FGF2 specifies hESC-derived definitive endoderm into foregut/midgut cell lineages in a concentration-dependent manner

Stem Cells

Volumn 28, Issue 1, 2010, Pages 45-56

  Ameri, Jacqueline ^a   Ståhlberg, Anders ^a   Pedersen, Jesper ^a   Johansson, Jenny K ^a   Johannesson, Martina M ^a   Artner, Isabella ^a   Semb, Henrik ^a  

^a LUND UNIVERSITY   (Sweden)

Author keywords

Definitive endoderm; Differentiation; FGF signaling; Fibroblast growth factor 2; Human embryonic stem cells; Pancreatic endoderm

Indexed keywords

FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 2; FIBROBLAST GROWTH FACTOR 4; FIBROBLAST GROWTH FACTOR RECEPTOR; HEPATOCYTE NUCLEAR FACTOR 3BETA; MITOGEN ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR CDX2;

ARTICLE; CELL DIFFERENTIATION; CELL FATE; CELL LINEAGE; CONCENTRATION RESPONSE; CONTROLLED STUDY; EMBRYO PATTERN FORMATION; EMBRYONIC STEM CELL; ENDODERM; GENE; GENE INDUCTION; HUMAN; HUMAN CELL; LIVER CELL; MIDGUT; MOLECULAR EVOLUTION; PANCREAS; PDX1 GENE; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SMALL INTESTINE; VERTEBRATE;

ACTIVINS; ANIMALS; CELL DIFFERENTIATION; CELL LINE; CELL LINEAGE; DIGESTIVE SYSTEM; DOSE-RESPONSE RELATIONSHIP, DRUG; EMBRYONIC STEM CELLS; ENDODERM; EVOLUTION; FIBROBLAST GROWTH FACTOR 2; GASTRULA; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEPATOCYTES; HOMEODOMAIN PROTEINS; HUMANS; INTESTINE, SMALL; MAP KINASE SIGNALING SYSTEM; MICE; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; PANCREAS; PROTEIN KINASE INHIBITORS; RECEPTORS, FIBROBLAST GROWTH FACTOR; TIME FACTORS; TRANS-ACTIVATORS; WNT PROTEINS;

VERTEBRATA;

EID: 75349111313     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.249     Document Type: Article

References (82)

1. Grapin-Botton A, Melton DA. Endoderm development: From patterning to organogenesis. Trends Genet 2000;16(3):124-130.
2. Wells JM, Melton DA. Vertebrate endoderm development. Annu Rev Cell Dev Biol 1999;15:393-410.
3. Dessimoz J, Opoka R, Kordich JJ et al. FGF signaling is necessary for establishing gut tube domains along the anterior-posterior axis in vivo. Mech Dev 2006;123(1):42-55.
4. Ang SL, Wierda A, Wong D et al. The formation and maintenance of the definitive endoderm lineage in the mouse: Involvement of HNF3/ forkhead proteins. Development 1993;119(4):1301-1315.
5. Cardoso WV, Lu J. Regulation of early lung morphogenesis: Questions, facts and controversies. Development 2006;133(9):1611-1624.
6. Rossi JM, Dunn NR, Hogan BL et al. Distinct mesodermal signals, including BMPs from the septum transversum mesenchyme, are required in combination for hepatogenesis from the endoderm. Genes Dev 2001;15(15):1998-2009.
7. Bhushan A, Itoh N, Kato S et al. Fgf10 is essential for maintaining the proliferative capacity of epithelial progenitor cells during early pancreatic organogenesis. Development 2001;128(24):5109-5117.
8. Dichmann DS, Miller CP, Jensen J et al. Expression and misexpression of members of the FGF and TGFbeta families of growth factors in the developing mouse pancreas. Dev Dyn 2003;226(4):663-674.
9. Hart A, Papadopoulou S, Edlund H. Fgf10 maintains notch activation, stimulates proliferation, and blocks differentiation of pancreatic epithelial cells. Dev Dyn 2003;228(2):185-193.
10. Wells JM, Melton DA. Early mouse endoderm is patterned by soluble factors from adjacent germ layers. Development 2000;127(8):1563-1572.
11. Yamauchi H, Miyakawa N, Miyake A et al. Fgf4 is required for left-right patterning of visceral organs in zebrafish. Dev Biol 2009;332(1): 177-185.
12. Serls AE, Doherty S, Parvatiyar P et al. Different thresholds of fibroblast growth factors pattern the ventral foregut into liver and lung. Development 2005;132(1):35-47.
13. Roszell BR, Mondrinos MJ, Seaton A et al. Efficient derivation of alveolar type II cells from embryonic stem cells for in vivo application. Tissue Eng Part A 2009;15(11):3351-3365.
14. Deutsch G et al. A bipotential precursor population for pancreas and liver within the embryonic endoderm. Development 2001;128(6): 871-881.
15. Hebrok M, Kim SK, Melton DA. Notochord repression of endodermal Sonic hedgehog permits pancreas development. Genes Dev 1998; 12(11):1705-1713.
16. Kim SK, MacDonald RJ. Signaling and transcriptional control of pancreatic organogenesis. Curr Opin Genet Dev 2002;12(5):540-547.
17. Johannesson M, Ståhlberg A, Ameri J et al. FGF4 and retinoic acid direct differentiation of hESCs into PDX1-expressing foregut endoderm in a time- and concentration-dependent manner. PLoS One 2009;4(3):e4794.
18. Cowan CA et al. Derivation of embryonic stem-cell lines from human blastocysts. N Engl J Med 2004;350(13):1353-1356.
19. Heins N, Englund MC, Sjöblom C et al. Derivation, characterization, and differentiation of human embryonic stem cells. Stem Cells 2004; 22(3):367-376.
20. D'Amour KA, Bang AG, Eliazer S et al. Production of pancreatic hormone-expressing endocrine cells from human embryonic stem cells. Nat Biotechnol 2006;24(11):1392-1401.
21. Bustin SA. Absolute quantification of mRNA using real-time reverse transcription polymerase chain reaction assays. J Mol Endocrinol 2000;25(2):169-193.
22. Stahlberg A, Aman P, Ridell B et al. Quantitative real-time PCR method for detection of B-lymphocyte monoclonality by comparison of kappa and lambda immunoglobulin light chain expression. Clin Chem 2003;49(1):51-59.
23. Kanai-Azuma M, Kanai Y, Gad JM et al. Depletion of definitive gut endoderm in Sox17-null mutant mice. Development 2002;129(10): 2367-2379.
24. McGrath KE, Koniski AD, Maltby KM et al. Embryonic expression and function of the chemokine SDF-1 and its receptor, CXCR4. Dev Biol 1999;213(2):442-456.
25. Bouwmeester T, Kim S, Sasai Y et al. Cerberus is a head-inducing secreted factor expressed in the anterior endoderm of Spemann's organizer. Nature 1996;382(6592):595-601.
26. Blum M, Gaunt SJ, Cho KW et al. Gastrulation in the mouse: The role of the homeobox gene goosecoid. Cell 1992;69(7):1097-1106.
27. Morrison GM, Oikonomopoulou I, Migueles RP et al. Anterior definitive endoderm from ESCs reveals a role for FGF signaling. Cell Stem Cell 2008;3(4):402-415.
28. Ang SL, Rossant J. HNF-3 beta is essential for node and notochord formation in mouse development. Cell 1994;78(4):561-574.
29. Jung J, Zheng M, Goldfarb M et al. Initiation of mammalian liver development from endoderm by fibroblast growth factors. Science 1999; 284(5422):1998-2003.
30. Gualdi R, Bossard P, Zheng M et al. Hepatic specification of the gut endoderm in vitro: Cell signaling and transcriptional control. Genes Dev 1996;10(13):1670-1682.
31. Landry C, Clotman F, Hioki T et al. HNF-6 is expressed in endoderm derivatives and nervous system of the mouse embryo and participates to the cross-regulatory network of liver-enriched transcription factors. Dev Biol 1997;192(2):247-257.
32. Rausa F, Samadani U, Ye H et al. The cut-homeodomain transcriptional activator HNF-6 is coexpressed with its target gene HNF-3 beta in the developing murine liver and pancreas. Dev Biol 1997;192(2):228-246.
33. Li J, Ning G, Duncan SA. Mammalian hepatocyte differentiation requires the transcription factor HNF-4alpha. Genes Dev 2000;14(4): 464-474.
34. Keng VW, Yagi H, Ikawa M et al. Homeobox gene Hex is essential for onset of mouse embryonic liver development and differentiation of the monocyte lineage. Biochem Biophys Res Commun 2000;276(3): 1155-1161.
35. Jonsson J, Carlsson L, Edlund T et al. Insulin-promoter-factor 1 is required for pancreas development in mice. Nature 1994;371(6498): 606-609.
36. Offield MF, Jetton TL, Labosky PA et al. PDX-1 is required for pancreatic outgrowth and differentiation of the rostral duodenum. Development 1996;122(3):983-995.
37. Seymour PA, Freude 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(6):1865-1870.
38. Lynn FC, Smith SB, Wilson ME et al. Sox9 coordinates a transcriptional network in pancreatic progenitor cells. Proc Natl Acad Sci U S A 2007;104(25):10500-10505.
39. Pedersen JK, Nelson SB, Jorgensen MC et al. Endodermal expression of Nkx6 genes depends differentially on Pdx1. Dev Biol 2005;288(2): 487-501.
40. Kawaguchi Y, Cooper B, Gannon M et al. The role of the transcriptional regulator Ptf1a in converting intestinal to pancreatic progenitors. Nat Genet 2002;32(1):128-134.
41. Zhou Q et al. A multipotent progenitor domain guides pancreatic organogenesis. Dev Cell 2007;13(1):103-114.
42. Schwitzgebel VM, Law AC, Rajagopal J et al. Expression of neurogenin3 reveals an islet cell precursor population in the pancreas. Development 2000;127(16):3533-3542.
43. Gradwohl G et al. Neurogenin3 is required for the development of the four endocrine cell lineages of the pancreas. Proc Natl Acad Sci U S A 2000;97(4):1607-1611.
44. Lee CS, Sund NJ, Vatamaniuk MZ et al. Foxa2 controls Pdx1 gene expression in pancreatic beta-cells in vivo. Diabetes 2002;51(8): 2546-2551.
45. Gu G, Brown JR, Melton DA. Direct lineage tracing reveals the ontogeny of pancreatic cell fates during mouse embryogenesis. Mech Dev 2003;120(1):35-43.
46. Lyttle BM, Li J, Krishnamurthy M et al. Transcription factor expression in the developing human fetal endocrine pancreas. Diabetologia 2008;51(7):1169-1180.
47. Goto H, Tomono Y, Ajiro K et al. Identification of a novel phosphorylation site on histone H3 coupled with mitotic chromosome condensation. J Biol Chem 1999;274(36):25543-25549.
48. Ishii Y, Rex M, Scotting PJ et al. Region-specific expression of chicken Sox2 in the developing gut and lung epithelium: Regulation by epithelial-mesenchymal interactions. Dev Dyn 1998;213(4):464-475.
49. Gontan C, de Munck A, Vermeij M et al. Sox2 is important for two crucial processes in lung development: branching morphogenesis and epithelial cell differentiation. Dev Biol 2008;317(1):296-309.
50. Barzon L, Boscaro M, Pacenti M et al. Evaluation of circulating thyroid-specific transcripts as markers of thyroid cancer relapse. Int J Cancer 2004;110(6):914-920.
51. Costa RH, Kalinichenko VV, Lim L. Transcription factors in mouse lung development and function. Am J Physiol Lung Cell Mol Physiol 2001;280(5):L823-L838.
52. Kelly SE, Bachurski CJ, Burhans MS et al. Transcription of the lung-specific surfactant protein C gene is mediated by thyroid transcription factor 1. J Biol Chem 1996;271(12):6881-6888.
53. Bolton SJ, Pinnion K, Marshall CV et al. Changes in Clara cell 10 kDa protein (CC10)-positive cell distribution in acute lung injury following repeated lipopolysaccharide challenge in the rat. Toxicol Pathol 2008;36(3):440-448.
54. Min H, Danilenko DM, Scully SA et al. Fgf-10 is required for both limb and lung development and exhibits striking functional similarity to Drosophila branchless. Genes Dev 1998;12(20): 3156-3161.
55. Mailleux AA, Tefft D, Ndiaye D et al. Evidence that SPROUTY2 functions as an inhibitor of mouse embryonic lung growth and morphogenesis. Mech Dev 2001;102(1-2):81-94.
56. Miller LA, Wert SE, Whitsett JA. Immunolocalization of sonic hedgehog (Shh) in developing mouse lung. J Histochem Cytochem 2001; 49(12):1593-1604.
57. Pepicelli CV, Lewis PM, McMahon AP. Sonic hedgehog regulates branching morphogenesis in the mammalian lung. Curr Biol 1998; 8(19):1083-1086.
58. Bellusci S, Furuta Y, Rush MG et al. Involvement of Sonic hedgehog (Shh) in mouse embryonic lung growth and morphogenesis. Development 1997;124(1):53-63.
59. Freund JN, Domon-Dell C, Kedinger M et al. The Cdx-1 and Cdx-2 homeobox genes in the intestine. Biochem Cell Biol 1998;76(6): 957-969.
60. Tolkunova E, Cavaleri F, Eckardt S et al. The caudal-related protein cdx2 promotes trophoblast differentiation of mouse embryonic stem cells. Stem Cells 2006;24(1):139-144.
61. van den Akker E, Forlani S, Chawengsaksophak K et al. Cdx1 and Cdx2 have overlapping functions in anteroposterior patterning and posterior axis elongation. Development 2002;129(9):2181-2193.
62. Gamer LW, Wright CV. Murine Cdx-4 bears striking similarities to the Drosophila caudal gene in its homeodomain sequence and early expression pattern. Mech Dev 1993;43(1):71-81.
63. Scholzen T, Gerdes J. The Ki-67 protein: From the known and the unknown. J Cell Physiol 2000;182(3):311-322.
64. Hart AW, Baeza N, Apelqvist A et al. Attenuation of FGF signalling in mouse beta-cells leads to diabetes. Nature 2000;408(6814): 864-868.
65. Le Bras S, Miralles F, Basmaciogullari A et al. Fibroblast growth factor 2 promotes pancreatic epithelial cell proliferation via functional fibroblast growth factor receptors during embryonic life. Diabetes 1998;47(8):1236-1242.
66. Ye F, Duvillie B, Scharfmann R. Fibroblast growth factors 7 and 10 are expressed in the human embryonic pancreatic mesenchyme and promote the proliferation of embryonic pancreatic epithelial cells. Diabetologia 2005;48(2):277-281.
67. Ornitz DM, Xu J, Colvin JS et al. Receptor specificity of the fibroblast growth factor family. J Biol Chem 1996;271(25):15292-15297.
68. Ornitz DM, Itoh N. Fibroblast growth factors. Genome Biol 2001; 2(3):REVIEWS300.
69. Jiang J, Au M, Lu K et al. Generation of insulin-producing islet-like clusters from human embryonic stem cells. Stem Cells 2007;25(8): 1940-1953.
70. Kroon E, Martinson LA, Kadoya K et al. Pancreatic endoderm derived from human embryonic stem cells generates glucose-responsive insulin-secreting cells in vivo. Nat Biotechnol 2008;26(4):443-452.
71. Shim JH, Kim SE, Woo DH et al. Directed differentiation of human embryonic stem cells towards a pancreatic cell fate. Diabetologia 2007;50(6):1228-1238.
72. Hay DC, Fletcher J, Payne C et al. Highly efficient differentiation of hESCs to functional hepatic endoderm requires ActivinA and Wnt3a signaling. Proc Natl Acad Sci U S A 2008;105(34):12301-12306.
73. Pei H, Yang Y, Xi J et al. Lineage restriction and differentiation of human embryonic stem cells into hepatic progenitors and zone 1 hepatocytes. Tissue Eng Part C Methods 2009;15(1):95-104.
74. Dessimoz J, Grapin-Botton A. Pancreas development and cancer: Wnt/beta-catenin at issue. Cell Cycle 2006;5(1):7-10.
75. Kumar M, Jordan N, Melton D et al. Signals from lateral plate mesoderm instruct endoderm toward a pancreatic fate. Dev Biol 2003; 259(1):109-122.
76. Grapin-Botton A, Constam D. Evolution of the mechanisms and molecular control of endoderm formation. Mech Dev 2007;124(4): 253-278.
77. D'Amour KA, Agulnick AD, Eliazer S et al. Efficient differentiation of human embryonic stem cells to definitive endoderm. Nat Biotechnol 2005;23(12):1534-1541.
78. Gadue P, Huber TL, Paddison PJ et al. 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 U S A 2006;103(45):16806-16811.
79. Kubo A, Shinozaki K, Shannon JM et al. Development of definitive endoderm from embryonic stem cells in culture. Development 2004; 131(7):1651-1662.
80. Tada S et al. Characterization of mesendoderm: A diverging point of the definitive endoderm and mesoderm in embryonic stem cell differentiation culture. Development 2005;132(19):4363-4374.
81. Yasunaga M, Era T, Furusawa C et al. Induction and monitoring of definitive and visceral endoderm differentiation of mouse ES cells. Nat Biotechnol 2005;23(12):1542-1550.
82. Elghazi L, Cras-Méneur C, Czernichow P et al. Role for FGFR2IIIb-mediated signals in controlling pancreatic endocrine progenitor cell proliferation. Proc Natl Acad Sci U S A 2002;99(6):3884-3889.