 1 antibody is the urea cycle enzyme carbamoyl phosphate synthetase 1. Lab Invest 88: 78-88.
26. Cheng W, Guo L, Zhang Z, Soo HM, Wen C, Wu W, Peng J. 2006. HNF factors form a network to regulate liver-enriched genes in zebrafish. Dev Biol 294: 482-496.
27. Clements D, Cameleyre I, Woodland HR. 2003. Redundant early and overlapping larval roles of Xsox17 subgroup genes in Xenopus endoderm development. Mech Dev 120: 337-348.
28. Clotman F, Lannoy VJ, Reber M, Cereghini S, Cassiman D, Jacquemin P, Roskams T, Rousseau GG, Lemaigre FP. 2002. The onecut transcription factor HNF6 is required for normal development of the biliary tract. Development 129: 1819-1828.
29. Clotman F, Jacquemin P, Plumb-Rudewiez N, Pierreux CE, Van der Smissen P, Dietz HC, Courtoy PJ, Rousseau GG, Lemaigre FP. 2005. Control of liver cell fate decision by a gradient of TGF beta signaling modulated by Onecut transcription factors. Genes Dev 19: 1849-1854.
30. Coffinier C, Gresh L, Fiette L, Tronche F, Schutz G, Babinet C, Pontoglio M, Yaniv M, Barra J. 2002. Bile system morphogenesis defects and liver dysfunction upon targeted deletion of HNF1beta. Development 129: 1829-1838.
31. Colletti M, Cicchini C, Conigliaro A, Santangelo L, Alonzi T, Pasquini E, Tripodi M, Amicone L. 2009. Convergence of Wnt signaling on the HNF4alpha-driven transcription in controlling liver zonation. Gastroenterology 137: 660-672.
32. Conlon FL, Lyons KM, Takaesu N, Barth KS, Kispert A, Herrmann B, Robertson EJ. 1994. A primary requirement for nodal in the formation and maintenance of the primitive streak in the mouse. Development 120: 1919-1928.
33. Cook D, Fry MJ, Hughes K, Sumathipala R, Woodgett JR, Dale TC. 1996. Wingless inactivates glycogen synthase kinase-3 via an intracellular signalling pathway which involves a protein kinase C. Embo J 15: 4526-4536.
34. Crawford LW, Foley JF, Elmore SA. 2010. Histology atlas of the developing mouse hepatobiliary system with emphasis on embryonic days 9.5-18.5. Toxicol Pathol 38: 872-906.
35. Dessimoz J, Opoka R, Kordich JJ, Grapin-Botton A, Wells JM. 2006. FGF signaling is necessary for establishing gut tube domains along the anterior-posterior axis in vivo. Mech Dev 123: 42-55.
36. Ehrman LA, Yutzey KE. 2001. Anterior expression of the caudal homologue cCdx-B activates a posterior genetic program in avian embryos. Dev Dyn 221: 412-421.
37. Enzan H, Himeno H, Hiroi M, Kiyoku H, Saibara T, Onishi S. 1997. Development of hepatic sinusoidal structure with special reference to the Ito cells. Microsc Res Tech 39: 336-349.
38. Erker L, Grompe M. 2007. Signaling networks in hepatic oval cell activation. Stem Cell Res 1: 90-102.
39. Finley KR, Tennessen J, Shawlot W. 2003. 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: 681-684.
40. Friedman JR, Larris B, Le PP, Peiris TH, Arsenlis A, Schug J, Tobias JW, Kaestner KH, Greenbaum LE. 2004. Orthogonal analysis of C/EBPbeta targets in vivo during liver proliferation. Proc Natl Acad Sci USA 101: 12986-12991.
41. Gadue P, Huber TL, Paddison PJ, Keller GM. 2006. Wnt and TGF-beta signaling are required for the induction of an in vitro model of primitive streak formation using embryonic stem cells. Proc Natl Acad Sci USA 103: 16806-16811.
42. Galli LM, Barnes T, Cheng T, Acosta L, Anglade A, Willert K, Nusse R, Burrus LW. 2006. Differential inhibition of Wnt-3a by Sfrp-1, Sfrp-2, and Sfrp-3. Dev Dyn 235: 681-690.
43. Gao X, Sedgwick T, Shi YB, Evans T. 1998. Distinct functions are implicated for the GATA-4, -5, and -6 transcription factors in the regulation of intestine epithelial cell differentiation. Mol Cell Biol 18: 2901-2911.
44. Germain S, Howell M, Esslemont GM, Hill CS. 2000. Homeodomain and winged-helix transcription factors recruit activated Smads to distinct promoter elements via a common Smad interaction motif. Genes Dev 14: 435-451.
45. Giera S, Braeuning A, Kohle C, Bursch W, Metzger U, Buchmann A, Schwarz M. 2010. Wnt/beta-catenin signaling activates and determines hepatic zonal expression of glutathione S-transferases in mouse liver. Toxicol Sci 115: 22-33.
46. Gkretsi V, Apte U, Mars WM, Bowen WC, Luo JH, Yang Y, Yu YP, Orr A, St-Arnaud R, Dedhar S, Kaestner KH, Wu C, Michalopoulos GK. 2008. Liver-specific ablation of integrin-linked kinase in mice results in abnormal histology, enhanced cell proliferation, and hepatomegaly. Hepatology 48: 1932-1941.
47. Goessling W, North TE, Lord AM, Ceol C, Lee S, Weidinger G, Bourque C, Strijbosch R, Haramis AP, Puder M, Clevers H, Moon RT, Zon LI. 2008. APC mutant zebrafish uncover a changing temporal requirement for wnt signaling in liver development. Dev Biol 320: 161-174.
48. Graham TA, Weaver C, Mao F, Kimelman D, Xu W. 2000. Crystal structure of a beta-catenin/Tcf complex. Cell 103: 885-896.
49. Hagos EG, Fan X, Dougan ST. 2007. The role of maternal Activin-like signals in zebrafish embryos. Dev Biol 309: 245-258.
50. Hand NJ, Master ZR, Eauclaire SF, Weinblatt DE, Matthews RP, Friedman JR. 2009. The microRNA-30 family is required for vertebrate hepatobiliary development. Gastroenterology 136: 1081-1090.
51. Haramoto Y, Tanegashima K, Onuma Y, Takahashi S, Sekizaki H, Asashima M. 2004. Xenopus tropicalis nodal-related gene 3 regulates BMP signaling: an essential role for the pro-region. Dev Biol 265: 155-168.
52. Hart M, Concordet JP, Lassot I, Albert I, del los Santos R, Durand H, Perret C, Rubinfeld B, Margottin F, Benarous R, Polakis P. 1999. The F-box protein beta-TrCP associates with phosphorylated beta-catenin and regulates its activity in the cell. Curr Biol 9: 207-210.
53. Heller RS, Stoffers DA, Hussain MA, Miller CP, Habener JF. 1998. Misexpression of the pancreatic homeodomain protein IDX-1 by the Hoxa-4 promoter associated with agenesis of the cecum. Gastroenterology 115: 381-387.
54. Howard L, Rex M, Clements D, Woodland HR. 2007. Regulation of the Xenopus Xsox17alpha(1) promoter by co-operating VegT and Sox17 sites. Dev Biol 310: 402-415.
55. Hu M, Kurobe M, Jeong YJ, Fuerer C, Ghole S, Nusse R, Sylvester KG. 2007. Wnt/beta-catenin signaling in murine hepatic transit amplifying progenitor cells. Gastroenterology 133: 1579-1591.
56. Huber O, Korn R, McLaughlin J, Ohsugi M, Herrmann BG, Kemler R. 1996. Nuclear localization of beta-catenin by interaction with transcription factor LEF-1. Mech Dev 59: 3-10.
57. Hudson C, Clements D, Friday RV, Stott D, Woodland HR. 1997. Xsox17alpha and -beta mediate endoderm formation in Xenopus. Cell 91: 397-405.
58. Huelsken J, Vogel R, Brinkmann V, Erdmann B, Birchmeier C, Birchmeier W. 2000. Requirement for beta-catenin in anterior-posterior axis formation in mice. J Cell Biol 148: 567-578.
59. Hunter MP, Wilson CM, Jiang X, Cong R, Vasavada H, Kaestner KH, Bogue CW. 2007. The homeobox gene Hhex is essential for proper hepatoblast differentiation and bile duct morphogenesis. Dev Biol 308: 355-367.
60. Hussain SZ, Sneddon T, Tan X, Micsenyi A, Michalopoulos GK, Monga SP. 2004. Wnt impacts growth and differentiation in ex vivo liver development. Exp Cell Res 292: 157-169.
61. Ikeda S, Kishida S, Yamamoto H, Murai H, Koyama S, Kikuchi A. 1998. Axin, a negative regulator of the Wnt signaling pathway, forms a complex with GSK-3beta and beta-catenin and promotes GSK-3beta-dependent phosphorylation of beta-catenin. Embo J 17: 1371-1384.
62. Imamura M, Kojima T, Lan M, Son S, Murata M, Osanai M, Chiba H, Hirata K, Sawada N. 2007. Oncostatin M induces upregulation of claudin-2 in rodent hepatocytes coinciding with changes in morphology and function of tight junctions. Exp Cell Res 313: 1951-1962.
63. Jacquemin P, Pierreux CE, Fierens S, van Eyll JM, Lemaigre FP, Rousseau GG. 2003. Cloning and embryonic expression pattern of the mouse Onecut transcription factor OC-2. Gene Expr Patterns 3: 639-644.
64. Jung J, Zheng M, Goldfarb M, Zaret KS. 1999. Initiation of mammalian liver development from endoderm by fibroblast growth factors. Science 284: 1998-2003.
65. Kamiya A, Gonzalez FJ. 2004. TNF-alpha regulates mouse fetal hepatic maturation induced by oncostatin M and extracellular matrices. Hepatology 40: 527-536.
66. Kamiya A, Kinoshita T, Ito Y, Matsui T, Morikawa Y, Senba E, Nakashima K, Taga T, Yoshida K, Kishimoto T, Miyajima A. 1999. Fetal liver development requires a paracrine action of oncostatin M through the gp130 signal transducer. Embo J 18: 2127-2136.
67. Kanai-Azuma M, Kanai Y, Gad JM, Tajima Y, Taya C, Kurohmaru M, Sanai Y, Yonekawa H, Yazaki K, Tam PP, Hayashi Y. 2002. Depletion of definitive gut endoderm in Sox17-null mutant mice. Development 129: 2367-2379.
68. Kelly OG, Pinson KI, Skarnes WC. 2004. The Wnt co-receptors Lrp5 and Lrp6 are essential for gastrulation in mice. Development 131: 2803-2815.
69. Kelly RG, Brown NA, Buckingham ME. 2001. The arterial pole of the mouse heart forms from Fgf10-expressing cells in pharyngeal mesoderm. Dev Cell 1: 435-440.
70. Kemler R, Hierholzer A, Kanzler B, Kuppig S, Hansen K, Taketo MM, de Vries WN, Knowles BB, Solter D. 2004. Stabilization of beta-catenin in the mouse zygote leads to premature epithelial-mesenchymal transition in the epiblast. Development 131: 5817-5824.
71. Kemp C, Willems E, Abdo S, Lambiv L, Leyns L. 2005. Expression of all Wnt genes and their secreted antagonists during mouse blastocyst and postimplantation development. Dev Dyn 233: 1064-1075.
72. Kodama Y, Hijikata M, Kageyama R, Shimotohno K, Chiba T. 2004. The role of notch signaling in the development of intrahepatic bile ducts. Gastroenterology 127: 1775-1786.
73. Kumar M, Jordan N, Melton D, Grapin-Botton A. 2003. Signals from lateral plate mesoderm instruct endoderm toward a pancreatic fate. Dev Biol 259: 109-122.
74. Kyrmizi I, Hatzis P, Katrakili N, Tronche F, Gonzalez FJ, Talianidis I. 2006. Plasticity and expanding complexity of the hepatic transcription factor network during liver development. Genes Dev 20: 2293-2305.
75. Laverriere AC, MacNeill C, Mueller C, Poelmann RE, Burch JB, Evans T. 1994. GATA-4/5/6, a subfamily of three transcription factors transcribed in developing heart and gut. J Biol Chem 269: 23177-23184.
76. Lemaigre FP. 2003. Development of the biliary tract. Mech Dev 120: 81-87.
77. Li J, Ning G, Duncan SA. 2000. Mammalian hepatocyte differentiation requires the transcription factor HNF-4alpha. Genes Dev 14: 464-474.
78. Li Y, Rankin SA, Sinner D, Kenny AP, Krieg PA, Zorn AM. 2008. Sfrp5 coordinates foregut specification and morphogenesis by antagonizing both canonical and noncanonical Wnt11 signaling. Genes Dev 22: 3050-3063.
79. Lilien J, Balsamo J. 2005. The regulation of cadherin-mediated adhesion by tyrosine phosphorylation/dephosphorylation of beta-catenin. Curr Opin Cell Biol 17: 459-465.
80. Lindsley RC, Gill JG, Kyba M, Murphy TL, Murphy KM. 2006. Canonical Wnt signaling is required for development of embryonic stem cell-derived mesoderm. Development 133: 3787-3796.
81. Liu C, Li Y, Semenov M, Han C, Baeg GH, Tan Y, Zhang Z, Lin X, He X. 2002. Control of beta-catenin phosphorylation/degradation by a dual-kinase mechanism. Cell 108: 837-847.
82. Liu P, Wakamiya M, Shea MJ, Albrecht U, Behringer RR, Bradley A. 1999. Requirement for Wnt3 in vertebrate axis formation. Nat Genet 22: 361-365.
83. Liu W, Li L, Li G, Garritano F, Shanske A, Frenz DA. 2008. Coordinated molecular control of otic capsule differentiation: functional role of Wnt5a signaling and opposition by sfrp3 activity. Growth Factors 26: 343-354.
84. Loeppen S, Koehle C, Buchmann A, Schwarz M. 2005. A beta-catenin-dependent pathway regulates expression of cytochrome P450 isoforms in mouse liver tumors. Carcinogenesis 26: 239-248.
85. Loomes KM, Russo P, Ryan M, Nelson A, Underkoffler L, Glover C, Fu H, Gridley T, Kaestner KH, Oakey RJ. 2007. Bile duct proliferation in liver-specific Jag1 conditional knockout mice: effects of gene dosage. Hepatology 45: 323-330.
86. Lozier J, McCright B, Gridley T. 2008. Notch signaling regulates bile duct morphogenesis in mice. PLoS One 3: e1851.
87. Lu CC, Robertson EJ. 2004. Multiple roles for Nodal in the epiblast of the mouse embryo in the establishment of anterior-posterior patterning. Dev Biol 273: 149-159.
88. Luzzatto AC. 1981. Hepatocyte differentiation during early fetal development in the rat. Cell Tissue Res 215: 133-142.
89. Margagliotti S, Clotman F, Pierreux CE, Beaudry JB, Jacquemin P, Rousseau GG, Lemaigre FP. 2007. The Onecut transcription factors HNF-6/OC-1 and OC-2 regulate early liver expansion by controlling hepatoblast migration. Dev Biol 311: 579-589.
90. Margagliotti S, Clotman F, Pierreux CE, Lemoine P, Rousseau GG, Henriet P, Lemaigre FP. 2008. Role of metalloproteinases at the onset of liver development. Dev Growth Differ 50: 331-338.
91. Martin M, Gallego-Llamas J, Ribes V, Kedinger M, Niederreither K, Chambon P, Dolle P, Gradwohl G. 2005. Dorsal pancreas agenesis in retinoic acid-deficient Raldh2 mutant mice. Dev Biol 284: 399-411.
92. Matsui T, Kinoshita T, Morikawa Y, Tohya K, Katsuki M, Ito Y, Kamiya A, Miyajima A. 2002. K-Ras mediates cytokine-induced formation of E-cadherin-based adherens junctions during liver development. Embo J 21: 1021-1030.
93. Matsui T, Raya A, Kawakami Y, Callol-Massot C, Capdevila J, Rodriguez-Esteban C, Izpisua Belmonte JC. 2005. Noncanonical Wnt signaling regulates midline convergence of organ primordia during zebrafish development. Genes Dev 19: 164-175.
94. Matsumoto K, Yoshitomi H, Rossant J, Zaret KS. 2001. Liver organogenesis promoted by endothelial cells prior to vascular function. Science 294: 559-563.
95. Matsumoto K, Miki R, Nakayama M, Tatsumi N, Yokouchi Y. 2008. Wnt9a secreted from the walls of hepatic sinusoids is essential for morphogenesis, proliferation, and glycogen accumulation of chick hepatic epithelium. Dev Biol 319: 234--247.
96. McCrea PD, Gumbiner BM. 1991. Purification of a 92-kDa cytoplasmic protein tightly associated with the cell-cell adhesion molecule E-cadherin (uvomorulin). Characterization and extractability of the protein complex from the cell cytostructure. J Biol Chem 266: 4514-4520.
97. McCrea PD, Turck CW, Gumbiner B. 1991. A homolog of the armadillo protein in Drosophila (plakoglobin) associated with E-cadherin. Science 254: 1359-1361.
98. McLin VA, Rankin SA, Zorn AM. 2007. Repression of Wnt/beta-catenin signaling in the anterior endoderm is essential for liver and pancreas development. Development 134: 2207-2217.
99. Medlock ES, Haar JL. 1983. The liver hemopoietic environment: I. Developing hepatocytes and their role in fetal hemopoiesis. Anat Rec 207: 31-41.
100. Michalopoulos GK, Bowen WC, Mule K, Luo J. 2003. HGF-, EGF-, and dexamethasone-induced gene expression patterns during formation of tissue in hepatic organoid cultures. Gene Expr 11: 55-75.
101. Micsenyi A, Tan X, Sneddon T, Luo JH, Michalopoulos GK, Monga SP. 2004. Beta-catenin is temporally regulated during normal liver development. Gastroenterology 126: 1134-1146.
102. Mikels AJ, Nusse R. 2006. Purified Wnt5a protein activates or inhibits beta-catenin-TCF signaling depending on receptor context. PLoS Biol 4: e115.
103. Mohamed OA, Clarke HJ, Dufort D. 2004. Beta-catenin signaling marks the prospective site of primitive streak formation in the mouse embryo. Dev Dyn 231: 416-424.
104. Monga SP. 2009. Role of Wnt/beta-catenin signaling in liver metabolism and cancer. Int J Biochem Cell Biol.
105. Monga SP, Mars WM, Pediaditakis P, Bell A, Mule K, Bowen WC, Wang X, Zarnegar R, Michalopoulos GK. 2002. Hepatocyte growth factor induces Wnt-independent nuclear translocation of beta-catenin after Met-beta-catenin dissociation in hepatocytes. Cancer Res 62: 2064-2071.
106. Monga SP, Monga HK, Tan X, Mule K, Pediaditakis P, Michalopoulos GK. 2003. Beta-catenin antisense studies in embryonic liver cultures: role in proliferation, apoptosis, and lineage specification. Gastroenterology 124: 202-216.
107. Munemitsu S, Albert I, Souza B, Rubinfeld B, Polakis P. 1995. Regulation of intracellular beta-catenin levels by the adenomatous polyposis coli (APC) tumor-suppressor protein. Proc Natl Acad Sci USA 92: 3046-3050.
108. Nakamura T, Hamada F, Ishidate T, Anai K, Kawahara K, Toyoshima K, Akiyama T. 1998. Axin, an inhibitor of the Wnt signalling pathway, interacts with beta-catenin, GSK-3beta and APC and reduces the beta-catenin level. Genes Cells 3: 395-403.
109. Naldini L, Vigna E, Narsimhan RP, Gaudino G, Zarnegar R, Michalopoulos GK, Comoglio PM. 1991a. Hepatocyte growth factor (HGF) stimulates the tyrosine kinase activity of the receptor encoded by the proto-oncogene c-MET. Oncogene 6: 501-504.
110. Naldini L, Weidner KM, Vigna E, Gaudino G, Bardelli A, Ponzetto C, Narsimhan RP, Hartmann G, Zarnegar R, Michalopoulos GK. 1991b. Scatter factor and hepatocyte growth factor are indistinguishable ligands for the MET receptor. Embo J 10: 2867-2878.
111. Negishi T, Nagai Y, Asaoka Y, Ohno M, Namae M, Mitani H, Sasaki T, Shimizu N, Terai S, Sakaida I, Kondoh H, Katada T, Furutani-Seiki M, Nishina H. 2010. Retinoic acid signaling positively regulates liver specification by inducing wnt2bb gene expression in medaka. Hepatology 51: 1037-1045.
112. Norgaard GA, Jensen JN, Jensen J. 2003. FGF10 signaling maintains the pancreatic progenitor cell state revealing a novel role of Notch in organ development. Dev Biol 264: 323-338.
113. Nyeng P, Norgaard GA, Kobberup S, Jensen J. 2007. FGF10 signaling controls stomach morphogenesis. Dev Biol 303: 295-310.
114. Nyeng P, Norgaard GA, Kobberup S, Jensen J. 2008. FGF10 maintains distal lung bud epithelium and excessive signaling leads to progenitor state arrest, distalization, and goblet cell metaplasia. BMC Dev Biol 8: 2.
115. Ober EA, Verkade H, Field HA, Stainier DY. 2006. Mesodermal Wnt2b signalling positively regulates liver specification. Nature 442: 688-691.
116. Odom DT, Zizlsperger N, Gordon DB, Bell GW, Rinaldi NJ, Murray HL, Volkert TL, Schreiber J, Rolfe PA, Gifford DK, Fraenkel E, Bell GI, Young RA. 2004. Control of pancreas and liver gene expression by HNF transcription factors. Science 303: 1378-1381.
117. Ohlsson H, Karlsson K, Edlund T. 1993. IPF1, a homeodomain-containing transactivator of the insulin gene. EMBO J 12: 4251-4259.
118. Onuma Y, Takahashi S, Haramoto Y, Tanegashima K, Yokota C, Whitman M, Asashima M. 2005. Xnr2 and Xnr5 unprocessed proteins inhibit Wnt signaling upstream of dishevelled. Dev Dyn 234: 900-910.
119. Ornitz DM, Itoh N. 2001. Fibroblast growth factors. Genome Biol 2: REVIEWS3005.
120. Ozawa M, Kemler R. 1998. Altered cell adhesion activity by pervanadate due to the dissociation of alpha-catenin from the E-cadherin.catenin complex. J Biol Chem 273: 6166-6170.
121. Papkoff J, Aikawa M. 1998. WNT-1 and HGF regulate GSK3 beta activity and beta-catenin signaling in mammary epithelial cells. Biochem Biophys Res Commun 247: 851-858.
122. Papkoff J, Rubinfeld B, Schryver B, Polakis P. 1996. Wnt-1 regulates free pools of catenins and stabilizes APC-catenin complexes. Mol Cell Biol 16: 2128-2134.
123. Parviz F, Matullo C, Garrison WD, Savatski L, Adamson JW, Ning G, Kaestner KH, Rossi JM, Zaret KS, Duncan SA. 2003. Hepatocyte nuclear factor 4alpha controls the development of a hepatic epithelium and liver morphogenesis. Nat Genet 34: 292-296.
124. Perea-Gomez A, Vella FD, Shawlot W, Oulad-Abdelghani M, Chazaud C, Meno C, Pfister V, Chen L, Robertson E, Hamada H, Behringer RR, Ang SL. 2002. Nodal antagonists in the anterior visceral endoderm prevent the formation of multiple primitive streaks. Dev Cell 3: 745-756.
125. Piedra J, Martinez D, Castano J, Miravet S, Dunach M, de Herreros AG. 2001. Regulation of beta-catenin structure and activity by tyrosine phosphorylation. J Biol Chem 276: 20436-20443.
126. Piedra J, Miravet S, Castano J, Palmer HG, Heisterkamp N, Garcia de Herreros A, Dunach M. 2003. p120 Catenin-associated Fer and Fyn tyrosine kinases regulate beta-catenin Tyr-142 phosphorylation and beta-catenin-alpha-catenin Interaction. Mol Cell Biol 23: 2287-2297.
127. Pilcher KE, Krieg PA. 2002. Expression of the Wnt inhibitor, sFRP5, in the gut endoderm of Xenopus. Gene Expr Patterns 2: 369-372.
128. Preisegger KH, Factor VM, Fuchsbichler A, Stumptner C, Denk H, Thorgeirsson SS. 1999. Atypical ductular proliferation and its inhibition by transforming growth factor beta1 in the 3, 5-diethoxycarbonyl-1, 4-dihydrocollidine mouse model for chronic alcoholic liver disease. Lab Invest 79: 103-109.
129. Qian D, Jones C, Rzadzinska A, Mark S, Zhang X, Steel KP, Dai X, Chen P. 2007. Wnt5a functions in planar cell polarity regulation in mice. Dev Biol 306: 121-133.
130. Rastegar M, Rousseau GG, Lemaigre FP. 2000. CCAAT/enhancer-binding protein-alpha is a component of the growth hormone-regulated network of liver transcription factors. Endocrinology 141: 1686-1692.
131. Rhee J, Buchan T, Zukerberg L, Lilien J, Balsamo J. 2007. Cables links Robo-bound Abl kinase to N-cadherin-bound beta-catenin to mediate Slit-induced modulation of adhesion and transcription. Nat Cell Biol 9: 883-892.
132. Rimm DL, Koslov ER, Kebriaei P, Cianci CD, Morrow JS. 1995. Alpha 1(E)-catenin is an actin-binding and -bundling protein mediating the attachment of F-actin to the membrane adhesion complex. Proc Natl Acad Sci USA 92: 8813-8817.
133. Roberts DJ, Johnson RL, Burke AC, Nelson CE, Morgan BA, Tabin C. 1995. Sonic hedgehog is an endodermal signal inducing Bmp-4 and Hox genes during induction and regionalization of the chick hindgut. Development 121: 3163-3174.
134. Rossi JM, Dunn NR, Hogan BL, Zaret KS. 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.
135. Roura S, Miravet S, Piedra J, Garcia de Herreros A, Dunach M. 1999. Regulation of E-cadherin/Catenin association by tyrosine phosphorylation. J Biol Chem 274: 36734-36740.
136. Rubinfeld B, Albert I, Porfiri E, Fiol C, Munemitsu S, Polakis P. 1996. Binding of GSK3beta to the APC-beta-catenin complex and regulation of complex assembly. Science 272: 1023-1026.
137. Sakanaka C, Leong P, Xu L, Harrison SD, Williams LT. 1999. Casein kinase iepsilon in the wnt pathway: regulation of beta-catenin function. Proc Natl Acad Sci USA 96: 12548-12552.
138. Sala FG, Curtis JL, Veltmaat JM, Del Moral PM, Le LT, Fairbanks TJ, Warburton D, Ford H, Wang K, Burns RC, Bellusci S. 2006. Fibroblast growth factor 10 is required for survival and proliferation but not differentiation of intestinal epithelial progenitor cells during murine colon development. Dev Biol 299: 373-385.
139. Sasaki K, Matsumura G. 1986. Haemopoietic cells of yolk sac and liver in the mouse embryo: a light and electron microscopical study. J Anat 148: 87-97.
140. Scardigli R, Gargioli C, Tosoni D, Borello U, Sampaolesi M, Sciorati C, Cannata S, Clementi E, Brunelli S, Cossu G. 2008. Binding of sFRP-3 to EGF in the extra-cellular space affects proliferation, differentiation and morphogenetic events regulated by the two molecules. PLoS One 3: e2471.
141. Schmidt C, Bladt F, Goedecke S, Brinkmann V, Zschiesche W, Sharpe M, Gherardi E, Birchmeier C. 1995. Scatter factor/hepatocyte growth factor is essential for liver development. Nature 373: 699-702.
142. Schneider SQ, Finnerty JR, Martindale MQ. 2003. Protein evolution: structure-function relationships of the oncogene beta-catenin in the evolution of multicellular animals. J Exp Zool B Mol Dev Evol 295: 25-44.
143. Sekhon SS, Tan X, Micsenyi A, Bowen WC, Monga SP. 2004. Fibroblast growth factor enriches the embryonic liver cultures for hepatic progenitors. Am J Pathol 164: 2229-2240.
144. Sell S, Leffert HL. 2008. Liver cancer stem cells. J Clin Oncol 26: 2800-2805.
145. Serls AE, Doherty S, Parvatiyar P, Wells JM, Deutsch GH. 2005. Different thresholds of fibroblast growth factors pattern the ventral foregut into liver and lung. Development 132: 35-47.
146. Shin D, Shin CH, Tucker J, Ober EA, Rentzsch F, Poss KD, Hammerschmidt M, Mullins MC, Stainier DY. 2007. Bmp and Fgf signaling are essential for liver specification in zebrafish. Development 134: 2041-2050.
147. Simion A, Laudadio I, Prevot PP, Raynaud P, Lemaigre FP, Jacquemin P. 2010. MiR-495 and miR-218 regulate the expression of the Onecut transcription factors HNF-6 and OC-2. Biochem Biophys Res Commun 391: 293-298.
148. Sinner D, Rankin S, Lee M, Zorn AM. 2004. Sox17 and beta-catenin cooperate to regulate the transcription of endodermal genes. Development 131: 3069-3080.
149. Spee B, Carpino G, Schotanus BA, Katoonizadeh A, Vander Borght S, Gaudio E, Roskams T. 2010. Characterisation of the liver progenitor cell niche in liver diseases: potential involvement of Wnt and Notch signalling. Gut 59: 247-257.
150. Stafford D, Hornbruch A, Mueller PR, Prince VE. 2004. A conserved role for retinoid signaling in vertebrate pancreas development. Dev Genes Evol 214: 432-441.
151. Strick-Marchand H, Weiss MC. 2002. Inducible differentiation and morphogenesis of bipotential liver cell lines from wild-type mouse embryos. Hepatology 36: 794-804.
152. Suksaweang S, Lin CM, Jiang TX, Hughes MW, Widelitz RB, Chuong CM. 2004. Morphogenesis of chicken liver: identification of localized growth zones and the role of beta-catenin/Wnt in size regulation. Dev Biol 266: 109-122.
153. Suzuki E, Evans T, Lowry J, Truong L, Bell DW, Testa JR, Walsh K. 1996. The human GATA-6 gene: structure, chromosomal location, and regulation of expression by tissue-specific and mitogen-responsive signals. Genomics 38: 283-290.
154. Swiatek W, Tsai IC, Klimowski L, Pepler A, Barnette J, Yost HJ, Virshup DM. 2004. Regulation of casein kinase I epsilon activity by Wnt signaling. J Biol Chem 279: 13011-13017.
155. Tan X, Behari J, Cieply B, Michalopoulos GK, Monga SP. 2006. Conditional deletion of beta-catenin reveals its role in liver growth and regeneration. Gastroenterology 131: 1561-1572.
156. Tan X, Yuan Y, Zeng G, Apte U, Thompson MD, Cieply B, Stolz DB, Michalopoulos GK, Kaestner KH, Monga SP. 2008. Beta-catenin deletion in hepatoblasts disrupts hepatic morphogenesis and survival during mouse development. Hepatology 47: 1667-1679.
157. Tatsumi N, Miki R, Katsu K, Yokouchi Y. 2007. Neurturin-GFRalpha2 signaling controls liver bud migration along the ductus venosus in the chick embryo. Dev Biol 307: 14-28.
158. Thompson MD, Awuah P, Singh S, Monga SP. 2010. Disparate cellular basis of improved liver repair in beta-catenin-overexpressing mice after long-term exposure to 3, 5-diethoxycarbonyl-1, 4-dihydrocollidine. Am J Pathol 177: 1812-1822.
159. Tiso N, Filippi A, Pauls S, Bortolussi M, Argenton F. 2002. BMP signalling regulates anteroposterior endoderm patterning in zebrafish. Mech Dev 118: 29-37.
160. Tomizawa M, Garfield S, Factor V, Xanthopoulos KG. 1998. Hepatocytes deficient in CCAAT/enhancer binding protein alpha (C/EBP alpha) exhibit both hepatocyte and biliary epithelial cell character. Biochem Biophys Res Commun 249: 1-5.
161. Vassy J, Kraemer M, Chalumeau MT, Foucrier J. 1988. Development of the fetal rat liver: ultrastructural and stereological study of hepatocytes. Cell Differ 24: 9-24.
162. Vincent SD, Dunn NR, Hayashi S, Norris DP, Robertson EJ. 2003. Cell fate decisions within the mouse organizer are governed by graded Nodal signals. Genes Dev 17: 1646-1662.
163. Wallace KN, Pack M. 2003. Unique and conserved aspects of gut development in zebrafish. Dev Biol 255: 12-29.
164. Wang YK, Samos CH, Peoples R, Perez-Jurado LA, Nusse R, Francke U. 1997. A novel human homologue of the Drosophila frizzled wnt receptor gene binds wingless protein and is in the Williams syndrome deletion at 7q11.23. Hum Mol Genet 6: 465-472.
165. Wang Z, Dolle P, Cardoso WV, Niederreither K. 2006. Retinoic acid regulates morphogenesis and patterning of posterior foregut derivatives. Dev Biol 297: 433-445.
166. Watt AJ, Zhao R, Li J, Duncan SA. 2007. Development of the mammalian liver and ventral pancreas is dependent on GATA4. BMC Dev Biol 7: 37.
167. Wawrzak D, Metioui M, Willems E, Hendrickx M, de Genst E, Leyns L. 2007. Wnt3a binds to several sFRPs in the nanomolar range. Biochem Biophys Res Commun 357: 1119-1123.
168. Wells JM, Melton DA. 2000. Early mouse endoderm is patterned by soluble factors from adjacent germ layers. Development 127: 1563-1572.
169. Williams JM, Oh SH, Jorgensen M, Steiger N, Darwiche H, Shupe T, Petersen BE. 2010. The role of the Wnt family of secreted proteins in rat oval "stem" cell-based liver regeneration: Wnt1 drives differentiation. Am J Pathol 176: 2732-2742.
170. Yamasaki H, Sada A, Iwata T, Niwa T, Tomizawa M, Xanthopoulos KG, Koike T, Shiojiri N. 2006. Suppression of C/EBPalpha expression in periportal hepatoblasts may stimulate biliary cell differentiation through increased Hnf6 and Hnf1b expression. Development 133: 4233-4243.
171. Yang W, Yan HX, Chen L, Liu Q, He YQ, Yu LX, Zhang SH, Huang DD, Tang L, Kong XN, Chen C, Liu SQ, Wu MC, Wang HY. 2008. Wnt/beta-catenin signaling contributes to activation of normal and tumorigenic liver progenitor cells. Cancer Res 68: 4287-4295.
172. Yost C, Torres M, Miller JR, Huang E, Kimelman D, Moon RT. 1996. The axis-inducing activity, stability, and subcellular distribution of beta-catenin is regulated in Xenopus embryos by glycogen synthase kinase 3. Genes Dev 10: 1443-1454.
173. Zeng G, Apte U, Micsenyi A, Bell A, Monga SP. 2006. Tyrosine residues 654 and 670 in beta-catenin are crucial in regulation of Met-beta-catenin interactions. Exp Cell Res 312: 3620-3630.
174. Zeng G, Awan F, Otruba W, Muller P, Apte U, Tan X, Gandhi C, Demetris AJ, Monga SP. 2007. Wnt'er in liver: expression of Wnt and frizzled genes in mouse. Hepatology 45: 195-204.
175. Zhang W, Yatskievych TA, Cao X, Antin PB. 2002. Regulation of Hex gene expression by a Smads-dependent signaling pathway. J Biol Chem 277: 45435-45441.
176. Zhang W, Yatskievych TA, Baker RK, Antin PB. 2004. Regulation of Hex gene expression and initial stages of avian hepatogenesis by Bmp and Fgf signaling. Dev Biol 268: 312-326.
177. Zhao R, Watt AJ, Li J, Luebke-Wheeler J, Morrisey EE, Duncan SA. 2005. GATA6 is essential for embryonic development of the liver but dispensable for early heart formation. Mol Cell Biol 25: 2622-2631.
178. Zorn AM, Mason J. 2001. Gene expression in the embryonic Xenopus liver. Mech Dev 103: 153-157.