FGF signaling segregates biliary cell-lineage from chick hepatoblasts cooperatively with BMP4 and ECM components in vitro

Developmental Dynamics

Volumn 237, Issue 5, 2008, Pages 1268-1283

  Yanai, Masaaki ^a,b   Tatsumi, Norifumi ^a   Hasunuma, Noboru ^a,b   Katsu, Kenjiro ^a   Endo, Fumio ^a,b   Yokouchi, Yuji ^a  

^a KUMAMOTO UNIVERSITY   (Japan)

^b KUMAMOTO UNIVERSITY   (Japan)

Author keywords

Bile duct; Biliary epithelial cell; BMP; Differentiation; ECM; Epithelial mesenchymal interaction; FGF; Hepatoblast; Hepatocyte; Liver

Indexed keywords

BASIC FIBROBLAST GROWTH FACTOR; BONE MORPHOGENETIC PROTEIN 4; FIBROBLAST GROWTH FACTOR RECEPTOR; KERATINOCYTE GROWTH FACTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BILIARY EPITHELIAL CELL; CELL CULTURE; CELL DIFFERENTIATION; CELL LINEAGE; CELL MATURATION; CHICK; CONTROLLED STUDY; EPITHELIUM CELL; EXTRACELLULAR MATRIX; IN VITRO STUDY; INTRAHEPATIC BILE DUCT; LIVER CELL; LIVER DEVELOPMENT; MESENCHYME CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

ANIMALS; BILE DUCTS; BONE MORPHOGENETIC PROTEINS; CELL DIFFERENTIATION; CELL LINEAGE; CELLS, CULTURED; CHICKENS; EPITHELIAL CELLS; EXTRACELLULAR MATRIX; FIBROBLAST GROWTH FACTOR 2; FIBROBLAST GROWTH FACTOR 7; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEMATOPOIETIC STEM CELLS; HEPATOCYTE GROWTH FACTOR; HOMEODOMAIN PROTEINS; KERATIN-19; LIVER; MESODERM; MORPHOGENESIS; RECEPTORS, FIBROBLAST GROWTH FACTOR; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 43449132096     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.21520     Document Type: Article

References (70)

1. Ader T, Norel R, Levoci L, Rogler LE. 2006. Transcriptional profiling implicates TGFβBMP and Notch signaling pathways in ductular differentiation of fetal murine hepatoblasts. Mech Dev 123:177-194.
2. Alagille D, Estrada A, Hadchouel M, Gautier M, Odievre M, Dommergues JP. 1987. Syndromic paucity of interlobular bile ducts (Alagille syndrome or arteriohepatic dysplasia): review of 80 cases. J Pediatr 110:195-200.
3. Amenta PS, Harrison D. 1997. Expression and potential role of the extracellular matrix in hepatic ontogenesis: a review. Microsc Res Tech 39:372-386.
4. Antoine M, Wirz W, Tag CG, Gressner AM, Wycislo M, Müller R, Kiefer P. 2006. Fibroblast growth factor 16 and 18 are expressed in human cardiovascular tissues and induce on endothelial cells migration but not proliferation. Biochem Biophys Res Commun 346:224-233.
5. Antoine M, Wirz W, Tag CG, Gressner AM, Marvituna M, Wycislo M, Hellerbrand C, Kiefer P. 2007. Expression and function of fibroblast growth factor (FGF) 9 in hepatic stellate cells and its role in toxic liver injury. Biochem Biophys Res Commun 361:335-341.
6. Arman E, Haffner-Krausz R, Chen Y, Heath JK, Lonai P. 1998. Targeted disruption of fibroblast growth factor (FGF) receptor 2 suggests a role for FGF signaling in pregastrulation mammalian development. Proc Natl Acad Sci USA 95:5082-5087.
7. Aylsworth AS, Sulik KK. 1993. Liver, gallbladder, and pancreas. In: Stevenson RE, Hall JG, Goodman RM, editors. Human malformations and related anomalies, vol. II. New York: Oxford University Press. p 445-474.
8. Baloch Z, Klapper J, Buchanan L, Schwartz M, Amenta PS. 1992. Ontogenesis of the murine hepatic extracellular matrix: an immunohistochemical study. Differentiation 51:209-218.
9. Bellusci S, Grindley J, Emoto H, Itoh N, Hogan BL. 1997. Fibroblast growth factor 10 (FGF10) and branching morphogenesis in the embryonic mouse lung. Development 124:4867-4878.
10. Ben-Ze'ev A, Robinson GS, Bucher NL, Farmer SR. 1988. Cell-cell and cell-matrix interactions differentially regulate the expression of hepatic and cytoskeletal genes in primary cultures of rat hepatocytes. Proc Natl Acad Sci USA 85:2161-2165.
11. 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.
12. Bissell DM, Arenson DM, Maher JJ, Roll FJ. 1987. Support of cultured hepatocytes by a laminin-rich gel. Evidence for a functionally significant subendothelial matrix in normal rat liver. J Clin Invest 79:801-812.
13. Bladt F, Riethmacher D, Isenmann S, Aguzzi A, Birchmeier C. 1995. Essential role for the c-met receptor in the migration of myogenic precursor cells into the limb bud. Nature 376:768-771.
14. Bush KT, Sakurai H, Steer DL, Leonard MO, Sampogna RV, Meyer TN, Schwesinger C, Qiao J, Nigam SK. 2004. TGF-β superfamily members modulate growth, branching, shaping, and patterning of the ureteric bud. Dev Biol 266:285-298.
15. Caron JM. 1990. Induction of albumin gene transcription in hepatocytes by extracellular matrix proteins. Mol Cell Biol 10:1239-1243.
16. Cascio S, Zaret KS. 1991. Hepatocyte differentiation initiates during endodermal-mesenchymal interactions prior to liver formation. Development 113:217-225.
17. 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.
18. 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 TGFβ signaling modulated by Onecut transcription factors. Genes Dev 19:1849-1854.
19. 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 HNF1β. Development 129:1829-1838.
20. Crawford JM. 2002. Development of the intrahepatic biliary tree. Semin Liver Dis 22:213-226.
21. Deng CX, Wynshaw-Boris A, Shen MM, Daugherty C, Ornitz DM, Leder P. 1994. Murine FGFR-1 is required for early postimplantation growth and axial organization. Genes Dev 8:3045-3057.
22. Duncia JV, Santella JB, Higley CA, Pitts WJ, Wityak J, Frietze WE, et al. 1998. MEK inhibitors: the chemistry and biological activity of U0126, its analogs, and cyclization products. Bioorg Med Chem Lett 8:2839-2844.
23. Enzan H, Okita T, Fujita H, Iijima S. 1974. Light and electron microscopic studies on the development of periportal bile ducts of the human embryo. Acta Pathol Jpn 24:427-447.
24. Francis PH, Richardson MK, Brickell PM, Tickle C. 1994. Bone morphogenetic proteins and a signalling pathway that controls patterning in the developing chick limb. Development 120:209-218.
25. Germain L, Noel M, Gourdeau H, Marceau N. 1988. Promotion of growth and differentiation of rat ductular oval cells in primary culture. Cancer Res 48:368-378.
26. Goldfarb M. 1996. Functions of fibroblast growth factors in vertebrate development. Cytokine Growth Factor Rev 7:311-325.
27. Hamburger V, Hamilton H. 1951. A series of normal stages in the development of the chick embryo. J Exp Morph 88:49-92.
28. Haruna Y, Saito K, Spaulding S, Nalesnik MA, Gerber MA. 1996. Identification of bipotential progenitor cells in human liver development. Hepatology 23:476-481.
29. Hoffman MP, Kidder BL, Steinberg ZL, Lakhani S, Ho S, Kleinman HK, Larsen M. 2002. Gene expression profiles of mouse submandibular gland development: FGFR1 regulates branching morphogenesis in vitro through BMP- and FGF-dependent mechanisms. Development 129:5767-5778.
30. Jung J, Zheng M, Goldfarb M, Zaret KS. 1999. Initiation of mammalian liver development from endoderm by fibroblast growth factors. Science 284:1998-2003.
31. Lee PL, Johnson DE, Cousens LS, Fried VA, Williams LT. 1989. Purification and complementary DNA cloning of a receptor for basic fibroblast growth factor. Science 245:57-60.
32. Lemaigre FP. 2003. Development of the biliary tract. Mech Dev 120:81-87.
33. Lemaigre F, Zaret KS. 2004. Liver development update: new embryo models, cell lineage control, and morphogenesis. Curr Opin Genet Dev 14:582-590.
34. Li L, Krantz ID, Deng Y, Genin A, Banta AB, Collins CC, Qi M, Trask BJ, Kuo WL, Cochran J, Costa T, Pierpont ME, Rand EB, Piccoli DA, Hood L, Spinner NB. 1997. Alagille syndrome is caused by mutations in human Jagged1, which encodes a ligand for Notch1. Nat Genet 16:243-251.
35. Logan M, Tabin, C. 1998. Targeted gene misexpression in chick limb buds using avian replication-competent retroviruses. Methods 14:407-420.
36. Masui T, Wakefield LM, Lechner JF, LaVeck, MA, Sporn MB, Harris, CC. 1986. Type beta transforming growth factor is the primary differentiation- inducing serum factor for normal human bronchial epithelial cells. Proc Natl Acad Sci USA 83:2438-2442.
37. Matthews RP, Plumb-Rudewiez N, Lorent K, Gissen P, Johnson CA, Lemaigre F, Pack M. 2005. Zebrafish vps33b, an ortholog of the gene responsible for human arthrogryposis-renal dysfunction-cholestasis syndrome, regulates biliary development downstream of the onecut transcription factor hnf6. Development 132:5295-5306.
38. McCright B, Lozier J, Gridley, T. 2002. A mouse model of Alagille syndrome: Notch2 as a genetic modifier of Jag1 haploinsufficiency. Development 129:1075-1082.
39. Mohammadi M, McMahon G, Sun L, Tang C, Hirth P, Yeh BK, Hubbard SR, Schlessinger J. 1997. Structures of the tyrosine kinase domain of fibroblast growth factor receptor in complex with inhibitors. Science 276:955-960.
40. Nakayama, M., Matsumoto, K., Tatsumi, N., Yanai, M., and Yokouchi, Y. 2006. Id3 is important for proliferation and differentiation of the hepatoblasts during the chick liver development. Mech Dev 123:580-590.
41. Nguyen HQ, Danilenko DM, Bucay N, DeRose ML, Van GY, Thomason A, Simonet WS. 1996. Expression of keratinocyte growth factor in embryonic liver of transgenic mice causes changes in epithelial growth and differentiation resulting in polycystic kidneys and other organ malformations. Oncogene 12:2109-2119.
42. Oda T, Elkahloun AG, Pike BL, Okajima K, Krantz ID, Genin A, Piccoli DA, Meltzer PS, Spinner NB, Collins FS, Chandrasekharappa SC. 1997. Mutations in the human Jagged1 gene are responsible for Alagille syndrome. Nat Genet 16:235-242.
43. Ornitz DM, Itoh N. 2001. Fibroblast growth factors. Genome Biol 2:REVIEWS3005.
44. Pasquale EB, Singer SJ. 1989. Identification of a developmentally regulated protein-tyrosine kinase by using anti-phosphotyrosine antibodies to screen a cDNA expression library. Proc Natl Acad Sci USA 86:5449-5453.
45. Powers CJ, McLeskey SW, Wellstein A. 2000. Fibroblast growth factors, their receptors and signaling. Endocr Relat Cancer 7:165-197.
46. 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.
47. Sato M, Kitazawa T, Iwai T, Seki J, Sakato N, Kato J, Takeya T. 1991. Isolation of chicken-bek and a related gene; identification of structural variation in the ligand-binding domains of the FGF-receptor family. Oncogene 6:1279-1283.
48. 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.
49. Schuetz EG, Li D, Omiecinski CJ, Muller-Eberhard U, Kleinman HK, Elswick B, Guzelian, PS. 1988. Regulation of gene expression in adult rat hepatocytes cultured on a basement membrane matrix. J Cell Physiol 134:309-323.
50. Shah KD, Gerber MA. 1989. Development of intrahepatic bile ducts in humans. Immunohistochemical study using monoclonal cytokeratin antibodies. Arch Pathol Lab Med 113:1135-1138.
51. Shah KD, Gerber MA. 1990. Development of intrahepatic bile ducts in humans. Possible role of laminin. Arch Pathol Lab Med 114:597-600.
52. Shiojiri N. 1984. The origin of intrahepatic bile duct cells in the mouse. J Embryol Exp Morphol 79:25-39.
53. Shiojiri N. 1994. Transient expression of bile-duct-specific cytokeratin in fetal mouse hepatocytes. Cell Tissue Res 278:117-123.
54. Shiojiri N, Nagai Y. 1992. Preferential differentiation of the bile ducts along the portal vein in the development of mouse liver. Anat Embryol (Berl) 185:17-24.
55. Shiojiri N, Lemire JM, Fausto N. 1991. Cell lineages and oval cell progenitors in rat liver development. Cancer Res 51:2611-2620.
56. Spagnoli FM, Amicone L, Tripodi M, Weiss MC. 1998. Identification of a bipotential precursor cell in hepatic cell lines derived from transgenic mice expressing cyto-Met in the liver. J Cell Biol 143:1101-1112.
57. Steinberg Z, Myers C, Heim VM, Lathrop CA, Rebustini IT, Stewart JS, Larsen M, Hoffman MP. 2005. FGFR2b signaling regulates ex vivo submandibular gland epithelial cell proliferation and branching morphogenesis. Development 132:1223-1234.
58. Suzuki A, Iwama A, Miyashita H, Nakauchi H, Taniguchi H. 2003. Role for growth factors and extracellular matrix in controlling differentiation of prospectively isolated hepatic stem cells. Development 130:2513-2524.
59. 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.
60. Vukicevic S, Kleinman HK, Luvten FP, Roberts AB, Roche NS, Reddi AH. 1992. Identification of multiple active growth factors in basement membrane Matrigel suggests caution in interpretation of cellular activity related to extracellular matrix components. Exp Cell Res 202:1-8.
61. Weaver M, Dunn NR, Hogan BL. 2000. Bmp4 and Fgf10 play opposing roles during lung bud morphogenesis. 127:2685-2704.
62. Welm BE, Freeman KW, Chen M, Contreras A, Spencer DM, Rosen JM. 2002. Inducible dimerization of FGFR1: development of a mouse model to analyze progressive transformation of the mammary gland. J Cell Biol 157:703-714.
63. Wilson JW, Groat CS, Leduc EH. 1963. Histogenesis of the Liver. Ann NY Acad Sci 111:8-24.
64. Wood RL. 1965. An electron microscope study of developing bile canaliculi in the rat. Anat Rec 151:507-529.
65. Yamaguchi TP, Harpal K, Henkemeyer M, Rossant J, 1994. fgfr-1 is required for embryonic growth and mesodermal patterning during mouse gastrulation. Genes Dev 8:3032-3044.
66. 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.
67. Yanai M, Tatsumi N, Endo F, Yokouchi Y. 2005. Analysis of gene expression patterns in the developing chick liver. Dev Dyn 233:1116-1122.
68. Yokouchi Y, Vogan KJ, Pearse RV, Tabin CJ. 1999. Antagonistic signaling by Caronte, a novel Cerberus-related gene, establishes left-right asymmetric gene expression. Cell 98:573-583.
69. 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.
70. Zhang X, Ibrahimi OA, Olsen SK, Umemori H, Mohammadi M, Ornitz DM. 2006. Receptor specificity of the fibroblast growth factor family. The complete mammalian FGF family. J Biol Chem 281:15694-15700.